Archival tagging of subadult and adult common thresher sharks (Alopias vulpinus) off the coast of southern California
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The common thresher shark (Alopias vulpinus) is a secondary target species of the California drift gillnet fishery (CA-DGN) and supports a growing recreational fishery in California waters. This study used archival tags to examine the movement patterns and habitat preferences of common threshers of the size range captured in the CA-DGN (>120 cm fork length). Depth and temperature-logging archival tags were deployed on 57 subadult and adult common threshers in the Southern California Bight. Tags from five individuals (8.8%) were recovered, and 154 days of data were successfully obtained from four of these. By night, shark movements were primarily limited to waters above the thermocline, which ranged in depth from 15 to 20 m. Sharks were significantly deeper by day, and daytime vertical distribution consisted of two distinct modes: a ‘shallow mode’ (wherein sharks occupied only the upper 20 m of the water column) and a ‘deep mode’ (characterized by frequent vertical excursions below the thermocline). This modal switch is interpreted as relating to regional differences in abundance of surface-oriented prey and prey in deeper water. Maximum dive depth was 320 m, greatest dive duration was 712 min, minimum temperature experienced during a dive was 9.1°C, and dive descent rate was significantly greater than ascent rate. Sharks inhabited waters corresponding to a sea surface temperature range of 16 to 21°C. The nocturnal depth distribution of common threshers has implications for management of drift gillnet deployment depths in the CA-DGN.
The common thresher shark (Alopias vulpinus) is a large pelagic species with a cosmopolitan distribution in subtropical and temperate seas (Compagno 2001). Along the west coast of North America, this species occurs from Baja California, Mexico to British Columbia, Canada (PFMC 2003), and is commercially important throughout this range. In Baja California waters, the common thresher is a target of drift gillnet (Olvera 2009) and artisanal shark fisheries (Cartamil 2009). In U.S. waters, it is an important secondary target species of the California drift gillnet fishery (CA-DGN) for broadbill swordfish (Xiphias gladius) and constitutes the largest commercial shark fishery in California waters (CDFG 2009). In addition, the common thresher supports a growing recreational fishery in southern California (Heberer et al. 2010). Analyses of CA-DGN catch patterns suggest that the common thresher overwinters offshore of Baja California and migrates north in the spring (Hanan et al. 1993; Smith and Aseltine-Nielson 2001). The highest concentration of common threshers is thought to occur in the Southern California Bight (SCB), a region extending from Point Conception, California (34°N latitude), to Cabo Colonet, Mexico (31°N latitude) (Carlucci et al. 1986; Hanan et al. 1993).
Acoustic telemetry studies in the SCB have shown that juvenile common threshers generally utilize shallow waters over the continental shelf as a nursery habitat (Cartamil et al. 2010a), while subadult and adult common thresher [i.e., >120 cm fork length (FL)] occur in deeper waters offshore of the continental shelf (Cartamil et al. 2010b). Larger sharks made vertical excursions by day to depths of up to 220 m that were suggestive of foraging behavior, whereas nocturnal depths were generally limited to the upper 20 m of the water column and were strongly constrained by the depth of the thermocline. However, the logistical constraints of acoustic telemetry limited these studies to less than 75 h, which may not be long enough to encompass the full range of behaviors exhibited by the species.
To obtain longer records of the movement patterns of larger common thresher sharks, a study was carried out using non-transmitting archival tags. These tags can record a range of high-resolution environmental data for periods ranging from days to years. They can be implanted or secured externally and have been used extensively on pelagic fishes (Block et al. 1998; Ishida et al. 2001; West and Stevens 2001; Schaefer and Fuller 2002; Schaefer et al. 2007). Archival tags are limited in that they do not gather the full compliment of ambient data possible through active acoustic telemetry tracking, and the fish must be re-captured in order for the data to be extracted from the tag. However, these limitations are balanced by a substantially longer archived data stream. This paper reports the findings of a study in which archival tags were used to examine the depth, temperature preferences, and movement patterns of common thresher sharks in the SCB. Specific goals were to (1) determine whether behavioral trends identified by acoustic telemetry tracking (Cartamil et al. 2010b) persist over longer time periods, (2) examine variability in common thresher shark movement patterns over several weeks, and (3) quantify the relationship between habitat preference and common thresher shark vulnerability to west coast fisheries. Tagging was restricted to subadult and adult common threshers, which are the size classes most commonly captured in the CA-DGN (PFMC 2003).
Tags were pre-programmed to collect ambient temperature and depth at 1.88-min intervals (except tag 1: 0.94 min intervals) with a resolution of ~0.2°C and <2.0 m. Tags had dimensions of 8 mm × 16 mm × 27 mm, weighed 5 g in air (2 g in water), and had a memory storage capacity of approximately 44 d (except tag 1: 22 d memory capacity). Acquisition of archived data was dependent upon re-capture of the animal by commercial or recreational fishers, and thus, each tag had reward information and a contact phone number displayed on the exterior. Data were acquired from recovered tags using TagTalk1100 software.
An overview of each shark’s vertical movements was obtained by plotting depth against time of day. Vertical distribution was further examined by calculating aggregate time-at-depth distributions in 10-m bins, during both day and night periods. The mean thermocline depth for each shark record was estimated by determining the dive-depth range over which the rate of temperature change exceeded 1°C per 5 m of vertical change (Cartamil et al. 2010b). Differences in depth between night and day, between vertical distribution modes (explained in Results), and differences in nocturnal depths during full, new, and intermediate moons (full and new moons refer to the day of each full or new moon and the 2 days preceding and following it) were examined by fitting an ANOVA-type model to the data using weighted least squares. The weights were equal to the inverse of the variance of depth values for each data set tested and are a conservative means of incorporating variability in depth among periods into the analysis. The dependent variable for these models was the average depth during a specified period. Independent variables included a shark effect, to account for animal-specific differences in overall average depth, a vertical distribution mode effect, night/day effect, and lunar period.
To examine diving behavior of common thresher sharks, individual dives were defined as vertical excursions that began in the upper 20 m of the water column, spanned a minimum depth of 15 m, and were followed by a return to the upper 20 m. These discrete diving periods were quantified in terms of total dive duration, maximum dive depth, and minimum dive temperature. Where dives were followed by a post-dive interval in the warmer waters of the mixed layer, fixed-effect analysis of covariance (ANCOVA) was used to investigate the relationship between post-dive time interval and the above calculated dive parameters (as covariates) using each shark as a fixed effect. Descent and ascent rates were calculated for each dive and compared with a general linear model using each shark as a fixed effect. For all statistical tests, results were considered significant at the p < 0.05 level.
Shark thermal preferences were determined by pooling temperature data in 1°C bins and calculating the percentage of time spent at each bin during day and night periods. The sea surface temperature (SST) range experienced by sharks was estimated using tag temperature data collected at a depth of <2 m.
Tag and recapture data for five thresher sharks released with archival tags in the SCB
11 June 2004
17 Dec 2005
27 April 2004
5 July 2007
31 May 2004
15 Nov 2004
15 June 2004
30 Aug 2004
23 June 2004
22 Dec 2007
Total number of days of archived data collected for each shark, the number of days each shark spent in shallow and deep mode, and the mean (±SD) depths occupied by the shark in each mode during day and night (excluding dives), relative to average thermocline (TC) depth
Shallow mode depths (m)
Deep mode depths (m)
TC depth (m)
10.77 ± 3.54
17.06 ± 4.33
12.34 ± 4.16
17.44 ± 4.55
18.8 ± 1.6
6.46 ± 2.75
8.49 ± 3.18
7.05 ± 1.94
9.60 ± 2.91
13.8 ± 2.1
6.94 ± 2.33
9.85 ± 2.96
7.15 ± 3.24
10.03 ± 3.41
15.7 ± 1.1
5.98 ± 3.07
8.19 ± 3.85
8.09 ± 3.16
10.34 ± 4.94
15.4 ± 1.6
Shallow and Deep modes of behavior relate to the daytime distribution of tagged common thresher sharks. The archival records of each shark show abrupt switches between Shallow and Deep modes that may be related to the vertical distribution and abundance of prey. Small coastal pelagic fishes such as the northern anchovy (Engraulis mordax), Pacific sardine, and Pacific mackerel comprise the majority of common thresher shark diet in the SCB (Preti et al. 2001, 2004) and typically occur in surface waters during daylight hours (Allen and DeMartini 1983). Sharks exhibiting Shallow mode behavior may be foraging near the surface when these prey species are abundant. The switch to a Deep mode of vertical distribution may occur when surface prey are scarce and sharks commence foraging for deeper prey such as Pacific hake (Merluccius productus) (Preti et al. 2001, 2004), which commonly occurs beyond the continental shelf at depths of up to 500 m (Ressler et al. 2007). Other potential deep-water prey include louvar (Luvarus imperialis), market squid (Loligo opalescens), and rockfishes (Sebastes sp.) (Preti et al. 2001, 2004). Deep and Shallow modes of diving have previously been described for other pelagic fish species such as swordfish (Sepulveda et al. 2010) and yellowfin tuna (Thunnus albacares) (Schaefer et al. 2007).
An alternative explanation for the diving behavior of common thresher sharks is that it provides an efficient mechanism for transportation. Weihs (1973) asserted that negatively buoyant fish might move from place to place with less energy expenditure by adopting a ‘swim-glide’ mode of locomotion, wherein the shark would be expected to descend slowly and ascend at a faster rate. However, the dive profiles of archivally tagged common threshers reveal the opposite tendency, as has been reported for several pelagic sharks (Carey and Scharold 1990; Nakano et al. 2003; Dewar et al. 2004; Sepulveda et al. 2004). Common thresher shark ‘fast-down’, ‘slow-up’ dive profiles may be indicative of prey searching as has been previously postulated for similar species (Carey and Scharold 1990; Nakano et al. 2003).
Nocturnal depth preference appears to be strongly influenced by the depth of the thermocline, and over 90% of nocturnal depth readings were located above estimated thermocline depths. Why did common thresher sharks inhabit such shallow waters by night? One possibility is that they are foraging in the mixed layer. However, several factors argue against this. First, northern anchovy and Pacific sardine schools often disperse at night (Allen and DeMartini 1983), which could make predation more difficult. Secondly, the common thresher utilizes a unique mode of predation, wherein prey is struck with the elongate upper lobe of the caudal fin prior to capture (Gubanov 1972; Aalbers et al. 2010), and this behavior may require light levels higher than those available at night. A nocturnal preference for the warmer mixed layer after daytime predatory activity could be a form of post-feeding thermoregulation; common threshers might benefit from warmer temperatures by increased digestive rate and assimilation efficiency (Wurtsbaugh and Neverman 1988). However, feeding periodicity has not been investigated for this species, and the possibility of nocturnal feeding cannot be ruled out.
Unlike other shark species that dive deep during full moons (Carey and Scharold 1990; West and Stevens 2001; Weng et al. 2007), lunar phase had no effect upon the nocturnal depth of common threshers. However, typical southern California spring weather conditions [characterized by a dense and persistent marine cloud layer caused by the intrusion of warm Pacific air moving over colder waters (LaDochy and Brown 2003)] prevailed during May and June 2004 when most archival data were collected, and may have decreased lunar illumination sufficiently to prevent a light response. Additionally, if common thresher shark foraging is predominantly a daytime activity, nocturnal depth would not be expected to be influenced by changes in prey vertical distribution corresponding to lunar illumination.
Temperatures at the maximum depths attained by common threshers were up to 12°C lower than those at the surface. Prolonged exposure to low temperatures during dives imposes various physiological stresses such as a reduction in cardiovascular function (Blank et al. 2004), power output (Altringham and Block 1997), and temporal resolution of vision (Fritsches et al. 2005). However, the common thresher possesses vascular retia that enable it to elevate red muscle temperature above that of ambient water (Bone and Chubb 1983; Bernal and Sepulveda 2005; Sepulveda et al. 2005), and this capability for regional endothermy may allow the common thresher to withstand cooler temperatures for longer durations than pelagic ectotherms of similar mass. For example, the blue shark (Carey and Scharold 1990), scalloped hammerhead shark (Sphyrna lewini) (Klimley 1993), and ocean sunfish (Cartamil and Lowe 2004) dive through temperature gradients as severe as those encountered by the common thresher, but do not usually remain at maximum depth for more than a few minutes; this is reflected in their ‘yo-yo’ dive patterns. By contrast, almost 40% of common thresher dives were longer than 30 min and 11% were longer than 100 min, with a maximum dive duration of 712 min.
Common thresher sharks often made several dives throughout the day that were punctuated by short surface intervals, which could facilitate recovery from reduced body temperature incurred during dives (Carey and Robison 1981; Carey and Scharold 1990; Cartamil and Lowe 2004; Dewar et al. 2004). No relationship was found between the depth, temperature or duration of dives and subsequent surface intervals for archivally tagged common threshers. Therefore, while these intervals may be physiologically beneficial, their duration does not appear to be constrained by thermal stress incurred during the preceding dive.
Most of the U.S. commercial and recreational catch of the common thresher shark occurs in the SCB (Hanan et al. 1993; PFMC 2003). This importance of this region is further illustrated by the recapture of all tagged common threshers in the SCB, with three sharks caught by the CA-DGN, and two by recreational fishers. A tag return rate of 8.8% is considered fairly high for pelagic sharks (Kohler and Turner 2001) and reflects the fishing pressure on this species. Nevertheless, this rate likely underestimates the actual capture of tagged common threshers due to trans-boundary movements into Mexican waters (Baquero 2006), where tags from sharks captured in Mexican fisheries (Cartamil 2009; Olvera 2009) are often discarded at sea (D. Cartamil, personal observation). The possibility also exists that some tags were lost due to shedding, although the maximum time-at-liberty of 1,277 d suggests that the tag attachment was generally secure.
Off southern California, recreational fishing for common threshers has increased over the past decade and now is believed to significantly contribute to the total annual harvest of this species off the U.S. west coast. This sport fishery targets thresher sharks by trolling baited lures at depths of up to 20 m during the day (Heberer et al. 2010). Based on the daytime depth distribution within the waters of the upper mixed layer observed in this study, it is apparent that thresher sharks are vulnerable to recreational fishing gear throughout a majority of the daylight hours.
Within U.S. waters, the primary fishery impacting the common thresher is the CA-DGN. Drift gillnets are set at dusk and retrieved before dawn, and therefore, it is the nocturnal depth distribution of the common thresher shark that determines its susceptibility to CA-DGN gear. In the present study, only 23% of nocturnal depth readings were located below six fathoms, suggesting that catch rates of the common thresher could be reduced by increasing the minimum net depth (i.e., setting at depths of >6 fathoms) or increased by setting nets shallower than 6 fathoms, depending upon fishery management goals appropriate to the stock condition. In addition, because vertical behavior is strongly tied to thermocline depth, the latter could potentially be used to adaptively manage driftnet set depths to influence shark catches.
California Sea Grant (Grant # R/F-193) provided research funding and traineeship support for D. Cartamil, C. Sepulveda, and N. Wegner. D. Cartamil was also supported by a fellowship from the Alliance for Graduate Education and the Professoriate, and the Tuna Industry Endowment Fund. Additional funding was received by the William H. and Mattie Wattis Harris Foundation, the Tinker Foundation, the Moore Family Foundation, UC Mexus-CONACYT, the CA Ocean Protection Council, and the Save Our Seas Foundation. We thank J. Steinitz and the SIO Development Office for help in obtaining private funding and the Southwest Fishery Science Center for use of the R/V ‘Phoenix’. Thanks to C. Lennert for statistical advice, J. Blum for Matlab assistance, and E. Kisfaludy, J. Schram and J. Gaeta for help with field operations. All procedures were performed under the guidelines of the Institutional Animal Care and Use Committee of the University of California, San Diego (protocol S00080).
This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
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