Mar Biol (2007) 152:503–525 DOI 10.1007/s00227-007-0689-x
RESEARCH ARTICLE
Movements, behavior, and habitat utilization of yellowfin tuna (Thunnus albacares) in the northeastern Pacific Ocean, ascertained through archival tag data
Kurt M. Schaefer Æ Daniel W. Fuller Æ Barbara A. Block
Received: 23 August 2006 / Accepted: 28 March 2007 / Published online: 21 June 2007 Springer-Verlag 2007
Abstract Sixty-eight yellowfin tuna, Thunnus albacares, resulted in discrimination of four distinct behaviors. When (60-135 cm fork length) were caught and released with exhibiting type-1 diving behavior (78.1% of all days at implanted archival tags offshore off Baja California, liberty) the fish remained at depths less than 50 m at night Mexico, during October 2002 and October 2003. Thirty-six and did not dive to depths greater than about 100 m during fish (53%) were recaptured and the data were downloaded the day. Type-2 diving behavior (21.2% of all days at from all 36 recovered tags. Time at liberty ranged from 9 to liberty) was characterized by ten or more dives in excess of 1,161 days, and the data were analyzed for the 20 fish that 150 m during the day. Type-2 diving behavior is apparently were at liberty for 154 or more days. The accuracy in the a foraging strategy for fish targeting prey organisms of the position estimates, derived from light-level longitude data deep-scattering layer during the day, following nighttime and sea-surface temperatures (SSTs) based latitude, is foraging within the mixed layer on the same prey. Yel- about 0.41 in longitude and 0.82 in latitude, in this lowfin tuna exhibited occasional deep-diving behavior, and region. The movement paths, derived from position esti- some dives exceeded 1,000 m, where ambient tempera- mates, for the 20 yellowfin indicated that 19 (95%) re- tures were less than 5 C. Surface-oriented behavior, de- mained within 1,445 km of their release locations. The fined as the time fish remained at depths less than 10 m for estimated mean velocity along movement paths was more than 10 min, were evaluated. The mean number and 77 km/day. The southern and northern seasonal movement duration of surface-oriented events per day for all fish was paths observed for yellowfin off Baja California are influ- 14.3 and 28.5 min, respectively. Habitat utilization of enced by the seasonal movements of the 18 C SST iso- yellowfin, presented as monthly composite horizontal and therm. Cyclical movements to and from suitable spawning vertical distributions, indicates confined geographical dis- habitat (‡24 C SST) was observed only for mature fish. For tributions, apparently resulting from an affinity to an area the 12 fish that demonstrated site fidelity, the mean 95 and of high prey availability. The vertical distributions indicate 50% utilization distributions were 258,730 km2 and 41,260 greater daytime depths in relation to a seasonally deeper km2, respectively. Evaluations of the timed depth records mixed layer and a greater proportion of daytime at shal- lower depths in relation to a seasonally shallower mixed layer. Communicated by P.W. Sammarco.
K. M. Schaefer (&) Á D. W. Fuller Inter-American Tropical Tuna Commission, Introduction 8604 La Jolla Shores Drive, La Jolla, CA 92037-1508, USA e-mail: [email protected] Yellowfin tuna, Thunnus albacares, a large epipelagic oceanic species, occurs worldwide in subtropical and B. A. Block tropical seas (Collette and Nauen 1983). Yellowfin is the Tuna Research and Conservation Center, Hopkins Marine Station, Stanford University, principal target species of a large high-seas international 120 Oceanview Boulevard, Pacific Grove, CA 93950, USA fishery in the eastern Pacific Ocean (EPO), from which the 123 504 Mar Biol (2007) 152:503–525 annual catch in 2000 was nearly one-third the world Block 2005). Tagging studies using plastic dart tags or catches of yellowfin (Bayliff 2002). The annual catch of acoustic tags, and studies of longline catch records have yellowfin by all types of gear combined in the EPO has previously provided valuable information on these topics. averaged 297,000 mt (range 226,000–440,000 mt) from ATs record swimming depths, ambient and internal tem- 1985 to 2004 (Anonymous 2005). A recent stock assess- peratures, and ambient light levels. The light data can be ment for yellowfin in the EPO (Hoyle and Maunder 2006) processed using astronomical algorithms to provide daily indicates that the biomass decreased during 2002–2004 and estimates of longitudes and latitudes (Hill 1994; Hill and that the stock is likely below the level corresponding to the Braun 2001; Ekstrom 2004), and daily sea-surface tem- average maximum sustainable yield (AMSY), with recent peratures (SSTs) recorded by the tags matched to SSTs fishing mortality rates about 20% above those corre- from remote sensing can be used to significantly improve sponding to the AMSY. estimates of latitude (Teo et al. 2004; Clear et al. 2005; Tagging studies on yellowfin in the EPO have indicated Domeier et al. 2005; Nielsen et al. 2006). Current-gener- movements to be mostly restricted to less than 1,852 km ation ATs are capable of storing data for up to 5 years, (Fink and Bayliff 1970; Bayliff and Rothschild 1974; providing a unique opportunity to evaluate the influence of Bayliff 1979, 1984). Geographic variation observed in seasonal and annual environmental variability and onto- morphometrics and gill raker counts of yellowfin in the genetic changes on tuna movement patterns, behavior, and EPO results from restricted movements, limited mixing, habitat utilization. and environmental variation (Schaefer 1992). Life history The objectives of this investigation are to elucidate characteristics for yellowfin in the EPO, including age at movement patterns, behavior, and habitat utilization of size, growth, and reproductive biology, also indicate yellowfin in the northern region of the EPO, and to eval- geographic variation (Schaefer 1998; Schaefer 2001). In uate the influence of oceanographic factors on those char- addition, a recent genomic study utilizing microsatellite acteristics. This information has direct applications for variation has provided evidence of discrete northern and improving stock assessments of yellowfin in the EPO. southern populations of yellowfin in the EPO (Diaz-Jaimes and Uribe-Alcocer 2006). Yellowfin tuna possess both central and lateral counter- Materials and methods current heat exchangers, which provide the ability to con- serve metabolic heat and elevate their body temperatures Tag releases above that of ambient water temperatures (Carey 1973; Graham 1975; Dizon and Brill 1979). This enhanced Twenty-five yellowfin were captured, tagged, and released thermal inertia slows the body temperature cooling rate, during 12–13 October 2002 on ‘‘the ridge’’ (25.73 N providing the capability for the fish to undertake brief dives 113.13 W) about 111 km northwest of Magdalena Bay, into cooler waters below the thermocline to exploit deep and 43 during 9–16 October 2003 at Guadalupe Island prey resources or escape predators (Neill et al. 1976; Ste- (29.07 N 118.23 W), Alijos Rocks (24.97 N 115.76 W), vens and Neill 1978). and on ‘‘the ridge’’ (25.73 N 113.13 W) from about 37– Apparent depth distributions, temperature preferences, 111 km northwest of Magdalena Bay (Fig. 1a). Tagging and vertical movements of yellowfin in the Pacific, by size was conducted during regularly-scheduled 10-day trips on and time of day, have been reported based on studies using the FV Royal Star, a 28-m long-range sportfishing vessel. ultrasonic telemetry (Carey and Olson 1982; Holland et al. The ATs used in this study were model LTD_2310 1990; Block et al. 1997, 1999) and analyses of longline manufactured by Lotek Wireless Inc. (St John’s, NF, fishing records (Sund et al. 1981; Boggs 1992). Those Canada) (Lotek Wireless Inc. 2006). The tag body is studies have indicated vertical movements of yellowfin to cylindrical, measuring 16 mm in diameter and 70 mm in be predominantly restricted to depths of the mixed layer, length, and weighing 40 g in air. The tag is designed for but occasionally below the thermocline for short periods. implantation into the peritoneal cavity of the fish so that the Elucidating the physiological and behavioral constraints, sensor stalk protrudes outside the fish through an incision along with the environmental variables that define habitat in the abdominal wall. Information about reporting the for yellowfin, including depth and temperature distribu- recovery of the tag and the associated reward (US$500) tions, can improve stock assessments through standardi- was printed in English, Spanish, and Japanese on the 316 zation of purse-seine and longline catch and effort data stainless steel casing of the tag body. (Hinton and Nakano 1996; Brill and Lutcavage 2001). The depth, internal, and ambient temperatures, and light Geolocating archival tags (ATs) can vastly improve our level were stored in the memory of the tag at 1-min understanding of yellowfin movements, behavior, and intervals. At this sampling rate, the memory of each tag habitat (Arnold and Dewar 2001; Gunn and Block 2001; (8 MB) is capable of storing 979 days (2.7 years) of those 123 Mar Biol (2007) 152:503–525 505
resolution of 1 and 0.05% of full scale, respectively. The temperature sensing is a range of 0–30 C, with an accuracy and resolution of 0.1 and 0.05 C, respectively. The light sensing has nine decades of sensitivity, a resolution of 32 points/decade, and is capable of detecting light to a depth of 440 m (Schaefer and Fuller 2006). Yellowfin tuna were captured during the day on rod and reel with live sardines on circle hooks (sizes 1/0–7/0). Each fish was brailed from the water at the side of the vessel with a heavy-gauge aluminum rigid-framed net of knotless webbing and placed either in a tagging cradle ventral side up or on a foam pad covered with smooth vinyl, depending upon the size of the fish. Its eyes were immediately covered with a wet synthetic chamois, the hook was removed, and the condition of the fish was determined. If the fish was in excellent condition (i.e., no damage to the eyes or gills and no significant bleeding), the surgery required for implanting the AT was initiated. An incision about 2 cm long was made with a sterile surgical scalpel blade (Bard Parker no. 20) in the abdominal wall about 1/3 the distance from the anus to- ward the base of the pelvic fins and about 2 cm to the left of the centerline of the fish. Special care was taken to cut through the dermis only and partially through the muscle, but not into the peritoneal cavity. A gloved finger was inserted into the incision and forced through the muscle into the peritoneal cavity. The tag, sterilized in povidone– iodine solution (10%), was inserted through the incision into the peritoneal cavity, with the stalk protruding out- side. The incision was closed with two sutures using a sterile needle and suture material [Ethicon (PDSII) size 0, cutting cp-1, 70 cm]. Each fish was also tagged with one numbered 12.5-cm green plastic dart tag (Hallprint Pty. Ltd. 2006), using tubular stainless steel applicators. Tags were inserted into the dorsal musculature with the barbed heads passing be- tween the pterygiophores below the base of the second dorsal fin, from either side of the fish. Information for Fig. 1 Thunnus albacares. a Positions of release for 25 fish during October 2002 (blue circles) and 43 fish during October 2003 (red reporting the recovery of the fish and for receiving the circles); b Areas of recapture for 13 fish released during October 2002 reward (US$500) for return of the fish was printed in (blue circles) and 23 fish released October 2003 (red circles) Spanish on the tags. Lastly, 1.5–3.0 ml of 100-mg/ml oxytetracycline hydrochloride solution were injected into the dorsal musculature with a disposable automatic vacci- data. The tag also has a telescoping feature which makes it nator. possible to continue recording data after the memory is full The 68 yellowfin released with ATs were measured for by overwriting alternate daily data sets starting at the fork length to the nearest centimeter, using increments beginning of the deployment. The memory of the tag is marked on the cradle liner or with a caliper. The fish were also partitioned into a ‘‘day log’’ which includes estimates then either picked up by hand from the cradle or slid along of daily position, SST, minimum and maximum depth, and the wet foam pad on the deck and released back into the battery voltage. Software in the tag processes the light level ocean. The total time that the fish were out of the water was and pressure data, corrects for light attenuation, and logs about 2 min. All fish released with ATs were observed to the position estimates in the ‘‘day log.’’ The depth sensing swim away from the vessel after release, and all appeared is to a maximum of 2,000 m, with an accuracy and to be in good condition. 123 506 Mar Biol (2007) 152:503–525
Tag recoveries given in Table 1. Recaptures from 2002 releases extended from about 185 km west by northwest of Cabo San Lucas Thirteen (52%) of 25 yellowfin tuna released in 2002 and to about 8 N 120 W (Fig. 1b). Yellowfin recaptures from 23 (53.5%) of the 43 released in 2003 had been recap- 2003 releases extended from Guadalupe Island, 111– tured by 1st April 2006. Data were downloaded and 185 km west by southwest of Cabo San Lucas, to 20 N processed from all 36 tags. The fish lengths, release and 114 W (Fig. 1b). Fourteen of the tags were recovered recapture dates and locations, and number of days at from fish caught by purse-seine vessels with scientific liberty of the 36 fish from which ATs were recovered are observers aboard, ten from fish caught by purse-seine
Table 1 Thunnus albacares. Release and recapture information for 36 fish for which tags were recovered Tag no. Length (cm) Release Recapture Days at liberty Location (dd) Date Location (dd) Date
401 67 25.73 N 113.13 W 12-Oct-02 25.73 N 113.13 W 26-Oct-02 13.7 405 86 29.07 N 118.23 W 09-Oct-03 29.02 N 118.22 W 26-Oct-03 16.6 450 126 24.97 N 115.76 W 12-Oct-03 24.97 N 115.76 W 31-Oct-03 18.3 478 91 25.73 N 113.13 W 13-Oct-02 8.27 N 119.83 W 25-Apr-04 559.7 509 93 25.73 N 113.13 W 12-Oct-02 22.07 N 109.33 W 06-Aug-03 297.7 525 90 25.73 N 113.13 W 12-Oct-02 23.58 N 111.70 W 17-Dec-05 1160.7 535 77 25.73 N 113.13 W 12-Oct-02 25.73 N 113.13 W 26-Oct-02 13.7 545 95 25.73 N 113.13 W 12-Oct-02 25.73 N 113.13 W 26-Oct-02 13.7 549 85 29.07 N 118.23 W 09-Oct-03 22.40 N 111.08 W 25-Apr-04 198.4 580 74 25.73 N 113.13 W 12-Oct-02 25.75 N 113.15 W 22-Oct-02 9.7 604 75 25.73 N 113.13 W 12-Oct-02 25.72 N 113.13 W 21-Oct-02 8.7 644 98 25.73 N 113.13 W 13-Oct-02 20.30 N 109.18 W 11-Aug-03 301.7 801 86 25.73 N 113.13 W 12-Oct-02 25.77 N 113.12 W 21-Oct-02 8.7 806 73 25.73 N 113.13 W 12-Oct-02 20.72 N 111.47 W 19-Jul-03 279.7 826 94 25.73 N 113.13 W 13-Oct-02 23.38 N 111.17 W 27-Jul-03 286.7 827 76 25.25 N 112.80 W 15-Oct-03 23.55 N 108.85 W 17-Mar-04 153.7 902 70 25.73 N 113.13 W 12-Oct-02 25.73 N 113.13 W 26-Oct-02 13.7 1425 92 29.07 N 118.23 W 09-Oct-03 29.08 N 118.24 W 26-Jul-04 290.6 1440 89 29.07 N 118.23 W 09-Oct-03 29.18 N 118.23 W 18-Nov-03 39.6 1443 127 24.97 N 115.76 W 12-Oct-03 24.97 N 115.75 W 02-Nov-03 20.6 1444 123 24.97 N 115.76 W 12-Oct-03 24.97 N 115.76 W 12-Nov-03 30.5 1448 87 29.07 N 118.23 W 09-Oct-03 22.83 N 110.53 W 24-Apr-04 197.4 1455 85 29.07 N 118.23 W 09-Oct-03 22.40 N 111.08 W 25-Apr-04 198.6 1461 67 25.72 N 113.12 W 16-Oct-03 22.75 N 111.25 W 26-Apr-04 192.7 1478 129 24.97 N 115.76 W 12-Oct-03 24.97 N 115.75 W 11-Nov-03 29.6 1497 65 25.25 N 112.80 W 15-Oct-03 25.22 N 112.87 W 03-Nov-03 18.7 1503 131 24.97 N 115.76 W 12-Oct-03 24.97 N 115.75 W 08-Nov-03 26.3 1506 75 25.10 N 112.75 W 15-Oct-03 24.08 N 112.57 W 23-Jun-04 251.3 1514 83 29.07 N 118.23 W 09-Oct-03 23.40 N 111.17 W 26-Jul-04 290.5 1526 78 25.25 N 112.80 W 15-Oct-03 22.55 N 110.97 W 17-Apr-04 184.7 1547 77 25.25 N 112.80 W 15-Oct-03 23.67 N 112.08 W 08-Jun-04 236.7 1549 85 29.07 N 118.23 W 09-Oct-03 28.99 N 118.22 W 24-Oct-03 14.4 1550 86 29.07 N 118.23 W 09-Oct-03 22.68 N 110.88 W 17-Apr-04 190.6 1559 75 25.25 N 112.80 W 15-Oct-03 22.33 N 110.98 W 25-Apr-04 192.7 1569 86 24.97 N 115.76 W 11-Oct-03 20.47 N 114.15 W 16-Jun-04 248.3 1895 130 24.97 N 115.76 W 12-Oct-03 24.98 N 115.77 W 05-Apr-04 175.4 The lengths (fork length) are those measured at release. The locations are given in decimal degrees (dd)
123 Mar Biol (2007) 152:503–525 507 vessels without scientific observers, 11 from fish caught The AT data sets from 20 yellowfin at liberty for 154 or by sportfishing boats, and one from a fish caught by a more days were selected for detailed evaluations of their live-bait pole-and-line vessel. movement paths, behaviors, and habitat utilizations. The Four fish (tag nos. 401, 535, 545, and 902) that were AT data from 12 of the 20 fish that exhibited site fidelity, released together on ‘‘the ridge’’ were recaptured together were used to generate and evaluate monthly composite on 26th October 2002 after 14 days at liberty in a set by a home range distributions and vertical habitat distributions, purse-seine vessel. Two fish (tag nos. 549 and 1455) that by day and night, along with composite thermal profiles were released together at Guadalupe Island, did not leave derived from the AT data. Guadalupe Island together, but were recaptured together on For the 20 fish at liberty for 154 or more days, the 25th April 2004 after 198 days at liberty, in a set by a behavior for each day at liberty was classified as type-1 or purse-seine vessel. Two yellowfin (tag nos. 1526 and 1550) type-2 diving behavior. Type-1 diving behavior was char- released in 2003, one at Guadalupe Island and the other on acterized by remaining primarily in depths of less than ‘‘the ridge,’’ were recaptured the same day by the same 100 m. Type-2 diving behavior was defined as the behavior purse-seine vessel in two different sets within about 1.9 km of fish that made ten or more dives to depths greater than of each other. 150 m during the daytime, within a 24-h period. Surface- oriented behavior was defined as the behavior of fish that Data processing remained less than 10 m below the surface for periods greater than 10 min. For each fish, the numbers and dura- Data were downloaded from the tags, and initial exploratory tions of each behavioral event were determined throughout data analyses were conducted, using software provided by the period at liberty. the tag manufacturer (Lotek Wireless 2006). For a daily The AT data sets, for each of the 20 recaptured yel- longitude estimated by light, the latitude at which the SST lowfin at liberty for 154 or more days, were separated into recorded by the tag best matched a remotely-sensed SST periods of nighttime and daytime by using light-level re- along the longitudinal meridian was selected as the corre- cords. Nighttime was classified as the period between the sponding latitude estimate, using the methodology of time of the first record after dusk when there was no rec- Teo et al. (2004). The accuracy and precision of the daily ognizable light from the sun until the time of the last record position estimates were evaluated by calculating the (before dawn) of no recognizable light from the sun. The differences between the known recapture locations for 36 individual data sets for night and day were used in evalu- yellowfin, determined by global-positioning systems aboard ations of diel differences in behavior and habitat utiliza- the fishing vessels, and the corresponding SST-adjusted tion. position estimates. Each set of position estimates for individual yellowfin was integrated into a Geographic Information System Results (GIS). The animal movement analyst extension (AMAE) (Hooge and Eichenlaub 1997; Hooge et al. 2001) and the Reliability of the position estimates ArcView (Environmental Systems Research Institute, Inc., Redlands, CA, USA) GIS program were used for mapping The estimated mean accuracy and precision in the position movement paths and for performing various spatial estimates of longitude, from the light-level data, provided analyses of the data. The site fidelity test in AMAE, by the day log feature of the ATs were 0.41 and 0.13 , employing 1,000 random walks, was used to test the null respectively (Table 2). The estimated mean accuracy and hypothesis of random movement. The test is a modified precision in the position estimates of latitude, from Monte Carlo random walk, starting at the location of re- matching SST data, were 0.82 and 0.28 , respectively lease and constrained by the coastline, and uses the actual (Table 2). sequence of distances between position estimates to Additional information on the reliability of position determine walk points. The fixed-kernel home range estimates derived from the processed AT light-level data model in the AMAE, which incorporates a least-squares and from daily SST data matched to SST data from remote cross-validation smoothing function, was used to assess sensing was obtained by calculating the distances between probabilistic home ranges of fish for which the null known recapture positions and estimated positions (Ta- hypothesis was rejected in the site fidelity test. The 95 ble 2). The average distance between actual and estimated and 50% utilization distributions (probability contours) recapture positions is 108.08 km (95%CI = 28.54). The were chosen to describe the areas probably used (95%) distance between actual and estimated recapture positions and the probable core areas (50%) of activity, respec- ranged from 17.85 to 282.58 km, with just seven obser- tively, of individual fish. vations exceeding 185 km. 123 508 Mar Biol (2007) 152:503–525
Table 2 Thunnus albacares. The accuracy and precision in estimated longitudes from light-level data, and latitudes from sea-surface tem- perature data for 35 fish Tag no. Recapture longitude (dd) Difference Recapture latitude (dd) Difference Distance from actual (km) Actual Estimate Actual Estimate
401 113.13 W 113.30 W 0.17 25.73 N 25.53 N 0.20 28.00 405 118.22 W 118.20 W 0.02 29.02 N 28.39 N 0.63 70.02 450 115.76 W 115.90 W 0.14 24.97 N 24.04 N 0.93 104.30 478 119.83 W 119.40 W 0.43 8.27 N 9.27 N 1.00 120.73 509 109.33 W 108.90 W 0.43 22.07 N 22.02 N 0.05 44.63 525 111.78 W 112.30 W 0.52 23.58 N 23.82 N 0.24 59.26 535 113.13 W 113.00 W 0.13 25.73 N 25.84 N 0.11 17.85 545 113.13 W 113.50 W 0.37 25.73 N 23.25 N 2.48 278.10 549 111.08 W 112.50 W 1.42 22.40 N 21.23 N 1.17 195.87 580 113.15 W 113.10 W 0.05 25.75 N 25.93 N 0.18 20.61 604 113.13 W 113.30 W 0.17 25.72 N 26.19 N 0.47 54.91 644 109.18 W 110.10 W 0.92 20.30 N 18.85 N 1.45 187.72 801 113.12 W 113.30 W 0.18 25.77 N 25.75 N 0.02 18.15 806 111.47 W 110.70 W 0.77 20.72 N 19.47 N 1.25 160.48 826 111.17 W 111.40 W 0.23 23.38 N 23.29 N 0.09 25.50 827 108.85 W 109.00 W 0.15 23.55 N 23.77 N 0.22 28.82 902 113.13 W 113.50 W 0.37 25.73 N 24.79 N 0.94 110.88 1425 118.24 W 118.10 W 0.14 29.08 N 26.54 N 2.54 282.58 1440 118.23 W 119.30 W 1.07 29.18 N 29.31 N 0.13 104.75 1443 115.75 W 116.20 W 0.45 24.97 N 24.74 N 0.23 52.08 1444 115.76 W 116.30 W 0.54 24.97 N 26.10 N 1.13 136.73 1448 110.53 W 111.30 W 0.77 22.83 N 22.68 N 0.15 80.64 1455 111.08 W 112.50 W 1.42 22.40 N 22.68 N 0.28 149.01 1461 111.25 W 111.40 W 0.15 22.75 N 22.37 N 0.38 44.95 1478 115.75 W 116.20 W 0.45 24.97 N 25.93 N 0.96 115.84 1503 115.75 W 116.10 W 0.35 24.97 N 27.33 N 2.36 264.56 1506 112.57 W 112.50 W 0.07 24.08 N 23.86 N 0.22 25.47 1514 111.17 W 111.20 W 0.03 23.40 N 20.96 N 2.44 271.15 1526 110.97 W 110.90 W 0.07 22.55 N 22.24 N 0.31 35.19 1547 112.08 W 112.30 W 0.22 23.67 N 23.12 N 0.55 65.10 1549 118.22 W 118.60 W 0.38 28.99 N 26.67 N 2.32 260.48 1550 110.88 W 110.20 W 0.68 22.68 N 21.93 N 0.75 108.79 1559 110.98 W 111.50 W 0.52 22.33 N 21.88 N 0.45 73.25 1569 114.15 W 113.70 W 0.45 20.47 N 20.61 N 0.14 49.34 1895 115.77 W 115.50 W 0.27 24.98 N 23.77 N 1.21 137.20 Mean 0.41 0.82 108.08 95%CI 0.13 0.28 28.54 The longitudes and latitudes are given in decimal degrees (dd). The differences are that between the actual recapture longitude or latitud and the corresponding estimates. Distance from actual is the distance between the actual recapture position and the estimated position for that day
Movement patterns and spatial statistics 1,161 days are given in Table 3. The movement paths for the 20 fish indicated 19 (95%) remained within 1,445 km The movement paths derived from position estimates of their release locations. The greatest westward movement indicated that all fish remained east of 124 W, west of by a fish (tag no. 1569) was about 872 km west of its 106 W, north of 3 N, and south of 30 N. Data for the release position over 248 days at liberty and the greatest estimated movement paths for 20 fish at liberty from 154 to southward movement by a fish (tag no. 478) was about 123 Mar Biol (2007) 152:503–525 509
Table 3 Thunnus albacares. Spatial statistics for 20 fish at liberty for 154 or more days Tag no. n Distance (km) x speed (km/day) Linearity MSD (km 107) Site fidelity (P) 95% UD (km2) 50% UD (km2)
478 548 56,355 100.63 0.035094 71.10 70.9 NA NA 509 293 21,107 70.83 0.029803 18.70 66.7 NA NA 525 1,042 75,509 64.97 0.002320 4.22 99.9 211,606 19,609 549 198 15,104 75.90 0.079030 22.70 43.4 NA NA 644 298 31,048 102.81 0.027848 13.10 99.5 525,784 88,836 806 278 27,784 99.59 0.008737 9.21 99.7 519,982 75,804 826 275 18,617 64.87 0.015609 7.30 96.1 268,690 25,800 827 150 10,200 66.22 0.050266 3.63 97.5 177,829 25,501 1425 283 20,040 68.87 0.005931 5.06 99.8 184,612 35,218 1448 195 15,985 80.73 0.073569 19.94 56.8 NA NA 1455 193 13,689 68.79 0.085078 20.06 31.2 NA NA 1461 191 12,469 64.61 0.036022 4.44 97.0 162,702 20,230 1506 251 16,592 65.84 0.009143 6.64 95.2 260,675 31,142 1514 283 21,472 73.79 0.054226 14.51 84.1 NA NA 1526 182 12,916 69.82 0.024599 4.16 99.0 242,519 59,515 1547 237 18,675 78.80 0.009987 4.03 99.8 241,767 41,170 1550 188 15,623 81.80 0.065046 21.40 47.3 NA NA 1559 191 12,967 67.17 0.027208 4.53 97.8 218,914 62,096 1569 236 20,495 82.31 0.022832 19.80 76.3 NA NA 1895 167 15,644 88.88 0.005074 1.73 99.9 89,678 10,198 n is the total number of geographic locations in the dataset. Distance is the total distance traveled per dataset. Linearity is the ratio of the distance between the dataset endpoints and the total distance traveled. MSD is the mean squared distance from the center of activity. P is the proportion of MSD values, from a Monte Carlo simulation, greater than the MSD value from the observed data. UD is the utilization distribution, for the 95% and 50% probability levels, reported as area in km2. NA stands for not applicable, as those estimates are valid only if the movement path indicates site fidelity
2,621 km south of its release position over 560 days at northerly movement in early June as SSTs in that area liberty. The fish (tag no. 525) that was at liberty the greatest began to increase above 24 C. Northward movement time (1,161 days) was never more than 913 km from continued during June and July, while staying in SSTs its release position. The estimated mean speeds along above 20 C, until the fish was recaptured by a purse-seine movement paths ranged from 65 to 103 km/day (grand vessel at about 23 N111 W on 27 July 2003. mean = 76.9 km/day, 95%CI = 5.8 km/day). The hypoth- The movement path of a 90-cm yellowfin at release esis that the observed movement path is random was (tag no. 525), at liberty for 1,161 days, is plotted in rejected for 12 of the 20 fish (Table 3). There was no Fig. 3. After release on 13th October 2002 the fish re- significant correlation (r = 0.14, P > 0.05) between the mained in the general area (23–26 N and 113–115 W) for number of days at liberty and the corresponding 95% uti- about 5 months, then moved rapidly southward in March lization distributions (Table 3). to an area off the southern tip of Baja California (Fig. 3a). The movement path of a 94-cm yellowfin tuna at release The fish remained in the general area (22–24 N and 111– (tag no. 826), at liberty for 287 days, is plotted in Fig. 2 114 W) west of the southern tip of Baja California during integrated with monthly composite imagery from remotely- April 2003 through most of July, until moving northward sensed SST data. After release on 13th October 2002, the in late July. The fish moved further northward, returning fish remained in the general area (24–26 N and 113– to the area where it was released, during August and 115 W) off Baja California, for about 4 months until SSTs September 2003, the last 2 months of its first year at dropped to approximately 19 C in late January, at which liberty. During the second year at liberty (Fig. 3b), the time the fish began to move southward. The fish continued fish remained in a relatively restricted area (22–25 N southward during February through April as the 19 C and 112–114 W) during the first 9 months (October isotherm moved south, reaching an area 111–185 km north 2003–June 2004). In July 2004, the fish moved rapidly of the Revillagigedo Islands (18 N and 112–114 W) in southward to an area (18 N and 112–114 W) within the May, where SSTs ranged from 20 to 24 C. The fish spent Revillagigedo Islands Archipelago, and remained there for approximately 3 weeks in this area before beginning a 4 months during the period of August through November, 123 510 Mar Biol (2007) 152:503–525
Fig. 2 Thunnus albacares. Movement path for a fish (tag no. 826), at location. The white dots and lines are the position estimates and liberty for 287 days, integrated with monthly composite imagery from movement paths, respectively. The red square in July is the recapture remotely-sensed SST data. The red square in October is the release location
where SSTs averaged 25.3 C (range 22.5–27.5 C). In the ment paths observed for fish off Baja California are most third year at liberty (Fig. 3c), the fish remained between likely influenced by the seasonal movements of the 18 C 18 and 22 N and 112 and 113 W during October and SST isotherm. November of 2004. For 7 months from December of 2004 to mid-June 2005 the fish remained in the same relatively Behavior restricted area (22–25 N and 112–114 W) west of southern Baja California, as during the previous year. During the Evaluation of the depth and temperature records for yel- later part of June 2005 the fish moved south of 22 Ntoas lowfin tuna carrying ATs in the northern EPO resulted in far as about 19 N, and remained in the area from about the discrimination of four distinct behaviors: (1) type-1 116 to 112 W where SSTs averaged 25.5 C (range 21.2– diving, (2) type-2 diving, (3) deep-diving, and (4) surface- 28.5 C) during July to October 2005. The fish moved oriented. For the 20 fish at liberty for 154 or more days, north of 22 N in November to the same restricted area behavior types 1, 2, 3, and 4 were classified for each day at where it had spent the majority of its life, west of liberty, and the duration of each behavior was determined southern Baja California, where it was subsequently (Table 4). recaptured on 17th December 2005 at which time it was 162 cm long, weighed 84 kg and it was determined to be Type-1 diving behavior a mature female. The position estimates for a 92-cm yellowfin (tag no. The fish remained primarily between the surface and 1425) released at Guadalupe Island indicated residency 50 m at night and between the surface and 100 m during there for the entire 291 days at liberty, where the average the day (Fig. 5). The percentage of total days classified as SST recorded by the implanted AT was 18.6 C (range type-1 diving behavior for individual fish ranged from 16.7–21.4 C). In addition, position estimates for a 130-cm 53.5 to 98.3% (mean = 78.1%; 95%CI = 5.1%). The fish (tag no. 1895) released at Alijos Rocks indicated res- mean duration of type-1 diving behavior ranged from 3.6 idency there for the entire 175 days at liberty, where the to 47.7 days (grand mean = 10.0 days, 95%CI = 4.5 days) average SST recorded by the implanted AT was 19.8 C (Table 4). (range 17.6–24.6 C). A histogram of the daily SSTs recorded in the day log of Type-2 diving behavior the ATs for the 20 yellowfin listed in Table 3, indicates that 95% of the observations are ‡18.3 C (Fig. 4). This The fish remained primarily between the surface and indicates that the southern and northern seasonal move- 50 m at night and from 50 to 300 m during the day 123 Mar Biol (2007) 152:503–525 511
Fig. 3 Thunnus albacares. Movement path for a fish (tag no. 525), at liberty for 1,161 days, plotted along with bathymetry. a Year 1 after release on October 13, 2002; b year 2 after release; c year 3 including an additional 3 months up to recapture on December 17, 2005
123 512 Mar Biol (2007) 152:503–525
Fig. 4 Thunnus albacares. 180 SSTs recorded in day log of n = 5752 Lotek LTD_2310 archival tags 160 from 20 fish in Table 3 140
120
100
80
60 Number of Observations 40
20
0 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 Temperature (C)
Table 4 Thunnus albacares. Summary statistics from the classification of daily behavior of 20 yellowfin tuna at liberty for 154 or more days Tag no. Type-1 diving Type-2 diving Surface oriented % days Events x Duration % days Events x Duration Events x Events/day x Duration
478 75.7 58 7.4 24.3 57 2.4 8,348 16.0 25.4 509 74.2 25 9.6 25.8 24 3.5 3,054 10.9 23.5 525 53.5 129 4.9 46.5 128 4.2 15,843 14.8 38.1 549 77.8 23 7.9 22.2 22 1.9 2,292 12.4 30.9 644 71.5 45 5.1 28.5 44 1.9 4,457 15.6 25.2 806 89.6 26 9.7 10.4 25 1.2 4,601 17.8 26.8 826 71.0 29 7.6 29.0 28 2.9 4,084 15.1 30.4 827 85.1 15 8.8 14.9 14 1.6 2,576 18.1 27.8 1425 98.3 6 47.7 1.7 5 1.0 2,052 10.2 32.5 1448 78.7 32 5.2 21.3 31 1.4 1,856 10.8 30.1 1455 71.8 26 5.5 28.2 25 2.2 1,788 11.2 27.8 1461 78.2 28 5.4 21.8 27 1.6 3,003 16.4 28.3 1506 86.1 19 11.4 13.9 18 1.9 3,524 15.1 28.6 1514 63.9 38 4.9 36.1 37 2.8 3,564 13.7 28.9 1526 65.9 34 3.6 34.1 33 1.9 1,981 11.4 28.6 1547 80.6 28 6.9 19.4 27 1.7 4,052 18.5 30.0 1550 90.1 15 11.5 9.9 14 1.4 2,035 12.4 29.1 1559 80.8 24 6.5 19.2 23 1.6 3,504 19.4 32.4 1569 90.7 21 10.8 9.3 20 1.2 2,967 12.8 23.0 1895 92.6 8 20.5 7.4 7 1.9 2,119 12.6 23.4 Mean 78.1 31.5 10.0 21.2 30.5 2.0 3,943 14.3 28.5 95%CI 5.1 12.1 4.5 5.1 12.1 0.4 1,599 1.3 1.7 The definitions for the three behavioral types and the classification criteria used are given in the text. The percentage of the total days at liberty for which an individual was classified as exhibiting a behavioral type is given as % days. The total number of events observed and classified in each dataset for a behavioral type and the mean duration for those events are given. Durations are given in days, except for surface-oriented events, which are given in minutes
(Fig. 6). Figure 6b shows 30 dives in excess of 150 m a range of 181–302 m. As seen in Fig. 6b, during ascents with an average duration of 11 min and a range of 6– following dives the fish usually return only to depths 15 min. The mean depth of these 30 dives is 246 m, with within the lower mixed layer, presumably to behaviorally 123 Mar Biol (2007) 152:503–525 513
Fig. 5 Thunnus albacares. A Time (Local) Depth and temperature records 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 for a fish (tag no. 826) 0 22.3 exhibiting type-1 diving behavior. a Seven days, November 27–December 2, 15 22.1 2002; b one day, November 29, 2002. Estimated location is 24.5 N 113.7 W 30 21.9
45 20.3 Depth (m) Temperature (C) 60 18.4
75 17.4
90 15.7
B Time (Local) 22:30 1:30 4:30 7:30 10:30 13:30 16:30 19:30 22:30 1:30 0 22.3
10 22.1 20
30 21.9
40 20.3 50 Depth (m) Temperature (C) 60 18.4
70 17.4 80
90 15.7 thermoregulate, before undertaking another dive. The Deep-diving behavior percentage of total days classified as type-2 diving behavior for individual fish ranged from 1.7 to 46.5% Only five of the 20 fish (tag nos. 478, 525, 1448, 1506, and (mean = 21.2%; 95%CI = 5.1%). The mean duration of 1550) in Table 4 exhibited a combined total of ten dives in type-2 diving behavior ranged from 1.0 to 4.2 days (grand excess of 500 m. For those ten dives, the average depth mean = 2.0 days, 95%CI = 0.4 days) (Table 4). For type- was 1,028 m (95%CI 107.9 m; range 737–1,173 m), and 2 diving behavior, the mode for the time the first dive of duration was 45.8 min (95%CI 16.3 min; range 22– the day occurred was 0605 h (95%CI = 0.004 h) 94 min). Three of the dives occurred between 0632 and (Fig. 7a), the mean number of dives per day was 20.2 0940 h, five between 1,302 and 2,002 h, and two occurred (95%CI = 0.49) (Fig. 7b), the mean duration of dives was at night at 0012 and 0246 h. The estimated minimum size 10.3 min (95%CI = 0.04 min), the mean depth of all of a fish exhibiting a deep dive was 95 cm. The fish at dives was 190.2 m (95%CI = 0.36) (Fig. 7c). This type liberty the longest (tag no. 525) did not exhibit a deep dive of diving behavior occurred primarily during the first until it was at liberty for 658 days at an estimated size of two quarters of the year (Fig. 7d) and the mode of the 150 cm. minimum ambient temperature experienced was 12.3 C An example of deep-diving behavior exhibited by an (Fig. 8a), and the maximum DT was 18.8 C with a mode estimated 144-cm yellowfin (tag no. 478), for a dive of of 8.2 C (Fig. 8b). 1.5 h duration is shown in Fig. 9. The dive profile shows a 123 514 Mar Biol (2007) 152:503–525
Fig. 6 Thunnus albacares. A Time (Local) Depth and temperature records 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 18:00 6:00 for a fish (tag no. 826) 0 20.0 exhibiting type-2 diving behavior. a Seven days, February 13–19, 2003; 50 19.7 b one day, February 13, 2003. Estimated location is 21.5 N 100 13.4 112.3 W
150 11.9
Depth (m) 200 11.7 Temperature (C)
250 11.4
300 10.3
350 10.1
B Time (Local) 22:30 1:30 4:30 7:30 10:30 13:30 16:30 19:30 22:30 1:30 0 20.0
50 19.7
100 13.4
150 11.9
Depth (m) 200 11.7 Temperature (C)
250 11.4
300 10.3
350 10.1 maximum depth of 1,160 m, followed by three interesting (Fig. 10a). The duration of events peaked at between 0.25 steps during the beginning phase of the ascent. The and 0.5 h (Fig. 10b). The events occurred throughout the ambient temperature preceding the dive was 28.4 C, the day and night, with a greater proportion at night and a minimum ambient temperature recorded during the dive minimum during the first 4 h following sunrise (Fig. 10c). was 4.5 C, and the fish remained for 1.2 h in ambient The events of greatest duration occur during the first 4 h temperatures below 6 C. The peritoneal cavity temperature following sunset (Fig. 10d). fell from 28.4 to 14.4 C during the dive, and it took about 40 min to return to the initial level following the dive. Habitat
Surface-oriented behavior The habitat utilization by the 12 yellowfin that exhibited site fidelity (Table 3), is presented as monthly composite The mean number of surface-oriented events per day ran- horizontal and vertical spatial distributions (Fig. 11). The ged from 10.2 to 19.4 (grand mean = 14.3, 95%CI = 1.3). horizontal and vertical distributions were similar in Octo- The mean duration of surface-oriented events ranged ber and November, and were reflective of the areas in from 23.0 to 38.1 min (grand mean = 28.5 min, 95%CI = which the fish were tagged and released and the thermal 1.7 min) (Table 4). For surface-oriented behavior, the structure of their environment. There was a southward shift weighted total number of events per month ranged from in the horizontal density distributions of the yellowfin about 11 to 23, with a peak from July to September beginning in December and continuing into May, followed 123 Mar Biol (2007) 152:503–525 515
AB500 160 n = 1437 n = 1437 450 140 400 120 350
300 100
250 80 Frequency 200 Frequency 60 150 40 100 20 50
0 0 0:00 2:00 4:00 6:00 8:00 10:00 12:00 14:00 16:00 18:00 20:00 22:00 10 14 18 22 26 30 34 38 42 46 50 54 58 62 66 70 Hour Number of Dives
12500 D 80 C n = 28795 n = 1437 70 10000 60
50 7500
40
5000 30 Number of Dives
20 2500
Percent of Days Classified as Type II Type as Classified Days of Percent 10
0 0 150 200 250 300 350 400 450 JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC Depth (m) Month
Fig. 7 Thunnus albacares. Summary of all dives, for type-2 diving d percent of days classified as type-2 diving behavior by behavior for 20 fish in Table 3. a Time the first dive of the day month, weighted by the number of days per month for which events occurred; b total number of dives for each day; c depth of all dives; occurred by a slight northward shift from June through August. The purse-seine vessels were from sets ranging from 5 to 55 mt thermal profiles of the vertical habitat of the yellowfin of yellowfin, with an average of 18.2 mt. illustrate a cooling of SSTs and deepening of the mixed layer into February and then a steady increase in SSTs and Tag recoveries shallowing of the mixed layer in March through Septem- ber. The corresponding vertical distributions of the fish for The high recapture rate (53%) for yellowfin tagged with those periods indicate greater daytime depths in relation to ATs in 2002 and 2003 in this study was not unexpected as the deeper mixed layer into February, and then in March– Fink and Bayliff (1970) reported recapture rates of 47.2 September a greater proportion of daytime at shallower and 67.1% for yellowfin tagged with conventional plastic depths in relation to the shallower mixed layer. dart tags (PDTs) off Baja California during 1962 and 1963, respectively. In addition to the 68 yellowfin released with ATs in this study, we released 255 yellowfin in 2002 and Discussion 100 yellowfin in 2003, in similar condition and in the same areas and time periods, with PDTs only. To date 57 The results obtained in this study are important for (22.4%) and 16 (16%) of those yellowfin released in 2002 understanding the horizontal and vertical movement and 2003 with PDTs, respectively, have been confirmed as patterns, diving and surfacing behaviors, and habitat utili- having been recaptured. A significantly higher percentage zation on spatial and temporal scales previously undocu- of yellowfin with ATs were reported as recaptured com- mented for yellowfin. These results should be considered pared to those with only PDTs (P < 0.05), indicating that representative of the behavior of tagged individuals while tagging mortality was probably no greater for the fish with swimming within a school of yellowfin, as the 20 recap- ATs than the fish with just PDTs, and reporting rates are tured fish at liberty for 5 months or more, were all captured better with ATs due to the enhanced value of the reward. and released in schools and subsequently recaptured from The AT recapture rates were consistent for releases in schools. Of those 20 fish, the 17 (85%) recaptured by 2002 (52%) and 2003 (53.5%), but variable with respect to 123 516 Mar Biol (2007) 152:503–525
Fig. 8 Thunnus albacares. For A 9000 all dives for days classified as n = 28798 type-2 diving behavior for 20 8000 fish in Table 3. a Minimum ambient temperatures; b DT 7000 between SST and minimum ambient temperature 6000 y c
n 5000 e u q e
r 4000 F
3000
2000
1000
0 8 9 10 11 12 13 14 15 16 Temperature (C)
B 5000 n = 28798 4500
4000
3500
y 3000 c n e
u 2500 q e r
F 2000
1500
1000
500
0 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 Delta T (SST - Min T)
Fig. 9 Thunnus albacares. Time (Local) Depth and temperature records 16:55 17:10 17:25 17:40 17:55 18:10 18:25 18:40 18:55 19:10 19:25 19:40 19:55 for a fish (tag no. 478) 0 30 exhibiting deep-diving 100 behavior. Estimated location is 200 25 7.5 N 117.1 W 300
400 20
500
600 15
Depth (m) 700 Temperature (C)Temperature 800 10
900
1000 Depth (m) 5 AmbientTemperature (C) 1100 Peritoneal Temperature (C) 1200 0
release location. The recapture rates for fish released on ‘‘the 2003 were 41% (n = 9) and 70% (n = 7), respectively. ridge’’ in 2002 and 2003 were 52 and 64%, respectively, Although these recapture rates may be indicative of high whereas those for Guadalupe Island and Alijos Rocks in regional exploitation rates, the spatial and temporal
123 Mar Biol (2007) 152:503–525 517
25 AB32000 30000 28000 20 26000 24000 22000 15 20000 18000 16000 14000 10 12000 Number of Events 10000 8000 5
Weighted Surface Orientated Events 6000 4000 2000 0 0 1 2 3 4 5 6 7 8 9 10 11 12 0.25 1.50 2.75 4.00 5.25 6.50 7.75 9.00 10.25 11.50 Month Duration (h)
CD4500 1200
4000 1000 3500
3000 800
2500 600 2000 Number of Events
1500 Duration in Minutes 400
1000 200 500
0 0 0 2 4 6 8 10 12 14 16 18 20 22 0:00 3:00 6:00 9:00 12:00 15:00 18:00 21:00 0:00 Hour Time
Fig. 10 Thunnus albacares. Summary of surface-oriented events. a events; c hour of the day the events occurred; d beginning time and Total number of surface-oriented events per month, weighted by the duration of each event number of days per month for which events occurred; b duration of variability in fishing effort including targeting yellowfin in tral Pacific (Itano and Holland 2000), and the western areas of high abundance and their catchability when asso- Pacific (Sibert and Hampton 2003). These findings elicit the ciated with dolphins, makes it difficult to validate. need for spatial stratification in regional stock assessments for yellowfin, including incorporation of geographically- Movement patterns specific fishing mortality rates and life history character- istics. The high degree of residency seen for yellowfin in The movement paths for the 20 yellowfin at liberty for 154 this study and apparent low mixing rate within the EPO or more days (Table 3), indicate that 19 (95%) of the fish regional stock, makes this localized ‘‘substock’’ potentially remained within 1,445 km of their points of release. The more vulnerable to depletion by high levels of fishing effort movement patterns were primarily in southern and northern in the area. In support of this hypothesis is recent genetic directions, remaining within 833 km east or west of the data that shows significant degree of heterogeneity between longitudes at which they were released. Previous studies of eastern Pacific yellowfin using microsatellite loci (Diaz- yellowfin movements off Baja California, based on tagging Jaimes and Uribe-Alcocer 2006). It appears fishery-wide with PDTs, indicated primarily northern and southern resolutions to control fishing effort and catch are unlikely to movements mostly restricted to near the coast of Baja prevent localized depletion in the eastern Pacific. California (Fink and Bayliff 1970). For the 12 yellowfin Little is known regarding environmental influences on that demonstrated site fidelity (Table 3), including the fish the geographical distributions and probable movements of that was at liberty the greatest time (tag no. 525), the yellowfin tuna in the Pacific, aside from the influence of average 95 and 50% utilization distributions during their SSTs on northern and southern ranges (Blackburn 1968; times at liberty were 258,730 km2 (95%CI = 84,349 km2) Sund et al. 1981). Blackburn (1968, 1969) considered and 41,260 km2 (95%CI = 15,712 km2), respectively. These yellowfin to be most abundant in SSTs of 20–30 C, but results indicate regional fidelity for yellowfin within this present in SSTs of 18–31 C. Ortega-Garcia (1998) reported area. Similar conclusions were reached from recent evalu- yellowfin to be distributed in regions where SSTs are ations of yellowfin data for tagging with PDTs in the cen- 17–31 C. Yellowfin movement off Baja California was
123 518 Mar Biol (2007) 152:503–525 previously reported to follow a shift in the 20 C SST moved southward during June 2005 and remained again for isotherm, southward in the autumn and northward in 4 months during the period of July through October, where summer (Blackburn 1969). In the current study, however, it SSTs averaged 25.5 C (range 21.2–28.5 C). These sea- was found that seasonal latitudinal shifts in the 18 C SST sonal cyclical movements and habitat shifts from 20 to isotherms off Baja California strongly influenced the 24 C SSTs to those predominantly greater than 24 C SST northern distribution of yellowfin and their latitudinal were most likely associated with spawning. It appears that movements within this area. only the mature portion of the population of yellowfin The monthly composite 95% utilization distributions of undertook long-distance movements, mostly cyclical, with yellowfin (Fig. 11) are relatively confined in comparison to juveniles resident year round within a highly-productive the large geographical area of apparently favorable thermal foraging area. Some dispersion was also observed, as one habitat based on SST. Thus, it does not appear that SST of these fish (tag no. 478) exhibited the longest movement alone is sufficient for standardization of catch and effort path away from the release location, 2,621 km, and perhaps data. It is noteworthy that the geographical distributions of would not have returned from that area with year round the yellowfin catches by purse-seine vessels in the EPO suitable spawning habitat. during 1965–1998 (Watters 1999) do not appear to be randomly distributed, but aggregated or clustered. Habitat Behavior requirements for the residence of a significant biomass of yellowfin off southern Baja California undoubtedly in- The data obtained in this study from 20 yellowfin at liberty cludes high forage concentrations. Berger et al. (1988) from 154 to 1,161 days with implanted ATs, provides a have reported moderately high levels of primary produc- significant improvement in our understanding of their tion in this region. High concentrations of yellowfin forage behavior and physiological capacity. Type-1 and type-2 (Alverson 1963) have been reported to occur during most diving behaviors were both characterized by remaining months in this area (Longhurst 1966; Moser et al. 1993). within the mixed layer at night, but throughout the day The confined 95% utilization distributions and relatively routinely making dives below the bottom of the mixed concise cyclical movement patterns shown in this study, layer. Previously, ultrasonic telemetry studies of yellowfin suggest that yellowfin have the ability to navigate, perhaps in the Pacific, consisting of acoustic tracking individual using geomagnetic fields and/or celestial bodies for their animals for 1–3 days on the continental shelf or near compass orientation, enabling them to maintain an affinity islands, reported vertical movements to be primarily to this biologically-rich area. Walker et al. (1984) have restricted to within the mixed layer, and occasional brief postulated a magnetic sense organ and possible compass in dives below the thermocline (Carey and Olson 1982; yellowfin, and the ability of captive yellowfin to discrim- Holland et al. 1990; Block et al. 1997; Brill et al. 1999). As inate between different magnetic fields has been demon- seen for yellowfin in this study, AT data recovered from strated. Yellowfin may also have a home range with other tunas including southern bluefin tuna (T. maccoyii) genetically-imprinted geographical coordinates that enable (Gunn and Block 2001), Pacific bluefin tuna (T. orientalis) them to remain within restricted boundaries. (Kitagawa et al. 2000, 2007; Itoh et al. 2003), Atlantic There were three yellowfin (tag nos.478, 525, and 644) bluefin tuna (T. thynnus) (Block et al. 2001), bigeye tuna that probably reached sexual maturity and were reproduc- (T. obesus) (Schaefer and Fuller 2002; Musyl et al. 2003; tively active during times at liberty in this study, based on Evans et al. 2005), albacore (T. alalunga) (Uosaki 2004), estimates of growth and maturity for this area (Wild 1986; and skipjack (Katsuwonus pelamis) (Ogura 2003), have all Schaefer 1998, 2001). Each of those fish undertook sea- demonstrated distinct diurnal variability, consisting of sonal southward movements into suitable spawning habitat, shallower distributions at night than during the day. with SSTs greater than about 24 C (Schaefer 1998, 2001). Type-2 diving behavior, previously unreported for For the fish at liberty the greatest time (tag no. 525) we yellowfin, appears to be an alternative foraging strategy, confirmed that it was a mature female 162 cm in length and targeting prey organisms of the vertically-migrating deep weighing 84 kg at recapture. The movement path (Fig. 3) scattering layer (DSL) during the day, probably in areas and ambient temperature data recorded by the tag indicated and times when forage is not available within the upper that during the second year at liberty this fish, at an esti- 100 m. Tont (1976) reported mean daytime depths of the mated length of 139 cm, moved southward during July DSL of 282 m in the California Current and 319 m in the 2004 and remained for 4 months during the period of tropical eastern Pacific, which coincides fairly well with August through November, where SSTs averaged 25.3 C the depths of yellowfin exhibiting type-2 diving behavior. (range 22.5–27.5 C). Following a cyclical northward The mode in the distribution of times of the first type-2 movement, returning to the same area from which it had dive is 06:05 h, corresponding with the descending DSL at departed and remaining for several months, the fish again dawn (Fig. 7a) (Fiedler et al. 1998). This daytime foraging 123 Mar Biol (2007) 152:503–525 519 behavior by yellowfin on the DSL prey organisms is Bigeye tuna carrying ATs in the equatorial EPO were probably a continuation of foraging on the same prey the estimated to spend 54% of their days at liberty targeting previous night within the mixed layer. prey organisms of the DSL during the day, in depths of Twelve of the 20 yellowfin at liberty for 154 or more 200–350 m (12 C) with relatively few brief vertical forays days were recaptured in association with dolphins in purse- into the mixed layer to thermoregulate (Schaefer and Fuller seine sets. The average length of the 12 fish was 116.3 cm 2002). In contrast, type-2 diving behavior by yellowfin in (95%CI = 14.65; range = 89–172 cm). For the last 10 days the northern EPO is characterized by relatively frequent prior to recapture, the average percentage of days classified brief dives to depths of 150–250 m (12 C), the same as type-2 diving behavior for the fish associated with dol- minimum ambient temperature to those experienced by phins was 31% (95%CI = 18.7%; range = 0–100%), and bigeye in equatorial EPO. Whereas yellowfin possess for the eight fish not associated with dolphins when central and lateral heat exchangers, with the lateral retia recaptured was 30% (95%CI = 23.7%; range = 0–80%). vessel surface area relatively small, bigeye possess highly- For the 12 fish recaptured with dolphins the first time they developed lateral heat exchangers, with the central heat- exhibited type-2 diving behavior was an average of 26 days exchanger lost or reduced and additional retia that function after release (range = 7–46 days), at an average length to elevate temperatures of their viscera, eyes, and brains of 86 cm (95%CI = 5.7 cm; range = 72–100 cm), and for (Godsil and Byers 1944; Gibbs and Collette 1967; Collette those fish not recaptured with dolphins was an average 34 1978; Carey 1982; Graham and Dickson 2001). The in- days after release (range = 12–73 days), at an average creased heat exchanger surface area are thought to enable length of 93 cm (95%CI = 15.3; range = 76–135 cm). bigeye tuna to remain for extended periods of time well Considering the value in being able to discriminate whether below the thermocline (Holland et al. 1992; Brill and tagged yellowfin were with dolphins, we conducted other Bushnell 2001; Brill et al. 2005). The maximum swimming exploratory data analyses of the AT data, but eventually depths of yellowfin were previously described as limited to concluded that the depth data alone are impractical for such water temperatures 8 C below the SST (Brill et al. 1999). classification. A potential basis for the association of yel- In the present study the distribution of the differences be- lowfin schools with dolphin herds in the EPO is the tween SSTs and minimum ambient temperatures experi- inherent ability for dolphins to more efficiently locate enced during all dives by yellowfin for days classified as concentrations of DSL prey organisms with their sonar type-2 diving behavior, show a maximum of 18.8 C, with capabilities (Au 1993), as both species are known to feed the mode at 8.2 C (Fig. 8). on these prey (Alverson 1963; Perrin et al. 1973; Robertson Yellowfin deep-diving behavior, dives in excess of and Chivers 1997). It appears that yellowfin form strong 500 m, was exhibited by five fish for a combined total of bonds with dolphins as they will swim rapidly to remain ten dives. There are a few plausible reasons why yellowfin with dolphins even when being chased by purse-seine may undertake these occasional extreme dives into great vessels and speedboats during fishing operations. Dolphin depths, including searching for food, predator avoidance, diving behavior consists of diurnal differences in patterns, or exploration of bathymetry. During the 1.5-h duration with relatively shallow cyclical dives during the day to dive to 1,160 m (4.5 C) by a 144-cm yellowfin in this depths mostly less than 20 m, (above the thermocline), study (Fig. 9), the peritoneal temperature of the fish fell whereas diving bouts below the thermocline began about from 28.4 to 14.4 C, and the difference between SST and 30 min after sunset and lasted until about 30 min before minimum ambient temperature experienced was 23.9 C. sunrise (Chivers and Scott 2002). Dolphin diving below the This particular dive, based on its profile, was probably a thermocline could be for improved performance of their foraging event, in contrast to shorter-duration deep dives. sonar and foraging on DSL prey organisms (Robertson and The three staircase steps in the profile following the ascent Chivers 1997). The findings in this study indicate type-2 phase appear to be indicative of powered ascent and sub- diving behavior occurs about equally whether yellowfin are sequent gliding events (Weihs 1973). Such behavior may associated or not associated with dolphins. Understanding also serve as a stealth technique for capturing prey, by the dynamics of the association of yellowfin with dolphins minimizing detection, and subsequent avoidance. has been pursued for many years, with a primary motiva- The diving and thermal data in this study indicate that tion being dolphin-safe fishing by purse-seine vessels the depth and temperature tolerances of yellowfin are far (Joseph 1994; Perrin 2004). The critical missing informa- greater than previously assumed. The ability to remain for tion on frequency and duration of associative events could prolonged periods at extreme depths and temperatures are potentially be obtained by using yellowfin, as autonomous limited by a combination of the physiological capacity for samplers, with implanted acoustic ATs to validate when body size, heat retention, thermal inertia, cardiac function, they are associated with dolphins by recording the dolphins and individual tolerance for thermal stress. Deep dives in sonar pulse trains (Wang et al. 2005). excess of 1,000 m have also been reported from AT data 123 520 Mar Biol (2007) 152:503–525
Pernce t Peerntc -75 -60 -45-30 -15 0 105 3 405 6 75 -60-45-30-150 154 30 5 60
15 15 A B 45 45
75 75
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135 135
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225 225
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811 147201 22326 9 32 811 14217 0 23226 9 32 Temperatur e (C) Tmpere atur e()C Peernc t Peetrc n -60 -45-30 -150 154 3065 0 --45060 --3 150 15304560
15 15 C D 45 45
75 75
105 150
153 153
156 156
159
Depth (m) 159 Depth (m)
252 252
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8111 1427202326392 8111 1427202362392 Tmpere atur e()C Tpem eeratu r()C
Fig. 11 Thunnus albacares. Monthly horizontal and vertical com- days; j July: five fish, 179 days; k August: two fish, 101 days; l posite utilization distributions for the 12 fish exhibiting site fidelity in September: one fish, 90 days. The left panels for each month illustrate Table 3. a October: 12 fish, 278 days; b November: 12 fish, 392 days; the 95% (blue) and 50% (red) weighted fixed-kernel density c December: 12 fish, 426 days; d January: 12 fish, 416 days; e distributions. The right panels are depth frequencies by night (black February: 12 fish, 383 days; f March: 12 fish, 402 days; g April: 11 bars) and day (open bars) and average temperature within depth fish, 331 days; h May: seven fish, 270 days; i June: seven fish, 228 intervals (blue) for Atlantic bluefin tuna (Block et al. 2001), bigeye tuna behavior is useful for evaluating optimal detection periods in the EPO (Schaefer and Fuller 2002) and the Coral Sea for the use of remote-sensing techniques for conducting (Evans et al. 2005), and yellowfin in the Indian Ocean fisheries-independent abundance estimation of this species, (Dagorn et al. 2006). utilizing airborne optical equipment including LIDAR Yellowfin tuna schools exhibiting surface-oriented (Gauldie et al. 1997; Lo et al. 2000; Larese 2005). behavior during the day have been called breezers, boilers, black spots, and shiners and during the night fireballs, Habitat white spots, and poppers by tuna fisherman (Scott 1969). Surface-oriented behavior by yellowfin has been observed The horizontal and vertical habitat utilization by yellowfin in association with feeding activities, floating objects, and the influence of seasonal oceanographic conditions dolphins, whales, and whale sharks, and with courtship and on the distributions described in this study provides an spawning behavior. The greater seasonal occurrence during improved ecological understanding for this species in the July through October and the frequency and duration dur- northern EPO. The seasonal latitudinal shifts in the hori- ing the night of yellowfin surface-oriented events observed zontal habitat utilization distributions off southern Baja in this study (Fig. 10), is relevant to understanding catch- California (Fig. 11) appear to be influenced by the 18 C ability (vertical vulnerability plus spatial vulnerability) by SST isotherm, as only 5% of the SST observations re- purse-seine vessels, and may be useful to incorporate into corded by tags in yellowfin were less than 18.3 C (Fig. 4). the standardization of catch and effort data. In addition, this There are, however, a few divergent examples in this study, information on occurrence and duration of surface-oriented including the yellowfin (tag no. 1425) that resided at 123 Mar Biol (2007) 152:503–525 521
Peerc nt Percetn -60 -45 -30 -15 015430650 -06 -540--53 1015304560
15 15 E F 4545 45
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8111 14 7220 3226392 81111472202362392 Tmpere atur e()C Tpaem err teu (C) Peerntc Pernce t -75 -65 0 --04 35-051 103546075 -90 -60 0 -003 30609 G 15 H 15 45 45
75 75
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8111 14 7 202232639 2 8111 14 720 236232 9 2 Tmpere atur e()C Tmpere atur e()C
Fig. 11 continued
Guadalupe Island during its 291 days at liberty, including The relatively short duration of the dives, 10.3 min on the entire winter, when SSTs fell to a minimum of 16.7 C. average, indicates yellowfin, in contrast to bigeye, do not Although it has been determined that the 18 C SST iso- have the thermoregulatory physiological capacity to re- therm influences the habitat utilization by yellowfin near main for prolonged periods below the mixed layer (Brill the northern extent of their distribution off Baja California, et al. 2005). They do, however, have the physiological elucidating the various factors responsible for the confined ability to fairly rapidly increase their body temperature horizontal distributions is complex. The horizontal habitat following a dive to within about 0.5 C of ambient, upon utilization by yellowfin in the EPO is, however, strongly ascent to the bottom of the mixed layer. Yellowfin, bluefin, influenced by geographic features such as gulfs and islands, and albacore tunas exhibit a cold-induced cardiac brady- bathymetric features such as banks, ridges, and seamounts, cardia when exposed to acute changes in water temperature and dynamic physical oceanographic processes such as (Korsmeyer et al. 1997; Blank et al. 2004). This decrease gyres, upwelling, eddies, convergence, and frontal zones in cardiac performance with temperature results in a (Sund et al. 1981). High prey densities have been shown to reduction of the cardiac output during a dive. Recent be associated with these features and processes, providing measurements of atrial and ventricular sarcoplasmic good foraging areas for which yellowfin exhibit a high reticulum calcium cycling indicate that yellowfin tuna have affinity (Blackburn 1968, 1969). a lower capacity than bluefin to maintain calcium ATPase Vertical movements of yellowfin are not restricted by (SERCA2) activity in the cold. Increased expression of the the depth of the thermocline, but by body temperature SERCA2 enzyme has been shown to be correlated with cooling rates and physiological performance at depths cold tolerance in Thunnus (Landeira-Fernandez et al. below the mixed layer. The repetitive type-2 diving 2004). The rapid ascents following short duration bounce behavior during the day, to depths of 150–250 m and about dives most likely is required for reoxygenation of the 12 C ambient temperature, observed for 21% of days in oxygen stores. Utilizing this bounce diving capability, this study, indicates the thermal capacity for yellowfin to along with repetitive diving, is an efficient strategy for exploit prey at substantial depths below the thermocline. optimizing foraging time below the thermocline. 123 522 Mar Biol (2007) 152:503–525
Fig. 11 continued
This study indicates that 78% of days at liberty yel- indicate that yellowfin spend, on average, 93.0% (range lowfin encountered sufficient forage within the mixed layer 73.0–93.5%) of their time in the mixed layer at night and, to depths of 100 m while utilizing habitats close to the on average, 21.3% (range 12.1–31.0%) of their time below coast or islands (Table 4). In contrast, in the offshore EPO, the mixed layer during the day. Habitat-based stock within the mixed layer and depths of less than 100 m, the assessment models have been developed for the integration concentrations of forage organisms are far less abundant of behavioral and environmental data, in order to stan- during the day, due to their highly patchy distributions dardize catch and effort, based on estimating fishing depths (Blackburn et al. 1970). Thus, foraging on DSL prey of longline gear in relation to the vertical distribution of the organisms at night in the mixed layer and during the day target species by time of day (Hinton and Nakano 1996; below the thermocline by yellowfin is potentially a far Bigelow et al. 2002, 2003). We suggest that the data pro- more common behavior in the offshore EPO, then indicated vided in this study on horizontal and vertical habitat uti- by the 21% of days at liberty (Table 4) estimated in this lization by yellowfin, and also the surfacing behavior, be study. considered for integration into stock assessment models for The monthly composite vertical and thermal distribu- exploring vulnerability to detection and catchability by tions for yellowfin in this study (Fig. 11) indicate seasonal purse-seine vessels. Considering the regional fidelity ob- variability, with greater daytime depths in relation to the served for yellowfin in this study area, and the variability in deeper mixed layer and a greater proportion of daytime at the oceanography throughout the EPO, additional archival shallower depths in relation to the shallower mixed layer. tagging studies in other regions should be encouraged. ATs recovered from yellowfin in this study have provided extensive and unique data on their vertical thermal habitat Acknowledgments This research was supported by the Tagging of that should be useful for habitat-based standardization of Pacific Pelagics, a program of the Census of Marine Life. We are indebted to Captain T. Ekstrom and crew aboard the FV Royal Star catch and effort data for yellowfin by purse-seine and for their invaluable assistance, and to all the passengers who partic- longline fisheries in the northern EPO. The data in Fig. 11 ipated enthusiastically in catching fish to be tagged and released.
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We thank Shimano American Corporation and Izorline International Pacific bluefin tuna hearts in response to acute temperature Corporation for product support of our tuna tagging efforts. We are change. J Exp Biol 207:881–890 grateful to vessel owners, captains, fishers, unloaders, and industry Block BA (2005) Physiological ecology in the 21st century: representatives for returning recovered ATs. We are thankful to the Advancements in biologging science. Integr Comp Biol personnel of the IATTC Ensenada and Mazatlan field offices for 45:305–320 assistance in recovering ATs. We also thank S. Teo, R. Matteson, and Block BA, Keen KE, Castillo B, Dewar H, Freund EV, Marcinek DJ, M. Castleton for processing the SST-adjusted latitude estimates and Brill RW, Farwell C (1997) Environmental preferences of G. Strout. We appreciate the constructive comments on drafts of the yellowfin tuna (Thunnus albacares) at the northern extent of its manuscript provided by W. Bayliff, R. 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