Kurt M. Schaefer, Daniel W. Fuller and Barbara A. Block

Transcription

1 Vertical Movements and Habitat Utilization of Skipjack (Katsuwonus pelamis), Yellowfin (Thunnus albacares), and Bigeye (Thunnus obesus) Tunas in the Equatorial Eastern Pacific Ocean, Ascertained Through Archival Tag Data Kurt M. Schaefer, Daniel W. Fuller and Barbara A. Block Abstract Skipjack, yellowfin, and bigeye tunas were caught and released with implanted archival tags in the equatorial eastern Pacific Ocean between 24 and 26. The depth and temperature data from five recovered archival tags for each species were analyzed and compared among species while at liberty within the same geographically defined area. Evaluations of the timed depth records resulted in discrimination of distinct vertical movement patterns for each species, including association with floating objects, daytime foraging below the thermocline in depths of the deep scattering layer, surface orientation, and deep diving in excess of 5 m. During the daytime, skipjack and yellowfin tunas occasionally exhibited repetitive bounce-dive foraging behavior well below the thermocline to depths of the deep scattering layer, between 225 and 4 m. Bigeye tuna were foraging during the daytime at similar depths of about m, except when undertaking upward forays. The deepest dives recorded for skipjack, yellowfin, and bigeye tunas were 596, 122, and 1695 m, respectively. The vertical habitat utilization distributions indicate that skipjack, yellowfin, and bigeye tunas, when not associated with floating objects, spent 99, 96, and 92%, respectively, of their time above the thermocline during the night, but spent 37, 44, and 57%, respectively, of their time below the thermocline during the day. The apparent species-specific physiological abilities and tolerances to environmental characteristics of their vertical habitat, including dissolved oxygen and temperature, are evaluated. Results of this study on the comparative vertical movements, behavior, and habitat utilization for these species, should also be useful in evaluations of species-specific vulnerability to purse-seine and longline fisheries in this region. Keywords Archival tags Behavior Habitat Movements Tunas K.M. Schaefer (B) Inter-American Tropical Tuna Commission, 864 La Jolla Shores Drive, La Jolla, CA , USA kschaefer@iattc.org J.L. Nielsen et al. (eds.), Tagging and Tracking of Marine Animals with Electronic Devices, Reviews: Methods and Technologies in Fish Biology and Fisheries 9, DOI 1.17/ , C Springer Science+Business Media B.V

2 122 K.M. Schaefer et al. Introduction The large-scale purse-seine fishery targeting tuna aggregations associated with floating objects in the equatorial eastern Pacific (EEPO) catches primarily skipjack and bigeye tunas, with lesser amounts of yellowfin tuna. Additionally, significant catches of unassociated skipjack schools, as well as yellowfin in association with dolphins are also made between about 5 N and 15 S (Anonymous 26). Bigeye and yellowfin are the primary target species of the Asian distant-water longline fisheries operating in this same geographical area of the EEPO (Anonymous 26). It is important to conduct field studies seeking to understand the comparative behavior of skipjack, yellowfin, and bigeye tunas, particularly when associated with floating objects, to attempt to standardize the purse-seine catch per unit of effort (CPUE) for inclusion in stock assessments (Maunder 25). In addition, results from such studies can potentially yield solutions for minimizing undesirable catches by purse-seine vessels of species associated with floating objects, through modifications in fishing techniques, yet still maintain high CPUE levels for skipjack (Schaefer and Fuller 25; Schaefer and Fuller 27c). In recent years tagging experiments utilizing electronic tags, particularly archival tags (ATs), with free-ranging tunas, have provided significant data toward understanding the movements, habitat utilization, and physiology for those species investigated (Gunn and Block 21; Block 25). A study of bigeye in the EEPO, utilizing archival tags, provided an opportunity for classification of daily behavior types, including association with floating objects and daytime foraging at depths of the deep scattering layer (DSL), from relatively long time series records, and also defining diurnal and seasonal changes in habitat utilization distributions (Schaefer and Fuller 22). A study of skipjack in the EEPO (Schaefer and Fuller 27a), utilizing archival tags, provided astonishing insights into skipjack behavior, including repetitive bounce diving, to daytime depths similar to those occupied by bigeye for probable foraging within the DSL, and also provided data to construct diurnal habitat utilization distributions. Field studies utilizing acoustic telemetry and echosounder imaging to simultaneously observe bigeye and skipjack tunas within large multispecies aggregations associated with floating objects in the EEPO (Schaefer and Fuller 25), have provided additional information on the behavior of these species. Although an investigation of yellowfin tuna behavior, utilizing archival tags, in a study off Baja California, Mexico (Schaefer and Fuller 27b) indicated their ability to also perform repetitive bounce diving behavior to depths of the DSL similar to that observed for skipjack tuna, nothing has previously been published regarding their vertical movements and habitat utilization in the EEPO. The objectives of this investigation were to elucidate and compare the vertical movement patterns and habitat utilization distributions of skipjack, yellowfin, and bigeye tunas, utilizing archival tag data, within the same geographical area of the EEPO. By evaluating the behavioral and physiological constraints, along with the environmental variables, that define the vertical habitat for these species, we can improve our understanding of their behavior and provide useful information for inclusion in stock assessments and resource management applications (Brill et al. 25; Maunder et al. 26; Hobday and Hartmann 26).

3 Vertical Movements and Habitat Utilization of Tunas 123 Materials and Methods Tag Releases Tagging was conducted on the chartered FV Her Grace, a 17.7 m pole-and-line fishing vessel. The details regarding the materials and methods utilized in the capture, tagging, and release of the tunas are given in the papers by Schaefer and Fuller (22; 27a,b). The capture and release locations for the five bigeye from which archival tag data sets were recovered and used in this study was in close proximity to a Tropical Atmosphere-Ocean (TAO) mooring at about 2 S95 W. The capture and release locations for the five skipjack and five yellowfin from which archival tag data sets were recovered and used in this study was in close proximity to a TAO mooring at about 2 N95 W. The LTD 231 (Lotek Wireless, Inc. St. John s, Newfoundland, Canada) geolocating archival tags implanted in the peritoneal cavity of the bigeye and yellowfin were programmed to sample depths, ambient and internal temperatures, and light levels at 1-min intervals. The LTD 11 (Lotek Wireless, Inc. St. John s, Newfoundland, Canada) non-geolocating archival tags implanted in the peritoneal cavity of the skipjack were programmed to sample depths and temperatures at 3-s intervals. Tag Recoveries Data on the lengths of the fish and years in which they were released and recaptured are given in Table 1. Recapture locations by species are shown in Fig. 1, ranging from 37 km to 2292 km and 123 to 259 for skipjack, from 514 km to 2487 km and 8 to 332 for yellowfin, and from 2 km to 1358 km and 269 to 328 for bigeye, of their release locations. Table 1 Summary of archival tag data utilized for behavioral comparisons Species Number Tag type Length Year Days of data Skipjack 5 LTD Yellowfin 5 LTD Bigeye 5 LTD Data Processing Data were downloaded from the tags using software provided by the tag manufacturer. The data from the LTD 11 tags recovered from skipjack consisted of d of depth and temperature data from each tag. The light-based geolocation data obtained from the LTD 231 tags recovered from yellowfin and bigeye, were processed using the unscented Kalman filter with a sea-surface temperature matching program described by Lam et al. (28), to obtain the most probable movement paths, along with the adjusted daily position estimates.

4 124 K.M. Schaefer et al. Fig. 1 Linear displacements for five skipjack tunas, carrying non-geolocating archival tags, and movement paths for five yellowfin and fivebigeyetunas,carrying geolocating archival tags, released in the equatorial eastern Pacific Ocean. Release positions are indicated by white squares and recapture positions indicated by colored stars for each species. The white box indicates the area from which the vertical movements data for the three species is compared The area defined as 5 Nto5 S and 9 W to 15 W in the EEPO (Fig. 1) was chosen for comparisons of the vertical movements and habitat utilization of the skipjack, yellowfin, and bigeye tunas. For five skipjack, all the recovered archival tag data, consisting of a total of 48 days of data (Table 1), were utilized, assuming they remained within this area during their first 1 d at liberty. For the five yellowfin and five bigeye tuna only the archival tag depth and temperature data sets corresponding to estimated positions along the most probable movement paths within the defined area, were used in the analyses (Fig. 1). For yellowfin, this consisted of a total of 137 d of data, and for bigeye a total of 425 d of data (Table 1). For each of the three species the behavior for each day at liberty was classified as associated or unassociated with floating objects, based partially on the observed behavioral characteristics from ultrasonic telemetry observations of skipjack and bigeye associated simultaneously with floating objects in this area (Schaefer and Fuller 25). Behavior associated with floating objects was characterized by fish remaining primarily at depths, during the day, less than that of the thermocline, 2 C isotherm (Fiedler and Tally, 26). Associative behavior, based on analyses of the species-specific depth data collected by archival tags recovered from fish released in association with floating objects, was defined as when yellowfin remained 98%, and bigeye remained 92.5% of the time above the 2 C isotherm. Behavior unassociated with floating objects included bounce-diving for skipjack and yellowfin, defined as the behavior of fish that made 1 or more dives to depths greater than 15 m during the daytime within a 24-h period. For bigeye, characteristic unassociated deep behavior was defined as fish descending previous to dawn, apparently tracking the DSL, undertaking brief upward excursions to within the mixed layer during the day and tracking the DSL to the surface during its ascent at dusk. Surface-oriented

5 Vertical Movements and Habitat Utilization of Tunas 125 behavior was defined as the behavior of fish that remained less than 1 m below the surface for periods greater than 1 min. Deep-diving behavior was defined as when fish exceeded 5 m in depth. The AT data sets were separated into periods of nighttime and daytime by using the times of nautical twilight. Nighttime was classified as the period between the time of the first evening record after nautical twilight until the time of the last morning record before nautical twilight. The individual data sets for night and day were used in evaluations of diel differences in behavior and habitat utilization. Dissolved oxygen concentrations at depth, based on shipboard measurements within the defined study area in 25, were extracted from the World Ocean Atlas (Garcia et al. 26) in order to include them in graphical overlays, along with other environmental data, such as ambient temperature and depth, to conduct evaluations of the comparative behavior and physiology of these tunas relative to those values. Results Associative and Non-associative Behavior with Floating Objects The vertical movements for a representative 66-cm skipjack during the first week following tagging and release are shown in Fig. 2a. The fish remained relatively shallow, within the mixed layer, and associated with the drifting vessel for just over 3 h before the vessel abruptly departed and separated from the tuna aggregation. Within 48 h of the separation, non-associative behavior, consisting of relatively shallow nighttime depths and bounce diving during the day to depths between about 15 m to 3 m, are illustrated in Fig. 2a. The vertical movements for the first complete 24-h period following tagging and release (Fig. 2b) illustrate in finer detail the associative behavior with the vessel, including the depth of the fish relative to that of 2 C isotherm, conventionally used to represent thermocline depth in the equatorial Pacific (Fiedler and Talley 26). The fish is observed to remain above that depth when associated with the vessel. A greater range in the depth of the vertical movements is observed during the night, with a greater average depth than during the day. The vertical movements for a representative 52-cm yellowfin during the first week following tagging and release are shown in Fig. 3a. The fish remained relatively shallow, within the mixed layer, and associated with the drifting vessel for just over 24 h before the vessel abruptly departed and separated from the tuna aggregation. Non-associative behavior, consisting of bounce diving during the day, with dives from about 15 m to 2 m and relatively shallow at night, began almost immediately after the separation of the vessel from the tuna aggregation and lasted for about 48 h. Following that event, the fish exhibited associative behavior with a floating object for the following 4 d of this record. The vertical movements for the first complete 24-h period following tagging and release (Fig. 3b) illustrate in finer detail the associative behavior with the vessel, including the depth of the fish relative to that of the 2 C isotherm. The fish is observed to remain primarily above that depth when associated with the vessel. The fish was on average, shallower at night

6 126 K.M. Schaefer et al a b 2 C Fig. 2 Depth and temperature records for the first week after release for a 66-cm skipjack, released in April 24, with an implanted Lotek LTD11 archival tag (a) and the first 24-h period following release (b). The black bars indicate night time

7 Vertical Movements and Habitat Utilization of Tunas Vessel Separation a C b 12.8 Fig. 3 Depth and temperature records for the first week after release for a 52-cm yellowfin, released in April 26, with an implanted Lotek LTD231 archival tag, (a) and the first 24-h period following release (b). The black bars indicate night time

8 128 K.M. Schaefer et al a C b 15. Fig. 4 Depth and temperature records for the first week after release for an 88-cm bigeye, released in May 25, with an implanted Lotek LTD231 archival tag (a) and the first 24-h period following release (b). The bigeye remained associated with the tagging vessel for nine days following release. The black bars indicate night time

9 Vertical Movements and Habitat Utilization of Tunas 129 Table 2 Summary statistics from the classification of daily behavior of the five individuals of each species. The mean duration of bounce-diving, characteristic, and associative events is given in days, and that for surface orientation in minutes Bounce-diving Associative Surface Oriented Species % days Events Mean Duration % days Events Mean Duration Events Events/day Mean Duration Skipjack Mean Yellowfin Mean Characteristic Bigeye Mean

10 13 K.M. Schaefer et al. and exhibited considerable range in vertical movements, whereas during the day it was at a consistently greater depth, just above the thermocline. The vertical movements for a representative 88-cm bigeye during the first week following tagging and release are shown in Fig. 4a. The fish remained relatively shallow, primarily within the mixed layer, and associated with the drifting vessel for this period until the vessel departed 9 d following the tagging event, and separated from the tuna aggregation. The vertical movements for the first complete 24-h period following tagging and release (Fig. 4b) illustrate in finer detail the associative behavior with the vessel, including the depth of the fish relative to that of 2 C isotherm. The fish is observed to remain above that depth when associated with the vessel. For this initial 24-h period, following tagging and release, there do not appear to be any diurnal differences in the vertical movement patterns or the depths utilized. The summary statistics from the classification of daily behavior, as being associative behavior, for the five individuals of each species throughout their times at liberty within the area, is given in Table 2. Considering the limited duration of time series data collected for the five skipjack, we do not present the summary statistics for this behavior. For yellowfin the percentage of days classified as associative per fish ranged from 2.7% to 19.4% (mean = 1.4%) and for bigeye from 11.2% to 25.% (mean = 15.9%). For yellowfin the number of associative events per fish ranged from 3 to 18 (mean = 6.8), and for bigeye from 2 to 1 (mean = 4.4). For yellowfin the duration of events per fish ranged from 1 d to 5 d (mean = 1.4 d), and for bigeye from 1 d to 14 d (mean = 3.7 d). Skipjack and Yellowfin Non-associative Bounce-Diving Behavior An example of a day of bounce-diving behavior for a 66-cm skipjack is shown in Fig. 5a. There was a distinct diurnal vertical movement pattern, from shallow at night to a U-shaped pattern of bounce diving during the day to depths of about m. The fish was apparently tracking the descending DSL prey field for foraging, beginning just before dawn and returning to the surface at around dusk. The depths of the dives coincide with reported daytime DSL depths of 3 4 m in the EEPO (Fiedler et al. 1998). The total number of bounce dives in Fig. 5a, greater than 15 m, is 5, with a mean duration between descent and ascent of 6.8 min. Note the line superimposed in Fig. 5a at 25 m and ambient temperature of 12.2 C, where the dissolved oxygen concentration (DO) is estimated to be about 1 ml/l. The frequency of the greatest depth for each day in which bounce diving was observed by the five skipjack is shown in Fig. 5b. The range of observations is m, with a mean of 299 m. The frequencies for the minimum ambient and peritoneal temperatures for all bounce dives deeper than 15 m (Fig. 5c) show a mean ambient temperature of 12.7 C and mean peritoneal temperature of 22.9 C. An example of a day of bounce diving-behavior for a 52-cm yellowfin is shown in Fig. 6a. There was a distinct diurnal vertical movement pattern, shallow at night

11 Vertical Movements and Habitat Utilization of Tunas ml/l Dissolved Oxygen a Frequency Frequency b c Minimum Ambient Temperature Minimum Peritoneal Temperature Fig. 5 Bounce-diving behavior for a 66-cm skipjack released in April 24 (a). Summary of bounce-diving events for the five skipjack, showing the frequency of the greatest depth for each day (b), and the frequencies for the minimum ambient and internal temperatures for all bounce dives deeper than 15 m (c)

12 132 K.M. Schaefer et al a 1 ml/l Dissolved Oxygen Frequency Frequency b c Minimum Ambient Temperature Minimum Peritoneal Temperature Fig. 6 Bounce-diving behavior for a 52-cm yellowfin released in April 26 (a). Summary of bounce-diving events for the five yellowfin showing the frequency of the greatest depth for each day (b), and the frequencies for the minimum ambient and internal temperatures for all bounce dives deeper than 15 m (c)

13 Vertical Movements and Habitat Utilization of Tunas 133 to bounce diving during the day, apparently tracking the descending DSL prey field for foraging. Most dives ranged between 225 and 275 m, and again note the overlay of the estimated depth of the DO at 1 ml/l of 25 m and ambient temperature of about 12.5 C. The total number of bounce dives greater than 15 m in Fig. 6a, was 27, with a mean duration between descent and ascent of 13.5 min. The frequency of the greatest depth for each day in which bounce diving was observed by the five yellowfin is shown in Fig. 6b. The range of observations is m, with a mean of 294 m, close to what was found for skipjack tuna. The frequencies for the minimum ambient and peritoneal temperatures for all bounce dives deeper than 15 m (Fig. 6c) shows a mean ambient temperature of 12.9 C and mean peritoneal temperature of 23.5 C, also very similar to what was found for the skipjack tuna. Bigeye Non-associative Characteristic Behavior An example of a day of non-associative characteristic behavior for a 88-cm bigeye is shown in Fig. 7a. There is a distinct diurnal vertical movement pattern observed, from shallow at night to much greater depths, below the thermocline, during the day. The fish descended before dawn, probably tracking and foraging on the DSL prey organisms. As it did so this fish remained for periods of up to 2 h 7 min at depths it apparently searched between 2 and 275 m and undertook just 9 upward excursions to mixed layer depth apparently to warm up before returning to the same depth zone to continue foraging on DSL prey organisms and then tracking the DSL to the surface during its ascent at dusk. Again note the overlay of the depth of the DO at 1 ml/l at 25 m and ambient temperature of about 11.8 C. The frequency of the greatest depth for each day in which the five bigeye were observed is shown in Fig. 7b. The range of observations is m, with a mean of 328 m, slightly deeper but still very similar to the skipjack and yellowfin daytime bounce diving depths in this area. The frequencies for the minimum ambient and peritoneal temperatures for all non-associative characteristic days by bigeye (Fig. 7c) show a mean ambient temperature of 11.5 C and mean peritoneal temperature of 15.7 C. These data indicate that bigeye are within their comfort zone foraging for prolonged periods at these depths, allowing their peritoneal cavity temperatures to decrease to about 8 C below the average of those for the skipjack and yellowfin, because of their greater tolerance for low ambient temperatures and DO. The summary statistics from the classification of daily behavior, as bounce diving for skipjack and yellowfin or non-associative characteristic for bigeye, for the five individuals of each species throughout their times at liberty within the area, are given in Table 2. The percentage of days classified as bounce diving per fish ranged from 54.1 to 75.7% (mean = 66.3%) for skipjack, and from 8.8 to 72.1% (mean = 31.7%) for yellowfin, and for non-associative characteristic behavior per fish from 15.8 to 56.3% (mean = 32.3%) for bigeye. The number of bounce-diving events per fish ranged from 1 to 2 (mean = 1.4) for skipjack, and from 5 to 28 (mean = 12.8)

14 134 K.M. Schaefer et al a ml/l Dissolved Oxygen 11.4 Frequency Frequency b c Minimum Ambient Temperature Minimum Peritoneal Temperature Fig. 7 Characteristic non-associative behavior for an 88-cm bigeye released in May 25 (a). Summary of characteristic non-associative events for the five bigeye, showing the frequency of the greatest depth for each day (b), and the frequencies for the minimum ambient and internal temperatures (c) for yellowfin, and for non-associative characteristic behavior per fish from 4 to 22 (mean = 11.8) for bigeye. The duration of events per fish ranged from 5 to 7 d (mean = 6.3 d) for skipjack, from 1 to 15 d (mean = 2.7 d) for yellowfin, and from 2.4 to 6.5 d (mean = 3.4 d) for bigeye.

15 Vertical Movements and Habitat Utilization of Tunas 135 Surface-Oriented Behavior The summary statistics for the mean number of surface-oriented events per day, from the classification of unassociated behavior, for the five individuals of each species throughout their times at liberty within the area, is given in Table 2. The mean number of surface-oriented events per fish ranged from 83 to 128 (mean = 19) for skipjack, from 213 to 2271 (mean = 88) for yellowfin, and from 112 to 1951 (mean = 87) for bigeye. The number of surface-oriented events per day per fish ranged from 1 to 25 (mean = 11.7) for skipjack, from 1 to 42 (mean = 1.1) for yellowfin, and from 11 to 37 (mean = 7.9) for bigeye. The duration of these events per fish ranged from 1 to 56 min (mean = 23.1 min) for skipjack, from 1 to 267 min (mean = 21.2 min) for yellowfin, and from 1 to 412 min (mean = 22.5 min) for bigeye. Deep-Diving Behavior An example of a 596-m deep dive by a 66-cm skipjack, along with the ambient temperature and DO concentration profiles, is shown in Fig. 8a. The profile of the dive relative to the climatological oceanography is most interesting, particularly when considering that the DO concentration fell below 1 ml/l at depths greater than about 25 m, and at 3 m the DO was about.63 ml/l. The fish, however, was able to physiologically tolerate at least 2 min in that environment. It should also be noted that at an ambient temperature of 1 C at 3 m the fish s peritoneal cavity temperature cooled only to about 22 C during this dive. An example of a 122-m dive by a 51-cm yellowfin, along with ambient temperature and DO concentration profiles, is shown in Fig. 8b. The fish tolerated at least 4 min at an ambient temperature of about 6 C, with an average DO value of about 1.5 ml/l, well above the minimum value of about.5 ml/l at 4 m, in the minimum DO zone. This dive profile appears to indicate the cooling of core temperature to about 14 C during this dive, before the fish ascended back into the warm upper mixed layer. An example of a 1695-m dive for an 84-cm bigeye, along with temperature and oxygen profiles, is shown in Fig. 8c. The fish tolerated at least 4 min at an ambient temperature from 1 to 3 C, and DO concentration values from about 1 to 2 ml/l. This dive profile appears to indicate the cooling of core temperature to about 18 C during this dive, before the fish ascended back into the warm upper mixed layer. Vertical Habitat Utilization The vertical habitat utilization distributions for the five skipjack, yellowfin, and bigeye tuna, for unassociated behavior, is presented as composite distributions, by night and day, along with the thermal profiles in Figs. 9a,b,c, respectively. The

16 136 K.M. Schaefer et al. 12: 12:1 12:2 12:3 12:4 12:5 13: Depth 5 Dissolved Oxygen 1 Peritoneal Temperature a Ambient Temperature Dissolved Oxygen (ml/l) :55 2:1 2:25 2:4 2:55 3:1 3:25 3:4 3: b Dissolved Oxygen (ml/l) 22:35 22:5 23:5 23:2 23:35 23:5 : c Dissolved Oxygen (ml/l) Fig. 8 Deep-diving behavior, with temperature and oxygen profiles, for a 66-cm skipjack (a), 51-cm yellowfin (b), and 84-cm bigeye (c)

17 Vertical Movements and Habitat Utilization of Tunas Percent a Percent Percent Night Day Ambient Temperature b c Fig. 9 Vertical habitat utilization distributions, by day and night, for the five skipjack (a), yellowfin (b), and bigeye (c), for all days for which the behavior was classified as unassociated

18 138 K.M. Schaefer et al. distributions for the skipjack indicate that the fish remained above the depth of the thermocline (44 m) during the night 98.6% of the time, but spent 37.7% of their time below the thermocline during the day. The distributions for the yellowfin indicate that the fish remained above the depth of the thermocline (46 m) during the night 96.2% of the time, but spent 43.6% of their time below the thermocline during the day. The distributions for the bigeye indicate that the fish remained above the depth of the thermocline (7 m) during the night 91.7% of the time, but spent 57.2% of their time below the thermocline during the day. Discussion The results obtained in this study are useful for comparative evaluations of vertical movement patterns and habitat utilization distributions of skipjack, yellowfin, and bigeye tunas on previously undocumented spatio-temporal scales. Knowledge about the behavior of each of these species, when associated and not associated with floating objects, in the EEPO where large-scale industrial purse-seine and longline fisheries operate, are important for understanding their behavior, assessing their catchability, and evaluating potential modifications to fishing techniques for reduction of the bycatches of non-target species (Brill et al. 25; Maunder 25; Maunder et al. 26). Since 1994 purse-seine fishing effort directed at tunas associated with fish-aggregating devices (FADS) has significantly increased in the EEPO, resulting in substantial increases in catches of skipjack and bigeye tunas. The vertical movement patterns for the three species observed in this study, when associated with floating objects, are similar to those reported by Schaefer and Fuller (25) for skipjack and bigeye tunas associated with floating objects in the EEPO. This associative behavior with floating objects is characterized by swimming depths predominantly shallower than the depth of the thermocline, throughout the day and night, with average nighttime depths slightly deeper or shallower than those during the day. The differences in nighttime depths relative to daytime depths of these tunas when associated with floating objects, is apparently dependent on the presence or absence of prey organisms of the DSL within the mixed layer, with the former providing nighttime foraging opportunities, which appears to result in greater average nighttime depths. Ultrasonic telemetry studies on the simultaneous behavior of skipjack, yellowfin, and bigeye tunas associated with drifting fish-aggregating devices in the central Pacific Ocean also indicated swimming depths to be predominantly shallower than the thermocline depth, about 115 m, throughout the day and night, but with average nighttime depths shallower than those during the daytime (Matsumoto et al. 26). There is insufficient archival tag data from the five skipjack, due to their short periods at liberty in this study, for any reasonable estimate of the percentage of days skipjack spent associated with floating objects. For yellowfin tuna, there may be some biases in separating associative behavior with floating objects from other types of shallow behavior within the mixed layer. However, we believe based on

19 Vertical Movements and Habitat Utilization of Tunas 139 observations of vertical movements of yellowfin when known to be associated with floating objects following releases and preceding recaptures, the estimate of an average of 1.4% of days at liberty (Table 2) is reasonable. For bigeye the estimate of an average of 15.9% of days at liberty and duration of 3.7 d (Table 2) associated with floating objects is fairly close to the estimates of 18.7% and 3.1 d, previously estimated from 23 archival tag data sets from bigeye at liberty in this area for more than 3 d (Schaefer and Fuller 22). Whereas the average number of associative events with floating objects by yellowfin (6.8) is slightly greater than for bigeye (4.4), the average duration of the events is significantly greater for bigeye (3.7 d) than for yellowfin (1.4 d) (Table 2). It appears, based on these observations and the greater overall recapture rate of 43.% for bigeye versus 16.6% for yellowfin from concurrent conventional tagging in this area (Anonymous 28) that bigeye have a greater affinity for floating objects, and thus a greater vulnerability to capture by purse-seine vessels than do yellowfin in this area. The repetitive bounce diving events, observed in this study, were previously reported for these skipjack (Schaefer and Fuller 27a) and for yellowfin in the Pacific Ocean off northern Mexico (Schaefer and Fuller 27b). These events occurred between dawn and dusk to daytime depths of the vertically-migrating DSL (Tont 1976; Kuznetsov et al. 1982) apparently for foraging on prey organisms consisting primarily of mesopelagic fish and cephalopods. The diel vertical movement pattern for unassociated bigeye observed in this study, consisting of tracking prey items of the vertically-migrating DSL (Longhurst 1976; Josse et al. 1998), was previously reported for bigeye in this area (Schaefer and Fuller 22). Depths of the DSL in the tropical eastern Pacific have been reported to be 3 4 m during the day and 1 m at night (Tont 1976; Fiedler et al. 1998). Variation in daytime DSL depths is probably a function of light penetration (which is regulated by biological production) and absorption of light by chlorophyll and phaeopigments (Tont 1976). Based on the classification percentages of daily behavior types for each of the three species in Table 2, there are obviously other common vertical movement patterns for these species, when unassociated with floating objects, undoubtedly related to prey availability and successful foraging strategies. We believe the estimate of 66% of days in which skipjack were classified as exhibiting bounce-diving behavior in this study (Table 2) may not be representative of their annual vertical foraging patterns, due to the short duration of the time series data obtained. Regardless, the average duration of 6.3 d of bounce-diving behavior observed for skipjack clearly indicates that this is a common foraging strategy employed by skipjack in this area. The percentage of days classified as bounce diving for yellowfin (31.7%) and characteristic behavior for bigeye (32.3%) (Table 2) are very similar, with the average number of events per fish and average durations of events also similar for the two species. The percentage of days classified as bounce diving for 19 yellowfin at liberty for 3 or more days in an earlier study in the Pacific off northern Mexico (Schaefer and Fuller 27b) was 21.2%. This lower percentage of days yellowfin spent foraging on DSL prey organisms in that coastal region off Mexico is probably the result of availability of other prey and foraging opportunities within the mixed layer. The percentage of days classified as characteristic behavior

20 14 K.M. Schaefer et al. for 23 bigeye in this area in the earlier study was 54.3% (Schaefer and Fuller 22). The lower percentage of days spent foraging on DSL prey organisms by bigeye in the present study is potentially a result of availability of other prey and thus a different successful foraging strategy. The results from the present study indicate that yellowfin and bigeye were spending similar amounts of their time during the day foraging on prey organisms of the DSL in this area. An ecological benefit of endothermy in tunas is an expanded thermal niche, including exploitation of their vertical habitat (Block 1991; Graham and Dickson 21). There are several anatomical and physiological differences between skipjack, yellowfin, and bigeye (Brill and Bushnell 21; Graham and Dickson 21; Brill et al. 25) that would explain why skipjack and yellowfin unlike bigeye, are unable to remain for extensive periods at optimal daytime foraging depths (Holland and Sibert 1994; Schaefer and Fuller 22). Skipjack and yellowfin exhibit repetitive bounce diving behavior apparently to employ behavioral and physiological thermoregulation to gain partial independence from cold water effects on temperature-dependent rate functions (Graham and Dickson 24). Thermal inertia also helps stabilize body temperatures during dives, and larger bigeye tuna have been reported to have slower cooling rates than do smaller individuals (Schaefer and Fuller 22; Malte et al. 27). Tuna s heart rates are reduced by lower temperatures and hypoxia, so excursions below the thermocline may be limited by the heart s diminished capacity to supply the oxygen requirements of the endothermic tissues (Brill and Bushnell 21). It appears that skipjack and yellowfin tunas exhibit bounce diving events because of their physiological inability to remain at depths of the DSL and the low DO concentrations (less than 2 ml/l). There may well also be a low oxygen/temperature effect. Bigeye, although their vertical habitat is undoubtedly constrained by hypoxic conditions (perhaps anything less than about 1. ml/l), can remain at depths of 25 3 m for prolonged periods, undertaking upward excursions when they get cold, with the frequency related to fish size and thermal inertia (Schaefer and Fuller, 22; Malte et al. 27). The prolonged deep-diving events by skipjack and yellowfin tunas below the depth of the oxygen minimum zone in the EEPO, appear to confirm that low DO concentrations are an important factor restricting their foraging time at 25 3 m. It is apparent that characteristic bigeye daytime unassociated behavior and the occasional bounce-diving behavior observed for skipjack and yellowfin tunas to depths of 25 3 m in the EEPO is related to foraging on prey organisms of the DSL. The DO concentration at 25 m in this area is about 1. ml/l. Laboratory studies have indicated that bigeye are more tolerant of lower ambient oxygen concentrations (hypoxia) (Bushnell et al. 199) and their blood has a higher oxygen affinity than yellowfin or skipjack tunas (Lowe et al. 2). Based on the bigeye archival tag data and the DO at depth profiles presented in this study, it appears that the value that Hanamoto (1987) had previously reported of 1 ml/l, 17% saturation at 15 C appears to be fairly close to the lower oxygen concentration boundary for bigeye in the EEPO.

21 Vertical Movements and Habitat Utilization of Tunas 141 It was reported from laboratory experiments that the lower lethal temperature is 15 C and lower lethal DO level is 1.9 ml/l for skipjack (Dizon et al. 1977; Gooding et al. 1981), so it appears that it is a combination of their physiological limits to low temperature and DO that limits the amount of time skipjack are able to remain within this zone of the DSL for foraging. Although the empirical data regarding lethal limits for temperature and oxygen concentrations have not been reported for yellowfin, we assume somewhat similar physiological limitations to their bounce diving behavior and inability to remain at these depths for prolonged periods, as seen for bigeye tuna. The rapid ascents following short duration bounce dives by skipjack and yellowfin are most likely required for reoxygenation of the oxygen stores. Laboratory research determining the comparative lower lethal ambient temperatures and DO concentrations for all three of these tuna species must be conducted if we are to understand the physiological limitations to their vertical movements and habitat utilization observed by archival tags. Information on the surface-oriented behavior of these tuna species, as reported in this study (Table 2) is relevant to understanding catchability (vertical vulnerability plus spatial vulnerability) by purse-seine vessels, and may be useful to incorporate into the standardization of catch and effort data (Maunder M. 25). In addition, this information on occurrence and duration of surface-oriented behavior is useful for evaluating optimal detection periods for the use of remote-sensing techniques for conducting fisheries-independent abundance estimation of this species. The number of surface-oriented events per day observed in this study appears highest for skipjack and lowest for bigeye, with the mean duration of events nearly equal for the three species (Table 2). Deep-diving behavior, dives in excess of 5 m, was observed for each of the three species in this study. Some plausible reasons why they undertake these occasional extreme dives into great depths include foraging behavior, predator avoidance, or exploration of bathymetry. The profiles of these dives including depths, ambient and internal temperatures, and DO concentrations are very informative (Fig. 8). The skipjack and yellowfin dive profiles illustrate fairly remarkable tolerances to low ambient tempertures and DO concentrations at depths, which are probably close to the lower physiological tolerances for these species. The bigeye dive profile also illustrates remarkable physiological thermoregulation, plus an understanding of the basis of how these fish can survive dives to depths in excess of 1 m, well below the oxygen minimum zone (about 3 5 m) where the DO concentrations are about 2 ml/l. The composite depth and temperature habitat utilization distributions for the three tuna species while exhibiting non-associative behavior with floating objects in this study (Fig. 9), indicate obvious daytime species-specific variability. These distributions indicate that skipjack, yellowfin, and bigeye tunas spent 37, 44, and 57%, respectively, of their time below the thermocline during the day, with bigeye spending the greatest percentage of time at depths within the DSL. The archival tag data sets for the three species of tunas in this study have provided extensive and unique data on comparative vertical thermal habitat that should be useful for habitat-based standardization of catch and effort data by purse-seine

22 142 K.M. Schaefer et al. and longline fisheries in the EEPO. Habitat-based stock assessment models have been developed for the integration of behavioral and environmental data, in order to standardize catch and effort, based on estimating fishing depths of longline gear in relation to the vertical distribution of the target species, such as bigeye tuna, by time of day (Maunder et al. 26). We suggest that information such as that provided in this study from archival tagging data on the vertical habitat utilization for each of these species, and also surface-oriented behavior, be considered for exploring vulnerability to detection and catchability by purse-seine vessels and integrated into stock assessment models for standardization of catch-per-unit of effort (CPUE) data for purse-seine vessels. Large-scale studies using archival tags are needed to improve our understanding of skipjack, yellowfin, and bigeye tuna movements, behavior, and habitat utilization, which will provide useful information for improving stock assessments for these species. Elucidating behavior may also permit the design of optimal fishing strategies for these species, including reduction of current bycatch levels associated with purse-seine fishing around floating objects. Conclusion Our investigations utilizing archival tags implanted in skipjack, yellowfin, and bigeye tunas provide new insights into the comparative vertical movements, behavior, habitat utilization, and physiology of these species in the EEPO. The vertical movements and habitat utilization, obtained from archival tagging data, for skipjack in the western Pacific Ocean (Ogura 23) and bigeye near the Hawaiian Islands (Musyl et al. 23) and the Azores Islands (Arrizabalaga 28) are very different than those observed for these species in the EEPO. Our findings include the frequency and duration of all three species for associative behavior with floating objects, foraging behavior at daytime depths of the DSL, surface-associated behavior, deep-diving behavior, and vertical and thermal habitat utilization distributions at night and during daytime. Along with the knowledge obtained from archival tag data on the ecology, including movements and habitat utilization, of these species, estimation of the species-specific vulnerability to longline and purse-seine fisheries can be significantly improved. Far greater knowledge of the physiological abilities and tolerances of these species derived through laboratory studies, and their habitat utilization derived through archival tags, are required to understand changes in their behavior and gear vulnerability relative to variable oceanographic conditions in order to develop appropriate procedures for standardization of CPUE. Acknowledgments This research was made possible through financial contributions by the Japan Fisheries Agency, Taiwan Fisheries Agency, United States Tuna Foundation, and the Tagging of Pacific Pelagics (Census of Marine Life). We are grateful to vessel owners, captains, fishermen, unloaders, industry representatives, and Inter-American Tropical Tuna Commission field office staff for assistance in recovering the archival tags. We appreciate the constructive comments on drafts of the manuscript provided by W. Bayliff, and two anonymous reviewers.

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