OCEANOGRAPHIC IMPLICATIONS FOR THE MANAGEMENT OF ATLANTIC BLUEFIN TUNA, THUNNUS THYNNUS

OCEANOGRAPHIC IMPLICATIONS FOR THE MANAGEMENT OF ATLANTIC BLUEFIN TUNA, THUNNUS THYNNUS By, Gaelin Rosenwaks Date: Approved: Dr. Richard Barber, Advisor Dr. William H. Schlesinger, Dean Master s project submitted in partial fulfillment of the requirements for the Master of Environmental Management degree in the Nicholas School of the Environment and Earth Sciences of Duke University 2004 1

ABSTRACT Atlantic bluefin tuna, Thunnus thynnus, have been targeted and exploited by fishermen for thousands of years and continue to be an important commercially and recreationally caught fish. These powerful swimmers are able to cross the Atlantic Ocean rapidly, creating a need for international management. In this study, pop-off satellite archival tags are used to reveal the patterns of the Atlantic bluefin movements. The fish show distinct behaviors that are coherent with large-scale oceanographic features. They seem to use various oceanographic cues in their determination of location although these cues vary for individual fish. Using ocean color and sea surface temperature images, this study seeks to define these patterns of movement in relation to these cues in order to better understand the behavior of the Atlantic bluefin tuna. The ocean is not a static environment so determination of oceanographic cues may prove essential to proper management of ABFT and determination of stock dynamics. 2

TABLE OF CONTENTS I. Introduction II. Tuna Natural History i. Physiological Adaptations for a Pelagic Lifestyle ii. History of Fishery and Management iii. Tag-A-Giant III. Materials and Methods i. Tags ii. Fish iii. Analysis IV. Results i. Overview of Results ii. The Eastern Fish iii. The Western Residents iv. Behavior of Fish 02680 during two weeks in February V. Discussion i. Movements ii. Fish 02680 iii. Management Implications VI. Conclusions VII. Figures VIII. Acknowledgements IX. Literature Cited 3

LIST OF FIGURES Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 7 Figure 8 Figure 9 Figure 10 Figure 11 Map of Atlantic Bluefin Management Boundaries Pop-off Satellite Tag Set Up PAT-Tag Endpoint Location Map April Fish Tracks Overlayed on Ocean Color and Sea Surface Temperature 30-day Composite Images Map of Eastern Fish Tracks May Fish Tracks Overlayed on Ocean Color and Sea Surface Temperature 30-day Composite Images Flow Chart Describing Atlantic Bluefin Movements during PAT tag Deployment June Fish Tracks Overlayed on Ocean Color and Sea Surface Temperature 30-day Composite Images July Fish Tracks Overlayed on Ocean Color and Sea Surface Temperature 30-day Composite Images Fish LTD1013 track during April, Overlayed on Ocean Color and Sea Surface Temperature 30-day Composite Images Map of Western Resident Fish Tracks for Duration of Tag Deployment. Figure 12 Fish Track of Fish 02680 for February 1-February 17, 2003 Figure 13 Fish 02680 Pressure Depth Temperature Profiles for 8 Days in the First Two Weeks of February 4

I. INTRODUCTION The Atlantic bluefin tuna (ABFT), Thunnus thynnus, is a highly migratory species found throughout the Atlantic Ocean and Mediterranean Sea. ABFT grow to over 3 m and can weigh more than 680 kg. These powerful swimmers can migrate across the Atlantic Ocean rapidly (Block, et al. 2001), and they have evoked the interest of scholars, poets and fishermen since the times of Aristotle. Fishermen have harvested ABFT for thousands of years in the Mediterranean Sea (Maggio, 2000) and began to harvest them in the United States in the early 1900s (Buck, 1995). The life history of the ABFT and the intense fishing pressure on them make management of their fisheries difficult. Furthermore, the trans-atlantic movement of ABFT creates a need for international management. Currently, the ABFT are divided into two management units, an eastern and western unit based on the assumption that the ABFT are two stocks. Population estimates of the western stock show a 90% decline in spawning stock biomass, while eastern stocks have not shown as dramatic a decline. To aid in the recovery of the western spawning stock, catch quotas in the west are currently less than 2,500 metric tons, as opposed to the east, where catches are on the order of thirty times higher. While ABFT are managed with total allowable catch quotas, size limits, and gear restrictions, modifications of current regulations and additional measures focusing on ecologically realistic management (Testimony of David Wilmot, 2003) are necessary to help rebuild their populations in the face of increasing fishing pressure. In order to further our understanding of ABFT, tagging studies have been developed to address behavior, mixing rates, spawning site fidelity, and population dynamics (Block, et al, 2001). The tagging research has shown that ABFT behavior is 5

much more complex than once thought, but with the new observations, we now can begin to describe, if not explain, the movements and migratory behavior of these fish with greater detail and precision. These tags can help to elucidate questions regarding west to east crossing, mixing and mortality rates, and movements in relation to oceanographic variables. The seasonal movements of ABFT are complex across space scales from the ocean basin to local fronts. Their migratory behavior is roughly coherent with large-scale oceanographic features; however, the behaviors of individual fish show a variety of different preferences and patterns. It is not clear why an individual fish follows a given movement behavior, but all movements seem to be in relation to thermal fronts or ocean color gradients with different fish orienting to different values and staying within that range. In order to address the questions arising from the movements of ABFT, it is necessary to understand how the changing environment affects these movement patterns. In this study, recent observations from innovative new electronic tags are analyzed to determine the migratory behavior of ABFT and the management implications of this complex behavior. 6

II. TUNA NATURAL HISTORY i. PHYSIOLOGICAL ADAPTATIONS TO A PELAGIC LIFESTYLE The life history of ABFT is difficult to study due to their pelagic habitat, however great progress has been made in the understanding of ABFT migratory movements, depth preferences and thermal preferences through various tagging studies (Block, et al, 1998; Brill, et al, 2002). ABFT have the widest thermal niche of all Scombridae fish due to their large body size and ability to conserve metabolic heat (Carey and Teal, 1966). They are endothermic and have been found in waters as cool as 3 C and, when entering spawning grounds, water as warm as 29.5 C, (Carey and Teal, 1966; Block, et al, 1998, Block, et al, 2001). Endothermy in tunas is achieved through various physical adaptations including a high metabolic rate, specialized tissues, a large heart and counter current heat exchangers (Altringham and Block, 1997; Graham and Dickson, 2001; Brill and Bushnell, 2001; Korsmeyer and Dewar, 2001). Tunas are able to elevate red muscle temperatures by axial positioning of aerobic muscle mass in the circulatory system as well as counter current heat exchangers, rete mirabilia (Carey and Teal, 1966). The rete mirabilia reduce the heat loss at the gills and body surfaces so that heat generated by muscle contraction is conserved. ABFT are able to maintain internal body temperatures over 21 C above ambient temperatures (Block, et al, 2001; Marcinek, et al, 2001). Along with the lateral counter current heat exchangers, ABFT have additional heat exchangers in the cranial cavity and viscera giving the ABFT and other bluefin species an added ability to stay warm (Carey, et al, 1984). Ambient temperature therefore does not appear to set strict physiological limits on the movements 7

of bluefin tuna throughout much of the world s oceans, however the heart is outside of the counter current heat exchangers which may limit cardiac performance in very cold waters (Blank, et al, 2004). Other physical attributes, particularly morphological characteristics, contribute to the success of bluefin tunas in their pelagic environment and their niche as powerful swimmers. Tunas are fusiform fishes, a form that maximizes swimming efficiency. In addition, tunas have a body thickness to length ratio that is close to optimal for minimizing drag (Hertel, 1966). They have a zone of modified skin that appears to reduce microturbulence to decrease drag while they are swimming. Other attributes to diminish drag are a narrow caudal peduncle and lateral keels to direct the movement of the water. Dorsal finlets also serve to minimize drag as the body tapers after the midline. One of the most impressive characteristics of tuna external physiology is the presence of slots on the body surface in which the pectoral fins fit snuggly when not in use. Most of the thrust for swimming comes from the caudal fin, increasing swimming efficiency due to the aforementioned characteristics (Altringham and Block, 1997). ABFT have two known spawning areas, one in the Gulf of Mexico and another in the Mediterranean Sea (McGowan and Richards, 1989; NRC, 1994). Spawning occurs from mid-april to mid-june in the Gulf of Mexico, and from June to August in the Mediterranean Sea (Rodriquez-Roda, 1967; Baglin, 1982; NRC Report, 1994). In addition to temporal differences in spawning, studies have shown that the age of sexual maturity in the two spawning areas is different with the Gulf of Mexico spawners reaching maturity at ten years and 200 cm (Baglin, 1982), while the Mediterranean spawners reach maturity earlier at five years and 130 cm (Rodriguez-Roda, 1967). 8

Questions still exist as to the degree of mixing between the fish spawning at these sites and whether additional spawning sites exist (NRC Report, 1994; Lutcavage, et al, 1999). However with various tagging studies and improving electronic tag technology, great strides have been made in understanding ABFT behavior and migration patterns (Block et al, 1998; Block et al, 2001; Brill, et al, 2002). The mixing rate of ABFT in the Atlantic, once thought to be less than 2%, is now thought to be at least 20%, creating a need for a reassessment of management practices (NRC Report, 1994). ii. HISTORY OF FISHERY AND MANAGEMENT The Atlantic bluefin tuna have been targeted and exploited by fishermen for thousands of years and continue to be an important commercially and recreationally caught fish. Prized for their amazing fight, ABFT have been targeted in the sport fishing industry throughout the 20 th Century, with various recreational tournaments landing thousands of fish that were discarded after being weighed. The commercial fishery in the United States began to grow in the 1960s with the market demand for ABFT increasing. The 1970s saw a large number of vessels targeting small fish for canneries, while longline vessels targeted higher quality fish for the sashimi market in Japan. Before this time, larger fish were deemed unfit for human consumption and canning and were sold to dog and cat food producers (Buck, 1995). This practice ended with the increased demand for high quality tuna meat by the Japanese who saw the stocks of Pacific Bluefin declining rapidly and costs for their distant water fishing fleet increasing. The development of modern refrigeration and new methods to rapidly cool fish created a market for fresh bluefin, previously thought to be low quality because the high 9

endothermic body temperatures of the large fish caused them to spoil quickly (Bergin, et al. 1996). Dwindling numbers of ABFT in the 20 th century led to the ratification of the International Convention for the Conservation of Atlantic Tunas in 1966. This convention mandated the formation of a commission, the International Commission for the Conservation of Atlantic Tunas (ICCAT) whose mission is to maintain the populations of tunas and tuna-like fishes found in the Atlantic Ocean and adjacent seas at levels permitting the maximum sustainable catch for food and other purposes (ICCAT, 1966). With authority over the management of ABFT, the ICCAT has set forth regulations on the fishery since its inception in 1969. The stock of ABFT was in rapid decline in the l970s with an ever-decreasing catch per unit effort. This decline led to the ICCAT and the United States National Marine Fisheries Service performing various stock assessments for ABFT to put forth better management practices. In 1981, the ICCAT scientists recommended that the population of ABFT be divided into two management units, an eastern and western stock. The stock assessments confirmed that stocks of ABFT were in severe decline but when divided, only the western stock was in immediate danger. The ICCAT passed a resolution dividing the Atlantic Ocean into two management units with the recommendation to decrease the western quota to as near zero as possible (ICCAT, 1981). The boundary was placed at forty-five degrees West longitude in the Northern hemisphere and twenty-five degrees West longitude in the Southern hemisphere. This boundary essentially divided the ocean in half, down the length of the Atlantic Basin (FIGURE 1). While the placement of the boundary appears 10

arbitrary, it was based on what were then currently accepted theories of migration and population subdivision. In 1981, conventional tagging studies illustrated that trans-atlantic migrations occurred, but the degree of mixing was unknown although presumed to be less than 2% (NRC, 1994). With the knowledge of the limited mixing, two spawning locations, varying sizes of maturity and smaller fish in the Mediterranean, the available observations seemed to indicate that the two-stock theory was justified (Safina, 2001). Dividing the populations also had positive political implications because, with the division, a property right was assigned to both sides of the Atlantic. The US felt that they could adequately manage the western stock of ABFT while the European and African countries would be free to manage and exploit the eastern stock of ABFT as they saw fit (Whynott, 1995). Nearly all of the member nations supported this recommendation including the US, Japan, and Canada, who were to split the western quota. The division enabled the western Atlantic countries to implement strict regulations without the direct involvement of the eastern Atlantic countries in hopes of establishing a recovery plan for the western resident tunas (Buck, 1995). In addition to the two management units, the quota allotted to the western Atlantic was reduced by 55%, a compromise from the recommended near zero quota. This quota was to cover scientific monitoring. Since 1981, the eastern and western stocks of ABFT are assessed every second year, and the western quota is adjusted. In 1983, size limits on ABFT were imposed for the entire Atlantic, stopping the harvest of fish smaller than 3.2 kg, captured in the Mediterranean for canneries. In 1990, the western management unit s quota was to be reduced by another 50%, but this reduction was strongly opposed by the industry, so the 11

quota was reduced by only 10%. The decreasing quotas for the western Atlantic have created an asymmetric distribution of effort and catch in the Atlantic Ocean with the eastern Atlantic harvesting at least two-thirds of the average ABFT catch (Fontenau, 1996). The asymmetric quotas for ABFT and emerging scientific evidence for increased trans-basin mixing have led to the re-evaluation of current management practices, particularly two-stock management. The ICCAT realizes that new scientific evidence points to more mixing than previously thought and has passed resolutions to re-examine the boundary between the east and west Atlantic as early as 1996 (ICCAT, 1996). In 2000, the ICCAT passed a resolution to examine the degree of mixing of the migrating fish and the appropriateness of the boundary (ICCAT, 2000). This move was followed with a resolution to increase tagging studies, using state-of-the-art electronic tags to examine further the behavior of these elusive fish, and increase genetic studies, and larval and spawning studies to test the degree of mixing between spawning sites (ICCAT, 2001). iii. TAG-A-GIANT The Tag-a-Giant program was developed in 1996 by Dr. Barbara Block of the Hopkins Marine Station, Stanford University, to help understand the behaviors and movements of ABFT. Tag-a-Giant is a comprehensive tagging study in which electronic tags are deployed on ABFT in January off the coast of North Carolina. The waters off of North Carolina in the winter provide a unique and ideal setting for this tagging effort as the ABFT aggregate in tremendous numbers not far from the coast. 12

III. MATERIALS AND METHODS i. Tags Sixteen Pop-off Satellite Archival Tags (PAT-Wildlife Computers, Redmond, Washington, USA) were deployed on Atlantic bluefin tuna off the coast of North Carolina in January 2003 during Tag-A-Giant. These tags are hardware version 2.5 and software version 2.08e. PAT tags previously have been described (Marcinek, et al, 2001; Gunn and Block, 2001). PAT tags are external tags attached to the fish with a monofilament leader with a titanium dart that is inserted through the bony surface plates, the pterygiophores, at the base of the second dorsal fin (Figure 2). Half of the tags were then anchored down to the fish with an additional loop to aid in attachment and increase the deployment duration. The tags collect pressure, temperature and light data, and are programmed to pop-off on a specific date at which time a metal pin attached to the tag and leader corrodes, releasing the tag. The tag floats to the surface where it transmits the recorded data via the Argos satellite system. The tags were programmed to collect pressure readings, ambient temperature and light levels at 2-minute intervals. The tags used in this study were programmed to return light level data and temperature vs. depth profile data. From the daily light curves, local noon is calculated giving an estimation of longitude. Temperature vs. depth data could then be used to obtain sea surface temperatures by taking the temperature when depth equals zero. This data yields daily thermal profiles of the water column. In addition to the PAT tags, 106 surgically implanted archival tags were deployed in Carolina 2003. One of the tags was returned within the first year of deployment and is 13

included in this data set. The tag yields the same data as the PAT tag in addition to internal body temperature. The archival tag (LOTEK Model 2310, LOTEK Wireless Fish and Wildlife Monitoring, Canada) is hardware version LTD2310A and software version 1.0.107. The tag was programmed to record data in 2-minute intervals. ii. Fish The seventeen fish were tagged during the Tag-a-Giant Carolina 2003 program. The fish were caught on hook and line, using heavy tackle, by the tagging boats and other recreational fishing boats out of the Morehead City Waterfront, North Carolina, USA via a transfer process previously described (Block et al, 1998). The fish were caught in the waters surrounding Cape Lookout, North Carolina, USA during January. The size range of the PAT-tagged fish was 198-216 cm curved length (mean curve length 209.5± 5.6 cm). Once the fish was on board the tagging boat, the eye was covered and a saltwater hose was used to ventilate the gills during the tagging process. The tag was inserted at the base of the second dorsal fin through the pterygiophores. In addition to the PAT tag, the fish were also conventionally tagged (Floy Tag, Seattle, Washington, USA) to help identify recaptured fish. Ten of the sixteen PAT tagged fish were double tagged with a surgically implanted archival tag in addition to the PAT tag. iii. Analysis Pop-up positions were transmitted via the Argos satellite system as the satellite passed over the tag transmitting on the surface of the ocean. Geolocation positions were 14

calculated using light levels to estimate longitude and sea surface temperature recorded by the tag to estimate latitude (Teo, et al, in press). Pat Decoder version 7.08.005 was used to calculate longitude by estimating local noon from light curves generated from tag light sensor readings (Wildlife Computers, Redmond, Washington, USA; Hill and Braun, 2002). Longitude estimates were filtered by discarding movements of more than 2 degrees longitude per day as outliers. The PAT temperature depth (PDT) function of the tag yielded information about thermal profiles of the water column as well as a sea surface temperature (SST) measurement for each geolocation point. The longitude was combined with the recorded SST for each day. Latitudes were then determined by matching this recorded information to satellite collected SSTs from weekly Moderate Resolution Imaging Spectroradiometer (MODIS) data. The latitudinal search area ranged from 20ºN to 60ºN with maximum latitudinal movement limited to 2 degrees per day. The light level longitude error was 1.30 degrees, and the SST estimated latitude error was 1.89 degrees for the PAT tags; the error for archival tags was.78 degrees longitude and.90 degrees latitude (Teo, et al, in press). The geolocation data were then plotted in a geographic information system (GIS) using ArcGis version 8.1. These plots yielded fish tracks. The geolocation points were then plotted over SeaWiFS (Sea-viewing Wide Field of View Sensor) ocean color imagery and MODIS Aqua SST imagery, provided by the SeaWiFS Project, NASA/Goddard Space Flight Center and ORBIMAGE. 15

IV. RESULTS i. Overview of Results Data were obtained from seventeen electronically tagged fish from Tag-a-Giant, Carolina 2003. Of the seventeen tags, sixteen were PAT tags and one was an archival tag recovered by a Spanish Longliner in the Central Atlantic. Data were obtained from all of the deployed PAT tags, with transmission from fifteen of the tags. One fish was recaptured before its tag released, and the tag was returned, yielding a full archival data set. The 100% transmission rate from the tags illustrates the high survivorship of the fish tagged using these methods. As this included ten double-tagged fish, the fish with surgically implanted archival tags appear to have high survivorship from the tagging procedure. The deployment length ranged from four to nine months with one tag popping up in March, three tags in May, one tag in June, one tag in July, six tags in August and four tags in September. The archival tag was recovered in May. The pop-up locations are illustrated in Figure 3. Nine of the sixteen PAT-tags were anchored to the fish with a loop. The average deployment for the tags with the loop was 212 days, while the tags, not anchored with the loop, had shorter deployments averaging 158 days. The ABFT show extensive use of the entire water column with dives exceeding 1000 m, the limit of the depth sensor on the tags. However, ABFT spend 97% of the time in the upper 300 m of the water column. While on the continental shelf, the bluefin are constrained by bathymetry. One can determine the point at which the tuna leaves the shelf areas because the tunas start a series of deep dives, probably seeking prey. 16

All of the fish remain in the waters off of North Carolina or in the South Atlantic Bight for the winter months, where diving was shallow and thermal ranges were narrow. In early spring, the fish move offshore and north with dive depths and thermal ranges increasing (Figure 4). The first fish to move offshore leaves the Carolina area on March 18 while the last fish leaves on April 25. The fish are indistinguishable in this initial movement north, but in May, the fish show distinct patterns with two of the PAT-tagged fish moving to the eastern Atlantic. The fact that 17.6% of the fish in this data set cross the ICCAT boundary indicates a high degree of eastern movement among these tagged fish. The fish which did not cross the Atlantic remain in the western Atlantic where they aggregate in the waters off of New England in the late summer and early fall. ii. The Eastern Fish Two of the sixteen PAT tags deployed in Carolina 2003 popped up in the eastern Atlantic Ocean, Fish 02609 at longitude 23.768W and Fish 02503 at longitude 4.989W. These tags were deployed on January 13 and January 16 respectively and popped up on August 6 and August 12 (Figure 5). In addition, one archival tag, LTD1013, was recovered by a Spanish longline fisherman at longitude 34.42W on May 6, 2003. These fish show distinct patterns of movements to the eastern Atlantic as shown in Figure 5. Fish 02609 and Fish 02503 are together with the other fourteen PAT-tagged fish in April (Figure 4) before beginning their movement east in May (Figure 6). All sixteen PATtagged fish exhibit northward movement in April. While Fish 02609 and Fish 02503 are with the other fish during the winter months in Carolina and moving north during April, 17

they show different behavior in May, June and July (Figure 7). The two fish migrate across the Atlantic Ocean rapidly in May arriving in the Eastern Atlantic in late May and early June. Fish 02609 crossed in 39 days while Fish 02503 crossed in 36 days. Fish 02609 and Fish 02503, while both reaching the eastern aggregation area in the Rockall Island region in late May, take different routes (Figure 6). Both fish follow fronts, but they follow different ones in their routes across the ocean. Fish 02503 moves from an area of 16.4-18.8ºC water north into cooler, 13.4-14.8ºC, nutrient rich water, while 02609 stays in warmer, 18.2-21.0ºC, less productive water in its movement east. The fish remain in the Rockall Island region for all of June (Figure 8). This region is highly productive during the summer months based on ocean color (Figure 9). However, the fish show two distinct patterns in July, with Fish 02609 remaining in the Rockall Island region with similar behavior to that exhibited in June while Fish 02503 moves south and then further east into the Bay of Biscay where the tag popped up (Figure 9). The average SST in the eastern aggregation area was 15.81-17.75ºC. During this time, the fish did not dive below 300 m because they were constrained by bathymetry as when in Carolina on the Continental Shelf. The tags were not programmed to transmit information on the amount of time spent at depth. Fish LTD 1013 shows a different pattern moving east from Carolina along a thermal front past Bermuda and into the Central Atlantic where the fish was harvested (Figure 10). Unlike Fish 02609 and Fish 02503, Fish LTD1013 moves east on March 18, 2003 staying in an average SST of 20.21ºC until reaching the central Atlantic where Fish 18

LTD1013 moved north into 15.47ºC SST water in May. The recovery location for Fish LTD1013 was in this cooler water of the central Atlantic. iii. The Western Residents Fourteen of the sixteen PAT-tagged fish remained in the western Atlantic for the entire time the tags were on the fish. All together in the winter months, the fish displayed different patterns in their movement to the waters off of New England where they aggregated in the late summer as seen in Figure 7. The fish do show some southerly movement into the South Atlantic Bight/Blake Plateau region in February and March directly after tagging. The fish move south and north between the South Atlantic Bight and North Carolina continental shelf during the winter months before moving north in April. In late March and early April, the fish begin moving north and off the continental shelf. At this time, maximum dive depths increased from 70 m to 220 m. A series of fish show a pattern of moving directly north along the continental shelf and through the mid- Atlantic Bight, while others move east towards Bermuda before turning north as seen in Figure 11. There are two main routes in the movement north, one going by Bermuda, the other through the Mid-Atlantic Bight or just off the Continental Shelf break. The series of fish that went east from Carolina towards Bermuda went to the Southern Grand Banks in late April and May. The fish that navigated through the Mid-Atlantic Bight in April were along the Continental shelf and Hudson Canyon during May. Four areas are common on the routes of ABFT on their way to spending late July and August on the 19

Continental Shelf off of New England and in the Gulf of Maine: The New York Bight, Hudson Canyon; the Gulf of Maine, New England Shelf; Bermuda; and the Southern Grand Banks. All of the western resident fish exhibit similar behavior in the late summer and early fall as they are aggregated on the Continental Shelf and in the Gulf of Maine by July and remained there for the duration of the tag deployment. The western resident fish stay in SST averaging 18.20-19.29ºC once in the waters off of New England. The average SST in April is 18.30ºC during their movement north. However this varies for different fish as illustrated in the MODIS Aqua SST 30-day Composite Image (Figure 4). The average temperature at the Shelf aggregation area during the late summer is 19.48ºC. iv. Behavior of Fish 02680 during two weeks in February Fish 02680 was a 216 cm fish tagged in Carolina on January 26, 2003. After being tagged with a PAT tag and an implanted archival tag, the fish swam south into the South Atlantic Bight region and Blake Plateau with a two-week move investigating the waters around the Bahamas (Figure 12). The average thermal profile for these two weeks is illustrated in Figure 13 where the average sea surface temperature (SST) was 21.1ºC. On February 1, 2003, Fish 02680 was in warm surface waters (21.8ºC). Fish 02680 stayed in this warm water mass while moving south until reaching cooler waters on February 4, 2003 in the Bahamas region. The thermal profiles illustrate that the fish was in a cooler than average water mass for 5 days after which Fish 02680 moved to the warmer water north of the Bahamas. Fish 02680 swam north into warmer water for 3 20

days, and returned to the cooler southern waters for 3 days before returning north to the Blake Plateau area by February 17,2003. Fish 02680 then moved north in April and the tag popped up in the water off New England on August 15, 2003. 21

V. DISCUSSION i. Movements The large tagging effort in the waters off of North Carolina is possible because the bluefin are in a tremendous aggregation there in the winter months. From this area, the bluefin go to all parts of the Atlantic Ocean. Fish tagged in the waters off of North Carolina go to spawning sites in both the Gulf of Mexico and Mediterranean Sea (Block, et al, 2001) as well as showing various movement patterns. It appears likely that this winter aggregation is a mixed stock from different regions of the Atlantic. The fish PATtagged in Carolina 2003 were all potentially mature fish, however none of the fish went to either spawning ground in the first year post-tagging even though the tags were on the fish for the entire western spawning season and at least part of the eastern spawning season. This suggests that the age and size to first maturity may be incorrect for both eastern and western fish with fish not reproducing until much later in life. This error would overestimate spawning stock biomass. Atlantic bluefin tuna exhibit behavior coherent with large-scale oceanographic features. All sixteen PAT-tagged fish stay in the waters off of Carolina and the South Atlantic Bight for the winter months as is consistent with previous tagging studies (Block et al, 2001; Boustany, et al, 2000). While distinct patterns are seen in the spring, all of the fish exhibit similar behavior at the start of their movement out of the waters around Carolina in April. Three of the fish cross the Atlantic Ocean, but in April, these fish are indistinguishable from the other western resident fish. Their behavior becomes distinct in 22

late April and May when the fish leave the western Atlantic and begin their rapid crossing of the Atlantic Ocean. While the two eastern fish cross the Atlantic and aggregate in the Rockall Island region south of Iceland, they take different routes to reach this destination. Fish LTD1013 swims east as well, however, this fish was harvested in the central Atlantic before it potentially could have reached this eastern aggregation area. The three fish swim roughly parallel to oceanographic fronts. They identify thermal fronts or ocean color differences, but the specific cues are not the same for the three fish. They seem to orient to a particular temperature or other oceanographic cue such as ocean color and stay within that range. Fish LTD1013 swims east along a more southern route past Bermuda into the central Atlantic in late March and April, while Fish 02503 departs the western Atlantic in early May before Fish 02609 and stays in cooler more productive water. Fish 02503 crossed into the cooler water and stays in this water mass, arriving at Rockall Island in 39 days. Fish 02609 stays to the south in warmer, less productive water before turning north into the cooler water to arrive at Rockall Island in 36 days. These fish take three routes in their journeys illustrating, that while the endpoint of the two PAT-tagged fish may be the same, the individual fish exhibit distinct behaviors and patterns. Therefore, while the fish cross the Atlantic, it is difficult to predict individual fish behavior as illustrated by the known and varied patterns of the tagged fish. In June, July and August, the eastern fish show two distinct patterns. Fish 02609 stays in the aggregation area around Rockall Island, a highly productive zone where these fish have been seen for many years (Hardy, 1959). Fish 02503 moved south to the waters off of Portugal in July before moving into the Bay of Biscay where the tag popped-up. 23

While it is unknown why the movement occurred, the Bay of Biscay and waters surrounding Portugal have harbored an ABFT fishery for centuries (Hardy, 1959; Ravier and Fromentin, 2001; Rodriguez-Marin, et al, 2003). It remains unclear if these fish will eventually enter the Mediterranean Sea to spawn in the late summer and fall, or if they will return to North Carolina in the following winter. Block, et al (2001) described the western resident pattern of bluefin behavior. The fourteen western resident fish showed various patterns through the spring, with some patterns emerging. The two main routes taken to the waters off of New England are east towards Bermuda and then north, and the other through the Mid-Atlantic Bight or just off the Continental Shelf. During April, the eastern fish show the same patterns. However in May, the patterns diverge with the following four areas common on the routes of ABFT on their way to spending late July and August on the shelf surrounding New England: The New York Bight, Hudson Canyon area; Bermuda; the Southern Grand Banks; and the Gulf of Maine and New England Continental Shelf area. Like the eastern fish, the western resident fish show distinct individual behavior with some of the fish staying in warmer, less productive water along a front longer, and others heading directly into the productive waters of the Gulf of Maine. All of the fish stay out of the oligotrophic water but move roughly parallel to the various fronts. In July and August, the fish are clearly staying north and shoreward of the warm water pushing them into the cooler shelf waters. Unlike the eastern fish which show divergent behaviors in late summer, all of the western fish are in a tight aggregation on the shelf in late summer. As the shelf waters cool further in response to the change in seasonal solar heating, Block, et al (2001) describe the movement of the fish back south to the waters of Carolina for late fall and winter. 24

While the fish show individual behavior in the cues they follow during this migration, they do exhibit the rough coherence to large-scale oceanographic features that characterizes most of their large-scale migratory movements. ii. FISH 02680 The movement south by fish 02680 in the first two weeks of February illustrates an investigative behavior with frequent changes in direction. Fish 02680 swims south from Carolina, through the Blake Plateau region and to the Bahamas where the water was cooler (Figure 12), then swims south but meets a colder water mass in the Bahamas, as illustrated in Figure 13. Upon reaching the cool water, the fish moves through the Bahamas only to move north into warmer waters. Fish 02680 again changes direction and heads back south to the Bahamas only to change direction again and head back to the warm waters around the Blake Plateau. Fish 02680 seems to be avoiding the slightly cooler water encountered in the Bahamas illustrated in its move to the warmer water to the north. This temperature avoidance behavior has been described for Albacore tuna, Thunnus alalunga (Laurs, et al, 1977) where the fish reversed direction when entering cold water. Fish 02680 appears to be investigating potential habitat in the Bahamas region, but once it is found to be unsuitable, returns to the warmer waters to the north. It is not known why the fish ventures south during the winter months although it appears that the fish is moving south into this region looking for food. While it is known that the Florida Straits and Blake Plateau are breeding grounds for the ABFT (McGowan and Richards, 1989; Baglin, 1982), the significance of the spawning in this area is unknown, and the water temperatures in February are cool for breeding. 25

iii. Management Implications This analysis supports the criticism that the assumptions made in the current management of ABFT are oversimplified and even critically flawed. ABFT are facing very high fishing pressure and mortality, as two of the fish were caught by commercial fishermen within the first six months after deployment. Clearly, the assumed 2% mixing rate between the two management units is much too low; this analysis indicates that a mixing rate of 20% is more realistic. In addition, the management assumptions fail to appreciate the potential complexity and multiplicity of patterns exhibited by the ABFT in their movements between feeding and spawning areas. Movement patterns may be determined by changing oceanography that makes them difficult to predict, as oceanographic patterns may be different each year. Therefore, static assessments of mixing rates may be impossible. The individual aspect of the movement patterns makes it particularly difficult to predict these patterns for the population as a whole. 26

VI. CONCLUSIONS Bluefin migratory behavior is a complex mixture of certain patterns and individuality. At the moment, there is no insight into which fish exhibits a certain behavior or movement pattern. For this reason, the problems facing management are more complex than previously assumed. Fish show coherence to large-scale oceanographic features, but with a degree of individuality complicating applications for the population as a whole. In addition, the ocean is not a static environment so determination of oceanographic cues may prove essential to proper management of ABFT and determination of stock dynamics. 27

VII. FIGURES Figure 1 Map of the Atlantic Bluefin Tuna management boundaries as defined by the ICCAT in 1981. The Atlantic Bluefin is currently regulated as two stocks divided at the 45º West meridian in the Northern Hemisphere. 28

a c b d FIGURE 2 a) a Pop-off Satellite Archival Tag with monofilament leader and titanium dart (Wildlife Computers, Redmond, Washington, USA) b) close-up of the titanium dart, inserted through the pterygiophores of the fish. c) The tag is placed below the second dorsal fin and inserted through the pterygiophores d) once inserted, the tag is anchored to the fish with a loop. 29

Figure 3 Endpoint locations for the 16 PAT tagged fish (yellow triangles) and 1 returned archivally tagged fish (yellow circle). Three of the seventeen fish crossed the ICCAT border into the eastern Atlantic; a mixing rate of 17.6%. The archival tag was recaptured by a Spanish longline fisherman. 30

Figure 4 April Fish Tracks overlayed on a 30-day composite SeaWiFS ocean color image (top) and MODIS Aqua SST image (bottom). Western resident fish (white circles), Fish 02503 (red circles) and Fish 02609 (yellow circles) are together moving north out of Carolina. 31

Figure 5 The eastern fish, Fish 02503 (green circles), Fish 02609 (yellow circles) and Fish LTD1013 (orange triangles) cross the Atlantic Ocean, remaining in the eastern Atlantic for the summer and early fall. LTD 1013 was recovered by a Spanish fisherman in mid-may in the central Atlantic. The pop-up endpoints for Fish 02503 (green and black triangle) and Fish 02609 (yellow and black triangle) are both in the eastern Atlantic. 32

Figure 6 May fish tracks overlayed on SeaWiFS ocean color 30-day composite (top) and MODIS Aqua SST 30-day composite (bottom). The western residents (white circles) stay along the east coast of the United States and Southern Canada while Fish 02503 (red circles) and Fish 02609 (yellow circles) swim east over the ICCAT boundary. Fish LTD1013 (yellow triangles) was captured in the central Atlantic on May 6. 33

Figure 7 Flow chart describing the movements of the Atlantic Bluefin Tuna after leaving the waters off of Carolina. 34

Figure 8 June fish tracks overlayed on SeaWiFS ocean color 30-day composite (top) and MODIS Aqua SST 30-day composite (bottom). The division between the eastern and western fish is clear as late summer approaches. The eastern fish (yellow and red circles) are arriving in the eastern Atlantic aggregation area, Rockall region. 35

Figure 9 July fish tracks overlayed on SeaWiFS ocean color 30-day composite (top) and MODIS Aqua SST 30-day composite (bottom). The western resident fish (white circles) are aggregated on the Continental Shelf off of New England, USA while the eastern fish (yellow and red circles) show two patterns, one remaining in the Rockall region (pop-up location is indicated by yellow and black triangle), the other going south and into the Bay of Biscay where the tag popped up (red and black triangle). 36

Figure 10 Archival Tag LTD 1013 track during April overlayed on ocean color and SST satellite images (30-day composites). Fish LTD1013 swims past Bermuda and into the Central Atlantic roughly parallel to an oceanographic front where a Spanish longliner recovered the tag on May 6, 2003. 37

Figure 11 Western resident fish tracks (white circles). The fish remain in the waters off of North Carolina and the South Atlantic Bight in the winter, after which they move offshore and north in April, reaching the Continental Shelf off of New England in the late summer. 38

Figure 12 Fish 02680 swims south to the Bahamas in the first two weeks of February exhibiting habitat searching with clear changes in direction when encountering cooler water in the Bahamas. The colored triangles are daily geolocation points during this twoweek interval. 39

1-February-2003 Location: 79.21W 31.82N 4-February-2003 Location: 77.63W 26.54N 0 Temperature (C) 18 19 20 21 22 23 24 0 Temperature (C) 18 19 20 21 22 23 24 20 20 40 40 60 60 80 80 100 100 120 120 8-February-2003 Location: 76.82W 26.59N 10-February-2003 Location: 77.31W 27.99N 0 Temperature (C) 18 19 20 21 22 23 24 0 Temperature (C) 18 19 20 21 22 23 24 20 20 40 40 60 60 80 80 100 100 120 11-February-2003 Location: 77.31W 28.56N 120 12-February-2003 Location: 77.94W 26.94N 0 Temperature (C) 18 19 20 21 22 23 24 0 Temperature(C) 18 19 20 21 22 23 24 20 20 40 40 60 60 80 80 100 100 120 0 13-February-2003 Location: 77.45W, no lat Temperature(C) 18 19 20 21 22 23 24 120 0 17-February-2003 Location: 77.63W 32.48N Temperature (C) 18 19 20 21 22 23 24 20 20 40 40 60 60 80 80 100 100 120 120 Figure 13 Pressure Depth Temperature Profiles in the first two weeks of February for Fish 02680 illustrating habitat and temperature investigating. The pink curve represents the average thermal profile for the two weeks, the blue curve is the daily thermal profile for each geolocation point. Fish 02680 is in warmer water on the Blake Plateau before swimming south and entering cooler water in the Bahamas after which it changes direction to the north into warmer water. 40

VIII. ACKNOWLEDGEMENTS I am indebted to my advisors, Dr. Richard Barber of Duke University, and Dr. Barbara Block of Stanford University, for the integral roles they played in my project. Dr. Barber always helped me look at the data from new and exciting viewpoints. Dr. Block welcomed me into her lab and taught me everything there is to know about electronic tagging and big fish. Being part of her lab has been an invaluable experience. I would also like to thank the entire Block Lab at Hopkins Marine Station and everyone at the Tuna Research and Conservation Center, including but not limited to Chuck Farwell, Robbie Schallert, Andy Seitz, Steve Teo, Kevin Weng, and Dr. Tom Williams. I particularly want to thank Andre Boustany for being an outstanding mentor, always willing to answer all of my questions with incredible patience. These tagging efforts would not be possible without the amazing Tag-A-Giant team and all of the recreational fishermen transferring fish during TAG. I would like to thank Captain John Jenkins, Captain Dale Britt, Captain Charles Perry and Alan Willis for making me feel at home on their boats and always making me smile. 41

IX. LITERATURE CITED Altringham, J. D. and Block, B.A. 1997. Why Do Tuna Maintain Elevated Slow Muscle Temperatures? Power Output of Muscle Isolated from Endothermic and Ectothermic Fish. The Journal of Experimental Biology 200, 2617-2627. Baglin, Raymond E. 1982. Reproductive Biology of Western Atlantic Bluefin Tuna. Fishery Bulletin: Vol. 80, No. 1. 121-134. Bergin, A., and Haward, M. Japan s Tuna Fishing Industry: A Setting Sun or a New Dawn? New Science Publishers. New York. 1996. Blank, J. M., Morrissette, J.M., Landeira-Fernandez, A., Blackwell, S. 2004. In situ cardiac performance of Pacific bluefin tuna hearts in response to acute temperature change. Journal of Experimental Biology: Vol. 207, No. 5, 881-890. Block, B.A., Dewar, H., Farwell, C., and Prince, E. 1998. A new satellite technology for tracking the movements of Atlantic Bluefin Tuna. Proceedings of the National Academy of Science, Vol. 95, pp. 9384-9389. Block, B. A., Dewar, H., Blackwell, S.B., Williams, T.D., Prince, E.D., Farwell, C.J., Boustany, A., Teo, S.L.H., Seitz, A., Walli, A., and Fudge, D. (2001). Migratory Movements, Depth Preferences, and Thermal Biology of Atlantic Bluefin Tuna. Science Vol. 293, pages 1310-1314. Boustany, A.M., Marcinek, D.J., Keen, J., Dewar, H., and Block, B.A. 2001. Movements and Temperature Preferences of Atlantic Bluefin Tuna off North Carolina: A Comparison of Acoustic, Archival and Pop-up Satellite Tags. Electronic Tagging and Tracking in Marine Fisheries, 89-108. Brill, R. and Bushnell, P.G., 2001. The Cardiovascular System of Tunas. In Block, B.A. and Stevens, E.D. (ed.) 2001. Tuna: Physiology, Ecology and Evolution. Volume 19. San Diego, CA: Academic Press. 79-120. Brill, R., Lutcavage, M., Metzger, G., Bushnell, P., Arendt, M., Lucy, J., Watson, C., Foley, D. 2002. Horizontal and Vertical Movements of Juvenile Bluefin Tuna in Relation to Oceanographic Conditions of the Western North Atlantic, Determined with Ultrasonic Telemetry. Fishery Bulletin 100: 155-167. Buck, Eugene. 1995. Atlantic Bluefin Tuna: International Management of a Shared Resource. In CRS Report for Congress 95-367. Carey, F. and Teal, J.M. 1966. Heat Conservation in Tuna Fish Muscle. Proceedings of the National Academy of Sciences 56: 1464-1469. 42

Carey, F., Kanwisher, J.W., and Stevens, E.D. 1984. Bluefin Tuna Warm their Viscera During Digestion. Journal of Experimental Biology 109: 1-20. Fontenau, A. 1996. Mediterranean tunas and associated species: fishing, research and resource management. Resource and Environmental Issues Relevant to Mediterranean Fisheries Management, J.F. Caddy (ed) Rome: FAO, 1996. Graham, J.B., and Dickson, K.A. 2001. Anatomical and Physiological Specializations for Endothermy. In: Block, B.A. and Stevens, E.D. (ed.) 2001. Tuna: Physiology, Ecology and Evolution. Volume 19. San Diego, CA: Academic Press. 121-165. Gunn, J. and Block, B.A. 2001. Advances in Acoustic, Archival, and Satellite Tagging of Tunas. In: Block, B.A. and Stevens, E.D. (ed.) 2001. Tuna: Physiology, Ecology and Evolution. Volume 19. San Diego, CA: Academic Press. 167-224. Hardy, Sir Alister. 1959. The Open Sea: Its Natural History, Part II: Fish and Fisheries. Houghton Mifflin Company. Boston. 77-82. Hertel, H. 1966. Structure, Form and Movement. New York: Reinhold. Hill, R.D., and Braun, M.J. 2001. Geolocation by light level. The next step: Latitude. Reviews in Methods and Technologies in Fish Biology and Fisheries (Sibert, J., and Nielson, J., eds.) Vol. 1. Kluwer Academic, Dordrecht, The Netherlands. International Convention for the Conservation of Atlantic Tunas. May 14,1966. Rio de Janeiro, Brazil. ICCAT. 81-1. Recommendation on Bluefin Management Measures. 1981. ICCAT. 96-5. Resolution for SCRS to evaluate the appropriateness of the current boundary between East and West Atlantic bluefin tuna. 1996. ICCAT. 00-11. Resolution for SCRS to examine effects of mixing and consideration of appropriateness of current boundary for E-W management units. 2000. ICCAT. 01-9. Resolution for SCRS mixing report on Atlantic bluefin. 2001. Korsmeyer, K.E. and Dewar, H. 2001. Tuna Metabolism and Energetics. In: Block, B.A. and Stevens, E.D. (ed.) 2001. Tuna: Physiology, Ecology and Evolution. Volume 19. San Diego, CA: Academic Press. 35-78. Laurs, R.M., Yuen, H.S.H., and Johnson, J.H. 1977. Small-scale movements of albacore tuna, Thunnus alalunga, in relation to ocean features as indicated by ultrasonic tracking and oceanographic sampling. Fishery Bulletin: Vol. 75, No. 2. 347-355. 43