Two-year migration of adult female white sharks (Carcharodon carcharias) reveals widely separated nursery areas and conservation concerns
© 2013 Domeier and Nasby-Lucas; licensee BioMed Central Ltd. 2013
Received: 18 July 2012
Accepted: 19 February 2013
Published: 4 April 2013
Satellite tagging programs have provided detailed information about the migratory patterns of northeastern Pacific white sharks, revealing a seasonal migration between a vast offshore region and coastal aggregation sites. Although adult males undergo annual round-trip migrations, photo-identification programs have noted that sexually mature females may only visit coastal aggregation sites once every 2 years, a behavior that is presumably linked to an estimated 18-month gestation period. The whereabouts of females during their full 2-year migration were previously unknown, because of the limited battery capacity of satellite pop-up tags.
Through the use of satellite-linked radio-telemetry tags with multi-year tracking capability, we describe the 2-year migratory pattern for four mature female white sharks tagged at Guadalupe Island, Mexico. The 2-year migration comprised four phases: 1) an Offshore Gestation Phase (which had an average duration of 15.5 months; 2) a Pupping Phase, which occurred along the Mexican coast between the months of April and August; 3) a Pre-Aggregation Phase (when the females were in transition between the Pupping Phase and Guadalupe Island; and 4) the Guadalupe Island Aggregation Phase, which began when the mature females arrived at Guadalupe Island between late September and early October.
Long-term satellite tracking of mature female white sharks highlighted the connectivity between a single presumed mating site at Guadalupe Island, and two widely separated pupping sites along the Mexican coast. The Offshore Gestation Phase provided evidence that the females remained offshore for up to 16 months during their 2-year migration cycle. The Pupping Phase along the Mexican coast coincided with the seasonal presence of young-of-the-year white sharks along the coast of North America, and with a presumed gestation period of 18 months, this placed mating between October and January, during the period when white sharks are known to be at Guadalupe Island. Tracking data during the time sharks were offshore showed that mature males and females are spatially segregated, except for their concurrent seasonal presence at Guadalupe Island. These discoveries provide important new details about the complete life history of northeastern Pacific white sharks while identifying crucial regions in which young-of-the-year, juveniles and adult females are most vulnerable.
KeywordsWhite shark Mating Pupping Migration Baja Mexico Pacific Gestation
The white shark (Carcharodon carcharias) is a charismatic, apex predator that routinely migrates thousands of kilometers [1–10], and yet regional population structure exists on a global scale [5, 10, 11]. Because there are no physical boundaries separating the white-shark populations, behavioral traits that limit mixing may be the mechanism responsible for the observed population structure. One hypothesis, based upon DNA analysis, suggests that females have restricted geographic movement patterns but males are likely far-ranging . Electronic tagging studies have presented seemingly contradictory results, with both sexes found to follow wide-ranging migratory patterns [3–8], with one female tracked across the Indian Ocean . The discovery of male and female seasonal site fidelity among white sharks [2, 5, 12, 13], termed ‘philopatry’, provided the first evidence of a behavioral trait that could restrict gene flow. It has been suggested that new white shark populations are founded by straying individuals, and the tendency for philopatry is what eventually differentiates the new population from the ancestral population [5, 11, 14, 15]. However, philopatry will only lead to unique population structure if the behavior is focused on mating and/or pupping sites. Identifying mating and pupping sites and describing the connectivity between them can be extremely challenging when studying a highly migratory fish of relatively low abundance such as the white shark, but if accomplished, the results would have significant genetic and conservation implications [16, 17].
Electronic tagging of adult white sharks in the northeastern Pacific has identified a previously unknown pelagic life-history phase, with sharks spending roughly half of their time in the deep-ocean environment, sometimes traveling as far as the Hawaiian Islands before returning to the continent [3, 4]. Despite this pelagic phase, photographic identification (photo-ID) programs have shown white sharks to exhibit strong seasonal philopatry to one of two aggregation sites in the northeastern Pacific [12, 13, 18]: one off central California, USA, and the other at Guadalupe Island (GI), Mexico. Hundreds of sharks have been tracked from these aggregation sites, but only one individual (a sub-adult female) is known to have visited both sites . Males visit these aggregation sites every year whereas adult females are typically seen every other year [8, 12, 18, 19]. This 2-year migration pattern for females is likely associated with a presumed 18-month gestation cycle .
Multi-year tracking of adult female white sharks, combined with other direct and indirect life-history observations, could identify mating and pupping sites for the tracked individuals, as well as the connectivity between these important sites. To date, satellite pop-up tags have been unable to provide data/tracks on white sharks spanning more than 1 year, but the design of a satellite-linked radio-telemetry (SLRT) tag with a multi-year battery capacity, together with the development of methods for the capture, tagging, and release of large adult white sharks, allowed for a new research approach used in this study.
Here we describe a 2-year migratory pattern for mature female white sharks, and document the connectivity between a single presumed mating site at GI and two widely separated pupping sites along the Mexican coast. This discovery is an important addition to our understanding of the life history of the white shark, a species currently listed as ‘vulnerable’ by the World Conservation Union (IUCN), and which is protected under the Convention on the International Trade in Endangered Wild Flora and Fauna (CITES) .
Results and discussion
Tagging and tracking data for tagged GI female white sharks
Shark number a
Total length, m
F77 year 1b
F77 year 2
Data from the GI SLRT-tagged sharks, combined with previously published life-history observations, allowed for the synthesis and description of a multi-year migratory pattern for mature, female white sharks. The 2-year migration was found to consist of four phases: 1) an offshore gestation phase (OGP), which began when the females depart GI, and ended when they migrated to coastal regions during the pupping season; 2) a pupping phase (PP), defined as the time the females remained in the coastal waters of Baja California, Mexico, during the known pupping season ; 3) a pre-aggregation phase (PAP), when the females were in transition between the PP and GI; and 4) the GI aggregation phase (GIAP). Although the occurrence of each of these phases was seasonal, the timing and duration of each phase varied to some degree between individuals.
Offshore gestation phase
The OGP is the longest phase of an adult white shark's migratory pattern (14-16 month duration), meaning mature females spend more time in pelagic habitats than in any other habitat type. Females experience significantly warmer SSTs by remaining offshore, perhaps facilitating optimal growth of developing embryos .
Preferred prey for females in offshore waters is unknown. An expedition to the male focal area, the SOFA, found the presence of three species of spawning squid (Architeuthis sp. and Ommastrephes sp.) and sperm whales, but no small marine mammals, and very little other epipelagic life . Mature females travel east/west over a much broader area than the males, so it is possible that the preferred offshore prey differs between males and females. White sharks have never been documented to prey on healthy, large cetaceans, and are probably too small to do so; however, it cannot be overlooked that adult white-shark migrations overlap with large cetacean migrations in many parts of the world. Sperm whales and white sharks coincide within the SOFA core , white sharks and calving humpback whales coincide in Hawaii  and the south Pacific , and white sharks coincide with northern right whales off the east coast of the USA . The growing circumstantial evidence that white sharks migrate to regions with relatively high whale density suggests a foraging link; whether the sharks are actively predating or simply scavenging upon the whales (and/or calves) is not known.
The OGP ended when the females migrated to coastal habitats along the Baja California Peninsula.
Previously published analyses of fisheries data have identified seasonal pulses of young-of-the-year (YOY) white-shark pups, from April through August, within YOY hotspots along the western coast of North America [8, 24, 25]. The timing of SLRT-tagged females into coastal waters coincided with the identified PP. Our presumed pregnant SLRT-tagged females migrated to coastal waters between 10 April and 3 June (median 27 May) and departed between 20 June and 15 August (median 30 July) (Table 1). The duration of this PP varied from 52 to 77 days (mean 68 days). The approximately 2-month duration of the PP for tagged female sharks precluded precise identification of the location and timing of parturition, and it is unknown whether pups are born simultaneously or sequentially over a period.
The purpose of the PAP can only be speculated. The females could benefit from the pinniped populations of GI if they migrated directly to the island from the pupping grounds, but the presence of males may be a deterrent. The migratory behavior of the tagged females during the PAP supports the hypothesis that females actively avoid males until the mating season [7, 8]. The PAP may be a period when the females are physiologically preparing to mate again, while avoiding the risks associated with should say inhabiting the same space as adult males.
Guadalupe Island aggregation phase
The GIAP was a period of seasonal residency at GI presumably the time and place of mating . The GI arrival of three tagged females occurred over a relatively narrow temporal window between 11 September and 6 October (Table 1). The percentage of time that SLRT tag transmissions were located within 15 km of GI peaked at close to 100% during the months of October and November (8%, 55%, 98%, 97%, 74%, 52%, and 7%, for August to February, respectively). Conspecific wounds to both male and female white sharks are frequently seen at GI [8, 12], confirming that the mating aggregation does involve risk of injury. Male/male aggression certainly occurs, because wounds are seen prior to the arrival of females, but whether the males are defending mating sites or prey resources is unknown.
The GIAP ended when the females departed for the open ocean between 7 December and 25 January (median 23 December) (Table 1), after 83 to 136 days at the island.
Alternative mating hypothesis
Jorgensen et al.  have proposed an alternative life-history hypothesis that is contradictory to the hypothesis proposed by Domeier . The major difference between these hypotheses pertains to the timing and location of mating. Jorgensen et al.  speculated that white sharks are mating during their offshore phase, whereas Domeier proposed that mating occurs during seasonal, near-shore, adult aggregations. The hypothesis that white sharks are mating at coastal aggregation sites is supported by a growing body of indirect evidence: 1) the presence of mature females at GI with fresh conspecific bite wounds on the lateral surfaces of their head, pectoral fins, and flanks ; 2) the finding of spermatophores in the claspers of males at the GI and central California aggregation sites ; 3) a strong spatiotemporal overlap in the distribution of males and females at the GI and central California aggregation sites ; 4) strong sexual segregation during the offshore phase ; 5) the finding that peak presence of white sharks at GI does not correspond with the seasonal peak abundance of pinnipeds, suggesting that foraging is not the primary motivation for the aggregation , and 6) as presented here, a match between the estimated duration of gestation and the time between coastal aggregations and the known pupping season. By contrast, the hypothesis that mating is occurring offshore was not supported by any substantiating evidence, except for the speculative interpretation of diving patterns derived from electronic tags.
The offshore-mating hypothesis is based upon the conjecture that a described vertical-diving pattern (rapid oscillatory diving (ROD)) is a result of a lek-like mating behavior in the core of the SOFA . This interpretation is problematic from several perspectives. Lek-like mating systems involve the gathering of males at a traditional site for the purpose of ritualized courtship display. The males compete for the attention of females, and in turn, the females select a specific male for mating. Although the peak in ROD behavior, and thus presumed offshore mating, occurs during June/July in a period when the distribution of males temporarily constricts, even the constricted offshore space is vast (estimated to be about 64,000 km2 ). Lek-like mating would require the males to be in a very small space to allow females to observe the courtship of several males at once. No electronic-tag data have ever indicated that sharks are densely populating a small, traditional offshore site. Lek-like mating systems have been described for some species of fish , but leks have never been seen among elasmobranchs. Females that mate in lek systems select a single male deemed superior to other males, thus the fact that white-shark pups from a single litter tested positive for multiple paternity  argues against lek-like mating for this species.
It is challenging to ascribe any behavior to vertical movement data in the absence of visual observations. The seasonal constriction of the SOFA and the ROD-type diving pattern could be due to the pursuit of a seasonally available prey. An expedition to this region during the constriction identified the presence of three species of spawning squid and sperm whales , but again, the absence of behavioral observations deems it impractical to assign any cause to the ROD diving pattern. Diving patterns and mating systems aside, there are other strong arguments against the hypothesis that white sharks are mating during the offshore phase of their migratory pattern. First, electronic-tag data indicate that males and females are largely segregated during the offshore period , and second, the proposed mating during June/July  would equate to December/January pupping (accepting the 18-month gestation estimate ). Females arrive at adult aggregation sites approximately in September, and depart in December to end of February. No YOY have been seen at the adult aggregation sites, no obviously pregnant females have been sighted at GI, and pupping is known to occur approximately April through July.
The revelation that GI supports two Mexican coastal-nursery areas separated by 1000 to 2000 km gives rise to major conservation implications. In some coastal-shark species, females have been shown to be philopatric to specific nursery regions [30–33]. Longer-term tracking could provide confirmation of such behavior in white sharks, and explain the presence of persistent YOY hotspots [8, 24, 25, 34] and the genetic indication that females do not disperse . Females may be returning to their place of birth to pup; this phenomenon, called ‘natal homing’, has been suggested for sharks , but not yet documented. The existence of natal homing in white sharks would explain the genetic indication that dispersion of this species is sex-biased. Furthermore, natal homing creates population vulnerability; the removal of females that support a specific pupping region would cause a loss of genetic diversity and the collapse of that nursery.
The return of gravid females to coastal regions where active commercial fisheries take place presents the most vulnerable life-history stage for adult females, a threat confirmed by documented mortalities in the Sea of Cortez in 1996 , 2004 , and 2012 (reported in popular media: http://www.petethomasoutdoors.com/2012/04/great-white-shark-catches-appear-on-the-rise-sea-of-cortez-.html). The SLRT-tagged shark F98 had been reporting regular position data but ceased sending messages soon after exiting the Sea of Cortez, and she has not been subsequently re-sighted at GI; fishery-related mortality is a reasonable explanation. The 1-year offshore migratory pattern of adult males exposes them to far less commercial fishery pressure than females, because they rarely stray towards the coast of Mexico.
In addition to the threat to gravid females along the coast, there is also a threat to YOY and juvenile white sharks, which are found along the continental shelf in the near-shore regions. Adult white sharks are capable of breaking through most commercial fishing gear to escape, but YOY and juvenile white sharks do not have the mass and strength to do the same, therefore juveniles represent the most vulnerable stage for this species. Care must be taken to protect both the adult females and juveniles and their nursery habitats.
This is the first long term, continuous tracking study of individual adult female white sharks. Our results not only confirmed a 2-year migratory pattern for adult females, they also provide unifying support for the natural history hypothesis proposed by Domeier . This hypothesis proposed that Guadalupe Island serves as a mating site for adult white sharks, and that this site is visited every year by adult males, but only once every two years by reproductively active females. The migratory pattern described here also supports the previously published estimate of gestation period (18 months ); a time that we found adult females to spend entirely in the open ocean. Our tracking has highlighted a previously unknown period of vulnerability for adult females: the period of time they are exposed to coastal fisheries when they migrate to the coast of North America to give birth. Adult males from GI, however, do not share this period of vulnerability, since they do not travel to the coast of North America once they reach sexual maturity .
Although the exact location of parturition cannot be determined from our tracking, it is clear that females that mate at GI support recruitment of YOY to two widely separated nursery areas; one on the Pacific side of the Baja California Peninsula and the other in the Sea of Cortez. If further tracking reveals that females are philopatric to very specific pupping grounds, the preservation of genetic diversity will depend upon the proper management of both the adult females and pups that support specific nursery area.
Satellite-linked radio-telemetry tagging
Four mature female white sharks were tagged (SPOT5 SLRT tags; SPOT-257A, Inline Finmount, 4 holes, 7 × 7; Wildlife Computers, Redmond WA, USA) at GI, Mexico in 2008 and 2009 (Table 1) as described previously by Domeier and Nasby-Lucas . In summary, sharks were attracted to the research vessel by baiting a custom-made circle hook (Mustad, Gjövik, Norway) with a tuna or salvaged marine-mammal carcass. The baited hook was suspended behind the vessel via a plastic float. Four to six large plastic floats (22 kg flotation each) were evenly spaced along the line to keep the shark near the surface while providing drag. Once a shark was hooked, a smaller boat was used to follow the shark, bring the animal to the surface by shortening the distance between the floats and the shark, and guide the shark onto a large submerged platform that was attached to the larger research vessel. Once on the platform, the shark was hydraulically raised above the waterline. An irrigation hose was immediately placed in the mouth of the shark to flush seawater over the gills, the hook was removed, and a wet towel was placed over the head to protect the eyes and calm the animal. The time taken to capture the four female sharks ranged from 45 to 162 minutes (mean 77 minutes), and tagging time ranged from 14 to 17 minutes (mean 16 minutes). Each shark was measured and sex recorded prior to release. Determination of sexual maturity for female white sharks was based on a total length of at least 4.5 m .
SLRT tags were attached to the apex of the shark’s first dorsal fin by drilling four small holes through the fin, and securing the tag with plastic bolts. Each time a tagged shark’s dorsal fin was out of the water, a wet/dry switch activated the transmitter. Tags were programmed to transmit a maximum of 250 messages per day. If the tag remained out of the water long enough for an Argos satellite to receive four consecutive transmissions, the Doppler-shift-induced frequency change allowed calculation of the tag’s location  with associated location error. All messages, even those that did not provide location, gave a status message that included the SST recorded at the location of the tagged shark.
Argos position processing
All transmitted location positions were processed using a Kalman filter and reprocessed by Argos with a smoothing algorithm. The Kalman filter  computes the platform location and an error estimate, based on the Argos Doppler frequency measurements obtained up to the date of the location. The smoother is based on the Rauch-Tung-Striebel formulae , which combines, in a backward-time recursive process, some quantities produced by the Kalman filter. The Rauch-Tung-Striebel smoother computes the location and the error conditioned on all the measurements recorded (that is, past, present, and future available measurements). Location data were further selected with a speed filter between consecutive points, using the maximum estimated sustained speed of 192 km/day .
Date of the start and end of the PP were determined either directly by date of location data when available to indicate movement from the OGP to the PP, or by examining SST associated with transmitted status messages, and matching these to moderate resolution imaging spectroradiometer (MODIS) weekly SST data from the National Aeronautics and Space Administration (NASA) Aqua satellite. The date of the end of GIAP was determined by examining the first point away from GI and calculating the date of departure back in time, based on published average speed during travel (77 km/day ). All location points during the offshore phase for all four sharks were used to determine a MCP for the region used while offshore. MCP was determined using the minimum bounding geometry tool in ArcGIS. The percentage of location data from August to February within 15 km of GI was calculated by using a frequency of 1 location per day, and using all data from the four tagged female sharks during those months.
Guadalupe Island, Mexico
Guadalupe Island aggregation phase
Minimum convex polygon
Offshore gestation phase
Rapid oscillatory diving
Satellite-linked radio telemetry
Sea surface temperature
Shared offshore foraging area
Funding for this study was provided by the Offield Family Foundation, Guy Harvey Ocean Foundation and National Geographic via Fischer Productions. Invaluable field assistance was provided by C. Fischer, B. McBride and the crew of the M/V Ocean. We thank L. Wheeler and E. Andrews of the Marine Mammal Center for their assistance in the collection of salvaged whale blubber. We thank O. Sosa-Nishizaki, F. Galván-Magaña, and M. Hoyos-Padilla for assistance in obtaining Mexican permits. Research was conducted in accordance with permits through SEMARNAT (Secretaría de Medio Ambiente y Recursos Naturales), and CONANP (Comisión Nacional de Áreas Naturales Protegidas). The cover image was given with the permission of Michael L. Domeier.
- Boustany AM, Davis SF, Pyle P, Anderson SD, Le Boeuf BJ, Block BA: Expanded niche for white sharks. Nature 2001, 415: 35–36.View ArticleGoogle Scholar
- Bonfil R, Meyer M, Scholl MC, Johnson R, O’Brien S, Oosthuizen H, Swanson S, Kotze D, Paterson M: Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 2005, 310: 100–103. 10.1126/science.1114898PubMedView ArticleGoogle Scholar
- Weng KC, Boustany AM, Pyle P, Anderson SD, Brown A, Block BA: Migration and habitat of white sharks ( Carcharodon carcharias ) in the eastern Pacific Ocean. Mar Biol 2007, 152: 877–894. 10.1007/s00227-007-0739-4View ArticleGoogle Scholar
- Domeier ML, Nasby-Lucas N: Migration patterns of white sharks Carcharodon carcharias tagged at Guadalupe Island, Mexico, and identification of an eastern Pacific shared offshore foraging area. Mar Ecol Prog Ser 2008, 370: 221–237.View ArticleGoogle Scholar
- Jorgensen SJ, Reeb CA, Chapple TK, Anderson S, Perle C, Van Sommeran SR, Fritz-Cope C, Brown AC, Klimley AP, Block BA: Philopatry and migration of Pacific white sharks. Proc R Soc B 2010, 277: 679–688. 10.1098/rspb.2009.1155PubMed CentralPubMedView ArticleGoogle Scholar
- Bonfil R, Francis MP, Duffy C, Manning MJ, O’Brien S: Large-scale tropical movements and diving behavior of white sharks Carcharodon carcharias tagged off New Zealand. Aquat Biol 2010, 8: 115–123.View ArticleGoogle Scholar
- Domeier ML, Nasby-Lucas N: Sex specific migration patterns and sexual segregation for adult white sharks in the northeastern Pacific. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:133–146.View ArticleGoogle Scholar
- Domeier ML: A new life-history hypothesis for white sharks, Carcharodon carcharias , in the northeastern Pacific. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:199–224.View ArticleGoogle Scholar
- Jorgensen S, Chapple TK, Anderson S, Hoyos M, Reeb C, Block BA: Connectivity among white shark coastal aggregation areas in the northeastern Pacific. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:159–168.View ArticleGoogle Scholar
- Duffy C, Francis MP, Manning MJ, Bonfil R: Regional population connectivity, oceanic habitat, and return migration revealed by satellite tagging of white sharks, Carcharodon carcharias , at New Zealand aggregation sites. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:301–318.View ArticleGoogle Scholar
- Pardini AT, Jones CS, Noble LR, Kreise B, Malcom H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Duffy CAJ, Martin AP: Sex-biased dispersal of great white sharks. Nature 2001, 412: 139–140. 10.1038/35084125PubMedView ArticleGoogle Scholar
- Domeier M, Nasby-Lucas N: Annual re-sightings of photographically identified white sharks ( Carcharodon carcharias ) at an eastern Pacific aggregation site (Guadalupe Island, Mexico). Mar Biol 2007, 150: 977–984. 10.1007/s00227-006-0380-7View ArticleGoogle Scholar
- Anderson SD, Chapple TK, Jorgensen SJ, Klimley AP, Block BA: Long-term individual identification and site fidelity of white sharks, Carcharodon carcharias , of California. Mar Biol 2011, 158: 1233–1237. 10.1007/s00227-011-1643-5PubMed CentralPubMedView ArticleGoogle Scholar
- Gubili C, Duffy CAJ, Cliff G, Wintner SP, Shivji M, Chapman D, Bruce BD, Martin AP, Sims DW: Application of molecular genetics for conservation of the white shark, Carcharodon carcharias , L.1758. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:357–380.View ArticleGoogle Scholar
- Gubili C, Bilgin R, Kalkan E, Ünsal Karhan S, Jones CS, Sims DW, Kabasakal H, Martin AP, Noble LR: Antipodean white sharks on a Mediterranean walkabout? Historical dispersal leads to genetic discontinuity and an endangered anomalous population. Proc R Soc B 2011, 278: 1679–1686. 10.1098/rspb.2010.1856PubMed CentralPubMedView ArticleGoogle Scholar
- Avise JC: Molecular Markers, Natural History, and Evolution. Sunderland: Sinauer & Associates; 2004.Google Scholar
- Waples RS, Gaggiotti O: What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 2006, 15: 1419–1439. 10.1111/j.1365-294X.2006.02890.xPubMedView ArticleGoogle Scholar
- Nasby-Lucas N, Domeier ML: Use of photo identification to describe a white sharks aggregation at Guadalupe Island, Mexico. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:381–392.View ArticleGoogle Scholar
- Anderson S, Pyle P: A temporal, sex-specific occurrence pattern among white sharks ( Carcharodon carcharias ) at the South Farallon Islands, California. Calif Fish Game 2003, 89: 96–101.Google Scholar
- Mollet H, Cliff G, Pratt H, Stevens J: Reproductive biology of the female shortfin mako, Isurus oxyrinchus Rafinesque , 1810, with comments on the embryonic development of lamnoids. Fish Bull 2000, 98: 299–318.Google Scholar
- Dulvy NK, Baum JK, Clarke S, Compagno LJV, Cortés E, Domingo A, Fordham S, Fowler S, Francis MP, Gibson C, Martinez J, Musick JA, Soldo A, Stevens JD, Valent S: You can swim but you can't hide: the global status and conservation of oceanic pelagic sharks and rays. Aquat Conservat Mar Freshwat Ecosyst 2008, 18: 459–482. 10.1002/aqc.975View ArticleGoogle Scholar
- Domeier ML, Nasby-Lucas N, Palacios DM: The Northeastern Pacific white shark Shared Offshore Foraging Area (SOFA): A first examination and description from ship observations and remote sensing. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:147–158.View ArticleGoogle Scholar
- Taylor JKD, Mandelman JW, McLellan WA, Moore MJ, Skomal GB, Rotstein DS, Kraus SD: Shark predation on North Atlantic right whales ( Eubalaena glacialis ) in the southeastern United States calving ground. Mar Mamm Sci 2013, 29: 204–212. 10.1111/j.1748-7692.2011.00542.xView ArticleGoogle Scholar
- Lowe CG, Blasius ME, Jarvis ET, Mason TJ, Goodmanlowe GD, O'Sullivan JB: Historic fishery interactions with white sharks in the southern California bight. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:169–186.View ArticleGoogle Scholar
- Santana-Morales O, Sosa-Nishizaki O, Escobedo-Olvera MA, Oñate-González EC, O'Sullivan JB, Cartamil D: Incidental catch and ecological observations of juvenile white sharks, Carcharodon carcharias , in western Baja California, Mexico: Conservation implications. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:187–198.View ArticleGoogle Scholar
- Galván-Magaña F, Hoyos-Padilla EM, Navarro-Serment CJ, Márquez-Farías F: Records of white shark, Carcharodon carcharias , in the Gulf of California, Mexico. Mar Biodiversity Rec 2010, 3: 1–6.View ArticleGoogle Scholar
- Jorgensen SJ, Arnoldi NS, Estess EE, Chapple TK, Rückert M, Anderson SD, Block BA: Eating or meeting? Cluster analysis reveals intricacies of white shark ( Carcharodon carcharias ) migration and offshore behavior. PLoS One 2012, 7: e47819. http://www.plosone.org/article/info:doi/10.1371/journal.pone.0047819 10.1371/journal.pone.0047819PubMed CentralPubMedView ArticleGoogle Scholar
- Domeier ML, Nasby-Lucas N, Lam CH: Fine-scale habitat use by white sharks at Guadalupe Island, Mexico. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:121–132.View ArticleGoogle Scholar
- Höglund J, Alatalo RV: Leks. Princeton: Princeton University Press; 1995.View ArticleGoogle Scholar
- Feldheim KA, Gruber SH, Ashley MV: The breeding biology of lemon sharks at a tropical nursery lagoon. Proc R Soc Lond B 2002, 269: 1655–1661. 10.1098/rspb.2002.2051View ArticleGoogle Scholar
- Mourier J, Planes S: Direct genetic evidence for reproductive philopatry and associated fine‐scale migrations in female blacktip reef sharks ( Carcharhinus melanopterus ) in French Polynesia. Mol Ecol 2013, 22: 201–214. 10.1111/mec.12103PubMedView ArticleGoogle Scholar
- Portnoy DS, McDowell JR, Heist EJ, Musick JA, Graves JE: World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus . Mol Ecol 2010, 19: 1994–2010. 10.1111/j.1365-294X.2010.04626.xPubMedView ArticleGoogle Scholar
- Tillett BJ, Meekan MG, Field IC, Thorburn DC, Ovenden JR: Evidence for reproductive philopatry in the bull shark Carcharhinus leucas . J Fish Biol 2012, 80: 2140–2158. 10.1111/j.1095-8649.2012.03228.xPubMedView ArticleGoogle Scholar
- Bruce BD, Bradford RW: Habitat use and spatial dynamics of juvenile white sharks, Carcharodon carcharias , in eastern Australia. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:225–254.View ArticleGoogle Scholar
- Hueter RE, Heupel MR, Heist EJ, Keeney DB: Evidence of philopatry in sharks and implications for the management of shark fisheries. J Northw Atl Fish Sci 2005, 35: 239–247.View ArticleGoogle Scholar
- Castro JI: A summary of observations on the maximum size attained by the white sharks. In Global Perspectives on the Biology and Life History of the White Shark. Edited by: Domeier ML. Boca Raton: CRC Press; 2012:85–90.View ArticleGoogle Scholar
- Francis MC: Observations of a pregnant white shark with a review of reproductive biology. In Great white sharks: the biology of Carcharodon carcharias. Edited by: Klimley AP, Ainley DG. San Diego: Academic Press; 1996:157–172.View ArticleGoogle Scholar
- Taillade M: Animal tracking by satellite. In Wildlife telemetry: remote monitoring and tracking of animals. Edited by: Priede IG, Swift SM. London: Ellis Horwood; 1992:149–160.Google Scholar
- Kalman RE: A new approach to linear filtering and prediction problems. Trans ASME J Basic Eng 1960, 82: 35–45.View ArticleGoogle Scholar
- Rauch HE, Tung F, Striebel CT: Maximum likelihood estimates of linear dynamic systems. AIAA J 1965, 3: 1445–1450. 10.2514/3.3166View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.