Philopatry and migration of Pacific white sharks

Abstract

Advances in electronic tagging and genetic research are making it possible to discern population structure for pelagic marine predators once thought to be panmictic. However, reconciling migration patterns and gene flow to define the resolution of discrete population management units remains a major challenge, and a vital conservation priority for threatened species such as oceanic sharks. Many such species have been flagged for international protection, yet effective population assessments and management actions are hindered by lack of knowledge about the geographical extent and size of distinct populations. Combining satellite tagging, passive acoustic monitoring and genetics, we reveal how eastern Pacific white sharks (Carcharodon carcharias) adhere to a highly predictable migratory cycle. Individuals persistently return to the same network of coastal hotspots following distant oceanic migrations and comprise a population genetically distinct from previously identified phylogenetic clades. We hypothesize that this strong homing behaviour has maintained the separation of a northeastern Pacific population following a historical introduction from Australia/New Zealand migrants during the Late Pleistocene. Concordance between contemporary movement and genetic divergence based on mitochondrial DNA demonstrates a demographically independent management unit not previously recognized. This population's fidelity to discrete and predictable locations offers clear population assessment, monitoring and management options.

Figure 1.

Site fidelity and homing of white sharks (Carcharodon carcharias) tagged along the central California coast during 2000–2007 revealed by PAT records. (a–f) Site fidelity demonstrated by six individual tracks (yellow lines; based on five-point moving average of geolocations). Triangles indicate tag deployment locations and red circles indicate satellite tag pop-up endpoints (Argos transmissions) for white sharks returning back to central California shelf waters after offshore migrations. (g) Site fidelity of all satellite tagged white sharks (n = 68) to three core areas in the NEP included the North American continental shelf waters, the waters surrounding the Hawaiian Island Archipelago and the white shark ‘Café’. Yellow circles represent position estimates from light- and SST-based geolocations (Teo et al. 2004), and red circles indicate satellite tag endpoint positions (Argos transmissions), respectively.

Figure 2.

White shark migratory cycle and site fidelity revealed by a combination of acoustic and satellite tagging. (a) Detections of tagged white sharks by an array of acoustic receivers (see figure 5b for map) along the central California coast show seasonal presence and absence pulses. Twenty individuals carried acoustic tags deployed in 2006 (red bars), 31 in 2007 (blue bars) and 27 in 2008 (green bars), respectively. The number of detections per day was normalized by the number of sharks tagged and the number of active receivers. Dashed line indicates when acoustic tagging began. (b) Longitude geolocation estimates from PAT tag records between October 2005 and June 2008 show a corresponding seasonal onshore–offshore migration pattern. Shading indicates peak onshore periods.

Figure 3.

Seasonal migratory pattern and distribution of male (n = 32), female (n = 23) and unsexed (n = 14) white sharks tagged in central California (arrow) with PAT tags. Yellow (male), magenta (female) and grey (unsexed) circles represent position estimates from light- and SST-based geolocation. The peak offshore period was between April and July and the peak onshore period between September and November, respectively. Male positions are plotted over female, then unsexed positions, respectively, showing a higher aggregation of males in the Café between April and July, while females moved in and out of the same area.

Figure 4.

Male and female C. carcharias movement and habitat use at the white shark ‘Café’. (a) Longitude geolocations of 32 males (black) and 23 females (magenta) tagged with satellite tags during 7 separate years plotted over one seasonal cycle revealed the consistent converging of males near 133° W (Café) between April and July. (b) The frequency of geolocations over longitude demonstrates that while offshore, males (black) are more focused in the Café while females (magenta) are more dispersed between the Café and Hawaii. (c) Rapid oscillatory diving behaviour in the Café identified (from archival recovery tags) by an order of magnitude increase in median vertical displacement rate occurring between 15 April and 15 July (n = 4 sharks; p = 0.003; t-test). Bars indicate the average median displacement rate among individuals (n = 4;±s.d.). (d–g) Four individual archival records (all male; PAT #s 45, 49, 54 and 22; electronic supplementary material, table S1) recovered from white sharks visiting the Café showing longitude (left axis), depth (right axis) and vertical displacement rate (colour scale) over time. Oscillatory diving occurs primarily between 15 April and 15 July, during the same period when males are most aggregated, despite earlier arrival.

Figure 5.

White sharks tagged with acoustic transmitters along the central California coast (2006 and 2007 deployments) detected by acoustic receivers reveal periods of presence and absence. (a) Acoustic detections over time revealed the presence (1-day vertical bands coloured by location; see panel (b) for colour key; Hawaii indicated by cyan) and absence (dark blue; between first and last detections) of individuals near receivers (250 m detection range). Circles, coloured by location, represent the presence of individuals (photographed) with failed tags (electronic supplementary material, figure S1). Triangles indicate start and end times for data collection, coloured by location, respectively. (b) Receiver locations scaled in size by mean residence time (days in text) from north to south include TOM (green), REY (yellow), SEFI (orange) and ANI (red). Lines connecting locations are scaled in thickness relative to the number of transits between adjoining sites. (c) The number of transits by white sharks between receiver sites determined from acoustic detection at one site followed by a subsequent detection at another.

Figure 6.

Phylogeny of unique haplotypes found in Indo-Pacific white sharks inferred from comparisons of mitochondrial DNA control region sequences (1109 base pairs) of 59 individuals from the central California coast with previously published sequences from SA and ANZ. Bayesian tree branch lengths reflect substitutions per site. The number of samples comprising each haplotype is given in parentheses if greater than 1. GenBank accession numbers are indicated for each haplotype followed by the location of the sample. Bayesian posterior probabilities are indicated above nodes while likelihood bootstrap values are shown below. NEP sharks from California (CA) form a monophyletic clade (bootstrap = 58%, Bayesian posterior probability = 60%). Individuals from the two dominant lineages within this clade had similar migratory patterns.