Multi-predator community at Southeast Farallon Island (SEFI)

Long-term intensive monitoring surveys, combined with electronic tagging and observational studies, revealed the frequency and modality of cryptic interactions amongst marine predator populations at SEFI. Seasonality in white shark and killer whale presence matched annual cycles in prey aggregations, namely juvenile (age 0–3) northern elephant seals (Mirounga angustirostris) that first haulout during spring molt (peaking in April and May) and then again in the fall (peaking in October and November) (Fig. 1). An estimated 219 adult and sub-adult white sharks ((130, 275) 95% credible intervals) aggregate and feed at SEFI and adjacent elephant seal rookeries around Point Reyes during this fall haulout period58. Long-term (1972–2010) birth rates of elephant seals at SEFI are variable (median = 198 births/year; mean = 232; SD = 132) and have decreased to a relatively stable level over the past decade, while the regional population continues to rapidly increase59. Additionaly, California sea lions (Zalophus californianus), Steller sea lions (Eumetopias jubatus), harbor seals (Phoca vitulina ricardii), and northern fur seals (Callorhinus ursinus) also haul out at SEFI at various times of the year55.

Killer whale pod observations occurred year-round on 57 occasions between 1987 and 2013 (Fig. 1C). These sparse occurrences peaked in May, concurrent with gray whale calf migrations, followed by a secondary fall peak during October and November (Fig. 1C). The co-occurrence of white sharks and killer whales was confined to fall, coincident with the peak in adult white shark activity at SEFI (Fig. 1B). During the fall overlap (September–November) killer whale pods were recorded during daily surveys ( mean = 7.7 hr/day; weather permitting) from the island lighthouse at various distances from SEFI on 18 out of 1998 survey days in eight different years: 1992, 1995–1998, 2000, 2001, 2009, and 2013 (Table 1). The recorded duration of these 18 visits ranged from a maximum of 5.5 hours to less than an hour. When killer whale ecotype could reliably be identified (n = 5), mammal-eating transient pods were the most common visitors to SEFI (four of five), while offshore individuals were identified on a single occasion in 2009 when both offshores and transients were observed (Table 1).

Table 1 Summary of killer whale observations during fall (September 1 – November 30) standardized surveys at Southeast Farallon Island between 1987 and 2013. Full size table

White sharks aggregated at SEFI annually, where the observed number of predations by sharks peaked during October and November (Fig. 2B). During the fall surveys, a mean of 40 observed predations (±16 SD; N = 27 years) by sharks occurred annually on elephant seals and unidentified pinniped prey. In years when killer whales were not observed or were sighted 3 or more km from shore (N = 19), the distribution of predation events on pinnipeds peaked between mid-October and mid-November (Fig. 2B). In years when killer whales were sighted <3 km from shore (N = 9), this predation rate was depressed and truncated (Fig. S3 and Table S1). Therefore, annual predation rates on pinnipeds were significantly impacted when killer whale activity occurred at a distance threshold <3 km from the SEFI seal haul-out.

Figure 2 Predator-prey relationship between white sharks (Carcharodon carcharias) and elephant seals (Mirounga angustirostrous) altered by the presence of killer whales (Orcinus orca) at Southeast Farallon Island (SEFI). (A) Annual predation rate by C. carcharias as a function of mean fall (Sept. – Nov.) M. angustirostrous counts fit with a log-log regression line (dashed black line) showing confidence interval (dashed blue lines). Points are years where no flight response was detected, and triangles are the years in which a flight response was observed, near or before the peak of the C. carcharias season (≤November 2, inverted triangles), and near the end of the season (≥November 19, upright triangles). For comparison, an equivalent regression fit excluding flight years is shown with red dotted lines. (B) Seasonal C. carcharias kill rate as a function of the observed distance of O. orca activity to SEFI. The distribution of observed predations was reduced and truncated as a function of O. orca proximity to the common foraging ground (distance given in legend in km). Full size image

Overall, the observed annual rate of predation by sharks was positively correlated with the abundance of elephant seals present (R2 = 0.191, p = 0.023) (Fig. 2A). However, in years when killer whales occurred in close proximity to the island during or before peak shark abundance, the observed rate of predation by sharks deviated most from this relationship dropping 3.5 to 7-fold from the long-term average of 6.02 ± 2.4 predations per 100hrs (SD), to 1.73, 1.29, and 0.84 respectively in 1997, 2009, and 2013 (Fig. 2B). In 2000 by contrast, killer whales also occurred close to SEFI, but much later in the season (November 18; Table 1) resulting in no deviation from the expected annual predation rate (Fig. 2A).

Displacement of white sharks and flight response

Acoustic tag detections documented the abrupt and consistent flight of white sharks from SEFI in 2009, 2011, and 2013 (Figs 3 and SI). In the best-documented instance, killer whales from two separate pods (offshore and transient ecotypes; Table 1) arrived at SEFI on November 2, 2009, when 17 previously tagged white sharks were present. Killer whales were present at SEFI for just over 2.5 hours between 12:48 and 15:30 local time, remained on the western side of SEFI during approach and initiated three separate killing bouts on pinnipeds, then departed to the north. There were no observations of direct predation on white sharks, and all tagged animals were later confirmed alive through acoustic detections; still predations on untagged white sharks could not be ruled out.

Figure 3 The flight response of white sharks (Carcharodon carcharias) triggered by the presence of killer whales (Orcinus orca) at a common foraging site, Southeast Farallon Islands (SEFI). (A) Mean daily number of acoustic tagged C. carcharias detected (2007–2013; excluding 2009; shaded standard error) at Central California receivers colored by location: Tomales Point (green), Southeast Farallon Islands (orange and orange/yellow), Año Nuevo Island (blue), and Point Reyes (purple). (B) The number of tagged C. carcharias detected per day at each site (respectively colored) during the 2009 season showing the sudden departure of all tagged individuals from SEFI in response to O. orca (Nov 2) presence. Note the subsequent influx around Año Nuevo Island where the shaded orange area represents individuals present at SEFI during killer whale interactions. (C) Detections of each tagged shark at color-coded locations are shown along the horizontal timeline illustrating the abrupt departure from SEFI by tagged C. carcharias following O. orca presence (between vertical black lines) and subsequent avoidance. Solid orange diamonds indicate the western SEFI receiver while orange with yellow centers indicate the eastern receiver. (D) Precise receiver locations are indicated by the right corner of each solid diamond and the left corner of the yellow filled diamond. Full size image

Desertion of SEFI by all tagged sharks followed the foraging behavior of killer whales close to SEFI. Regular daily detections of 17 tagged animals at two stationary acoustic receivers moored on eastern and western sides of SEFI (SI) discontinued abruptly following the appearance of killer whales (Fig. 3). Overall, the mean number of white sharks detected per day at SEFI declined from a seasonal maximum to zero for the remainder of the season. Declines in detections followed a spatial gradient, immediately subsiding at the western receiver most proximal to killer whale observations, followed by a tapering of detections over the following hours at the eastern receiver (Fig. 3). Seven hours and 50 minutes following the event, no tagged sharks remained within receiver range at SEFI and 16 individuals (of 17 displaced tagged sharks) were not detected at SEFI again until the following season (July 2010 or later). One individual returned a week later (November 8), and was detected at SEFI three times over 73 minutes, before departing and being re-detected at Año Nuevo Island (ANI) on November 24.

Anomalous shark absences at SEFI for the remainder of the 2009 season resulted in influxes of displaced individuals at mainland aggregation sites. Within 2 to 13 days of departing SEFI following the killer whale disturbance at SEFI, seven tagged individuals relocated nearly 90 km to the south at ANI. Three individuals were redetected at Tomales Point for extended periods, before two of these continued to ANI (Fig. 3). These influxes at mainland sites resulted in daily totals of individual sharks detected at ANI increasing sharply from 4 day−1 on 2 November to 10 day−1 by 14 November and peaking at 16 day−1 by 23 November. In contrast, SEFI remained virtually shark-free for the remaining season. Three tagged individuals not initially present during the killer whale event were detected subsequently at SEFI, though for abbreviated durations (0.25, 1, and 11 hours, respectively) compared to mean SEFI residency periods of 35 days32. Two of these three sharks were then subsequently detected at mainland aggregation sites (Fig. 3).

Acoustic tag records provided a clear ‘signature’ for understanding and estimating flight responses of sharks relative to other killer whale occurrences at SEFI during years when sufficient active tags were present (see Table 1). The well-documented incident in 2009 was consistent with previous observations of cessation of seal predation at SEFI by white sharks following brief killer whale visits52,60. Acoustic tag records revealed two additional similar signatures at SEFI: November 20, 2011, with 10 tagged individual present, and October 31, 2013, with 3 tagged individuals present (see SI). Inclement weather resulting in poor visibility precluded visual confirmation of killer whales for the former event (no surveys that day) in 2011. On the 2013 occasion, 13 killer whales were observed during regular shark visual surveys from SEFI. In both cases following typical flight responses, no further tag detections were recorded at SEFI for the remainder of the season (see SI). Similarly, no further predations of pinnipeds by white sharks were observed during the remaining visual surveys in 2011 and 2013, and only a single predation during the remaining season in 2009 near Mid-Farallon Island, 3.4 km northwest of SEFI. In summary, a white shark flight response from SEFI related to killer whale occurrence was identified in four separate years, along with a fifth flight response with unconfirmed attribution (Table 1). While intensive observer survey data are lacking at TOM and ANI, no equivalent flight response was ever apparent in acoustic tagging data with continuous coverage between 2006 and 2013.

Ecological roles and context of killer whale-shark interactions

Transient killer whales were present in the two flight response years when ecotypes could be reliably determined (1997, 2009), whereas offshore individuals were identified in addition to transients in the 2009 disturbance. In determining the ecological relationship between white sharks and killer whales, understanding whether their interactions are defined by predator-prey or competitive aggression interactions depends on killer whale ecotype. Mammal-eating transient killer whales45 are direct competitors, but also pose a predatory threat as illustrated in the 1997 event52 (see introduction). Interactions with the offshore ecotype are potentially predatory, as well as competitive. Offshore killer whales are known to forage on teleosts and elasmobranchs, the latter forming a potentially important dietary component as evidenced by apical teeth worn flat, presumably from the abrasive shark skin50, and observations of repeated feeding on Pacific sleeper sharks, Somniosus pacificus61. Residents are likely a weak competitor (for teleosts) and potentially not a predation threat45,49. Whether white sharks might distinguish a predatory versus competitive threat remains unknown, but the result may be the same. Like predation pressure, interspecific competitive aggression can similarly drive behavior that reduces encounter rates, shape habitat use, and shift activity schedules8,62. Only one direct predation on white sharks by killer whales was ever confirmed on white sharks at SEFI52, yet white sharks vacating SEFI, effectively freed up potential pinniped resources for the killer whales and restricted white shark access to those resources.

Risk effects among top ocean predators

This study demonstrates the occurrence of risk effects among upper trophic level marine predators. The key interactions surrounding the phenomena remained cryptic and rarely observed despite intensive long-term visual surveys and multi-year continuous electronic tracking coverage. In the rare instances when both predators co-occurred at SEFI, antagonistic interactions between them resulted in the extended displacement of foraging white sharks via risk effects (Fig. 3), and in turn reduced local predation pressure on seals (Fig. 2). Despite exceptionally brief killer whale visits to SEFI (2.4–5 hr) during well-documented events near the peak white shark foraging season, the observed predation rate on pinnipeds by white sharks during those years decreased (Fig. 2). It is unlikely that killer whale predation on pinnipeds could compensate for the reduction in predation by white sharks following their displacement. Of the predation events observed at the surface in 15,383 hours of lighthouse surveys between 1987 and 2013, 912 were attributed to white sharks and only 5 events on 3 dates to killer whales.

Killer whales exert top-down effects in various systems by directly reducing meso-predator density through consumption1,4 as well as eliciting shifts in prey behaviors and distributions due to risk effects63,64. Similarly, large sharks can have a direct regulatory influence over their prey populations6,65,66, and induce food-safety tradeoffs67 including avoidance behavior68,69. This study suggests that intraguild interactions between killer whales and white sharks may result in cascading effects at lower trophic levels by reducing consumptive (and possibly non-consumptive) effects on elephant seals. Quantifying the indirect population-level effects killer whales induce on white sharks may have on elephant seals locally and regionally remains an important future direction. Northern elephant seals are undergoing rapid habitat expansion and population growth, following long-term human exploitation and extreme depletion59. Any population regulatory effects white sharks, killer whales, and their interactions have on elephant seals could become more significant as elephant seals approach an equilibrium level.

Occasional consumption of the highly-caloric liver of white sharks may confer ancillary energetic benefits to the killer whale. The fitness loss to white sharks from direct lethal interactions with killer whales is unambiguous. But avoidance behaviors in response to killer whale presence could also impact white shark fitness by restricting spatiotemporal access and activity to habitats that are sub-optimal or more competitive (more densely populated by conspecifics). Intimidation and predation risk pervasively affects entire populations, not just the individuals directly killed16. Potential consequences of displacement to white sharks should be evaluated within the ecological context of their migratory phenology. Fall-time aggregations and site fidelity of NEP white sharks along the central California coast immediately precede extensive offshore migrations to relatively oligotrophic waters32,60,70. Despite spending one third of their time in coastal California habitats, adults assimilate nearly half their protein from coastal foraging41. Concentrated energy acquisition during this coastal phase is stored in the oil-rich liver mass and is expended during long migrations (1000–3000 km) to seasonal offshore subtropical habitats43, where males increase diving activity extensively32,38. Disruptions of foraging prior to migration is known to negatively impact migratory performance in numerous long-distance migrating species30,71,72. Future efforts should aim to measure the impact and ecological implications of these risk effects on white shark fitness and elephant seal population dynamics.