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Sustained Disruption of Narwhal Habitat Use and Behavior in The Sustained disruption of narwhal habitat use and behavior in the presence of Arctic killer whales Greg A. Breeda,1, Cory J. D. Matthewsb, Marianne Marcouxb, Jeff W. Higdonc, Bernard LeBlancd, Stephen D. Petersene, Jack Orrb, Natalie R. Reinhartf, and Steven H. Fergusonb aInstitute of Arctic Biology, University of Alaska, Fairbanks, AK 99775; bArctic Aquatic Research Division, Fisheries and Oceans Canada, Winnipeg, MB, Canada R3T 2N6; cHigdon Wildlife Consulting, Winnipeg, MB, Canada R3G 3C9; dFisheries Management, Fisheries and Oceans Canada, Quebec, QC, Canada G1K 7Y7; eAssiniboine Park Zoo, Winnipeg, MB, Canada R3R 0B8; and fDepartment of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada R3T 2N2 Edited by James A. Estes, University of California, Santa Cruz, CA, and approved January 10, 2017 (received for review July 17, 2016) Although predators influence behavior of prey, analyses of elec- Electronic tracking tags are also frequently used to track verte- tronic tracking data in marine environments rarely consider how brates in marine systems. Although there is evidence that marine predators affect the behavior of tracked animals. We collected animals adjust their behavior under predation threat (21, 22, 12), an unprecedented dataset by synchronously tracking predator few data or analyses exist showing how predators affect the (killer whales, N = 1; representing a family group) and prey movement of tracked marine animals. These data are lacking (narwhal, N = 7) via satellite telemetry in Admiralty Inlet, a because marine environments are more difficult to observe and large fjord in the Eastern Canadian Arctic. Analyzing the move- tracked animals often move over scales much larger than their ment data with a switching-state space model and a series of terrestrial counterparts, making it difficult to measure predator mixed effects models, we show that the presence of killer whales density in situations where tracking tags are deployed on prey. strongly alters the behavior and distribution of narwhal. When Instead, analyses have tended to focus on habitat preference, killer whales were present (within about 100 km), narwhal moved resource distribution, and the oceanographic controls of primary closer to shore, where they were presumably less vulnerable. production (23–25). If predators are affecting the behavior of Under predation threat, narwhal movement patterns were more tracked animals without being considered or recognized, partic- ECOLOGY likely to be transiting, whereas in the absence of threat, more ularly in situations where exposure to predators is chronic, infer- likely resident. Effects extended beyond discrete predatory events ence about which habitats animals prefer could be biased. More- and persisted steadily for 10 d, the duration that killer whales over, nonconsumptive effects of predators, such as lost foraging remained in Admiralty Inlet. Our findings have two key conse- opportunities, could manifest as nutritional stress or starvation quences. First, given current reductions in sea ice and increases that is incorrectly attributed to changes in productivity. in Arctic killer whale sightings, killer whales have the poten- Here, we show using unprecedented telemetry data from syn- tial to reshape Arctic marine mammal distributions and behavior. chronously tracked and interacting predator (killer whale Orci- Second and of more general importance, predators have the nus orca) and prey (narwhal Monodon monoceros) collected potential to strongly affect movement behavior of tracked marine in the Eastern Canadian Arctic (ECA) that persistent inter- animals. Understanding predator effects may be as or more impor- action with killer whales induces changes in both behavior tant than relating movement behavior to resource distribution or and habitat use of narwhal. Previous findings, in this system bottom-up drivers traditionally included in analyses of marine ani- (26) and elsewhere (6, 27–32), have shown that killer whales eli- mal tracking data. cit a variety of antipredator responses in other marine mamm- als. However, these earlier observations are generally limited to predator–prey dynamics j sea ice j biologging j climate change j trait-mediated effects Significance onsumptive effects (alternatively termed “density-mediated Ceffects”) of predators on prey refer to the mortality incurred Predators are widely understood to impact the structure when predators kill and consume prey during predation events. and stability of ecosystems. In the Arctic, summer sea ice is They can control prey populations and in certain circumstances, rapidly declining, degrading habitat for Arctic species, such as restructure ecosystems through trophic cascades (1–3). Noncon- polar bears and ringed seals, but also providing more access sumptive effects (also termed “trait-mediated effects”) can sim- to important predators, such as killer whales. Using data ilarly affect prey populations by altering species’ behavior and from concurrently tracked predator (killer whales) and prey space use under perceived or real predation risk, which are (narwhal), we show that the presence of killer whales sig- associated with decreased fitness through loss of access to nificantly changes the behavior and distribution of nar- key foraging areas, disrupted social structure, increased energy whal. Because killer whales are effective predators of many expenditure and stress imposed by persistent vigilance and marine mammals, similar predator-induced changes would be escape behaviors, and decreased reproductive success (3–7). expected in the behavior of tracked animals in marine ecosys- Nonconsumptive effects are sublethal (8, 9), but because they tems worldwide. However, these effects are rarely considered can impact many individuals in a population simultaneously, the and may frequently go unrecognized. cumulative effect may exceed consumptive effects (8, 10–12). In terrestrial systems, movement data collected by electronic Author contributions: C.J.D.M., J.W.H., S.D.P., and S.H.F. designed research; C.J.D.M., B.L., telemetry tracking tags have been used to clearly show that J.O., and N.R.R. performed research; G.A.B. and M.M. analyzed data; and G.A.B. and carnivores affect prey species’ use of space and habitat selec- C.J.D.M. wrote the paper. tion (13–15), and these nonconsumptive effects can negatively The authors declare no conflict of interest. impact population dynamics (10, 13, 11). When large enough, This article is a PNAS Direct Submission. such effects have even been suggested to lead to trophic cascades Data deposition: The data reported in this paper are available in Dataset S1. (16, 17, 3). However, there is disagreement about whether non- 1To whom correspondence should be addressed. Email: [email protected]. consumptive effects can be strong enough to cause trophic cas- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. cades, even in well-studied exemplar systems (18–20). 1073/pnas.1611707114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1611707114 PNAS Early Edition j 1 of 6 Downloaded by guest on October 2, 2021 we show that behavioral changes extend beyond discrete preda- tion or attack events and that the mere presence of killer whales in a system can cause relatively large and persistent changes in behavior and space use in prey species. Our data show that changes persist for the entire period of exposure of narwhal to killer whales. Narwhal behavior quickly returned to normal after killer whales left the system. These dynamics, persistent change in a system (in this case, narwhal behavior) while an affecting agent (killer whales) is present followed by rapid recovery after the affecting agent is removed, suggest that killer whales act as a press disturbance when present. Our findings also have relevance for the future of Arctic ecosystems. Arctic summer sea ice cover is declining (33, 34), which is affecting lower trophic levels through increased pri- mary productivity, changes in plankton community structure, and altered benthic–pelagic coupling (35–37). Sea ice loss also affects ice-dependent upper trophic-level species, such as ringed seals (Phoca hispida), bearded seals (Erignathus barbatus), and polar bears (Ursus maritimus), that use the ice as a platform to for- age and breed (38–43). In addition, summer sea ice historically served as a barrier to many open water species. Ice degradation now allows a number of marine mammal species, with limited or no historical presence in the Arctic, regular summer access (44, 45). In the ECA, killer whales were historically limited to Fig. 1. Map of all tracking data after sSSM fitting. Numbers indicate day more open segments and blocked from large areas, including all of killer whale tag deployment (the first point of every fifth day is num- of Hudson Bay. Now, in areas killer whales had historical sum- bered to indicate days since deployment). Red and blue colors indicate sSSM- mer presence, such as in Davis Strait and Lancaster Sound (46), inferred behavior for narwhal—all seven narwhal tracks are plotted using they arrive earlier, leave later, and are more numerous (47, 48), the red/blue color code for behavioral state. Killer whale and narwhal tag- whereas in regions of no historical presence, such as Hudson ging locations are indicated by yellow and cyan circles, respectively. Inferred Bay, they are observed annually (47). Thus, Arctic warming may behavior is not shown for the tracked killer whale, which is plotted in green. bring
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