Fear dynamically structures the ocean’s pelagic zone

Abstract

Fear of predation can have wide-ranging ecological effects.1Brown J.S. Laundré J.W. Gurung M. The ecology of fear: optimal foraging, game theory, and trophic interactions.J. Mammal. 1999; 80: 385-399Crossref Scopus (763) Google Scholar, 2Creel S. Christianson D. Relationships between direct predation and risk effects.Trends Ecol. Evol. 2008; 23: 194-201Abstract Full Text Full Text PDF PubMed Scopus (671) Google Scholar, 3Laundré J.W. Hernández L. Ripple W.J. The landscape of fear: ecological implications of being afraid.Open Ecol. J. 2010; 3: 1-7Crossref Scopus (409) Google Scholar, 4Ripple W.J. Beschta R.L. Wolves and the ecology of fear: can predation risk structure ecosystems?.Bioscience. 2004; 54: 755-766Crossref Scopus (464) Google Scholar This is especially true in the ocean’s pelagic zone, the Earth’s largest habitat, where vertical gradients in light and primary productivity force numerous taxa to migrate vertically each night to feed at the surface while minimizing risk from visual predators.5Longhurst A.R. Vertical migration.in: Cushing E.D. Walsh J.J. The Ecology of the Seas. W.B. Saunders Company, 1976: 116-137Google Scholar, 6Aksnes D.L. Utne A.C.W. A revised model of visual range in fish.Sarsia. 1997; 82: 137-147Crossref Scopus (154) Google Scholar, 7Hays G.C. A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations.Hydrobiologia. 2003; 503: 163-170Crossref Scopus (509) Google Scholar Despite its importance and the fact that it is driven by spatial differences in perceived risk,8Gaynor K.M. Brown J.S. Middleton A.D. Power M.E. Brashares J.S. Landscapes of fear: spatial patterns of risk perception and response.Trends Ecol. Evol. 2019; 34: 355-368Abstract Full Text Full Text PDF PubMed Scopus (162) Google Scholar diel vertical migration (DVM) is rarely considered within the “landscape of fear”3Laundré J.W. Hernández L. Ripple W.J. The landscape of fear: ecological implications of being afraid.Open Ecol. J. 2010; 3: 1-7Crossref Scopus (409) Google Scholar,8Gaynor K.M. Brown J.S. Middleton A.D. Power M.E. Brashares J.S. Landscapes of fear: spatial patterns of risk perception and response.Trends Ecol. Evol. 2019; 34: 355-368Abstract Full Text Full Text PDF PubMed Scopus (162) Google Scholar,9Bleicher S.S. The landscape of fear conceptual framework: definition and review of current applications and misuses.PeerJ. 2017; 5: e3772Crossref PubMed Scopus (61) Google Scholar framework.10Beltran R.S. Kendall-Bar J.M. Pirotta E. Adachi T. Naito Y. Takahashi A. Cremers J. Robinson P.W. Crocker D.E. Costa D.P. Lightscapes of fear: how mesopredators balance starvation and predation in the open ocean.Sci. Adv. 2021; 7: eabd9818Crossref PubMed Scopus (14) Google Scholar It is also far from the only such process in the pelagic zone. We used continuous, year-long records from an upward-looking echosounder and broadband hydrophone at a cabled observatory off Central California, USA, to observe avoidance reactions by several groups of pelagic animals to the presence of their predators. As expected, vertical migration was ubiquitous, but we also observed behaviors at shorter and longer timescales that were best explained by fear of predation. The presence of foraging odontocetes induced immediate diving behavior in mesopelagic sound-scattering layers, and schools of epipelagic fishes induced similar reaction in layers of zooplankton and mesopelagic micronekton. At longer timescales, the presence of fish schools significantly deepened vertical migration, rearranging life throughout the water column. We argue that behavioral reactions to predation risk are common in the pelagic zone at a range of spatiotemporal scales and that our understanding of food webs and biogeochemical cycling in this immense biome will be incomplete unless we account for fear.

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