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      Whiskers as hydrodynamic prey sensors in foraging seals

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          Unlike humans, most mammals have mobile facial whiskers, yet their natural movement and function are unknown due to observational difficulties, even in well-studied terrestrial whisker specialists (rodents). We report a remarkable case of whiskers contributing to mammal foraging in an extreme underwater environment: the deep, dark ocean. Our animal-borne video cameras revealed that elephant seals captured moving prey by sensing water movement. Their whiskers extended forward ahead of the mouth. Seals performed rhythmic whisker movement to search for hydrodynamic cues, a whisker movement homologous to terrestrial mammals exploring their environment. Based on direct observations, we show how deep-diving seals locate their prey without the biosonar used by whales, revealing another mammalian adaptation to complete darkness.

          Abstract

          The darkness of the deep ocean limits the vision of diving predators, except when prey emit bioluminescence. It is hypothesized that deep-diving seals rely on highly developed whiskers to locate their prey. However, if and how seals use their whiskers while foraging in natural conditions remains unknown. We used animal-borne tags to show that free-ranging elephant seals use their whiskers for hydrodynamic prey sensing. Small, cheek-mounted video loggers documented seals actively protracting their whiskers in front of their mouths with rhythmic whisker movement, like terrestrial mammals exploring their environment. Seals focused their sensing effort at deep foraging depths, performing prolonged whisker protraction to detect, pursue, and capture prey. Feeding-event recorders with light sensors demonstrated that bioluminescence contributed to only about 20% of overall foraging success, confirming that whiskers play the primary role in sensing prey. Accordingly, visual prey detection complemented and enhanced prey capture. The whiskers’ role highlights an evolutionary alternative to echolocation for adapting to the extreme dark of the deep ocean environment, revealing how sensory abilities shape foraging niche segregation in deep-diving mammals. Mammals typically have mobile facial whiskers, and our study reveals the significant function of whiskers in the natural foraging behavior of a marine predator. We demonstrate the importance of field-based sensory studies incorporating multimodality to better understand how multiple sensory systems are complementary in shaping the foraging success of predators.

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          Most cited references54

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          Hunting behavior of a marine mammal beneath the antarctic fast Ice

          The hunting behavior of a marine mammal was studied beneath the Antarctic fast ice with an animal-borne video system and data recorder. Weddell seals stalked large Antarctic cod and the smaller subice fish Pagothenia borchgrevinki, often with the under-ice surface for backlighting, which implies that vision is important for hunting. They approached to within centimeters of cod without startling the fish. Seals flushed P. borchgrevinki by blowing air into subice crevices or pursued them into the platelet ice. These observations highlight the broad range of insights that are possible with simultaneous recordings of video, audio, three-dimensional dive paths, and locomotor effort.
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            Foraging Behavior and Success of a Mesopelagic Predator in the Northeast Pacific Ocean: Insights from a Data-Rich Species, the Northern Elephant Seal

            The mesopelagic zone of the northeast Pacific Ocean is an important foraging habitat for many predators, yet few studies have addressed the factors driving basin-scale predator distributions or inter-annual variability in foraging and breeding success. Understanding these processes is critical to reveal how conditions at sea cascade to population-level effects. To begin addressing these challenging questions, we collected diving, tracking, foraging success, and natality data for 297 adult female northern elephant seal migrations from 2004 to 2010. During the longer post-molting migration, individual energy gain rates were significant predictors of pregnancy. At sea, seals focused their foraging effort along a narrow band corresponding to the boundary between the sub-arctic and sub-tropical gyres. In contrast to shallow-diving predators, elephant seals target the gyre-gyre boundary throughout the year rather than follow the southward winter migration of surface features, such as the Transition Zone Chlorophyll Front. We also assessed the impact of added transit costs by studying seals at a colony near the southern extent of the species’ range, 1,150 km to the south. A much larger proportion of seals foraged locally, implying plasticity in foraging strategies and possibly prey type. While these findings are derived from a single species, the results may provide insight to the foraging patterns of many other meso-pelagic predators in the northeast Pacific Ocean.
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              Spatial organization of the extracellular matrix regulates cell-cell junction positioning.

              The organization of cells into epithelium depends on cell interaction with both the extracellular matrix (ECM) and adjacent cells. The role of cell-cell adhesion in the regulation of epithelial topology is well-described. ECM is better known to promote cell migration and provide a structural scaffold for cell anchoring, but its contribution to multicellular morphogenesis is less well-understood. We developed a minimal model system to investigate how ECM affects the spatial organization of intercellular junctions. Fibronectin micropatterns were used to constrain the location of cell-ECM adhesion. We found that ECM affects the degree of stability of intercellular junction positioning and the magnitude of intra- and intercellular forces. Intercellular junctions were permanently displaced, and experienced large perpendicular tensional forces as long as they were positioned close to ECM. They remained stable solely in regions deprived of ECM, where they were submitted to lower tensional forces. The heterogeneity of the spatial organization of ECM induced anisotropic distribution of mechanical constraints in cells, which seemed to adapt their position to minimize both intra- and intercellular forces. These results uncover a morphogenetic role for ECM in the mechanical regulation of cells and intercellular junction positioning.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                pnas
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                13 June 2022
                21 June 2022
                13 June 2022
                : 119
                : 25
                : e2119502119
                Affiliations
                [1] aNational Institute of Polar Research , Tokyo 190-8518, Japan;
                [2] bDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo , Tokyo 113-0032, Japan;
                [3] cSchool of Biology, University of St Andrews , Fife KY16 9SY, United Kingdom;
                [4] dDepartment of Ecology and Evolutionary Biology, University of California , Santa Cruz, CA 95060;
                [5] eInstitute of Marine Sciences, University of California , Santa Cruz, CA 95060;
                [6] fCentre for Ecology and Conservation, University of Exeter , Penryn TR10 9FE, United Kingdom;
                [7] gDepartment of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo , Chiba 277-0882, Japan;
                [8] hDepartment of Polar Science, The Graduate University for Advanced Studies , Tokyo 190-8518, Japan
                Author notes
                1To whom correspondence may be addressed. Email: tadachi@ 123456ucsc.edu .

                Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC; received October 26, 2021; accepted April 18, 2022

                Author contributions: T.A., Y.N., and A.T. designed research; T.A., Y.N., P.W.R., D.P.C., L.A.H., R.R.H., W.I., and A.T. performed research; T.A., Y.N., and A.T. contributed new analytic tools; T.A. analyzed data; and T.A., Y.N., P.W.R., D.P.C., L.A.H., R.R.H., W.I., and A.T. wrote the paper.

                Author information
                https://orcid.org/0000-0002-0233-5782
                https://orcid.org/0000-0002-8668-3839
                https://orcid.org/0000-0002-9868-0408
                Article
                202119502
                10.1073/pnas.2119502119
                9231483
                35696561
                e66099e8-b674-4bae-8b6c-99449866e64f
                Copyright © 2022 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                : 18 April 2022
                Page count
                Pages: 7
                Funding
                Funded by: MEXT | Japan Society for the Promotion of Science (JSPS) 501100001691
                Award ID: 12J04316
                Award ID: 15H06824
                Award ID: 16J02935
                Award Recipient : Taiki Adachi Award Recipient : Akinori Takahashi
                Funded by: MEXT | Japan Society for the Promotion of Science (JSPS) 501100001691
                Award ID: 23255001
                Award ID: 15K14793
                Award ID: 20H00650
                Award Recipient : Taiki Adachi Award Recipient : Akinori Takahashi
                Funded by: DOD | USN | Office of Naval Research (ONR) 100000006
                Award ID: N00014-10-1-0356
                Award ID: N00014-13-1-0134
                Award Recipient : Daniel P. Costa
                Categories
                video, Video
                research-article, Research Article
                eco, Ecology
                414
                Biological Sciences
                Ecology

                deep ocean,mammal,sensory system,whisker,bio-logging
                deep ocean, mammal, sensory system, whisker, bio-logging

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