{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T14:05:29Z","timestamp":1753884329737,"version":"3.41.2"},"reference-count":93,"publisher":"The Company of Biologists","license":[{"start":{"date-parts":[[2018,1,1]],"date-time":"2018-01-01T00:00:00Z","timestamp":1514764800000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["OCE-1356966"],"award-info":[{"award-number":["OCE-1356966"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>In coastal ecosystems, attributes of fluid motion can prompt animal larvae to rise or sink in the water column and to select microhabitats within which they attach and commit to a benthic existence. In Echinoid (sea urchin and sand dollar) larvae living along wave-exposed shorelines, intense turbulence characteristic of surf zones can cause individuals to undergo an abrupt life-history shift characterized by precocious entry into competence: the stage at which larvae will settle and complete metamorphosis in response to local cues. However, the mechanistic details of this turbulence-triggered onset of competence remain poorly defined. Here, we evaluate in a series of laboratory experiments the time course of this turbulence effect, both the rapidity with which it initiates, and how long it perdures. We find that larvae become competent with turbulence exposures as brief as 30 sec, with longer exposures inducing a greater proportion of larvae to become competent. Intriguingly, larvae can remember such exposures for a protracted period (at least 24 hrs), a pattern reminiscent of long-term potentiation. Turbulence also induces short-term behavioral responses that last less than 30 mins, including cessation of swimming, that facilitate sinking and thus contact of echinoid larvae with the substrate. Together these results yield a novel perspective on how larvae find their way to suitable adult habitat at the critical settlement transition, and also open new experimental opportunities to elucidate the mechanisms by which planktonic animals respond to fluid motion.<\/jats:p>","DOI":"10.1242\/jeb.187351","type":"journal-article","created":{"date-parts":[[2018,12,20]],"date-time":"2018-12-20T14:04:41Z","timestamp":1545314681000},"source":"Crossref","is-referenced-by-count":3,"title":["Brief exposure to intense turbulence induces a sustained life-history shift in echinoids"],"prefix":"10.1242","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4862-9663","authenticated-orcid":false,"given":"Mathew C.","family":"Ferner","sequence":"first","affiliation":[{"name":"San Francisco Bay National Estuarine Research Reserve and Estuary & Ocean Science Center, San Francisco State University, Tiburon, CA 94920, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jason","family":"Hodin","sequence":"additional","affiliation":[{"name":"Friday Harbor Laboratories, University of Washington, Friday Harbor, WA 98250, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gabriel","family":"Ng","sequence":"additional","affiliation":[{"name":"Bodega Marine Laboratory and Department of Evolution and Ecology, University of California at Davis, Bodega Bay, CA 94923, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Brian","family":"Gaylord","sequence":"additional","affiliation":[{"name":"Bodega Marine Laboratory and Department of Evolution and Ecology, University of California at Davis, Bodega Bay, CA 94923, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","published-online":{"date-parts":[[2018,1,1]]},"reference":[{"key":"2021042513393247900_JEB187351C1","doi-asserted-by":"crossref","first-page":"121","DOI":"10.2307\/4134601","article-title":"Role of protein kinase C, G-protein coupled receptors, and calcium flux during metamorphosis of the sea urchin Strongylocentrotus purpuratus","volume":"210","author":"Amador-Cano","year":"2006","journal-title":"Biol. Bull."},{"key":"2021042513393247900_JEB187351C2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v067.i01","article-title":"Fitting linear mixed-effects models using lme4","volume":"67","author":"Bates","year":"2015","journal-title":"J. Statist. Softw."},{"key":"2021042513393247900_JEB187351C3","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1093\/icb\/icl004","article-title":"What is metamorphosis?","volume":"46","author":"Bishop","year":"2006","journal-title":"Integr. Comp. Biol."},{"key":"2021042513393247900_JEB187351C4","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1111\/j.1440-169X.1989.00589.x","article-title":"The control of sea urchin metamorphosis: ionic effects","volume":"31","author":"Cameron","year":"1989","journal-title":"Dev. Growth Differ."},{"key":"2021042513393247900_JEB187351C5","doi-asserted-by":"crossref","first-page":"157","DOI":"10.7773\/cm.v28i2.217","article-title":"Induction of metamorphosis with KCl in three species of sea urchins and its implications in the production of juveniles","volume":"28","author":"Carpizo-Ituarte","year":"2002","journal-title":"Cienc. Mar."},{"key":"2021042513393247900_JEB187351C6","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1093\/icb\/ics092","article-title":"Biomechanics of larval morphology affect swimming: Insights from the sand dollar Dendraster excentricus: Integr","volume":"52","author":"Chan","year":"2012","journal-title":"Comp. Biol."},{"key":"2021042513393247900_JEB187351C7","first-page":"283","article-title":"Perspectives: Settlement and metamorphosis of marine invertebrate larvae","volume-title":"Settlement and Metamorphosis of Marine Invertebrate Larvae","author":"Chia","year":"1978"},{"key":"2021042513393247900_JEB187351C8","first-page":"219","article-title":"Echinoderm metamorphosis: fate of larval structures","volume-title":"Settlement and Metamorphosis of Marine Invertebrate Larvae","author":"Chia","year":"1978"},{"key":"2021042513393247900_JEB187351C9","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/BF00235145","article-title":"Fine structural study of the statocysts in the veliger larva of the nudibranch, Rostanga pulchra","volume":"214","author":"Chia","year":"1981","journal-title":"Cell Tissue Res."},{"key":"2021042513393247900_JEB187351C10","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1038\/nrn2149","article-title":"TRP channels in mechanosensation: direct or indirect activation?","volume":"8","author":"Christensen","year":"2007","journal-title":"Nat. Rev. Neurosci."},{"key":"2021042513393247900_JEB187351C11","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1242\/jeb.037200","article-title":"Morphology\u2013flow interactions lead to stage-selective vertical transport of larval sand dollars in shear flow","volume":"213","author":"Clay","year":"2010","journal-title":"J. Exp. Biol."},{"key":"2021042513393247900_JEB187351C12","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1016\/j.jocn.2010.04.020","article-title":"Sodium selenate specifically activates PP2A phosphatase, dephosphorylates tau and reverses memory deficits in an Alzheimer's disease model","volume":"17","author":"Corcoran","year":"2010","journal-title":"J. Clin. 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Fluid Mech."},{"key":"2021042513393247900_JEB187351C38","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1146\/annurev-marine-120709-142753","article-title":"Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites","volume":"3","author":"Hadfield","year":"2011","journal-title":"Ann. Rev. Mar. Sci."},{"key":"2021042513393247900_JEB187351C39","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1201\/9781420036602.ch13","article-title":"Natural chemical cues for settlement and metamorphosis of marine-invertebrate larvae","volume-title":"Marine Chemical Ecology","author":"Hadfield","year":"2001"},{"key":"2021042513393247900_JEB187351C40","doi-asserted-by":"crossref","first-page":"3801","DOI":"10.1242\/jeb.059618","article-title":"Developmentally regulated multisensory integration for prey localization in the medicinal leech","volume":"214","author":"Harley","year":"2011","journal-title":"J. Exp. Biol."},{"key":"2021042513393247900_JEB187351C41","doi-asserted-by":"crossref","first-page":"174","DOI":"10.2307\/4134556","article-title":"Molecular mechanisms of memory storage in Aplysia","volume":"210","author":"Hawkins","year":"2006","journal-title":"Biol. Bull."},{"key":"2021042513393247900_JEB187351C42","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1007\/s11022-004-5592-y","article-title":"Sterile polystyrene culture dishes induce transformation of polyps into medusae in Aurelia aurita (Scyphozoa, Cnidaria)","volume":"25","author":"Herrmann","year":"2003","journal-title":"Methods Cell Sci."},{"key":"2021042513393247900_JEB187351C43","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1186\/1471-213X-14-22","article-title":"A detailed staging scheme for late larval development in Strongylocentrotus purpuratus focused on readily-visible juvenile structures within the rudiment","volume":"14","author":"Heyland","year":"2014","journal-title":"BMC Dev. Biol."},{"key":"2021042513393247900_JEB187351C44","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1093\/icb\/icl038","article-title":"Expanding networks: signaling components in and a hypothesis for the evolution of metamorphosis","volume":"46","author":"Hodin","year":"2006","journal-title":"Integr. Comp. Biol."},{"key":"2021042513393247900_JEB187351C45","doi-asserted-by":"crossref","first-page":"150114","DOI":"10.1098\/rsos.150114","article-title":"Rethinking competence in marine life cycles: ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence","volume":"2","author":"Hodin","year":"2015","journal-title":"R. Soc. Open Sci."},{"key":"2021042513393247900_JEB187351C46","first-page":"190","article-title":"I feel that! Fluid dynamics and sensory aspects of larval settlement across scales","volume-title":"Evolutionary Ecology of Marine Invertebrate Larvae","author":"Hodin","year":"2018"},{"key":"2021042513393247900_JEB187351C47","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1186\/s40850-018-0034-5","article-title":"Turbulence exposure recapitulates desperate behavior in late-stage sand dollar larvae","volume":"3","author":"Hodin","year":"2018","journal-title":"BMC Zool."},{"key":"2021042513393247900_JEB187351C48","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1086\/699827","article-title":"Sand dollar larvae show within-population variation in their settlement induction by turbulence","volume":"235","author":"Hodin","year":"2018","journal-title":"Biol. Bull"},{"key":"2021042513393247900_JEB187351C49","doi-asserted-by":"crossref","first-page":"243","DOI":"10.3354\/meps10542","article-title":"Orientation from open water to settlement habitats by coral reef fish: Behavioral flexibility in the use of multiple reliable cues","volume":"493","author":"Igulu","year":"2013","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"2021042513393247900_JEB187351C50","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1111\/j.1439-0485.2009.00288.x","article-title":"Turbulence-plankton interactions: a new cartoon","volume":"30","author":"Jumars","year":"2009","journal-title":"Mar. Ecol."},{"key":"2021042513393247900_JEB187351C51","first-page":"71","article-title":"Nutrient fluxes to planktonic osmotrophs in the presence of fluid motion","volume":"34","author":"Karp-Boss","year":"1996","journal-title":"Oceanogr. Mar. Biol."},{"key":"2021042513393247900_JEB187351C52","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1007\/BF00380003","article-title":"Recruitment of marine invertebrates: the role of active larval choices and early mortality","volume":"54","author":"Keough","year":"1982","journal-title":"Oecologia"},{"key":"2021042513393247900_JEB187351C53","first-page":"309","article-title":"Sensory environments, larval abilities and local self-recruitment","volume":"70S","author":"Kingsford","year":"2002","journal-title":"Bull. Mar. Sci."},{"key":"2021042513393247900_JEB187351C54","doi-asserted-by":"crossref","first-page":"135","DOI":"10.3354\/meps122135","article-title":"Planktivorous feeding in calm and turbulent environments, with emphasis on copepods","volume":"122","author":"Ki\u00f8rboe","year":"1995","journal-title":"Mar. Ecol. Progr. Ser."},{"key":"2021042513393247900_JEB187351C55","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1080\/08927010701492250","article-title":"Mini review: hydrodynamics of larval settlement into fouling communities","volume":"23","author":"Koehl","year":"2007","journal-title":"Biofouling"},{"key":"2021042513393247900_JEB187351C56","doi-asserted-by":"crossref","first-page":"47","DOI":"10.3354\/meps10193","article-title":"Wind chop and ship wakes determine hydrodynamic stresses on larvae settling on different microhabitats in fouling communities","volume":"479","author":"Koehl","year":"2013","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"2021042513393247900_JEB187351C57","doi-asserted-by":"crossref","first-page":"jeb165696","DOI":"10.1242\/jeb.165696","article-title":"Environmental acoustic cues guide the biosonar attention of a highly specialised echolocator","volume":"221","author":"Lattenkamp","year":"2018","journal-title":"J. Exp. Biol."},{"key":"2021042513393247900_JEB187351C58","doi-asserted-by":"crossref","first-page":"248","DOI":"10.2307\/1938736","article-title":"How distribution and abundance influence fertilization success in the sea urchin Strongylocentrotus franciscanus","volume":"73","author":"Levitan","year":"1992","journal-title":"Ecology"},{"key":"2021042513393247900_JEB187351C59","doi-asserted-by":"crossref","first-page":"1973","DOI":"10.1098\/rstb.2007.2082","article-title":"A review of fish swimming mechanics and behaviour in altered flows","volume":"362","author":"Liao","year":"2007","journal-title":"Phil. Trans. R. Soc. B"},{"key":"2021042513393247900_JEB187351C60","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1152\/physrev.00014.2003","article-title":"Long-term potentiation and memory","volume":"84","author":"Lynch","year":"2004","journal-title":"Physiol. 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Biol."},{"key":"2021042513393247900_JEB187351C63","doi-asserted-by":"crossref","first-page":"46","DOI":"10.2307\/1542066","article-title":"The effects of hydrodynamic shear stress on fertilization and early development of the purple sea urchin Strongylocentrotus purpuratus","volume":"188","author":"Mead","year":"1995","journal-title":"Biol. Bull."},{"key":"2021042513393247900_JEB187351C64","doi-asserted-by":"crossref","first-page":"117","DOI":"10.3354\/meps11914","article-title":"Early metamorphosis is costly and avoided by young, but physiologically competent, marine larvae","volume":"559","author":"Mos","year":"2016","journal-title":"Mar. Ecol. Prog. Ser."},{"key":"2021042513393247900_JEB187351C65","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1007\/BF00355484","article-title":"Larval recruitment in response to manipulated field flows","volume":"116","author":"Mullineaux","year":"1993","journal-title":"Mar. 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