{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T15:37:31Z","timestamp":1788968251278,"version":"build-2803163510"},"reference-count":46,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2021,11,24]],"date-time":"2021-11-24T00:00:00Z","timestamp":1637712000000},"content-version":"vor","delay-in-days":327,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["PRFB1907211"],"award-info":[{"award-number":["PRFB1907211"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["PRFB1907156"],"award-info":[{"award-number":["PRFB1907156"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["IOS-2128033"],"award-info":[{"award-number":["IOS-2128033"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["EF-2128033"],"award-info":[{"award-number":["EF-2128033"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000006","name":"Office of Naval Research","doi-asserted-by":"publisher","award":["N00014-14-1-0533"],"award-info":[{"award-number":["N00014-14-1-0533"]}],"id":[{"id":"10.13039\/100000006","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000006","name":"Office of Naval Research","doi-asserted-by":"publisher","award":["N00014-09-1-0352"],"award-info":[{"award-number":["N00014-09-1-0352"]}],"id":[{"id":"10.13039\/100000006","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010952","name":"Museum of Comparative Zoology, Harvard University","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100010952","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,12,22]]},"abstract":"<jats:title>Synopsis<\/jats:title>\n               <jats:p>Shark skin is covered in dermal denticles\u2014tooth-like structures consisting of enameloid, dentine, and a central pulp cavity. Previous studies have demonstrated differences in denticle morphology both among species and across different body regions within a species, including one report of extreme morphological variation within a 1 cm distance on the skin covering the branchial pouches, a region termed \u201cinterbranchial skin.\u201d We used gel-based profilometry, histology, and scanning electron microscopy to quantify differences in denticle morphology and surface topography of interbranchial skin denticles among 13 species of sharks to better understand the surface structure of this region. We show that (1) interbranchial skin denticles differ across shark species, and (2) denticles on the leading edge of the skin covering each gill pouch have different morphology and surface topography compared with denticles on the trailing edge. Across all species studied, there were significant differences in denticle length (P = 0.01) and width (P = 0.002), with shorter and wider leading edge denticles compared with trailing edge denticles. Surface skew was also higher in leading edge denticles (P = 0.009), though most values were still negative, indicating a surface texture more dominated by valleys than peaks. Overall, leading edge denticles were smoother-edged than trailing edge denticles in all of the species studied. These data suggest two hypotheses: (1) smoother-edged leading edge denticles protect the previous gill flap from abrasion during respiration, and (2) ridged denticle morphology at the trailing edge might alter water turbulence exiting branchial pouches after passing over the gills. Future studies will focus on determining the relationship between denticle morphology and water flow by visualizing fluid motion over interbranchial denticles during in vivo respiration.<\/jats:p>","DOI":"10.1093\/iob\/obab034","type":"journal-article","created":{"date-parts":[[2021,12,1]],"date-time":"2021-12-01T05:05:54Z","timestamp":1638335154000},"source":"Crossref","is-referenced-by-count":42,"title":["Dermal Denticle Diversity in Sharks: Novel Patterns on the Interbranchial Skin"],"prefix":"10.1093","volume":"3","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9293-2088","authenticated-orcid":false,"given":"Molly K","family":"Gabler-Smith","sequence":"first","affiliation":[{"name":"Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138 USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4964-5048","authenticated-orcid":false,"given":"Dylan K","family":"Wainwright","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology, Yale University, 165 Prospect Street, New Haven, CT, 06511 USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Greta A","family":"Wong","sequence":"additional","affiliation":[{"name":"Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138 USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0731-286X","authenticated-orcid":false,"given":"George V","family":"Lauder","sequence":"additional","affiliation":[{"name":"Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138 USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,12,22]]},"reference":[{"key":"2021122217022283500_bib1","doi-asserted-by":"crossref","first-page":"1132","DOI":"10.1002\/jmor.20836","article-title":"Diversity of dermal denticle structure in sharks: skin surface roughness and three-dimensional morphology","volume":"279","author":"Ankhelyi","year":"2018","journal-title":"J Morphol"},{"key":"2021122217022283500_bib2","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1080\/10236244.2011.569991","article-title":"A video and photographic study of aggregation, swimming and respiratory behaviour changes in the grey nurse shark (Carcharias taurus) in response to the presence of SCUBA divers","volume":"44","author":"Barker","year":"2011","journal-title":"Mar Fresh Behav Physiol"},{"key":"2021122217022283500_bib4","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1007\/s003480050400","article-title":"Experiments with three-dimensional riblets as an idealized model of shark skin","volume":"28","author":"Bechert","year":"2000","journal-title":"Exp Fluids"},{"key":"2021122217022283500_bib3","first-page":"457","volume-title":"Drag reduction with riblets in nature and engineering","author":"Bechert","year":"2007"},{"key":"2021122217022283500_bib6","first-page":"98","article-title":"Lancelets, cyclostomes, sharks","volume-title":"Fishes of the western North Atlantic, Part 1","author":"Bigelow","year":"1948"},{"key":"2021122217022283500_bib5","first-page":"1","article-title":"Mechanics of respiratory pumps","volume-title":"Fish biomechanics","author":"Brainerd","year":"2006"},{"key":"2021122217022283500_bib7","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1006\/jtbi.2001.2325","article-title":"Computational fluid dynamics in the oral cavity of ram suspension-feeding fishes","volume":"210","author":"Cheer","year":"2001","journal-title":"J Theor Biol"},{"key":"2021122217022283500_bib8","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1111\/jfb.12705","article-title":"Biological characterization of the skin of shortfin mako shark Isurus oxyrinchus and preliminary study of the hydrodynamic behaviour through computational fluid dynamics","volume":"87","author":"D\u00edez","year":"2015","journal-title":"J Fish Biol"},{"key":"2021122217022283500_bib9","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3099\/MCZ2.1","article-title":"Evolutionary and ecological relationships of gill slit morphology in extant sharks","volume":"161","author":"Dolce","year":"2013","journal-title":"Bull Mus Comp Zool"},{"key":"2021122217022283500_bib10","doi-asserted-by":"crossref","first-page":"20170828","DOI":"10.1098\/rsif.2017.0828","article-title":"Shark skin-inspired designs that improve aerodynamic performance","volume":"15","author":"Domel","year":"2018","journal-title":"J R Soc Interface"},{"key":"2021122217022283500_bib11","volume-title":"Fundamentals of dimensional metrology","author":"Dotson","year":"2015"},{"key":"2021122217022283500_bib11a","doi-asserted-by":"crossref","first-page":"20180473","DOI":"10.1098\/rsif.2018.0473","article-title":"Passive bristling of mako shark scales in reversing flows","volume":"15","author":"Du Clos","year":"2018","journal-title":"J R Soc Interface"},{"key":"2021122217022283500_bib12","doi-asserted-by":"crossref","first-page":"1501","DOI":"10.1242\/jeb.202.11.1501","article-title":"Mechanics of ventilation in swellsharks, Cephaloscyllium ventriosum (Scyliorhinidae)","volume":"202","author":"Ferry-Graham","year":"1999","journal-title":"J Exp Biol"},{"key":"2021122217022283500_bib13","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1242\/jeb.151.1.175","article-title":"Aspects of shark swimming performance determined using a large water tunnel","volume":"151","author":"Graham","year":"1990","journal-title":"J Exp Biol"},{"key":"2021122217022283500_bib14","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1002\/bimj.200810425","article-title":"Simultaneous inference in general parametric models","volume":"50","author":"Hothorn","year":"2008","journal-title":"Biom J"},{"key":"2021122217022283500_bib15","author":"ISO 25178-2","year":"2012"},{"key":"2021122217022283500_bib16","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1007\/978-1-4614-3997-4_9","article-title":"Shark skin boundary layer control","volume-title":"Natural locomotion in fluids and on surfaces","author":"Lang","year":"2012"},{"key":"2021122217022283500_bib17","doi-asserted-by":"crossref","first-page":"060502","DOI":"10.1103\/PhysRevFluids.1.060502","article-title":"Structure, biomimetics, and fluid dynamics of fish skin surfaces","volume":"1","author":"Lauder","year":"2016","journal-title":"Phys Rev Fluids"},{"key":"2021122217022283500_bib18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v069.i01","article-title":"Least-squares means: the R package lsmeans","volume":"69","author":"Lenth","year":"2016","journal-title":"J Stat Softw"},{"key":"2021122217022283500_bib19","first-page":"93","article-title":"Muscular system. Gross anatomy and functional morphology of muscles","volume-title":"Sharks, skates, and rays: the biology of elasmobranch fishes","author":"Liem","year":"1999"},{"key":"2021122217022283500_bib20","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1002\/jmor.20047","article-title":"Scale morphology ad flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus","volume":"273","author":"Motta","year":"2012","journal-title":"J Morphol"},{"key":"2021122217022283500_bib21","volume-title":"Pharyngeal denticles (placoid scales) of sharks, with notes on the dermal skeleton of vertebrates","author":"Nelson","year":"1970"},{"key":"2021122217022283500_bib22","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1242\/jeb.063040","article-title":"The hydrodynamic function of shark skin and two biomimetic applications","volume":"215","author":"Oeffner","year":"2012","journal-title":"J Exp Biol"},{"key":"2021122217022283500_bib23","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1002\/ar.22850","article-title":"Comparison of the structure and composition of the branchial filters in suspension feeding elasmobranchs","volume":"297","author":"Paig-Tran","year":"2014","journal-title":"Anat Rec"},{"key":"2021122217022283500_bib24","article-title":"nlme: linear and nonlinear mixed effects models","author":"Pinheiro","year":"2020"},{"key":"2021122217022283500_bib26","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1002\/jmor.21222","article-title":"The denticle surface of thresher shark tails: three-dimensional structure and comparison to other pelagic species","volume":"281","author":"Popp","year":"2020","journal-title":"J Morphol"},{"key":"2021122217022283500_bib25","first-page":"157","article-title":"A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum","volume-title":"Environ Biol Fishes","author":"Pratt","year":"2001"},{"key":"2021122217022283500_bib28","volume-title":"Engineering metrology and measurements","author":"Raghavendra","year":"2013"},{"key":"2021122217022283500_bib29","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1071\/MF9920123","article-title":"Functional aspects of placoid scales: a review and update","volume":"43","author":"Raschi","year":"1992","journal-title":"Mar Freshw Res"},{"key":"2021122217022283500_bib27","volume-title":"R: a language and environment for statistical computing","author":"R Core Team","year":"2020"},{"key":"2021122217022283500_bib30","first-page":"483","article-title":"Morphology and hydrodynamic effects of the scales of fast swimming sharks","volume":"30","author":"Reif","year":"1985","journal-title":"Fortschr Zool"},{"key":"2021122217022283500_bib31","first-page":"1","author":"Reif","year":"1985","journal-title":"Squamation and ecology of sharks"},{"key":"2021122217022283500_bib32","doi-asserted-by":"crossref","first-page":"85","DOI":"10.2307\/1540652","article-title":"Active branchial and ram gill ventilation in fishes","volume":"148","author":"Roberts","year":"1975","journal-title":"Biol Bull"},{"key":"2021122217022283500_bib33","volume-title":"A physical introduction to fluid mechanics","author":"Smits","year":"2000"},{"key":"2021122217022283500_bib34","doi-asserted-by":"crossref","first-page":"S47","DOI":"10.1098\/rsbl.2003.0006","article-title":"Shark skin: function in feeding","volume":"270","author":"Southall","year":"2003","journal-title":"Proc R Soc Lond B Biol Sci"},{"key":"2021122217022283500_bib35","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1093\/icb\/17.2.343","article-title":"Body form and locomotion in sharks","volume":"17","author":"Thomson","year":"1977","journal-title":"Am Zool"},{"key":"2021122217022283500_bib36","doi-asserted-by":"crossref","first-page":"e0235342","DOI":"10.1371\/journal.pone.0235342","article-title":"Armored eyes of the whale shark","volume":"15","author":"Tomita","year":"2020","journal-title":"PLoS One"},{"key":"2021122217022283500_bib37","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1643\/CI-17-683","article-title":"Captive birth of tiger shark (Galeocerdo cuvier) reveals a shift in respiratory mode during parturition","volume":"106","author":"Tomita","year":"2018","journal-title":"Copeia"},{"key":"2021122217022283500_bib38","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1007\/BF00392492","article-title":"Mating in the reef white-tip shark Triaenodon obesus","volume":"84","author":"Tricas","year":"1985","journal-title":"Mar Biol"},{"key":"2021122217022283500_bib39","first-page":"20190103","article-title":"How smooth is a dolphin? The ridged skin of odontocetes","volume-title":"Biol Lett","author":"Wainwright","year":"2019"},{"key":"2021122217022283500_bib40","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1007\/978-3-319-74144-4_10","article-title":"Mucus matters: the slippery and complex surfaces of fish","volume-title":"Functional surfaces in biology III.","author":"Wainwright","year":"2017"},{"key":"2021122217022283500_bib41","doi-asserted-by":"crossref","first-page":"1626","DOI":"10.1111\/2041-210X.12778","article-title":"Imaging biological surface topography in situ and in vivo","volume":"8","author":"Wainwright","year":"2017","journal-title":"Methods Ecol Evol"},{"key":"2021122217022283500_bib42","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1242\/jeb.060095","article-title":"Oxygen utilization and the branchial pressure gradient during ram ventilation of the shortfin mako, Isurus oxyrinchus: is lamnid shark\u2013tuna convergence constrained by elasmobranch gill morphology?","volume":"215","author":"Wegner","year":"2012","journal-title":"J Exp Biol"},{"key":"2021122217022283500_bib43","doi-asserted-by":"crossref","first-page":"1656","DOI":"10.1242\/jeb.097097","article-title":"Biomimetic shark skin: design, fabrication and hydrodynamic function","volume":"217","author":"Wen","year":"2014","journal-title":"J Exp Biol"},{"key":"2021122217022283500_bib44","doi-asserted-by":"crossref","first-page":"066010","DOI":"10.1088\/1748-3190\/10\/6\/066010","article-title":"Hydrodynamic function of biomimetic shark skin: effect of denticle pattern and spacing","volume":"10","author":"Wen","year":"2015","journal-title":"Bioinspir Biomim"},{"key":"2021122217022283500_bib45","first-page":"191","article-title":"Kurtosis as peakedness, 1905\u20132014. R.I.P.","volume-title":"Am Stat","author":"Westfall","year":"2014"}],"container-title":["Integrative Organismal Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/iob\/advance-article-pdf\/doi\/10.1093\/iob\/obab034\/41281352\/obab034.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/iob\/article-pdf\/3\/1\/obab034\/41890292\/obab034.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/iob\/article-pdf\/3\/1\/obab034\/41890292\/obab034.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,12,22]],"date-time":"2021-12-22T19:48:17Z","timestamp":1640202497000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/iob\/article\/doi\/10.1093\/iob\/obab034\/6438440"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021]]},"references-count":46,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12,22]]}},"URL":"https:\/\/doi.org\/10.1093\/iob\/obab034","relation":{},"ISSN":["2517-4843"],"issn-type":[{"value":"2517-4843","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021]]},"published":{"date-parts":[[2021]]},"article-number":"obab034"}}