Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates

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Frazier" }, { "@type": "Person", "name": "William B. Driggers III" }, { "@type": "Person", "name": "Glenn F. Ulrich" } ], "publisher": { "@type": "Organization", "name": "F1000Research", "logo": { "@type": "ImageObject", "url": "https://f1000research.com/img/AMP/F1000Research_image.png", "height": 480, "width": 60 } }, "image": { "@type": "ImageObject", "url": "https://f1000research.com/img/AMP/F1000Research_image.png", "height": 1200, "width": 150 }, "description": "Longevity of Rhizoprionodon terraenovae and Carcharhinus acronotus in the western North Atlantic Ocean was examined using direct age estimates from vertebral sections and tag-recapture data. Time-at-liberty ranged from 7.7-14.0 years (mean =10.1) for R. terraenovae and 10.9-12.8 years (mean =11.9) for C. acronotus. Maximum estimated longevity was determined to be 19.8 years through tag-recapture data and 18.5 years from direct age estimates for R. terraenovae and 22.8 years through tag-recapture data and 20.5 years through direct age estimates for C. acronotus. These longevity estimates represent a large increase over previous estimates and may have significant effects on analyses that depend on longevity including lifetime fecundity, mortality rates, demographic analyses and stock assessments." } { "@context": "http://schema.org", "@type": "BreadcrumbList", "itemListElement": [ { "@type": "ListItem", "position": "1", "item": { "@id": "https://f1000research.com/", "name": "Home" } }, { "@type": "ListItem", "position": "2", "item": { "@id": "https://f1000research.com/browse/articles", "name": "Browse" } }, { "@type": "ListItem", "position": "3", "item": { "@id": "https://f1000research.com/articles/3-190/v2", "name": "Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae..." } } ] } Home Browse Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae... ALL Metrics - Views Downloads Get PDF Get XML Cite How to cite this article Frazier BS, Driggers III WB and Ulrich GF. Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.12688/f1000research.4767.2 ) NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article. Close Copy Citation Details Export Export Citation Sciwheel EndNote Ref. Manager Bibtex ProCite Sente EXPORT Select a format first Track Share ▬ ✚ Research Note Revised Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] Bryan S. Frazier 1 , William B. Driggers III 2 , Glenn F. Ulrich 1 Bryan S. Frazier 1 , William B. Driggers III 2 , Glenn F. Ulrich 1 PUBLISHED 27 Jan 2015 Author details Author details 1 South Carolina Department of Natural Resources, Marine Resources Research Institute, Charleston, SC, 29412, USA 2 National Marine Fisheries Service, Southeast Fisheries Science Center, Mississippi Laboratories, Pascagoula, MS, 39567, USA OPEN PEER REVIEW DETAILS REVIEWER STATUS This article is included in the Elasmobranch biology & conservation collection. Abstract Longevity of Rhizoprionodon terraenovae and Carcharhinus acronotus in the western North Atlantic Ocean was examined using direct age estimates from vertebral sections and tag-recapture data. Time-at-liberty ranged from 7.7-14.0 years (mean =10.1) for R. terraenovae and 10.9-12.8 years (mean =11.9) for C. acronotus . Maximum estimated longevity was determined to be 19.8 years through tag-recapture data and 18.5 years from direct age estimates for R. terraenovae and 22.8 years through tag-recapture data and 20.5 years through direct age estimates for C. acronotus . These longevity estimates represent a large increase over previous estimates and may have significant effects on analyses that depend on longevity including lifetime fecundity, mortality rates, demographic analyses and stock assessments. READ ALL READ LESS Keywords Rhizoprionodon, Carcharhinus, shark, longevity Corresponding Author(s) Bryan S. Frazier ( [email protected] ) Close Corresponding author: Bryan S. Frazier Competing interests: No competing interests were disclosed. Grant information: These data were based on a 20 year longline survey and numerous grants have funded the survey over the years. Funding for the longline survey was provided by the Federal Aid in Sport fish Restoration Act, the Southeast Area Monitoring and Assessment Program, the Atlantic States Marine Fisheries Commission, the National Marine Fisheries Federal Assistance Program, and the South Carolina State Recreational Fisheries Advisory Committee. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Copyright: © 2015 Frazier BS et al . This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication). How to cite: Frazier BS, Driggers III WB and Ulrich GF. Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.12688/f1000research.4767.2 ) First published: 12 Aug 2014, 3 :190 ( https://doi.org/10.12688/f1000research.4767.1 ) Latest published: 27 Jan 2015, 3 :190 ( https://doi.org/10.12688/f1000research.4767.2 ) Revised Amendments from Version 1 This research note has been updated to incorporate suggestions by the reviewers. Figures have been added of the oldest aged vertebra section for each species. All mention of Faben's theoretical maximum age have also been removed from the note. An additional Rhizoprionodon terraenovae recapture was encountered and those data were added to the research note (Shark L2881). Also background information about the number of each species tagged and recaptured was added. This research note has been updated to incorporate suggestions by the reviewers. Figures have been added of the oldest aged vertebra section for each species. All mention of Faben's theoretical maximum age have also been removed from the note. An additional Rhizoprionodon terraenovae recapture was encountered and those data were added to the research note (Shark L2881). Also background information about the number of each species tagged and recaptured was added. See the authors' detailed response to the review by Marcus Drymon See the authors' detailed response to the review by Alastair Harry READ REVIEWER RESPONSES Introduction Tag-recapture data grant researchers the opportunity to synthesize a vast array of information for species they are studying. Sharks, in particular, are well suited for tagging studies due to their migratory behavior, longevity, and relatively large size, which allows tagging at all life stages ( Bonham et al. , 1949 ). Valuable information gained from recapture data includes greater understanding of species-specific migratory patterns, stock structure, spatial and temporal distribution, site fidelity/residence times, and life histories ( Kohler & Turner, 2001 ). Among life history parameters needed to best manage populations of fishes, robust longevity estimates are of paramount importance, particularly for iteroparous species, such as sharks. For example, assuming age at maturity, reproductive periodicity, and brood size are constant, the lifetime fecundity of a given species is directly linked to its lifespan. Longevity estimates for sharks are generally derived from von Bertalanffy Growth Function (VBGF) parameter estimates (i.e. growth constant); however, VBGF parameter estimates can be heavily affected by low sample sizes, incomplete sampling among size classes and/or difficulties associated with age estimation of large individuals ( Goldman, 2004 ; Francis et al. , 2007 ). Obtaining accurate longevity estimates can be hampered by the low probability of catching older individuals as they represent a small portion of the entire population, difficulty associated with capturing large specimens that are more capable of escaping gear than smaller conspecifics, and the reduction of older individuals in the population due to fishing pressure ( Bishop et al. , 2006 ). Additionally, age underestimation has been documented in multiple shark species including long-lived species such as the Porbeagle, Lamna nasus (Bonnaterre, 1788) ( Francis et al. , 2007 ) and the Australian School Shark, Galeorhinus galeus (L. 1758) ( Kalish & Johnston, 2001 ), and species with intermediate life histories such as the Bonnethead, Sphyrna tiburo (L. 1758) ( Frazier et al. , 2014 ). Due to the above factors, tag-recapture records, when available, are the most reliable source of longevity data as maximum time-at-liberty for any individual within the population would represent the highest directly known longevity. Based on tag-recapture data and direct age estimates, herein we report on the longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae (Richardson, 1836) and Blacknose Sharks Carcharhinus acronotus (Poey, 1860), both of which are common in the coastal waters off the southeastern United States. Methods Sharks were captured and tagged during survey operations conducted by the South Carolina Department of Natural Resources Adult Red Drum and Coastal Shark Longline Program (SCDNR) (see Ulrich et al. , 2007 for longline protocol). Collection, handling and tagging of specimens was authorized and controlled under the SCDNR scientific permit issued to employees of SCDNR. Upon capture, the fork length (FL) and sex of each shark was recorded. For those sharks deemed to be in good health, a Hallprint © nylon dart tag, labeled with unique identifying numbers, was inserted into the dorsal musculature at the base of the first dorsal fin prior to release. As tagged sharks were at liberty in the wild, recaptured specimens were reported by a number of sources, including recreational anglers, commercial fishermen and SCDNR. Estimated measurements at recapture were obtained from recreational and commercial fishermen and direct measurements were recorded from specimens recaptured by SCDNR. When possible, a sample of 8–10 vertebrae were removed from the cervical region of the vertebral column from recaptured sharks. In the case of recaptured specimens from commercial fishermen, sharks were already deceased and vertebrae were removed. In the case of recaptured specimens from SCDNR, a IACUC protocol approved for graduate students who had previously worked with SCDNR on elasmobranch studies was followed; the vertebral column was severed by serrated knife in two cervical locations. To estimate age at recapture, vertebrae were prepared for analyses following the protocol of Frazier et al. , 2014 . Initial vertebral growth band counts were conducted by three unbiased readers with no knowledge of specimen length or time-at-liberty. If band counts differed among readers, sections were independently re-read until agreement was reached. Age at recapture was estimated under the assumptions: (1) the birthmark was formed prior or shortly after parturition, (2) the second band was formed 6 months later during the first winter, and (3) the third band was formed 1 year later. Therefore, we subtracted 1.5 from each total band count to calculate age in years (e.g. Loefer & Sedberry, 2003 ; Driggers et al. , 2004 ). Age estimates at recapture were also determined by adding time-at-liberty to backtransformed ages at tagging. Species and sex-specific von Bertalanffy growth function parameters from Loefer & Sedberry, 2003 ( R. terraenovae ) and Driggers et al. , 2004 ( C. acronotus ) were used to backtransform age at tagging using the following equation: Age= ( 1n ( 1- L t L ∞ ) -k ) +t o Where: L t = length at age t, L ∞ = theoretical maximum length, k = coefficient of growth, t o = theoretical age at which length equals zero. A paired t-test was used to determine if age estimates from vertebral sections were significantly different than backtransformed age estimates. Statistical results were considered significant at α < 0.05. Results Rhizoprionodon terraenovae From 1993 to 1998 a total of 3,419 R. terraenovae were tagged and released, of these 155 were recaptured. Five R. terraenovae (four male and one female) were recaptured with times at liberty ranging from 7.7 to 14.0 years (mean ± S.D. = 10.1 ± 2.7). Length at initial tagging, and when available, length at recapture are listed in Table 1 . Backtransformed age at tagging and recapture ranged from 3.8–10.3 years and from 11.8 to 19.8 years, respectively ( Table 1 ). Vertebrae were sampled from Shark L5242 and the direct age estimate from the vertebral section was 18.5 years old ( Figure 1 ). Precise measurements were taken for L5242 at tagging and recapture; over 12.1 years-at-liberty this shark grew 28 mm (2.3 mm/year). All five sharks were recaptured within 15 km of initial tagging. Figure 1. Sectioned vertebra from Atlantic Sharpnose Shark Rhizoprionodon terraenovae L5242. Consensus band count was 20 band pairs (age = 18.5 years). Table 1. Initial tagging and recapture information for Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus long-term recaptures from the South Carolina Department of Natural Resources Adult Red Drum and Coastal Shark Longline Program. Fork length (FL) at initial tagging, length at recapture, growth, days and years at liberty, backtransformed age at initial tagging and recapture and direct age estimates are provided. Species Tag # Initial FL (mm) Recapture FL (mm) Growth (mm) Days at Liberty Years at Liberty Sex Backtransformed Age at Initial Tagging Backtransformed Age at Recapture Direct Age Estimate R. terraenovae L2881 776 828* 52 5098 14.0 Male 5.2 19.2 - R. terraenovae L4774 815 883* 68 3237 8.9 Female 10.1 19.0 - R. terraenovae L5173 737 - - 2937 8.0 Male 3.8 11.8 - R. terraenovae L5242 802 830 28 4438 12.1 Male 7.7 19.8 18.5 R. terraenovae L7250 810 838* 28 2806 7.7 Male 10.3 18.0 - C. acronotus L2910 876 960 84 4352 11.9 Male 4.5 16.4 15.5 C. acronotus L1515 878 1055 177 4678 12.8 Female 4.2 17.0 14.5 C. acronotus L3384 1020 - - 3986 10.9 Male 11.9 22.8 20.5 *Denotes approximate measurements as provided by recreational anglers. Carcharhinus acronotus From 1993 to 2013 a total of 1,537 C. acronotus were tagged and released, of these 24 were recaptured. Three C. acronotus were recaptured (two males and one female) with times at liberty ranging from 10.9 to 12.8 years (mean ± S.D. = 11.9 ± 1.0). Backtransformed age at tagging and recapture ranged from 4.2 to 11.9 years and 16.4 to 22.8 years, respectively ( Table 1 ). Vertebrae were obtained from all recaptured C. acronotus . Age estimates from vertebral sections ranged from 14.5 to 20.5 years ( Figure 2 ). Precise measurements were taken at capture and recapture for sharks L2910 and L1515. L2910 was at liberty for 12.0 years and grew 84 mm (7.0 mm/year). L1515 was at liberty for 12.8 years and grew 177 mm (13.8 mm/year). All recaptured C. acronotus were recovered within 15 km of initial tagging. Figure 2. Sectioned vertebra from Blacknose Shark Carcharhinus acronotus L3384. Consensus band count was 22 band pairs (age = 20.5 years). Age estimates and comparisons In recaptures with both direct and backtransformed age estimates, backtransformed age estimates were significantly larger (paired t-test, t = 4.82, P = 0.02) ( Table 1 ). From direct age estimates, R. terraenovae observed maximum longevity increased by 9.5 years for males (previously 9+ years [ Loefer & Sedberry, 2003 ]), and no vertebrae were available from female recaptures ( Table 2 ). Table 2. Observed maximum longevity from sectioned age estimates, and backtransformed maximum longevity from tag and recapture data for Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus . Species Study Sex Observed Maximum Longevity (years) Backtransformed Maximum Longevity (years) R. terraenovae western North Atlantic Loefer & Sedberry, 2003 Female 11+ - Male 9+ - R. terraenovae Current Female - 22.9 Male 18.0 19.8 C. acronotus western North Atlantic Driggers et al. , 2004 Female 12.5 - Male 10.5 - C. acronotus Current Female 14.5 17.0 Male 20.5 22.8 C. acronotus observed maximum longevity from sectioned age estimates increased by 2 years for females and 8 years for males (12.5 and 10.5 years for females and males respectively [Driggers et al. , 2001]). Backtransformed maximum longevity was 4.5 years older than published estimates for females and 12.3 years older for males. Discussion The backtransformed and direct age estimates documented herein greatly increase the known longevity for R. terraenovae and C. acronotus , which could significantly affect population dynamics models that include longevity as a parameter. Interestingly, the maximum directly estimated ages for both species were associated with male sharks. A review of published shark age and growth studies shows that, in most studies, females have a greater or equal longevity than males (e.g. Carlson & Baremore, 2003 ; Carlson & Parsons, 1997 ; Carlson et al. , 1999 ; Driggers et al. , 2004 ; Drymon et al. , 2006 ; Frazier et al. , 2014 ). Therefore, we believe that we did not sample older females and suggest that the longevity estimates we observed for each species be applied to males and females. Backtransformed age estimates from recaptures were in all cases larger than direct age estimates. This could be evidence that direct ages were underestimated, however direct age estimates only differed by an average of 1.8 years (range 1.0–2.5 years). Observed differences could be due to low sample size or individual variability in growth. The rearranged VBGF gives an estimate of average age-at-length based on parameter estimates. Therefore, specimens could have been younger or older than the average estimated age at time of tagging thus accounting for the discrepancy. Conversely, if the species-specific VBGF do not adequately describe the growth of R. terraenovae and C. acronotus then the observed differences would be expected. However, the growth models utilized were from studies with robust sample sizes that included all size classes ( Loefer & Sedberry, 2003 ; Driggers et al. , 2004 ). The age estimates from this study greatly increase longevity for both species; however, actual life spans could be even longer. The specimens recaptured from this study were tagged in the first few years of the SCDNR longline program (1994–1996). Given project species-specific recapture rates of less than 3% and reported tag shedding rates for nylon dart tags as high as 41% to 63% ( Xiao et al. , 1999 ), the chances of recapturing a shark at liberty for 10+ years are small. The fact that eight were encountered and all exceeded published longevity estimates lends support to this assertion. The data gathered from these recaptures also highlights the importance of continuing long term surveys and tagging efforts. While return rates of tagged sharks are notoriously low, our data demonstrate that continued tagging efforts are essential to provide the most up to date and reliable estimates of maximum longevity. Ideally, to obtain the best possible longevity estimates for a given species, future efforts should focus on tagging neonate sharks with the hope of recapturing them as they approach the end of their lifespans. Author contributions BF, WD and GU were involved with longline survey operations as well as tagging and recapturing the sharks. BF and WD aged specimens. BF and WD prepared manuscript for publication, and all authors were involved in revising the draft manuscript and agree to the final content. Competing interests No competing interests were disclosed. Grant information These data were based on a 20 year longline survey and numerous grants have funded the survey over the years. Funding for the longline survey was provided by the Federal Aid in Sport fish Restoration Act, the Southeast Area Monitoring and Assessment Program, the Atlantic States Marine Fisheries Commission, the National Marine Fisheries Federal Assistance Program, and the South Carolina State Recreational Fisheries Advisory Committee. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Acknowledgements We are grateful to the many folks that have helped the longline program over the years, especially Doug Oakley, Catherine Riley, Josh Loefer, Christian Jones, Carrie Hendrix, Jonathan Richardson, Erin Levesque, Henry Davega, Rob Dunlap and Ashley Shaw. We thank reviewers Marcus Drymon and Alastair Harry for their constructive comments on drafts of this note. This is contribution 727 of the South Carolina Marine Resource Center. Faculty Opinions recommended References Bishop SDH, Francis MP, Duffy C, et al. : Age, growth, maturity, longevity and natural mortality of the shortfin mako shark (Isurus oxyrinchus) in New Zealand Waters. Mar Freshwater Res. 2006; 57 (2): 143–154. Publisher Full Text Bonham K, Sanford FB, Clegg W, et al. : Biological and vitamin A studies of dogfish ( Squalus suckleye ) in the State of Washington. Washington State Department of Fisheries. Biological Report. 1949; 49A : 83–114. Reference Source Carlson JK, Baremore IE: Changes in biological parameters of Atlantic sharpnose shark Rhizoprionodon terraenovae in the Gulf of Mexico: evidence for density-dependent growth and maturity? Mar Freshwater Res. 2003; 54 (3): 227–234. 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Fisheries Research and Development Corporation, Canberra. 2001; 116–129. Kohler NE, Turner PA: Shark tagging: a review of conventional methods and studies. Environ Biol Fish. 2001; 60 (1–3): 191–223. Publisher Full Text Loefer JK, Sedberry GR: Life history of the Atlantic sharpnose shark ( Rhizoprionodon terraenovae ) (Richardson, 1836) off the Southeastern United States. Fish Bull. 2003; 101 : 75–88. Reference Source Ulrich GF, Jones CM, Driggers WB II, et al. : Habitat utilization, relative abundance, and seasonality of sharks in the estuarine and nearshore waters of South Carolina. In Shark nursery grounds of the Gulf of Mexico and East Coast waters of the United States (McCandless, CT NE Kohler, and HL Pratt Jr. editors), American Fisheries Society. Symposium 50, Bethesda, Maryland. 2007; 125–139. Reference Source Xiao Y, Brown LP, Walker TI, et al. : Estimation of instantaneous rates of tag shedding for school shark, Galeorhinus galeus , and gummy shark, Mustelus antarcticus , by conditional likelihood. Fish Bull. 1999; 97 (1): 170–184. Reference Source Comments on this article Comments (0) Version 2 VERSION 2 PUBLISHED 12 Aug 2014 ADD YOUR COMMENT Comment Author details Author details 1 South Carolina Department of Natural Resources, Marine Resources Research Institute, Charleston, SC, 29412, USA 2 National Marine Fisheries Service, Southeast Fisheries Science Center, Mississippi Laboratories, Pascagoula, MS, 39567, USA Competing interests No competing interests were disclosed. Grant information These data were based on a 20 year longline survey and numerous grants have funded the survey over the years. Funding for the longline survey was provided by the Federal Aid in Sport fish Restoration Act, the Southeast Area Monitoring and Assessment Program, the Atlantic States Marine Fisheries Commission, the National Marine Fisheries Federal Assistance Program, and the South Carolina State Recreational Fisheries Advisory Committee. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Article Versions (2) version 2 Revised Published: 27 Jan 2015, 3:190 https://doi.org/10.12688/f1000research.4767.2 version 1 Published: 12 Aug 2014, 3:190 https://doi.org/10.12688/f1000research.4767.1 Copyright © 2015 Frazier BS et al . This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication). Download Export To Sciwheel Bibtex EndNote ProCite Ref. Manager (RIS) Sente metrics Views Downloads F1000Research - - PubMed Central info_outline Data from PMC are received and updated monthly. - - Citations open_in_new 0 open_in_new 0 open_in_new SEE MORE DETAILS CITE how to cite this article Frazier BS, Driggers III WB and Ulrich GF. Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.12688/f1000research.4767.2 ) NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS track receive updates on this article Track an article to receive email alerts on any updates to this article. TRACK THIS ARTICLE Share Open Peer Review Current Reviewer Status: ? Key to Reviewer Statuses VIEW HIDE Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions Version 2 VERSION 2 PUBLISHED 27 Jan 2015 Revised Views 0 Cite How to cite this report: Harry A. Reviewer Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5743.r7492 ) The direct URL for this report is: https://f1000research.com/articles/3-190/v2#referee-response-7492 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 29 Jan 2015 Alastair Harry , Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Australia Approved VIEWS 0 https://doi.org/10.5256/f1000research.5743.r7492 I think the changes made have ... Continue reading READ ALL I think the changes made have strengthened the manuscript and have no further comments. Competing Interests: No competing interests were disclosed. I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Harry A. Reviewer Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5743.r7492 ) The direct URL for this report is: https://f1000research.com/articles/3-190/v2#referee-response-7492 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Respond or Comment COMMENT ON THIS REPORT Version 1 VERSION 1 PUBLISHED 12 Aug 2014 Views 0 Cite How to cite this report: Drymon M. Reviewer Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5090.r5801 ) The direct URL for this report is: https://f1000research.com/articles/3-190/v1#referee-response-5801 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 02 Sep 2014 Marcus Drymon , Department of Marine Sciences, University of South Alabama, Mobile, AL, USA Approved VIEWS 0 https://doi.org/10.5256/f1000research.5090.r5801 This manuscript reports increased longevity for two common species of small coastal sharks (Atlantic Sharpnose Shark Rhizoprionodon terraenovae and Blacknose Shark Carcharhinus acronotus ) based on tag recapture data. These findings are particularly interesting given the previously assumed longevity of these ... Continue reading READ ALL This manuscript reports increased longevity for two common species of small coastal sharks (Atlantic Sharpnose Shark Rhizoprionodon terraenovae and Blacknose Shark Carcharhinus acronotus ) based on tag recapture data. These findings are particularly interesting given the previously assumed longevity of these species, and are clearly relevant to population models that include longevity as a parameter for these species. This note is clearly written, and conclusions from this work are appropriately presented; moreover, these data illustrate the benefit of long-term fisheries-independent monitoring and tagging programs for long-lived species such as sharks. These data are clear, concise, and important to the continued successful management of these two species; as such, they are worthy of publication. The two tables presented are sufficient to convey the data discussed. Given the straightforward nature of these data and their appropriate interpretation by the Authors, I have no major comments. There are two typos in the first paragraph of the Discussion (detailed below) which should be addressed. In the sentence “A review of published shark age and growth studies shows that, in most studies, that females have a greater…,” remove that. In the sentence “Therefore, we believe that we did not sample older females and suggest that the longevity estimates maximum observed longevity we observed for each species…,” revise “ longevity estimates maximum observed longevity” as desired. Competing Interests: No competing interests were disclosed. I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Drymon M. Reviewer Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5090.r5801 ) The direct URL for this report is: https://f1000research.com/articles/3-190/v1#referee-response-5801 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Author Response 27 Jan 2015 Bryan Frazier , South Carolina Department of Natural Resources, Marine Resources Research Institute, Charleston, SC, 29412, USA 27 Jan 2015 Author Response The authors thank the reviewer for the suggested edits, all have been incorporated. Competing Interests: No competing interests were disclosed. The authors thank the reviewer for the suggested edits, all have been incorporated. The authors thank the reviewer for the suggested edits, all have been incorporated. Competing Interests: No competing interests were disclosed. Close Report a concern Respond or Comment COMMENTS ON THIS REPORT Author Response 27 Jan 2015 Bryan Frazier , South Carolina Department of Natural Resources, Marine Resources Research Institute, Charleston, SC, 29412, USA 27 Jan 2015 Author Response The authors thank the reviewer for the suggested edits, all have been incorporated. Competing Interests: No competing interests were disclosed. The authors thank the reviewer for the suggested edits, all have been incorporated. The authors thank the reviewer for the suggested edits, all have been incorporated. Competing Interests: No competing interests were disclosed. Close Report a concern COMMENT ON THIS REPORT Views 0 Cite How to cite this report: Harry A. Reviewer Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5090.r5802 ) The direct URL for this report is: https://f1000research.com/articles/3-190/v1#referee-response-5802 NOTE: it is important to ensure the information in square brackets after the title is included in this citation. Close Copy Citation Details Reviewer Report 26 Aug 2014 Alastair Harry , Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Australia Approved with Reservations VIEWS 0 https://doi.org/10.5256/f1000research.5090.r5802 This research note presents data on the long-term recapture of seven individuals of two species of coastal sharks from the Northwest Atlantic; Rhizoprionodon terranovae , and the Carcharhinus acronotus . Based on their length at tagging, all individuals appeared to be either ... Continue reading READ ALL This research note presents data on the long-term recapture of seven individuals of two species of coastal sharks from the Northwest Atlantic; Rhizoprionodon terranovae , and the Carcharhinus acronotus . Based on their length at tagging, all individuals appeared to be either mature or close to maturity, but were recaptured between 7.7 and 12.8 years later. As neither species was reported to be particularly long-lived these results are interesting, and provide evidence that both species live longer than currently thought. Age was also estimated and compared in four of the samples by reading sectioned vertebrae. These data contribute to growing evidence that longevity of sharks is often underestimated when based on vertebral ageing methods, and that some aspects of elasmobranch demography that have been inferred from these studies (e.g. survival) may be biased. I’m glad the authors have taken the time and effort to document these observations, as there are relatively few long-terms studies of this kind. While I think the data themselves are worthy of publication, I don’t think any of the subsequent analysis contributed hugely to the paper. Published growth curves are used to estimate the age at tagging, which is then added to the time at liberty to get a ‘backtransformed age at recapture’. Unfortunately, neither of these original growth studies presented the model variance, a detailed description of the data, or even any plots of the size at age data! Without this information, it is hard to get an idea of how variable size-at-age is for these species (and it is clearly quite variable), or the representativeness of the original sampling, etc. Personally, I think other information could be more useful, like photographs of the two oldest vertebrae sections for reference. I recommend two revisions to the research note. Firstly, some more background information is required on the tagging study itself. It is not stated how many sharks were tagged and recaptured over the duration of the whole study, nor is it clear why these seven were chosen specifically (presumably they weren't the only recaptures). Secondly, I disagree that Fabens’ theoretical method for estimating longevity is the usual method of estimating longevity. I don’t see the value with making comparisons to theoretical longevity later on in the paper and find this confusing. For example, the ‘theoretical maximum longevities’ of R. terranovae are stated to be 7.1 and 6.9 years for females and males respectively, but Loefer and Sedberry (2003) reported actual longevities of 10 and 9 years. Competing Interests: No competing interests were disclosed. I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above. Close READ LESS CITE CITE HOW TO CITE THIS REPORT Harry A. Reviewer Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5090.r5802 ) The direct URL for this report is: https://f1000research.com/articles/3-190/v1#referee-response-5802 NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article. COPY CITATION DETAILS Report a concern Author Response 28 Jan 2015 Bryan Frazier , South Carolina Department of Natural Resources, Marine Resources Research Institute, Charleston, SC, 29412, USA 28 Jan 2015 Author Response The authors appreciate the suggested revisions offered by the reviewer. We agree that it is unfortunate that the original age and growth studies did not present individual length at age ... Continue reading The authors appreciate the suggested revisions offered by the reviewer. We agree that it is unfortunate that the original age and growth studies did not present individual length at age data with their published growth curves. While we felt it most appropriate to cite the peer reviewed publications, it should be noted that these data are available for Carcharhinus acronotus (SEDAR 21 DW-36, http://www.sefsc.noaa.gov/sedar/download/S21_DW_36.pdf?id=DOCUMENT) as a working paper for United States SouthEast Data, Assessment and Review C. acronotus stock assessment. Unfortunately, there are no publicly accessible documents showing variation in length-at-age for Rhizoprionodon terraenovae . The authors agree with the reviewer that images of the oldest aged vertebra for each species are appropriate, and we have added those figures. As requested, the authors have added minimal background information detailing the total tagged and recaptured of each species. The authors feel adding additional background information beyond this would not be of value to readers. The recaptures that were used for this note were chosen due to their lengthy times-at-liberty. Recaptures with shorter times-at-liberty were not used as they would be less informative given variability in length-at-age. The authors agree with the reviewer that including Faben's theoretical maximum longevities were confusing and we have removed these data from the note. The authors appreciate the suggested revisions offered by the reviewer. We agree that it is unfortunate that the original age and growth studies did not present individual length at age data with their published growth curves. While we felt it most appropriate to cite the peer reviewed publications, it should be noted that these data are available for Carcharhinus acronotus (SEDAR 21 DW-36, http://www.sefsc.noaa.gov/sedar/download/S21_DW_36.pdf?id=DOCUMENT) as a working paper for United States SouthEast Data, Assessment and Review C. acronotus stock assessment. Unfortunately, there are no publicly accessible documents showing variation in length-at-age for Rhizoprionodon terraenovae . The authors agree with the reviewer that images of the oldest aged vertebra for each species are appropriate, and we have added those figures. As requested, the authors have added minimal background information detailing the total tagged and recaptured of each species. The authors feel adding additional background information beyond this would not be of value to readers. The recaptures that were used for this note were chosen due to their lengthy times-at-liberty. Recaptures with shorter times-at-liberty were not used as they would be less informative given variability in length-at-age. The authors agree with the reviewer that including Faben's theoretical maximum longevities were confusing and we have removed these data from the note. Competing Interests: No competing interests were disclosed. Close Report a concern Respond or Comment COMMENTS ON THIS REPORT Author Response 28 Jan 2015 Bryan Frazier , South Carolina Department of Natural Resources, Marine Resources Research Institute, Charleston, SC, 29412, USA 28 Jan 2015 Author Response The authors appreciate the suggested revisions offered by the reviewer. We agree that it is unfortunate that the original age and growth studies did not present individual length at age ... Continue reading The authors appreciate the suggested revisions offered by the reviewer. We agree that it is unfortunate that the original age and growth studies did not present individual length at age data with their published growth curves. While we felt it most appropriate to cite the peer reviewed publications, it should be noted that these data are available for Carcharhinus acronotus (SEDAR 21 DW-36, http://www.sefsc.noaa.gov/sedar/download/S21_DW_36.pdf?id=DOCUMENT) as a working paper for United States SouthEast Data, Assessment and Review C. acronotus stock assessment. Unfortunately, there are no publicly accessible documents showing variation in length-at-age for Rhizoprionodon terraenovae . The authors agree with the reviewer that images of the oldest aged vertebra for each species are appropriate, and we have added those figures. As requested, the authors have added minimal background information detailing the total tagged and recaptured of each species. The authors feel adding additional background information beyond this would not be of value to readers. The recaptures that were used for this note were chosen due to their lengthy times-at-liberty. Recaptures with shorter times-at-liberty were not used as they would be less informative given variability in length-at-age. The authors agree with the reviewer that including Faben's theoretical maximum longevities were confusing and we have removed these data from the note. The authors appreciate the suggested revisions offered by the reviewer. We agree that it is unfortunate that the original age and growth studies did not present individual length at age data with their published growth curves. While we felt it most appropriate to cite the peer reviewed publications, it should be noted that these data are available for Carcharhinus acronotus (SEDAR 21 DW-36, http://www.sefsc.noaa.gov/sedar/download/S21_DW_36.pdf?id=DOCUMENT) as a working paper for United States SouthEast Data, Assessment and Review C. acronotus stock assessment. Unfortunately, there are no publicly accessible documents showing variation in length-at-age for Rhizoprionodon terraenovae . The authors agree with the reviewer that images of the oldest aged vertebra for each species are appropriate, and we have added those figures. As requested, the authors have added minimal background information detailing the total tagged and recaptured of each species. The authors feel adding additional background information beyond this would not be of value to readers. The recaptures that were used for this note were chosen due to their lengthy times-at-liberty. Recaptures with shorter times-at-liberty were not used as they would be less informative given variability in length-at-age. The authors agree with the reviewer that including Faben's theoretical maximum longevities were confusing and we have removed these data from the note. Competing Interests: No competing interests were disclosed. Close Report a concern COMMENT ON THIS REPORT Comments on this article Comments (0) Version 2 VERSION 2 PUBLISHED 12 Aug 2014 ADD YOUR COMMENT Comment keyboard_arrow_left keyboard_arrow_right Open Peer Review Reviewer Status info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions Reviewer Reports Invited Reviewers 1 2 Version 2 (revision) 27 Jan 15 read Version 1 12 Aug 14 read read Alastair Harry , James Cook University, Townsville, Australia Marcus Drymon , University of South Alabama, Mobile, AL, USA Comments on this article All Comments (0) Add a comment Sign up for content alerts Sign Up You are now signed up to receive this alert Browse by related subjects keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2015 Harry A. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 29 Jan 2015 | for Version 2 Alastair Harry , Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Australia 0 Views copyright © 2015 Harry A. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (0) Approved info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions I think the changes made have strengthened the manuscript and have no further comments. Competing Interests No competing interests were disclosed. I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. reply Respond to this report Responses (0) Harry A. Peer Review Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5743.r7492) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. The direct URL for this report is: https://f1000research.com/articles/3-190/v2#referee-response-7492 keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2014 Drymon M. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 02 Sep 2014 | for Version 1 Marcus Drymon , Department of Marine Sciences, University of South Alabama, Mobile, AL, USA 0 Views copyright © 2014 Drymon M. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (1) Approved info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions This manuscript reports increased longevity for two common species of small coastal sharks (Atlantic Sharpnose Shark Rhizoprionodon terraenovae and Blacknose Shark Carcharhinus acronotus ) based on tag recapture data. These findings are particularly interesting given the previously assumed longevity of these species, and are clearly relevant to population models that include longevity as a parameter for these species. This note is clearly written, and conclusions from this work are appropriately presented; moreover, these data illustrate the benefit of long-term fisheries-independent monitoring and tagging programs for long-lived species such as sharks. These data are clear, concise, and important to the continued successful management of these two species; as such, they are worthy of publication. The two tables presented are sufficient to convey the data discussed. Given the straightforward nature of these data and their appropriate interpretation by the Authors, I have no major comments. There are two typos in the first paragraph of the Discussion (detailed below) which should be addressed. In the sentence “A review of published shark age and growth studies shows that, in most studies, that females have a greater…,” remove that. In the sentence “Therefore, we believe that we did not sample older females and suggest that the longevity estimates maximum observed longevity we observed for each species…,” revise “ longevity estimates maximum observed longevity” as desired. Competing Interests No competing interests were disclosed. I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard. reply Respond to this report Responses (1) Author Response 27 Jan 2015 Bryan Frazier, South Carolina Department of Natural Resources, Marine Resources Research Institute, Charleston, SC, 29412, USA The authors thank the reviewer for the suggested edits, all have been incorporated. View more View less Competing Interests No competing interests were disclosed. reply Respond Report a concern Drymon M. Peer Review Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5090.r5801) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. The direct URL for this report is: https://f1000research.com/articles/3-190/v1#referee-response-5801 keyboard_arrow_left Back to all reports Reviewer Report 0 Views copyright © 2014 Harry A. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 26 Aug 2014 | for Version 1 Alastair Harry , Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Australia 0 Views copyright © 2014 Harry A. This is an open access peer review report distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. format_quote Cite this report speaker_notes Responses (1) Approved With Reservations info_outline Alongside their report, reviewers assign a status to the article: Approved The paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. Not approved Fundamental flaws in the paper seriously undermine the findings and conclusions This research note presents data on the long-term recapture of seven individuals of two species of coastal sharks from the Northwest Atlantic; Rhizoprionodon terranovae , and the Carcharhinus acronotus . Based on their length at tagging, all individuals appeared to be either mature or close to maturity, but were recaptured between 7.7 and 12.8 years later. As neither species was reported to be particularly long-lived these results are interesting, and provide evidence that both species live longer than currently thought. Age was also estimated and compared in four of the samples by reading sectioned vertebrae. These data contribute to growing evidence that longevity of sharks is often underestimated when based on vertebral ageing methods, and that some aspects of elasmobranch demography that have been inferred from these studies (e.g. survival) may be biased. I’m glad the authors have taken the time and effort to document these observations, as there are relatively few long-terms studies of this kind. While I think the data themselves are worthy of publication, I don’t think any of the subsequent analysis contributed hugely to the paper. Published growth curves are used to estimate the age at tagging, which is then added to the time at liberty to get a ‘backtransformed age at recapture’. Unfortunately, neither of these original growth studies presented the model variance, a detailed description of the data, or even any plots of the size at age data! Without this information, it is hard to get an idea of how variable size-at-age is for these species (and it is clearly quite variable), or the representativeness of the original sampling, etc. Personally, I think other information could be more useful, like photographs of the two oldest vertebrae sections for reference. I recommend two revisions to the research note. Firstly, some more background information is required on the tagging study itself. It is not stated how many sharks were tagged and recaptured over the duration of the whole study, nor is it clear why these seven were chosen specifically (presumably they weren't the only recaptures). Secondly, I disagree that Fabens’ theoretical method for estimating longevity is the usual method of estimating longevity. I don’t see the value with making comparisons to theoretical longevity later on in the paper and find this confusing. For example, the ‘theoretical maximum longevities’ of R. terranovae are stated to be 7.1 and 6.9 years for females and males respectively, but Loefer and Sedberry (2003) reported actual longevities of 10 and 9 years. Competing Interests No competing interests were disclosed. I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above. reply Respond to this report Responses (1) Author Response 28 Jan 2015 Bryan Frazier, South Carolina Department of Natural Resources, Marine Resources Research Institute, Charleston, SC, 29412, USA The authors appreciate the suggested revisions offered by the reviewer. We agree that it is unfortunate that the original age and growth studies did not present individual length at age data with their published growth curves. While we felt it most appropriate to cite the peer reviewed publications, it should be noted that these data are available for Carcharhinus acronotus (SEDAR 21 DW-36, http://www.sefsc.noaa.gov/sedar/download/S21_DW_36.pdf?id=DOCUMENT) as a working paper for United States SouthEast Data, Assessment and Review C. acronotus stock assessment. Unfortunately, there are no publicly accessible documents showing variation in length-at-age for Rhizoprionodon terraenovae . The authors agree with the reviewer that images of the oldest aged vertebra for each species are appropriate, and we have added those figures. As requested, the authors have added minimal background information detailing the total tagged and recaptured of each species. The authors feel adding additional background information beyond this would not be of value to readers. The recaptures that were used for this note were chosen due to their lengthy times-at-liberty. Recaptures with shorter times-at-liberty were not used as they would be less informative given variability in length-at-age. The authors agree with the reviewer that including Faben's theoretical maximum longevities were confusing and we have removed these data from the note. View more View less Competing Interests No competing interests were disclosed. reply Respond Report a concern Harry A. Peer Review Report For: Longevity of Atlantic Sharpnose Sharks Rhizoprionodon terraenovae and Blacknose Sharks Carcharhinus acronotus in the western North Atlantic Ocean based on tag-recapture data and direct age estimates [version 2; peer review: 2 approved] . F1000Research 2015, 3 :190 ( https://doi.org/10.5256/f1000research.5090.r5802) NOTE: it is important to ensure the information in square brackets after the title is included in this citation. The direct URL for this report is: https://f1000research.com/articles/3-190/v1#referee-response-5802 Alongside their report, reviewers assign a status to the article: Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit. 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