DOCSLIB.ORG

Time-Dependent Rate Phenomenon in Viruses

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Time-Dependent Rate Phenomenon in Viruses JVI Accepted Manuscript Posted Online 1 June 2016 J. Virol. doi:10.1128/JVI.00593-16 Copyright © 2016 Aiewsakun and Katzourakis. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. 1 Title 2 Time-dependent rate phenomenon in viruses 3 Running title 4 Time-dependent rate phenomenon in viruses Downloaded from 5 6 Authors 7 Pakorn Aiewsakuna and Aris Katzourakisa# http://jvi.asm.org/ 8 9 Author Affiliations 10 aDepartment of Zoology, University of Oxford, Oxford, UK on June 7, 2016 by guest 11 #Address correspondence to Aris Katzourakis, [email protected]. 12 13 Word count 14 Abstract: 244; text: 7226 15 Keywords 16 Short-term long-term rate discrepancy, time-dependent rate phenomenon, rate of viral evolution, power law 1 17 Abstract 18 Among the most fundamental questions in viral evolutionary biology are how fast viruses evolve and how their 19 rates vary among viruses and fluctuate through time. Traditionally, viruses are loosely classed into two groups: 20 slow-evolving DNA viruses and fast-evolving RNA viruses. As viral evolutionary rate estimates become more 21 available, it appears that the rates are negatively correlated with the measurement timescales, and that the 22 boundary between the rates of DNA and RNA viruses might not be as clear as previously thought. In this study, Downloaded from 23 we collected 396 viral evolutionary rate estimates across almost all viral genome types and replication 24 strategies, and examined their rate dynamics. We showed that the time-dependent rate phenomenon exists 25 across multiple levels of viral taxonomy, from the Baltimore classification viral groups to genera. We also 26 showed that, by taking the rate-decay dynamics into account, a clear division between the rates of DNA and http://jvi.asm.org/ 27 RNA as well as reverse-transcribing viruses could be recovered. Surprisingly, despite large differences in their 28 biology, our analyses suggested that the rate-decay speed is independent of viral types, and thus it might be 29 useful for better estimation of the evolutionary timescale of any virus. To illustrate this, we used our model to on June 7, 2016 by guest 30 re-estimate evolutionary timescales of extant lentiviruses, which were previously suggested to be very young 31 by standard phylogenetic analyses. Our analyses suggested that they are millions of years old, consistent with 32 paleovirological evidence, and therefore for the first time, reconciled molecular analyses of ancient and extant 33 viruses. 2 34 Importance 35 This work provides direct evidence that viral evolutionary rate estimates decay with their measurement 36 timescales, and that the rate-decay speeds do not differ significantly among viruses despite the vast 37 differences in their molecular features. With the rate-decay dynamics adjusted for, the division between the 38 rates of dsDNA, ssRNA, and ssDNA/reverse-transcribing viruses could be seen more clearly than before. Our 39 results provide a guideline for further improvement of molecular clock. As a demonstration of this, we used Downloaded from 40 our model to re-estimate the timescales of modern lentiviruses, which were previously thought to be very 41 young, to be millions of years old. This result matches the estimate from paleovirological analyses, thus 42 bridging the gap between ancient and extant viral evolutionary studies. http://jvi.asm.org/ on June 7, 2016 by guest 3 43 Introduction 44 An accurate and precise knowledge of the rate of viral evolution is central to the reconstruction of viral natural 45 history, necessary for the calculation of many evolutionary parameters, from viral age estimates to population 46 size. Generally, viruses are loosely classed into two groups according to their rates of evolution: ‘slow- 47 evolving’ and ‘fast evolving’ viruses. DNA viruses, especially double-stranded DNA (dsDNA) viruses, are 48 traditionally thought of as slow-evolving viruses. To estimate molecular evolutionary rates, the absolute Downloaded from 49 timescales for the observed genetic differences are required, and these can be derived from the divergence 50 dates and/or sampling dates of the study subjects. Many dsDNA viruses have been shown to have an 51 extremely stable co-speciation history with their hosts, and therefore their divergence dates can be directly 52 inferred from those of their hosts. On the basis of these observations, their rates have been estimated to be in http://jvi.asm.org/ 53 the order of 10-7 to 10-9 nucleotide substitutions per site per year (s/n/y) (1–5), comparable to those of their 54 hosts (6, 7). 55 on June 7, 2016 by guest 56 RNA viruses are, on the other hand, typically regarded as fast-evolving viruses. RNA viruses are generally 57 characterised by frequent cross-species transmissions in nature; as a result, it is often difficult to calibrate 58 their evolutionary rates using host evolutionary timescales. Their rates are thus often calculated by using 59 molecular sequences collected at different time points (heterochronous molecular datasets). In this case, the 60 differences among sampling times provide the timescales for the observed genetic divergence. Based on these 61 analyses, their rates are commonly estimated to be between 10-2 and 10-5 s/n/y (8–11), 2-7 orders of 62 magnitude higher than the typical rates of dsDNA viruses. 63 64 This conventional concept of a dichotomy between the rates of DNA and RNA viral evolution has recently been 65 challenged however, and it seems that the boundary between the rates of DNA and RNA viruses might not be 4 66 as clear as previously thought (11–14). For example, analyses of heterochronous molecular datasets of dsDNA 67 and single-stranded DNA (ssDNA) viruses revealed that DNA viruses are in fact capable of evolving very rapidly 68 over short timescales, with rates ranging between 10-3-10-6 s/n/y (15–19), comparable to the estabished rates 69 of many RNA viruses. On the other hand, when the co-speciation assumption is applicable with RNA viruses, 70 such as deltaretroviruses, hantaviruses, and foamy viruses, analyses suggest that their long-term rates of 71 evolution are extremely low, estimated to be in the range of 10-7-10-8 s/n/y (20–23), comparable to those of Downloaded from 72 dsDNA viruses. Paleovirological analyses also showed that many ancient endogenous viruses related to RNA 73 viruses exhibit high similarity to their modern-day counterparts despite them being millions of years old (24). 74 This provides independent evidence indicating that RNA viruses can indeed evolve very slowly over geological 75 timescales (24). By naïvely combining all of the rate estimates together, the ranges of the rate estimates of http://jvi.asm.org/ 76 both DNA and RNA viral evolution appear to be extremely wide, spanning from 10-3 to 10-9 s/n/y for DNA 77 viruses and 10-2 to 10-8 s/n/y for RNA viruses, largely overlapping with one another. As a result, there is an 78 emerging consensus that there is no strict division between the rates of DNA and RNA viruses (13, 14). on June 7, 2016 by guest 79 80 As viral evolutionary rate estimates become more available, it is becoming increasingly clear that viral 81 evolutionary rates appear to vary over time, continuously decreasing with the timescale of rate measurement 82 (25–27). Many hypotheses have been proposed to explain this time-dependent rate phenomenon (TDRP), 83 including temporal changes in selection pressure and/or viral biology, as well as the facts that short-term rates 84 are methodologically prone to overestimation and the long-term ones tend to be underestimated (see (25) for 85 review). This phenomenon may at least partly explain the observed large variation and overlap of viral 86 evolutionary rate estimates. 87 5 88 Another consequence of the TDRP is that naïvely transferring the rate estimates over different timescales for 89 evolutionary inference can severely bias the outcome (25–27). The best illustration of this is perhaps the 90 severe underestimation of the evolutionary timescales of extant viruses by current standard phylogenetic 91 tools. For example, while paleovirological analyses unequivocally show that simian immunodeficiency viruses 92 (SIVs) are millions of years old (28, 29), all previous standard phylogenetic analyses, which do not account for 93 the TDRP, suggest that they are young, sharing a most recent common ancestor (MRCA) less than a million Downloaded from 94 years ago (8, 30–32). One pragmatic approach to solve this problem is to use models describing the empirical 95 relationship between the rate estimates and their measurement timescales to correct for the TDRP effects in 96 evolutionary analyses (27, 33). Our study of foamy viruses has shown that a power-law rate decay model can 97 describe the TDRP very well empirically, and thus it may be useful as a tool for correcting for the effects of the http://jvi.asm.org/ 98 TDRP (27). 99 100 In this study, we collected 396 viral nucleotide substitution rates across almost all viral molecular features and on June 7, 2016 by guest 101 replication strategies, and examined their TDRP dynamics at various taxonomical levels by using the power- 102 law rate decay model as the basis of our investigation. We also examined how the rate dynamics differ among 103 viruses, and re-examined the concept of fast- and slow-evolving viruses. Lastly, we demonstrated the use of 104 our TDRP model by estimating the evolutionary timescale of extant lentiviruses, which has always been 105 severely underestimated by standard phylogenetic analyses. 6 106 Materials and Methods 107 Data collecting and constructing phylogenetically independent datasets of rate 108 estimates 109 396 viral nucleotide substitution rate estimates were collected from 133 pieces of published literature.
Load more

Recommended publications
  • Mandrillus Leucophaeus Poensis)
    Ecology and Behavior of the Bioko Island Drill (Mandrillus leucophaeus poensis) A Thesis Submitted to the Faculty of Drexel University by Jacob Robert Owens in partial fulfillment of the requirements for the degree of Doctor of Philosophy December 2013 i © Copyright 2013 Jacob Robert Owens. All Rights Reserved ii Dedications To my wife, Jen. iii Acknowledgments The research presented herein was made possible by the financial support provided by Primate Conservation Inc., ExxonMobil Foundation, Mobil Equatorial Guinea, Inc., Margo Marsh Biodiversity Fund, and the Los Angeles Zoo. I would also like to express my gratitude to Dr. Teck-Kah Lim and the Drexel University Office of Graduate Studies for the Dissertation Fellowship and the invaluable time it provided me during the writing process. I thank the Government of Equatorial Guinea, the Ministry of Fisheries and the Environment, Ministry of Information, Press, and Radio, and the Ministry of Culture and Tourism for the opportunity to work and live in one of the most beautiful and unique places in the world. I am grateful to the faculty and staff of the National University of Equatorial Guinea who helped me navigate the geographic and bureaucratic landscape of Bioko Island. I would especially like to thank Jose Manuel Esara Echube, Claudio Posa Bohome, Maximilliano Fero Meñe, Eusebio Ondo Nguema, and Mariano Obama Bibang. The journey to my Ph.D. has been considerably more taxing than I expected, and I would not have been able to complete it without the assistance of an expansive list of people. I would like to thank all of you who have helped me through this process, many of whom I lack the space to do so specifically here.
    [Show full text]
  • Primate Conservation 2006 (20): 1–28
    Contents General Primates in Peril: The World’s 25 Most Endangered Primates, 2004–2006 ..................................................................................1 Russell A. Mittermeier, Cláudio Valladares-Pádua, Anthony B. Rylands, Ardith A. Eudey, Thomas M. Butynski, Jörg U. Ganzhorn, Rebecca Kormos, John M. Aguiar and Sally Walker Neotropical Region On a New Species of Titi Monkey, Genus Callicebus Thomas (Primates, Pitheciidae), from Western Bolivia with Preliminary Notes on Distribution and Abundance ...............................................................................................................29 Robert. B. Wallace, Humberto Gómez, Annika Felton and Adam M. Felton Identifi cation, Behavioral Observations, and Notes on the Distribution of the Titi Monkeys Callicebus modestus Lönnberg, 1939 and Callicebus olallae Lönnberg, 1939 ..............................................................................41 Adam Felton, Annika M. Felton, Robert B. Wallace and Humberto Gómez A Survey of Primate Populations in Northeastern Venezuelan Guayana .....................................................................................47 Bernardo Urbani A History of Long-term Research and Conservation of Northern Muriquis (Brachyteles hypoxanthus) at the Estação Biológica de Caratinga/RPPN-FMA .......................................................................................................................53 Karen B. Strier and Jean Philippe Boubli Africa English Common Names for Subspecies and Species of African Primates
    [Show full text]
  • DRILL INFO Issue 11, January 2011 Dear Members, Dear Friends of the Drill
    DRILL INFO Issue 11, January 2011 Dear members, dear friends of the Drill, First of all we want to wish you a happy new year. We hope you all had a pleasant and peaceful Christmas. In this issue we want to inform you about great fundraising campaigns for the drills. We also want to inform you about the conservation status of the drill on Bioko Island. Enjoy reading it. Your editorial team Sumbo Male Drill “Sumbo” from “Erlebnis-Zoo-Hanover” dead The head of the Drill family of Hanover zoo had to be euthanized on October 11th 2010 after a long disease. 2004 “Sumbo” was diagnosed for typ-1-diabetes. The keepers were able to train him to tolerate daily insulin injections and to get urine samples from to him to measure the blood glucose. Thanks to this perfect collaboration between “Sumbo” and the keepers the male recovered and became famous nationwide. Unfortunately his health status became worst in the beginning of 2010. It became more and more difficult to adjust the insulin and “Sumbo” started to suffer under the side effects of this disease, like loss of weight and neuropathy. In October the hard decision to release him from his suffering had to be made. “Sumbo” came to Hanover in February 2001 from the Zoo Rabat/Morocco to follow up the successful breeding tradition. Most important is the fact, that “Sumbo” was born 1991 in the wild and hence is not related to the captive Drills living in Europe. He fulfilled the expectations in Hanover and fathered 17 offspring in total, who are now for example living in Spain and England.
    [Show full text]
  • The World's 25 Most Endangered Primates, 2006-2008
    Primate Conservation 2007 (22): 1 – 40 Primates in Peril: The World’s 25 Most Endangered Primates, 2006 – 2008 Russell A. Mittermeier 1, Jonah Ratsimbazafy 2, Anthony B. Rylands 3, Liz Williamson 4, John F. Oates 5, David Mbora 6, Jörg U. Ganzhorn 7, Ernesto Rodríguez-Luna 8, Erwin Palacios 9, Eckhard W. Heymann 10, M. Cecília M. Kierulff 11, Long Yongcheng 12, Jatna Supriatna 13, Christian Roos 14, Sally Walker 15, and John M. Aguiar 3 1Conservation International, Arlington, VA, USA 2Durrell Wildlife Conservation Trust – Madagascar Programme, Antananarivo, Madagascar 3Center for Applied Biodiversity Science, Conservation International, Arlington, VA, USA 4Department of Psychology, University of Stirling, Stirling, Scotland, UK 5Department of Anthropology, Hunter College, City University of New York (CUNY), New York, USA 6Department of Biological Sciences, Dartmouth College, Hanover, NH, USA 7Institute of Zoology, Ecology and Conservation, Hamburg, Germany 8Instituto de Neuroetología, Universidad Veracruzana, Veracruz, México 9Conservation International Colombia, Bogotá, DC, Colombia 10Abteilung Verhaltensforschung & Ökologie, Deutsches Primatenzentrum, Göttingen, Germany 11Fundação Parque Zoológico de São Paulo, São Paulo, Brazil 12The Nature Conservancy, China Program, Kunming, Yunnan, China 13Conservation International Indonesia, Jakarta, Indonesia 14 Gene Bank of Primates, Deutsches Primatenzentrum, Göttingen, Germany 15Zoo Outreach Organisation, Coimbatore, Tamil Nadu, India Introduction among primatologists working in the field who had first-hand knowledge of the causes of threats to primates, both in gen- Here we report on the fourth iteration of the biennial eral and in particular with the species or communities they listing of a consensus of 25 primate species considered to study. The meeting and the review of the list of the World’s be amongst the most endangered worldwide and the most in 25 Most Endangered Primates resulted in its official endorse- need of urgent conservation measures.
    [Show full text]
  • Ogunjemite Inaugural 92
    THE FEDERAL UNIVERSITY OF TECHNOLOGY, AKURE MONKEYS AND APES: MAN IN ITS REMINISCENCE INAUGURAL LECTURE SERIES 92 Delivered by Professor Babafemi George Ogunjemite B.Sc. (Port-Harcourt), M. Tech., Ph.D. (Akure) Professor of Primate Community Ecology On Tuesday 21st November, 2017 Prologue: The eyes of all wait upon thee; thou give their meat in due season. Thou openest thine hand, and satisfied the desire of every living thing. Psalms 145:15 and 16 Professor Babafemi George Ogunjemite B.Sc. (Port-Harcourt), M. Tech., Ph.D. (Akure) Professor of Primate Community Ecology The Vice Chancellor The Deputy Vice-Chancellor (Academic) The Registrar Principal Officers of the University Deans and Directors Heads of Departments / Units Distinguished Members of Senate Other academic and Professional Colleagues Obas and Chiefs Distinguished Guests and Friends of the University Members of my Family Gentlemen of the Press Ladies and Gentlemen Great FUTARIANS It is a great privilege to present the 92nd Inaugural Lecture of this great University, the third from the Department of Ecotourism and Wildlife Management, and the fourth on the subject matter of Wildlife Management in the University. Previous issues by my worthy predecessors have emphasised the importance of wildlife resources to mankind, yet the problem confronting nature has not abated. Late Prof T. A. Afolayan spoke on the topic ''Man's inhumanity to nature; the over exploitation of wildlife resources''. Our attitude to wildlife did not change. Prof E. A. Agbelusi's topic was ''Wildlife resources; a national heritage''. We are yet to manage these resources on a sustainable basis to realise their importance for our national growth and development.
    [Show full text]
  • Further Declines of Threatened Primates in the Korup Project Area, South-West Cameroon
    Oryx Vol 36 No 3 July 2002 Further declines of threatened primates in the Korup Project Area, south-west Cameroon Matthias Waltert, Lien, Koen Faber and Michael Mu¨ hlenberg Abstract The diurnal primate community of the red-eared monkey decreased between the two survey Korup area of south-west Cameroon is rich in species years, whilst remaining constant or increasing in unlogged and high in endemism. Two years monitoring in the forest. The frequency of associations of guenon species Support Zone around Korup National Park have shown did not diCer between logged and unlogged study that, although all species of the original community are sites, but encounters of associations of all four guenon still present, Preuss’ red colobus and drill, which were species were only found in unlogged forest. We strongly considered to be threatened in the early 1990s, have recommend enforcement of anti-poaching activities declined further and are probably facing local extinction. inside the Korup National Park, and establishment of Densities of the crowned monkey also seem to have wildlife management in the Support Zone, as only a com- declined. Only mona and putty-nosed monkeys have bined strategy can successfully guarantee the persistence an expanded distribution, and densities that are within of the wildlife of the region. the range of those reported from previous studies in the region. Although hunting is the most important cause Keywords Cameroon, hunting, Korup National Park, of these declines, logging also appears to be having a participatory wildlife survey, primates, selective logging, detrimental eCect. In logged forest group densities of West Africa.
    [Show full text]
  • Population Status, Threats, and Conservation of Preuss's Red Colobus
    James Madison University JMU Scholarly Commons Masters Theses, 2020-current The Graduate School 8-2020 Population status, threats, and conservation of Preuss's red colobus (Piliocolobus preussi) and other diurnal primates in the Ndokbou forest, Littoral Region, Cameroon Ruth Bowers-Sword Follow this and additional works at: https://commons.lib.jmu.edu/masters202029 Part of the Biodiversity Commons, Environmental Studies Commons, Other Animal Sciences Commons, and the Other Ecology and Evolutionary Biology Commons Recommended Citation Bowers-Sword, Ruth, "Population status, threats, and conservation of Preuss's red colobus (Piliocolobus preussi) and other diurnal primates in the Ndokbou forest, Littoral Region, Cameroon" (2020). Masters Theses, 2020-current. 12. https://commons.lib.jmu.edu/masters202029/12 This Thesis is brought to you for free and open access by the The Graduate School at JMU Scholarly Commons. It has been accepted for inclusion in Masters Theses, 2020-current by an authorized administrator of JMU Scholarly Commons. For more information, please contact [email protected]. Population status, threats, and conservation of Preuss’s red colobus (Piliocolobus preussi) and other diurnal primates in the Ndokbou forest, Littoral Region Cameroon Ruth Bowers-Sword A thesis submitted to the Graduate Faculty of JAMES MADISON UNIVERSITY In Partial Fulfillment of the Requirements for the degree of Master of Science Department of Biology August 2020 FACULTY COMMITTEE: Committee Co-Chair: Dr. Roshna Wunderlich Committee Co-Chair: Dr. Joshua Linder Committee Members/ Readers: Dr. Dana Moseley Dedication To Emily Mettler, I will forever strive to carry the adventurous free spirit you embodied in everything you did. Unimaginably missed. ii Acknowledgements The completion of this project was made possible from funding and support provided by the James Madison University W.
    [Show full text]
  • Further Declines of Threatened Primates in the Korup Project Area, South-West Cameroon
    Oryx Vol 36 No 3 July 2002 Further declines of threatened primates in the Korup Project Area, south-west Cameroon Matthias Waltert, Lien, Koen Faber and Michael Mu¨ hlenberg Abstract The diurnal primate community of the red-eared monkey decreased between the two survey Korup area of south-west Cameroon is rich in species years, whilst remaining constant or increasing in unlogged and high in endemism. Two years monitoring in the forest. The frequency of associations of guenon species Support Zone around Korup National Park have shown did not diCer between logged and unlogged study that, although all species of the original community are sites, but encounters of associations of all four guenon still present, Preuss’ red colobus and drill, which were species were only found in unlogged forest. We strongly considered to be threatened in the early 1990s, have recommend enforcement of anti-poaching activities declined further and are probably facing local extinction. inside the Korup National Park, and establishment of Densities of the crowned monkey also seem to have wildlife management in the Support Zone, as only a com- declined. Only mona and putty-nosed monkeys have bined strategy can successfully guarantee the persistence an expanded distribution, and densities that are within of the wildlife of the region. the range of those reported from previous studies in the region. Although hunting is the most important cause Keywords Cameroon, hunting, Korup National Park, of these declines, logging also appears to be having a participatory wildlife survey, primates, selective logging, detrimental eCect. In logged forest group densities of West Africa.
    [Show full text]
  • 18 List of Contributors
    18 List of contributors Author: Ke*epa:\>oe ’ocJ*apcH&e>>oe IRepe0*e>4e =aJk4’ocJ*apcH&e>>Z6 =aJR>Z6 Oe>Hp Jens H. Kuhn, MD, ScD, MSc B4pJco:o(44 4 #4oHex>o:o(44 «BekHop» Research Scholar, Division of Tumor Virology, Ke*epa:\>o6 C:J0$Z Bo =a*2opJ&CLepe New England Primate Research Center (NEPRC), 1aV4HZ Apa&AoHpe$4He:e64#:a(oBo:JR4b Department of Microbiology and Molecular Genet- Qe:o&eka ;4>4cHepcH&o 1*pa&ooxpa>e>4b 4 ics, Harvard Medical School (HMS), 1 Pine Hill CoP4a:\>o(oPa2&4H4b (K’I= ’=O B# Drive, Southborough, MA 01772-9102, U.S.A.; «BekHop» PocBoHpe$>a*2opa) [Federal State Scien- Phone: þ1 (508) 786-3326; Fax: þ1 (508) 786- tific Institution – State Research Center for Virol- 3317; Email: fi[email protected]. Member, ogy and Biotechnology ‘‘Vector’’ of the Federal CBW Scientists Working Group, Center for Arms Service for Surveillance on Consumer Rights Pro- Control and Non-Proliferation, Washington, D.C., tection and Human Well-being of the Ministry of U.S.A.; Email: [email protected] Health and Social Development of Russia (FSRI SRCVB ‘‘Vector’’, Rospotrebnadzor)], Ko:ZPo&o Editor: [Koltsovo], 630559, =o&oc4$4pckab o$:acH\ [Novosibirsk Region], Pocc4b [Russia]; Phone: Charles H. Calisher, PhD þ7 (383) 3366173; Fax: þ7 (383) 3367409; Email: Professor, Arthropod-borne and Infectious Diseases [email protected] Laboratory, Department of Microbiology, Im- munology and Pathology, College of Veterinary M. Javad Aman, PhD Medicine, Colorado State University, Fort Collins, President and Chief Scientific Officer, Integrated CO 80523, U.S.A.; Phone: þ1 (970) 491-2987; BioTherapeutics Inc.
    [Show full text]
  • The World's 25 Most Endangered Primates 2012–2014
    Front cover photo: Male Tonkin snub-nosed monkey Rhinopithecus avunculus © Le Van Dung Primates in Peril: The World’s 25 Most Endangered Primates 2012–2014 Edited by Christoph Schwitzer, Russell A. Mittermeier, Anthony B. Rylands, Lucy A. Taylor, Federica Chiozza, Elizabeth A. Williamson, Janette Wallis and Fay E. Clark Illustrations by Stephen D. Nash IUCN SSC Primate Specialist Group (PSG) International Primatological Society (IPS) Conservation International (CI) Bristol Zoological Society (BZS) This publication was supported by the Margot Marsh Biodiversity Foundation and the Humane Society International. Published by: IUCN SSC Primate Specialist Group (PSG), International Primatological Society (IPS), Conservation International (CI), Bristol Zoological Society (BZS) Copyright: ©2014 Conservation International All rights reserved. No part of this report may be reproduced in any form or by any means without permission in writing from the publisher. Inquiries to the publisher should be directed to the following address: Russell A. Mittermeier, Chair, IUCN SSC Primate Specialist Group, Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA. Citation (report): Schwitzer, C., Mittermeier, R. A., Rylands, A. B., Taylor, L. A., Chiozza, F., Williamson, E. A., Wallis, J. and Clark, F. E. (eds.). 2014. Primates in Peril: The World’s 25 Most Endangered Primates 2012–2014. IUCN SSC Primate Specialist Group (PSG), International Primatological Society (IPS), Conservation International (CI), and Bristol Zoological Society, Arlington, VA. iv+87pp. Citation (species): Mbora, D. N. M. and Butynski, T. M. 2014. Tana River red colobus Piliocolobus rufomitratus (Peters, 1879). In: C. Schwitzer, R. A. Mittermeier, A. B. Rylands, L. A. Taylor, F. Chiozza, E. A. Williamson, J.
    [Show full text]
  • PRIMATE CONSERVATION the Journal of the IUCN/SSC Primate Specialist Group
    ISSN 0898-6207 PRIMATE CONSERVATION The Journal of the IUCN/SSC Primate Specialist Group Number 22 2007 Primate Conservation is produced and circulated courtesy of the Margot Marsh Biodiversity Founda- tion, the Center for Applied Biodiversity Science at Conservation International, the Los Angeles Zoo, and the Department of Anatomical Sciences of the State University of New York at Stony Brook. SPECIES SURVIVAL COMMISSION Primate Conservation The journal of the IUCN/SSC Primate Specialist Group Center for Applied Biodiversity Science Conservation International 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA ISSN 0898-6207 Abbreviation: Primate Conserv. DOI: 10.1896/ci.cabs.2007.primate.conserv.22 Editors Russell A. Mittermeier, Conservation International, Arlington, VA, USA Anthony B. Rylands, Center for Applied Biodiversity Science, Conservation International, Arlington, VA, USA IUCN/SSC Primate Specialist Group Chairman Russell A. Mittermeier, Conservation International, Arlington, VA, USA Deputy Chair Anthony B. Rylands, Center for Applied Biodiversity Science, Conservation International, Arlington, VA, USA Coordinator – Section on Great Apes Liz Williamson, Stirling University, Stirling, Scotland, UK Regional Coordinators – Neotropics Mesoamerica – Ernesto Rodríguez Luna, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Mexico Andean Countries – Erwin Palacios, Conservation International Colombia, Bogotá, Colombia, and Eckhard W. Heymann, Deutsches Primatenzentrum, Göttingen, Germany Brazil and the Guianas – M.
    [Show full text]
  • ORANGUTAN (Pongo) CARE MANUAL
    ORANGUTAN (Pongo) CARE MANUAL CREATED BY THE AZA Ape Taxon Advisory Group & Orangutan Species Survival Plan® Program IN ASSOCIATION WITH THE AZA Animal Welfare Committee Orangutan (Pongidae/Pongo) Care Manual Orangutan (Pongo) Care Manual Published by the Association of Zoos and Aquariums in association with the AZA Animal Welfare Committee Formal Citation: AZA Ape Taxon Advisory Group. (2017). Orangutan (Pongo) Care Manual. Silver Spring, MD: Association of Zoos and Aquariums. Original Completion Date: February 2015 Authors and Significant Contributors: Anne Nacey Maggioncalda, Duke University, (former) Primate researcher Barb Weber, Disney’s Animal Kingdom, Zoological Manager Barbara Lester, Houston Zoo, Primate Curator (retired) Beth Schaefer, Los Angeles Zoo, General Curator Carol Sodaro, Brookfield Zoo, Associate Curator of Carnivores, Chicago Zoological Society, Orangutan SSP Husbandry Advisor Christine M. Cassella, Cleveland Metroparks Zoo, (former) Graduate Research Associate Christine Mallar, Zoo Atlanta (former) Primate Keeper Cindy Cossaboon, Denver Zoo, Primate Keeper Craig Demitros, Brookfield Zoo, Associate Curator of Primates Danielle Fogarty, Brookfield Zoo, Primate Keeper Deb Schmidt, Ph.D., Saint Louis Zoo, Animal Nutritionist Dina Bredahl, Cheyenne Mountain Zoo, Animal Care Manager Elizabeth Frank, Milwaukee County Zoo, Primate Curator (retired) Eve Lyon, Audubon Zoo, Primate Curator (retired) Eve Watts, Audubon Zoo, Primate researcher (retired) Ian Singleton, Ph.D., Sumatran Orangutan Conservation Programme, Director Ingrid Porton, Saint Louis Zoo, Primate Curator (retired) Jan W. Rafert, Milwaukee County Zoo, Primate Curator (retired) Jane Anne Franklin, Louisville Zoo, Curator of Mammals and Animal Training Supervisor Jill Mellen, Ph.D., Disney’s Animal Kingdom, Education & Science Director (retired) Joe Smith, DVM, Fort Wayne Children’s Zoo, Director of Animal Programs Karen S.
    [Show full text]