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Current threats faced by Neotropical parrot populations

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Current threats faced by Neotropical parrot populations
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  Contents lists available at ScienceDirect Biological Conservation  journal homepage: www.elsevier.com/locate/biocon Current threats faced by Neotropical parrot populations I. Berkunsky a, ⁎ , P. Quillfeldt b , D.J. Brightsmith c , M.C. Abbud d , J.M.R.E. Aguilar e ,U. Alemán-Zelaya f  , R.M. Aramburú g , A. Arce Arias h , R. Balas McNab i , T.J.S. Balsby  j ,J.M. Barredo Barberena k , S.R. Beissinger l , M. Rosales m , K.S. Berg n , C.A. Bianchi n , E. Blanco o ,A. Bodrati p , C. Bonilla-Ruz q , E. Botero-Delgadillo r , S.B. Canavelli s , R. Caparroz t , R.E. Cepeda a ,O. Chassot f  , C. Cinta-Magallón q , K.L. Cockle bv , G. Daniele g , C.B. de Araujo u , A.E. de Barbosa v ,L.N. de Moura w , H. Del Castillo x , S. Díaz y , J.A. Díaz-Luque bu , L. Douglas aa ,A. Figueroa Rodríguez ab , R.A. García-Anleu i , J.D. Gilardi z , P.G. Grilli bt , J.C. Guix ac ,M. Hernández ad , A. Hernández-Muñoz ae , F. Hiraldo af  , E. Horstman ag , R. Ibarra Portillo ah ,J.P. Isacch ai , J.E. Jiménez aj , L. Joyner ak , M. Juarez g , F.P. Kacoliris g , V.T. Kanaan al ,L. Klemann-Júnior am , S.C. Latta an , A.T.K. Lee ao , A. Lesterhuis ap , M. Lezama-López aq , C. Lugarini v ,G. Marateo g , C.B. Marinelli a , J. Martínez ar , M.S. McReynolds as , C.R. Mejia Urbina at ,G. Monge-Arias f  , T.C. Monterrubio-Rico au , A.P. Nunes av , FdP Nunes aw , C. Olaciregui ax ,J. Ortega-Arguelles ay , E. Paci fi co af  , L. Pagano g , N. Politi az , G. Ponce-Santizo i ,H.O. Portillo Reyes ba , N.P. Prestes ar , F. Presti bb , K. Renton bc , G. Reyes-Macedo bd , E. Ringler be ,L. Rivera az , A. Rodríguez-Ferraro bx , A.M. Rojas-Valverde bf  , R.E. Rojas-Llanos bg ,Y.G. Rubio-Rocha bh , A.B.S. Saidenberg bi , A. Salinas-Melgoza bw , V. Sanz o , H.M. Schaefer bj ,P. Scherer-Neto bk , G.H.F. Seixas bl , P. Sera fi ni bm , L.F. Silveira bi , E.A.B. Sipinski d , M. Somenzari bm ,D. Susanibar bn , J.L. Tella af  , C. Torres-Sovero bo , C. Tro fi no-Falasco a , R. Vargas-Rodríguez bp ,L.D. Vázquez-Reyes bq , T.H. White Jr br , S. Williams bs , R. Zarza x , J.F. Masello b a  Instituto Multidisciplinario sobre Ecosistemas y Desarrollo Sustentable, CONICET   —  Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina b  Justus-Liebig-Universität Giessen, Department of Animal Ecology and Systematics, Giessen, Germany  c Texas A&M University, Schubot Exotic Bird Health Center, Department of Veterinary Pathobiology, College of Veterinary Medicine, USA d  Sociedade de Pesquisa em Vida Selvagem e Educaç ã  o Ambiental, Brazil e Universidade Federal de Sergipe, Brazil f   Programa Lapa Verde, Centro Cientí   fi co Tropical, Costa Rica g  Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Argentina h  Area de Conservación Pací   fi co Central ACOPAC, Programa de Vida Silvestre, Costa Rica i Wildlife Conservation Society, Guatemala  j  Aarhus University, Denmark k Grupo de Ecología y Conservación de Islas, A.C. (GECI), Mexico l University of California, Berkeley, Department of Environment Science, Policy&Management, Berkeley, USA m Universidad Nacional Federico Villarreal, Peru n Universidade Federal de Goiás, Brazil o  Instituto Venezolano de Investigaciones Cientí   fi cas, Venezuela p  Proyecto Selva de Pino Paraná, Argentina q Unidos por las Guacamayas A. C., Mexico r  SELVA: Investigación para la conservación en el Neotrópico, Colombia s  Instituto Nacional de Tecnología Agropecuaria, Argentina t University of Brasília, Brazil u Universidade Federal da Paraíba, Centro de Ciências Exatas e da Natureza, Brazil v Centro Nacional de Pesquisa e Conservaç ã  o de Aves Silvestres/ICMBio, Brazil w Universidade Federal do Pará, Instituto de Ciências Biológicas, Brazil x Guyra Paraguay, Paraguay  y University of Colorado, Department of Integrative Biology, USA z The World Parrot Trust, UK  aa  BirdsCaribbean, USA ab  Fundacion del Rio, Nicaragua ac Universitat de Barcelona, Spain ad  Sociedad Conservacionista Audubon de Venezuela, Venezuela ae Universidad de Sancti Spíritus ¨José Martí Pérez¨, Cuba http://dx.doi.org/10.1016/j.biocon.2017.08.016 Biological Conservation 214 (2017) 278–2870006-3207/ © 2017 Elsevier Ltd. All rights reserved. M R  af   Estación Biológica de Doñana CSIC, Spain ag  Fundación Pro-Bosque, Ecuador  ah Compañeros en Vuelo PIF-SV, El Salvador  ai  Instituto de Investigaciones Marinas y Costeras, CONICET   —  Universidad Nacional de Mar del Plata, Argentina aj University of North Texas, Biological Sciences, USA ak One Earth Conservation, White Plains, NY, USA al  Instituto Espaço Silvestre, Brazil am Universidade do Estado do Amazonas, Brazil an  National Aviary, Conservation and Field Research, Pittsburgh, PA, USA ao University of Cape Town, South Africa ap  Birdlife International, UK  aq  Paso Pací   fi co, Nicaragua ar Universidade de Passo Fundo, Brazil as  Biola University, USA at  Ministerio del Ambiente y los Recursos Naturales (MARENA), Nicaragua au Universidad Michoacana de San Nicolas de Hidalgo, Mexico av  Fundaç ã  o Universidade Federal de Mato Grosso do Sul, Brazil aw  AQUASIS, Brazil ax  Fundación Botánica y Zoológica de Barranquilla, Colombia ay  Provita, Venezuela az CIT Jujuy, CONICET   —  UNJu, Argentina ba  Fundación de Ciencias para el Estudio y la Conservación de la Biodiversidad (INCEBIO), Honduras bb UNESP, Instituto de Biociências de Botucatu, Brazil bc Universidad Nacional Autónoma de México, Estación Biología Chamela, Instituto de Biología, Mexico bd Vinculación Interdisciplinaria para el Desarrollo Ambiental y lo Social, Mexico be  Messerli Research Institute, University of Veterinary Medicine, Austria bf   Museo Noel Kemp  ff   Mercado, Bolivia bg Gobierno Autónomo Departamental de Santa Cruz, Bolivia bh Universidad Autónoma de Sinaloa, Mexico bi  Museu de Zoologia da Universidade de Sao Paulo (MZUSP), Brazil bj University of Freiburg, Evolutionary Biology and Animal Ecology, Germany  bk  Museu de História Natural Cap ã  o da Imbuia, Brazil bl  Fundaç ã  o Neotropica do Brasil, Brazil bm CEMAVE: Centro Nacional de Pesquisa para a Conservaç ã  o das Aves Silvestres, Brazil bn CORBIDI, Peru bo  Asociación Fauna Forever, Peru bp University of San Francisco Xavier de Chuquisaca, Bolivia bq Universidad Nacional Autónoma de México, Museo de Zoología, Facultad de Ciencias, Mexico br U.S. Fish and Wildlife Service, Puerto Rican Parrot Recovery Program, Puerto Rico bs  Echo, Parrots and People, Netherlands bt Cátedra de Ecología General y Recursos Naturales, Universidad Nacional Arturo Jauretche, Argentina bu  Fundación para la Investigación y Conservación de los Loros en Bolivia (CLB), Santa Cruz de la Sierra, Bolivia bv  Instituto de Bio y Geociencias del NOA, CONICET, Argentina bw  Laboratorio Nacional de Análisis y Síntesis Ecológica, Universidad Nacional Autónoma de México, Mexico bx  Depto. de Estudios Ambientales, Universidad Simón Bolívar, Caracas, Venezuela A R T I C L E I N F O  Keywords: ConservationEndangeredMacawParakeetPsittacidaePsittaciformes A B S T R A C T Psittaciformes (parrots, cockatoos) are among the most endangered birds, with 31% of Neotropical species underthreat. The drivers of this situation appear to be manifold and mainly of anthropogenic srcin. However, thisassessment is based on the last extensive consultation about the conservation situation of parrots carried out inthe 1990s. Given the rapid development of anthropogenic threats, updated data are needed to strategize con-servation actions. Using a population approach, we addressed this need through a wide-ranging consultationinvolving biologists, wildlife managers, government agencies and non-governmental conservation organizations.We gathered up-to-date information on threats a ff  ecting 192 populations of 96 Neotropical parrot species across21 countries. Moreover, we investigated associations among current threats and population trends. Many po-pulations were a ff  ected by multiple threats. Agriculture, Capture for the Pet Trade, Logging, each of them af-fected> 55% of the populations, suggesting a higher degree of risk than previously thought. In contrast toprevious studies at the species level, our study showed that the threat most closely associated with decreasingpopulation trends is now Capture for the local Pet Trade. Other threats associated with decreasing populationsinclude Small-holder Farming, Rural Population Pressure, Nest Destruction by Poachers, Agro-industry Grazing,Small-holder Grazing, and Capture for the international Pet Trade. Conservation actions have been implementedon< 20% of populations. Our results highlight the importance of a population-level approach in revealing theextent of threats to wild populations. It is critical to increase the scope of conservation actions to reduce thecapture of wild parrots for pets. ⁎ Corresponding author.  E-mail address:  berkunsk@exa.unicen.edu.ar (I. Berkunsky).  I. Berkunsky et al.  Biological Conservation 214 (2017) 278–287  279  1. Introduction The order Psittaciformes (parrots and cockatoos; hereafter parrots)is among the most threatened avian orders (i.e. Critically Endangered,Endangered, and Vulnerable sensu International Union forConservation of Nature, IUCN, 2012; Bennett and Owens, 1997,Butchart et al., 2004, Olah et al., 2016). Although  fi gures vary amongsources, the Parrot Action Plan and BirdLife International agree that 28to 29% of parrot species are threatened (Snyder et al., 2000; BirdLifeInternational, 2017). Moreover, the IUCN Red List considers that morethan half of all parrot species are currently experiencing populationdeclines (BirdLife International, 2017). The deterioration in conserva-tion status of parrots can be traced back to well before the 1980s(Pasquier, 1980; Beissinger and Snyder, 1992; Collar, 1996; Snyderet al., 2000; Wiley et al., 2004). The drivers of the current populationdeclines appear to be manifold, but include a mix of intrinsic biologicalfactors and external threats, the latter often of anthropogenic srcin(e.g., Wright et al., 2001; Bush et al., 2014; Martin et al., 2014). At thetime of its publication in 2000, the IUCN Parrot Action Plan (Snyderet al., 2000) highlighted that the main threats to parrots were habitatloss and degradation (70 species), capture of birds for the pet trade (30species), introduction of exotic species (15 species), persecution as al-leged crop pests (10 species), and disease (2 species). A similar scenariohas also been described in many studies of individual species, incountry-based action plans, and in recent comparative studies and re-views (Masello et al., 2010; Botero-Delgadillo and Páez, 2011; Schuncket al., 2011; Marsden and Royle, 2015; Olah et al., 2016). However, thelast extensive consultation with wild parrot experts and conservationorganizations from around the world was carried out in the late 1990sduring the preparation of the Parrot Action Plan. Since then, BirdlifeInternational has solicited input on threatened species, but informationfrom many parrot experts, including many of the current authors, hasnot made its way into recent status reviews. Given the rapid develop-ment of many anthropogenic threats, such as habitat loss, climatechange, and the spread of disease (Hansen et al., 2012, 2013; Regnardet al., 2015), information compiled over 15 years ago is now unlikely tobe valid, and studies based on present day  fi eld information are ur-gently needed.During the 25th International Ornithological Congress (22 − 28August 2010) in Campos do Jordão, Brazil, the Working GroupPsittaciformes (WGP) of the International Ornithologists' Union (http://psittaciformes.internationalornithology.org) was formed, comprisingspecialists in parrot research and conservation. One of the  fi rst objec-tives of this group was to update and increase our knowledge of thethreats a ff  ecting parrots. A regional approach was adopted to evaluatethreats facing Psittaciformes and a review of the conservation status of large Afrotropical parrots has been completed (Martin et al., 2014). Thepresent study evaluates current threats faced by Neotropical parrotsfollowing a population-based approach. We adopted this approach as 1)threats may vary considerably among populations of the same species(Rusello et al., 2010; Masello et al., 2011, 2015; Wenner et al., 2012),2) adopting populations as the unit for conservation may help identifyand reverse conservation problems while species are still common andensures that genetic variation is preserved (Lindenmayer and Burgman,2005), and 3) the population-level conservation approach is less af-fected by changes in organismic taxonomy. Consequently, we reporthere novel information on the severity and scope of threats a ff  ecting192 Neotropical parrot populations of 96 species across 21 countries.We also investigate underlying associations among current threats andpopulation trends, and relate them to conservation actions and prio-rities. 2. Methods  2.1. Data sources A questionnaire regarding the threats a ff  ecting parrot populationswas distributed among the co-authors, which include researchers whopublished in the  fi eld during last ten years, members of the WGP, andactive wildlife managers and conservationists from 33 non-govern-mental and governmental conservation organizations in the Neotropics.In order to facilitate the proper interpretation of our results, a tabulatedversion of the information delivered by each contributor is provided inTable A1 of  Appendix A.Information for each of the 192 parrot populations includes thefollowing: 1) identity and geographical area of expertise of the con-tributor, 2) the population's historic (before 1970), recent (1970 – 2000)and current (since ca. 2001) occurrence and abundance, 3) current(since ca. 2001) population trend, 4) current threats a ff  ecting parrotpopulations, and 5) current conservation and research activities in eachpopulation (Table A1 and Table A2 of  Appendix A). Occurrence andabundance information was classi fi ed in six categories: unknown, ab-sent, vagrant, occasional, fragmented populations, and widespread.Population trend information comprised four main categories: de-creasing, stable, increasing, and uncertain. The category  “ decreasing ” was split in four sub-categories: minor decrease if the population re-duction was under 30% since ca. 2001, moderate decrease (30 – 50%since ca. 2001), major decrease (50 – 80% since ca. 2001) and extremedecrease (> 80% since ca. 2001; Table A1 of  Appendix A; Fig. 1). To aid assessment of data quality, we provided details of data sources forpopulation trend and current threats in Table A2. Data provided by thecontributors to our study srcinated mostly in peer review papers butalso in reports, thesis, monographies, national action plans, and some  inlitt.  communications (references available in Table A2 of  Appendix A).To further help comparisons between our study and previous work, wealso provide the Red List Status, the IUCN-BirdLife International Po-pulation Trend, and information sources used for all species included inthis study (Table A2 of  Appendix A, BirdLife International, 2017). We de fi ned a population as a cluster of individuals with a highprobability of mating with each other compared to their probability of mating with a member of some other population (Pianka, 1994). Forinstance, the burrowing parrot  Cyanoliseus patagonus  colony located inEl Cóndor, north-eastern Patagonia was considered one population, theburrowing parrot in the Coquimbo region of Chile was considered an-other population, and the like (Table A1 of  Appendix A). Locality de-tails, country, and biological species identity for all our 192 Neotropical Fig. 1.  Current population trends for the 192 parrot populations studied across theNeotropical zoogeographical region. Di ff  erent levels of decrease are denoted by di ff  erentshades. Black: minor decrease, light grey: moderate decrease, dark grey: major decrease,and white: extreme decrease. The population trend for each of the 192 studied popula-tions is provided in Table A4 of  Appendix A.  I. Berkunsky et al.  Biological Conservation 214 (2017) 278–287  280  parrot populations are given in Table A1. In order to facilitate theidenti fi cation of speci fi c populations for each analysis in this study, weassigned a population number to each of the studied populations (seeTable A1, Table A4 and Table A5). In 25 cases, we investigated morethan one population per parrot species e.g. 4 populations of chestnut-fronted macaw  Ara severus , 3 of blue-headed parrot  Pionus menstruus , 4of white-eyed parakeet  Psittacara leucophthalmus  (for further detail seeTable A2 of  Appendix A).In our study, we used the relevant categories of the hierarchicalUni fi ed Classi fi cation of Direct Threats from the IUCN and theConservation Measures Partnership (CMP) (hereafter IUCN-CMP cate-gories; IUCN and CMP, 2012, Table 1). IUCN and CMP classify the threats in hierarchical levels (levels 1, 2 and 3; Table 1, IUCN and CMP, 2012). For further descriptions of the threat categories used here seeIUCN and CMP (2012). In all statistical analyses, we used the IUCN-CMP threat categories in Level 3, except for a few cases where onlyLevel 2 categories exist (Table 1; IUCN and CMP, 2012). To investigate general trends and to improve visualization and clarity, we used theIUCN-CMP threat categories in Level 1 (hereafter: major threat cate-gories) in some of the  fi gures in this study e.g. Fig. 2. Following Martin et al. (2014), and in order to account for speci fi c threats that may a ff  ectparrots (Snyder et al., 2000; Martin et al., 2014), some of the IUCN-CMP categories were further subdivided. The IUCN-CMP category ‘ Biological Resource Use (BirdLife International, 2017) ’  in Level 1 wassplit into three categories of: Hunting, Pet Trade, and Logging. TheIUCN-CMP category  ‘ Hunting&Collecting Terrestrial Animals (5.1)Intentional Use (5.1.1) ’  was split into four categories: Hunting forTraditional Ceremonies, Hunting for Food, Capture for Pet Trade: local,Capture for Pet Trade: international. Additionally, we used the morespeci fi c threat category  ‘ Road Construction ’  instead of the IUCN-CMPcategory  ‘ Roads&Railroads (4.1) ’  (IUCN and CMP, 2012), as all casesin our study corresponded to the construction of new roads and not toexisting roads (see Table A1). We also used a combined threat category ‘ Droughts/Deserti fi cation ’  to replace the IUCN-CMP categories  ‘ HabitatShifting&Alteration (11.1) ’  and  ‘ Droughts (11.2) ’ , which occurred asone combined intermingled threat in our study (see Table A1 of Appendix A). Following IUCN recommendations (IUCN, 2013), con- tributors indicated the timing, scope (i.e. proportion of the a ff  ectedpopulation) and severity (i.e. the overall decline) of the threats facingeach population in their geographical area of expertise (see raw in-formation in Table A1). We used ordinal categories to indicate thescope of the threat: a) minor, a ff  ects a negligible proportion of thepopulation, b)< 50%, a ff  ects the minority of the population, c)50 − 90%, a ff  ects the majority of the population, d)> 90%, a ff  ects thewhole population, and e) unknown (Table A1). We de fi ned the cate-gories of severity as follows: a) none, i.e. no decline, b) minimal,causing or likely to cause negligible declines, c)  fl uctuating, causing orlikely to cause  fl uctuations, d) slow decline, causing or likely to causerelatively slow, but signi fi cant, declines (< 20% over 10 years or threegenerations), e) fast decline, causing or likely to cause rapid declines(> 20% over 10 years or three generations), and f) unknown (TableA1). For timing we de fi ned the categories as follows: a) 0, only in thepast (and unlikely to return), b) 1, only in the past (no direct a ff  ect butlimiting), c) 2, now suspended but could come back in the long term, d)3, now suspended (could come back in the short term), e) 4, continuing,f) 5, only in the future (could happen in the short term), g) 6, only in thefuture (could happen in the long term), and h) uncertain or unknown(Table A1).Details of research and conservation activities in progress in thestudied populations and the priority level for those activities are alsoprovided in Table A1. Activities reported include: population mon-itoring (compilation of biodiversity inventories that include parrots,bird atlases, nest record card schemes, monitoring of breeding at-tempts), demographic and ecological research (habitat use, feedingecology, breeding biology), management (activities aimed at directlyboosting individual survival or breeding success, provision of nestboxes, planting of food trees, direct protection of nesting/roostingsites), population reinforcement, and species re-introduction (Table A1of  Appendix A).  2.2. Analysis We used Cohen's kappa coe ffi cient (K) to test for the degree of concordance between categories of scope and severity of threats(Cohen, 1960). Index values are: no concordance (lower than 0.2),discrete (between 0.2 and 0.4), moderate (between 0.4 and 0.6), sub-stantial (between 0.6 and 0.8) and almost perfect (higher than 0.8). Formost of the threats considered (72%), we found no concordance (TableA3). Moderate concordance was observed between scope and severityfor threats associated with Climate Change, Construction of dams, De-crease in the frequency of natural  fi res, and Small-scale logging (TableA3).To study the pattern of association among reported threats andpopulation trends, a multiple correspondence analysis (MCA) was car-ried out using the ca package in the R statistical environment (Nenadicand Greenacre, 2007, R Development Core Team, 2016). We included a total of 26 categorical variables (i.e. the reported population trend, andthe 25 speci fi c threat categories considered in this study; see Table A4and Table A5). For the MCA, the variable  “ population trend ”  had twocharacter states:  “ stable or increasing ”  and  “ decreasing ” . The valuesused for the remaining 25 threat variables corresponded to the scope of current (i.e. threats which timing value was 4) threats pooled into twocharacter states: 0 for scope values of 0 and 1; and 1 for scope values of 2 and 3 (Table A5 of  Appendix A). The outcome of this analysis is a setof coordinates indicating the association between the di ff  erent variablesand their character states (population trends and threat scope). Weplotted the low-dimensional Euclidean space to examine the associa-tions among the categories: highly associated variables result in closercoordinates (Table 1, Fig. 3). Here, we selected multiple correspon- dence analysis based on a simple Correspondence Analysis (CA;Benzécri, 1973) of the indicator matrix (setting lambda =  “ indicator ” ),and visualized the results using symmetric maps with the row and Fig. 2.  Major threat categories currently a ff  ecting the 192 parrotpopulations studied across the Neotropical zoogeographical re-gion. Data were classi fi ed according to the IUCN-CMP Level 1threat categories, except for category  ‘ Biological Resource Use ’ ,which was split in three categories i.e. hunting, pet trade, andlogging with the aim to account for some speci fi c threats found toa ff  ect parrots (Snyder et al., 2000; Martin et al., 2014). For rawdata see column  “ timing ” , value  “ 4 ”  in Table A1 of  Appendix A.  I. Berkunsky et al.  Biological Conservation 214 (2017) 278–287  282
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