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ORNITOLOGIA NEOTROPICAL An International Journal of Neotropical Ornithology published by the THE NEOTROPICAL ORNITHOLOGICAL SOCIETY Volume 23 2012 Supplement PROCEEDINGS OF THE IX NEOTROPICAL ORNITHOLOGICAL CONGRESS Cusco-Peru, 8-14 November 2011 Edited by Jack Clinton Eitniear Organized by The Neotropical Ornithological Society & Peruvian Ornithologists’ Union

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ornitologia neotropical

an international Journal of neotropical ornithology published by the

tHe neotropical ornitHological SocietY

Volume 23 2012 Supplement

PROCEEDINGS OF THE

IX NEOTROPICALORNITHOLOGICAL CONGRESS

Cusco-Peru, 8-14 November 2011

Edited by

Jack Clinton Eitniear

Organized by

The Neotropical Ornithological Society & Peruvian Ornithologists’ Union

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THE NEOTROPICAL ORNITHOLOGICAL SOCIETY (Founded 4 December 1987)

President: Jorge L. Pérez-Emán, Instituto de Zoología y Ecología Tropical, Universidad Centralde Venezuela, Apartado Postal 47058, Caracas 1041-A, Venezuela (E-mail:[email protected]).

President-elect: Juan Ignacio Areta, CICyTTP-CONICET, Materi y España, Diamante (3105),Entre Ríos, Argentina (E-mail: [email protected]).

Editor: André-A. Weller, Zoologisches Forschungsmuseum A. Koenig, Adenauerallee 160,53113 Bonn, Germany (E-mail: [email protected]).

Treasurer: Daniel Lebbin, Neotropical Ornithological Society, P.O. Box 185, The Plains, VA20198-0185, USA (E-mail: [email protected]); membership, financial matters.

Secretary: Jennifer Cahill, Centro de Biodiversidad y Genetica, Universidad Mayor de SanSimón, Calle Sucre y Parque La Torre, Casilla 538, Cochabamba, Bolivia (E-mail:[email protected]).

Board Members-at-Large: Daniel Cadena (Colombia), Cristián Estades (Chile), Eduardo E.Iñigo-Elías (México), Marcos Raposo (Brazil), Pedro Scherer Neto (Brazil), andUrsula Valdez (Peru).

Membership Secretary: Jack Clinton Eitniear, c/o Center for the Study of Tropical Birds, Inc.,218 Conway Drive, San Antonio, TX 78209-1716, USA (E-mail: [email protected]);missing issues, back issues.

Past Presidents: Mario A. Ramos, Washington, DC, USA; François Vuilleumier, New York, NY,USA; Patricia Escalante, México, D.F., México; Joseph M. Wunderle, Luquillo, PR,USA.

Past Editors: Karl-L. Schuchmann, Bonn, Germany (1987–1997); Raymond McNeil, Chateau-guay, Canada (1997–2008).

Patrons: Robert G. Goelet, New York, NY, USA; Luc Hoffmann, Le Sambuc, France.Book reviews: John G. Blake, Department of Wildlife Ecology and Conservation, 117 Newins-

Ziegler Hall, PO Box 110430, University of Florida, Gainesville, FL 32611, USA(E-mail: [email protected]).

Obituaries: James W. Wiley, Maryland Cooperative Fish & Wildlife Research Unit, University ofMaryland Eastern Shore, 1120 Trigg Hall, Princess Anne, MD 21853, USA.

Exchange of Ornitología Neotropical with other journals: Tom Webber, Florida Museum of NaturalHistory, Gainesville, FL 32611, USA (E-mail: [email protected]).

Editorial BoardLuiz dos Anjos, Brazil Olaf Jahn, Germany Angela Schmitz, GermanyJuan I. Areta, Argentina Eric Mellink, Mexico Karl-L. Schuchmann, GermanyIgor Berkunsky, Argentina Adolfo Navarro-S., Mexico Jean-Marc Thiollay, FranceRosendo M. Fraga, Argentina Marcos Raposo, Brazil Marcelo F. Vasconcelos, BrazilHarold F. Greeney, Ecuador John Rappole, USA Francisco Vilella, USASebastian K. Herzog, Bolivia W. Douglas Robinson, USA Graziele H. Volpato, BrazilDiego Hoffmann, Brazil Ernesto R. Inzunza, USA James W. Wiley, USA

Art for the cover page representing the Thorn-tailed Rayadito is by François Vuilleumier.

eDitorial StaFF/grUpo eDitorialEditor/Editor ..............................................................................................................Jack clinton eitniear

Spanish Editor/Editor de Espanol ...........................................................................................luis Sandova

Editorial Committee/ Comité de Editorial Steve Mcgehee Deanna K Dawson Juan ignacio areta Donald J. Brightsmith Maria a. echeverry Kent rylander gwen Brewer Juan cornejo Joe Wunderle

Typesetting/ Composición ..............................phil Wolfe graphic Design (www.pwgraphicdesign.com)

Printing/Impresión .........................................................prestige printing (www.prestigeprintingsa.com)

art for the cover page representing the thorn-tailed rayadito is by François Vuilleumier.

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NEOTROPICAL

ORNITHOLOGICAL

SOCIETY

Brooklyn, January 20, 2011

Dr. Paul B. Hamel

[email protected]

US Forest Service

Dr. David Diaz

[email protected]

Aves & Conservación/BirdLife en Ecuador

Dr. David Caro

[email protected]

Fundación ProAves

Dr. Tino Aucca

[email protected]

Asociacion de Ecosistemas Andinos (ECOAN)

Dr. Pancho Sornoza

[email protected]

Fundación Jocotoco

Dear Drs. Hamel, Diaz, Caro, Aucca, Sornoza,

We are pleased to inform you that your proposal entitled “Conservation biology of Cerulean

Warbler, a vulnerable migratory species dependent on lands managed for coffee, coal and forest products”

has been accepted as symposium as part of the IXth

Neotropical Ornithological Congress (NOC) in Cusco,

Perú, November 8-14, 2011. We believe that this topic will be of considerable interest to Congress

participants.

We wish to emphasize to all symposia conveners that we encourage them to make a

substantial effort to synthesize and summarize the state of the art or knowledge in the topic or field of their

symposium. Conveners are expected to summarize the potential recommendations, problem areas, or

patterns, etc. arising from their symposium’s presentations. Without such a summary and synthesis, a

symposium will be indistinguishable from a regular contributed paper session. A symposium should be more

than just a collection of presentations on similar topics or taxa and organizers are strongly encouraged to

coach or direct their participants to adhere to themes, issues, or problems. The more guidance and direction

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the conveners provide to their speakers prior to the symposium the more effective the symposium is likely to

be.

The full texts of Symposium presentations (excluding introductory and concluding remarks), properly

peer-reviewed and delivered on due time, will be published in the Proceedings of the IXth

Neotropical

Ornithological Congress, as a supplement to the respective Volume of Ornitología Neotropical, the Quarterly

Journal of the Neotropical Ornithological Society. A maximum of approximately 8-15 printed pages

(including tables, figures, and references) will be devoted to each accepted symposium paper. Symposium

conveners are responsible for having the five papers of their respective symposium peer-reviewed by them

and independent reviewers, and to edit them according to Ornitología Neotropical format (see attached

instructions). The five paper package (3 printed copies and a CD), accompanied with a cover letter (that

includes the name of the symposium and the titles of the papers), must be sent by the conveners by mail or

email to Dr. Jack Eitniear (addresses will be provided soon), the Editor for the NOC Proceedings, or

delivered to him at the registration desk of the NOC in Cusco, not later than November 8, 2011.

We appreciate your efforts in organizing this symposium for the Congress and wish you all the best as

editors, reviewers, and leaders of your symposium. Your efforts have the potential to advance Neotropical

ornithology and will contribute to the success of the Congress. We wish you well in this endeavor.

Sincerely,

Jose G. Tello Scientific Program Co-chair

[email protected]

Department of Biology

Long Island University

Brooklyn, NY 11201

U.S.A.

Thomas Valqui Scientific Program Co-chair

[email protected]

Secretary of the Unión de Ornitólogos del Perú (UNOP)

Calle Santa Rita 105 Of. 202

Urb. Huertos de San Antonio, Surco

PERÚ

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Symposium S1 –

Conservation biology of Cerulean Warbler, a vulnerable

migratory species dependent on lands managed for coffee, coal

and forest products

Convener Paul B. Hamel

Co-conveners David Diaz, David Caro, Tino Aucca, Pancho Sornoza

Symposium Synopsis

Since 2001, Cerulean Warbler (Dendroica cerulea) has sparked intense research and

conservation action as well as considerable public policy attention. This IUCN-listed Vulnerable

bird is a potential flagship species for conservation of Neotropical resident and Nearctic

migratory birds in the northern Andes of Venezuela, Colombia, Ecuador, Peru, and potentially

Bolivia. Activities coordinated through the Cerulean Warbler Technical Group demonstrate the

opportunities, difficulties, frustrations, failures, and remarkable successes made possible by

collaborative partnerships. The species will not persist without coordinated management,

conservation, monitoring, and research activities throughout its extensive range. As such the

biology of the bird, and the working of the conservation partnership surrounding it, are a model

for other, ongoing or future international partnerships. The symposium is will review the

structure, progress, and accomplishments of the Cerulean Warbler Technical Group over the

period 2001-2011.

The purpose of the symposium is to document the increases in our knowledge of

Cerulean Warbler in this period throughout the range of the species as an example for others to

benefit from our successes and avoid our failures. Cerulean Warbler Technical Group has four

subcommittees, devoted to Breeding Season Research, Breeding Season Monitoring, Breeding

Season Conservation, and Nonbreeding Season Issues. Immense progress has been achieved in

each of these areas since 2001. Our collective efforts have produced strategically important

policy assistance to the U.S. Fish and Wildlife Service and to IUCN in status determination of

the species. Framework conservation plans for the nonbreeding season and for the population

rangewide have been developed and promulgated. Especially in regard to conservation

implementation and understanding of migration, however, the achievements do not yet meet the

needs for the birds. Linking the understanding of the biology of the birds as outlined by research

accomplishments to needed conservation implementation through a monitoring feedback process

is a vital unmet need. The goal of the symposium is to inform our Neotropical Ornithological

Congress audience of the biology of the birds in a way that conservation action will be made

more likely to succeed and to demonstrate the passage of energy within the group from a

primarily information gathering to a primarily conservation implementation function. We seek

the input and consultation of the NOC audience to clarify our thinking about the most efficacious

ways to meet the needs we presently understand.

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ornitologia neotropical 23: 275–281, 2012© the neotropical ornithological Society

CERULEAN WARBLER TECHNICAL GROUP: COORDINATING INTERNATIONAL RESEARCH AND CONSERVATION

Deanna K. Dawson1, T. Bently Wigley2, & Patrick D. Keyser3

1 USGS Patuxent Wildlife Research Center, Laurel, MD, USA. E-mail: [email protected] 2 National Council for Air and Stream Improvement, Inc., Clemson, SC, USA.

3 Department of Forestry, Wildlife and Fisheries, University of Tennessee, Knoxville, TN, USA.

Resumen. – El Grupo Técnico de la Reinita Cerúlea: coordinación de investigación y conservación internacional. – La conservación eficaz de especies de preocupación requiere del intercambio y colabo-ración entre los conservacionistas y actores locales. El Grupo Técnico de la Reinita Cerúlea (GTRC) es un consorcio de biólogos y administradores de agencias de gobierno, organizaciones no gubernamentales, per-sonas del ámbito académico e industrial, que están dedicados a encontrar soluciones pro-activas, basadas en la ciencia para la conservación de la Reinita Cerúlea (Setophaga cerulea). Constituido en los Estados Unidos en 2001, el alcance del GTRC pronto se amplió para tratar la ecología y conservación de la especie tanto en su área reproductiva como no-reproductiva, conjuntamente con biólogos de Sur y Centro América. En 2004, el GTRC hace el lanzamiento de la Iniciativa de Conservación de la Reinita Cerúlea, un conjunto de actividades que tienen como objetivo abordar las necesidades de información y conservación de la es-pecie. Esto incluye (1) estudios para evaluar la respuesta de la Reinita Cerúlea a las prácticas de manejo forestal en el núcleo de su área de reproducción y la identificación de tierras sujeto de minería que podrían ser reforestadas en beneficio de la especie, (2) estudios de ecología y demografía en el área invernal e (3) investigación de la distribución de la Reinita Cerúlea en las áreas reproductivas y de invernada además durante la migración. Se ha completado un amplio plan de acción para la conservación, junto con un plan de conservación del rango de distribución no-reproductivo más detallado. El GTRC y sus socios ahora avanzan con actividades de conservación en los sitios, mientras se abordan necesidades de información todavía no satisfechas.

Abstract. – Effective conservation for species of concern requires interchange and collaboration among conservationists and stakeholders. The Cerulean Warbler Technical Group (CWTG) is a consortium of biolo-gists and managers from government agencies, non-governmental organizations, academia, and industry, who are dedicated to finding pro-active, science-based solutions for conservation of the Cerulean Warbler (Setophaga cerulea). Formed in the United States in 2001, CWTG’s scope soon broadened to address the species’ ecology and conservation on both the breeding and non-breeding ranges, in partnership with biologists from South and Central America. In 2004, CWTG launched the Cerulean Warbler Conservation Initiative, a set of activities aimed at addressing information and conservation needs for the species. These include (1) studies in the core breeding range to assess Cerulean Warbler response to forest management practices and to identify mined lands that could be reforested to benefit the species, (2) ecological and de-mographic studies on the winter range, and (3) surveys of Cerulean Warbler distribution on the breeding and winter ranges and during migration. A rangewide conservation action plan has been completed, along with a more detailed conservation plan for the non-breeding range. CWTG and partners now move forward with on-the-ground conservation, while still addressing unmet information needs.

Key Words: Cerulean Warbler, Setophaga cerulea, Cerulean Warbler Technical Group, Appalachians, north-ern Andes, international conservation, conservation partnerships.

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groups, seeking extra protection for the species and its habitats, petitioned the U.S. Fish and Wildlife Service (USFWS), the federal agency charged with managing and conserving migratory birds in the U.S., to list cerulean Warbler as threatened under the endangered Species act. USFWS ruled in December 2006 that listing the species was not warranted (U.S. Fish and Wildlife Service 2006), but has designated cerulean Warbler as a Focal Species, to receive priority emphasis and attention; the agency also committed to support collaborative international conservation efforts for the species. in canada, cerulean Warbler is listed as threatened under the federal Species at Risk Act, but was reclassified as Endangered in november 2010 by the committee on the Status of endangered Wildlife in canada (coSeWic 2010). cerulean Warbler is listed as Vulnerable by the international Union for conservation of nature and natural resources (Birdlife international 2008), but has no legal protection in countries in the non-breeding range.

cerUlean WarBler tecHnical groUp

the cerulean Warbler technical group (cWtg) is a consortium of biologists and managers from government agencies, non-governmental organizations, academia, and industry, who are dedicated to finding pro-active, science-based solutions for conservation of the cerulean Warbler. Formed in the U.S. in 2001, cWtg’s scope soon broadened to address the species’ ecology and conservation during all phases of its annual cycle, in partnership with biologists from South and central america. The first Cerulean Warbler ‘summit’ was held in Shepherdstown, West Virginia, in December 2002. a steering committee was appointed, as were subcommittees to address issues and foster research, monitoring, or conservation activities on the breeding and non-breeding

introDUction

persistent and widespread declines in breeding populations of the cerulean Warbler (Setophaga cerulea) have made it a species of conservation concern (rich et al. 2004). the species is a neotropical migrant, nesting in eastern north america, and wintering in the andean region of northwestern South america (primarily colombia, Venezuela, and ecuador). population trends estimated from data from the north american Breeding Bird Survey (BBS) show a decline across the breeding range of 3% per year from 1966, when the BBS was started, through 2009 (Sauer et al. 2011), although the trend has leveled somewhat (-1.22% per year) since 2000. population trends have declined similarly in the core breeding range in the appalachian Mountains Bird conservation region (ohio Hills and northern cumberland plateau physiographic areas; see http://www.partnersinflight.org/bcps/pifplans.htm).

Habitat loss and alteration are considered to be important limiting factors for the species. on the breeding range, cerulean Warblers use mature deciduous forests, most commonly in uplands but also along rivers, with large trees and a broken, structurally diverse canopy, in predominantly forested landscapes. Much of the core breeding range is managed as commercial forestland, and is underlain by coal deposits; mining by mountaintop removal/valley fill is of particular concern in some locations. on the winter range, cerulean Warblers occupy a relatively narrow band of elevation (~500-2,500 m) that roughly coincides with the prime growing zone for coffee; cattle grazing and other agricultural land uses are also prevalent in this region (guhl 2008). there, they use broad-leaved evergreen forests and agroforestry systems, especially coffee grown under shade.

cerulean Warblers are protected in the United States under the Migratory Bird treaty act. in 2000, a coalition of conservation

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ranges; the subcommittee that focuses on the non-breeding range became known as ‘el grupo cerúleo’. participation in cWtg and its subcommittees has always been voluntary and flexible, but usually a core group of individuals is involved, with others drawn in as interested or needed to assist with specific tasks.

From its inception, cWtg has included both technical experts and stakeholders, so they could work collaboratively to identify and implement conservation actions. indeed, wildlife biologists from the forest products industry, a major land owner in the core breeding range, were among cWtg’s founding members (Hamel et al. 2004). cWtg also has reached out to the coal industry, hosting a meeting in charleston, West Virginia, in March 2006, to learn about their operations and economic constraints, to provide them with background information on cerulean Warblers, and to discuss how they could participate in cerulean Warbler conservation. More recently, cWtg has sought to engage the South american coffee industry in conservation of cerulean Warblers and associated resident bird species of concern.

cerUlean WarBler conSerVation initiatiVe

in 2004, cWtg launched the cerulean Warbler conservation initiative (cWci). the initial focus was to address rangewide information needs deemed critical to devise an effective conservation strategy for the species. it was recognized that certain forest management practices likely are detrimental to cerulean Warblers, while others might enhance habitat for the species. existing information on cerulean Warbler habitat associations was synthesized to develop preliminary guidelines for managing forests to improve their suitability for the species (Hamel 2006, Hamel & rosenberg 2007). Surveys were conducted on private lands in the core breeding range, especially those

owned or managed by the forest industry, to fill gaps in data on cerulean Warbler distribution collected in the earlier cerulean Warbler atlas project (rosenberg et al. 2000). in addition, a research experiment was conducted to assess response of cerulean Warblers and associated bird species of concern to commonly applied forest management practices, replicated at one or more study areas in Kentucky, ohio, tennessee, and West Virginia (larkin et al. 2012). this research was complemented by other studies of cerulean Warbler response to forest management in arkansas (Hamel et al. 2010), indiana (register & islam 2008, islam et al. 2012), pennsylvania (rodewald 2004, Stoleson 2004), and West Virginia (Wood et al. 2005). Research results are being used to refine the preliminary forest management guidelines to produce Best Management practices for improving forest structure for cerulean Warblers.

cerulean Warblers are generally associated with ridges in the core breeding range (rosenberg et al. 2000, Weakland & Wood 2005); thus, coal mining by mountaintop removal can have significant negative impacts through direct destruction of breeding habitat and degradation of the adjacent forest by creating extensive ‘hard’ edges (Buehler et al. 2006, Wood et al. 2006). the cWci advanced long-term habitat restoration on mined lands by using geospatial models and maps of cerulean Warbler distribution and abundance (Shumar 2009) to identify and prioritize areas that could be reforested to benefit the species (Wood et al. 2010), in partnership with the appalachian regional reforestation initiative (Smith et al. 2012).

on the non-breeding range, a workshop, held in Quito, ecuador, in november 2005, brought together cerulean Warbler biologists and geographic information System experts from north america, colombia, Venezuela, ecuador, peru, and Bolivia to evaluate available digital geospatial data, and to integrate data

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across the winter range. cerulean Warbler locations, compiled from documented observations and museum specimens, and physical, climatic, and land cover variables were used to develop a predictive model of their winter distribution (Barker et al. 2006). Field surveys were conducted to confirm historic locations and find new ones, and to test the preliminary distribution model. the model was then refined, in order to identify regions and habitats likely to be important for the species, and thus focus on-the-ground conservation efforts (colorado et al. 2008, Fundación proaves et al. 2010). in a parallel effort, spring surveys were carried out in central america and Mexico to identify sites and habitats used by cerulean Warblers on their northward migration (Welton et al. 2012). a preliminary model of potential stopover habitat was generated, and awaits further testing and refinement. Ecological and demographic studies of overwintering cerulean Warblers were conducted in colombia (colorado 2011, colorado et al. 2012, Muñoz & colorado 2012), complementing earlier and concurrent research in Venezuela (Jones et al. 2000, Bakermans et al. 2009). these studies highlight the importance to cerulean Warblers of shade-grown coffee plantations, indicating that partnering with coffee growers or the coffee industry holds promise as a conservation strategy for the winter range.

the surveys and research component of the cWci were funded largely by a series of challenge grants from the national Fish and Wildlife Foundation, matched by non-federal in-kind and monetary contributions from participating institutions, the forest industry, non-governmental organizations, and individuals. additional funding from the USDa Forest Service (international programs) and The Nature Conservancy supported field investigations on the winter range.

While the various survey and research activities were underway, initial on-the-ground conservation actions were undertaken

(Santander et al. 2012, Skolnik et al. 2012), including establishment, by Fundación proaves and american Bird conservancy, of a cerulean Warbler reserve in Colombia, the first South American reserve established to benefit a bird species that breeds in north america. cWtg also worked to formulate a conservation strategy and lay the groundwork for future conservation actions. the second international cerulean Warbler summit was convened in Morgantown, West Virginia, in February 2007, at which participants set a desired goal of doubling the current population, and identified conservation actions needed to achieve that goal. the resulting rangewide conservation action plan (U.S. Fish and Wildlife Service 2007) outlines general conservation actions to address information gaps and threats to habitat during both the breeding and non-breeding periods, and to identify and address non-habitat limiting factors.

in october 2008, cWtg met jointly with the golden-winged Warbler (Vermivora chrysoptera) Working group in Bogotá and San Vicente de chucurí, colombia, at a workshop on conservation planning for migratory and resident birds in the northern andes. presentations at this combined international summit, the third to focus on cerulean Warbler and the second on golden-winged Warbler, provided updates on their non-breeding distribution and ecology, and on ongoing research and conservation activities. Background information was presented on the history and status of coffee and cacao production in colombia, and opportunities for collaborative conservation with industry, growers, and local communities were discussed. objectives and possible actions for on-the-ground conservation were identified, and remaining information needs were prioritized. a conservation plan for cerulean Warbler on its non-breeding range was completed in august 2010 (Fundación proaves et al. 2010); this effort was led by Fundación proaves and

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american Bird conservancy, with considerable input and assistance from cWtg.

DiScUSSion

our accomplishments over the past decade are considerable, and have greatly expanded understanding of cerulean Warbler distribution and ecology (Hamel et al. 2004). information gaps remain, particularly the routes and stopover habitats used during migration, but the time has arrived for cWtg to pass the baton to the conservation community. an important element of a comprehensive conservation program is to protect sites that host significant populations of Cerulean Warblers or receive high or regular use. However, conservation efforts based solely on land acquisition and preservation are no longer realistic, and likely would not be effective for this species. Habitat manipulations (e.g., thinning, planting) may be required to enhance forests in appalachia or agroforestry systems in the Andes to benefit Cerulean Warblers; because the economic productivity of these lands must be sustained, partnering with land owners or managers is a necessity. it is critical, however, that on-the-ground conservation be conducted in an adaptive framework that includes monitoring the response of cerulean Warblers and other species of concern, so that management actions can be tailored to achieve the desired outcome and to increase our knowledge of the species’ ecology and habitat requirements. in this way, the research and conservation communities will continue to collaborate in conservation efforts to provide for the cerulean Warbler and increase its numbers.

reFerenceS

Bakermans, M. H., a. c. Vitz, a. D. rodewald, & c. g. rengifo. 2009. Migratory songbird use of shade coffee in the Venezuelan andes with

implications for conservation of cerulean Warbler. Biol. conserv. 142: 2476–2483.

Barker, S., S. Benítez, J. Baldy, D. cisneros Heredia, g. colorado Zuluaga, F. cuesta, i. Davidson, D. Díaz, a. ganzenmueller, S. garcía, M. K. girvan, e. guevara, p. Hamel, a. B. Hennessey, o. l. Hernández, S. Herzog, D. Mehlman, M. i. Moreno, e. ozdenerol, p. ramoni-perazzi, M. romero, D. romo, p. Salaman, t. Santander, c. tovar, M. Welton, t. Will, c. pedraza, & g. galindo. 2006. Modeling the South american range of the cerulean Warbler. In proceedings of the 2006 eSri international User conference, San Diego, california, USa. available at proceedings.esri.com/library/userconf/proc06/papers/papers/pap_1656.pdf

Birdlife international. 2008. Dendroica cerulea. In iUcn 2011. iUcn red list of threatened Species (version 2011.2). available at www.iucnredlist.org/ [accessed 20 December 2011]

Buehler, D. a., M. J. Welton, & t. a. Beachy. 2006. predicting cerulean Warbler habitat use in the cumberland Mountains of tennessee. J. Wildl. Manag.: 1763–1769.

chesser, r. t., r. c. Banks, F. K. Barker, c. cicero, J. l. Dunn, a. W. Kratter, i. J. lovette, p. c. rasmussen, J. V. remsen, Jr., J. D. rising, D. F. Stotz, & K. Winker. 2011. Fifty-second supplement to the american ornithologists’ Union Check-list of North American Birds. auk 128: 600–613.

colorado, g. J. 2011. ecology and conservation of neotropical-nearctic migratory birds and mixed-species flocks in the Andes. Ph.D. diss. ohio State Univ., columbus, ohio, USa. available at http://etd.ohiolink.edu/send-pdf.cgi/colorado%20gabriel%20J.pdf?osu1291646331/ [accessed 25 January 2012]

colorado, g., p. Hamel, a. rodewald, & W. thogmartin. 2008. el grupo cerúleo: collaboration to assess nonbreeding range of cerulean Warbler in South america. ornitol. neotrop. 19(Suppl.): 521–529.

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colorado, g. J., p. B. Hamel, a. D. rodewald, & D. Mehlman. 2012. advancing our understanding of the non-breeding distribution of cerulean Warbler (Setophaga cerulea) in the andes. ornitol. neotrop. 23(Suppl.): 309–317.

coSeWic. 2010. coSeWic assessment and status report on the cerulean Warbler Dendroica cerulea in canada. committee on the Status of endangered Wildlife in canada, ottawa, canada. available at http:// www.sararegistry.gc.ca/status/status_e.cfm/ [accessed 21 February 2012]

Fundación proaves, american Bird conservancy & el grupo cerúleo. 2010. conservation plan for the cerulean Warbler on its nonbreeding range - plan de conservación para la reinita cerúlea sobre su rango no reproductivo. conserv. colomb 12: 1–62.

guhl, a. 2008. café y cambio de paisaje en colombia, 1970–2005. Fondo editorial Universidad eaFit, Banco de la república, Medellín, colombia.

Hamel, p. B. 2006. adaptive forest management to improve habitats for cerulean Warbler. proceedings of Society of american Forests national convention.

Hamel, p. B., D. K. Dawson, & p. D. Keyser. 2004. How we can learn more about the cerulean Warbler (Dendroica cerulea). auk 121: 7–14.

Hamel, p. B., & K. V. rosenberg. 2007. Developing management guidelines for cerulean Warbler breeding habitat. pp. 264–374 in Buckley, D. S., & W. r. clatterbuck (eds). proceedings of the 15th central hardwood forest conference, USDa Forest Service gen. tech. rep. SrS-101.

Hamel, p. B., M. Staten, r. Wishard, & c. g. Smith, iii. 2010. cerulean Warbler response to silvicultural manipulations on managed forestland in Desha co., arkansas, third year results. pp. 475–479 in Stanturf, J. a. (ed.). proceedings of the 14th biennial southern silvicultural research conference. USDa Forest Service gen. tech. rep. SrS-121.

islam, K., J. Wagner, r. Dibala, M. Macneil, K. Kaminski, & l. (p.) Young. 2012. cerulean

Warbler (Setophaga cerulea) response to changes in forest structure in indiana. ornitol. neotrop. 23(suppl.): 335–341.

Jones, J., p. ramoni-perazzi, e. H. carruthers, & r. J. robertson. 2000. Sociality and foraging behavior of the cerulean Warbler in Venezuelan shade coffee plantations. condor 102: 958–962.

larkin, J. l., p. B. Wood, t. J. Boves, J. Sheehan, D. a. Buehler, p. D. Keyser, a. D. rodewald, t. a. Beachy, M. H. Bakermans, a. evans, g. a. george, M. e. McDermott, F. l. newell, K. a. perkins, M. White, & t. B. Wigley. 2012. Breeding season concerns and response to forest management: can forest management produce more breeding birds? ornitol. neotrop. 23(Suppl.): 287–290.

Muñoz, J. M., & g. J. colorado. 2012. Foraging ecology of the cerulean Warbler (Setophaga cerulea) in andean agroforestry ecosystems. ornitol. neotrop. 23(suppl.): 359–366.

register, S. M., & K. islam. 2008. effects of silvicultural treatments on cerulean Warbler (Dendroica cerulea) abundance in southern indiana. Forest ecol. Manag. 255: 3502–3505.

rich, t. D., c. J. Beardmore, H. Berlanga, p. J. Blancher, M. S. W. Bradstreet, g. S. Butcher, D. W. Demarest, e. H. Dunn, W. c. Hunter, e. e. iñigo-elias, J. a. Kennedy, a. M. Martell, a. o. panjabi, D. n. pashley, K. V. rosenberg, c. M. rustay, J. S. Wendt, & t. c. Will. 2004. partners in Flight north american landbird conservation plan. cornell lab of ornithology, ithaca, new York, USa.

rodewald, a. D. 2004. landscape and local influences of forest management on Cerulean Warblers in pennsylvania. pp. 472–477 in Yaussy, D. a., D. M. Hix, r. p. long, & p. c. goebel (eds). proceedings of the 14th central hardwood forest conference. USDa Forest Service gen. tech. rep. ne-316.

rosenberg, K. V., S. e. Barker, & r. W. rohrbaugh. 2000. an atlas of cerulean Warbler populations: 1997–2000 breeding seasons. Final report submitted to U.S. Fish and Wildlife Service. cornell lab of ornithology, ithaca, nY, USa.

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Santander, t., a. Soria, & e. a. guevara. 2012. conservando el hábitat invernal de la reinita cerúlea (Setophaga cerulea) en ecuador. ornitol. neotrop. 23(suppl.): 343–350.

Sauer, J. r., J. e. Hines, J. e. Fallon, K. l. pardieck, D. J. Ziolkowski, Jr., & W. a. link. 2011. the north american Breeding Bird Survey, results and analysis 1966 – 2009 (version 3.23.2011). USgS patuxent Wildlife research center, laurel, Maryland, USa. available at http://www.mbr-pwrc.usgs.gov/bbs/bbs.html/ [accessed 20 December 2011]

Shumar, M. B. 2009. predictive modeling techniques with application to the cerulean Warbler (Dendroica cerulea) in the appalachian Mountains Bird conservation region. M.Sc. thesis, West Virginia Univ., Morgantown, West Virginia, USa. available at http://wvuscholar.wvu.edu:8881

Skolnik, B., D. Wiedenfeld, r. Dettmers, c. aucca, l. Daza, H. Valle, F. Sornoza, J. robayo, D. Diaz, J. Fitzgerald, D. lebbin, & p. B. Hamel. 2012. conservation planning and accomplishments for protection of cerulean Warbler (Setophaga cerulea) nonbreeding habitat. ornitol. neotrop. 23(Suppl.): 319–329.

Smith, B. W., J. Botero, J. l. larkin, a. D. rodewald, p. B. Wood, p. n. angel, & S. e. eggerud. 2012. integrating conservation management, species protection and economic viability into sustainable land use practices for the cerulean Warbler (Setophaga cerulea) in the appalachian and northern andes Mountains. ornitol. neotrop. 23(suppl.): 329–334.

Stoleson, S. H. 2004. cerulean Warbler habitat use in an oak-northern hardwoods transition zone: implications for management. In Yaussy, D. a.,

D. M. Hix, r. p. long, & p. c. goebel (eds). proceedings of the 14th central hardwood forest conference. USDa Forest Service gen. tech. rep. ne-316.

U.S. Fish and Wildlife Service. 2006. endangered and threatened Wildlife and plants; 12-month finding on a petition to list the Cerulean Warbler (Dendroica cerulea) as threatened with critical Habitat. Fed. regist. 71: 70717–70733.

U.S. Fish and Wildlife Service. 2007. a conservation action plan for the cerulean Warbler (Dendroica cerulea). available at http://www.fws.gov/migratorybirds/currentBirdissues/Management/ FocalSpecies/plans/ceruleanWarbler.pdf [accessed 20 December 2011]

Weakland, c. a., & p. B. Wood. 2005. cerulean warbler (Dendroica cerulea) microhabitat and landscape-level habitat characteristics in southern West Virginia. auk 122: 497–508.

Welton, M. J., D. l. anderson, g. J. colorado, p. B. Hamel, & D. calderón-F. 2012. cerulean Warbler (Setophaga cerulea) spring migration stopover in northern Middle america. ornitol. neotrop. 23(suppl.): 291–307.

Wood, p. B., J. p. Duguay, & J. V. nichols. 2005. cerulean warbler use of regenerated clearcut and two-age harvests. Wildl. Soc. Bull. 33: 851–858.

Wood, p. B., S. B. Bosworth, & r. Dettmers. 2006. cerulean Warbler abundance and occurrence relative to large scale edge and habitat characteristics. condor 108: 154–165.

Wood, p. B., M. e. McDermott, & M. B. Shumar. 2010. cerulean Warbler conservation initiative 4: identify and prioritize mined lands for reforestation. Final report to national council for air and Stream improvement.

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BREEDING SEASON CONCERNS AND RESPONSE TO fOREST MANAGEMENT: CAN fOREST MANAGEMENT PRODUCE MORE

BREEDING BIRDS?

J. L. Larkin1, P. B. Wood2, T. J. Boves3, J. Sheehan2, D. A. Buehler3, P. D. Keyser3, A. D.

Rodewald4, T. A. Beachy3, M. H. Bakermans4, A. Evans1, G. A. George2, M. E. McDermott2, f.

L. Newell4, K. A. Perkins2, M. White1, & T. B. Wigley5

1 Department of Biology, Indiana University of Pennsylvania, Indiana, Pennsylvania; E-mail: [email protected].

2 US Geological Survey West Virginia Cooperative Fish and Wildlife Research Unit, West Virginia University, Morgantown, West Virginia.

3 Department of Forestry, Wildlife, and Fisheries, University of Tennessee, Knoxville, Tennessee.

4 School of Natural Resources, Ohio State University, Columbus, Ohio. 5 National Council of Air and Stream Improvement, Inc., Clemson University,

Clemson, South Carolina.

Resumen. – ¿Preocupaciones de temporada y respuesta a la gestión forestal: gestión forestal puede producir más de aves de cría? – Las Reinitas Cerúleas (Setophaga cerulea) , una de las especies de aves que ha declinado más rápidamente in Norte América, están asociadas con doseles heterogéneos de bosques maduros de hoja ancha. Sin embargo, la edad de la mayoría de bosques que se han regenerado por segunda o tercera vez en el este de Norte América no es suficiente para que ocurra una mortalidad natural de los árboles que mantengan un dosel estructuralmente diverso. Investigaciones previas sugieren que el manejo de los bosques por medio de la tala selectiva puede crear condiciones aptas como las del hábitat reproductivo de la Reinita Cerúlea. Llevamos a cabo un estudio para examinar la respuesta de la Reinita Cerúlea a la variación de la perturbación del dosel debido a tala de árboles. Específicamente, tres tratamientos de tala y una parcela no talada como referencia fueron replicados en siete áreas en cuatro es-tados Apalaches de 2005-2010. Comparamos la respuesta demográfica de la Reinita Cerúlea antes y cuatro años después de la tala. En general en todas las áreas de estudio, la Reinita Cerúlea se mantuvo estable en la parcela no talada e incremento significativamente el primer año después de taladas las parcelas de tala intermedia. Durante los tres años posteriores a la tala, la densidad territorial para las parcelas de tala intermedia se mantuvo significativamente grande en comparación a las parcelas de referencia. Sin embargo, en las parcelas de referencia los nidos tuvieron una mayor sobrevivencia que en las parcelas no taladas. La única excepción fue la sobrevivencia de los nidos entre las parcelas de referencia y las de tala intermedia en los sitios del norte que no difirieron. Nuestros resultados indican que talas intermedias probablemente benefician a la Reinita Cerúlea en alguna parte de su distribución reproductiva. Sin embargo, investigaciones adicionales son necesarias para examinar el efecto de la tala sobre el fitness y estimar las implicaciones a nivel de población. En particular para saber si: ¿El efecto de un gran número de individuos anidando compensa el bajo éxito reproductivo, en sitios de tala intermedia? Hasta que los investigadores provean in-formación al respecto, recomendamos que las decisiones de manejo sean basadas en condiciones locales, particularmente en bosques donde la población de la Reinita Cerúlea sea alta.

Abstract. – Cerulean Warblers (Setophaga cerulea), one of the fastest declining avian species in North America, are associated with heterogeneous canopies in mature hardwood forests. However, the age of most second and third-growth forests in eastern North American is not sufficient for natural tree mortality to

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maintain structurally diverse canopies. Previous research suggests that forest management through timber harvest also may create conditions suitable as Cerulean Warbler breeding habitat. We conducted a multi-state study that examined Cerulean Warbler response to varying degrees of canopy disturbance created by operational timber harvest. Specifically, 3 harvest treatments and an un-harvested reference plot were replicated on 7 study areas in 4 Appalachian states in 2005-2010. We compared pre-harvest and four years post-harvest demographic response of Cerulean Warblers. Over all study areas, Cerulean Warbler territory density remained stable in un-harvested reference plots and increased significantly the first year post-harvest on intermediate harvest plots. By year 3 post-harvest, territory density remained significantly greater for intermediate harvest than reference plots, and marginally greater for light and heavy harvests than reference plots. However, un-harvested reference plots had greater nest survival than most harvest treatments. The one exception was nest survival between reference plots and the intermediate harvest on the northern study areas did not differ. Our results indicate that intermediate harvests likely benefit Cerulean Warblers in some portions of the species’ breeding range. However, additional research is needed to better examine fitness consequences of timber harvests and to estimate population-level implications. In particular, does the greater number of nesting individuals, particularly in intermediate harvests, compensate for lower nesting success? Until researchers provide such insight, we recommend management decisions be based on local conditions, particularly in forests where Cerulean Warbler populations are high.

Key words: Cerulean Warbler, breeding habitat, timber harvest, nest success, territory density, body condition.

the cerulean Warbler (Setophaga cerulea) is a neotropical migratory songbird that has gained widespread attention as a species of conservation and management concern. the species has experienced range-wide declines over the last 40 years (Sauer et al. 2008), especially in historically high-density areas of the appalachian Mountains (Hamel 2000). in eastern north america, breeding habitat for cerulean Warblers is characterized by heterogeneous canopies in mature hardwood forests, which occur naturally in the appalachians due to topography and large-scale disturbances including fire, wind events, ice storms, and insect outbreaks. though natural tree senescence once played an important role in creating heterogeneous canopies (lorimer 1980), particularly in old-growth forests, the age of most second- and third-growth forests in eastern north American is not sufficient for natural tree mortality to maintain structurally diverse canopies (lorimer and Frelich 1994). Forest management also may be used to create forest conditions favored by cerulean Warblers and other disturbance-adapted species (e.g. Wood et al. 2005, Bakermans and rodewald 2009).

However, prior to extensive use of silviculture to enhance habitat for such species, detailed habitat selection and demographic studies are needed to ensure that such actions do not have unintended negative consequences.

Here in, we present the results and their implications from a 6-year cerulean Warbler breeding grounds study conducted by members of the cerulean Warbler technical group as part of the cerulean Warbler conservation initiative (Dawson et al. 2012). Specifically, we investigated the extent to which silvicultural techniques differing in canopy removal might serve as tools to manage habitat for cerulean Warblers in the central appalachian Mountains, USa. We selected 7 study areas within the core cerulean Warbler breeding range of the central hardwoods’ mixed-mesophytic forest region (Fig. 1). Study areas were located in West Virginia (n 5 3), tennessee (n 5 2), ohio (n 5 1), and Kentucky (n 5 1), each within a matrix of mature hardwood forest. We selected study areas based on the presence of cerulean Warbler breeding populations and the potential to implement silvicultural prescriptions via partial timber harvest. We randomly assigned 4 silvicultural treatments to 4 20-ha plots at

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each study area: light, intermediate, and heavy canopy disturbance, as well as an unharvested reference plot. each treatment included a 10-ha harvested area (except on reference plots), and two 5-ha buffers of undisturbed forest on either end of the harvest to examine edge effects. light harvest mimicked forests disrupted by multiple tree-fall gaps; we reduced basal area (Ba) and overstory canopy cover (cc) on these treatments by approximately 20% (residual Ba 5 21.3 6 1.0 [Se] m2/ha; residual cc 5 60.9 ± 5.5%). intermediate harvests mimicked more

severe natural disturbances such as fire, wind events, or larger tree fall gaps; here we reduced Ba and cc by approximately 40% (residual Ba 5 14.3 6 1.2 m2/ha; residual cc 5 45.5 6 6.4%). Heavy harvests emulated severe natural disturbances such as strong wind events, severe ice-storms, landslides, or more intense fire; we reduced Ba and cc by approximately 75% (residual Ba 5 6.3 6 1.1 m2/ha; residual cc 5 18.2 6 4.3%). We left control plots undisturbed throughout the life of the study (Ba 5 26.9 6 1.3 m2/ha; cc 5 73.2 6 5.2%). on all treatments,

Fig. 1. locations of seven cerulean Warbler Forest Management study sites in the appalachian Mountains. all sites were located within the core of the cerulean Warbler breeding range. Map symbols indicate esti-mated range of the species, as “range” the estimated breeding range of the birds based upon Dunn and garrett (1997, Hamel 2000), and as “BBS core range” based on the analyses of Breeding Bird Survey data conducted by Baldy (2005).

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disturbances were applied uniformly across the 10-ha stand. overstory species composition was largely unchanged by the disturbances and residual stands on the intermediate and heavy treatments were comprised of dominant and co-dominant trees. We compared cerulean Warbler territory density two years pre-harvest (2005, 2006) and four years post-harvest (2007–2010). additionally, we compared nest survival and male age structure and condition (using body mass and wing-mass residuals) of captured males four years post-harvest.

although mean densities of cerulean Warblers remained stable on unharvested reference plots across all study areas (Boves 2011, Boves et al. 2013), numbers on reference plots were consistently lower than on experimental harvest plots following treatment. During the first year post-harvest, Cerulean Warbler density on the intermediate harvest increased significantly and by a greater amount than on the other harvest treatments or on the reference plots. in year 2 post-harvest, density on the intermediate harvest remained higher than on other harvest treatments and reference plots, and density increase was marginally greater on light harvest than reference plots (p , .10). By year 3 post-harvest, density increase was significantly greater for intermediate harvest than reference plots, and marginally greater for light and heavy harvest treatments than reference plots in year 4 post-harvest, densities on intermediate and heavy treatments remained higher than on the reference plots. Density declined on the light harvest treatment and was no longer different than that on the reference plots. territorial male age structure did not differ among treatments, but male body condition was better in harvested treatments compared to unharvested plots (Boves 2011).

nest survival of cerulean Warbler was a function of site, year, and silvicultural treatment (Boves 2011, Boves et al. 2013). after accounting for regional and annual differences in nest survival, cerulean Warblers in the unharvested

controls had greater nest survival and more fledglings per successful nest than those in harvested treatments. Because nest survival was greater on southern (tennessee) than northern sites, we treated the two regions separately in analyses related to treatment effects. in southern sites, nest success was higher on the unharvested reference plots than on light (χ2

1 5 15.02, P , 0.0001), intermediate (χ2

1 5 4.41, P 5 0.04), or heavy treatment plots (χ2

1 5 15.02, P , 0.0001). in northern sites, nest success on the unharvested reference plots was marginally higher than on the light harvest plots (χ2

1 5 3.50, P 5 0.06) or in the buffers (χ2

1 5 3.12, P 5 0.08), but similar to the intermediate harvest plots.

although patterns of density and body condition suggested that cerulean Warblers are attracted to harvest-generated disturbances in mature forest ecosystems of the appalachian Mountains, the lower nest success in harvested plots raises the possibility that recent harvests may function in some cases as ecological traps. additional research is needed to better examine fitness consequences of timber harvests and to estimate population-level implications. in particular, does the greater number of nesting individuals, particularly in intermediate harvests, compensate for lower nesting success? For example, we detected an average of 10.5 territories/10ha on intermediate harvests (10.5 territories x 0.34 nest success 3 2.6 average young fledged per successful nest 5 9.3 young/10ha) compared to 4.25 territories/10ha on unharvested plots (4.25 territories 3 0.42 success x 2.25 average young fledged per successful nest 5 4.0 young/10ha) across all northern sites. in this example, the greater number of young produced and better adult condition (assuming adult condition contributes to higher annual survival) on intermediate harvests may substantially outweigh higher nesting success observed on the unharvested reference plots. Ultimately, we recommend management decisions be based on local conditions, particularly in forests where cerulean Warbler populations are high.

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Baldy, J. 2005. climate preferences of the cerulean Warbler on summer territory. M.Sc. thesis, Univ. of Memphis, Memphis, tennessee, USa.

Boves, t. J. 2011. Multiple responses by cerulean Warblers to experimental forest disturbance in the appalachian Mountains. ph.D. diss., Univ. of tennessee, Knoxville, tennessee, USa.

Boves, t.J., D.a. Buehler, J. Sheehan, p.B. Wood, a.D. rodewald, J.l. larkin, p.D, Keyser, F.l. newell, g.a. george, a. evans, M.H. Bakermans, a. evans, t.a. Beachy, M.e. McDermott, K.a. perkins, M. White, & t.B. Wigley. 2013. emulating natural disturbances for declining late-successional species: a case study of the consequences for cerulean warblers (Setophaga cerulea). ploS one. Available 4 Jan 2013 at http://dx.plos.org/10.1371/journal.pone.0052107.

Dawson, D. K., t. B. Wigley, & p. D. Keyser. 2012. cerulean Warbler technical group: coordinating international research and conservation. ornitol. neotrop. 23(Suppl.): 279–285.

Dunn, J. & K. L. Garrett. 1997. A field guide to warblers of North America. Houghton Mifflin co., Boston, Massachusetts, USa.

Hamel, p. B. 2000. cerulean Warbler (Dendroica cerulea). In poole, a., & F. gill (eds). the Birds of north america, no. 511. the birds of north america, inc., philadelphia, pennsylvania, USa.

lorimer, c. g. 1980. age structure and disturbance history of a southern appalachian virgin forest. ecology 61: 1169–1184.

lorimer, c. g., & l. e. Frelich. 1994. natural disturbance regimes in old-growth northern hardwoods - implications for restoration efforts. J. For. 92: 33–38.

Sauer, J. r., J. e. Hines, & J. Fallon. 2008. the north american Breeding Bird Survey, results and analysis 1966–1999. Version 5.15.2008, USgS patuxent Wildlife research center, laurel, Maryland, USa.

Wood, p. B., J. p. Duguay, & J. V. nichols. 2005. cerulean warbler use of regenerated clearcut and two-age harvests. Wildl. Soc. Bull. 33: 851–858.

acKnoWleDgMentS

Funding for this project was provided by the national Fish and Wildlife Foundation through a grant with the national council for air & Stream improvement, inc., U.S. Fish and Wildlife Service, U.S. Forest Service, MeadWestvaco corporation, Kentucky Department of Fish and Wildlife resources, ohio Division of Wildlife, School of environment & natural resources at ohio State University, tennessee Wildlife resources agency, Department of Forestry, Wildlife and Fisheries at the University of tennessee, the nature conservancy through a U.S. Fish and Wildlife Service Hcp planning grant with the tennessee Wildlife resources agency, West Virginia Division of natural resources Wildlife Diversity program, USgS West Virginia cooperative Fish and Wildlife research Unit, Department of Biology at indiana University of pennsylvania. this research was conducted on U.S. Forest Service’s Daniel Boone national Forest and Monongahela national Forest, on public lands owned by the tennessee Wildlife resources agency and the West Virginia Division of natural resources, and on private lands owned by Forest land group/Wagner Forest Management and MeadWestvaco. We appreciate the cooperation and assistance of these agencies/groups and the efforts of their forest management personnel for assistance with study site selection, design of harvesting treatments, and especially implementation of harvests. Finally, we are most grateful for the dedicated service of over 80 field technicians. Their contribution to our improved understanding of cerulean Warbler breeding ecology cannot be overstated.

reFerenceS

Bakermans, M. H., & a. D. rodewald. 2009. think globally, manage locally: the importance of steady-state forest features for a declining songbird. Forest ecol. Manag. 258: 224–232.

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SPRING MIGRATION STOPOVER By CERULEAN WARBLERS IN NORTHERN MIDDLE AMERICA

Melinda J. Welton1, David L. Anderson2, Gabriel J. Colorado3, Paul B. Hamel4,

& Diego Calderón-f.5

1Gulf Coast Bird Observatory, 5241 Old Harding Road, Franklin, TN 37064 USA, E-mail: [email protected]

2Department of Biological Sciences and Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803

3Instituto de Biología, Universidad de Antioquia, Calle 67 No. 53-108 Oficina 7- 233, Medellín, Colombia

4U.S. Forest Service, Center for Bottomland Hardwoods Research, P.O. Box 227, 432 Stoneville Rd., Stoneville, MS 38776 USA

5COLOMBIA Birding, Carrera 83A No.37C-45, Medellin, Colombia

Resumen. – El paso de la Reinita Cerúlea durante la migración de primavera en el norte de América Central. – La Reinita Cerúlea (Setophaga cerulea) realiza una de las migraciones más largas entre los passeriformes pequeños, viajando aproximadamente 4.000 km entre las aéreas de anidación al este de Norte América y su residencia no-reproductiva al norte de Sur América. Sin embargo, a diferencia de otras aves migratorias, poco es conocido sobre este aspecto de la ecología de esta especie. Entre 2004 y 2009, equipos de biólogos residentes y extranjeros realizaron censos en 181 transectos lineales durante la última semana de marzo y las primeras tres semanas de abril en Belice, sur de México, Guatemala, Honduras y Nicaragua. En general, los resultados confirmaron la hipótesis de Ted Parker (1994) de que las Reinitas Cerúleas paran temprano en abril en las montañas bajas de la costa del Caribe al norte de América Central. Sin embargo, en contraste con las observaciones de Reinitas Cerúleas realizadas por Parker entre 600 y 750 m en Belice, en este proyecto las observaciones se distribuyeron uniformemente a estas elevaciones así como por encima y por debajo de este rango. Por otro lado, la frecuencia de observaciones de Reinitas Cerúleas fue mucho mayor en Belice, el sur de México y el centro de Guatemala que en cualquier otro lugar. Los números relativamente bajos de Reinitas Cerúleas encontrados durante la migración de primavera (134 individuos durante 701 h de investigación) ponen en duda la sugerencia de Parker de que la totalidad de la población de Reinitas Cerúleas se detiene en las montañas que miran hacia el Caribe del norte de América Central. Nosotros sugerimos otra hipótesis consistente con los resultados hasta la fecha; esta hipótesis propone que varias de estas aves vuelan directamente desde Sur América a Norte América en la primavera.

Abstract. – The Cerulean Warbler (Setophaga cerulea) has one of the longest migrations of any small passerine, traveling approximately 4,000 km between breeding grounds in eastern North America and non-breeding residency in northern South America. However, unlike many migratory birds, little is known about this aspect of the ecology of this species. In 2004 – 2009 teams of resident and foreign biologists conducted 181 line-transect surveys in Belize, southern Mexico, Guatemala, Honduras, and Nicaragua, during the last week in March and the first three weeks of April. Results generally confirm Parker’s (1994) hypothesis that Cerulean Warblers stop in low mountains on the Caribbean coast of northern Central America in early April. However, in contrast to Parker’s observations of Cerulean Warblers between 600 and 750 m in Belize, sightings in this project were evenly distributed at these and elevations above and below this range. The frequency of encountering Cerulean Warblers was higher in Belize, southern Mexico and central Guatemala than elsewhere. The relatively low numbers of Cerulean Warblers encountered during spring migration (134 individuals during 701 h of surveys) call into question Parker’s suggestion that the entire population of Ceru-

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observations exist for this species during spring and fall migration with the exception of those compiled by ted parker in the spring of 1992 in Belize (parker 1994). parker observed up to 100 individual cerulean Warblers from 3 to 10 april 1992 in mature subtropical lower montane forests between 600 and 750 m elevation in the columbia river Forest reserve in the Maya Mountains of southern Belize (Fig. 1). He observed from one to six cerulean Warblers foraging in individual mixed-species canopy flocks of native and migrant birds. Based on his observations, parker proposed that during the first two weeks of April the species’ entire population stops over in caribbean-facing mountains of northern Middle america. parker also proposed this stopover region extended from eastern Mexico, through southern Belize, across guatemala and northern Honduras, and possibly northwestern nicaragua.

We initiated a multiyear investigation of the occurrence of the cerulean Warbler in northern Middle america during spring migration to answer these questions. our specific objectives were: 1) to test Parker’s predictions of cerulean Warbler distribution and habitat use, 2) to evaluate the timing of migration during the assumed period of peak movement, 3) to estimate the elevational and geographic distribution of cerulean Warblers migrating through northern Middle america, and 4) to describe the composition of mixed-species canopy flocks with which Cerulean Warblers were often associated.

MetHoDS

Study areas. our study region included southern Belize, southeastern Mexico, central

lean Warblers stops over in the Caribbean-facing mountains of northern Middle America. We suggest a new hypothesis consistent with results to date, that many of these birds fly directly from South America to North America in the spring.

Key words: Cerulean Warbler, long-distance migration, migratory stopover, mixed-species flocks, northern Middle America, Setophaga cerulea.

introDUction

Migration may be the most difficult aspect to study in the life history of a nearctic-neotropical migrant bird because of the transitory nature of the phenomenon and the geographic complexity of the event. However, because this stage may occupy as much as one-third of a species’ annual cycle (Mehlman et al. 2005, newton 2006), explain as much as 85% of annual mortality (Sillett and Holmes 2002), and is subject to climatic variability to an increasing extent (lehikoinen and Sparks 2010), identification (Moore et al. 2005, Holmes 2007) and preservation of stopover habitat is of the utmost importance (gauthreaux 1999, Moore 2000, Mehlman et al. 2005), especially when developing a conservation strategy for a species of high conservation concern.

cerulean Warbler (Setophaga cerulea) is such a species of high conservation concern (rich et al. 2004, Birdlife international 2008) because of its long-term population decline as measured on the breeding grounds in eastern north america (robbins et al. 1992, Veit et al. 2005, Sauer et al. 2011). Much of this decline has been attributed to the loss (Hamel 2000a), degradation, and fragmentation (Veit et al. 2005, Wood et al. 2006) of mature forest on both the breeding (Wood et al. 2005) and wintering grounds (robbins et al. 1992, parker 1994, Hamel 2000b).

this species also has one of the longest migrations of any warbler or passerine of similar size, traveling approximately 4,000 km between the breeding grounds in eastern north america and the wintering grounds in northern South america (Hamel 2000a, Hamel 200b). Unlike most migratory birds, however, remarkably few specimens or published

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guatemala, northern Honduras, and western Nicaragua. As a first stage of this project, surveys were conducted in 2004 in the same location where parker (1994) recorded his cerulean Warbler observations at Union

camp, in the columbia river Forest reserve in southern Belize (16°23’55”n, 89°08’34”W, Fig. 1). although parker (1994) described the southern portion of that Belize site as having “particularly tall trees,” we found severe but

Fig. 1. Map of study areas in Middle america searched for cerulean Warblers during spring migration 2004–2009.

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localized damage to the forest canopy caused by Hurricane iris in october 2001, and from a forest clearing made by a temporary illegal guatemalan incursion.

in 2005–2009 some survey locations were chosen because they conformed to parker’s predictions that cerulean Warblers were stopping in mature lower montane forests of caribbean-facing mountains (table 1). other locations were specifically chosen because they differed from these conditions and were located in mature forests on non-caribbean-facing slopes, at higher or lower elevations than those predicted by parker (1994), or differed in both respects. Because of cerulean Warbler occurrence in shade coffee plantations in South america (e.g., Jones et al. 2000, Bakermans et al. 2009, colorado 2011), a set of surveys was completed in this habitat type, as well as locations of historic specimen collections in Mexico, guatemala, and Honduras. a complete list of survey locations appears as an appendix.

Field Surveys. We assessed cerulean Warbler presence using transect survey records, and cerulean Warbler relative abundance by calculating the encounter frequency of both cerulean Warblers (number of cerulean Warblers/hour of survey) and of flocks (number of flocks/hour of survey). Transect surveys were conducted usually along existing forest trails (Bibby et al. 2000). Surveys started within one half hour after dawn and occasionally in the late afternoon, with an average time of four hours per survey. observers walked slowly (approximately 1km/hour) scanning mid-story, upper-story, and emergent trees for mixed-species flocks or single foraging birds. Survey dates were standardized each year to encompass the last week of March through the third week of april (comprehensive survey dates were 25 March to 22 april). Surveys were conducted by one to six teams of Mexican, guatemalan, Honduran, nicaraguan, and foreign biologists.

Before each season a training session was given to team leaders and most assistants on survey methods and Cerulean Warbler identification.

During fieldwork conducted 2005–2007 we noted and identified to species all individuals in the mixed-species canopy flocks that we encountered. incidental observations of cerulean Warblers were also recorded. playback songs of cerulean Warbler or lesser greenlet (Hylophilus decurtatus), a common flock associate, were used for most flocks in 2005–2007 to enhance cerulean Warbler detectability.

reSUltS

During 181 transect surveys conducted in spring 2004–2009 we recorded 134 cerulean Warblers (98 males, 35 females, 1 unknown) in 69 of the 386 flocks recorded (Table 1). Eight incidental observations of cerulean Warbler were also made during this period. one incidentally observed cerulean Warbler was found away from any mixed-species foraging flock. Virtually all observations of Cerulean Warbler occurred in the canopy or upper mid-story of primary or mature secondary forests; four cerulean Warblers were observed in the shade trees of rustic shade coffee plantations.

nearly all cerulean Warblers (132 of 134, 98%) were found on caribbean-facing slopes (χ2 1 df 5 25, p , 0.005), although the encounter frequency of flocks was more equally divided between caribbean and non-caribbean facing slopes (χ2 1 df 5 2.8, p . 0.1). Distributions of both Cerulean Warblers (χ2 2 df 5 0.4, p . 0.5) and flocks (χ2 2 df 5 0.8, p . 0.5) in our three elevation categories were nearly identical to those expected based on the number of surveys conducted (table 2). cerulean Warbler encounter frequency was not uniform during the study period, with an apparent decrease after 13 april (93% of birds observed 2–14 april, median date 8 april; Fig. 2). the number of Cerulean Warblers detected in flocks ranged from one to five individuals (Fig 3).

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were in an area of historic cerulean Warbler records, with one cerulean Warbler being detected at one of these sites.

Five sites were surveyed because there was at least one historic cerulean Warbler record for that site in Mexico (2 sites), guatemala (1 site), and Honduras (2 sites; table 3). cerulean Warblers were encountered at three of these sites, where the original forest overstory remained intact. the habitat at two historic sites had been fragmented by human activities and no cerulean Warblers were found there.

eighteen surveys, totalling 57 hours, were conducted in rustic shade coffee plantations, during which two cerulean Warblers were recorded in 46 enumerated flocks (Cerulean Warbler encounter frequency of 0.04 birds/h). the 18 plantations were equally split between caribbean and non-caribbean facing slopes (1 cerulean Warbler encountered in each). Most plantations (16) were at elevations similar or higher than the range predicted by parker (1994); both cerulean Warblers were observed at higher elevations. Five of the 18 rustic plantation sites were chosen only because they

Table 1. Cerulean Warbler survey totals in five countries in Middle America, 2004–2009

country n, surveysn, survey locations

n, survey hours

n, cerulean Warbler

detections N, flocks

Belize 9 3 31.50 16 n/a

Mexico 19 9 62.15 16 57

guatemala 61 13 261.93 62 120

Honduras 79 16 301.99 31 198

nicaragua 13 4 43.05 9 11

total 181 45 700.62 134 386

Table 2. Surveys by geophysical location in five countries in Middle America, 2004–2009.

Survey location n, surveys n, survey h

n, cerulean Warbler

detections N, flocks

cerulean Warblers

detected per survey h

Flocks encountered per survey h

topographic position

caribbean facing 148 581.56 132 303 0.23 0.52

not caribbean facing 33 119.07 2 83 0.02 0.70

elevation

Below 500m 102 403.29 75 226 0.19 0.56

500m – 850m 46 159.24 32 93 0.20 0.58

above 850m 33 138.10 27 67 0.20 0.49

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Fig. 2. Survey effort and encounter frequency of cerulean Warblers per hour of survey effort by date dur-ing field surveys in Middle America in March-April 2004–2009.

FIG. 3. Mean proportion of mixed-species foraging flocks observed in Middle America 2005–2007 contain-ing different numbers of cerulean Warblers, mean 6 1 SE of 67 completely enumerated flocks observed in each of the years: 2005, n 5 12 flocks; 2006, n 5 26 flocks; 2007, n 5 29 flocks.

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cerulean Warbler. Fourteen males and one female from 10 flocks responded to the playback: 3 males and one female responded by coming closer to the speaker, 9 males vocalized by either chipping (2 males), singing one territorial song (1 male), or by singing whisper songs (Schafer 1917, Johnson & Kermott 1991; 6 males). two males in one flock were already singing territorial songs before playback was used.

Replicate surveys. twenty-three survey routes were surveyed more than once in Mexico (3 sites), guatemala (4 sites), and Honduras (16 sites). each such site was surveyed from two to four times between years or with a minimum of 3 days between surveys. at 17 (74%) of the sites the results of subsequent surveys were the same as the initial survey; either no cerulean Warblers were encountered during any of the surveys (11 sites), or cerulean Warblers were found during each survey (6 sites). at four sites cerulean Warblers were recoded only on the first survey, and at two sites Cerulean Warblers were recorded only on the second survey.

all cerulean Warblers observed during formal surveys were found in mixed-species foraging flocks. In 68 flocks that contained at least one cerulean Warbler we recorded 107 other avian species. an additional 65 species were encountered only in one or more of 236 fully enumerated flocks in which Cerulean Warbler was not recorded (table 4). thirty-two species occurred in at least 10% of the flocks. Among these were seven species that occurred in at least 20% of all flocks of either group. rank order of species occurring in at least 10% of flocks was similar (rs 5 0.79, n 5 28, p , 0.0001; cerulean Warbler excluded from the comparison). Six of seven species found in more than 20% of the flocks, and 10 of 18 species recorded in at least 10% of flocks in both groups, were migratory species. Seven of these belonged to the family parulidae. the most frequent species, occurring in 61% of all flocks enumerated, was Lesser Greenlet.

Playback response. three team leaders used cerulean Warbler song playback consistently during surveys in 2006 – 2007. recordings of cerulean Warbler or lesser greenlet were played to 31 flocks that contained at least one

table 3. Sites of historic cerulean Warbler observations that were surveyed during the current study.

country / Survey site n, surveys n, survey hn, cerulean

Warbler detectionscurrent

habitat condition

Mexico

Bonampak archeological site 2 8.58 3 intact

palenque archeological site 2 4.05 0 fragmented

Guatemala

San gil ecological reserve 4 13.03 9 intact

Honduras

lago de Yojoa 6 22.33 0 fragmented lancetilla Botanical garden and research center 1 4.00 1 intact

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Table 4. Species recorded in at least 10% of flocks enumerated in this study.

common name1, 2 Scientific Name

Flocks including cerulean Warbler

Flocks without cerulean Warbler

all Flocks

Plain Xenops Xenops minutus 8 18 26olivaceous Woodcreeper Sittasomus griseicapillus 7 14 21ivory-billed Woodcreeper Xiphorhynchus flavigaster B3 17 24 41Mexican [Black-faced] antthrush Formicarius analis (moniliger) 7 8 15ochre-bellied Flycatcher Mionectes oleagineus B 10 26 36red-capped Manakin Pipra mentalis 9 16 25Yellow-throated Vireo* Vireo flavifrons 8 9 17philadelphia Vireo* Vireo philadelphicus 8 20 28red-eyed Vireo* Vireo olivaceus B 18 44 62tawny-crowned greenlet Hylophilus ochraceiceps B 12 40 52Lesser Greenlet Hylophilus

decurtatus B 53 131 184green Shrike-Vireo Vireolanius pulchellus 8 21 29White-breasted Wood- Wren Henicorhina leucosticta 9 18 27Wood thrush* Hylocichla mustelina 7 12 19Worm-eating Warbler* Helmitheros vermivorum 10 22 32golden-winged Warbler* Vermivora chrysoptera 21 22 43Black-and-white Warbler* Mniotilta varia B 37 83 120Tennessee Warbler* Oreothlypis

peregrina B 22 78 100American Redstart* Setophaga ruticilla B 28 69 97cerulean Warbler* Setophaga cerulea 68 0 68Magnolia Warbler* Setophaga magnolia B 27 88 115Blackburnian Warbler* Setophaga fusca 18 23 41Chestnut-sided Warbler*

Setophaga pensylvanica B 32 84 116

Black-throated Green* Warbler Setophaga virens B 19 48 67

golden-crowned Warbler Basileuterus culicivorus B 11 30 41Wilson’s Warbler* Cardellina pusilla B 14 31 45

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the site in 2004, we have established that they do. in fact, cerulean Warblers were the most common neotropical migrant encountered during the three and a half days of surveys around Union camp in the columbia river Forest from 2–5 april 2004.

other major goals of the project were to assess the extent of the geographic area over

DiScUSSion

the initial goal of this project was to determine whether large numbers of cerulean Warblers continue to use the same location in the columbia river Forest in southern Belize where parker (1994) made his original observations in 1992. Based on a field visit to

table 4. continued.

common name1, 2 Scientific Name

Flocks including cerulean Warbler

Flocks without cerulean Warbler

all Flocks

red-crowned ant-tanager Habia rubica 10 17 27Summer tanager* Piranga rubra B 12 48 60red-legged Honeycreeper Cyanerpes cyaneus B 7 30 37Black-faced grosbeak Caryothraustes poliogaster B 12 32 44Baltimore oriole* Icterus galbula B 8 27 35olive-backed euphonia euphonia gouldi B 8 26 34

number of Flocks 68 236 304total Species 108 164 173total Species registrations 722 1795 2517

Species in .10% of flocks 32 18 22registrations of Species in .10% of flocks 545 939 1470proportion of registrations in species in .10% of flocks 0.75 0.52 0.58

Species in .20% of flocks 12 8 9registrations of Species in .20% of flocks 360 629 929proportion of registrations in species in .20% of flocks 0.50 0.35 0.37

1Species marked in bold occurred in more than 20% of flocks of both subsamples.2asterisks indicate migratory species.3Species marked “B” were encountered in more than 10% of flocks in both subsamples.

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The timing of our observations confirms Parker’s findings and the suggestions of Hamel (2000a) that the spring migration period in Middle america is a short one. Most of the cerulean Warblers observed in this study were found in the first two weeks of April; however, insufficient surveys were conducted in March and late april to more fully complete our understanding of the timing of cerulean Warbler spring migration in the region.

the similarity of the composition of flocks in which Cerulean Warblers were and were not recorded suggests that these warblers were not selecting flocks based upon composition. rather it appears that they were selecting flocks based upon availability. The large number of enumerated flocks in which cerulean Warblers were not found indicates that substantial capacity exists for the birds to join additional flocks during migration. Why the warblers were not found in more flocks is an open question.

on the basis of its frequency and abundance in flocks, Lesser Greenlet is likely a nuclear species of canopy flocks in northern Middle america (Botero 2002, Srinivasan et al. 2010). although the use of playback of lesser greenlet vocalizations likely affected the detection rate of this species, previous studies (robinson et al. 2000, anderson & naka 2011) have also shown that lesser greenlet is numerically dominant in upper strata of moist forests of Middle america, including at sites used in the present study. the high frequency of migratory species in these flocks suggests that mixed-species flocks in Middle American forests are particularly important for migratory birds, perhaps especially warblers, during passage. the 11 migratory warbler species found in at least 10% of all flocks accounted for 33% of all species identifications in the 701 hours of fieldwork.

Although our results affirm that northern Middle america is a stopover area for migrating cerulean Warblers in the spring,

which cerulean Warblers occur during spring migration, to determine the characteristics of the habitat they utilize, and to determine the timing of migration stopover in Middle america. parker (1994) hypothesized that during spring migration cerulean Warblers are found in “suitable lower montane forest facing the caribbean coast”. our results generally concur with the second part of the hypothesized distribution in the forest on caribbean-facing slopes. However, we encountered cerulean Warblers at nearly the same frequency at all elevations surveyed. We believe that this finding calls into question the first part of the hypothesis, and suggests that the birds probably make landfall over a broad range of elevations.

another interesting contrast to parker’s hypothesis that the spring stopover region extends from eastern Mexico, through southern Belize, across guatemala and northern Honduras, and possibly into northwestern nicaragua is that the birds we encountered were not equally distributed within this region. Although we did find Cerulean Warblers on the caribbean facing slopes throughout this area, the frequency of encountering cerulean Warblers was much higher in southern Mexico, southern Belize, central guatemala, and northwestern Honduras, suggesting that there may be a higher density of cerulean Warblers in the narrow arc within this region.

Shade coffee plantations are an important habitat type for cerulean Warblers during the non-breeding season in northern South america (Bakermans et al. 2009, Sanchez-clavijo et al. 2009, colorado et al. 2012). although rustic shade plantations were actively sought for survey locations during this study, few cerulean Warblers were found in this habitat type. We are unable to assess from available data whether this habitat is important to cerulean Warblers during spring migration, and recommend further studies to address this question.

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during spring migration, as is the case for Swainson’s Warbler (Catharus ustulatus; ruegg et al. 2006). tankersley & orvis (2003) offer additional insight into this possibility.

regardless of the origin or proportion of the global population of cerulean Warblers stopping over in northern Middle america, this area is of critical importance to a substantial segment of this population. thus, we believe it is important not only to identify the extent of this stopover range, but also to integrate conservation of cerulean Warbler and other migratory species into the management and protection status of these lands. indeed, the list of species found in more than 10% of Middle American flocks surveyed during the spring migration period is a good basis for use in training observers in identification of flock members. consequently we recommend that the next phase of spring migration study should be the development and field-validation of a predictive habitat model for cerulean Warbler during spring migration in Middle america (see, e.g., Barker et al. 2006, Buehler et al. 2006). implementing conservation management objectives into the land use activities of the inhabitants of lands identified as important by the model, using methods similar to those of Fundación proaves et al. (2010), Skolnik et al., (2012), or Santander et al. (2012), will be a distinct positive step in an action plan to protect valuable stopover habitat from loss or degradation.

acKnoWleDgMentS

We are grateful to the many organizations and individuals who provided material and monetary support, namely: US Fish and Wildlife Service through the neotropical Migratory Bird conservation act and Focal Species Strategies campaign, american Bird conservancy, the nature conservancy, lyndhurst Foundation, tucker Foundation, linnean Society of london percy Sladen

the relatively low numbers of cerulean Warblers encountered (134 individuals during 701 hours of surveys) calls into question the suggestion (parker 1994) that the entire population is stopping in this small geographic area to replenish fat reserves consumed in their flight across the western Caribbean ocean and before crossing the gulf of Mexico. in addition, relatively few springtime observations exist of cerulean Warblers along the coast of northern South america (gc pers. obs.; n. Bayly pers. com.) or along the gulf coast of the United States (http://ebird.org/content/ebird/about/occurrence-maps/cerulean-warbler [accessed 2/2012]). given that the southerly winds aloft in early spring are favorable for migratory movements from South to north america (gauthreaux et al. 2005), the physical proportion of cerulean Warblers favorable to long-distance flight (Averill 1920), and the flight ranges predicted for other small songbirds (nisbet et al. 1963, Bayly & gomez 2011), we hypothesize that cerulean Warblers, especially in the eastern portion of the non-breeding range, fly directly from highland wintering grounds in northern South america to the highland breeding grounds in the southeastern United States or into the riverine forests along the Mississippi corridor. We further speculate that the birds wintering in the western portion of the non-breeding range move northward and eastward along the northern Andes and then fly directly to north america.

one alternative hypothesis to explain the occurrence of cerulean Warblers in spring in northern Middle america is that these birds have encountered weather or other difficulties that do not allow them to make the direct over-water flight. A reverse pattern may exist in the fall when cerulean Warblers are regularly found in a relatively small region of caribbean-facing slopes in costa rica (e. carman pers. com.). a second hypothesis is that the birds are following multiple pathways

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Bibby, c. J., n. D. Burgess, D. a. Hill, & S. H. Mustoe. 2000. Bird census techniques. Second edition. academic press, San Diego, california, USa.

Birdlife international. 2008. Dendroica cerulea. In iUcn 2011. iUcn red list of threatened Species (version 2011.2). available at www.iucnredlist.org/ [accessed 20 December 2011]

Botero, C.A. 2002. Is the White-flanked Antwren (Formicariidae: Myrmotherula axillaris) a nuclear species in mixed-species flocks? A field experiment. J. Field ornithol. 73: 74–81.

Buehler, D. a., M. J. Welton, & t. a. Beachy. 2006. predicting cerulean Warbler habitat use in the cumberland Mountains of tennessee. J. Wildl. Manag.: 1763–1769.

colorado, g. J. 2011. ecology and conservation of neotropical-nearctic migratory birds and mixed-species flocks in the Andes. Ph.D. diss. ohio State Univ., columbus, ohio, USa. available at http://etd.ohiolink.edu/send-pdf.cgi/colorado%20gabriel%20J.pdf?osu1291646331/ [accessed 25 January 2012]

colorado, g. J., p. B. Hamel, a. D. rodewald, & D. Mehlman. 2012. advancing our understanding of the non-breeding distribution of cerulean Warbler (Setophaga cerulea) in the andes. ornitol. neotrop. 23(Suppl.): 309–317.

Fundación proaves, american Bird conservancy & el grupo cerúleo. 2010. conservation plan for the cerulean Warbler on its nonbreeding range - plan de conservación para la reinita cerúlea sobre su rango no reproductivo. conserv. colomb 12: 1–62.

gauthreaux, S. a., Jr. 1999. neotropical migrants and the gulf of Mexico: the view from aloft. pp. 27–49 in K. p. able, (ed.). gatherings of angels: migrating birds and their ecology. cornell Univ. press, ithaca, new York, USa.

gauthreaux, S. a., Jr., J. e. Michi, & c. g. Belser. 2005. the temporal and spatial structure of the atmosphere and its influence on bird migration strategies. pp. 182–193 in greenberg r., & p. p. Marra(eds). Birds of two worlds: the ecology

Memorial Fund, and gulf coast Bird observatory. We thank our many collaborators and colleagues who contributed substantially to the success of this project, most especially D. Mehlman, D. pashley, K. girvan, t. Will, D. Buehler, t. Beachy, r. Steiner, M. Bonta, J. Betancourt, W. Maheia, l. Jones, B. eley, and l. chavarria. Most importantly, we are indebted to more than 44 field biologists in five countries, and especially Selvin Perez, without whom the fieldwork could not have been completed.

reFerenceS

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ornitologia neotropical 23: 307–315, 2012© the neotropical ornithological Society

ADVANCING OUR UNDERSTANDING Of THE NON-BREEDING DISTRIBUTION Of CERULEAN WARBLER (sEtOphAGA

CErulEA) IN THE ANDES

Gabriel J. Colorado1,3, Paul B. Hamel2, Amanda D. Rodewald3, & David Mehlman4

1Instituto de Biología, Universidad de Antioquia, Calle 67 No. 53-108 Oficina 7- 233, Medellín, Colombia Email: [email protected].

2US Forest Service, Center for Bottomland Hardwoods Research, P.O. Box 227, Stoneville, MS 38776, U.S.A.

3School of Environment and Natural Resources The Ohio State University, 2021 Coffey Road, Columbus, OH 43210-1085, U.S.A.

4The Nature Conservancy, Migratory Bird Program, 212 E. Marcy St., Suite 200, Santa Fe, NM 87501, U.S.A.

Resumen. – Hallazgos recientes en la distribución invernal de la Reinita Cerulea (setophaga cerulea) en los Andes. – Recientes reducciones poblacionales han incitado a la Unión Internacional para la Con-servación de la Naturaleza a listar a la Reinita Cerúlea (Setophaga cerulea: Parulidae) como una especie Vulnerable. Se cree que esta disminución puede estar relacionada con la pérdida de hábitat a través de todo su rango, principalmente debida a deforestación y degradación de sus hábitats. En respuesta, miembros de El Grupo Cerúleo, un subcomité del Grupo Técnico de la Reinita Cerúlea encargado de aspectos de la especie en sus cuarteles de invierno, desarrollaron un modelo predictivo de hábitat invernal para la Reinita a través del norte y centro de los Andes. Entre 2006-2010, llevamos a cabo muestreos de campo en Ven-ezuela, Colombia, Ecuador y Perú como parte de un esfuerzo para validar este modelo de hábitat. En este artículo, compartimos nuevos hallazgos sobre la distribución de la reinita cerúlea así como una revisión de análisis recientes acerca del poder de este modelo para predecir su rango invernal. Primero, nuestros datos muestran que la especie ocupa un rango altitudinal más amplio de lo considerado previamente. Segundo, las reinitas cerúleas emplean una variedad mayor de tipos de hábitat, incluyendo diferentes estados suce-sionales y agroecosistemas intensamente manejados. Tercero, la especie muestra una fuerte asociación con bandadas mixtas Neotropicales en su mayoría compuestas por especies de aves residentes. Colectiva-mente, estos hallazgos tienen importantes implicaciones para los esfuerzos de conservación en los Andes.

Abstract. – Recent population declines have prompted the International Union for the Conservation of Na-ture to list Cerulean Warbler (Setophaga cerulea: Parulidae) as a Vulnerable species. It is believed that this decline may be related to habitat loss through its entire range, mainly due to deforestation and degradation of its habitats. In response, members of El Grupo Cerúleo, a subcommittee of the Cerulean Warbler Technical Group that addresses wintering ground issues faced by the species, developed a predictive model of winter-ing habitat for Cerulean Warblers throughout the northern and central Andes. From 2006-2010, we conducted field surveys in Venezuela, Colombia, Ecuador and Peru to validate the winter habitat model. In this paper, we share new insights into the distribution of Cerulean Warblers and preview recent analyses of the ability of the habitat model to predict wintering range. First, our data show that Cerulean Warblers occupy a broader altitudinal range than previously thought. Second, wintering Cerulean Warblers utilize a wider variety of habitat types than formerly believed, including different successional stages and intensively-managed agroecosys-tems. Third, the species shows a strong association with mixed-species flocks, composed mostly of resident bird species. Collectively, these findings have important implications for conservation efforts in the Andes.

Key words: Cerulean Warbler, Setophaga cerulea, El Grupo Cerúleo, modeling assessment, distributional maps.

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In this paper we summarize the field tests of the model conducted during the 2006-2010 nonbreeding seasons. the analyses form part of a comprehensive effort by el grupo cerúleo to predict occurrence of cerulean Warbler in the northern and central andes. This study is the first rigorous, range-wide sample of the nonbreeding range of cerulean Warbler, and perhaps of any migratory songbird with an extensive nonbreeding range.

MetHoDS

to evaluate the accuracy and predictive power of the map presented by Barker et al. (2006), we conducted field surveys for Cerulean Warbler in 2006-2010. Barker et al. (2006) mapped 200,000 km2 of Andean landscapes identified by all five models as high probability Cerulean Warbler nonbreeding range. We randomly selected 20 of these model-identified locations across the northern and central andes for the field evaluation. Using the protocol of colorado et al. (2008), we began with the 20 initially-selected 1-km2 pixels, and selected nine additional 1-km2 pixels near each of them. each randomly selected location thus comprised a cluster of ten 1-km2 pixels; our final sample consisted of 200 pixels, representing 0.1% of the predicted range. Detailed methods of experimental design, as well as vegetation and bird sampling protocol are presented in colorado et al. (2008).

carrying out the rigorous sampling protocol (colorado et al. 2008) required an unusually arduous coordination process. in addition to planning and organizing the field visits into remote andean terrain in four countries, it was necessary to evaluate the security risk in each one of the selected pixels. location of pixels on google earth® satellite images provided initial reconnaissance. Identification of the closest towns or municipalities to every pixel, as well as routes and relative distances was done using DiVa-giS (http://www.diva-gis.

introDUction

the cerulean Warbler (Setophaga cerulea), a neotropical-nearctic migratory bird whose entire global population winters in the andes Mountains of South america, is a species of high conservation concern (Birdlife international 2004), because of its recent and persistent population decline (robbins et al. 1992, Hamel 2000). Despite our general lack of knowledge about the mechanisms behind this pattern, much of this decline has been attributed to the loss, degradation, and fragmentation of mature forest on both the breeding and wintering grounds (robbins et al. 1992, Hamel 2000, Hamel et al. 2004) and potentially the conversion of agroforestry systems into low-quality nonbreeding habitats (e.g. colorado 2011, colorado & rodewald in review).

the scarcity of information on the species’ nonbreeding distribution (robbins et al. 1992) and on characteristics of landscapes and habitats in nonbreeding areas (Jones et al. 2000) in the northern andes led the cerulean Warbler technical group in 2002 to choose to address nonbreeding season issues (Dawson et al. 2012). a major activity of the subcommittee devoted to nonbreeding issues, el grupo cerúleo, has been the delineation of nonbreeding distribution. Barker et al. (2006) developed five hypothetical models of potential nonbreeding distribution of the cerulean Warbler based on existing historical and recent records and combined these models into a single representation of the locations with the highest probability of encountering the species in the nonbreeding period. colorado et al. (2008) developed a detailed protocol to field verify the accuracy and predictive power of this distributional map. the primary objective of this work was to produce a useful predictive understanding of cerulean Warbler distribution that could contribute to conservation of this species in northern andean landscapes, an activity subsequently initiated by el grupo cerúleo partners in colombia, ecuador, and peru (Skolnik et al. 2012).

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org/), a free, downloadable mapping program (Hijmans et al. 2004, 2012). after acquiring this information, we formed and trained field crews in Venezuela, colombia, ecuador and peru who logistically supported the effort. local environmental and civil police/military authorities were contacted to get information on potential public disorder present in every area. Finally, we used gpS navigators to locate the center of every pixel. the rigorous random sampling approach to site selection in this project meant that the time required to reach the individual pixels frequently was greater than the amount of time required to sample them.

Field surveys were conducted during September-March of 2006 to 2010. no surveys were conducted after the middle of March when spring migration of cerulean Warblers could significantly alter probability of detection of the species. the surveys involved both area searches throughout the pixels and three 100-m transects, each located within relatively homogeneous habitat within the pixel. each transect was walked one or more times at a slow pace, during which, transect surveys all birds observed were recorded (colorado et al. 2008).

reSUltS

one hundred thirty-six 1-km2 pixels were fully surveyed in colombia (n 5 84), Venezuela (n 5 40), ecuador (n 5 9) and peru (n 5 3), representing 68% of all sites initially selected. Some pixels were easily accessed by road, while others required several days of difficult foot or mule travel (e.g. Serranía de los Yariguíes natural national park in colombia, Sangay national park in ecuador, Macizo del turimiquire in Venezuela). the remaining 64 pixels were not visited because of excessive time and distance to reach pixels (perú, n 5 17; Venezuela, n 5 14; colombia, n 5 1; ecuador, n 5 1), refusal of political entities in

control of the land to permit accessor safety concerns (colombia, n 5 25; Venezuela, n 5 6).

of the 136 visited sites, 97 showed some degree of deforestation, mainly concentrated in Venezuela and colombia. grazing was detected in 54 pixels, followed by agriculture (n 5 34) and illicit crops (n 5 3). Some degree of political instability was detected in approximately 37 visited pixels across the entire range, with landmines apparently present in 7 surveyed pixels. Finally, illegal mining was identified in 19 pixels.

Avian communities. We accumulated more than 26,000 records of 484 avian species from 41 families during 1935 surveys along 100-m transects. Most represented avian families were tyrannidae (N 5 45 species) and thraupidae (N 5 40 species). of the 32 neotropical-nearctic migratory bird species recorded, 20 (63%) including cerulean Warbler, were observed within mixed-species flocks. Blackburnian Warbler (Setophaga fusca) was the most abundant bird species recorded with 180 records during surveys, followed by red-eyed Vireo (Vireo olivaceus; 112 records) and Yellow Warbler (Setophaga petechia; 57 records). cerulean Warbler was the 14th most abundant migratory bird across the survey locations (colorado 2011, colorado & rodewald in review).

Cerulean Warbler occurrence. We detected cerulean Warblers in 23 of 136 surveyed pixels (17% naïve presence, uncorrected for imperfect probability of detection). the species was recorded on both western and eastern slopes of the andes as well as in isolated geographic ranges. it was regularly found at elevations higher (. 2000 m) than typically reported in the literature (; 600-1600 m; Fig. 1), including in andean oak (Quercus humboldtii) forests. cerulean Warbler showed a strong association with mixed-species flocks (88% of sightings; c2 5 9.9, d.f. 5 3, P , 0.05), recorded with

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approximately 100 flocking species, eight of them regional endemics.

Important areas for Cerulean Warbler in the Andes. areas with high levels of presence of cerulean Warbler (. 50% naïve presence) in colombia including subtropical forests of the Serranía de los Yariguíes natural national park, coffee (Coffea arabica) and cacao (Theobroma cacao) shade plantations in southern antioquia and caldas Departments, and montane forests in northern antioquia. in Venezuela, shade coffee plantations and secondary forests on the Mérida cordillera (Fig. 2) showed high levels of cerulean Warbler presence.

Habitat types. typical remaining andean forest landscapes were represented in the surveyed pixels, where we identified and surveyed five major habitat types: mature forest, secondary forest, shade coffee, pastures with isolated trees and successional. the only areas with extensive

forest cover were Serranía de los Yariguíes natural national park in colombia, Sangay national park in ecuador and cerro el trueno in el callao Municipality, trujillo State, Venezuela, with cerulean Warbler not detected in the latter. cerulean Warbler showed a strong association to forested habitats, including different successional stages and agroforestry systems, and it was absent from habitats without tree component (F 5 7.98, d.f.5 4, P , 0.05; Fig. 3).

DiScUSSion

over 70% of the forests in the northern andes in colombia and ecuador have been deforested or highly altered by human activity (laestadius et al. 2011). Deforestation associated with the establishment of agriculture and silvopastoral systems, urbanization and selective logging represents a major threat for loss of biodiversity (Henderson et al. 1991, orejuela 2000). our field surveys of randomly selected locations

Fig. 1. altitudinal distribution of cerulean Warbler in the andes.

2600-27002500-26002400-25002300-24002200-23002100-22002000-21001900-20001800-19001700-18001600-17001500-16001400-15001300-14001200-13001100-12001000-1100

900-1000800-900700-800600-700500-600

0 0.05 0.1 0.15 0.2 0.25

Proportion

Surveyed

Occupied

Elev

atio

n (m

asl)

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Fig. 2. important areas of occurrence of cerulean Warbler in the andes. in colombia, subtropical forests of the Serranía de los Yariguíes natural national park (1), coffee and cacao shade plantations in southern antioquia and caldas departments (2), and the montane forests in northern antioquia (3). in Venezuela, shade coffee plantations and secondary forests on the Mérida cordillera (4). Base map shows models of occurrence developed by Barker et al. 2006.

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with differing political, economic, cultural and sociological conditions.

Since we began our study additional information about cerulean Warbler use of nonbreeding habitats has been developed, especially in Venezuela (Bakermans et al. 2009) and colombia (Sánchez-clavijo et al. 2008, 2009). Herzog et al. (2009) suggested that the birds may no longer be found in Bolivia. areas typically considered to be high-quality habitat for the cerulean Warbler, particularly large tracts of mature primary (robbins et al. 1992) or secondary forest or shade plantations (e.g. coffee, cardamom [Elatteria cardamomum]; Jones et al. 2002, Bakermans et al. 2009, Sánchez-clavijo et al. 2009, Botero et al. 2010, Bakermans et al. 2012),

in the Northern Andes support these findings, showing that deforestation, in particular for cattle production, is a major threat for habitat preservation; 71% of surveyed pixels exhibited some alteration. Moreover, we also detected activites associated with political instability such as illegal crops and landmines that may have detrimental effects on forest conservation. collectively, these factors must be seen as disturbing causes of habitat loss for both resident and migratory birds that rely on tropical montane forests, including the cerulean Warbler. interestingly, our effort also has shown that the design and implementation of conservation strategies for this species is embedded in a complex framework encompassing countries

FIG. 3. Cerulean Warbler density by habitat. Different letters indicate significant differences among habitats in anoVa at a = 0.05.

1

0.9

0.8

0.7

0.6

0.5

0.4

0.3

0.2

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0MatureForest

SecondaryForest

Shadedmonoculture

Silvopasture No trees

b

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a

c

Habitat type

Indv

/ha

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conclUSion

once completed, this work will improve our ability to identify and predict the most important locations for cerulean Warblers. in particular, results will aid design of nature reserves in the montane and premontane forests. the strong association between cerulean Warbler and agroforestry/silvopastoral systems suggests that conservation efforts can provide important socio-economic opportunities as well as ecological benefits. Research interest in cerulean Warblers provides an avenue to foster conservation initiatives within local communities that support both sensitive migratory and endemic bird species of the region as Santander et al. (2012) demonstrate. Further analysis of the data presented here will improve our understanding of cerulean Warbler distribution across its winter range and thereby contribute to conservation of this species in andean landscapes.

acKnoWleDgMentS

We thank the U.S. Forest Service, national Fish and Wildlife Foundation, national council for air and Stream improvement (ncaSi), and The Nature Conservancy for financial support to conduct this research. our gratitude extends to Fundación proaves, colombia, and to aves & conservación, ecuador. We recognize with sincere thanks the dedication and efforts of the many field assistants who contributed their energies to the success of what they fondly called “la maldición cerulea.” Jason Jones, Kim Smith, and paolo ramoni-perazzi provided comments that improved the quality of this document.

reFerenceS

Bakermans, M. H., a. c. Vitz, a. D. rodewald, & c. g. rengifo. 2009. Migratory songbird use of shade coffee in the Venezuelan andes with

coincide with those surveyed locations where the species was detected in most of the pixels of a cluster. thus, our survey results support the hypothesis that the species’ is related positively to the amount of forest cover at a regional scale, it is virtually absent from areas without trees. This suggests that maintenance of a sufficient amount of presumed high-quality habitat such as extensive forested tracts in both the breeding and nonbreeding range is the single most important conservation need for supporting the species. nevertheless, certain management systems, such as shade coffee and possibly silvopastures, have the potential to support this and other bird species of conservation concern. regional conservation efforts should further explore how these systems can be used to meet both ecological and social needs in human-dominated landscapes of the andes (e.g., Botero et al. 2010, Fundación proaves et al. 2010). the strong degree of association of the cerulean Warbler with other resident and migratory birds in mixed-species flocks reflects the additional need for a multispecies approach to conservation of avian and other resources in andean landscapes as pivotal to successful conservation of cerulean Warbler.

We continue to analyze the bird count data using the techniques of occupancy modeling (MacKenzie et al. 2006). our modeling will estimate the rate of occupancy, corrected for imperfect probability of detection, for localities based on their prediction by Barker et al. (2006) as suitable (predicted by five models) or less suitable for cerulean Warbler (predicted by three or fewer models).

Further study of the distribution of the species in the andes is warranted, especially in the southern part of the modeled range. the imperfect knowledge of the distribution of the birds is reflected by the recent observations of individual cerulean Warblers in Bolivia (tobias & Seddon 2007, Quillen Vidoz, pers. com.), after Herzog et al. (2009) failed to find the species in Bolivia.

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Fundación proaves, american Bird conservancy & el grupo cerúleo. 2010. conservation plan for the cerulean Warbler on its nonbreeding range—plan de conservación para la reinita cerúlea sobre su rango no reproductivo. conserv. colomb 12: 1–62.

Hamel, p. B. 2000. cerulean Warbler (Dendroica cerulea). In poole, a., & F. gill (eds). the Birds of north america, no. 511. the birds of north america, inc., philadelphia, pennsylvania, USa.

Hamel, p. B., D. K. Dawson, & p. D. Keyser. 2004. How we can learn more about the cerulean Warbler (Dendroica cerulea). auk 121: 7–14.

Henderson a., S. p. churchill, & J. l. luteyn. 1991. neotropical plant diversity. nature 351: 21–22.

Herzog, S. K., V. H. gárcia-Solíz, & S. e. Da-vis. 2009. Status of the cerulean Warbler (Dendroica cerulea) at the southern terminus of its non-breeding range, with a review of other nearctic-neotropical migrant parulidae in Bolivia. ornitol. neotrop. 20: 121–130.

Hijmans, r. J., l. guarino, c. Bussink, p. Mathur, M. cruz, i. Barrantes, & e. rojas. 2004. DiVa-giS Versión 4. Sistema de Información Geográfica para el análisis de datos de distribución de especies. Manual. http://www.diva-gis.org/docs/DiVa-giS4_manual_esp.pdf.

Hijmans, r. J., l. guarino, & p. Mathur. 2012. DiVa-giS Version 7.5. Manual. http://www.diva-gis.org/docs/DiVa-giS_manual_7.pdf.

Jones, J., p. ramoni-perazzi, e. H. carruthers, & r. J. robertson. 2000. Sociality and foraging behavior of the cerulean Warbler in Venezuelan shade coffee plantations. condor 102: 958–962.

Jones, J., p. ramoni-perazzi, e. H. carruthers, & r. J. robertson. 2002. Species composition of bird communities in shade coffee plantations in the Venezuelan andes. ornitol. neotrop. 13: 397–412.

laestadius, l., p. potapov, a. Yaroshenko, & S. turubanova. 2011. global forest alteration, from space. Unasylva 238: 8–13.

MacKenzie, D. i., J. D. nichols, J. a. royle, K. H. pollock, l. l. Bailey, & J. e. Hines. 2006. occupancy estimation and Modeling -

implications for conservation of cerulean Warbler. Biol. conserv. 142: 2476–2483.

Bakermans, M. H., a. D. rodewald, a. c. Vitz, & c. rengifo. 2012. Migratory bird use of shade coffee: the role of structural and floristic features. agrofor. Systs. 85: 85–94.

Barker, S., S. Benítez, J. Baldy, D. cisneros Heredia, g. colorado Zuluaga, F. cuesta, i. Davidson, D. Díaz, a. ganzenmueller, S. garcía, M. K. girvan, e. guevara, p. Hamel, a. B. Hennessey, o. l. Hernández, S. Herzog, D. Mehlman, M. i. Moreno, e. ozdenerol, p. ramoni-perazzi, M. romero, D. romo, p. Salaman, t. Santander, c. tovar, M. Welton, t. Will, c. pedraza, & g. galindo. 2006. Modeling the South american range of the cerulean Warbler. In proceedings of the 2006 eSri international User conference, San Diego, california, USa. available at proceedings.esri.com/library/userconf/proc06/papers/papers/pap_1656.pdf

Birdlife international. 2004. threatened birds of the world 2004. cD-rom. Birdlife international, cambridge, UK.

Botero, J. e., a. M. lópez, r. espinoza, & c. casas. 2010. aves de zonas cafeteras del sur del Huila. Federación nacional de cafeteros de colombia – cenicafé, caldas, colombia. Disponible en http://www.cafesanisidro.com/site/librodeaves.pDF

colorado, g. J. 2011. ecology and conservation of neotropical-nearctic migratory birds and mixed-species flocks in the Andes. Ph.D. diss. Ohio State Univ., columbus, ohio, USa. available at http://etd.ohiolink.edu/send-pdf.cgi/colorado%20gabriel%20J.pdf?osu1291646331/ [accessed 25 January 2012]

colorado, g., p. Hamel, a. rodewald, & W. thogmartin. 2008. el grupo cerúleo: collaboration to assess nonbreeding range of cerulean Warbler in South america. ornitol. neotrop. 19(Suppl.): 521–529.

Dawson, D. K., t. B. Wigley, & p. D. Keyser. 2012. cerulean Warbler technical group: coordinating international research and conservation. ornitol. neotrop. 23(Suppl.): 279–285.

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157 in t. rich, M. del coro arizmendi, c. thompson, & D. Demarest, (eds.) proceedings of the 4th international partners in Flight conference, Mcallen, texas, 13-16 Feb 2008. available at http://www.pwrc.usgs.gov/pif/pubs/Mcallenproc/articles/piF09_Bird%20communities/Sanchezclavijo_piF09.pdf

Santander, t., a. Soria, & e. a. guevara. 2012. conservando el hábitat invernal de la reinita cerúlea (Setophaga cerulea) en ecuador. ornitol. neotrop. 23(suppl.): 343–350.

Skolnik, B., D. Wiedenfeld, r. Dettmers, c. aucca, l. Daza, H. Valle, F. Sornoza, J. robayo, D. Diaz, J. Fitzgerald, D. lebbin, & p. B. Hamel. 2012. conservation planning and accomplishments for protection of cerulean Warbler (Setophaga cerulea) nonbreeding habitat. ornitol. neotrop. 23(Suppl.): 319–329.

tobias, J. a., & n. Seddon. 2007. nine bird species new to Bolivia and notes on other significant records. Bull. Br. ornithol. club 127: 49–84.

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robbins, c. S., J. W. Fitzpatrick, & p. B. Hamel. 1992. a warbler in trouble: Dendroica cerulea. pp. 549–562 in Hagan iii, J. M., & D. W. Johnston (eds). ecology and conservation of neotropical Migrant landbirds. Smithsonian institution press, Washington, D.c., USa.

Sánchez-clavijo, l. M., r. espinosa, J. e. Botero, a. M. lópez, & n. g. Franco. 2008. la reinita cerúlea: una especie que depende del café y del carbón. Biocarta 13, cenicafé, chinchiná, caldas, colombia.

Sánchez-clavijo, l.M., J.e. Botero, & r. espinosa. 2009. assessing the value of shade coffee for bird conservation in the colombian andes at a local, regional, and national level. pp. 148–

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CONSERVATION PLANNING AND ACCOMPLISHMENTS fOR PROTECTION Of CERULEAN WARBLER (sEtOphAGA

CErulEA) NONBREEDING HABITAT

Benjamin Skolnik1, David Wiedenfeld1, Randy Dettmers2, Constantino Aucca3, Lina Daza4,

Heidy Valle4, francisco Sornoza5, Javier Robayo5,6, David Diaz7, Jane fitzgerald1,

Daniel Lebbin1, Paul B. Hamel8

1American Bird Conservancy, 1731 Connecticut Ave, Washington, DC, 20009, U.S.A. E-mail: [email protected]

2Division of Migratory Birds, U.S. Fish and Wildlife Service, 300 Westgate Center Drive Hadley, MA 01035

3Asociación Ecosistemas Andinos ECOAN, Urb. La Florida D-1B, Wanchaq, Cusco, Perú 4Fundación ProAves, Cra. 20 Nro. 36-61 Bogotá D.C., Colombia

5Fundación Jocotoco, Lizardo García E9-104 y Andrés Xaura, Quito, Ecuado 6 EcoMinga Foundation, Ecuador

7Aves y Conservación, Psje. Joaquín Tinajero E3-05 y Jorge Drom, Quito, Ecuador 8U.S Forest Service Center for Bottomland Hardwoods Research, P. O. Box 227, 432

Stoneville Rd. Stoneville, MS 38776 USA

Resumen. – Planificación y Logros de Conservación para la Protección del Hábitat durante la Tem-porada No Reproductiva de la Reinita Cerúlea. – La colaboración entre miembros del Grupo Técnico de la Reinita Cerúlea ha sido muy importante para la evaluación del estatus de la población, coordinar la plani-ficación de actividades futuras, y principalmente implementar acciones de conservación. Logros al presente incluyen una estrategia general para la conservación y manejo de la especie a través de su rango, un plan para la conservación de poblaciones no reproductivas incluyendo hábitats a nivel de paisaje, y un análisis sobre la economía de las comunidades locales. Desde entonces se han logrado implementar acciones de conservación en 355.701 ha que representa hasta 2% del rango no-reproductivo y beneficiando 35.570 individuos en la zona invernal en Sudamérica. Recomendamos mayor coordinación entre stakeholders para facilitar replicación e incremento de acciones de conservación en 4,4 millones ha adicionales para lograr la meta de doblar la población hasta 1.000.000 individuos. También, pedimos que la comunidad científica re-alice investigación en los mismos sitios que los proyectos de conservación para contribuir información sobre el monitoreo y la biología que serviría para adaptar las estrategias de conservación.

Abstract. – Vital to the work of the Cerulean Warbler Technical Group has been the collaboration among mem-bers to evaluate population status and coordinate planning for future activities, principally in conservation imple-mentation. Two plans have been produced, one a general strategy for the conservation and management of the species over its entire range, and a more restricted plan for conservation of non-breeding populations, their landscapes, and the economic vitality of the local communities. In the process several notable conservation im-plementation successes have been achieved affecting nearly 355,701 ha affecting as much as 2% of the species non-breeding range and benefiting an estimated 35,570 Cerulean Warblers on their non-breeding range in South America. We recommend increased coordination among stakeholders to enable the replication and scaling up of conservation actions on an additional 4.4 million ha, which will help achieve the stated goal of doubling the population to 1,000,000 individuals. Also, we urge the scientific community to engage in research at conservation project sites to contribute vital monitoring and biological information to adapt conservation strategies.

Key words: Conservation partnerships, Cerulean Warbler, wintering ground

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areas so as to increase local awareness and participation in conservation.

loss of suitable habitat along migratory pathways and in South america are clear threats (Hamel 2000), although low reproduction rates in fragmented landscapes on the breeding grounds may not be adequate to increase populations (Buehler et al. 2008). the two plans broadly detailed threats and limiting factors to the species across its entire range, highlighting a list of ten and five priorities, respectively. although considerable gaps exist in knowledge of the cerulean Warbler’s life history and threats, the information in the Plans has been sufficient to engage in preliminary conservation actions. the cWtg established a conservation objective of restoring cerulean Warbler populations to their levels in the 1980s, by doubling the current population. this paper documents on-the-ground efforts to deliver protection to the cerulean Warbler with particular emphasis on the non-breeding range a decade after the formation of cWtg. We suggest that although considerable investment has been made in a variety of projects in northern South america, more emphasis needs to be given to coordinating current projects, to improved evaluation of conservation projects as well as to careful scientific monitoring of effects on cerulean Warblers, and to replicating and expanding the scale of projects.

MetHoDS

pilot cerulean Warbler wintering ground conservation projects were undertaken in colombia, peru and ecuador based on hotspots within the distribution of the species in its non-breeding range (Barker et al. 2006). the map and geographic descriptions presented in the non-breeding plan highlight these potential hotspots by modelling natural forest remnants of the northern andes at the warbler’s preferred elevation (Josse et al.

introDUction

the dramatic decline of the cerulean Warbler (Setophaga cerulea) places the species among north america’s most rapidly declining neotropical migrant songbirds. numbers have decreased by almost 70% since 1966, and the species is listed as Vulnerable by iUcn (Birdlife international 2008). cerulean Warblers have experienced the steepest declines of any wood warbler in the United States, 3.2% per year for 40 years, 1966-2005 (Sauer et al. 2011). in recognition that a continuous, concerted, and collaborative multi-national effort was necessary to determine the cause of population declines and to coordinate an effective response over a large area, the cerulean Warbler technical group (cWtg) formed in 2001. Concentrated field surveys from 2003-2008 on the non-breeding grounds in central and South america contributed to improved knowledge of the species distribution. a petition to list the species by the United States Fish and Wildlife Service (USFWS) as a threatened species was found not warranted in 2006; however the compilation and analysis of existing information informed the creation of the USFWS conservation action plan (USFWS 2007). in 2010, a conservation plan for the cerulean Warbler on its non-breeding range, hereafter called the “non-breeding plan,” was written by paula caycedo for Fundación proaves (colombia) with input from members of grupo cerúleo, a subcommittee of the cWtg (Fundación proaves et al. 2010). respectively, the plans produced a general strategy for the conservation and management of the species over its entire range and a more detailed plan for conservation of non-breeding populations. the non-breeding plan addresses actions to increase the habitat value to cerulean Warblers of the landscapes in which the birds occur, as well as to maintain and improve the economic vitality of the local communities in these

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2008) with localities of over five hundred historic and recent observations of cerulean Warblers. to restore degraded landscapes and create habitat, trees were planted in a variety of treatments including reforestation plots of mixed native species, silvopastures, living fences, and agroforestry systems where shade coffee and other crops are produced. nurseries were established on community and private lands to produce the necessary saplings. trees were planted on community and private lands in peru, on farms and private forested areas in peru and colombia, and on degraded areas within protected areas owned by Fundación Jocotoco, ecoan and Fundación proaves in ecuador, peru and colombia, respectively.

in these projects a variety of methods were used to encourage landowners and community members to participate in reforestation and promote long-term stewardship of trees, including regulation and incentives. local institutions in peru, comunidades campesinas, offered strict rules for participation and required beneficiaries to attend meetings, work in nurseries and group tasks (faenas), and pay penalties for violating signed agreements. contracts were signed in peru and colombia with beneficiaries when saplings were delivered for planting that stipulated proper care and consequences for high plant mortality. conservation easements were included in the deeds of landowners in colombia for periods up to 15 years. Direct incentives given to beneficiaries included tree saplings (often fruiting or forestry species were desirable to landowners because of their commercial value), technical training, cement for irrigation systems, fencing, and signs for conservation easements. an outreach component allowed implementing partners to educate participants on the structure of these reforestation programs and the variety of benefits of reforestation and habitat protection.

additional landscape level projects conducted by industry, e.g., Biodiversity and

coffee growing program, national coffee Federation, colombia; by governments, e.g., Socio Bosque, Ecuador; non-profit groups, e.g., corredor de conservación guantiva- la rusia- iguaque, Fundación natura, the nature conservancy and others, colombia; or regional efforts spanning several countries, e.g., ecoregional strategy to conserve the Spectacled Bear (Tremarctos ornatus) in the northern andes (rodríguez et al. 2003) did not set out explicitly to benefit Cerulean Warblers but employed conservation strategies that likely benefit the species in its non-breeding range.

We also evaluated the extent of overlap between the modeled nonbreeding range of cerulean Warbler from Barker et al. (2006) and two sources of information about conservation areas in the nonbreeding range, the important Bird areas (iBa) of the andes (Birdlife international & conservation international 2005), and the World Database on protected areas (WDpa) in the andean countries (iUcn & Unep-WcMc 2010). We intersected the modeled nonbreeding range with digital maps of the iBa and WDpa in arcMap 10 (eSri 1999–2010). We estimated the area contained in iBas projected as nonbreeding habitat by four or five models of Barker et al. (2006), and calculated the proportion of nonbreeding range included in iBas, or in WDpas, from these area values using SaS 9.2 (SaS institute 2002–2008). The shapefile of IBAs was obtained from amiro perez-leroux and Francisco prieto in the Birdlife international Americas Regional Office in Quito, Ecuador. that of the WDpa was downloaded from (iUcn & Unep-WcMc. 2010).

reSUltS

of 455 iBas listed in Birdlife international & conservation international (2005), 433 were included in the modeled nonbreeding range of cerulean Warbler. Slightly more than half of the iBas, n 5 226 iBas, were predicted to

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have habitat for cerulean Warbler by at least four of the five models used by Barker et al. (2006), representing all the countries (Bolivia, n 5 2; colombia, n 5 91; ecuador, n 5 52; peru, n 5 35; and Venezuela, n 5 46). these iBas include 26% of the 600,000 km2 of andean landscape predicted as habitat by at least four of the models used by Barker et al. (2006). a smaller number, n 5 162 iBas, include areas predicted by all five of the models as habitat for the species, and account for 22% of the 173,000 km2 projected as habitat by all five of those models.

of 836 areas in the WDpa listed in iUcn & Unep-WcMc. (2010), n 5 391 were predicted to have habitat for cerulean Warbler by at least four of the five models used by Barker et al. (2006), representing all the countries (Bolivia, n 5 4; colombia, n 5 143; ecuador, n 5 65; peru, n 5 30; and Venezuela, n 5 149). these WDpas include 59% of the 600,000 km2 of andean landscape predicted as habitat by at least four of the models used by Barker et al. (2006). a smaller number, n 5 261 WDpas, include areas predicted by all five of the models as habitat for the species, and account for 42% of the 173,000 km2 projected as habitat by all five of those models.

conservation actions were undertaken on 355,701 ha in various pilot and landscape level projects in areas with predicted presence and documented high densities of cerulean Warbler in colombia, peru and ecuador. this area represents just over 0.5% of the 60,257,000 hectare non-breeding range based upon the sum of the area predicted by at least four of the five models employed by Barker et al. (2006). However, wintering habitat may be occupied at only 17% capacity, 10,000,000 ha, and considering that projects focused on areas of relatively high abundances of cerulean Warbler, perhaps as much as 3.6% of the occupied range was affected in the conservation projects reported here (colorado

et al. 2012). We treat the project areas by country.

Colombia. the Serranía de Yariguies, Santander Department, had the highest number of cerulean Warblers reported in colombia (Fundación proaves et al. 2010). in 2005, Fundación proaves established the 10 kilometer cerulean Warbler corridor linking the Yariguíes national park to cerro de la paz. Habitat protection strategies in the corridor include engaging landowners in reforestation and conservation easement programs as well as expanding three private protected areas, pauxi pauxi, cerulean Warbler and niceforo’s Wren reserves. landowners included 13 tracts, totaling 130 ha, as conservation easements into the deeds (Fundación proaves 2011a). these easements required a ban on timber harvesting and hunting and protection of existing forest in exchange for saplings for reforestation and other incentives (e.g. fencing to restrict cattle from forested areas). to date nearly 200,000 trees were planted on over 400 ha of shade coffee and cacao in two multi-year neotropical Migratory Bird conservation act projects (Fundación proaves 2011b). an alliance with local government and surrounding communities to support the corridor was established through the Yaré project, which contributes to reforestation and the restoration of the historic lengerke stone path that will be promoted as an ecotourism route. expansion of the corridor will take place in a three year project beginning in 2012 to reforest 150,000 trees on an additional 450 ha of agricultural lands. Forested lands and degraded lands targeted for restoration were acquired in the corridor, resulting in over 3,000 ha of land under private protection since 2005. land acquisition has also taken place in the northern central andes of colombia, another area noted for high cerulean Warbler concentrations, at arrierito anitqueño reserve (1,500 ha in 2010). in

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the corredor de conservación guantiva- la rusia- iguaque, the oak conservation corridor in colombia, Fundación natura colombia conducts activities designed to conserving oak (Quercus humboldtii and Colombobalanus excelsa); this project has protected and recuperated as well as promoted sustainable use on 52,122 ha of forests (cardenas & avella Muñoz 2007 & 2009).

the colombian national coffee Federation has conducted numerous initiatives restoring or protecting 75,500 ha of habitat within the cerulean Warbler range. For instance, along the Magdalena river basin, 65,000 ha have been reforested in the last twenty years and plans include planting another 7,000 ha in 2012. another initiative in nariño, Quindío, and Valle de cauca departments established 450 ha of biodiversity conservation corridors. Begun in 1991, the ecological coffee Fund has created 3,962 ha of protected areas as well as restored 1,600 ha and acquired 8,000 ha of forest in important watersheds. in addition to direct habitat creation or protection, the Federation certified 27,000 ha of coffee farms with environmentally friendly practices thus far in a four year project begun in 2010. not all certified coffee has equal benefits for Cerulean Warbler, but environmental certifications have direct benefits to habitat because of reduced pollution, watershed protection, shade trees, and other factors (Fischersworring 2008, lópez lópez et al. 2012).

Ecuador. the area of greatest documented concentration of cerulean Warblers in ecuador lies along the eastern slope of the andes. in 2006, the Jocotoco Foundation established the narupa reserve, napo province, which was subsequently expanded to 596 ha. private reserves maintained by ecoMinga Foundation also have multiple records of cerulean Warblers and provide habitat protection for the species. efforts are underway to work in the areas surrounding these private reserves

and engage communities in habitat protection in the buffer areas of several large national parks (Santander et al. 2012). cerulean Warbler occurs between 900 and 1400 m on the eastern slope of the andes in Zamora chinchipe province in southern ecuador (andrade et al. 2006). this area includes the tapichalaca reserve owned by Fundación Jocotoco. the reserve comprises 3,252 ha; since 2009 85,100 trees of 17 species were planted on acquired properties there with degraded habitat (Fundación Jocotoco 2011). on the western slope, Fundación Jocotoco also manages the 1,947 hectare río canandé reserve, where cerulean Warblers have been observed as well (lebbin pers. observ.).

the Socio Bosque program pays direct monetary incentives per hectare to private and community landowners to maintain forest cover; and through December, 2011 883,223 ha were protected through 1,563 contracts with 90,162 community and private landowners beneficiaries (Ministerio del ambiente 2012). of the total area affected, 25,154 ha are montane forest and constitute suitable cerulean habitat.

Peru. Most peruvian records of cerulean Warbler are from the northern departments. conservation efforts led by ecoan in northern peru include regional conservation planning, reforestation programs across the department of amazonas, promotion of shade coffee and silvopasture, education of local communities about migratory birds, and establishment and improvement of management of private and public protected areas. ecoan established the abra patricia-alto nieva private conservation area and 40-year term abra patricia-alto nieva conservation concession which total over 9,800 ha (angulo et al. 2008). ecoan also works with various community, local, and national government agencies to improve management of natural resources and

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condition and survival of the cerulean Warbler by protecting and improving non-breeding habitat in South america. the overall goal is to restore cerulean Warbler populations to 1980s levels and double population sizes from 560,000 estimated to exist in 1995 (rich et al. 2004) to 1,000,000 individuals.

in areas of key habitat, densities as high as 0.83 cerulean Warbler per ha has been documented (Jones et al. 2000). to get some idea as to the scale of number of hectares that would have to be affected by conservation measures, including both protection of already-existing habitat and restoration of habitat to make it suitable for wintering cerulean Warblers, we can make an estimate using some assumptions of distribution and abundance. assuming that the birds occur at a much lower density of 0.1 birds per ha average abundance in the areas affected by this conservation activity, approximately 10 million ha of wintering habitat would be required to meet the goal of 1 million individuals. the population of 560,000 (rich et al. 2004) would likely occupy 5,600,000 ha (560,000 individuals / 0.1 individuals per ha) of existing habitat, of which only part is protected. to achieve the goal of 1 million birds would therefore require about 4,400,000 ha of new, restored or improved habitat, assuming that there are no further losses in existing habitat, plus efforts to protect much of previously-existing 5,600,000 ha against losses. However, if we consider that cerulean Warblers are often more densely populated in key areas, then conservation on these lands would have a disproportionately larger effect on the overall population. the conservation efforts on 355,701 ha described in this paper are a significant first step towards this goal. Using the conservative figure of 0.1 birds per ha, conservation may have benefited up to 35,570 cerulean Warblers on 2% of the winter range.

cerulean Warblers may have a strong affinity to successional forests and agroforestry systems, such as shade coffee; and proximity to

the adjacent 182,000 hectare Bosque de protección alto Mayo, and establish future protected areas. the area has several records of cerulean Warbler and is indicated as an area of high probability in the non-breeding plan. the species may arrive to the Mayo river Valley in the fall moving to higher elevation through the Bosque de protección alto Mayo and then on to the upslope habitat at the abra patricia-alto nieva reserve and concession (aucca pers. observ.). Since 2004, a sustained reforestation campaign working with six community nurseries resulted in the planting of 810,253 native trees and shrubs of over 40 species and coffee bushes on roughly 300 ha in mixed forest, shade coffee, silvopasture and living fences systems on private or community-owned lands surrounding reserves managed by ecoan. in 2010, rainforest alliance, cenicafe, and el grupo cerúleo conducted workshops for peruvian coffee growers as an outreach resulting from the cerulean Warbler -golden-winged Warbler Summit in Bogota in 2008 (gabriel colorado and Jorge Botero, unpubl. data). these activities were conducted in tandem with model validation work on the non-breeding season model (colorado et al. 2008, 2012).

Venezuela. although areas of importance were identified in Venezuela, particularly in the Mérida cordillera (Jones et al. 2000, Bakermans et al. 2009, colorado et al. 2012), and many areas were revealed through the analysis of iBas and WDpa areas, we regret that no implementation actions were recorded specific to Cerulean Warbler conservation and we look forward to including this information in the future.

DiScUSSion

conservation projects began to address the first objective of the Non-breeding Plan that calls for the improvement of the physiological

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coffee industry and ecuadorian government will similarly bring long-term benefits from forest protection. these programs began as landscape scale, well-funded initiatives that impacted comparatively large areas. in contrast to the non-profit groups’ projects, their primary focus was economic benefits that resulted in improved livelihoods to hundreds of thousands of people. One-fifth of the incentives paid to landowners ($1.2 million USD through Dec 2011) have been re-invested in conservation or territorial consolidation that helps limit land invasions (Koning et al. 2011). given the urgency of habitat protection in the face of rapid deforestation, industry and government programs can provide a useful tool to affect change. Furthermore, these programs can provide a complement to site-specific projects because enrollment is open to private landowners. For example, coffee growers in the cerulean Warbler corridor can participate in the colombian national coffee Federation initiatives and the private landowners surrounding the narupa reserve in ecuador can enroll their forests in the Socio Bosque program.

the success of conservation efforts depends on good communication, outreach, and education of appropriate audiences. these build public awareness and support for bird conservation necessary to accomplish our goals for improving the status of species like the cerulean Warbler. education programs such as the Migratory Bird Festivals hosted in the cerulean Warbler corridor in colombia and educating farmers about the benefits of cultivating shade-grown coffee are two examples of efforts to address this issue.

Multi-national projects have provided a platform for the implementing partner groups to share best practices and replicate or adapt tactics to best fit realities in the field (American Bird Conservancy 2011). For instance, following a best-practices workshop held by american Bird conservancy in peru,

large contiguous forests may be an important factor as well (colorado et al. 2012). given variations in habitat quality, future non-breeding ground conservation actions should continue to focus on areas of documented high abundance of cerulean Warblers. pilot projects focused on sites that support high densities of cerulean Warblers employed two primary strategies: 1) maintenance of existing natural forest through easements and land acquisition, and 2) restoration of degraded areas through the promotion of shade-grown coffee, agro-forestry, silvopasture and reforestation. additional programs were identified that have direct benefits on Cerulean Warbler habitat through acquisition or direct payments to landowners for forest protection as well as restoration through reforestation.

the variety of efforts conducted to date provides a rich base of experience to guide future actions and evaluate and adapt the planning documents. initiatives in colombia, Ecuador and Peru carried out by non-profit conservation groups began with acquisition, restoration and protection of private lands. these institutions later incorporated landscape approaches that integrated surrounding communities and public protected areas. a long-term institutional presence provided opportunities to engage communities and build trust as well as build expertise in the field of reforestation. Besides the lasting benefits of environmental services provided by reforestation, including erosion control, nutrient retention and watershed protection, beneficiaries also received direct incentives and the commercial value of fruiting tree species. private reserves and reforestation programs, in particular, provided multiple benefits to residents. For instance, in the last decade, reforestation programs in three countries employed 55 individuals year-round and provided an additional 2,250 seasonal jobs (american Bird conservancy 2011). programs conducted by the colombian

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the colombian national coffee Federation, has carried out research on cerulean Warblers in coffee plantations (Sánchez-clavijo et al. 2008, 2009, Botero et al. 2010) and maintains ornithologists on staff who could provide vital research on the warblers in the Biodiversity and coffee growing program. previously, monitoring has been limited to gauging the successful implementation of project activities such as survival of tree species, easements signed and ha acquired, and avian monitoring was not conducted in part because of limited project funding. Monitoring is planned for 2012-2013 in the cerulean Warbler corridor in colombia. Wintering cerulean Warblers are generally difficult to detect and never abundant, and thus considerable time and expertise is needed in the field to complete a thorough monitoring program. Members of the cWtg and the ornithological community could bolster the efficacy of conservation programs by conducting research at project sites. research questions might ideally focus on the number of cerulean Warblers supported by different habitat protection strategies, noting habitat type and proximity to contiguous forests, so that more broad questions can be answered regarding the amount and type of habitat required to restore population levels of the 1980s (Hamel et al. 2012). an example of this sort of collaboration already exists in the case of cerulean Warbler records from reserves owned by Fundación proaves contributing to baseline estimates of occupancy (Hamel pers. observ.). these synergies could feed cerulean Warbler monitoring data back into conservation programs to assess and adapt strategies.

one success of the cWtg and grupo cerúleo is the collaborative spirit that these efforts have encouraged among stakeholders. increasingly, interest is growing among individuals and institutions for migratory bird conservation. pilot projects discussed here have attracted new support, such as Fondo

Fundación Jocotoco planned to implement a model agroforestry plot for teaching local landowners in ecuador; and Fundación proaves staff began implementing formal agreements with beneficiaries who received trees from colombian nurseries because these agreements increased landowners’ commitment to caring for the saplings. Migratory bird projects in multiple countries must manage for multiple species (cerulean Warbler is not the only high priority species on most of these properties). Because of the diversity of ecosystems, implementation varied considerably in these projects given the need to adapt similar initial approaches to specific local circumstances.

although the objectives in the cerulean Warbler non-breeding plan are of necessity general in calling for conservation actions and protection of wintering areas, many sites identified in the Plan have yet to receive conservation action. For instance, no known conservation was noted in Venezuela, the upper napo province of ecuador, or western slope of the eastern andes or the southern region of the eastern slope of the central andes in colombia, all potentially important non-breeding destinations of cerulean Warbler. given the dispersed range of the cerulean Warbler, a challenge of this study was to fully consider the impact of all projects. the growing portfolio or reducing emissions from Deforestation and Forest Degradation projects (Hübenthal et al. 2010), the contribution of national park systems, industry initiatives by foresters, cattle ranchers, fruit growers and cacao farmers need further analysis and consideration.

Unfortunately, none of these conservation projects conducted monitoring of cerulean Warblers or other migratory songbirds to assess the status of the species. in the case of Socio Bosque, Koning et al. (2011) note that no monitoring of biological indicators has taken place. cenicafé, the research center of

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important contributions of different entities, governmental, nongovernmental, commercial, and individual, to the conservation effort for the species.

acKnoWleDgMentS

We are grateful for the support from the cerulean Warbler technical Working group, grupo cerúleo, amos Butler audubon Society, association for Fish and Wildlife agencies Southern Wings, conservation leadership programme, elisha Mitchell audubon Society, gordon and Betty Moore Foundation, national Fish and Wildlife Foundation, organization of american States, robert Wilson and other private individuals, United Stated Fish and Wildlife Service, neotropical Migratory Bird conservation act program, United States Forest Service, Western Hemisphere Migratory Species initiative, and World land trust. We are indebted to Francisco prieto and amiro perez-leroux of the staff of Birdlife international, Quito, ecuador, for supplying digital maps of important Bird areas for us to use, and to Fabio Spiazzi for assistance with the calculations of areas. the manuscript benefitted from the comments of David Mehlman, Ken rosenberg, and tito Vilella.

reFerenceS

american Bird conservancy. 2011. inter-partner exchange and lessons learned Workshop on reforestation & community engagement. abra patricia, peru.

andrade p., galvez J., rodas F. & Sarango F. 2006. Determinación de la presencia y Distribución de cerulean Warbler (Dendroica cerulea) en el sur de ecuador. http://www.srs.fs.usda.gov/egc/research/projects/Surveyrpts2006/informe%20Dendroica%20cerulea_andrade_2006.pdf

angulo p., F., W. palomino c., H. arnal, c. aucca, & Ó. Uchofen. 2008. corredor de conservación de aves Marañon-alto Mayo:

para la acción ambiental support for cerulean Warbler corridor in colombia. new initiatives such as Southern Wings, a cooperative program coordinated by the association for Fish and Wildlife agencies that links state wildlife agencies with neotropical migratory bird projects in the tropics and the american Bird conservancy’s Migratory Bird program will drive continued growth of larger-scale, multi-national projects. national programs like Socio Bosque in ecuador are gaining interest in other countries, such as peru. in coming years, emphasis should be given to coordination among non-governmental, government and industry stakeholders on the non-breeding grounds as our analysis suggests current conservation initiatives are complimentary and strong alliances can be formed to strengthen one another’s programs. Efforts should be made to specifically expand conservation programs to the landscape scale to connect large forest blocks where cerulean Warblers seem to be more densely populated (colorado et al., 2012).

next steps needed to continue improvement of cerulean Warbler conservation planning and non-breeding ground conservation efforts include: (1) adapt implementation of the existing conservation plans, and apply occupancy-based modeling approaches to refine the identification of potential and demonstrated hotspots for conservation; (2) identify existing projects that can be expanded in scale and replicated in other locations; (3) identify and assess the protection status of stop-over sites and application of strategies to assure the continued existence of the sites as good habitat into the future; (4) continue high quality scientific research to address the important gaps in our knowledge identified in the research arena; (5) coordinate international, national, regional and local stakeholders in the adaptation of the conservation planning approaches to fit local conditions; and (6) develop mechanisms to recognize the

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Barker, S., S. Benitez, J. Baldy, D. cisneros Heredia, g. colorado Zuluaga, F. cuesta, i. Davidson, D. Diaz, a. ganzenmueller, S. garcia, M.K. girvan, e. guevara, p.B. Hamel, a.B. Hennessey, o.l. Hernández, S. Herzog, D. Mehlman, M.i. Moreno, e. ozdenerol, p. ramoni-perazzi, M. romero, D. romo, p. Salaman, t. Santander, c. tovar, M. Welton, t. Will, c. pedraza, & g. galindo. 2006. Modeling the South american range of the cerulean Warbler. In proceedings of the 26th eSri international users conference, San Diego, ca.

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rodríguez, D. F. cuesta, i. goldstein, l. g. naranjo, & o. l. Hernández. 2003. estrategia ecorregional para la conservación del oso andino – Tremarctos ornatus – en los andes del norte. World Wildlife Fund, Fundación Wii, ecociencia, and Wildlife conservation Society. cali, colombia.

Sánchez-clavijo, l. M., r. espinosa, J. e. Botero, a. M. lópez & n. g. Franco. 2008. la reinita cerúlea: una especie que depende del café y del carbón. Biocarta 13, cenicafé, chinchiná, caldas, colombia.

Sánchez-clavijo, l.M., J.e. Botero, & r. espinosa. 2009. assessing the value of shade coffee for bird conservation in the colombian andes at a local, regional, and national level. pp. 148–157 in t. rich, M. del coro arizmendi, c. thompson, & D. Demarest, (eds.) proceedings of the 4th international partners in Flight conference, Mcallen, texas, 13-16 Feb 2008. available at http://www.pwrc.usgs.gov/pif/pubs/Mcallenproc/articles/piF09_Bird%20communities/Sanchezclavijo_piF09.pdf

Santander, t., a. Soria, & e. a. guevara. 2012. conservando el hábitat invernal de la reinita cerúlea (Setophaga cerulea) en ecuador. ornitol. neotrop. 23(suppl.): 343–350.

Sauer, J.r., J.e. Hines, J.e. Fallon, K.l. pardieck, D.J. Ziolkowski, Jr., & W.a. link. 2011. the north american Breeding Bird Survey, results and analysis 1966 - 2009 (version 3.23.2011). USgS patuxent Wildlife research center, laurel, MD. available at http://www.mbr-pwrc.usgs.gov/bbs/bbs.html [accessed 20 December 2011]

SAS Institute. 2002–2008. SAS 9.2 TS Level1M0, XP_pro platform. SaS institute, cary, nc, USa.

USFWS Division of Migratory Bird Management Focal Species program. 2007. a conservation action plan for the cerulean Warbler (Dendroica cerulea). http://www.fws.gov/migratorybirds/currentBirdissues/Management/FocalSpecies/plans/ceruleanWarbler.pdf

rosenberg, & J. Jones. 2012. passing the baton of action from research to conservation implementation for cerulean Warbler (Setophaga cerulea). ornitol. neotrop. 23(Suppl.): 367–378.

Hübenthal, a., Starnfeld F. & D. carrión. 2010. Field Dialogue on reDD readiness in ecuador. the Forests Dialogue, papallacta, ecuador.

iUcn & Unep-WcMc. 2010. the World Database on protected areas (WDpa). cambridge, UK: Unep- WcMc. available at: www.protectedplanet.net [accessed 20/04/2012)].

Jones, J., p. ramoni-perazzi, e. H. carruthers, & r. J. robertson. 2000. Sociality and foraging behavior of the cerulean Warbler in Venezuelan shade coffee plantations. condor 102: 958–962.

Josse c., cuesta F., navarro g., Barrena V., cabrera e., chacón-Moreno e., Ferreira W., peralvo M., Saito J. and tovar a. 2008. Mapa de ecosistemas de los andes del norte y centrales. Bolivia, colombia, ecuador, perú and Venezuela can, programa regional ecoBona, conDeSan-proyecto páramo andino, programa Bioandes, ecociencia, natureServe, lta- UnalM, iavH, icae-Ula, cDc-UnalM, rUMBol Srl. lima.

Koning F., M. aguinaga, M. Bravo, M. chiu, M. lascano, t. lozada, and l. Suarez. 2011. Bridging the gap between forest conservation and poverty alleviation: the ecuadorian Socio Bosque program.

lópez lópez, a. M., r. espinosa aldana, g. M. lentijo Jiménez, & J. e. Botero echeverri. 2012. Herramientas de manejo del paisaje para la conservación de la biodiversidad. avances técnicos cenicafé 416: 1–12.

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rich, t. D., c. J. Beardmore, H. Berlanga, p. J. Blancher, M. S. W. Bradstreet, g. S. Butcher, D. W. Demarest, e. H. Dunn, W. c. Hunter, e. e. iñigo-elias, J. a. Kennedy, a. M. Martell, a. o. panjabi, D. n. pashley, K. V. rosenberg, c. M. rustay, J. S. Wendt, & t. c. Will. 2004. partners in

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INTEGRATING CONSERVATION MANAGEMENT, SPECIES PROTECTION, AND ECONOMIC VIABILITy INTO

SUSTAINABLE LAND USE PRACTICES fOR THE CERULEAN WARBLER (sEtOphAGA CErulEA) IN THE APPALACHIAN

AND NORTHERN ANDES MOUNTAINS

Brian W. Smith1, Jorge Botero2, Jeff L. Larkin3, Amanda D. Rodewald4, Petra B. Wood5,

Patrick N. Angel6, & Scott E. Eggerud7

1Appalachian Mountains Joint Venture, 1900 Kraft Drive, c/o Conservation Management Institute, Blacksburg, VA 24061, U.S.A. Current address: U.S. Fish and Wildlife Service,

Division of Migratory Birds Management, P.O. Box 25486, Denver Federal Center, Denver, CO 80225-0486. E-mail: [email protected]

2Cenicafe-FNC, Kilometro 4 - Vía Antigua a Manizales, Manizales, Caldas, Colombia 3Department of Biology, Indiana University of Pennsylvania, 126 Weyandt Hall,

Indiana, PA, U.S.A. 4School of Environment and Natural Resources, The Ohio State University,

2021 Coffey Road, Columbus, OH, U.S.A. 5West Virginia Cooperative Fish and Wildlife Research Unit, Biological Resources Division,

U.S. Geological Survey, P.O. Box 6125, 320 Percival Hall, West Virginia University, Morgantown, WV, U.S.A.

6U.S. Department of Interior, Office of Surface Mining Reclamation and Enforcement, 421 West Highway 80, London, KY, U.S.A.

7U.S. Department of Interior, Office of Surface Mining Reclamation and Enforcement, P.O. Box 703, Ona, WV, U.S.A.

Resumen. – Prácticas sostenibles de uso de tierra para las Reinitas Cerúleas. – La región montañosa de los Apalaches en Norteamérica sostiene cerca del 80% de la población reproductiva global de la Reinita Cerúlea (Setophaga cerulea), mientras que los Andes del norte al parecer albergan a la mayor parte de la población durante la época no reproductiva. Sin embargo, los paisajes forestales de los que depende la Re-inita Cerúlea en ambas regiones, son objeto de múltiples presiones antropogénicas, como la extracción de recursos naturales o varias formas de agricultura, siendo los productos de estos dos tipos de presión impor-tantes a nivel nacional y mundial. La viabilidad a largo plazo de la Reinita Cerúlea depende de asociaciones de conservación con numerosas industrias, cada una de ellas con objetivos y prácticas diferentes para el uso de tierra. Por lo tanto es esencial que los científicos de la conservación y las agencias de manejo de tierra, trabajen con los actores clave para desarrollar soluciones de conservación proactivas que se puedan integrar a las operaciones de la industria con un impacto mínimo para los beneficios económicos, requisitos de regulación, normas de seguridad y eficiencia en general. Trabajando en conjunto, los profesionales de la conservación y las varias industrias en ambas regiones, pueden lograr progresos enormes hacia la conser-vación y restauración de paisajes forestales, que puedan mantener poblaciones de la Reinita Cerúlea y que a la vez puedan sostener las economías locales en el futuro.

Abstract. – The Appalachian Mountain region in North America supports nearly 80% of the global breeding population of Cerulean Warbler (Setophaga cerulea), and the Northern Andes Mountains appear to support the majority of the population during the nonbreeding season. However, the forested landscapes that Ceru-

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in north america support nearly 80% of the global breeding population of cerulean Warbler (Blancher et al. 2007). During north america’s winter, the species primarily inhabits forests between 500 – 1500 m elevation in the northern andes Mountains (Hamel 2000, Fundación proaves et al. 2010). the two regions share several basic characteristics: (1) high biodiversity of plants and animals, (2) rugged terrain that is mostly forested yet highly fragmented, (3) abundant natural resources (forests, water, minerals, fossil fuels), and (4) rural communities that rely on extraction or growth of globally important products (e.g., coffee, coal, forest products, natural gas). therefore, the long-term viability of cerulean Warbler will require conservation partnerships with local communities and numerous industries, and the development of sustainable yet economically viable business practices (e.g.., Cerulean Warbler-friendly certifications or best management practices) and conservation strategies (Sánchez-clavijo et al. 2008).

it is essential that conservation scientists and land management agencies work with key stakeholders to develop proactive conservation solutions that can be integrated into industry operations with minimal impact to industry profits, regulatory requirements, safety standards, and overall efficiency. Recent efforts and future opportunities to engage the coal and coffee industries in north and South america, respectively, provide examples.

introDUction

over the last 15 years or so, the ornithological community has increased its focus on full life cycle conservation of nearctic-neotropical migrants, recognizing that breeding, migration, and nonbreeding seasons each play vital and inter-connected roles in both individual annual survival and reproductive success, and population long-term viability. Because full cycle conservation of nearctic-neotropical migrants is such a complex issue and is international in scope, numerous partnerships have developed in order to (1) gain a better understanding of limiting factors for long-distance migrants throughout their annual life cycles and (2) identify critical actions needed to conserve species of concern. one such partnership, the cerulean Warbler (Setophaga cerulea) technical group (cWtg), has focused more than a decade of coordinated time, intelligence, and resources on identifying critical limiting factors and strategic conservation actions for the species and its associates on the breeding and nonbreeding (wintering) grounds and along migratory pathways.

cerulean Warbler is a nearctic-neotropical migrant songbird that has experienced a rapid and long-term pop-ulation decline, primarily due to habitat fragmentation from human activity on its breeding and nonbreeding grounds. the diverse hardwood forests of the appalachian Mountain region

lean Warbler relies upon in both regions are subject to numerous anthropogenic stressors from the extraction of natural resources or various forms of agriculture, with products from both of these stressors being globally and domestically important. The long-term viability of Cerulean Warbler relies upon conservation partner-ships with numerous industries, each with different land management objectives and practices. Therefore, it is essential that conservation scientists and land management agencies work with key stakeholders to develop proactive conservation solutions that can be integrated into industry operations with minimal impact to industry profits, regulatory requirements, safety standards, and overall efficiency. Working in partnership, conservation professionals and the various industries in both regions can make tremendous progress in conserving and restoring forested landscapes that can sustain Cerulean Warbler populations and support local economies into the future.

Key words: Cerulean Warbler, Setophaga cerulea, Appalachian Mountains, Northern Andes Mountains, coal, forest products, coffee, conservation partnerships.

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CERULEAN WARBLER IN ANDES & APPALACHIANS

appalacHian MoUntainS BreeDing range anD coal

the highest densities of breeding cerulean Warbler (West Virginia, southeast ohio, eastern Kentucky, and northeastern tennessee) share a high degree of overlap with the appalachian coal Fields, an area that contains underlying seams of coal awaiting extraction, thousands of underground mines, and active or idle surface mines that range in size from a few hectares to over 1,000 hectares. the Surface Mining control and reclamation act (SMcra) of 1977 regulates the environmental effects of coal mining and the reclamation of impacted lands. Until recently, regulating agencies and companies responsible for reclamation focused on soil stability and control of water runoff and sedimentation. the practices employed since the passage of SMcra have led to severely compacted substrates on over 400,000 ha of mined lands in the appalachian region, most of which are primarily non-native grasses (cool season), or a combination of non-native grasses, shrubs, and trees. Most of these reclaimed areas are incapable of supporting the diverse hardwood forests that were present prior to mining activities. However, a broad constituency interested in reforestation of coal-mined lands began to develop in the mid-1990s, culminating in the formation of the appalachian regional reforestation initiative (arri) in 2004. the arri is a coalition of groups (including citizens, the coal industry, and government agencies) dedicated to restoring forests on coal-mined lands using the science-based Forestry reclamation approach (Fra; Burger et al. 2005, 2011)—not only on current and future surface mines, but also on the estimated 300,000 ha of “legacy” mines reclaimed since the passage of SMcra that still are not supporting native hardwood forests. the goals of arri for mine reclamation and restoration are to (1) plant more high-value and diverse hardwood trees, (2) increase the survival rates and growth of planted trees, and (3) expedite the establishment of forest

habitat through natural succession. Since the start of arri in 2004, approximately 70 million trees have been planted and approximately 41,683 ha restored to forests on newly mined land, and approximately 644,000 trees have been planted on about 372 ha of “legacy” surface mines. additionally, implementation of the Fra varies among the coal-producing states in the appalachian Mountains, with three states reporting between 90–100% of their mining permits require a forestry post-mining land use using the Fra methodology, whereas that percentage is much lower in other states. given the overlap of past and current mining activities with core breeding habitat for cerulean Warblers, the momentum gathering around mineland reforestation, and the additional reforestation efforts needed within core breeding habitat for cerulean Warbler, members of the cWtg and arri initiated a partnership in 2005 to promote and target reforestation of coal-mined lands (current, future, and legacy mines) to benefit cerulean Warbler and other forest-dependent wildlife in the appalachian Mountains.

a migratory bird habitat conservation partnership for the appalachian region, the appalachian Mountains Joint Venture (aMJV) was formed in 2007 (and formally approved by U.S. Fish and Wildlife Service in 2008) and joined both the cWtg and arri partnerships. the aMJV and cWtg began to develop products to help target reforestation projects and inform the coal industry about why such efforts were needed. For example, Shumar (2009) created a predictive map of cerulean Warbler abundance to help arri prioritize legacy mine reforestation projects with the highest potential for improving habitat for the species. the Shumar (2009) Bayesian hierarchical model for the appalachian Mountains Bird conservation region used count data from the north american Breeding Bird Survey (http://www.pwrc.usgs.gov/bbs/) and a suite of environmental covariates temporally matched to the 2001 national landcover Database. this map was then used to identify and prioritize previously

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mined lands for reforestation in a portion of the cerulean Warbler’s core breeding range (Wood et al. 2010; Fig. 1). the aMJV partnership also recently completed a science-based, expert-led process to identify focal areas on-the-ground conservation efforts for cerulean Warbler within the appalachian region, and members of the cWtg and aMJV are developing a “Best Management

practices” document for forest management activities to benefit the species. Although relatively new, the three partnerships (arri, cWtg, and aMJV) are making tremendous progress toward building a future landscape that can sustain both cerulean Warbler populations and local economies on appalachian breeding grounds of cerulean Warbler.

Fig. 1. predicted cerulean Warbler abundance was used to identify and prioritize previously mined lands for reforestation in a portion of the core breeding range (from Wood et al. 2010), where coal mining by mountaintop removal currently is being practiced. areas shown in white (exception: the area in white along the western boundary of the mountaintop mining area is a modeling anomaly) have the highest predicted abundance of Cerulean Warbler. Mined lands within these areas were identified as the highest priorities for reforestation based on their proximity to areas of high predicted abundance of cerulean Warbler.

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nortHern anDeS nonBreeD-ing range anD coFFee

recent research and surveys conducted by various cWtg partners throughout the winter range of cerulean Warbler have indicated a strong presence of the species in the coffee-growing region of the northern andes Mountains, with higher densities and more detections of cerulean Warblers in shade coffee plantations than in primary forest (Bakermans et al. 2009). cerulean Warblers that regularly foraged in shade coffee plantations had high monthly survival rates, gained weight through the winter, and showed fidelity to particular sites within and between winters (Botero et al. 2008, Bakermans et al. 2009, Sánchez-clavijo et al. 2010). However, for various reasons, conversion to shade coffee is not practical in all of the coffee growing regions in the northern andes, and implementing national-level conservation initiatives presents numerous challenges. For example, there are over 500,000 families that grow and sell coffee commercially in colombia, and nearly 95% of those family farms are less than 5 ha each (unpublished data, Federación nacional de cafeteros de colombia 2007). therefore, any coffee-related conservation initiative for cerulean Warbler must consider at least four general principles to be effective: (1) planning and implementation should be conducted at a regional or possibly national scale, but the initiative must provide tangible benefits to local communities and individual landowners; (2) conservation strategies should be science-based, targeted at productive wintering areas, and developed for both shade and sun coffee regions (i.e., where shade coffee is not a viable option, what other strategies exist to conserve cerulean Warbler habitat?); (3) local communities should be engaged in the conservation of fragile ecosystems linked to important environmental services, biodiversity, and watershed health; and (4) consumers of coffee worldwide must be educated on the link between coffee, conservation, and sustainable ecosystem function.

as an example, over the last decade, members of el grupo cerúleo have gathered data in colombia (and other countries in the northern andes) to guide on-the-ground conservation efforts. Based on data gathered, american Bird conservancy (aBc) and Fundación proaves began conserving land and working with local communities in central colombia, targeting an area that supports a high density of cerulean Warbler in primary forest and shade-coffee plantations. in 2006 and 2007, aBc and Fundación proaves purchased a total of 1,371 ha (which included a coffee plantation) to establish the cerulean Warbler reserve. Fundación proaves and aBc also worked with local communities over the next several years to educate and engage them in conservation efforts (Skolnik et al. 2012). in order to conserve cerulean Warbler non-breeding habitat, more conservation efforts such as these must be developed, and must be guided by the latest science, engage broad conservation partnerships, and incorporate local communities into planning efforts for sustainable economies and environments.

conclUSion

the long-term decline of cerulean Warbler (and many other nearctic-neotropical migrants) and a growing body of research on limiting factors both point to the critical importance of a full life cycle approach to conservation. Members of the cWtg and aMJV partnerships currently have sufficient information to strategically and effectively conserve and improve habitat for cerulean Warbler, to engage new partners, and to practice adaptive conservation as we learn more about the species. as we move forward into the implementation phase of cerulean Warbler conservation, we must develop conservation strategies for specific seasons, regions, and focal areas to ensure that we address limiting factors at multiple spatial and temporal scales. given the two major regions where our work will focus, our conservation strategies must ensure economic

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unused surface mined lands: Development, application, and adoption. In r. i. Barnhisel (ed.). proceedings of the 2011 national Meeting of the american Society of Mining and reclamation. Bismarck, north Dakota, USa.

Fundación proaves, american Bird conservancy & el grupo cerúleo. 2010. conservation plan for the cerulean Warbler on its nonbreeding range - plan de conservación para la reinita cerúlea sobre su rango no reproductivo. conserv. colomb 12: 1–62.

Hamel, p. B. 2000. cerulean Warbler Status assessment. U.S. Department of the interior, Fish & Wildlife Service, Minneapolis, Minnesota, USa.

Sánchez-clavijo, l. M., r. espinosa, J. e. Botero, a. M. lópez & n. g. Franco. 2008. la reinita cerúlea: una especie que depende del café y del carbón. Biocarta 13, cenicafé, chinchiná, caldas, colombia.

Sánchez-clavijo, l. M., r. espinosa, & J. Botero. 2010. priority and opportunities for migratory bird conservation in colombia’s coffee regions. Abstract: third Zoological congress of colombia, november 2010. Medellin, colombia.

Shumar, M. B. 2009. predictive modeling techniques with application to the cerulean Warbler (Dendroica cerulea) in the appalachian Mountains Bird conservation region. M.Sc. thesis, West Virginia Univ., Morgantown, West Virginia, USa. available at http://wvuscholar.wvu.edu:8881

Skolnik, B., D. Wiedenfeld, r. Dettmers, c. aucca, l. Daza, H. Valle, F. Sornoza, J. robayo, D. Diaz, J. Fitzgerald, D. lebbin, & p. B. Hamel. 2012. conservation planning and accomplishments for protection of cerulean Warbler (Setophaga cerulea) nonbreeding habitat. ornitol. neotrop. 23(Suppl.): 319–329.

Wood, p. B., M. e. McDermott, & M. B. Shumar. 2010. cerulean Warbler conservation initiative 4: identify and prioritize mined lands for reforestation. Final report to national council for air and Stream improvement.

viability and sustainability of natural resources, and the industries and local communities must be able to see tangible benefits from our efforts. Most importantly, however, we must continue to work through, and further expand, our partnerships; only through collaboration will our conservation goals be achieved at local, state, national, and international scales.

reFerenceS

Bakermans, M. H., a. c. Vitz, a. D. rodewald, & c. g. rengifo. 2009. Migratory songbird use of shade coffee in the Venezuelan andes with implications for conservation of cerulean Warbler. Biol. conservat. 142: 2476–2483.

Blancher, p. J., K. V. rosenberg, a. o. panjabi, B. alt-man, J. Bart, c. J. Beardmore, g. S. Butcher, D. Demarest, r. Dettmers, e. H. Dunn, W. easton, W. c. Hunter, e. e. iñigo-elias, D. n. pash-ley, c. J. ralph, t. D. rich, c. M. rustay, J. M. ruth, & t.c. Will. 2007. guide to the partners in Flight population estimates database. version: north american landbird conservation plan 2004. partners in Flight technical Series no 5. Available at http://www.partnersinflight.org/

Botero, J. e., l. M. Sánchez-clavijo, & r. espinosa. 2008. the cerulean Warbler in colombia’s coffee-growing regions. Abstract: cerulean and golden-winged Warbler Summit, Bogotá, colombia, october 2008.

Burger, J., D. graves, p. angel, V. Davis, & c. Zipper. 2005. the forestry reclamation approach. the appalachian regional reforestation initiative Forest reclamation advisory, U.S. Department of Interior, Office of Surface Mines Reclama-tion and enforcement. available at http://arri.osmre.gov/Fra/advisories/Fra_no.2.7-18-07.revised.pdf/ [accessed 30 January 2012]

Burger, J., c. Zipper, p. angel, D. evans, & S. eg-gerud. 2011. reforestation guidelines for

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CERULEAN WARBLER (sEtOphAGA CErulEA) RESPONSE TO CHANGES IN fOREST STRUCTURE IN INDIANA

Kamal Islam, Jennifer Wagner, Ryan Dibala, Margaret MacNeil, Kyle Kaminski,

& Lila (Prichard) young

Department of Biology, Ball State University, Muncie, IN 47306-0440, USA. E-mail: [email protected]

Resumen. – Respuesta de la Reinita Cerúlea a cambios en estructura forestal en el estado de Indi-ana en los E.E.U.U. – La Reinita Cerúlea (Setophaga cerulea), paseriforme Neotropical, ha sufrido una declinación en su tamaño poblacional durante las últimas cuatro décadas. Como consecuencia, ha sido catalogada como “En Peligro” en el estado de Indiana, Estados Unidos, y es considerada globalmente como especie de “conservación preocupante”. En los últimos cinco años (2007-2011), nuestra investigación se ha enfocado en cómo las poblaciones de la Reinita Cerúlea responden a los cambios del ambiente como resultado de diferentes prácticas de manejo del bosque en sus áreas de anidación. Como parte del Experi-mento en Ecosistemas de Madera Fina, un estudio experimental de gran escala y a largo plazo (100 años) sobre los impactos del manejo del bosque en plantas y vida silvestre, monitoreamos las poblaciones de la Reinita Cerúlea durante el periodo pre-tratamiento (2007 & 2008) y pos- tratamiento (2009 – 2011). En 2011, se inició un estudio sobre la biología de anidación. El área de estudio consiste de seis sitios con tratamiento y tres sitios control, todos ubicados dentro de nueve unidades de manejo en los bosques estatales de Yel-lowwood y Morgan – Monroe en el sur de Indiana. Las poblaciones de la Reinita Cerúlea respondieron positivamente (+75%) a sitios con tratamientos de edades uniformes y negativamente (-38%) a sitios con tratamientos de edades no uniformes en base al número de detecciones luego de la cosecha. También hubo un incremento (+62%) en el número de detecciones de la Reinita Cerúlea en los sitios control entre los años antes y después del tratamiento. El éxito de anidación fue mayor en los sitios control (41%) comparados con los sitios de tratamiento de edad uniforme (33%) y los de edad no uniforme (22%); sin embargo, estas diferencias no fueron significativas.

Abstract. – The Cerulean Warbler (Setophaga cerulea), a Neotropical migratory songbird, has declined in population size during the last four decades. As a consequence, it is listed as “Endangered” in the state of Indiana, USA, and is considered a species of “conservation concern” globally. For the last five years (2007-2011), our research has focused on how Cerulean Warbler populations respond to changes in their environ-ment as a result of different forest management practices on their breeding grounds. As part of the Hardwood Ecosystem Experiment, a large scale and long term (100 years) experimental study of forest management impacts on plants and wildlife, we monitored Cerulean Warbler populations during pre-treatment (2007 & 2008) & post-treatment (2009-2011) years. In 2011, we initiated a breeding biology study. Our study area consisted of six treatment & three control sites, all located within nine management units in the Yellowwood and Morgan-Monroe state forests of southern Indiana. Cerulean Warbler populations responded positively (+75%) to even-aged treatment sites and negatively (-38%) to uneven-aged treatment sites as determined by the number of detections after harvest. There was also an increase (+62%) in the number of Cerulean Warbler detections in the control sites between pre- and post-treatment years. Nesting success was highest in control sites (38%) compared with even-aged (35%) and uneven-aged (22%) sites; however, these differ-ences were not significant.

Key words: Cerulean Warbler, Dendroica cerulea, Setophaga cerulea, Relative Abundance, Nesting Suc-cess, Response To Silviculture.

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of the breeding range and that these gaps are likely of importance to the species (oliarnyk & robertson 1996, Hamel 2000, Bosworth 2003, Weakland & Wood 2005, Wood et al. 2006, Bakermans & rodewald 2009).

a parallel study by the cerulean Warbler technical group on response of this species to different forest treatments was conducted in ohio, West Virginia, Kentucky, and tennessee (Dawson et al. 2012, larkin et al. 2012). in another study in West Virginia, cerulean Warblers were present at a lower abundance and frequency in 15-18 year old regenerating clearcut stands compared to 70-80 year old mature second-growth forests (Wood et al. 2005). in southern indiana, cerulean Warbler habitat needs appeared to be supported by a 20-30 year cutting cycle combined with uneven-age management and timber stand improvement practices (register & islam 2008). cerulean Warbler response to experimental habitat manipulation has been identified as an important research priority (Hamel et al. 2004) in order to determine, in particular, specific characteristics of vegetation structure preferred by the birds and how to produce these vegetative characteristics on the landscape.

the Hardwood ecosystem experiment (Hee, see http://www.heeforeststudy.org/), a large scale and long term (100 years) experimental study of forest management impacts on plants and wildlife, was initiated in southern indiana in 2006. the Hee is a research collaboration between the indiana Department of natural resources, purdue University, Ball State University, indiana University of pennsylvania, indiana State University, Drake University, and the nature conservancy. the goal of this experiment is to understand social and ecological impacts of long-term forest management on public and private lands in indiana and in the broader central Hardwoods region. the primary objective is to develop even and uneven-

introDUction

cerulean Warblers (Setophaga cerulea) are small migratory songbirds that breed in the northeastern and Midwestern portions of north america and winter on the slopes of the andes (robbins et al. 1992, Hamel 2000). For the last 40 years, this species has declined at an annual rate of 4.1% (Sauer et al. 2008), the steepest decline of any north american parulid (Jones et al. 2008). as a consequence, it is listed as a top priority species for conservation action by partners in Flight (Hamel et al. 2004) and listed as “Vulnerable” by the international Union for conservation of nature (Birdlife international 2004). it was petitioned for listing as a threatened species under the endangered Species act (U.S. Fish & Wildlife Service 2002) but the petition to list was later denied as the action was not warranted (U.S. Fish & Wildlife Service. 2006). in indiana, the cerulean Warbler is listed as endangered.

cerulean Warblers prefer large tracts of mature deciduous forest (Hamel 2000). on the breeding grounds in the Midwest, specifically Indiana, Cerulean Warblers generally are associated with forests featuring a heterogeneous forest structure with multiple canopy layers created by multi-age stands of trees, and appear to prefer large dominant trees within their territories (Jones & islam 2006, roth & islam 2008). these forests are typically dominated by oaks (Quercus spp.) and hickories (Carya spp.) in the uplands with beech (Fagus grandifolia), northern red oak (Quercus rubra), sugar maple (Acer saccharum), and white ash (Fraxinus americana) as common mesic species in ravines (Homoya et al. 1985). these forests are characterized by canopy gaps that are created naturally through tree fall or fire, or anthropogenically from old logging roads and forest clearings. Several authors have also noted that cerulean Warblers are associated with canopy gaps in other parts

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aged silvicultural systems that maintain oak-dominated forest communities and landscapes. nine management units (303-483 ha in size with 200 ha core) were randomly selected in Morgan-Monroe (9716 ha) and Yellowwood state forests (9444 ha) in southern indiana (Fig. 1). Six of nine management units received one of two types of silvicultural treatments in 2008. three units (1, 7 & 8) received single tree selection with patch cutting to create uneven-aged forests (Fig. 1). these units each received eight cuts, which created openings ranging from 0.4 to 2 ha, dispersed across ridges, north and south slopes, and bottomlands. three units (3, 6 & 9) were treated with both shelterwood and clearcut harvests with the intent to create even-aged forests (Fig. 1). Shelterwood and clearcut harvested areas each received four cuts per unit. two 4 ha shelterwood harvests and two 4

ha clearcuts, applied to each of the three units, occurred on slopes in each cardinal direction. the three remaining units (2, 4 & 5) did not receive silvicultural treatment and served as controls (Fig. 1). all management units were comparable in tree structure and composition, and were characterized by ridgetops with steep, narrow drainages. For this study, 2007 and 2008 represent pre-treatment years, and 2009, 2010, and 2011 represent post-treatment data.

our objectives were to (1) measure cerulean Warbler relative abundance in study areas before and after forest treatments were applied and (2) monitor breeding success during the third year after harvest. We hypothesized that cerulean Warblers would occur in greater abundance in management units receiving forest treatments that removed fewer trees from the landscape, thereby

Fig. 1. location of nine study sites within Morgan, Monroe, and Brown counties in southern indiana.

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creating multiple canopy openings known to be attractive to this species.

MetHoDS

We established four study sites (1.96 km2

each) in Morgan-Monroe State Forest and five study sites (1.96 km2 each) in Yellowwood State Forest in the core of each management unit. We conducted 100-m fixed radius point count surveys during the month of May from 2007-2011, once at every site each year. every study site had seven linear transects with seven points, for a total of 49 points for each survey. points were spaced 200 m apart to minimize duplicate sampling as male cerulean Warblers were found to broadcast their songs approximately 100 m (Jones et al. 2000, Hamel et al. 2009). Surveys were conducted from approximately 05:30 to 10:30 eSt and none was initiated during periods of rain, wind, or any other phenomenon that would prevent vocalizations from being heard. We surveyed each point for a total of 5 minutes. The first 2 minutes were spent listening for singing males. this was followed by a minute of cerulean Warbler song broadcasting via audio cassette or Mp3 player and speaker to elicit a vocal response from any males in the immediate area. the last 2 minutes were spent listening without playback (Falls 1981). When a male cerulean Warbler was detected, we recorded both distance and compass direction from the survey point to prevent the same individual from being counted more than once during the 5 minute period. to eliminate potential bias on the sequence and date that units were sampled each year, we used a random numbers table to determine the order in which the study sites were surveyed from first to last.

territory mapping was conducted in May and June of 2011. Whenever a cerulean Warbler was observed singing repeatedly from a tree, we marked the tree with flagging tape and recorded the coordinates (Universal transverse

Mercator/UtM) of the tree location, using a garmin gpS 76 handheld global positioning System (gpS) unit. territories were considered to be completely mapped when a range of 5-12 trees were flagged. Whenever possible, we revisited known territories multiple times before final demarcation was determined. GPS coordinates were imported into arcMap to create territory polygons using the minimum convex polygon method.

nest searching commenced in May and June of 2011 in conjunction with territory mapping. Direct observation of a female on a male’s territory and her general behavior often exposed the location of the nest. additionally, we followed mated males and used audible clues such as “whisper singing” when they were in close proximity to a nest. once nests were found, they were monitored from the ground using binoculars and spotting scopes once every two to three days from incubation to fledging. We defined a successful nest where at least one nestling fledged, an unsuccessful nest as one that failed, and unknown as the number of territories that were monitored for signs of nesting but no nests or fledglings were found. We defined nesting success as follows: Successful nests/unsuccessful nests + unknown.

one-way analysis of Variance (anoVa) was performed to determine if there was any difference in the number of cerulean Warbler detections among even-aged (shelterwood/clearcut), uneven-aged (single tree selection with patch cutting), and control sites prior to harvest (2007 & 2008). post-harvest comparisons of anoVa data will be presented elsewhere. percent change in relative abundance was computed by taking the average relative abundance for the two pre-treatment years and comparing these values with the average relative abundance for the three post-treatment years for each group. a chi-square goodness-of-fit test was conducted to determine if there was any significant difference in nesting success among the three

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groups. We used Minitab 16 for all statistical tests. Significant differences were accepted at α 5 0.05 probability.

reSUltS

Over the five-year period, we detected a total of 576 male cerulean Warblers on our point counts (94 in 2007, 124 in 2008, 135 in 2009, 93 in 2010, and 130 in 2011). there was no significant difference in the number of cerulean Warbler detections (F 2,15 5 2.57, P 5 0.110) among the three groups (even-age, uneven-age, & control) for the two combined pre-treatment years (2007 & 2008). the number of detections between pre- and post-harvest years increased in even-aged sites (75%), decreased in uneven-aged sites (38%), and increased in control sites (62%, Fig. 2).

of 101 cerulean Warbler territories that were monitored intensively for nesting

activity in 2011, 31 territories had either a nest that fledged young or fledglings were observed in the territory, and these territories were considered successful. although nesting success differed among even-aged (14/40 5 35%), uneven-aged (8/37 5 22%), and control (9/24 5 38%) sites, these differences were not statistically significant (Pearson χ 2 5 2.303, df 5 2, P = 0.316).

DiScUSSion

the strength of our study is the Before-after control-impact design which allows us to make comparisons against pre-harvest data. our prediction that cerulean Warblers would occur in greater abundance in sites with small openings created by uneven-age harvest was not supported. Based on relative abundance estimates in the three year post-harvest period, sites in management units that received clearcuts and

Fig 2. relative abundance estimates of cerulean Warblers in response to silvicultural treatments in south-ern indiana, 2007-2011.

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populations resulting in lower cerulean Warbler productivity as suggested by a study in tennessee (Boves 2011), or if small openings are indeed beneficial to this species.

acKnoWleDgMentS

We thank J. grant, M. Holding, e. Koscielniak, l. nelson, a. ripley, D. rupp, J. Schindler, r. Stiller, and A. Wilson for assistance with field data collection and e. arnold for data entry. We also thank r. Kalb and c. Mycroft for coordinating the Hee project. our research was funded through grants from the indiana Department of natural resources through purdue University, U.S. Fish and Wildlife Service, amos W. Butler audubon Society, indiana academy of Science, and the Sponsored Programs Office and Chapter of Sigma Xi at Ball State University. We thank the reviewers, Deanna Dawson and paul Hamel, for their helpful comments which improved the manuscript.

reFerenceS

Bakermans, M. H., & a. D. rodewald. 2009. think globally, manage locally: the importance of steady-state forest features for a declining songbird. Forest ecol. Manag. 258: 224–232.

Birdlife international. 2004. threatened birds of the world 2004. cD-rom. Birdlife international, cambridge, UK.

Bosworth, S. B. 2003. cerulean Warbler relative abundance and frequency of occurrence relative to large-scale edge. M.Sc. thesis, West Virginia Univ., Morgantown, West Virginia, USa.

Boves, t. J. 2011. Multiple responses by cerulean Warblers to experimental forest disturbance in the appalachian Mountains. ph.D. diss., Univ. of tennessee, Knoxville, tennessee, USa.

Dawson, D. K., t. B. Wigley, & p. D. Keyser. 2012. cerulean Warbler technical group: coordinating international research and conservation. ornitol. neotrop. 23(Suppl.): 279–285.

shelterwood treatments attracted more cerulean Warblers compared to sites in units that received single tree selection with patch cutting. past research has suggested that cerulean Warblers are attracted to disturbances in the canopy (Bosworth 2003, Weakland & Wood 2005) but the size and extent of these disturbances has not been established. annual monitoring of cerulean Warbler populations in the management units will determine if the response to these openings continues as clearcuts and other harvested areas regenerate over time.

a study conducted in southern indiana found no significant difference in the number of cerulean Warbler detections among stands 2-30 years old (single tree selection and a combination of group and single tree selection) and unharvested reference sites (stands 35-100+ years old; register & islam 2008). in contrast, in a study in West Virginia, Wood et al. (2005) found that cerulean Warblers occurred in greater abundance in 70-80 year mature forests than in 15-18 year old stands that received clearcuts and two-age harvests. though statistically not significant, Cerulean Warblers were detected almost 5 times in greater abundance in the two-age harvest stands than in the clearcut stands (Wood et al. 2005).

even though control sites had higher nesting success (38%) than either of the treatment sites (even-aged-35%, uneven-aged-22%), there was no significant difference in nesting success. openings created by clearcuts and shelterwood treatments not only attracted cerulean Warblers when they first arrived to breed, but provided areas next to which males established territories, attracted and paired with females, and raised young. Our findings, however, are preliminary and are based on one year of reproductive data. continued monitoring of reproductive output at these forest treatment sites will determine if these sites attract cerulean Warblers only to serve as “ecological traps”, with increased predator and brood parasite

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oliarnyk, c. J., & r. J. robertson. 1996. Breeding behavior and reproductive success of cerulean warblers in southeastern ontario. Wilson Bull. 108: 673–684.

register, S. M., & K. islam. 2008. effects of silvicultural treatments on cerulean Warbler (Dendroica cerulea) abundance in southern indiana. Forest ecol. Manag. 255: 3502–3505.

robbins, c. S., J. W. Fitzpatrick, & p. B. Hamel. 1992. a warbler in trouble: Dendroica cerulea. pp. 549–562 in Hagan iii, J. M., & D. W. Johnston (eds). ecology and conservation of neotropical Migrant landbirds. Smithsonian institution press, Washington, D.c., USa.

roth, K. l., & K. islam. 2008. Habitat Selection and reproductive Success of cerulean Warblers in indiana. Wilson J. ornithol. 120: 105–110.

Sauer, J. r., J. e. Hines, & J. Fallon. 2008. the north american Breeding Bird Survey, results and analysis 1966–2007. Version 5.15.2008. USgS patuxent Wildlife research center, laurel, Maryland, USa.

U.S. Fish and Wildlife Service. 2002. endangered and threatened wildlife and plants; 90-day finding on a petition to list the cerulean warbler as threatened with critical habitat. Fed. regist. 67: 65083–65086.

U.S. Fish and Wildlife Service. 2006. endangered and threatened Wildlife and plants; 12-month finding on a petition to list the Cerulean Warbler (Dendroica cerulea) as threatened with critical Habitat. Fed. regist. 71: 70717–70733.

Weakland, c. a., & p. B. Wood. 2005. cerulean warbler (Dendroica cerulea) microhabitat and landscape-level habitat characteristics in southern West Virginia. auk 122: 497–508.

Wood, p. B., J. p. Duguay, & J. V. nichols. 2005. cerulean warbler use of regenerated clearcut and two-age harvests. Wildl. Soc. Bull. 33: 851–858.

Wood, p. B., S. B. Bosworth, & r. Dettmers. 2006. cerulean Warbler abundance and occurrence relative to large scale edge and habitat characteristics. condor 108: 154–165.

Falls, J. B. 1981. Mapping territories with playback: an accurate census method for songbirds. Stud. avian Biol. 6: 86–91.

Hamel, p. B. 2000. cerulean Warbler (Dendroica cerulea). In poole, a., & F. gill (eds). the Birds of north america, no. 511. the birds of north america, inc., philadelphia, pennsylvania, USa.

Hamel, p. B., D. K. Dawson, & p. D. Keyser. 2004. How we can learn more about the cerulean Warbler (Dendroica cerulea). auk 121: 7–14.

Hamel, p. B., M. J. Welton, c. g. Smith, iii, & r. p. Ford. 2009. test of partners in Flight effective detection distance for cerulean warbler. pp. 328–333 in rich, t. D., c. arizmendi, D. W. Demarest, & c. thompson (eds). tundra to tropics: connecting birds, habitats, and people. proc. 4th international partners in Flight conf. 13-16 February 2008, Mcallen, texas, USa.

Hardwood ecosystem experiment. 2010. available at http://www.ag.purdue.edu/programs/ hee/pages/default.aspx/ [accessed 21 January 2012]

Homoya, M. a., D. B. abrell, J. r. aldrich, & t. W. post. 1985. the natural regions of indiana. proc. indiana acad. Sci. 94: 245–268. available at http://gis.esri.com/library/userconf/ proc06/papers/papers/pap_1656.pdf.

Jones, J., W. J. Mcleish, & r. J. robertson. 2000. Density influences census technique accuracy for cerulean Warblers in eastern ontario. J. Field ornithol. 71: 46–56.

Jones, J., D. r. norris, M. K. girvan, J. J. Barg, t. K. Keyser, & r. J. robertson. 2008. Migratory connectivity and rate of population decline in a vulnerable songbird. condor 110: 538–544.

Jones, K. c., & K. islam. 2006. Selection of song perches by cerulean warblers. proc. indiana acad. Sci. 115: 37–43.

larkin, J. l., p. B. Wood, t. J. Boves, J. Sheehan, D. a. Buehler, p. D. Keyser, a. D. rodewald, t. a. Beachy, M. H. Bakermans, a. evans, g. a. george, M. e. McDermott, F. l. newell, K. a. perkins, M. White, & t. B. Wigley. 2012. Breeding season concerns and response to forest management: can forest management produce more breeding birds? ornitol. neotrop. 23(Suppl.): 287–290.

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CONSERVANDO EL HÁBITAT INVERNAL DE LA REINITA CERÚLEA (sEtOphAGA CErulEA) EN ECUADOR

Tatiana Santander1 G., Adrián Soria & Esteban A. Guevara

1Aves & Conservación – BirdLife en Ecuador, Pasaje Joaquín Tinajero E3–05 y Jorge Drom, Casilla 17–17 906, Quito, Ecuador. E-mail: [email protected]

Abstract. – Conserving the wintering grounds of Cerulean Warbler (setophaga cerulea) in Ecuador. – The aim of this project was to establish a Local Conservation Group (LCG) to preserve Important Bird Areas (IBA) and monitor the presence of the Cerulean Warbler (Setophaga cerulea) at its wintering grounds. The approach considers capacity building, and training among local actors to generate local skills to identify and address conservation threats at their sites as well as the management of their natural resources. Two LCGs were created at the southern buffer zone of Sumaco Napo – Galeras National Park Important Bird Area located in the north eastern Andean slopes of Ecuador, they include 44 members. The LCG have allowed implementing conservation activities designed to increase awareness among local people, children and au-thorities, as well as to provide the knowledge about the biology of Cerulean Warbler and other migratory and resident species. Bird observation and identification workshops were offered to support participatory monitoring activities of Cerulean Warbler habitat use and to show that avitourism could provide an alternative economic income.

Resumen. – El objetivo del proyecto fue el establecer un Grupo de Apoyo Local (GAL) como una herra-mienta para la conservación de las Áreas Importantes para la Conservación de las Aves (IBA) y monitorear la presencia de la Reinita Cerúlea (Setophaga cerulea) en las áreas de estudio. El enfoque consideró la creación de capacidades locales por medio de la enseñanza que permita atender los problemas de con-servación y mejorar el manejo de los recursos naturales. Dos GAL fueron creados en la zona de amor-tiguamiento ubicada al sur de la IBA del Parque Nacional Sumaco Napo – Galeras, los cuales cuentan en total con 44 miembros. El GAL actúa como un medio multiplicador que ha permitido implementar acciones de conservación enfocadas en incrementar la sensibilización ambiental entre las personas locales, niños y autoridades. De igual manera difundir información sobre la biología de la Reinita Cerúlea y otras especies de aves residentes y migratorias. Se ha brindado talleres en la observación e identificación de aves como apoyo a los monitoreos participativos de la Reinita Cerúlea y como una forma de proveer una alternativa económica como sería el aviturismo.

Key words: birdwatching, Important Bird Area, Setophaga cerulea, Local Conservation Group, Sumaco Napo Galeras National Park.

introDUcciÓn

la reinita cerúlea (Setophaga cerulea VU) migra principalmente al norte de Sudamérica durante la temporada no reproductiva, pasando el invierno boreal en las estribaciones de la cordillera de los andes (robbins et al. 1992, Hamel 2000, Fundación proaves et al. 2010).

Una parte importante de la distribución invernal de la especie se asienta sobre el lado oriental de los andes en ecuador donde comparte hábitat con otras especies migratorias como la reinita pechinaranja (Setophaga fusca), la reinita collareja (Cardellina canadensis), candelita norteña (Setophaga ruticilla), la reinita Blanquinegra (Mniotilta varia), el pibí

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ganado y cultivos principalmente de naranjilla (Solanum quitoense). esta situación nos brinda la oportunidad de generar información sobre el hábitat que ocupa la especie y luego establecer prioridades de manejo considerando que para el crecimiento de la naranjilla se requiere la tala completa del bosque, a diferencia de los cafetales donde se puede promover el cultivo de sombra. esto pone peligro la permanencia de los potenciales sitios de invernada de la especie. De esta manera, la sensibilización ambiental y la implementación de alternativas económicas sostenibles son herramientas prioritarias para la conservación.

a partir de septiembre de 2008 se inicia el trabajo en el pnSng gracias al apoyo del US Forest Service y tnc Migratory Bird program con talleres de avifauna básica y se afina la metodología para llevar a cabo el monitoreo de la reinita cerúlea. con las experiencias obtenidas, en la actualidad ejecutamos el proyecto “conservando el hábitat invernal de la reinita cerúlea en ecuador con grupos de apoyo local (gal)”, el cual cuenta con fondos del acta de conservación de aves Migratorias neotropicales para el periodo 2010 – 2012. el objetivo principal es el de consolidar y dar continuidad a las actividades ya iniciadas en la iBa del pnSng a través de la conformación de un gal que promueva actividades de conservación, sensibilización ambiental y manejo adecuado de sus recursos; además, proporcionar capacitación en observación e identificación de aves como una alternativa en el desarrollo del aviturismo, y obtener mayor información de la reinita cerúlea aplicando un monitoreo participativo (ciencia ciudadana).

Área De eStUDio Y MÉtoDoS

Área de estudio. el parque nacional Sumaco napo – galeras el cual comprende una superficie de 205.249 hectáreas (MAE 2010) y se encuentra al nororiente de ecuador (Fig. 1). tiene un rango de elevación que va desde los

Boreal (Contopus cooperi ), entre otras (ridgely & Greenfield 2001, Guevara & Santander 2010). por otro lado, el hecho de que la reinita Cerúlea pueda ocupar hábitat modificados por actividades humanas como cultivos de sombra o bordes de bosque, genera una oportunidad para la conservación e investigación de la especie en este tipo de ambientes mediante la participación de la gente (Fundación proaves et al. 2010).

Desde el año 2005 aves&conservación ha venido realizando estudios de la reinita cerúlea (datos no publicados), que en conjunto con otras investigaciones llevadas a cabo en el país (Juiña 2008) se ha podido establecer una línea base de registros e información ecológica de la especie. Sin embargo, varios aspectos ecológicos y socio-económicos relacionados a sitios de invernada de la reinita cerúlea en ecuador son poco conocidos, en comparación a los generados en la porción norte de su distribución invernal, especialmente en cultivos mixtos como los cafetales de sombra en colombia (Fundación proaves et al. 2010) y Venezuela (Barkermans et al. 2009).

considerando que algunas Áreas importantes para la conservación de las aves (iBas, del inglés important Bird areas) están cubiertas por el rango invernal de la Reinita Cerúlea, hemos identificado la IBA del parque nacional Sumaco napo – galeras (pnSng), además reserva de Biosfera como sitio prioritario para enfocar esfuerzos de conservación. el pnSng representa uno de los sitios con mayor número de registros para la especie que se han obtenido a través de las expediciones realizadas por aves&conservación y de acuerdo a mapas de distribución potencial es una zona con más altas probabilidades de la presencia de la especie (Barrer et al. 2010, Fundación proaves et al. 2010). además, en la zona de amortiguamiento del parque existe un paisaje mixto entre remanentes de bosque, bosque secundario, bordes de bosque, pastos para el

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900 a los 3900 m s.n.m por lo que incluye varios ecosistemas desde bosques subtropicales hasta páramo, este último encontrado en la cima del Volcán Sumaco (Freile & Santander 2005). el monitoreo se ejecuta en dos localidades del área de influencia al sur del PNSNG que se describen a continuación.

Wild Sumaco Wildlife Sanctuary (WSWS). está ubicado en la provincia de napo (00º41’S, 77º36’W, 1463 m s.n.m.) cerca de la comunidad de pacto Sumaco (Fig. 1). Se trata de un conjunto

de fincas que mantienen remanentes en buen estado de bosque siempreverde piemontano y bosque siempreverde montano bajo (Sierra 1999), además de bosques secundarios y pastizales. Se encuentran manejadas por la Fundación río pucuno, la cual ha dedicado la tierra a la conservación, especialmente al turismo de observación de aves.

Reserva Biológica del Río Bigal (rBrB). corresponde a la provincia de orellana (00º32’S, 77º25’W, 970 m s.n.m.), de igual

Fig. 1. localidades del proyecto en el área de amortiguamiento del parque nacional Sumaco napo – gal-eras, nororiente de ecuador.

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manera se ubica en la parte sur del pnSng siendo el río Bigal el límite de la reserva con el parque (Fig. 1). esta reserva está a cargo de la Fundación Sumac Muyu y mantiene principalmente bosque siempreverde piemontano (Sierra 1999) en buen estado de conservación aunque algunas partes han sido taladas selectivamente.

Grupos de Apoyo Local. la conformación de los gal se llevó a cabo a través de reuniones de socialización en las que participaron actores locales ubicados en el área cercana a los sitios de monitoreo. Una vez que se explicó la forma de trabajo de los gal, las personas interesadas en formar parte de los grupos acordaron asistir a las reuniones de carácter mensual. para facilitar el trabajo de coordinación se elaboró una base de datos de los actores locales. el propósito de las reuniones es tratar temas ambientales y de conservación que sean de interés, al mismo tiempo identificar y planificar acciones de conservación que serán ejecutadas por los miembros del gal con la finalidad de sensibilizar en el uso de los recursos, dar a conocer el proyecto, las especies de aves migratorias y afianzar los conocimientos provistos durante la capacitación. estas actividades se realizan con la producción de materiales y se acompañan de salidas de observación de aves, obras de títeres, pintura de murales, manualidades con materiales reciclados, dibujo y caritas pintadas para los niños que tienen buena acogida entre la población en general. adicionalmente, cada mes se lleva a cabo un taller relacionado principalmente a la observación e identificación de aves, monitoreo, aviturismo, guía de turismo, y buenas prácticas ambientales para el desarrollo del aviturismo.

Monitoreo participativo. Se realiza el monitoreo mensualmente en cada localidad liderado por el técnico ornitólogo y al menos uno de los

actores locales que hayan sido capacitados en técnicas de observación, identificación y censos de aves. para el monitoreo se emplean los censos audiovisuales en transectos lineales (Bibby et al. 1998). los transectos tienen ca. 1,5 – 2 km, se visitan durante dos días consecutivos a lo largo de la época no-reproductiva (septiembre – abril). al observar la reinita cerúlea se anotan datos detallados de la observación y de las bandadas mixtas en las que se encuentra.

reSUltaDoS

Se realizó una reunión de socialización por grupo, sin embargo dado que en la segunda reunión asistieron personas nuevas fue preciso realizar una presentación adicional. los gal de la iBa pnSng están constituidos por representantes de las dos localidades previamente descritas. en la localidad de WSWS, que llamamos “alta”, hay 25 miembros (14 hombres, 11 mujeres) entre guardaparques, profesores del colegio almindaris, Fundación río pucuno, reserva reinita cerúlea narupa, personas de la comunidad de pacto Sumaco y del centro de turismo comunitario. en este gal la totalidad de sus miembros son colonos, cuyo arribo a la zona es reciente y provienen del sector del volcán reventador, fueron reubicados en este sector debido a la fuerte erupción ocurrida a finales de los 1980. Estas personas son en su mayoría agricultores que se dedican principalmente al cultivo de naranjilla, además de la ganadería y en ocasiones a la extracción de madera. por otra parte, en la localidad de rBrB, que llamamos “baja”, hay 19 miembros (15 hombres, 4 mujeres) de organizaciones locales (Fundación Sumac Muyu, turismo comunitario de Waskila, red de turismo comunitrario Huataraco – Suno, Sociedad civil y comercial de turismo loreto – Kawsay), comunidades (San José de payamino, 8 de Diciembre, Huaticocha),

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guardaparques y estudiantes del colegio de turismo ramón andi. Un mayor porcentaje de miembros en este gal pertenecen a comunidades indígenas Kichwa dedicados de igual manera a actividades de agricultura y ganadería. en ambos grupos más de la mitad de los participantes son personas mayores de 25 años, con educación secundaria.

Se han llevado a cabo un total de 19 reuniones con los dos gal que corresponden a un período de 14 meses de ejecución del proyecto. Durante este tiempo ha sido posible su participación en dos ferias donde se habrá llegado a ca. 1000 personas; se organizó el Festival Mundial de las aves con la participación de 150 niños; se visitó la reserva reinita cerúlea en narupa (administrada por la Fundación Jocotoco) con los miembros del gal de la localidad alta; se celebró la navidad Verde y a las aves Migratorias, estas dos últimas en la escuela de pacto Sumaco con 80 niños. por otro lado, se ha gestionado tres talleres con la Fundación Mashcana en tecnologías limpias para las personas de los gal y otros miembros de la comunidad; se ha colaborado con el Ministerio del ambiente en el curso para 19 candidatos a guías naturalistas del pnSng; se ha mantenido reuniones con otras organizaciones para la coordinación de acciones como las Fundaciones Jocotoco, Sumac Muyu, río pucuno y paz y Desarrollo; y los gobiernos autónomos Descentralizados de Loreto y Archidona para la firma de acuerdos de cooperación.

en un período de un año (diciembre 2010 – 2011) se han llevado a cabo seis talleres teórico – prácticos, de dos días de duración cada uno, en observación e identificación de aves para cada gal (Fig. 2). Sin embargo, durante la mayoría de visitas se realizó una salida de observación de aves. los temas de la capacitación son integrales y han servido para que los participantes adquieran información no solamente de las aves sino que entiendan de manera general aspectos

de ecología, ornitología básica y conservación. en cuanto a las salidas prácticas han permitido a las personas aprender a utilizar los binoculares, la guía de campo y sobre todo reconocer las especies de aves, al momento contamos con un grupo de personas que pueden realizar una identificación principalmente visual de las aves de la iBa.

además, se han realizado dos talleres en técnicas de monitoreo en cada gal y de las c. 168 horas invertidas en los monitoreos entre octubre 2010 y diciembre 2011, al menos 132 h han sido realizadas en compañía de una persona del gal, de los cuales uno se encuentra realizando observaciones fuera de los censos estandarizados. en base a las capacitaciones y habilidades individuales hemos podido identificar al momento siete monitores potenciales. en este periodo existen 14 registros (3 hembras y 11 machos) de la reinita cerúlea. once corresponden al área de WSWS y 3 a la rBrB. en todos los casos la reinita cerúlea se encontraba acompañando bandadas mixtas. adicionalmente, en este período se han registrado las siguientes especies de aves migratorias: pibí Boreal, pibí occidental (C. sordidulus), Zorzal de Swainson (Catharus ustulatus), reinita pechinaranja, candelita norteña, reinita plañidera (Geothlypis philadelphia), reinita collareja, piranga roja (Piranga rubra) y piranga escarlata (P. olivacea). Se debe indicar que los resultados provenientes tanto de los monitoreos como del análisis del hábitat se publicarán por separado.

DiScUSiÓn

el empoderamiento local para la conservación de las IBAs en beneficio de la biodiversidad y la gente se encuentra entre los principales enfoques de Birdlife para generar un cambio (Birdlife internacional 2011). la creación de los grupos de apoyo local constituye una base multiplicadora de acciones locales que

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proyecto. la capacitación ha sido fundamental para que las personas entiendan los procesos ecológicos y tengan la información adecuada que les permita identificar las amenazas, defender sus propios intereses y desarrollar las estrategias de manejo de sus recursos naturales a mediano y largo plazo. De igual manera la participación del gal en los procesos de sensibilización con los niños de las comunidades ha sido enriquecedora y les ha permitido tener un rol activo además de un posicionamiento local. el empoderamiento de los habitantes locales mediante la conformación de los gal y la participación democrática en la toma de decisiones puede proporcionar un conocimiento invaluable sobre los saberes y la ecología local e incrementar la flexibilidad potencial en responder a la incertidumbre y el cambio en el uso de recursos naturales (endara com. pers.).

de otro modo sería difícil realizar. en base a nuestra experiencia es importante contar con un grupo variado de personas que no solo incluyan representantes de comunidades: es enriquecedor incluir a miembros de otras organizaciones, centros educativos y autoridades estatales ya sea de ministerio y gobiernos locales. en este caso, esto último lo constituyen los guardaparques del pnSng, quienes cumplen un rol fundamental en el grupo. Se podría decir que el nivel de representación de los diferentes actores responde a las dinámicas sociales e institucionales de cada una de las áreas, debido a esto en la localidad baja donde existen comunidades originarias indígenas se cuenta con una pobre participación de la mujer. por otro lado, las reuniones ofrecen un espacio de discusión y organización de los miembros donde se desarrollan capacidades de gestión ambiental y la toma de decisiones para la implementación del

Fig. 2. Miembros del gal durante una práctica de observación de aves.

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de desarrollar el aviturismo como alternativa económica sustentable que todavía no está bien desarrollada en el área. Sin embargo, tiene un gran potencial conjuntamente con el desarrollo de turismo de naturaleza y científico especialmente en el Volcán Sumaco y como parte de otras iniciativas que se están promoviendo en la zona.

la creación de los gal necesita una dinámica cuyo principal reto es su permanencia a lo largo del tiempo. el apoyo de una organización es apropiado para su fortalecimiento, desarrollo de propuestas y priorización de actividades. también en la integración de los miembros con el fin de que sus aportes sean significativos y se generen experiencias positivas que se puedan replicar. Sin embargo, se debe buscar y definir los niveles la co-participación de los actores involucrados así como recursos locales que ayuden a promover las actividades planteadas. en los gal que ha formado aves&conservación, las capacitaciones en la observación e identificación de aves y su aplicación en el aviturismo han sido los principales atrayentes pero hay que tener en cuenta que esta actividad no siempre se puede aplicar en todos los sitios donde se desea promover la conservación.

agraDeciMientoS

estamos muy agradecidos al personal de aves&conservación por su apoyo, principalmente David Díaz, adriana lara, claudia Vinueza, rolando Hipo y Sergio niquinga. este proyecto ha sido posible gracias al financiamiento otorgado por el Acta de conservación de aves Migratorias neotropicales y la asistencia de guy Foulks. los promotores locales carmen andi, Marta trujillo y thierry garcía han contribuido de manera importante a la ejecución del proyecto. a los voluntarios Marcelo armijos, Jorge Sandoval y Juan olivo. el apoyo de las fundaciones de base y sus representantes Jonas nilsson, Marion garcía,

Por otro lado, la identificación de aves en un país especialmente diverso como ecuador establece grandes desafíos. Debido a que el proceso de capacitación no termina aún no tenemos una evaluación; sin embargo, en un proceso previo, utilizando la misma metodología, con algunos miembros del gal de la localidad alta, el promedio fue de 3,81 puntos de 11 en las evaluaciones iniciales mientras que luego de cuatro talleres la puntuación promedio fue de 7,99 (guevara & Santander 2010). en este proyecto, el proceso de capacitación es el mismo pero se ha considerado por más tiempo y con más temas por lo que se espera que el aprendizaje sea el suficiente para que los participantes se familiaricen con las especies de aves de la zona permitiendo llegar a su identificación de manera visual y auditiva.

los proyectos basados en la ciencia ciudadana cada vez adquieren más relevancia y han demostrado su efectividad tanto en el levantamiento de información como en procesos de monitoreo, manejo de recursos, incidencia política, entre otros (Birdlife internacional 2010, Botero et al. 2010). en este proyecto la formación de los gal están concebidos con la finalidad promover la ciencia ciudadana para conducir un monitoreo participativo de la reinita cerúlea. Se considera que en el futuro la posibilidad de tener personas capacitadas puede incrementar el establecimiento de más transectos de monitoreo, cubriendo un área mayor y mantenida en el tiempo. además, los resultados del monitoreo sirven como una herramienta de empoderamiento de las comunidades al conocer la diversidad de aves que poseen (Botero et al. 2010) y permite que la gente se identifique con la investigación y conservación del hábitat y la reinita cerúlea, otras aves migratorias y la biodiversidad de la zona. es así, que la mayoría de personas, incluyendo los niños, en las zonas de estudio conocen de la reinita cerúlea aunque muy pocos la han visto. las capacitaciones, además, brindan a los participantes una alternativa

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del Huila. Federación nacional de cafeteros de colombia – cenicafé, caldas, colombia. Disponible en http://www.cafesanisidro.com/site/librodeaves.pDF

Freile, J. F., & t. Santander. 2005. Áreas importantes para la conservación de las aves en ecuador. aves&conservación, Birdlife internacional, conservación internacional & Ministerio del ambiente, Quito, ecuador.

Fundación proaves, american Bird conservancy & el grupo cerúleo. 2010. conservation plan for the cerulean Warbler on its nonbreeding range - plan de conservación para la reinita cerúlea sobre su rango no reproductivo. conserv. colomb 12: 1–62.

guevara, e., & t. Santander. 2010. preserving cerulean Warbler (Dendroica cerulea) winter habitat in ecuador. aves & conservación, Quito, ecuador.

Hamel, p. B. 2000. cerulean Warbler (Dendroica cerulea). In poole, a., & F. gill (eds). the Birds of north america, no. 511. the birds of north america, inc., philadelphia, pennsylvania, USa.

Juiña, M. 2008. estudio ecológico de reinita cerúlea (Dendroica cerulea) en las reservas de la Fundación de conservación Jocotoco - ecuador. Fundación Jocotoco, Quito, ecuador.

Ministerio del ambiente del ecuador (Mae). 2010. reservas de Biosfera del ecuador: lugares excepcionales. gtZ/geSoren, DeD, WcS, nci, UneSco, Quito. ecuador

Ridgely, R. S., & P. Greenfield. 2001. The Birds of ecuador: Status Distribution and taxonomy. cornell Univ. press. ithaca, new York, USa.

robbins, c. S., J. W. Fitzpatrick, & p. B. Hamel. 1992. a warbler in trouble: Dendroica cerulea. pp. 549–562 in Hagan iii, J. M., & D. W. Johnston (eds). ecology and conservation of neotropical Migrant landbirds. Smithsonian institution press, Washington, D.c., USa.

Sierra, r. 1999. propuesta preliminar de un sistema de clasificación de vegetación para el ecuador continental. proyecto instituto ecuatoriano Forestal y de Áreas naturales y de Vida Silvestre/global environmental Facility, ecociencia, Quito, ecuador.

Zoltan Waliczky, gerardo Vasquez y personas del centro de turismo comunitario de pacto Sumaco ha sido fundamental. De igual manera la colaboración de la geógrafa cayetana Salao, gonzalo aguirre e irma Jurrius del Ministerio del ambiente y los monitores locales Byron gualavisi y alex chimbo. expresamos nuestro agradecimiento a David Mehlman, carol lively y gabriel colorado por su colaboración en diferentes etapas del estudio de la reinita Cerúlea. El manuscrito se ha beneficiado de los acertados comentarios de paolo ramoni-perazzi y paul Hamel.

reFerenciaS

Bakermans, M. H., a. c. Vitz, a. D. rodewald, & c. g. rengifo. 2009. Migratory songbird use of shade coffee in the Venezuelan andes with implications for conservation of cerulean Warbler. Biol. conserv. 142: 2476–2483.

Barker, S., S. Benítez, J. Baldy, D. cisneros Heredia, g. colorado Zuluaga, F. cuesta, i. Davidson, D. Díaz, a. ganzenmueller, S. garcía, M. K. girvan, e. guevara, p. Hamel, a. B. Hennessey, o. l. Hernández, S. Herzog, D. Mehlman, M. i. Moreno, e. ozdenerol, p. ramoni-perazzi, M. romero, D. romo, p. Salaman, t. Santander, c. tovar, M. Welton, t. Will, c. pedraza, & g. galindo. 2006. Modeling the South american range of the cerulean Warbler. In proceedings of the 2006 eSri international User conference, San Diego, california, USa. available at proceedings.esri.com/library/userconf/proc06/papers/papers/pap_1656.pdf

Bibby, c., M. Jones, & S. Marsden. 1998. expedition Field techniques, Bird Surveys. expedition advisory centre, J. roy. geogr. Soc. lond., london, UK.

Birdlife international. 2011. empowering the grassroots—Birdlife, participation, and local communities. Birdlife international, cambridge, UK.

Botero, J. e., a. M. lópez, r. espinoza, & c. casas. 2010. aves de zonas cafeteras del sur

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POPULATION DISTRIBUTION, DENSITy AND HABITAT PREfERENCE Of THE CERULEAN WARBLER (sEtOphAGA

CErulEA) IN THE DELAWARE WATER GAP NATIONAL RECREATION AREA

Shannon Curley1, Terry Master1 & Gregory George2

1Department of Biological Sciences, East Stroudsburg University, 200 Prospect Street, East Stroudsburg, PA 18301. E-mail: [email protected]

2Department of Biological Sciences, Delaware Valley College, 700 East Butler Avenue, Doylestown, PA 18901

Resumen. – Distribución poblacional, densidad y preferencia de hábitat de la Reinita Cerúlea (setophaga cerulea) en el Área Nacional de Recreación del Paso de Agua de Delaware. – Recientemente, el rango de reproducción de la Reinita Cerúlea se ha expandido a bosques de crecimiento secundario y a tierras convertidas a la agricultura en el noreste de los Estados Unidos donde, de acuerdo al Estudio de Aves Reproductivas, la población está incrementando. A pesar de esta expansión en una parte del rango, la población como un todo está todavía en rápida declinación, suponiendo de esta manera que la calidad del hábitat reemplaza a la importancia de la expansión del mismo. El Área Nacional de Recreación del Paso de Agua de Delaware (ANRD) constituye una muestra de la reciente ocupación de hábitat en el noreste. Encontramos Reinitas Cerúleas anidando en densidades relativamente bajas, en comparación con el centro de la distribución en Virginia Occidental, en la mayoría de las partes australes y centrales del parque donde la especie fue confirmada. En uno de los sitios de estudio en particular, Freeman Tract Road, las densidades de anidación compiten con aquellas del centro de la distribución de la especie. Las parcelas de muestreo en los territorio se caracterizaron por un predominio más alto de lo esperado de nogal negro (Juglans nigra) y sicómoro americano (Platanus occidentalis) mientras que el roble rojo del norte (Quercus rubra) y especies de árboles siempreverdes fueron menos predominantes que en parcelas ubicadas al azar. Las parcelas territoriales también exhibieron un estrato arbustivo más desarrollado y alto. El hábitat reproductivo ocupado recientemente en el noreste, tal como el de ANRD, pueden de esta manera servir como una fortaleza en el futuro de la población y como un sitio de estudio para establecer esfuerzos que lleven a comprender los requerimientos de hábitat de la Reinita Cerúlea en el noreste de los Estados Unidos.

Abstract. – The breeding range of the Cerulean Warbler has expanded into second-growth forest and con-verted agricultural land in the northeastern United States where, according to the North American Breeding Bird Survey, the population is increasing. Despite this expansion in one part of its range, the population as a whole is still in rapid decline implying that habitat quality supersedes habitat expansion in importance. The Delaware Water Gap National Recreation Area (DEWA) in New Jersey and Pennsylvania, USA, is represen-tative of recently occupied northeastern habitat. We found Cerulean Warblers breeding at relatively low den-sities, compared to their core range in West Virginia, in most of the southern and central portions of the park to which the species was confined. On one particular study site, the Freeman Tract Road, breeding densities did rival those of the species’ core range. Sampling plots within Cerulean Warbler territories were character-ized by a higher than expected prevalence of black walnut (Juglans nigra) and American sycamore (Platanus occidentalis) while northern red oak (Quercus rubra) and evergreen tree species were less prevalent than on randomly placed plots. Territorial plots also exhibited a more developed and taller shrub layer. Recently occupied breeding habitat, such as DEWA, may thus serve as a population stronghold in the future and as a study site for efforts to further understand Cerulean Warbler habitat requirements in the northeastern U.S.

Key words: Cerulean Warbler, Distribution, Habitat Preference, Population Density

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in a localized area, thus warranting further investigation of abundance and distribution within the entire park.

Bird Surveys. one-km transect surveys were conducted within DeWa from 3–30 June 2009 and 26 May–28 June 2010 using a modified Emlen transect protocol (Emlen 1977). each transect was located along roads or trails that ran parallel to the Delaware river. placement of these transects was determined by overlaying a 2-km2 block grid over 2002 DeWa orthophotography using arcView giS® 9.1. Blocks were numbered and evaluated for habitat composition. transects were placed along roads or trails that ran parallel to the Delaware River in a stratified random fashion within blocks that met our predetermined criteria based on known habitat preferences of the cerulean Warbler.

transects were traversed on foot between 05:30–08:30 am. During each transect survey, any visual or auditory cues from cerulean Warblers were recorded as well as the distance and direction (either to the right or left) of the bird from the transect line, and the time of the detection. only observations that occurred within 50 m laterally from the transect line were recorded in order to minimize difficulties with cue attenuation at greater distances (ralph et al. 1995). During the 2009 field season, 10 transects were surveyed three times each for a total of 30 transect traverses. During the 2010 field season, four additional transects were added and all 14 transects were surveyed four times for a total of 56 transect traverses. ad hoc roadside surveys were also conducted opportunistically to supplement transect data in order to get an accurate representation of overall cerulean Warbler distribution within DeWa. Sites were revisited on separate, but never consecutive, days to further monitor cerulean Warbler activity.

Densities were determined by employing spot mapping of the registrations within the

introDUction

the cerulean Warbler (Setophaga cerulea) is a neotropical migrant songbird of conservation concern. Habitat fragmentation as a result of human activity has impacted much of its breeding range, and, consequently, the population is experiencing the most rapid rate of decline of any neotropical migrant songbird (Sauer et al. 2011). Simultaneously, the breeding range has expanded into second-growth forest on abandoned agricultural land in the northeastern United States where, according to the north american Breeding Bird Survey (see http://www.pwrc.usgs.gov/bbs), the pop-ulation is increasing. Despite this expansion in a portion of its range, the population as a whole is still in rapid decline implying that habitat quality supersedes habitat expansion in importance. this study, designed to document abundance, distribution and habitat preferences of cerulean Warblers in representative northeastern habitat, was conducted in the Delaware Water gap national recreation area (DeWa).

MetHoDS

Study Site. DeWa consists of nearly 70,000 acres on both the new Jersey and pennsylvania sides of the Delaware river, including parts of Sussex and Warren counties in new Jersey and Monroe, northampton and pike counties in pennsylvania. the park protects 40 miles of the Delaware river, the longest major undammed river in the eastern U. S., and one of the cleanest large rivers in the country. it is composed of a mosaic of habitats, including active agricultural land, river islands, palustrine wetlands, early successional habitats, hemlock-lined stream ravines and secondary but maturing upland and riparian deciduous forest. preliminary surveys in 2006 (t. Master, unpublished data), conducted in an area known as the Freeman tract road, revealed relatively high densities of cerulean Warblers

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given area of each transect. territory presence, whether detected by transect traverses or ad hoc surveys, was determined when cerulean Warbler activity was recorded on at least three separate occasions at the same location. Both methods were used to determine distribution in the park, but only transect surveys were used to calculate territorial densities.

Vegetation Surveys. a vegetation analysis was conducted during the summer of 2010 in order to determine if vegetation variables varied between random and occupied territory plots. For territory vegetation plots, favorite song trees (trees where a cerulean Warbler was frequently seen singing) or trees where activity was pronounced were used as the center point of the vegetation plot. Five stratified random vegetation plots were sampled every 200 m on each transect. each plot was randomly placed on the left or right side of the transect line (determined by coin flip) and a random number table was used to determine how far the plots would be placed laterally from the transect line at 10-m intervals out to 40 m. We used a modified BBird protocol (Martin et al. 1997) to measure vegetation variables including tree species composition, diameter at breast height (DBH), ecological importance Values (iV) (by adding relative density, relative frequency and relative dominance values determined from tree basal areas), foliage height distribution, and shrub layer height and coverage.

a pearson’s chi-squared analysis using r statistical language (r Development core team 2011) was used to determine if significant differences existed between tree species composition in random and territory plots. a subdivided contingency table was also used in r to determine which tree species had the most influence over tree species composition in territory plots. tree species occurring more or less frequently than expected on cerulean Warbler territories were determined by subtracting random plot iVs

from territory plot iVs. the residual numbers from these calculations were either positive or negative. positive values indicated trees occurring more frequently in territory plots than expected based on their availability within random plots. t-tests were conduced using Microsoft excel© and iBM SpSS© (version 18.0) to evaluate differences between territory plots and random plots in foliage height distribution and shrub height.

reSUltS

Distribution. in 2009 and 2010 cerulean Warblers were confirmed breeding within DEWA. In 2009, 22 singing males were recorded on the transects and ad hoc roadside surveys and in 2010, 68 singing males were observed (Fig. 1). in both years, the locations of cerulean Warbler territories were confined to the southern and central portions of DeWa.

Density. in 2009, cerulean Warblers were detected on five of the ten transects (x

– 5 0.20,

Se = 0.041) (Fig. 2). in 2010, eight of the 14 transects had cerulean Warbler territories ( x

– 5 0.24, Se 5 0.075) (Fig. 2). three of the four transects with cerulean Warbler territories in 2009 also had territories present in 2010. all transects without cerulean Warbler registrations and activity in 2009 showed no activity in 2010 either. all transects with no activity in either year were located in the northern portion of DeWa.

Habitat Preference. tree species composition was significantly different in random versus territory plots (χ2 5 187.2, df 5 14, p # 0.001). Black walnut (Juglans nigra), american sycamore (Platanus occidentalis), sugar maple (Acer saccharum), green ash (Fraxinus pennsylvanica), and slippery elm (Ulmus rubra), occurred more frequently on territory plots than expected (Fig. 3). tree species that occurred less frequently than expected included northern red oak

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Fig. 1. cerulean Warbler distribution within the Delaware Water gap national recreation area in 2009 and 2010.

Fig. 2. cerulean Warbler densities in the Delaware Water gap national recreation area in 2009 and 2010. transects ordered from southern most to northern most from left to right.

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Fig. 3. occurrence of tree species on territory plots. positive values indicate more frequent occurrence than expected while negative values indicate less frequent occurrence than expected when compared to random plots. Species: american beech (Fagus grandifolia, aMBe), ash spp. (aSH), black birch (BlBi), black locust (Robinia pseudoacacia, Bllo), black walnut (BlWa), eastern hemlock (eaHe), green ash (graS), northern red oak (nroa), red maple (Acer rubrum, reMa), slippery elm (Slel), sugar maple (SUMa), american sycamore (SYca), tulip poplar (Liriodendron tulipifera, tUpo), white oak (Quercus alba, WHoa) and white pine (WHpi).

(Quercus rubra), black birch (Betula lenta), eastern hemlock (Tsuga canadesis), and white pine (Pinus strobus) (Fig. 3).

There was no significant difference in foliage distribution at any height interval between territory and random plots (p = 0.84). the distribution of foliage was generally consistent among transects, with the majority of the vegetation occurring at the sub-canopy and canopy level. the mean shrub height was significantly higher in territory plots than in random plots, 2.1 m versus 1.0 m, (p , 0.0001). thus, occupied cerulean Warbler habitat was characterized by the presence of several deciduous tree species occurring more frequently than expected compared to random plots, a total lack of evergreen species,

and a well-defined shrub layer, indicating the presence of canopy gaps.

DiScUSSion

in both 2009 and 2010, cerulean Warblers were confined to the southern and especially the central portion of DeWa. at least in part, this restricted spatial distribution might be explained by their habitat preferences and breeding ecology, including a tendency to demonstrate site fidelity and clustered territoriality (colorado & cuadros 2004, Jones et al. 2004, Moreno et al. 2006, Bakermans 2008, roth & islam 2008). on transects where coniferous tree species, primarily white pine and eastern hemlock, were among the

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acKnoWleDgMentS

thanks are due to the pennsylvania State System of Higher education and the east Stroudsburg University Faculty Development and research committee for funding this project. We also thank Jeff Shreiner and the DeWa park resource and research planning Office for their permission to conduct our research. Joe Yuhas, Don Detwiler and Matt Bouboulis generously assisted in the field and nick ernst provided technical support.

reFerenceS

Baker, Frederick S. 1948. a revised tolerance table. J. Forest. 47: 179–181.

Bakermans, M. H. 2008. Demography and habitat use of cerulean Warblers on breeding and wintering grounds. ph.D. diss. ohio State Univ., columbus, ohio, USa.

Barg, J. J., D. M. aiama, J. Jones, & r. J. robertson. 2006. Within-territory use and microhabitat selection by male cerulean warblers (Dendroica cerulea). auk 123: 795–806.

colorado, g. J. & t. cuadros. 2004. Habitat use in wintering grounds by cerulean Warbler (Dendroica cerulea) in native vegetation and agroecosystems in the Western cordillera, northern colombia. Final report presented to the nature concervancy, Medellin, colombia.

emlen, J. t. 1977. estimating breeding season bird densities from transect counts. auk 94: 455–468.

george, g.a. 2008. Foraging ecology of male cerulean Warblers and other neotropical migrants. ph.D. diss., West Virginia Univ., Morgantown, West Virginia, USa.

Hamel, p. B. 2000. cerulean Warbler (Dendroica cerulea). In poole, a., & F. gill (eds). the Birds of north america, no. 511. the Birds of north america, inc., philadelphia, pennsylvania, USa.

Jones, J., J. J. Barg, t. S. Sillett, M. l. Veit, & r.J. robertson. 2004. Minimum estimates of survival and population growth for cerulean

dominant tree species, no cerulean Warbler activity was recorded.

Densities were generally lower than expected based on the preliminary surveys done in 2006 on the Freeman tract road (t. Master, unpublished data). However, densities at this site during the current study were comparable, and in some cases higher, than those reported from the core of the species’ breeding range in West Virginia (cf. Weakland & Wood 2005) and from Hamel (2000).

the tree species that occurred most frequently in territories and was most commonly used as a song perch within DeWa was black walnut. Black walnut is described as a shade intolerant tree that has to be a dominant or co-dominant species within a mixed-species stand in order to persist (Baker 1948). in DeWa, black walnut exhibits late leaf-out. a study by Barg et al. (2006) found that bitternut hickory (Carya cordiformis) was a preferred song post for cerulean Warblers in ontario. this species also exhibits late leaf-out like our black walnut. they suggested that tree species with late leaf-out may be coveted as song posts by providing less acoustic hindrance for song transmission and increased visibility for monitoring conspecifics. At a microhabitat scale, cerulean Warblers have been shown to prefer particular tree species within their territories even though these species may not be particularly common in surrounding habitat. george (2008) found that cerulean Warblers preferred foraging in chestnut oaks (Quercus prinus), hickories, and maples in West Virginia.

northern red oak was the tree species occurring least frequently on territories compared to random plots and was in fact among the most common species generally. george (2008) found that cerulean Warblers did not select northern red oak for foraging. this may be related to food resource availability, however conclusive evidence for this explanation has remained elusive.

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standards and applications. pp. 161–168 in ralph, c. J., J. r. Sauer, & S. Droege (eds.) Monitoring bird populations by point counts. USDa Forest Service gen. tech. rep. pSW-gtr-149.

roth, K. l., & K. islam. 2008. Habitat selection and reproductive success of cerulean Warblers in indiana. Wilson J. ornithol. 120: 105–110.

Sauer J. r., J. e. Hines, J. Fallon, K. l. pardieck, D. J. Ziolkowski, Jr., & W. a. link. 2011. the north american Breeding Bird Survey, results and analysis 1966-2010. Version 12.07.2011. available at http://www.mbr-pwrc.usgs.gov/bbs/bbs.html.

Weakland, c. a., & p. B. Wood. 2005. cerulean Warbler (Dendroica cerulea) microhabitat and landscape-level habitat characteristics in southern West Virginia. auk 122: 497–508.

warblers (Dendroica cerulea) breeding in ontario, canada. auk 121: 15–22.

Martin, t. e., c. r. paine, c. J. conway, W. M. Hochachka, p. allen, & W. Jenkins. 1997. BBIRD field protocol. Montana Cooperative Wildlife research Unit, University of Montana, Missoula, Montana, USa. available at http://www.umt.edu/bbird/protocol/default.aspx.

Moreno, M. i., a. Morales, & J. Velasquez. 2006b. evaluation of the range and distribution of Dendroica cerulea in colombia. Fundación proaves de colombia. Final report and presenation to the nature consevancy. June 2006.

r Development core team. 2011. r: a language and enviromnent for statistical computing. r Foundation for Statistical computing, Vienna, austria. available at http://www.r-project.org.

ralph, c. J., S. Droege, & J. r. Sauer. 1995. Managing and monitoring birds using point counts:

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ornitologia neotropical 23: 359–366, 2012© the neotropical ornithological Society

fORAGING ECOLOGy Of THE CERULEAN WARBLER (sEtOphAGA CErulEA) IN ANDEAN

AGROfORESTRy ECOSySTEMS

Jenny M. Muñoz1 & Gabriel J. Colorado2

1Universidad de Antioquia, Instituto de Biología, Apartado Aéreo 1226, Medellín, Colombia. E-mail: [email protected]

2Universidad de Antioquia, Instituto de Biología, Calle 67 No 53-108 Oficina 7-233. Medellin, Colombia. E-mail: [email protected]

Resumen. – Ecología alimentaria de la reinita cerulea (setophaga cerulea) en ecosistemas agrofores-tales Andinos – La ecología alimentaria permite conocer los requerimientos de las especies y enfocar los esfuerzos de conservación. Estudiamos la ecología alimentaria de la migratoria Neotropical reinita cerúlea (Setophaga cerulea) durante el invierno boreal en sus cuarteles de invierno en ecosistemas agroforestales de café en las cordilleras Occidental y Central de los Andes en Colombia. La reinita cerúlea se alimenta activamente en el follaje, picando principalmente en el haz de hojas verdes y en flores. Frecuentan arbustos y árboles de tamaño medio-alto donde se alimentan en el subdosel y sotobosque usando el estrato distal. Machos y hembras difirieron en la altura de alimentación, con los primeros alimentándose en las partes más altas de los árboles. Las reinitas usualmente forman parejas o pequeños grupos que se unen a bandadas mixtas. Adicionalmente documentamos el comportamiento social de la reinita cerúlea e interacciones com-petitivas con las migratorias Setophaga fusca y S. castanea.

Abstract. – Foraging ecology provides insight into species requirements and focus conservation efforts. We studied foraging ecology of the Neotropical migrant Cerulean warbler (Setophaga cerulea) during the winter season in coffee agroforestry ecosystems of the Central and Western Cordillera of the Andes in Colombia. Our findings show that this species is an active foliage gleaner. Cerulean Warbler primarily gleans prey off the upper surface on green leaves and flowers. It frequents shrubs and medium-high trees and forage most often in subcanopy and understory using the outer strata. There were sex differences in the foraging height. Frequently, Cerulean Warbler was encountered in pairs or small groups rather than join in mixed bird flocks. Additionally we documentedteh social behavior and competitive interaction with Setophaga fusca and S. castanea.

Key words: Setophaga cerulea, Neotropical migrant, foraging ecology, winter ground, agroforestry ecosys-tems, Colombia, and Cerulean warbler.

introDUction

recent population declines in the neotropical migrant cerulean Warbler have been widely documented (Buehler et al. 2008). However, most research efforts have been focused on the breeding grounds, and few studies have been published on the migratory and winter periods (robbins et al. 1992, Faaborg et al. 2010). Despite the lack of information

on limiting factors for this bird and other migrants on their wintering grounds, several studies suggest that habitat quality during the non-breeding season may strongly influence population performance and survival for at least some species of neotropical migrants (Marra & Holmes 2001, latta & Faaborg 2002, Sherry et al. 2005).

cerulean Warbler spends the boreal winter along the andes mountains of northern South

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ranging from 1400–1680 m.a.s.l. located in the municipalities of Fredonia (5°56’n, 75°39’W), Jerico (5°48’n, 75°48’W), and tamesis (5°45’n, 75°42’W) in antioquia Department, in the central and Western cordillera of the andes in colombia during the winter season 2010–2011. the study period embraced the dry season in this region.

Foraging observations. a focal individual approach was used to collect foraging observations. Focal individuals of cerulean Warbler were located using systematic searching from 6:00–12:00 h and 14:00–17:00 h walking along trails through the study habitat while listening and searching visually for birds. Once identified, individuals were followed and observations were made beginning 15 s after the initial sighting for up to 30 s. after an observation was finished, we typically moved 150 m from the location before collecting additional data to avoid resampling the same bird. each site was surveyed once every three days during the boreal winter period, resulting in 20 days of fieldwork in each location. information registered for each focal bird included sex, foraging height, substrate type (green leaf, dead leaf, flower, branch, air), substrate side (upper or lower surface, apex, base, middle), horizontal position within the tree (inner, middle, outer), vertical position (canopy, subcanopy, understory), and foraging maneuvers following the classification suggested by remsen & robinson (1990). additionally, if the bird was attending a mixed species flock, composition and flock size were recorded. Foraging records were documented using a voice recorder. Foraging rate was estimated as the number of prey capture attempts per min.

Data analysis. We tested for sex-related differences in foraging rate and foraging height using analysis of variance. in addition, we used a χ2 test to discern preferences in the substrate type, substrate surface and strata and we applied linear relation to evaluate the

america (Hamel 2000) and occurs within a limited elevational range (~ 500–2000 m, robbins et al. 2002) that has been heavily modified to agricultural land use. The high rate of conversion of natural to agricultural landscape and the potential negative consequences for biological diversity, have led to an increase interest in evaluating the role of agroecosystems in the sustainability of natural populations and biodiversity (pimentel et al. 1992, thiollay 1995) and on their suitability as nonbreeding grounds for migrants. in particular, agroforestry ecosystems (e.g. shade coffee) have been widely suggested to have high conservation value by supporting higher levels of biodiversity compared to other agricultural habitats (petit & petit 2003, Komar 2006, Botero et al. 2010).

Some research has focused on avian diversity in coffee plantations in the neotropics (Wunderle & latta 1996, greenberg et al. 1997, petit et al. 1999), but the suitability of this agroforestry ecosystem as wintering grounds for migratory birds, including some species of conservation concern such as cerulean Warbler, is still a key issue in ecology and conservation. While interest in wintering grounds appears to be growing (Faaborg et al. 2010), different aspects of the ecology and habitat use of this species such as foraging ecology, that can help to assess habitat quality (lyons 2005) and focus conservation efforts (petit et al. 1995), is weakly documented (Strong 2000). in this paper, we describe the foraging ecology of cerulean Warbler in shade coffee plantations on the Western and central cordillera of the colombian andes. We also evaluate the social behavior and interspecific relationships of Setophaga cerulea that we have observed.

MetHoDS

Study area. We conducted foraging observations of Setophaga cerulea in shade coffee plantations

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degree of association between foraging rate and season and the group size effect. all analyses were conducted using SpSS version 19.0 (iBM company 2010). Data were checked for normality. Statistical tests were considered significant at P = 0.05, values reported are means ± Se.

reSUltS

individual-based foraging observations were collected on 75 birds of undetermined age, 46 males and 29 females. cerulean Warbler was an active foliage-gleaner. the primary foraging substrate was leaves (75%), followed by branches (17%) and flowers (3%). Individuals most often used green leaves (χ2 5 409.26 , df 5 1, P , 0.0005) compared with dead leaves. 77% of the foraging events of the cerulean Warbler occurred on the lower surface of the leaves (χ2

5 132.71, df 5 1, P , 0.0005), significantly more often than the upper surface (23%). 32% of the times birds were sighted feeding in the middle part

of the leaves’ surface (table 1). they usually foraged using non aerial maneuvers (87%) such as glean (80%) and hang (7%); aerial (13%) maneuver such as sally-hover (5%), sally-strike (3%), flush pursue (2%), tumble-chase (3%) and leap (0.1%) made up a smaller proportion of the foraging attempts. glean was the most common foraging maneuver for male (87% observations) and female (73%), but males used this maneuver more frequently than females (χ2

5 9.14, df 5 1, P , 0.01). However, the other maneuvers were used proportionally by both sexes (χ2

5 3.95, df 5 1, P . 0.1).

cerulean Warbler foraged most often in the subcanopy (χ2

5 15.37, df 5 1, P , 0.0005) and in the outer horizontal strata (χ2

5 39.56, df 5 1, P , 0.0005) of trees. the species was never observed foraging on coffee plants or feeding on the ground. Males and females differed in the mean foraging height (F 1,74 5 4.48, P 5 0.03) with females foraging at 7.2 6 0.71 (range 2.0–20.0 m) and males foraging higher at 10.5 6 0.92 (range 3.0–30.0 m).

Maneuver Frequency Males Females

aerial 51

leap 3 2 1

Sally-strike 22 19 3

Sally-hover 11 7 4

Flush-pursue 7 1

tumble-chase 9 7 2

not aerial 496

glean 466 433 33

Hang 30 26 4

taBle 1. Foraging maneuver used by cerulean Warbler.

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cerulean Warbler foraging rate was about 5.4 6 0.45 captures per minute. no differences between the sexes were observed in the mean foraging rate (F 1,74 5 1.42, P 5 0.23), nor in the vertical (χ2

5 0.37, df 5 1, P 5 0.83 ), or horizontal(χ2

5 0.001, df 5 1, P 5 0.97) strata used for foraging.

cerulean Warblers were mostly found in pairs or in small groups of 3–8 individuals (2 6 0.2 birds) often associated with mixed species flocks (97% of observations). Eighty resident and 27 migratory species participated in these flocks with an average number of 14 6 8 species (range 4-46). cerulean Warbler was the third most common neotropical migrant foraging in mixed species flocks in the study area (Table 2). Direct and indirect agonistic interactions (e.g. chases and fights) by Setophaga fusca (17 males and 7 females) and S. castanea (2 males and 4 females) on S. cerulea in flocks larger than 12 species were observed. in addition, foraging rate remained constant across group size (β 5

0.0024 6 0.0027, t 5 0.885, P . 0.05; Fig. 1). We also detected an increase in the foraging rate throughout the season (β 5 0.0279 6 0.0098, t 5 2.86, P , 0.01).

DiScUSSion

Migratory birds may experience dramatic seasonal shifts in habitat types and food resources as they move between breeding and wintering grounds. Despite the preference cerulean Warbler shows for undisturbed mature forest while on the breeding grounds (Hamel 2000, Weakland & Wood 2005) and for mature mesophytic forest in West Virginia and Kentucky (george 2009), second growth forest and coffee plantations have shown to be common habitats on the wintering grounds (perfecto et al. 1996, greenberg et al. 1997, Jones et al. 2000)

cerulean warbler was a relatively common migrant in coffee plantations across the study

TABLE 2. Common migrant species occurring in 104 mixed species bird flocks.

Participation in flocks

Species N %

Setophaga fusca 93 90

Oreothlypis peregrina 71 68

Setophaga cerulea 58 56

Piranga rubra 45 43

Mniotilta varia 45 43

Pheucticus ludovicianus 34 33

Cardellina canadensis 32 31

Empidonax virescens 28 27

Setophaga ruticilla 13 13

Vermivora chrysoptera 12 12

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area, primarily foraging in the forest subcanopy using the outer strata by gleaning insects from leaf surfaces as described for the same habitat in Venezuela during the non-breeding season (Jones et al. 2000, 2002, Bakermans et al. 2009, 2011). Moreover, our results are similar to those reported on the breeding grounds in terms of frequency of foraging maneuvers and absence of sex differences. For example, gleaning was the primary foraging maneuver observed in West Virginia, Kentucky and Venezuela (65–95% of all maneuvers), and birds used more non-aerial maneuvers, which tend to be energetically less expensive (remsen & robinson 1990) and decreases the exposition of the individual to predation. this consistent pattern in foraging ecology across the year may suggest a fairly limited repertory of foraging methods in cerulean Warblers, as reported for prothonotary Warbler (Protonotaria citrea) in north carolina (lyons 2005).

Mean foraging rate for the species was consistent with previous studies of foraging behavior of other warblers in the neotropics.

Detailed recent studies on foraging behavior of cerulean Warblers during the non-breeding (Jones et al. 2000, Bakermans et al. 2011) and the breeding season (george 2009) did not report data on foraging rate. american redstarts (Setophaga ruticilla) attacked prey at a mean rate of about 5 attacks/minute during summer in a mature forest in new Hampshire , and 3.2 attacks/min during winter in mangrove in Jamaica (lovette & Holmes 1995).

our data suggest that cerulean Warbler increases its food intake throughout the winter season evidenced by increasing its foraging rate. this is consistent with the improvement in body condition of this warbler throughout the non-breeding season documented by colorado (2011) in shaded agroecosystems in the same study area. conversely, lovette & Holmes (1995) documented a decrease in the foraging rate of american redstarts in the late winter, attributing it to a low prey availability due to a decrease in leaf canopy cover. although we did not measure any environmental variables, our study sites did

Fig. 1. Foraging rate (captures/min) of Setophaga cerulea participating in flocks of different size (species number) in coffee plantations in colombian andes.

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of neotropical migrants and can shed additional insights on their requirements and thus on their overall conservation needs. comparative studies of foraging ecology and habitat quality between mature and disturbed habitats for migrants in the non-breeding season are needed in order to assess the value of these managed landscapes for neotropical migrants. Measures using the survival rates of the birds themselves or a variety of proxies for survival such us resource availability through foraging rate and overwinter site persistence are needed in order to conduct effective conservation activities such as those described by Skolnik et al. (2012).

acKnoWleDgMentS

We want to express our gratitude to Santiago David and David ocampo for their support in the field stage of this project, as well as to the local community for allowing us to work in the area. We thank the nature conservancy and US Forest Service, Office of International programs, for financial support to conduct this research; the instituto de Biología, Universidad de antioquia. We thank p. Hamel and p. ramoni who provided insightful comments that improved our manuscript.

reFerenceS

Bakermans, M. H., a. c. Vitz, a. D. rodewald, & c. g. rengifo. 2009. Migratory songbird use of shade coffee in the Venezuelan andes with implications for conservation of cerulean Warbler. Biol. conserv. 142: 2476–2483.

Bakermans, M. J., a. D. rodewald, a. c. Vitz, & c. rengifo. 2011. Migratory bird use of shade coffee: The role of structural and floristic features. agrofor. Systs. 76: 1–10.

Beauchamp, g. 1998. the effects of group size on mean food intake rate in birds. Biol. rev. camb. phil. Soc. 73: 449–472.

Botero, J. e., a. M. lópez, r. espinoza, & c. casas. 2010. aves de zonas cafeteras del sur

not experience any substantial change in both climate conditions or vegetation cover throughout the study period as reported by lovette & Holmes (1995).

the foraging activities of cerulean Warblers were concentrated in the subcanopy of the shading trees with male and female segregated vertically. this may indicate dominance by sex. Similar results of habitat segregation were observed for the species in Venezuela by Bakermans et al. (2011). However, these results differ from those published by Jones et al. (2000) who described that males and females appeared to forage at similar heights. Further study is needed to determine whether these differences correspond to sex segregation or to a particular distribution of food items in this agroforestry system.

our data suggest cerulean Warblers are strongly social both intra- and interspecifically during the winter season, virtually always associated with mixed-species flocks of resident and migratory birds. our work does not provide evidence of an effect of group size on the foraging rate of the species. this pattern where foraging rate remained constant has been documented in studies that reported an increase in aggressive interactions with group size (Beauchamp, 1998). consistently, Cerulean Warblers had interspecific agonistic interactions with other migrants in larger flocks, in which the smaller Cerulean Warblers were attacked and typically displaced by the larger individuals of other species. thus our work suggests a possible negative effect of group size on the foraging of the species.

in addition, this research provides further evidence that coffee plantations are frequently used by migrants, including the globally vulnerable species cerulean Warbler. these agroforestry systems can regularly support the mixed-species bird flocks with which Cerulean Warbler associates.

Finally, our study shows that foraging behavior can provide insights into the ecology

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behavior of the cerulean Warbler in Venezuelan shade coffee plantations. condor 102: 958–962.

Jones, J., p. ramoni-perazzi, e. H. carruthers & r. J. robertson. 2002. Species composition of bird communities in shade coffee plantations in the Venezuelan andes. ornitol. neotrop. 13: 397–412.

Komar, o. 2006. priority contribution: ecology and conservation of birds in coffee plantations: a critical review. Bird conserv. intern. 16: 1-23.

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Lyons, J. E. 2005. Habitat-specific foraging of prothonotary Warblers: deducing habitat quality. condor 107: 41–49.

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perfecto, i., r. a. rice, r. greenberg, & M. e. VanderVoort. 1996. Shade coffee: a disappearing refuge for biodiversity. BioScience 46: 598–608.

petit, D. r., J. e lynch, r. l. Hutto, J. g. Blake, & r. B. Waide. 1995. Habitat use and conservation in the neotropics. pp.145–197 in Martin t. e. & D. M. Finch (eds). ecology and management of neotropical migratory birds: a synthesis and rewiew of critical issues. oxford Univ. press, new York, USa.

petit, l. J., D. r. petit, D. g. christian, & H. D. W. powell. 1999. Bird communities of natural and modified habitats in Panama. Ecography 22: 292–304.

petit, l. J. & D. r. petit. 2003. evaluating the importance of human-modified lands for neotropical bird conservation. conserv. Biol. 17: 687–694.

del Huila. Federación nacional de cafeteros de colombia – cenicafé, caldas, colombia. Disponible en http://www.cafesanisidro.com/site/librodeaves.pDF

Buehler, D. a., J. J. giocomo, J. Jones, p. B. Hamel, c. M. rogers, t. a. Beachy, D. W. Varble, c. p. nicholson, K. l. roth, J. Barg, r. J. robertson, J. r. robb, & K. islam. 2008. cerulean Warbler reproduction, survival, and models of population decline. J. Wildl. Manag. 72: 646–653.

colorado, g. J. 2011. ecology and conservation of neotropical-nearctic migratory birds and mixed-species flocks in the Andes. Ph.D. diss. Ohio State Univ., columbus, ohio, USa. available at http://etd.ohiolink.edu/send-pdf.cgi/colorado%20gabriel%20J.pdf?osu1291646331/ [accessed 25 January 2012]

Faaborg, J., r. t. Holmes, a. D. anders, K. l. Bildstein, K. M. Duggers, S. a. gauthreaux, p. Heglund, K. a. Hobson, a. e. Jahn, D. H. Johnson, S. c. latta, D. J. levey, p. p. Marra, c. l. Merkord, e. nol, S. i. rothstein, t. W. Sherry, t. S. Sillett, F. r. thompson, & n. Warnock. 2010. recent advances in understanding migration systems of new World land birds. ecol. Monogr. 80: 3–48.

greenberg, r., p. Bichier, a. cruz, & r. reitsma. 1997. Bird populations in shade and sun coffee plantations in central guatemala. conserv. Biol. 11: 448–459.

greenberg, r., p. Bichier, a. cruz-angon, & r. reitsma. 1997. Bird populations in shade and sun coffee plantations in central guatemala. conserv. Biol. 11: 448–459.

george, g. a. 2009. Foraging ecology of male cerulean Warblers and other neotropical migrants. ph.D. diss., West Virginia Univ., Morgantown, West Virginia, USa.

Hamel, p. B. 2000. cerulean Warbler (Dendroica cerulea). In poole, a., & F. gill (eds). the Birds of north america, no. 511. the birds of north america, inc., philadelphia, pennsylvania, USa.

Jones, J., p. ramoni-perazzi, e. H. carruthers, & r. J. robertson. 2000. Sociality and foraging

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Skolnik, B., D. Wiedenfeld, r. Dettmers, c. aucca, l. Daza, H. Valle, F. Sornoza, J. robayo, D. Diaz, J. Fitzgerald, D. lebbin, & p. B. Hamel. 2012. conservation planning and accomplishments for protection of cerulean Warbler (Setophaga cerulea) nonbreeding habitat. ornitol. neotrop. 23(Suppl.): 319–329.

Strong, a. M. 2000. Divergent foraging strategies of two neotropical migrant warblers: implication for winter habitat use. auk 117: 381–392.

thiollay, J. M. 1995. the role of traditional agroforests in the conservation of rain forest bird diversity in Sumatra. conserv. Biol. 9: 335–353.

Weakland, c. a., & p. B. Wood. 2005. cerulean warbler (Dendroica cerulea) microhabitat and landscape-level habitat characteristics in southern West Virginia. auk 122: 497–508.

Wunderle, J. M., & S. c. latta. 1996. avian abundances in sun and shade coffee plantations and remnant pine forest in the cordillera central, Dominican republic. ornitol. neotrop. 17: 19–34.

pimentel, D., e. Stachow, D. a. takacs, H. W. Brubaker, a. r. Dumas, J. J. Meaney, J. S. o’neil, D. e. onsi, & D. B. corzilius. 1992. conserving biological diversity in agricultural forestry systems. BioScience 42: 354–362.

remsen, J. V., Jr., & S. K. robinson. 1990. a classification scheme for foraging behavior of birds in terrestrial habitats. Stud. avian Biol. 13: 144–160.

robbins, c. S., J. W. Fitzpatrick, & p. B. Hamel. 1992. a warbler in trouble: Dendroica cerulea. pp. 549–562 in Hagan iii, J. M., & D. W. Johnston (eds). ecology and conservation of neotropical Migrant landbirds. Smithsonian institution press, Washington, D.c., USa.

Sherry, t. W., M. D. Johnson, & a. M. Strong. 2005. Does winter food limit populations of migratory birds? .pp. 414–425. in greenberg, r., & p. p. Marra (eds). Birds of two worlds: the ecology and evolution of migration. Johns Hopkins Univ. press, Baltimore, Maryland, USa.

Sherry, t. W. 2000. Shade coffee: a good brew even in small doses. the auk 117: 563–568.

phamel
Sticky Note
Ms. Munoz received the outstanding student presentation award at the Congress for the presentation of this paper.
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ornitologia neotropical 23: 367–378, 2012© the neotropical ornithological Society

PASSING THE BATON Of ACTION fROM RESEARCH TO CONSERVATION IMPLEMENTATION fOR CERULEAN WARBLER

(sEtOphAGA CErulEA)

Paul B. Hamel1, David Mehlman2, Sebastian Herzog3, Kenneth V. Rosenberg4,

& Jason Jones5

1US Forest Service, Center for Bottomland Hardwoods Research, P. O. Box 227, 432 Stoneville Rd., Stoneville, MS 38776 USA, E-mail: [email protected]

2The Nature Conservancy, Migratory Bird Program, 212 E. Marcy St., Suite 200, Santa Fe, NM 87501 USA

3Asociación Civil Armonía, Av. Lomas de Arena # 400 “Barrio Palmira”, (Zona Palmasola), Santa Cruz, BOLIVIA

4Cornell Lab of Ornithology, 159 Sapsucker Woods Rd., Ithaca, NY 14850 USA

5Tetra Tech, Inc., 800 - 555 West Hastings Street, Vancouver, BC V6B 1M1 CANADA

Resumen. – Pasando el bastón de mando desde investigación a implementación conservacionista para la Reinita Cerúlea (setophaga cerulea). – Cuando El Grupo Cerúleo fue creado en el año 2002, la tarea de dilucidar la distribución no reproductiva, ecología y comportamiento de la Reinita Cerúlea (Setoph-aga cerulea) era enorme, nuestro entendimiento de los requerimientos de hábitat limitados, el temor fun-dado a la existencia de poco hábitat de buena calidad y las redes de socios de conservación dentro de Latino América y entre el Norte, Centro y Sudamérica eran pocas y distantes entre sí. Nuestros continuos esfuerzos por identificar y cultivar redes de socios en los numerosos países por los cuales pasa la Reinita Cerúlea, ha resultado en la generación de nuevo conocimiento acerca de la especie en sus territorios no reproductivos. El tiempo también ha llegado, a la luz de este conocimiento, para extender el trabajo del grupo desde un enfoque centrado en la investigación y adquisición de conocimiento a uno dirigido principalmente al manejo y restauración del hábitat y el desarrollo de estrategias de protección. El desarrollo e implement-ación de un programa de monitoreo que evalúe el éxito de las estrategias de conservación implementadas es esencial. Este programa debe también cumplir las muchas otras necesidades de propietarios de tierra y administradores. Dado el estado actual de la tenencia de tierra y las restricciones de recursos en materia de conservación en la mayor parte de América Latina, este cambio de enfoque representa un mayor énfasis en la educación, el alcance a y el diálogo con los administradores de la tierra y comunidades productoras de materia prima básica, quienes realmente impactan el hábitat en la mayor parte del ámbito geográfico. Además, el compromiso y participación continua de los consumidores de productos, muchos de los cuales pueden vivir lejos de los productores, será esencial para incrementar la disponibilidad de recursos destina-dos a conservación. La ampliación del énfasis hacia la implementación y educación requiere de la aplicación de un conjunto de habilidades diferentes a los que se requirieron durante las actividades iniciales de inves-tigación. Nuestro resumen de las contribuciones del simposio y de los logros y deficiencias del Grupo desde el año 2002 esboza una visión de un futuro seguro y sostenible para las poblaciones de la Reinita Cerúlea.

Abstract. – When El Grupo Cerúleo, a sub-committee of the Cerulean Warbler Technical Group, was formed in 2002, the task of elucidating the nonbreeding distribution, ecology and behavior of the Cerulean Warbler (Setophaga cerulea) was large, our understanding of habitat needs was limited, there was fear that little suitable habitat existed, and conservation partnerships within Latin America and between North, South, and Middle America were few and far between. Our continuing efforts have led to a network of partners in the numerous countries through which the species passes or spends up to 7-8 months in winter and a new

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(Universal Studios 2011), bolsters this potential, at least for activities in which north americans are engaged. in 2001 the cerulean Warbler technical group (cWtg) was formed to coordinate collaborative research and conservation related to this species.

Under guidance from the U.S. Fish and Wildlife Service Focal Species program, the cWtg collectively developed a rangewide conservation action plan for the cerulean Warbler (U.S. Fish and Wildlife Service 2007). More recently, a framework conservation plan for the cerulean Warbler during the nonbreeding season has been produced and distributed (Fundación proaves et al. 2010). our collective efforts have produced strategically important policy assistance to the U.S. Fish and Wildlife Service (U.S. Fish and Wildlife Service 2002, 2006a, 2006b), to iUcn in status determination of the species (Birdlife international 2008), and to land managers. throughout this process, the cWtg has served as a model for a cooperative, science-based, and non-regulatory approach to conservation that has been emulated by groups focused on other potential flagship species, such as golden-winged Warbler (Vermivora chrysoptera), Bicknell’s thrush (Catharus bicknelli), and rusty Blackbird (Euphagus carolinus).

introDUction

Declining population trends of cerulean Warbler (Setophaga cerulea) on its north american breeding grounds (Sauer et al. 2011) have sparked intense research and conservation action as well as considerable public policy attention (Hamel et al. 2004, U.S. Fish and Wildlife Service 2006a, Dawson et al. 2012). coordinated management, conservation, monitoring, and research activities throughout the species’ extensive range are believed to be important to its future persistence (U.S. Fish and Wildlife Service 2007, Fundación proaves et al. 2010). this iUcn-listed Vulnerable bird (Birdlife international 2008) is a potential flagship species (Bowen-Jones & Entwhistle 2002, clucas et al. 2008) for conservation of a diverse breeding avifauna in the appalachian and central Hardwood ecoregions of eastern north america, as well as for the extremely diverse neotropical resident and nearctic migratory birds of the northern andes in Venezuela, colombia, ecuador, peru, and Bolivia. popularity of cerulean Warbler with the North American public, reflected in a recent novel (Franzen 2010), memoir (Fallon 2011), and children’s television program

body of knowledge about the Cerulean Warbler on its nonbreeding range. The time has come, in light of this knowledge, to shift the focus of the group from research and information gathering to one primarily directed to habitat protection, management, and restoration. Developing a monitoring program that measures suc-cess of implemented conservation strategies and adaptively informs, as well as fits the constraints of land owners and managers, is essential. Given the current status of land ownership and resources available for conservation in most of Latin America, this change in focus means an increased emphasis on education of, outreach to, and dialogue with commodity-producing industries and communities who have responsibility for most land management across the species’ geographic range. Furthermore, increased engagement and participation of commodity consumers, many of whom live far away from the producers, will be essential to generate additional resources for conservation. The extension of emphasis to implementation and educa-tion requires application of different skill-sets than the initial research activities required. Our summary of symposium contributions and the achievements and shortcomings of the Cerulean Warbler Technical Group, in particular those of El Grupo Cerúleo since 2002, outlines a vision for a sustainable and secure future for Cerulean Warbler populations.

Key words: Cerulean Warbler, Dendroica cerulea, Setophaga cerulea, implementing research agenda, con-servation planning, local conservation action, international partnerships, coordinating agendas, integration of biodiversity with economic activity, trade-offs

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the 2011 symposium “Biología de la conservación de la reinita cerúlea, una especie migratoria vulnerable que depende de tierras cultivadas para café, carbón y productos forestales” (libro de resúmenes, IX Congreso de Ornitología Neotropical, cusco, perú, nov 2011) reviewed the structure, progress, and accomplishments of the cWtg, particularly those of the nonbreeding season subcommittee, el grupo cerúleo, over the period 2001-2011. one of the explicit goals of the symposium and associated meetings among cWtg members was to build on the conservation plan for the non-breeding range, outline the next steps for nonbreeding-season conservation, and re-energize a network of partners dedicated to conserving species and ecosystems in the northern andes. in this paper, we summarize work of the CWTG and the main findings presented at the 2011 symposium, and reflect on the next research and conservations steps for this iconic species.

aDVancing UnDerStanDing oF tHe SpecieS

activities of the cWtg conducted since its formation in 2001 (Hamel et al. 2004, Dawson et al. 2012) demonstrate the capacity of a focused group of collaborators to address and fill vital gaps in our understanding of this species, and to clear up numerous biological misunderstandings. in 2002, the cWtg organized into four subcommittees devoted to Breeding Season research, Breeding Season Monitoring, Breeding Season conservation, and nonbreeding Season issues, to facilitate development of reliable information that would support effective conservation action relevant to the full life-cycle of the birds. Subcommittee assignments reflect the limits of knowledge at the time cWtg formed, namely gaps in biological knowledge, and in methods to estimate population size and to produce

or enhance habitats for the species. the vital public education function was assigned to each subcommittee. Because knowledge of nonbreeding biology and distribution was particularly limited, el grupo cerúleo was assigned the challenge and opportunity of addressing all nonbreeding season concerns (Dawson et al. 2012).

contributions to the symposium indicate the immense progress that has been achieved in each of these areas of cWtg activity. in each area, the limits of activities outline needs for the future.

Breeding Season Research. larkin et al. (2012) present the highlights of the extensive forest management experiment carried out in the core of the breeding range directed to understanding cerulean Warbler population biology and the response of the species to a range of intensities of forest management. the research demonstrated a clear positive response by the birds to an intermediate intensity of forest harvest. How that response is reflected in demographic parameters of the species suggests that management strategies may need to vary across the landscape depending upon abundance and population trends of local populations (larkin et al. 2012, cf. Boves 2011). islam et al. (2012) describe a similar manipulative experiment of forest management in a more peripheral area of the range, in which territorial males responded positively to even-aged management and negatively to uneven-aged management; nesting success was similar among the treatments in that study. curley et al. (2012) document basic distributional and habitat features of the species in a location in new Jersey where the population is expanding. Density of territorial males there was generally lower than in the core of the range, and tree species composition of territories reflected discrimination by the birds for some tree species and against others.

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Breeding Season Monitoring. activities of the cWtg supplemented the comprehensive cerulean Warbler atlas project (rosenberg et al. 2000), and together with the ongoing analyses of the Breeding Bird Survey data set (Sauer et al. 2011) offer a regular estimate of the distribution, size, and trend of the breeding population. these activities are models for potential future counterparts in the nonbreeding grounds. although no paper in the symposium dealt strictly with breeding season monitoring activities, efforts are underway to develop a sampling design and protocol to carry out long-term trend monitoring at a finer scale than possible with the Breeding Bird Survey. in addition, it may be advisable to carry out a second cerulean Warbler atlas, to provide a new “snapshot” of the status of key sites and populations identified during the 1990s.

Breeding Season Conservation. results of the forest management experiment and increased knowledge of the locations of breeding concentrations of the species, particularly in regard to appalachian coal deposits (Buehler et al. 2006), set the stage for important opportunities for conservation and integrated management of cerulean Warblers in association with extraction of both renewable and nonrenewable resources. Smith et al. (2012) summarize the progress and opportunities in this important arena. collaboration with other conservation entities, such as the appalachian regional reforestation initiative (arri), will bear fruit in rehabilitated habitats for the species in the future (Smith et al. 2012). the model of cooperation with arri may be applicable to nonbreeding season conservation in the andes, and certainly offers opportunity for interaction between people in both parts of the species’ range (patrick n. angel, pers. comm.). recognition that cerulean Warblers depend on lands rich in coal deposits for breeding habitats (Buehler et al. 2006) and lands vital to the production of coffee (Coffea

arabica) in the nonbreeding range (Sánchez-clavijo et al. 2008, 2009, Bakermans et al. 2009) have led to linkages with other cooperative land management and conservation initiatives (Smith et al. 2012, Skolnik et al. 2012).

Nonbreeding Season Issues. Five contributions to the symposium deal directly with nonbreeding season biology and conservation of cerulean Warbler. Welton et al. (2012) are the first to report results from a systematic, hypothesis-driven survey of the species’ distribution and ecology during migration periods. Muñoz & colorado (2012) address foraging and behavioral ecology of the birds in colombia during the nonbreeding period, including interspecific interactions with other migratory species, interactions which cerulean Warblers routinely lose. colorado et al. (2012) summarize preliminary results of a rigorous field validation (Colorado et al. 2008, colorado 2011) of a nonbreeding season model of cerulean Warbler distribution in the andes. the model was developed by Barker et al. (2006) through a series of workshops organized by el grupo cerúleo members. While reinforcing some previous ideas about the geographic distribution of the species, colorado et al. (2012) extend our understanding of the nonbreeding habitats and elevational range of the cerulean Warbler in the andes, thereby suggesting some conservation activities. the workshops resulting in Barker et al. (2006) also contributed to development of the nonbreeding conservation plan (Fundación proaves et al. 2010). contributions to the symposium by Santander et al. (2012) and Skolnik et al. (2012) reflect expanded interest in conservation in South america.

paSSing tHe Baton oF action

these successes suggest that the time has arrived to shift from a focus driven primarily by research needs to one emphasizing

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conservation implementation in which research supports and evaluates conservation action as well as develops and clarifies biological theory. each cWtg function— biological research, population monitoring, conservation action and evaluation, and capacity building and public awareness— requires individuals with specific and frequently non-overlapping expertise and inclinations. We believe that our experience in passing through this transition will be useful to others engaged in integrating biological research into meaningful conservation action in multiple countries.

the hallmark of our approach to these activities, and probable key to the success achieved in the last ten years, is the conscious commitment of members of cWtg to work in concert with each other. two useful principles of engagement include admonitions to: (a) leave individual and institutional agendas outside the room and (b) draw circles to include, that is, include all relevant perspectives in the conversation. Both of these principles recognize that for each participant in a discussion related to this or other species, individual knowledge has limits and is conditioned by the experience of the individual, the policy and business climate of the institution for which they work, and the general attitude of the institutional sector.

Members of the cWtg won three awards for their collaborative efforts during the period 2001-2011. in 2007, el grupo cerúleo was recognized with a Wings across the americas international cooperation award from the U.S. Forest Service for the cerulean Warbler nonbreeding Habitat assessment (Barker et al. 2006). the award recognized 41 individuals representing almost as many institutions in Bolivia, canada, colombia, ecuador, peru, United States, and Venezuela. in 2008, el grupo cerúleo was awarded the U.S. Forest Service Southern research Station Director’s global Stewardship award, again recognizing the partnership efforts of individuals from

the seven principal countries in the species’ breeding and nonbreeding ranges. in 2011, the first U.S. Presidential Migratory Bird Federal Stewardship award recognized the contribution of the Office of Surface Mining of the U.S. Department of the interior for the work of the arri, including its contribution to the future conservation of the cerulean Warbler.

Five members of el grupo cerúleo, representing colombia, ecuador, peru, and United States, were involved in the planning of the 2011 symposium. Fifty-two different people from these countries, as well as Bolivia and canada, contributed to at least one paper in the symposium representing the breadth of effort expended by cWtg members to produce high quality technical information about the species (Hamel et al. 2004). these achievements are especially noteworthy given the great difficulty of studying this species in the field.

linking research accomplishments to conservation implementation through a process that includes monitoring feedback is a vital unmet need. in this context, the differing approaches of research biologists, conservation implementers, and mobilizers of public awareness may collide in less than useful ways. We anticipate that maintaining a collective balance between potentially competing interests will be difficult but worth the effort to maintain. another challenge in collaborative efforts is the inevitable tension between individual success and collective achievement, in which collective work toward common goals yields a greater degree of ultimate achievement than does emphasis on personal gain. to date, combined efforts of individual members of the cWtg have yielded both personal success illustrated by the abundant literature on the species developed over the decade, and collective achievement of new insights possible only through collaboration of teams of investigators (e.g.,

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Breeding Season Questions

• What are the economic implications of implementing silvicultural treatments that enhance cerulean Warbler habitat at various spatial and temporal scales?

• Assuming management guidelines are established, what level of implementation would be required to result in region-wide or range-wide population increases?

• What are the longer-term responses of cerulean Warblers to forest-management treatments, especially in regard to adult and juvenile survival, male vs. female response, nest predation and other causes of nest failure, and to changes in lepidopteran and other food resources?

• What are recommended best management practices for cerulean Warbler breeding habitat rangewide?

Migratory Season Questions

• What are the seasonal dynamics of use by Cerulean Warblers at identified migration stopover sites (will require continuous monitoring of specific sites)?

• Can we refine a migration stopover model with additional surveys and monitoring?

• What are the key threats and conservation opportunities at identified migration stopover sites?

• Where are critical stopover sites for cerulean Warblers that migrate directly across the gulf of Mexico or caribbean?

Nonbreeding Residency Season Questions

• What are the relative contributions of different measurable factors to the survival of cerulean Warblers during the nonbreeding period? are any of these limiting? is the combination itself limiting?

• What is the relative importance of native forest vs agroforestry landscapes

Jones et al. 2007, Buehler et al. 2008, larkin et al. 2012).

WHAT ARE THE NEXT RESEARCH StepS For tHe cWtg to taKe?

Dawson et al. (2012) describe succinctly the cWtg’s coordinated, interconnected and comprehensive approach to develop technical information about cerulean Warblers needed to address the species’ conservation needs. We have learned an impressive amount of new information about cerulean Warbler biology, demography, distribution, population status, management, and natural history that can be used to formulate and focus conservation actions, assess a much wider array of questions, and connect information about a single species to more general topics in biology and conservation practice.

However, the limits of our knowledge are extensive as well. Breeding season studies of demography and response to experimental forest management have still not led to tested and demonstrated best management practices. Validation of the nonbreeding distribution model of Barker et al. (2006), by colorado et al. (2008, 2012) and colorado (2011), represent only a beginning, although a solid one, to understanding the species’ nonbreeding distribution and habitat requirements. For example, recent sightings of cerulean Warbler in Bolivia (tobias & Seddon 2007, Q. Vidoz, pers. comm.) and southern perú (www.eBird.org) suggest that vast areas within the wintering distribution remain very poorly known.

cerulean Warbler remains a species notoriously difficult to study, for which high effort is required to achieve small sample sizes, few publishable results, and limited dependable knowledge to support conservation action. collaborative efforts, demonstrated to be possible by the cWtg forest management research project (larkin et al. 2012), may be the only way to further gains. Many important questions remain, among them the following:

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understanding population dynamics and trajectories. Dispersal and productivity also are elements of key ecological theories such as those regarding metapopulation dynamics (Hanski 1998). linking information gaps for cerulean Warbler to current debates about ecological theory should broaden interest in the species as a research subject and increase funding opportunities from traditional science venues for students and established researchers.

2. Conservation questions can be better answered through data sharing networks that maximize return on financial and field time investment. Many incoming graduate students face the challenge of not only developing research ideas but developing a network of knowledge and colleagues that provide the foundation for a successful research effort. groups like the cWtg can be a tremendous resource for individuals and organizations trying to break into a field and for facilitating large-scale research projects. the cWtg could moderate and provide a code of conduct for collaborative data-sharing among graduate students and other researchers at different institutions, and could serve as a repository of information. published data could be made available to facilitate meta-analyses or other wide ranging efforts (e.g., Buehler et al. 2008). the network could also house natural history observations that may be only a curiosity when viewed as an n of 1 (e.g., conspecific egg destruction; Boves et al. 2011) but whose value increases as similar observations are made in other locations (e.g., nest material kleptoparasitism; Jones et al. 2007). an internet communication listserve has been developed for those interested in cerulean Warblers (Brian Smith, pers. comm.).

throughout the species’ nonbreeding range? Does individual survivorship differ in these landscapes, and among the habitats that comprise them? Does differential survivorship of sexes exist in different habitats?

• Are anthropogenic habitats adequate to support healthy populations of cerulean Warblers into the future?

• How does our understanding of connectivity between breeding and nonbreeding seasons for different portions of the population inform our understanding of the relative importance of Venezuelan and colombian habitats vs those in perú and Bolivia?

• How can we strengthen our understanding of cerulean Warbler migratory connectivity that links specific breeding populations to specific wintering sites, thus enhancing the potential for linkages between conservation actions on the breeding and nonbreeding grounds?

• Is Cerulean Warbler vulnerable to interspecific interactions in mixed-species flocks during the nonbreeding period? Is the presence of mixed-species flocks a limiting factor for cerulean Warbler distribution and survival?

addressing these questions will require significant efforts. How can we motivate research interest in this high effort – low reward species? We offer two examples.

1. Filling information gaps hindering Cerulean Warbler conservation and management will provide useful contributions to important ecological theories. on the breeding grounds, two obvious conservation-related information gaps are (a) dispersal (adult, natal, post-fledging) and (b) factors limiting productivity. Dispersal must be understood in order to create and manage breeding habitat and habitat connectivity. information about factors limiting productivity is a critical piece of

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would benefit from the successful application of research-driven management practices.

WHAT ARE THE NEXT conSerVation StepS For tHe cWtg to taKe?

We believe there are several important questions that the cWtg should consider.

• Can conservation activities on the nonbreeding grounds affect enough habitat in the near term, perhaps the next ten years, to increase survivorship of the cerulean Warbler population by 5% annually?

• Can conservation activities on the breeding and nonbreeding grounds improve habitat conditions sufficiently for an increase of 5% in population abundance in the next ten years?

• Can research and monitoring provide sufficiently precise evaluation data on conservation projects to answer the above questions?

next steps for cerulean Warbler conservation on the nonbreeding grounds involve turning the existing conservation plan (Fundación proaves et al. 2010) into an action plan that can guide implementation. in Bogotá and San Vicente de chucurí, colombia, in 2008, cWtg established a strong connection with the colombian coffee industry and made substantial initial progress toward a “best management practices” approach to conservation of cerulean Warblers in the context in coffee production. However, due to recent downturns in the colombian coffee industry and in the global economy, this connection appears to have weakened and it may be appropriate to re-evaluate the emphasis on it in the conservation plan. For example, a shift in emphasis from management of coffee landscapes to management of watersheds may offer a way to restructure this focus. once an

a stellar example of this kind of opportunity is the cWtg forest management study detailed by larkin et al. (2012). a potential research collaboration on dispersal is another example of how this network could operate. Similar approaches to the study of differential body condition and its effect on survival, as well as nonbreeding habitat distribution, can be described. the study of adult and natal dispersal for a species with a broad geographic range requires the collection of data over a large spatial area and multiple years. the two published studies that have examined cerulean Warbler dispersal (Veit et al. 2005, girvan et al. 2007) were only successful through intense collaboration and support from a wide range of people. Both studies would have benefited greatly from the existence of a communication and data sharing network. Such an active network would facilitate identification of individuals with (a) similar interests and (b) the ability to collect useful ancillary data. For example, if three students based in three geographic regions (e.g., illinois, West Virginia, tennessee) were all interested in dispersal of cerulean Warblers as a thesis topic and all three knew that each other existed, it should be a relatively simple exercise to establish a research program that would allow each to have a stand-alone project while contributing data to the other two projects. not only can the study of dispersal be divided by dispersal type (e.g., adult, natal, post-fledging), it can be divided by quantification technique (e.g., isotopes, genetics, radio telemetry, mark- recapture/re-sight) and by the research context (e.g., managed versus unmanaged forest landscapes). The individual students would benefit from reduced research costs and increased sample sizes; the research community would benefit from robust sampling designs and the development of multiple lines of evidence; the conservation community would benefit from having access to robust data upon which to make management decisions; and the species

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successful collaborative conservation that is worthy of imitation elsewhere such as in the coffee producing regions of the nonbreeding range. Future conservation efforts need to maintain as high priority both the intended conservation outcomes and the activities and needs of local communities (e.g., Santander et al. 2012, Skolnik et al. 2012, Smith et al. 2012). For example, outreach to children is essential to implementation and long-term success of conservation projects.

For cerulean Warbler, it is critical to maintain both forest on appalachian ridges underlain by substantial coal deposits and agroforestry land uses on andean slopes suitable for production of coffee. those coal deposits and coffee resources also represent vital natural resources for humans. in each locale, the livelihood of the local population and of all those involved in the associated value chains depends upon the production, harvest, and export of those natural resources. investors and consumers worldwide also benefit from coal and coffee production. Future viability of the cerulean Warbler depends upon the balance between these needs. activities coordinated through the cerulean Warbler technical group demonstrate the opportunities, difficulties, frustrations, failures, and remarkable successes made possible by collaborative partnerships. as such, the biology of the bird, and the working of the conservation partnership surrounding it, are a model for other international and interdisciplinary partnerships. the challenges that lie ahead for the cWtg are daunting, and much work remains.

acKnoWleDgMentS

We are especially grateful to tom Will for important help to our thinking about this paper. all of us owe a debt to Dave Buehler for insisting that leadership develop in understanding biology of cerulean Warbler.

action plan is developed, cWtg and partners can move forward with carrying out the actions, using on-going research and monitoring in an adaptive way to assess their effect on demographic parameters such as survivorship and population size and then to refine them as necessary. conservation hotspots will need to be identified and confirmed, likely through the use of occupancy-based modelling (e.g., colorado et al. 2012), to focus conservation actions where they are likely to be most effective. coordinating international partners and adapting conservation approaches to fit conditions in different countries and regions will require considerable skill and understanding of the needs of individual partners. appropriate to this will be to develop innovative ways to recognize the important contributions of different entities (governmental, nongovernmental, commercial, and individual) to the conservation effort (Skolnik et al. 2012). evaluation of success of intended conservation actions will require partners to refine and expand existing survey and monitoring projects and use them as models to replicate in other locales, both on the wintering grounds and at migration stopover sites.

Smith et al. (2012) reinforce these notions by emphasizing the importance of developing conservation strategies applicable at multiple spatial and temporal scales that can deliver, through flexible partnerships, current, high-quality scientific information to those whose activities are likely to affect cerulean Warblers. critically important in this respect are both the sustainable extraction of natural resources (e.g., timber, coal) within the cerulean Warbler’s range and the continued economic viability of the rural communities, value chains, and investors reliant on those resources. conservation will be most successful if local communities, corporations, conservation entities, and governments are engaged in the work. the arri is an excellent example of

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This manuscript benefitted from the kind attention of t. Bently Wigley, Deanna Dawson, and paolo ramoni-perazzi. they, as well as all of the authors of this paper, and Kamal islam, Jeff larkin, Kim Smith, Scott Stoleson, tito Vilella, tom Will, and petra Bohall Wood served the important role of peer reviewers for papers in this symposium. esteban guevara and tatiana Santander kindly translated our abstract into a proper resumen for us, as well as those of most of the remaining papers in the symposium. We are grateful to carl Smith for assistance with technical editing of this and other contributions to the symposium. Jack clinton eitniear has extended numerous courtesies during the preparation of the manuscripts. the efforts of so many members of el grupo cerúleo and the cerulean Warbler technical group demonstrate that there is no end to what we can accomplish when we work together.

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