Articles

DISCOVERY OF TWO NEW LOCALITIESFOR TODD’S PARAKEET PYRRHURA PICTA CAERULEICEPS

USING DISTRIBUTION MODELS:ENHANCING KNOWLEDGE OFA LITTLE KNOWN

NEOTROPICAL BIRD

HALLAZGO DE DOS NUEVAS LOCALIDADESPARA EL PERIQUITO DE TODD PYRRHURA PICTA CAERULEICEPS

EMPLEANDO MODELOS DE DISTRIBUCIÓN GEOGRÁFICA:INCREMENTANDO EL CONOCIMIENTO DE UNAVE TROPICAL

POCO CONOCIDA

Esteban BOTERO-DELGADILLO1 *, Carlos Andrés PÁEZ1

and Jeyson SANABRIA-MEJÍA1

SUMMARY.—Todd’s parakeet Pyrrhura picta caeruleiceps is a geographically isolated race of paintedparakeet P. picta, a widespread species. Several authors highlight the need to recognize Todd’s parakeetat the species level, and despite past efforts to find new populations, no new locations have been found.We applied a Species Distribution Model (SDM) to guide a 30-day survey during 2011 to increaseinformation on its geographic distribution. Surveys resulted in the discovery of two new populations inLos Motilones Mountains, on the north-eastern boundary of Colombia withVenezuela. Our field surveyssupport previous arguments of a continuous geographic range from the northern part of the EasternCordillera to the Perijá Mountains. However, we did not find birds at the base of the Colombian slope ofthe Perijá Mountains, and confirming its absence there requires further study. Habitat loss at the threelocalities visited was high, with most remaining habitat represented by continuous gallery forests locatedon steep and humid slopes at higher altitudes. If conditions for population maintenance are only presentin those patches, it will be necessary to identify forest fragments that help maintain connectivity betweenpopulations on the northernmost part of the Eastern Cordillera and the Perijá Mountains. More surveysin the Perijá Mountains and in Venezuela are also recommended. This study provides further evidence ofthe usefulness of species distribution models to increase available information on rare or little known taxa.Key words: Colombia, field surveys, habitat loss, Los Motilones Mountains, probability of presence,

painted parakeet, Perijá Mountains.

Ardeola 59(2), 2012, 237-252

1 Selva: Investigación para la conservación en el Neotrópico, C/ 43 27A-55 Of. 201,Bogotá, Colombia.

* Corresponding author: esteban.botero@selva.org.co

INTRODUCTION

Todd’s parakeet Pyrrhura picta caerulei-ceps is one of the nine or so geographic racesof the painted parakeet Pyrrhura picta(Collar, 1997; but see Remsen et al., 2012),a species whose taxonomic affinities havejust started to be resolved (Joseph, 2000;Joseph, 2002; Joseph and Stockwell, 2002;Ribas et al., 2006). Recent works havesupported the recognition of three of its sub-species at the species level (see Remsen et al.,2012), but there is still debate on the needto recognize the remaining races (Joseph andStockwell, 2002; Arndt, 2008; see also Rem-sen et al., 2012), including the apparentlyallopatric Todd’s parakeet, sinú parakeet P. p.subandina and azuero parakeet P. p. einsen-manni (see Forshaw, 2010).The painted parakeet is considered as a

species of least concern (LC) for conserva-tion (BirdLife International, 2012), becausedespite its isolated and restricted distributionin northern Colombia and southern Panama,its range includes a vast area east of theAndes

(Ecuador, Peru, Bolivia, Brazil, Venezuelaand the Guianas) (Collar, 1997). Due tothis, little attention has been given to someof its restricted-range subspecies (Botero-Delgadillo and Páez, 2011a; 2011b). This isthe case for Todd’s parakeet, which seems tobe distributed only in the northernmost partof the eastern Andes of Colombia, and in LosMotilones and Perijá Mountains along theboundary between Colombia and Venezuela(Collar, 1997; Forshaw, 2010; Botero-Del-gadillo and Páez, 2011b). This subspecieshas lost ca. 70% of its original habitat withinits Colombian distribution, and its area ofoccupancy within Colombia is predicted tobe less than 3,700 km2 (Botero-Delgadillo etal., 2012). Given the extensive transforma-tion of native forests throughout its range, andits presumed geographic isolation from otherraces ofP. picta (Joseph and Stockwell, 2002;Botero-Delgadillo et al., 2012), this taxonshould be considered a priority followingIUCN criteria (see IUCN, 2011).Unfortunately, our knowledge of Todd’s

parakeet is poor and there have been few

Ardeola 59(2), 2012, 237-252

BOTERO-DELGADILLO, E., PÁEZ, C. A. and SANABRIA-MEJÍA, J.238

RESUMEN.—El periquito de Todd Pyrrhura picta caeruleiceps es una raza geográficamente aisladadel periquito pintado P. picta, una especie de amplia distribución. Varios autores han resaltado la nece-sidad de reconocer al periquito de Todd como especie, y pese a los esfuerzos para encontrar nuevaspoblaciones, no se ha encontrado una nueva localidad recientemente. En este estudio se usó un modelode distribución geográfica para guiar un muestreo de 30 días en 2011 que incrementase la informaciónsobre su distribución. Fruto de ello fue el descubrimiento de dos poblaciones en la serranía de Los Mo-tilones, en el límite nororiental de Colombia con Venezuela. Los muestreos apoyan previos argumentossobre la continuidad de su rango geográfico desde el norte de la Cordillera Oriental hasta la Serraníadel Perijá. No obstante, no encontramos esta ave en la vertiente colombiana del Perijá, por lo que con-firmar su ausencia allá será clave. Observamos una alta pérdida de su hábitat en las tres localidades vi-sitadas, encontrando que la mayoría del hábitat remanente estuvo representado por bosques de galeríacontinuos en pendientes elevadas y húmedas a mayores elevaciones. En el caso de que las condicionespropicias para el mantenimiento de sus poblaciones se encuentren en estos bosques, será necesario iden-tificar fragmentos que mantengan la conectividad de las poblaciones desde la Cordillera Oriental hastael Perijá. Se requiere más estudio en la Serranía del Perijá y Venezuela. Este trabajo provee evidenciaadicional de la utilidad de los modelos de distribución geográfica para aumentar la información sobretaxones poco conocidos.Palabras clave: Colombia, estudios de campo, pérdida de hábitat, periquito pintado, probabilidad de

presencia, Serranía de Los Motilones, Serranía del Perijá.

efforts to gather ecological or distributionalinformation since field surveys conducted byTodd (1947) and Phelps (1977) to describeP. subandina caeruleiceps and P. pictapantchkenkoi respectively. These latter twosubspecies are no longer considered validand both are treated as Todd’s parakeet P. p.caeruleiceps (Joseph and Stockwell, 2002;Arndt, 2008; Forshaw, 2010; Remsen et al.,2012). Recently, Fundación ProAves carried

out a series of expeditions that confirmed thepersistence of two populations in the typelocality of Todd’s parakeet and nearby areas(Tovar-Martínez, 2010; Botero-Delgadilloand Páez, 2011b) but failed to find this taxonin new areas where it might be present. Thiswas in spite of considerable effort beingexerted through more than 20 field expedi-tions during more than six months (C. A.Páez, unpub. data).

Ardeola 59(2), 2012, 237-252

TODD’S PARAKEET AND DISTRIBUTION MODELS 239

FIG. 1.—Geographic range covered by historical records of Todd’s parakeet in Colombia andVenezuela.[Distribución geográfica de registros históricos del periquito de Todd en Colombia y Venezuela.]

Considering that knowledge on geographicdistribution is essential to accurately evaluateany taxon’s conservation priorities (Pimmand Jenkins, 2010), this study aimed to pro-vide new ecological and distributional in-formation on Todd’s parakeet, an isolatedtaxon requiring effective conservation actions(Botero-Delgadillo and Páez, 2011a; 2011b).To achieve this, we used a Species Distribu-tion Model (SDM) to develop an efficient andless time consuming method for identifyingnew presence localities, and subsequentlymake a preliminary assessment of the currentstatus of populations and habitat availabilityat new localities.

METHODS

Populations under study

We have used all historical records forTodd’s parakeet for our analyses, includingrecords listed as either P. subandina caerulei-ceps or P. picta pantchkenkoi (see above).Eleven of the records used were distributed onthe northern portion of the Eastern Cordillerawithin the Norte de Santander department inColombia ). Seven records were located alongthe Los Motilones or the Perijá Mountains,three of them within the Cesar department inColombia and the remaining four within theZulia state in Venezuela (fig. 1).

Data collection and cleaning

Geographical records were obtained frompublic databases including Project BioMap(http://www.biomap.net/), DATAves (2006)and eBird (http://ebird.org/content/colombia),and also from the literature (Phelps, 1977;Paynter and Traylor, 1981; Joseph and Stock-well, 2002; Rodríguez-Mahecha and Hernán-dez-Camacho, 2002; Tovar-Martínez, 2010)and unpublished records (see acknowledge-

ments). We followed Chapman (2005) fordata cleaning and selection using DIVA-GIS(Hijmans et al., 2006). Three localities wereremoved due to their spatial proximity (e.g.located within 1 km of each other). All re-maining localities were used since there wereno environmental outliers among them; allrecords fell inside the 95.0 percentile in fivecumulative frequency curves of five climaticvariables (annual mean temperature, isother-mality, annual precipitation, temperatureannual range and precipitation seasonality).Therefore, we used 15 records from the origi-nal dataset for subsequent modelling.

Potential distribution modelling

Considering its good performance com-pared with other methods of climatic nicheprediction (Elith et al., 2006; Ortega-Huer-ta and Peterson, 2008), especially with re-duced sample sizes (Pearson et al., 2007), weused the MaxEnt algorithm for distributionmodelling (Phillips, 2010). We employedthe 15 geographical records and 15 variablesfrom the 19 bioclimatic variables of theWorldClim database at 1 km2 resolution(http://www.worldclim.org/) as input data.Bioclimatic variable selection was madefollowing Graham et al. (2010), leaving outvariables with redundant information suchas isothermality, temperature seasonality,temperature annual range and precipitationseasonality. Detailed information on selectedvariables and their annual mean and rangevalues for the region comprised by the 15 lo-calities are summarized in table 1.Given the limited dataset, we selected a

regularization constant equal to 1.0 in MaxEntand linear and quadratic features for trans-formation of the environment variables toavoid model overfitting (Phillips et al., 2006;Phillips and Dudik, 2008; Elith et al., 2011).We used a 10,000 sample point background,and the model extent was restricted to eleva-

Ardeola 59(2), 2012, 237-252

BOTERO-DELGADILLO, E., PÁEZ, C. A. and SANABRIA-MEJÍA, J.240

tions above 100 m in Andean ranges fromPeru to Colombia-Venezuela. We chose thelogistic model output to represent distribu-tions, given that it shows the taxon’s proba-bility of occurrence within each 1 km2 gridwith a value ranging from 0 to 1.Since resampling techniques have been

recommended when modelling distributionswith limited samples (Peterson et al., 2007),we selected the bootstrap option included inMaxEnt to evaluate the uncertainty around themodel’s performance (Dormann, 2007; Elithet al., 2011). Thus, the mean value of the area

under the Receiving Operative Characteris-tic curve (from now on AUC) for trainingdata from bootstrap replicates was taken as ameasure of our model’s performance and itsuncertainty was assessed through the AUC’sstandard deviation. To test model fit in rela-tion to presence data, we used the meanvalues for the regularized training gain andthe test gain (Phillips et al., 2006; Phillipsand Dudik, 2008). Although there was noextreme climatic variability among records(i.e. there were no climatic outliers), oursmall dataset could have caused high varia-

Ardeola 59(2), 2012, 237-252

TODD’S PARAKEET AND DISTRIBUTION MODELS 241

TABLE 1

Bioclimatic variables selected for modelling the potential distribution of Todd’s parakeet and theirannual mean and range values along the region comprised by the 15 historical records used.[Variables bioclimáticas seleccionadas para modelar la distribución potencial del periquito de Toddy sus valores medios anuales y rangos en la región con los 15 registros históricos utilizados.]

Bioclimatic variable Annual mean value (annual range)

Annual mean temp.* 22.3 (16.1-26.7)

Mean monthly temp. Range* 10.5 (10.3-10.9)

Annual precipitation** 1682 (1446-2391)

Precip. of wettest month** 307 (236-379)

Precip. of driest month** 31 (18-45)

Precip. of driest quarter** 139 (92-187)

Precip. of wettest quarter** 808 (618-998)

Precip. of warmest quarter** 603 (432-660)

Precip. of coldest quarter** 267 (168-565)

Mean temp. of coldest quarter* 20.1 (15.1-26.2)

Mean temp. of warmest quarter* 23.5 (16.6-27.1)

Mean temp. of wettest quarter* 22.6 (16.2-26.9)

Mean temp. of driest quarter* 20.9 (15.4-26.4)

Max. temp. of warmest month* 27.4 (22.1-32.8)

* Temperature in °C. Min.: minimum; Max.: maximum.** Precipitation values in mm.

bility in predicted areas among model repli-cates and an overprediction of the taxon’spresence around areas with close presencelocalities (Botero-Delgadillo, unpub. data).To avoid this, we ran 1,000 bootstrap repli-cates to stabilize the standard deviations ofthe models’ entropy and prevalence (see Elithet al., 2011 for details on these concepts),meaning that variability in the predicted areaand probability of occurrence within each1 km2 grid among all runs was low.We there-fore selected the mean value of all replicatesas a consensus model to represent the Todd’sparakeet potential distribution.

Field surveys and population counts

The logistic model output in ASCII formatwas imported into ArcGIS 9.3 (ESRI, 2008)to obtain a predicted area with occurrenceprobability grids at 1 km2 resolution. In orderto select potential field survey areas, we ini-tially discarded all cells with probability values< 0.6, and subsequently we pre-selected onlyzones with probability values ≥ 0.8 (see fig. 2).Since most records within Colombia come

from the northern portion of the EasternCordillera in the Norte de Santander depart-ment (fig. 1), the focus of this study was to

Ardeola 59(2), 2012, 237-252

BOTERO-DELGADILLO, E., PÁEZ, C. A. and SANABRIA-MEJÍA, J.242

FIG. 2.—Potential distribution model for Todd’s parakeet using the MaxEnt algorithm.A. Predicted areaof occurrence with respective probability of occurrence values. B. Detail of the study area includinghistorical records, municipalities, survey areas and model probability values. See the text for details onlocations of study sites.[Modelo de distribución potencial del periquito de Todd utilizando el algoritmo MaxEnt. A. Área pre-dicha de presencia con los respectivos valores de probabilidad de presencia. B. Detalle del área deestudio que incluye registros históricos, municipalidades, áreas de estudio y modelo con valores de pro-babilidad. Véase el texto para detalles de localización de los sitios de estudio.]

Ardeola 59(2), 2012, 237-252

TODD’S PARAKEET AND DISTRIBUTION MODELS 243

FIG. 3.—Areas surveyed for Todd’s parakeet in Los Motilones and Perijá Mountains in Colombia.A. Spatial locations of study sites with respect to altitude and proximity to towns/municipalities andto some of the taxon’s historical records. Ordered from south to north study sites were: Chiriguaná,Becerril and Manaure. B. An adult perched on a snag at Chiriguaná. C. Two birds feeding in a guavatree Psidium guajava at Becerril.[Áreas de estudio del periquito de Todd en las serranías de Los Motilones y del Perijá, Colombia.A. Localización espacial de los sitios de estudio en relación a la altitud y proximidad a pueblos/muni-cipalidades y a alguno de los registros históricos del taxón. Ordenados de sur a norte los sitios de es-tudio fueron: Chiriguaná, Becerril y Manaure. B. Adulto posado en una vara en Chiriguaná. C. Dosadultos alimentándose en un guayabo Psidium guajava en Becerril.]

confirm the subspecies occurrence along theLos Motilones and Perijá Mountains withinthe Cesar department (fig. 2). For logisti-cal limitations, we took into account onlysites with relative proximity to towns amongall areas with high presence probabilities,favouring those located between 2 and 20 kmaway from any municipality (fig. 3). To en-sure that any bird encountered correspondsto a new presence locality, a final requirementfor survey site selection was a minimum dis-tance of 20 km from known records of Todd’sparakeet (figure 3).Once all expedition sites were chosen

and referenced geographically (see Results),we conducted surveys in July, August andOctober 2011 during 10 days/month from06:30-12:30 h and 14:30-17:30 h. Becauseof topographical and logistical difficulties ateach site, we were not able to define the exten-sion and shape of any of the surveyed areas apriori. However, a minimum required area wasfixed on 5 km2, and the maximum area coveredvaried depending on topography at each site,but in all cases searches were carried out atelevations between 400 to 2,200 m based onthe taxon’s known altitudinal range (Botero-Delgadillo and Páez, 2011b). If birds weredetected, we stayed 10 more days to make afirst approximation of population status usingvantage point counts (see Wunderle, 1994).One count per day for 10 days was madefrom 06:00 to 08:00 h. Because this methodcannot be used to estimate detection proba-bilities (see Bibby et al., 2000), we couldonly estimate an interval for the populationsize at each locality. The intervals’ lowerlimit was set as the largest group observedon any one day while the higher limit wasconsidered as the maximum number of indi-viduals counted during any day. To avoidcounting the same individuals more thanonce, two to three observers at differentpoints gathered information simultaneouslyon the timing, flock size and flight directionof all detected groups (Wunderle, 1994).

Habitat assessment

Our habitat characterizations are expectedto represent a preliminary assessment ofhabitat suitability at survey localities and as away to explain potential presences/absences,but they do not intend to be a definitive answerto any of the patterns observed.We used a GPS at all study sites to delimi-

tate the area surveyed for further GIS analy-ses. Using ArcGIS 9.3, we combined studyarea polygons with 2008 Landsat derivedgeographic layers of land-use and ecosys-tems compiled in a public-access portal of theLand-use Planning Geographic InformationSystem (SIG-OT in Spanish) of the “AgustínCodazzi” Geographic Institute of Colombia(http://sigotn.igac.gov.co/sigotn/). This wasdonemainly for estimating the percentage lossof original cover and the area of remainingvegetation within each surveyed area. There-after, we determined the area of remainingforests plus secondary forests, early succes-sional areas and forestry plantations as a mea-sure of the potential habitat for the taxon,considering the available information onhabitat use for Todd’s parakeet and otherPyrrhura parakeets (Rodríguez-Mahechaand Hernández-Camacho, 2002; Botero-Del-gadillo and Páez, 2011b).In order to compare habitat availability

between areas where we found Todd’s para-keet and those where not, we estimated the ex-tension of all habitats present within each siteand compared ratios of available/unavailableareas. A ratio < 1 indicated that transformedareas were the dominant cover. These esti-mates were accompanied by in situ descrip-tions of human-derived landscape transforma-tion as an indirect verification of our analyses.Finally, we calculated the distance to hu-

man settlements around all study areas andthe proximity of settlements to forest rem-nants to infer potential pressures derived fromhuman activities at all sites. This was alsodone using ArcGIS 9.3.

Ardeola 59(2), 2012, 237-252

BOTERO-DELGADILLO, E., PÁEZ, C. A. and SANABRIA-MEJÍA, J.244

RESULTS

Modelling results

Our model performed well accordingto the mean AUC values for training data(0.98 ± 0.007), and the standard deviationaround the mean suggested that uncertain-ty surrounding the model’s performancewas low. Standard deviations around themean values of entropy (6.46 ± 0.3) andprevalence (0.03 ± 0.01) were also low,and tended to show the same values (i.e.stabilize) around the 600-700 replicates. Themean values of the regularized training gain(2.83 ± 0.35) and the test gain (3.63 ± 0.54)indicated that the consensus model fitted wellaround the presence data. However, the areaswith the highest probability of occurrencewere widespread along the Los Motilonesand Perijá Mountains and thus were not con-centrated on the localities used for modellingor their nearby areas (fig. 2).In general, the consensus model predicted

the species to occur between 500 and 2,200m.a.s.l. on both sides of the Perijá Moun-

tains, Los Motilones Mountains and smallportions of the northernmost part of theEastern Cordillera (fig. 2). The species’ cli-matic niche (i.e. potential distribution) waspredicted to cover ca. 8,000 km2.

Field surveys

Three localities were chosen for field sur-veys based on the criteria described above(see Methods): site number 1 was locatedwithin the Chiriguaná municipality at thebase of Los Motilones Mountains (we referto this site as Chiriguaná hereafter). Thiswas the southernmost site and was located17.8 km southeast of the La Jagua de Ibirico;site number 2 was within the boundariesof the Becerril municipality (from hereonBecerril), located 18.8 km southeast fromAgustín Codazzi; site number 3 was thenorthernmost location, situated at 3.4 kmeast of the Manaure municipality in thePerijá Mountains (hereon Manaure; figures2 and 3). Details on study areas and searchefforts are explained in table 2.

Ardeola 59(2), 2012, 237-252

TODD’S PARAKEET AND DISTRIBUTION MODELS 245

TABLE 2

Study sites and respective search effort for Todd’s parakeet during 2011 in Los Motilones and PerijáMountains, north-eastern Colombia.[Sitios de estudio del periquito de Todd y área muestreada en cada uno de ellos durante 2011 en las se-rranías de Los Motilones y del Perijá, noreste de Colombia.]

Study area Altitudinal range SurveyStudy site Coordinates (km2) (m.a.s.l.)* period**

Chiriguaná 9° 24’ 7’’ N, 73° 19’ 22’’W 4.7 513-1230 July 2011

Becerril 9° 53’ 19’’ N, 73° 8’42’’W 8.1 400-1760 August 2011

Manaure 10° 23’ 56’’ N, 72° 59’ 36’’W 9.1 698-2810 October 2011

* m.a.s.l.: meters above sea level.** Surveys lasted between 10 to 20 days depending upon whether parakeets were encountered (see Methods).

We found populations of Todd’s parakeetat Chiriguaná and Becerril (fig. 3). The newsite at Chiriguaná was located ca. 32 kmnortheast from a recent record near theCurumaní municipality and ca. 41 km south-west of the only historical record in LosMotilones Mountains at Hiroca (fig. 3). Thesite at Becerril was located ca. 21 km southfrom Hiroca, Colombia, and 17 km east fromFrontera in Venezuela, the type locality ofP. p. pantchkenkoi (fig. 3). We failed to findthe bird at Manaure, located at 39.6 km westfrom Las Lajas, where the most recent recordof Todd’s parakeet in Venezuela occurred.

Population counts

Forty-three records of Todd’s parakeet wereobtained during 10-day counts at Chiriguaná,mostly consisting of flocks of between 3 and10 birds (84% cumulative frequency), flying0-10 m above the forest canopy (81% ofobservations). Thirty-six observations weremade at Becerril, where in most cases flocks

contained 3-9 birds (88% cumulative frequen-cy), and again, almost all birds were flying0-10 m above the canopy (83%).According tothe largest flocks observed and the maximumnumber of birds counted at both localities,populations would number between 90 and121 individuals at Chiriguaná and between31 and 65 individuals at Becerril.

Habitat assessment

We found that the original vegetationcover (i.e. primary forest) had been com-pletely transformed within both study areaswhere Todd’s parakeet was recorded, whileit represented 27.6% (2.7 km2) of the totalarea at Manaure (fig. 4). However, when con-sidering primary forest plus secondary forestsand other types of secondary vegetation, wefound that potential habitat for Todd’s para-keet covered similar areas at the three sites,but being slightly less at Manaure (table 3,fig. 4). This similarity among sites was also re-flected in the estimation of the ratio of availa-

Ardeola 59(2), 2012, 237-252

BOTERO-DELGADILLO, E., PÁEZ, C. A. and SANABRIA-MEJÍA, J.246

TABLE 3

Habitat assessment values for the three study sites where searches for Todd’s parakeet were carried outduring 2011 in Los Motilones and Perijá Mountains, north-eastern Colombia.[Valoración del hábitat en tres sitios de estudio donde se efectuaron búsquedas del periquito de Todddurante 2011 en las serranías de Los Motilones y del Perijá, noreste de Colombia.]

Primary/ Remaining Secondary Potential Cattle Annualgallery habitat* vegetation habitat** pastures crops Availability

Study site forests (km2) (km2) (km2) (km2) (km2) (km2) ratio***

Chiriguaná 0 0 3.1 (66.3%) 3.1 (66.3%) 1.5 (33.5%) 0.009 (0.2%) 1.9

Becerril 0 0 4.5 (55.2%) 4.5 (55.2%) 3.6 (44.7%) 0 1.2

Manaure+ 2.1 (21.4%) 2.1 (21.4%) 2.5 (26.3%) 4.6 (47.7%) 5.1 (52.3%) 0 0.9

* Remaining habitat was taken as primary or gallery forest remnants.** Estimated as remaining habitat + secondary vegetation (including secondary forests).*** Estimated as potential habitat/cattle pastures + annual crops.

+ Todd’s parakeet was not recorded at Manaure.

Ardeola 59(2), 2012, 237-252

TODD’S PARAKEET AND DISTRIBUTION MODELS 247

FIG. 4.—Habitat transformation at the three survey sites for Todd’s parakeet in north-eastern Colombia.A. Vegetation cover within and around Chiriguaná. B. Forest burning and clearance at Chiriguaná.C. Vegetation cover within and around Becerril. D. Forest remnants at higher elevations at Becerril.E. Vegetation cover within and around Manaure. F. Detailed legend.[Transformación del hábitat en tres sitios de estudio del periquito de Todd en el noreste de Colombia.A. Cobertura de la vegetación en y alrededor de Chiriguaná. B. Incendio y aclarado de bosque en Chiri-guaná. C. Cobertura de la vegetación en y alrededor de Becerril. D. Remanentes del bosque a altitudeselevadas en Becerril. E. Cobertura de la vegetación en y alrededor de Manaure. F. Leyenda detallada.]

ble/unavailable sites, although Chiriguanáexhibited a higher value compared with Be-cerril and Manaure (table 3).The dominant vegetation cover at Chirigua-

ná was composed of fragments of secondaryforests and shrubby vegetation, separatedmainly by cattle pastures (table 3, fig. 4). AtBecerril, most areas were also covered bysecondary vegetation, but bordered by exten-sive pastures to the north (table 3) and withprimary forest fragments to the south (fig. 4).At Manaure, cattle pastures and savannasdominated the study site (table 3), which werealso extensively distributed throughout LosMotilones Mountains despite the presence ofprimary forest remnants (fig. 4).Logging and forest clearance to create

cattle pastures appeared to be the most im-portant pressures on Todd’s parakeet habitatat Chiriguaná and Becerril (fig. 4B), and mostforest fragments were separated by cattlepastures or transitional crops. At both locali-ties, it was evident that pressures leading todeforestation decreased at higher elevations,where continuous remnants of primary forestpersisted (figure 4D), only reaching loweraltitudes on steep slopes along watersheds.Despite this configuration of habitats, Todd’sparakeet were most frequently observed nearopen areas in gallery forests or forest rem-nants associated with steep slopes far fromhuman habitation.Although human settlements were located

8-10 km from the secondary forests surveyedboth at Chiriguaná and Becerril (fig. 4), wefound more than 10 farms distributed through-out both sites. In the case of Manaure, threemain towns were located between 1.7-5 kmfrom the study site, all associated with exten-sive (> 18 km2 each) zones for cattle nearby.

DISCUSSION

The use of Species Distribution Models(SDM) to identify potential areas for studying

rare species and to prioritize the conservationneeds of threatened taxa has increased re-cently (e.g. Elith and Leathwick, 2009; Freileet al., 2010). Here, we used SDM to designa 30-day survey during 2011 to increase in-formation on the geographic range of Todd’sparakeet, a little known and presumablythreatened subspecies of the painted parakeet(Botero-Delgadillo et al., 2012). Using thisapproach, we were able to discover two newlocalities for the taxon in the Los MotilonesMountains, a mountain massif where therewas only one 50 year old record from Hiroca(see Paynter and Traylor, 1981).Our model appeared to represent the cli-

matic and geographical distribution of thisparakeet well, since all historical records wereincluded within the predicted occupancy area,and both the variability of entropy and preva-lence and the uncertainty of model fit werelow. Field surveys confirmed that populationsof this bird persist in Los Motilones Moun-tains, and supports previous arguments, basedalso on distribution models, suggesting a con-tinuity in geographic range from the northernpart of the Eastern Cordillera to the PerijáMountains (Botero-Delgadillo and Páez,2011b; Botero-Delgadillo et al., 2012).The absence of Todd’s parakeet at Manau-

re during our surveys may be explained by avariety of different reasons and we will brieflymention some of them. First, we cannotdiscard the possibility that birds were tem-porarily absent while making latitudinal oraltitudinal migrations in search for food, sincesuch local movements are common amongAndean parrots and are presumed to occur inPyrrhura parakeets (Collar, 1997; Rodríguez-Mahecha and Hernández-Camacho, 2002;Botero-Delgadillo and Páez, 2011b). Second,it is possible that the population there couldbe smaller or harder to detect than in other lo-calities, thus rendering a 10-day search effortinsufficient to confirm its presence. Third, wemay not have recorded the parakeet simplybecause its populations were extirpated from

Ardeola 59(2), 2012, 237-252

BOTERO-DELGADILLO, E., PÁEZ, C. A. and SANABRIA-MEJÍA, J.248

Manaure and neighboring areas. Althoughfurther survey effort and habitat assessment isrequired, current evidence suggests that habi-tat degradation in the entire region surround-ing Manaure has been more severe comparedthan in nearby regions (Botero-Delgadilloand Páez, 2011b). In fact, this entire regionis dominated by cattle pastures, semi-perma-nent crops and opencast mining operations(Botero-Delgadillo and Páez, 2011b); wetherefore consider it unlikely that popula-tions inhabiting extensive primary forestsremnants around Las Lajas in Venezuela(fig. 3) could be also present on the Colom-bian side of the Perijá Mountains. Whateverthe case, further study at wider spatial andtemporal scales will be necessary to confirmits presence/absence in the Perijá range.Despite the fact that our criteria for survey

site selection were intended to ensure thatany record corresponded to a new presencelocality, it is open to discussion as to whetherbirds at Chiriguaná and Becerril can be con-sidered recently discovered populations ofTodd’s parakeet or whether they relate to thesame population. Parrots are extremely mo-bile birds with high dispersal capability, ableto fly several kilometers in a day regardless ofthe landscape configuration (Collar, 1997;Rodríguez-Mahecha and Hernández-Cama-cho, 2002). However, Pyrrhura parakeetsusually fly very close to the forest canopy(Collar, 1997; Gilardi and Munn, 1998) andseem to be sensitive to forest fragmentation(Botero-Delgadillo and Páez, 2011b). Ashas been suggested for other Andean speciesof Pyrrhura, our observations indicatethat Todd’s parakeet can cross small openareas (Botero-Delgadillo and Verhelst, 2011;Botero-Delgadillo and Páez, 2011b), butapparently depend on a continuous canopyfor movements at a landscape level (i.e. morethan 20 km). Further study is needed toconfirm if the dispersal capacity of Pyrrhurais reduced when forests have been severelytransformed. Based on current evidence, we

believe that birds at Chiriguaná and Becerrilrepresent different populations. We also be-lieve that the Chiriguaná population couldbe the same previously reported at Fronterain Venezuela, since only 12 km separatesboth areas and forests on both sides of LosMotilones remain connected (Botero-Del-gadillo, unpub. data).Our surveys suggest that proximity to hu-

man settlements or even farms is perhaps themain threat at Chiriguaná and Becerril. Asidefrom deforestation, human presence exertsother pressures upon Todd’s parakeet popula-tions, mainly capture for the pet trade. Somelocal people at both sites value this bird as apet, as has been reported from other localities(see Tovar-Martínez, 2010), and fledglingsare typically taken from cavity nests and sub-sequently raised before being sold (Tovar-Martínez, 2010; Botero-Delgadillo and Páez,2011b). This situation could become criti-cal since only 20% of the Todd’s parakeetknown range is covered by protected areas inColombia (Botero-Delgadillo et al., 2012).Increasing representation of the Todd’s para-keet range within protected areas on theColombian side of Los Motilones and PerijáMountains is critical, especially to ensureconnectivity among primary forest remnantsat higher elevations.

Concluding remarks

Here we provide additional evidence onthe potential usefulness of SDM to fill infor-mation gaps on rare or little known taxa.When interpreted cautiously, models basedon climatic niche and occurrence probabilitiescan help design less time-consuming andmoreeffective surveys, especially when logistic fa-cilities or resources are limited. We encourageresearchers to apply this valuable tool ifappropriate geographical data are available.Considering that most of the Todd’s

parakeet remaining habitat in Los Motilones

Ardeola 59(2), 2012, 237-252

TODD’S PARAKEET AND DISTRIBUTION MODELS 249

Mountains is represented by continuousgallery forests located on steep and humidslopes at higher elevations, it is possible thatconditions allowing for population growth(or at least maintenance) could be presentin those patches. If so, it will be necessaryto identify currently unprotected forest frag-ments that serve to maintain connectivitybetween populations distributed from thenorthernmost part of the Eastern Cordillera tothe Perijá Mountains (if they remain there).Future studies should focus on confirming

presence in other areas suggested by ourmodel, such as the Colombian slope of thePerijá Mountains, and the junction of theMerida Andes and the Eastern Cordillera(Botero-Delgadillo and Páez, 2011b).Evaluating our entire model in Colombia andVenezuela is also a priority research need.

ACKNOWLEDGEMENTS.—We thank Fonds fürbedrohte Papageien and Strunden PapageienStiftung for funding this work, and to René Wüstfor his advice and ideas for the entire project. Weespecially want to thank Miguel Lentino and JuanPablo López for sharing helpful information.Miguel Mejía, Pedro Pablo Contreras, DanielRodríguez and RamiroÁlvarez provided valuablehelp during field surveys. Nicholas Bayly, SandraEscudero and Camila Gómez made thoroughcomments on an earlier version of this manu-script. Two anonymous reviewers made valuablecomments that helped improve the manuscript.

BIBLIOGRAPHY

ARNDT, T. 2008.Anmerkungen zu einigen Pyrrhu-ra- formen mit der beschreibung einer neuenart und zweier neuer unterarten. Papageien, 8:278-286.

BIBBY, C. J., BURGESS, N. D., HILL, D. A. andMUSTOE, S. H. 2000. Bird Census Techniques.2nd ed. Academic Press. London.

BIRDLIFE INTERNATIONAL. 2012. Species factsheet:Pyrrhura viridicata. Downloaded fromhttp://www.birdlife.org on 02/01/2012.

BOTERO-DELGADILLO, E. and PÁEZ, C. A. 2011b.Plan de acción para la conservación de los lorosamenazados de Colombia 2010-2020: avances,logros y perspectivas. Conservación Colombia-na, 14: 7-16.

BOTERO-DELGADILLO, E. and PÁEZ, C. A. 2011b.Estado actual del conocimiento y conservaciónde los loros amenazados de Colombia. Conser-vación Colombiana, 14: 86-151.

BOTERO-DELGADILLO, E. and VERHESLT, J. C. 2011.Uso de hábitat del Periquito de Santa Marta(Pyrrhura viridicata) y sus variaciones espacio-temporales en la Sierra Nevada de Santa Marta.Conservación Colombiana, 14: 17-27.

BOTERO-DELGADILLO, E., PÁEZ, C. A. and BAYLY,N. 2012. Biogeography and conservationof Andean and Trans-Andean populations ofPyrrhura parakeets in Colombia: Modellinggeographic distributions to identify independentconservation units. Bird Conservation Interna-tional.

CHAPMAN, A. D. 2005. Principles of data quality.ver. 1.0. Report of the Global Biodiversity In-formation Facility. Global Biodiversity Infor-mation Facility. Copenhagen.

COLLAR, N. J. 1997. Family Psittacidae (Parrots).In, J. del Hoyo, A. Elliott and J. Sargatal (Eds.):Handbook of the birds of the world, volume 4:Sandgrouse to Cuckoos, pp. 280-477. Lynx Edi-cions. Barcelona.

DATAVES. 2006. Base de datos de la Red Nacio-nal de Observadores de Aves, cedida por la So-ciedad Antioqueña de Ornitología, modificadaal RRBB. Instituto de investigación de recursosbiológicos Alexander von Humboldt. Bogotá.

DORMANN, C. F. 2007. Promising the future?Global change projections of species distribu-tions. Basic and Applied Ecology, 8: 387-397.

ELITH, J., GRAHAM, C. H., ANDERSON, R. P.,DUDIK, M., FERRIER, S., GUISAN, A., HIJMANS,R. J., HUETTMANN, F., LEATHWICK, J., LEHMANN,A., LI, J., LOHMANN, L. G., LIOSELLE, B. A.,MANION, G., MORITZ, C., NAKAMURA, M.,NAKAZAWA, Y., OVERTON, J. M., PETERSON,A. T., PHILLIPS, S. J., RICHARDSON, K., SCA-CHETTIPEREIRA, R., SCHAPIRE, R. E., SOBERÓN,J., WILLIAMS, S., WISZ, M. S. and ZIMMERMANN,N. E. 2006. Novel methods improve predictionof species’ distributions from occurrence data.Ecography, 29: 129-151.

Ardeola 59(2), 2012, 237-252

BOTERO-DELGADILLO, E., PÁEZ, C. A. and SANABRIA-MEJÍA, J.250

ELITH, J. and LEATHWICK, J. R. 2009. The con-tribution of species distribution modelling toconservation prioritization. In, A. Moilanen, K.A. Wilson and H. P. Possingham (Eds.): Spa-tial conservation prioritization: Quantitativemethods & computational tools, pp. 70-93.Oxford University Press. Oxford.

ELITH, J., PHILLIPS, S. J., HASTIE, T., DUDÍK, M.,CHEE, Y. E. and YATES, C. J. 2011. A statisticalexplanation of MaxEnt for ecologists.Diversityand Distributions, 17: 43-57.

ESRI 2008. ArcGIS, version 9.3 for Windows.Environmental Systems Research Institute.Redlands. California.

FORSHAW, J. M. 2010. Parrots of the world. Prince-ton University Press. Princeton.

FREILE, J. F., PARRA, J. L. andGRAHAMN,C.H. 2010.Distribution and conservation of Grallaria andGrallaricula antpittas (Grallariidae) in Ecuador.Bird Conservation International, 20: 410-431.

GILARDI, J. D. and MUNN, C. A. 1998. Patterns ofactivity, flocking, and habitat use in the Peru-vian Amazon. The Condor, 100: 641-653.

GRAHAM, C. H., SILVA, N. andVELÁSQUEZ-TIBATÁ,J. 2010. Evaluating the potential causes of rangelimits of birds of the ColombianAndes. Journalof Biogeography, 37: 1863-1875.

HIJMANS, R. J., CRUZ, M. E. and GUARINO, L.2006. DIVA–GIS. ver. 5.4. Downloaded fromhttp://www.diva–gis.org/.

IUCN. 2011. Guidelines for using the IUCN RedList categories and criteria. ver. 9.0. IUCN Stan-dards and petitions subcommittee. Downloadedfrom http://www.iucnredlist.org/documents/RedListGuidelines.pdf on 15/12/2011.

JOSEPH, L. 2000. Beginning an end to 63 years ofuncertainity: The Neotropical parakeets knownas Pyrrhura picta and P. leucotis comprise morethan two species. Proceedings of the Academy ofNatural Sciences of Philadelphia, 150: 279-292.

JOSEPH, L. 2002. Geographical variation,taxonomy and distribution of some AmazonianPyrrhura parakeets. Ornitología Neotropical,13: 337-363.

JOSEPH, L. and STOCKWELL, D. 2002. Climaticmodeling of the distribution of some Pyrrhuraparakeets of Northwestern South America withnotes on their systematics and special referenceto Pyrrhura caeruleiceps Todd, 1947. Orni-tología Neotropical, 13: 1-8.

ORTEGA-HUERTA, M. and PETERSON, A. T. 2008.Modeling ecological niches and predicting geo-graphic distributions: a test of five methods. Re-vista Mexicana de Biodiversidad, 79: 205-216.

PAYNTER, JR., R. A. and TRAYLOR, JR. M. A. 1981.Ornithological gazetteer of Colombia. Museumof Comparative Zoology. Cambridge. Massa-chusetts.

PEARSON, R. G., RAXWORTHY, C. J., NAKAMURA,M. and PETERSON,A. T. 2007. Predicting speciesdistributions from small numbers of occur-rence records: a test case using cryptic geckosin Madagascar. Journal of Biogeography, 34:102-117.

PETERSON, A. T., PAPEŞ, M. and EATON, M. 2007.Transferability and model evaluation in eco-logical niche modeling: a comparison of GARPand MAXENT. Ecography, 30: 550-560.

PHELPS, JR.,W. H. 1977. Una nueva especie y dosnuevas subspecies de aves (Psittacidae, Fur-nariidae) de la Sierra de Perijá cerca de la di-visoria Colombo-Venezolana. Boletín de laSociedad Venezolana de Ciencias Naturales,134: 43-53.

PHILLIPS, S. J. 2010. Maxent software for specieshabitat modeling. ver. 3.3.3. Downloadedfrom http://www.cs.princeton.edu/~schapire/maxent/>.

PHILLIPS, S. J. ANDERSON, R. P. and SCHAPIRE, R.E. 2006. Maximum entropy modeling of speciesgeographic distributions. Ecological Modelling,190: 231-259.

PHILLIPS, S. J. and DUDIK, M. 2008. Modeling ofspecies distributions with Maxent: new exten-sions and a comprehensive evaluation. Ecogra-phy, 31: 161-175.

PIMM, S. L. and JENKINS, C. N. 2010. Extinctionsand the practice of preventing them. In, N. S.Sodhi and P. R. Ehrlich (Eds.): Conservationbiology for all, pp. 181-198. Oxford UniversityPress. NewYork.

REMSEN, J. V., CADENA, C. D., JARAMILLO, A.,NORES, M., PACHECO, J. F., ROBBINS, M. B.,SCHULENBERG, T. S., STILES, F. G., STOTZ, D. F.,and ZIMMER, K. J. 2012. A classification of thebird species of South America. ver. 15-01-2012.Downloaded from http://www.museum.lsu.edu/~Remsen/SACCBaseline.html.

RIBAS, C. C., JOSEPH, L. and MIYAKI, C. Y. 2006.Molecular systematic and patterns of diversifi-

Ardeola 59(2), 2012, 237-252

TODD’S PARAKEET AND DISTRIBUTION MODELS 251

cation in Pyrrhura (Psittacidae), with specialreference to the picta-leucotis complex. TheAuk, 123: 660-680.

RODRÍGUEZ-MAHECHA, J. V. and HERNÁNDEZ-CAMACHO, J. I. 2002. Loros de Colombia. Con-servación Internacional. Bogotá.

TODD, W. E. 1947. New South American parrots.Annals of the Carnegie Museum, 30: 331-338.

TOVAR-MARTÍNEZ, A. E. 2010. Redescubrimientoy notas sobre la ecología y vocalizaciones delPeriquito de Todd (Pyrrhura picta caeruleiceps)en el nororiente de Colombia. Ornitología Co-lombiana, 9: 48-55.

WUNDERLE, J. M. 1994. Métodos para contaraves terrestres del Caribe. General TechnicalReport SO-100. United States Department ofAgriculture and United States Forest Service.New Orleans. Louisiana.

Received: 13 February 2012Accepted: 19 May 2012

Editor: Javier Seoane

Ardeola 59(2), 2012, 237-252

BOTERO-DELGADILLO, E., PÁEZ, C. A. and SANABRIA-MEJÍA, J.252