AVIFAUNA OF THE MACHE CHINDUL ECOLOGICAL RESERVE, NORTHWEST ECUADOR
Luis Carrasco¹, Karl S. Berg², Jennifer Litz 1, Andrew Cook 1 , & Jordan Karubian1,3
1Fundación para la Conservación de los Andes Tropicales, Mariano Hurtado y Vicente Heredia N-5089, Quito, Ecuador.
2Environmental Science, Policy & Management, University of California, Berkeley, CA 94750, USA.
3Department of Ecology and Evolutionary Biology, Tulane University, 400 Boggs Building, New Orleans, LA 70118, USA. E-mail: [email protected]
Resumen. �– Avifauna de la Reserva Ecológica Mache Chindul, noroeste de Ecuador. �– Reporta-mos la avifauna de la Reserva Ecológica Mache Chindul (REMACH) de 120.000 ha al noroeste de Ecua-dor. El área de estudio se encuentra en una zona de transición poco estudiada entre tres grandesregiones biogeográficas neotropicales �– el Chocó, Tumbes y los Andes Tropicales �– cada una de lascuales contiene una excepcional diversidad y endemismo de aves y otros organismos. Reunimos datosdesde 1998�–99 y 2004�–11 en la Estación Biológica Bilsa (una reserva privada de 3500 hectáreas), envarias fincas, fragmentos forestales y comunidades distribuidas a través de la parte central de REMACH.En estos sitios utilizamos observaciones (registros auditivos y visuales), grabaciones de audio, redes deniebla, puntos de conteo y fotografías. Se registraron 360 especies de aves (263 géneros, 51 familias),incluyendo 57 especies amenazadas de la Lista Roja de Ecuador, 14 de las cuales también se encuent-ran amenazadas a nivel mundial; 23 especies endémicas �‘rango restringido�’ (15 y 8 Tumbes y Chocó ), y16 especies migratorias. Se registró evidencia reproductiva en 130 especies, y documentamos dospicos bien definidos de reproducción, los que corresponden a las estaciones seca y lluviosa. Nuestrosresultados proponen que REMACH representa una zona importante de transición entre las zonas bio-geográficas del Chocó y Tumbes, por lo tal debe ser considerada una prioridad para la conservación dela avifauna y otros taxones.
Abstract. �– We report on the avifauna of the 120,000 ha Mache Chindul Ecological Reserve (REMACH),northwest Ecuador. The study area is located in a poorly studied transition zone between three majorNeotropical biogeographic regions - the Chocó, Tumbesian, and Tropical Andes - each of which containsexceptional diversity and endemism in birds and other organisms. We collected data from 1998�–99 and2004�–11 from the Bilsa Biological Station (a 3500 ha private reserve) and several farms, forest frag-ments, and communities distributed across the central portion of REMACH using observations (aural andvisual), audio recordings, mist netting, point counts and photographs. We recorded 360 species of bird(263 genera, 51 families), including 57 threatened species on the Red List of Ecuador, 14 of which arealso globally threatened; 23 �‘restricted range�’ endemic species (15 Chocó and 8 Tumbesian); and 16migratory species. We recorded breeding activity for 130 species, and documented two distinctivepeaks of reproduction, corresponding to the wet and dry seasons, respectively. Our results suggest thatREMACH represents a transition zone between Chocó and Tumbesian biogeographic zones, and assuch should be considered a priority for conservation of avifauna and other taxa. Accepted 7 November2013.
Northwest Ecuador is situated at the conflu-ence of three major Neotropical biogeo-graphic zones: the Chocó, Tumbesian, andTropical Andes. Each of these biogeographiczones contains significant levels of diversityand endemism in birds and other organisms(Stattersfield et al. 1998, Stotz et al. 2007,Freile & Vázquez 2005, Conservation Inter-national 2007). The humid rainforests of theChocó biogeographic zone expand from anarrow mid-elevation band in southern Ecua-dor to encompass most of western slope ofthe Andes in northwest Ecuador, and con-tinue along the Pacific coast of Colombia andinto southwest Panama. Chocó forests con-tain the highest number of endemic bird spe-cies (62) in the Americas (Devenish et al.2009). The drier, deciduous and semi-decidu-ous forests of the Tumbesian zone occur tothe south of the Chocó, along the Pacificcoast of Ecuador to northern Peru, and con-tain the second highest number of endemicbird species (55) in the Americas (Devenish etal. 2009). Both the Chocó and Tumbesianzones are tied for third highest number ofglobally threatened species (18) in the Ameri-cas (Devenish et al. 2009). To the east, as ele-vation increases, one enters the �‘TropicalAndes�’ biogeographic zone (Ridgely &Greenfield 2001a) or the �‘North CentralAndes�’ Endemic Bird Area (Stattersfield et al.1998, Devenish et al. 2009), another hotspotof diversity and endemism. The overlap ofthese three biogeographic zones makesnorthwest Ecuador an exceptional priority forconservation of biodiversity at the global level(BirdLife International & Conservation Inter-national 2005, Orme et al. 2005).
The Mache Chindul Ecological Reserve(Reserva Ecológica Mache-Chindul, or RE-MACH), the second largest protected area innorthwest Ecuador, has been designated anImportant Bird Area (IBA) by BirdLife Inter-
national (BirdLife International & Conserva-tion International 2005). Although estab-lished as an �‘Absolute Reserve�’ by the Ecua-dorian government, REMACH contains alarge human population that contributes toongoing deforestation and defaunation(Sierra et al. 1999, BirdLife International &Conservation International 2005). Relativelylarge tracts of intact forest remain betweencommunities, the largest of which is BilsaBiological Station, a 3500 ha private reserve(Fig. 1); the Laguna de Cube, a 120 ha Ramsarsite (http://www.ramsar.org), is another nota-ble feature of REMACH.
Much remains to be learned about speciesoccurrences and basic ecology within RE-MACH. Published inventories exist for itsherpetofauna (Ortega et al. 2010) and vascularplants (Neill et al. 1999, Clark et al. 2006, Ce-rón et al. 2010), but for birds most availablestudies focus on the behavioral ecology of in-dividual species, or informal species lists (seebelow). One notable exception is the recentwork by Durães et al. (2013) on patterns ofavian diversity in relation to habitat type andquality. The most recent inventory of avianspecies (BirdLife International & Conserva-tion International 2005) lists 250 confirmedbird species, several of which are species ofconservation concern, but states that thisnumber is likely an underestimate and empha-sizes the need for additional sampling to bet-ter characterize local avifauna. We present in-formation on avian species occurrences andtiming of breeding within REMACH gener-ated over a 14 year sampling period. Our fin-dings are relevant for distributional studies andconservation planning, and provide a baselineof current conditions against which futurestudies of avian diversity may be compared.
METHODS
Study area. Fieldwork was conducted in theMache Chindul Reserve (REMACH), in the
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southwest portion of Esmeraldas provinceand northern portion of Manabí province,northwest Ecuador (Fig. 1). This area strad-dles the equator and is bounded by the PacificOcean to the west, where the cold Peruviancurrent from the south and warm Equatorialcounter current from the north meet, and bythe Andes cordillera to the east. These geo-graphical and oceanographic features areresponsible for abrupt changes in rainfall andtemperature along both latitudinal (i.e.,north�–south) and altitudinal (i.e., east�–west)gradients. These conditions, in combination
with significant barriers to dispersal in histori-cal and contemporary times, are associatedwith exceptional diversity and endemism inbirds and other organisms (ConservationInternational 2007). The Chocó biogeo-graphic zone to the north covers approxi-mately 100,000 km2 in area, while theTumbesian biogeographic zone to the southcovers a total of 130,000 km2 (Devenish et al.2009).
REMACH, which was created in 1996with an area of 119,172 ha (BirdLife Interna-tional & Conservation International 2005),
FIG. 1. Sampling locations within the Mache Chindul Ecological Reserve (REMACH), northwest Ecua-dor. Boundaries of Bilsa Biological Reserve, which was sampled intensively, are denoted. All mist net andpoint count sampling points outside Bilsa are shown by dots; sampling transects and locations for oppor-tunistic observation fall within the area bounded by mist net sampling points.
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represents the northernmost extent of an iso-lated, coastal mountain chain that beginsapproximately 250 km to the south in theprovinces of Santa Elena and Guayas. Thereserve extends from 0�–800 m a.s.l. and isbordered by the Pacific Ocean to the westand, to the east, by a plain approximately 50km wide which separates REMACH from theAndes proper. Average annual rainfall in thereserve ranges from 2�–3.5 m per year, withthe majority occurring January�–May; the dryseason extends from October�–December andis marked by cloudy and misty conditions (JKunpub. data). Rainfall is highest in the mostelevated portions of the reserve, and also inthe northern, Chocóan portions of thereserve. The most common habitat types arehumid and sub-humid evergreen forest.Dominant tree families include Arecaceae,Lauraceae, Rubiaceae, Myristicaceae, andMoraceae, (Clark et al. 2006) and canopyheight of primary forest is typically 30�–40 m.
The habitat in REMACH is a mix of pris-tine and secondary forest fragments with agri-cultural lands, with the proportion ofagricultural lands increasing rapidly over thepast 30 years (Sierra et al. 1999). REMACHcontains approximately 6500 human inhabit-ants living in 50 communities of mestizo,Afro-Ecuadorian, or indigenous (Chachi,Awa) descent separated by forest fragmentsof varying size and isolation (Ministerio deAmbiente 2010). Mestizos and Afro-Ecua-dorians typically work 20�–50 ha farms withapproximately two-thirds of the land underagriculture (cacao, pasture for cattle, corn,beans, rice, plantain, and African oil palm arethe principal crops) and one-third consistingof primary or secondary forest; indigenousgroups subsist primarily from hunting andtimber extraction.
Bilsa Biological Station, a private reserveof 3500 ha established in 1994 and operatedby Fundacion Jatun Sacha, is the largest con-tiguous tract of forest remaining in REM-
ACH. Bilsa is approximately two-thirdsprimary forest and one-third secondary for-est, regenerating 15�–25 years. It is located atthe eastern border of REMACH, approxi-mately in the center of the Reserve, near theborder of Esmeraldas and Manabí provinces(Fig. 1), and contains the highest point in thereserve. Outside of Bilsa, other forest frag-ments of varying size and quality, up toapproximately 500 ha in size, are scatteredthrough out the reserve. Unpublished birdlists have been generated for Bilsa by J. Car-rión, R. Clay, J. Hornbuckle, D. & M. Wolfamong others, providing an important foun-dation of knowledge for the current study.Another publication reported on rangeexpansions for eight species observed in Bilsa(Carrasco et al. 2008).
Data collection. Data collection occurred withina rectangular sampling area (approximately50,000 ha. or 40% of REMACH) extendingalong an east�–west axis bisecting the centralportion of REMACH (Fig. 1). The sampledarea ranges from 100�–800 m a.s.l, and corre-sponds to the most heavily forested area inthe reserve (though significant forested areasalso remain in the unsampled, northern por-tion of the reserve). Within the sampled area,a disproportionate amount of data collectiontook place in Bilsa and surrounding commu-nities to the east, with less time and effortdevoted to sampling lower elevation sites tothe west. Thus, despite the fact that our sam-pling area was centrally located and capturedmost elevation and habitat types found in thereserve, our data should be treated as a mini-mum estimate of species richness in RE-MACH that is likely to increase with furthersampling in additional areas.
Field data were collected from 1998�–1999(by KB) and 2004�–2011 (by remainingauthors) using mist nets, point counts,transect surveys, audio recordings, and oppor-tunistic observations. Data from 1998
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(February�–October) were collected viarepeated point counts along transects (estab-lished trails) within Bilsa (12 km of transect),and via audio recording transect surveysbetween Bilsa and surrounding communities(60 km of transects). Data from 1999 (March�–April) were collected via recordings of vocal-izations and additional transect surveys.Recordings were deposited at the Bioacous-tics collection, Florida Museum of NaturalHistory, Gainesville. From 2004�–11, we con-ducted 33 months of intensive sampling usingmist nets (October 2004�–August 2006, July�–August 2007, November 2008, October 2009,August�–December 2010, February 2011). Ourmist netting methodology was initiallydesigned to assess patterns of avian diversityin relation to habitat type, and the inventorywe present here is a by-product of these stud-ies (see Durães et al. 2013). In each samplingsession, eight mist nets (32 mm gauge, 12 x2.5 m) were distributed in a 250 m lineartransect and operated for 3 consecutive daysfrom 06:30�–13:00 h. Mist net sampling wasconducted at several sites within Bilsa (n = 21sites for 297 total days) and in smaller forestfragments distributed throughout the reserve(n = 14 sites for 42 total days). Additional datawere collected opportunistically at these sites,during travel between sampling sites, andduring visits to other areas in REMACH.
We also gathered data on avian breedingbehavior during each month during the studyperiod. Each of our data points consists of anobservation of "reproductive activity" by agiven species in a given month. Of 302 suchobservations, 152 (50%) were of females withactive brood patches that we captured in mistnets, and 121 (40%) were of active nests. Weconsider these observations to be valid indica-tors of reproductive condition within a givenmonth, and therefore included them in ouranalyses. The remaining 29 observations(10%) were of fledglings or dependent young,which we consider to be less reliable indica-
tors of reproduction in a given month becauseof variation across species in duration ofretaining dependent young. We excludedobservations of fledglings when assessingmonthly reproductive activity when they werenot immediately adjacent to a month in whichan active brood patch or active nest wasrecorded for the same species. In other words,if we (hypothetically) observed active nests fora given species in September and November,and we recorded fledged young in Januarythru July for this same species, the fledgedyoung observations would not be included inour analyses, but fledged young observed inAugust, October, or December would beincluded. This led us to include 13 observa-tions of fledglings and to exclude 16 observa-tions.
Birds were identified using Ridgely &Greenfield (2001a, b) and, for speciesrecorded 1998�–99, using Hilty & Brown(1986) and Ridgely et al. (1989, 1994). Whenany doubts existed about species identity,photographs or recordings were sent to ref-erees for assistance with identification. Wetook a conservative approach when preparingthis article, and only species identified withhigh degrees of confidence are included.Our primary nomenclature follows the SouthAmerican Classification Committee (SACC),an official committee of the American Orni-thologists Union (Remsen et al. 2013); wealso include nomenclature of BirdLife Inter-national (BirdLife International 2013) incases where it differs from that of SACC.Neotropical migrants were classified as suchusing detailed species accounts of Ridgely &Greenfield (2001a). When categorizing spe-cies as endemic to a given biogeographiczone, we employed BirdLife International�’sdefinition of a �‘restricted range endemicspecies�’: a species whose historical range is< 50,000 km2 and is centered within a particu-lar biogeographic zone (Stattersfield et al.1998, Devenish et al. 2009). We also provide
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information on those species consideredendemic by Ridgely and Greenfield (2001a)that are not included in Devenish et al. (2009).Threatened species were identified at the glo-bal level following the IUCN Red List ofThreatened Species (www.iucnredlist.org,IUCN 2011), and within Ecuador usingGranizo et al. (2002). A bird species was con-sidered to be �‘common�’ in REMACH if itwas observed or heard during 50% of ourvisits to REMACH (of 50 total visits duringthe study period) and/or if more than 50 totalindividuals were captured in mist nets; �‘lesscommon�’ if it was observed or heard during10�–49% of our visits and/or between 5�–49individuals were captured in mist nets; and�‘rare�’ it was observed or heard during < 10%of our visits and/or < 5 individuals werecaptured in mist nets.
RESULTS AND DISCUSSION
We registered a total of 360 species of birds(263 genera, 51 families) in REMACH. Thefull list of species with information on migra-tory, endemism, conservation, and breedingstatus is provided in a Supplementary Appen-dix (available online at karubian.tulane.edu/publications or by contacting the authors).The distribution of avian families was similarto most humid Neotropical sites: the familywith the largest number of species and generawas Tyrannidae (35 genera, 47 species), fol-lowed by Thraupidae (13, 25), Trochilidae (15,21), Thamnophilidae (15, 21), Accipitridae(15, 21), and Furnariidae (11, 14). Otherspecies-rich families include Emberizidae,Picidae, Parulidae, Columbidae, Troglody-tidae, and Psittacidae.
Our mist netting work from 2004�–2011provides insights into relative species abun-dances of forest-dwelling understory speciesin REMACH. During this period, we cap-tured and marked a total 7173 individual birds(i.e., excluding replicate captures of the same
individual), representing 186 species (52% ofthe total number of species we recorded). InBilsa, 10 of the 12 species most commonlycaptured in mist nets were hummingbirds andsmall frugivores, whereas in forest fragmentsoutside Bilsa, insectivores were more com-mon (7 of the 12 most common species). Ofthe 186 total species captured in mist nets inREMACH, only 12 (6.5%) were exclusive toareas outside Bilsa, suggesting that thereserve�’s avifauna outside of Bilsa may largelybe a nested sub-set of the avifauna found inBilsa (see also Durães et al. 2013).
Breeding. We observed breeding behavior in130 total species in REMACH, with repro-ductive behavior observed in every month ofthe year (Supplementary Appendix). Twoclear peaks of breeding activity, from Febru-ary�–May and October�–November, corre-spond to periods of maximum and minimumrainfall, respectively (Fig. 2). The wet seasonis associated with a peak in insect abundance(JK unpub. data), and most species appear tobreed in this period. The dry season coincideswith high levels of fruit production in atleast some trees (e.g., Miconia spp., Virola dixo-nii) and may be associated with an overallpeak in fruit production in REMACH (JKunpub. data). Species that appear to breedmainly in this period include small frugivoressuch as most manakin and tanager species.Many species appear to breed year-round;breeding activity was recorded at least eightmonths of the year for eight species includinginsectivores, frugivores, and nectarivores(Supplementary Appendix). The data pre-sented here are minimum values for repro-duction, and we consider it likely that at leastsome individuals of many species may breedin all months of the year in REMACH.
Information on selected focal taxa pro-vides a more detailed look at the diversityof species-specific breeding strategies amongREMACH avifauna. Activity of male
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Long-wattled Umbrellabirds (Cephalopterus pen-duliger) at lek sites is highest in the dry season,but most nests are recorded during the wetseason, perhaps suggesting a temporal discon-nect between display and nesting behavior inthis species (Tori et al. 2008). Umbrellabirdnests have been reported from other sites inEcuador at transition periods between rainyand dry seasons, in June (Mindo, PichinchaProvince by Karubian et al. 2003) and January(Buenaventura, El Oro Province by Greeneyet al. 2008); information from lek activity atthese sites is not available. The frugivorousGreen Manakin (Xenopipo holochlora), whichappears to nest exclusively in riparian areas inour study area (JK and P. Mena, unpub. data),exhibits two distinctive peaks in nesting, onein the dry season and one in the wet season. Asimilar bimodal breeding pattern has recentlybeen described for another riparian specialistin eastern Ecuador, the insectivorous SpottedBarbtail (Premnoplex brunnescens) (Greeney2010). Flame-rumped Tanager (Ramphocelus
icteronotus) and Brown Wood-Rail (Aramideswolfii) both have relatively short and focusedbreeding seasons, lasting only 2�–3 monthsduring the peak of the wet season (Karubianet al. 2011, JK and J. Olivo, unpub. data). TheBanded Ground-Cuckoo (Neomorphus radiolo-sus) also breeds during the peak of the rainyseason, and has the ability to re-nest followingnest failure (Karubian et al. 2007). This infor-mation from REMACH adds to the growingbody of information being generated by H.Greeney, J. Freile, and others on the richdiversity of reproductive strategies amongtropical bird species, and highlights the needfor additional studies that elucidate basicreproductive biology.
Migratory species. We recorded 16 migratory orpotentially migratory species as classified byRidgely & Greenfield (2001a) (Table 1). Themajority of these species are Neartic-Neotro-pical (boreal) migrants which breed in theNorthern Hemisphere and migrate southward
FIG. 2. Number of bird species recorded breeding in each month in the Mache Chindul EcologicalReserve, northwest Ecuador, summed across 2004�–2011.
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during the northern winter, including shore-birds, flycatchers, and warblers. Spotted Sand-piper (Actitis macularius), Summer Tanager(Piranga rubra), Acadian Flycatcher (Empidonaxvirescens), and Swainson�’s Thrush (Catharusustulatus) are relatively common in REMACH;other Neotropical migratory species appear tobe relatively scarce among the areas we sam-pled. Prior to this study, the Bay-breastedWarbler (Dendroica castanea) had been reportedfrom only three other localities in Ecuador(Ridgely & Greenfield 2001a), and REMACHcurrently represents the southernmost extentof its known range. The Swallow-tailed KiteElanoides forficatus has two subspecies, a resi-dent breeder in Ecuador (E. f. yetapa) and aboreal migrant (E. f. forficatus) (Ridgely &Greenfield 2001a). At Bilsa, this species fluc-tuates in a manner consistent with borealmigration (i.e., commonly observed in thenorthern winter and absent in the boreal sum-
mer), but at least some individuals are presentyear-round in lower-lying southern parts ofthe reserve (J. Olivo pers. comm.). Additionalinformation is required to resolve the migra-tory status of this species in REMACH, butwe include it as migratory until such informa-tion becomes avaialable. Osprey (Pandion hali-aetus), Little Blue Heron (Egretta caerulea), andTurkey Vulture (Cathartes aura) also havemigratory and non-migratory populations inEcuador (Ridgely & Greenfield 2001a), butbased on our anecdotal observations, we con-sider it likely that REMACH populations areresident.
We recorded no long-distance Australmigrants (species that breed in the SouthernHemisphere and migrate northward duringthe southern winter), corroborating obser-vations that long-distance Austral migrationis rare for birds occurring west of the Andesin Ecuador (Ridgely & Greenfield 2001a).
TABLE 1. Migratory bird species recorded in the Mache Chindul Ecological Reserve (Reserva EcológicaMache-Chindul, REMACH), northwest Ecuador, during 1998�–99 and 2004�–11. Classification of migra-tory status follows Ridgley & Greenfield 2001a. For more information refer to Supplementary Appendix(available online at karubian.tulane.edu/publications).
Family Scientific name English name Migrant typeAccipitridaeScolopacidae
The Red-eyed Vireo (Vireo olivaceus) hasAustral migrant, boreal migrant, and residentbreeding populations in Ecuador but the sub-species thought to occur in western Ecua-dor, V. o. griseobarbatus, is considered resident(Ridgely & Greenfield 2001a). We recordedoverwintering (non-breeding) individuals ofthree putative intratropical Austral migrantsthat migrate short distances bet-ween south-ern (breeding) and northern (non-breeding)ranges: Snowy-throated Kingbird (Tyrannusniveigularus), Crimson-breasted Finch (Rhodo-spingus cruentatus), and Gray-capped Cuckoo(Coccyzus lansbergi) (Ridgely & Greenfield2001a, J. Freile pers. com.)
Endemism. We recorded a total of 15 speciesendemic to the Chocó and 8 species endemicto the Tumbesian biogeographic zones fol-lowing BirdLife International�’s �‘restrictedrange species�’ (RRS) classification scheme(Stattersfield et al. 1998, Devendish et al. 2009)(Table 2). The number of endemic speciesincreases to 21 for the Chocó and 13 for theTumbesian using the classification scheme ofRidgely & Greenfield (2001a) (SupplementaryAppendix). In all cases, BirdLife InternationalRRS species are nested within Ridgely &Greenfield�’s (2001a) list of endemics. Werecorded an additional six species consideredendemic to the �‘Tropical Andes�’ region byRidgely & Greenfield (2001a), but no RRSspecies from BirdLife International�’s �‘NorthCentral Andes�’ region (Devendish et al. 2009).Thus, depending upon which scheme oneuses, REMACH contains anywhere from 23to 42 �‘endemic�’ species. This nearly two-folddiscrepancy indicates the need for a single,unified classification scheme. We give prece-dence to BirdLife International�’s RRS catego-rization scheme in the current study andpromote its use for other studies because,while noting that it is somewhat restrictiveand arbitrary, it applies a standardized meth-odology using up-to-date information that
can be applied at the global scale, and thus canbe compared across regions and time periods.
We recorded more Chocó than Tumbe-sian endemics, both at the species and individ-ual levels, suggesting that REMACH is moreclosely aligned with the Chocó biogreo-graphic zone. There are very few largeremaining tracts of forest in the drier, south-ern parts of REMACH, and it is possible thatthe Tumbesian endemics we have recorded inthese areas are relatively recent arrivalsexploiting newly available niches created byconversion of forests to agricultural land-scapes (J. Freile pers. com.). Alternatively, hab-itat conversion in the drier areas of the reservemay have extirpated sensitive Tumbesianendemics. Additional sampling in this area ofthe reserve is a priority. The low number ofAndean endemics likely reflects the fact thatREMACH is separated by the Andes properby a low lying, heavily deforested plain, andthat many Andean endemics are restricted torelatively high elevations. With the exceptionof Crimson-breasted Finch and Gray-backedHawk (Pseudastur occidentalis), we consider itlikely that all the endemic species were year-round residents and breeders in REMACH.We recorded reproductive behavior in REM-ACH for six RRS Chocó endemics, includingendangered species like Banded Ground-Cuckoo and Long-wattled Umbrellabird, andone RRS Tumbesian endemic, the EcuadorianThrush (Turdus maculirostris).
Endangered species. We recorded 14 globallythreatened species in REMACH, of which 2were Endangered (EN), 5 Vulnerable (VU),and 7 Near Threatened (NT) (IUCN 2013)(Table 2). At the national level, this numberswells to 57 species threatened within Ecua-dor, with 1 CR, 11 EN, 26 VU, and 19 NTspecies (Granizo et al. 2002) (SupplementaryAppendix). We recorded reproductive activityfor 4 IUCN species and an additional 17 spe-cies on the Ecuador Red List (Supplementary
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Appendix), and consider it likely that mostof the 57 threatened species breed inREMACH.
A high proportion of threatened speciesin REMACH are also RSS endemics (7/13Chocó and 3/8 Tumbesian endemics areIUCN listed; Table 2, Supplementary Appen-dix), likely because of loss of primary habitatthat these species depend upon. Many ofthese threatened species are also frugivoreswhose declines may impact seed dispersalprocesses and, ultimately, forest structure inthe reserve. In particular, large-seeded treespecies such as members of the Arecaceae,Lauraceae, and Myristicaceae families (palm,avocado, and nutmeg respectively) may expe-rience reductions in fruit removal and seedmovement as large frugivores like Long-wat-tled Umbrellabird and Great Currasow (Craxrubra) become more rare (Karubian et al.2010, 2012). This concern, compounded bythe fact that many large seed dispersal agentsare already functionally extinct in the reserve[e.g., Brown-headed spider monkey (Ateles fus-ciceps)], underscores the importance of viableavian seed dispersal processes for the long-term well-being of REMACH.
Many of the threatened bird species werecorded appear to have strongholds in Bilsa,suggesting that the primary forests found inthis reserve are key for their conservation. Forexample, Long-wattled Umbrellabird andBanded Ground-Cuckoo have stable androbust populations within Bilsa (Karubian &Carrasco 2008, JK unpub. data), but appear tobe rare or absent from many smaller andmore isolated fragments where, according tolocal residents, they were found 20�–30 yearsago. Conditions for threatened species appearto be more tenuous outside the Bilsa: our onerecord of the Grey-backed Hawk, a specieswhose total population size is estimated at100�–250 birds (IUCN 2011), is of a singleindividual killed by a hunter. In contrast, how-ever, the Brown Wood-rail appears to main-
tain healthy populations in relatively impactedsecondary forest and even agricultural land-scapes, although the species was alwaysrecorded in proximity to large tracts of pri-mary forest (Karubian et al. 2011).
In addition to highlighting the importanceof Bilsa as a core, �‘source�’ area for avifauna inthe reserve, these findings lead to severalother practical considerations for conserva-tion policy in REMACH. Additional samplingof privately owned forest fragments outsideBilsa, especially in the far northern and south-western portions of the reserve, is a clear pri-ority for future research. More informationon habitat preferences, basic ecology, andpopulation status of endangered specieswould be desirable for conservation statusand planning processes. The region alsohouses sub-species that may represent evolu-tionarily independent lineages at risk ofextinction in Ecuador in the short-term, suchas the Sapphire Quail-Dove (VU, Geotrygonpurpurata; G. saphirina purpurata in BirdLifeInternational nomenclature), Collared Aracari(VU, Pteroglossus torquatus), as well as othersubspecies that may be more resistant toanthropogenic activities but nonethelessdeserve more detailed study, such as White-throated Thrush (Turdus assimilis; T. a. daguaein BirdLife International nomenclature) (NT),and Scarled-rumped Cacique (Cacicus uropygia-lis; C. u. pacificus in BirdLife Internationalnomenclature) (NT)]. Another priority is todesign and implement effective conservationmeasures to assist local stakeholders withconservation. As evidenced by the case ofGrey-backed Hawk, environmental educa-tion designed to influence attitudes andresource management practices of local resi-dents would also be useful for conservation inthe reserve.
Conclusion. The high number of endemic (23)and endangered (14 global, 57 national) spe-cies from distinctive biogeographic zones in a
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relatively small area (120,000 ha) underscoresthe importance of REMACH as a transitionzone between major South American avifau-nas. Transition zones exhibit unusually rapidrates of species turnover and genetic, mor-
phological, and behavioral variation withinand between species (Smith et al. 1997, Tho-massen et al. 2010). These conditions mayserve as an engine for speciation and/or con-tribute to species persistence in the face of
TABLE 2. Threatened and endemic bird species recorded in the Mache Chindul Ecological Reserve(Reserva Ecológica Mache-Chindul, REMACH), northwest Ecuador, during 1998�–99 and 2004�–11.Family, scientific name (following SACC nomenclature, with BirdLife International nomenclature providedin parentheses in cases of non-concordance), and common name in English are provided for each species.Classification of endemic species into either the Chocó or Tumbesian biogeographic zones followsBirdLife International�’s �‘restricted range�’ species concept (Devendish et al. 2009). Classification of threat-ened species follows current IUCN Red List listings at the global level (EN = Endangered, VU = Vulnera-ble, NT = Near Threatened, LC = Least Concern). For more information including observed breeding, theobservation or capture method, and frequency of encounter for each species, refer to SupplementaryAppendix (available online at karubian.tulane.edu/publications).
Family Scientific name English name Endemic IUCNCuculidaeFalconidaeCotingidaeRamphastidaeCaprimulgidaePicidaeThraupidaeTinamidaeColumbidaePsittacidaeRamphastidaePicidaeTrochilidaeTrogonidaeThamnophilidaeAccipitridae
changing conditions, such as land conversionand climate change; for this reason, transitionzones are often priorities for conservation(Smith et al. 2001, 2005). Extensive habitatclearing for timber and agriculture has causedwestern Ecuador�’s forests to become one ofthe world�’s most threatened ecosystems(IUCN 2010). Indeed, this area is part of theonly region on earth (the Tropical Andes) thatcombines the top 5% of threat, diversity, andendemism among avian taxa in a single terres-trial biome (Orme et al. 2005). These factorslead us to conclude that, with appropriateconservation planning and activities, RE-MACH has the potential to provide a keystronghold for biodiversity of birds and othertaxa in coming years.
ACKNOWLEDGMENTS
We thank the local residents of REMACH forconserving what forest remains and providingaccess to their lands. We are grateful for theassistance provided by staff of the Founda-tion for the Conservation of the TropicalAndes (FCAT), especially D. Cabrera, F.Castillo, J. Cabrera, M. Gonzalez, P. Mena,and J. Olivo, and by staff of Jatun Sacha Foun-dation and Bilsa Biological Station, particu-larly C. Aulestia, J. Bermingham, S. Delgado,and M. McColm. We thank A.-A. Weller andone anonymous reviewer for comments on anearly version of this article, and are especiallygrateful for the outstanding comments madeby J. Freile and H. F. Greeney. R. Durães andT. B. Smith provided helpful feedback andassistance though out the study, and assistedwith figures and analyses in the publication.This project was supported by the NationalScience Foundation (OISE-0402137), UnitedStates Fish & Wildlife Service NeotropicalMigratory Bird Act, National GeographicSociety, Disney Worldwide ConservationFund, the Endowment for World Parks, andM. Nicolson. All research was conducted with
approval of the Ecuadorian Ministry of theEnvironment.
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