Composition Changes in a Subandean Avifauna after Long
Transcripción
Composition Changes in a Subandean Avifauna after Long
Society for Conservation Biology Composition Changes in a Subandean Avifauna after Long-Term Forest Fragmentation Author(s): Luis Miguel Renjifo Source: Conservation Biology, Vol. 13, No. 5 (Oct., 1999), pp. 1124-1139 Published by: Blackwell Publishing for Society for Conservation Biology Stable URL: http://www.jstor.org/stable/2641746 Accessed: 21/06/2010 14:03 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=black. 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Blackwell Publishing and Society for Conservation Biology are collaborating with JSTOR to digitize, preserve and extend access to Conservation Biology. http://www.jstor.org Composition Long-Term Changes Forest in a Subandean Avifauna after Fragmentation LUIS MIGUELRENJIFO* International Center for Tropical Ecology, Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, MO 63121-4499, U.S.A., and Fundaci6n Herencia Verde, A.A. 2681, Armenia, Columbia Abstract: Current understanding of the effects offorestfragmentation is based largely on studies in temperate regions, Australia, and Neotropical lowlands. In contrast, the consequences of anthropogenic forest fragmentation for Andean avifaunas are poorly understood, despite large-scale habitat loss and fragmentation. I assessed the effects of long-termnfragmentation on a subandean avifauna in Colombia by comparing the occurrence of bird species in forestfragments isolated over 50-90 years with the original avifauna. Prefragmentation bird composition was based on historical records and current species composition in continuous forest. The original avifauna had approximately 139 forest species and 45 species of open habitats. Among forest species, 30% wverecurrently extinct in fragmentedforest and 4% were regionally extinct. At least 23 nonforest species colonized the region from the lowlands following deforestation. Species with small geographic ranges and those that wverelocally)scarce or rare throughout their ranges were likely to be locally extinct. Forest raptors, terrestrial insectivores, and large frugivores were highly extinction prone, whereas nectarivores, small frugivores, and aerial insectivores were highly resilient; other guilds were intermediate. Antbirds (Fornicariidae, Thamnophilidae), Cotingas, and, especially, Icterids were highly extinction prone. Large body size was not a determinant of vulnerability except among frugivores. Sixty-two percent of the species of special conservation concern wvereextinct in fragments. These results suggest that only large forest tracts will ensure the survival of a large proportion of subandean avifaunas. Fragments of mature forest, however, may support a diverse avifauna, including small populations of globally endangered species several decades after isolation. Th-esefragments could play an imnportantrole in the restoration of local avifaunas. A good understanding of the mechanisms that allow persistence in such fragments may prove essential for the conservation of those species for which no large tracts of suitable habitat remzain. Cambios en la Composici6n de la Avifauna Subandina despues de una Fragmentaci6n de LargoPlazo del Bosque Resumen: El entendimiento que se tiene actualnente de los efectos de lafragmentaci6n de bosques esta basado en gran parte en sobre estudios de zonas templadas, Australia y tierras bajas del Neotr6pico. Por otra parte, las consecuencias de la fragmentaci6n antropogenica de bosques sobre las avifaunas andinas son poco conocidas, a pesar de la perdida yfragmentaci6n de habitats a gran escala. Evalue los efectos de la fragmentaci6n a largo plazo sobre una avifauna subandina en Colombia, comparando la avifauna en fragmentos aisladospor mas de 50-90 afnos con la avifauna original. La composici6n original de la avifauna se bas6 en registros hist6ricos y la conzposici6n actual en bosque continuio. La avifauna original tenfa aproximadamente 139 especies de bosque y 45 especies de habitats abiertos. El 30% de las aves de bosque se han extinguido en los bosquesfragmentados y el 4% se han extinguido regionalmente. Al menos 23 especies de zonas abiertas colonizaron la regi6n desde las tierras bajas siguiendo la deforestaci6n. Las especies con distribuciones geogrdficos restringidas, escasas localmente o raras a lo largo de su distribuci6n fueron propensas a extinguirse localmente. Las rapaces de interior de bosque, los insectfvoros terrestres y losfrugfvoros grandes fueron altaimente propensos a extinguirse; mientras que los nectarivoros, frugivoros pequenios e insectfvoros aereos fueron resilientes; otros gremniosfueron intermedios. Los hormigueros (Formicariidae y Thamnophil- ' Current address: Institutto de Investigaci6n de Recursos Biol6gicos Alexander von Humboldt, A.A. 8693, Santafe de Bogotd, Colombia, email [email protected] Paper submittedJaune 19, 1998; revised manuscript accepted Februa;y 3, 1999. 1124 Conservation Biology, Pages 1124-1139 Volume 13, No. 5, October 1999 Renjifo Long-Term Effectsof ForestFragmentatioz 1125 idae), las Cotingas y especialmente los Icteridos fueron altamente vulnerables. Tener un taman-o corporal grande no fue un determinante de vulnerabilidad excepto entre los frugivoros. El sesenta y dos porciento de las especies de preocupaci6n especial para la conservaci6n se extinguieron en los bosques fragmentados. Estos resultados sugieren que s6lamente areas grandes de bosque continuo asegurardn la supervivencia de una proporci6n grande de las avifaunas subandinas. Sin embargo, los fragmentos de bosque maduro pueden soportar una avifauna diversa que incluye poblaciones pequefnas de especies amenazadas mundialmente despues de varias decadas de aislamiento. Estos fragmentos podrian jugar un papel importante en la restauraci6n de avifaunas locales. Un buen entendimiento de los mecanismos que permiten la persistencia en fragmentos puede ser escencial para la conservaci6n de aquellas especies para las que no quedan remanentes de hdbitat grandes. Introduction Habitat fragmentation is one of the primary threats to bird populations throughout the world. Current understanding of the processes that lead to changes in fragmented ecosystems is based largely on studies in temperate regions, Australia,or Neotropical lowlands (Laurance & Bierregaard1997). Effects of anthropogenic forest fragmentation on tropical montane avifaunasare poorly documented, even though many montane species are particularly vulnerable because of small geographic ranges and narrow habitat requirements (Kattan 1992; Balmford & Long 1994; Renjifo et al. 1997). Lowland and montane avifaunasdiffer in trophic structure and taxonomic composition (Renjifo et al. 1997) and may, therefore, differ in their response to forest fragmentation. Several ecological and biogeographical traits have been associated with likelihood of extinction. For example, large species and species of forest interior that are reluctant to cross open areas are consistently reported to be extinction prone, whereas edge species are reported as resilient (Willis 1974, 1979; Leck 1979; Karr 1982; Stouffer & Bierregaard 1995a). Species that depend on spatially and temporally variable resources, such as fruit and nectar, often need to move over large areas and are also thought to be highly susceptible to fragmentation (Loiselle & Blake 1992). Frugivores, especially large species, are consistently found to be extinction prone (Restrepo et al. 1997). Some nectarivores, however, have been reported as resilient (Stouffer & Bierregaard1995b). Rarity also has been recognized as a predictor of extinction. Rare species include those with a small geographic distribution, narrow habitat specificity, or small population size (Terborgh & Winter 1980; Rabinowitz et al. 1986). In some Neotropical regions, such as the Colombian Andes and the Atlantic forest of Brazil, most species are rare in one or more of these dimensions (Kattan 1992; Goerck 1997). Species near the limits of their geographic range often are locally rare and, therefore, prone to extinction (Karr 1977; Rosenzweig & Lomolino 1997). In addition, demographic characteristics of populations play an important role in the extinction of local populations. Species with low adult survival rates or high population variability are extinction prone (Karr 1990). Species that move between fragments are less likely to go locally extinct because their populations could be supplemented through immigration and recolonization (Burkey 1989). For instance, although migratory species breeding in fragmented temperate forest often exhibit negative rates of recruitment, they persist because of their ability to recolonize fragments when arriving from their wintering grounds (Haila et al. 1993; Robinson et al. 1995; Brawn & Robinson 1996). Documentation of avian extinction in fragmented forests has followed two basic approaches (Kattan et al. 1994): a size-based and a historical-based approach. The first compares avifaunas in forest fragments of different size (e.g., Terborgh et al. 1997), and the second follows changes in avifauna composition over time at an area once covered by extensive forest that has been fragmented (e.g., Bierregaardet al. 1992). The historical approach offers a more direct measurement of extinctions, but, given that long-term historical data on the composition of specific avifaunas are rarely available, it is usually restricted to the short-term effects of fragmentation (but see Willis 1974; Kattan et al. 1994). The purpose of my study was to document changes in the avifauna of a subandean region (i.e., midmontane) 85 year after large-scale deforestation and fragmentation and to evaluate the association of extinction with factors such as body size, trophic group, phylogenetic background, migratory strategy, and rarity. I used a combination of historical and area-based data to overcome some of the limitations encountered previously. The study was possible due to a unique suite of characteristics in the study region. First, historical records of forest cover and avifauna predate landscape transformation. The study region was not settled in the eighteenth century and was covered by unbroken forest. In 1801 Alexander von Humboldt described it as "thick forest, completely uninhabited, with not a single cabin nor a means of subsistence" (in Santa 1993). Clearing of the forest began during the second half of the nineteenth century, with the establishment of five towns within the study region or immediate proximity (Valencia 1964; Santa 1993). The region was still primarily covered by extensive for- Conservation Biology Volume 13, No. 5, October 1999 1126 Long-TermEffectsofForestFragmentation Renjifo est in 1911 when the avifauna was first documented (Chapman 1917) but was extensively deforested shortly thereafter. Second, a large tract of forest remains in the region, which allows comparison between continuous forest and forest fragments. Finally, there are fragments of mature forest that allow the control of confounding effects of comparing prefragmentationmatureforest with secondary forest fragments. This study may help us understandwhat could happen if deforestation eliminates the last tracts of continuous forest in the CordilleraCentralof Colombia. lesser extent, exotic-tree plantations (i.e., Pinus, Cupressus, and Eucalyptus). Fragments are relatively small, usually <20 ha, but a few large remnants (>100 ha) occur in inaccessible canyons. The northwestern part of the study region, within Ucumari Regional Park and Otuin-QuimbayaFauna and Flora Sanctuary, is covered by extensive mature and secondary subandean forest (hereafter called continuous forest). There, subandean forest covers several thousand hectares and is continuous toward the north and east of the study region with tens of thousands of hectares of Andean forest. Methods DataCollection StudyRegion The avifaunaof the southern part of the study region was examined in 1911 by ArthurAllen and Leo Miller during an expedition of the American Museum of NaturalHistory (AMNH).Detailed accounts of species collected, description of collecting sites and explored areas, and landscape photographs were published by Chapman (1917). In addition, I examined voucher specimens, field notes on species seen but not collected, and numerous unpublished photographs of Salento, Filandia, and surrounding landscapes obtained during the expedition at the archives of the AMNH.These sources provided data on the avifauna and extent of forest cover in 1911. I studied current bird species composition from January 1996 to January 1997 in eight fragments surrounded by pastures, eight fragments surrounded by exotic-tree plantations, and eight plots within continuous forest. Study sites ranged from 1.5 to 16.2 ha. All fragments were remnants of mature forest that had been isolated for 50-90 years. The avifaunaat each study site was determined by The study region encompassed an area of approximately 21,000 ha with elevations between 1750 and 2100 m, and ran north-south on the west slope of the Cordillera Central of the Colombian Andes (lat 04041'N, long 75?35'W) in the municipalities of Circasia, Salento, Filandia (Quindio Department), Pereira, and Santa Rosa de Cabal (Risaralda Department) (Fig. 1). The area has a mild climate with an average annual rainfallof 2515 mm, 170 C yearly mean temperature, and daily variation exceeding monthly variation in temperature; frost is absent (Corporacio6nAutonoma Regional del Quindio and Instituto Nacional de Estudios Ambientales, unpublished data). The rainfall pattern is bimodal, with drier periods toward the beginning and middle of the year (Witte 1995), and the area is classified as subandean forest (sensu Cuatrecasas 1958). Forest fragments in the study region exist in humanmodified landscapes dominated by pastures and, to a b) a) inFigure 2100m 1700m ----------- ............... * CaribbeanSea tion of the study region in the Cordillera Central. Shaded areas within the study region (b) indi- sAo 4zw PacT1ic Ocean l _ t! 7 o t COLOMBIA \ t/ F_| 'a ** ?_* ** {<t_, 7roads \ n * * . iii *a/ento J/ ~ ircasi 2km Crai2 1999 cate largeforest tracts; towns are shown in black. Light black lines indicate contour lines (1700 m, _~ ~**9 < Conservation Biology Volume 13, No. 5, October _ ,9 *J_ _/lt>\ \ 1. Location of the study region (a) and study sites within the region (b). Shaded areas within the map of Colombia (a) indicate mountains above 1000 m, and a circle with a star shows the loca- SaIento\ W 2100 m); heavy black lines mark connecting towns. Fragments within pastures are represented by asterisks, fragments within exotictreeplantations are represented by stars, andplots within continuous forest are represented by circles with a star. Long-Term Effects ofForest Fragmentation Renjifo point counts (Blondel et al. 1981) and systematic followup sampling. Each count lasted 15 minutes, and all individuals seen or heard were recorded. Counts were followed by a 1-hourperiod of systematic sampling covering the interior of the fragment or plot to record species not detected during point counts. I visited each site every 4-6 weeks, for a total of 10 visits. A visit consisted of two or three point counts plus an hour of follow-up sampling; the number of counts varied with fragment size. Counts were done between 0620 and 1030 hours except on mornings with strong winds or rain. Identification of bird calls was assisted by recordings obtained with a tape recorder equipped with a semidirectional microphone and by comparison with a reference collection. When I was in doubt, determinations were verified or made by specialists (F. G. Stiles, Universidad Nacional de Colombia; M. Isler and P. Isler, SmithsonianInstitution;T. Schulenberg, Field Museum of NaturalHistory);unidentified bird voices accounted for <0.5% of the records. In addition, I recorded species I observed throughout the study region, especially in the landscape matrices, between August 1995 and May 1997. A complementary study of the avifauna associated with pastures and exotic-tree plantations was done by Calvachi(1999). Species Classificationand Analysis Species were categorized into subgroups for data analysis according to their diets, migratory strategy, rarity, elevational center of abundance, body weight, and habitat association by means of data from literature accounts (Hilty & Brown 1986; Isler & Isler 1987; Stiles & Skutch 1989; Karr et al. 1990; Arango 1993; Stotz et al. 1996; Restrepo & G6mez 1998; Stattersfield et al. 1998) and field observations. Raritywas evaluated at three different scales: geographic range size, local relative abundance, and relative abundance in the Neotropics. Geographic range was classified as small (?50,000 km2) or large (>50,000 kM2) (Stattersfield et al. 1998). Local relative abundance was based on number of records during 180 point counts within the eight continuous forest plots: rare, 0-2; uncommon, 2-10; moderately common, 1130; common, >30. For comparative purposes, relative abundance of migrants was based on point counts conducted during the months when they were present in the region. Relative abundance in the Neotropics was based on data of Stotz et al. (1996). Elevational center of abundance followed data of Stotz et al. (1996): lowland, 0-900 m; foothill, 900-1600 m; subandean, 1600-2600 m; high Andean, above 2600 m. Center of abundance was adjusted to match the actual distribution of the species in the Cordillera Central, which in some cases differs from that elsewhere in the Neotropics (Hilty & Brown 1986). For instance, Russet-backed Oropendolas (Psarocolius angustifrons) and Scarlet-rumpedCaciques (Cacicus uropygialis) are montane species in the An- 1127 dean region of Colombia, although the former is common in the Amazonian lowlands and the latter is common in Choc6 and the Central American lowlands (Hilty & Brown 1986). Species were assigned to four size classes based on body weights: 1, ?25 g; 2, 25-50 g; 3, 50-100 g; 4, > 100 g. Species associated with forest, forest edges, and open areas were treated separately. Forest species reported by the AMNHwere regarded as part of the original avifauna. Forest species recorded during this study were also assumed part of the original avifauna unless they were clearly outside of their usual distribution. Species recorded once or twice during field work and outside of their normal distribution were classified as vagrants and excluded from analysis. The region's birds were classified as extant if they were present in both continuous forest and fragments, regionally extinct if they were present at the beginning of the century and currently absent from both fragmented landscapes and continuous forest, and extinct in the modified landscapes if absent in forest fragments but present in continuous forest; thus, the latter category includes the second category. The modified landscapes are called Salento-Filandia.Forest species recorded three or fewer times in only one fragment were considered greatly reduced and were coded as absent from fragmented landscapes. Association of extinction with different ecological traits were analyzed with G tests, Mann-Whitney U tests, and Fisher exact tests, contingent upon the nature of the data. When expected frequencies were needed, random extinctions were assumed and categories were pooled or removed to fit the assumptions of the test used (Sokal & Rohlf 1995). Small numbers per category prevented meaningful statistical analysis in some instances. Where this was the case, trends are discussed rather than tested. Results and discussion focus on forest species unless otherwise stated. Results Even by 1911, substantial deforested areas existed along the trail from Filandia to Salento, around both towns, and in the valley along the Quindio River close to Salento. Nevertheless, open areas likely covered <20% of the study region in 1911; continuous forest covers <20% of the region today. Landscape photographs suggest that some fragments included in this study were already isolated from continuous forest in 1911. AvifaunaComposition A total of 249 bird species has been reported within the study region: 132 species during the AMNH expedition, 109 additional species found during my study, and eight species recorded in 1989 by Naranjo (1994) and in 1997 Conservation Biology Volume 13, No. 5, October 1999 1128 Lonag-Term Effectsof ForestFragmentation Renjifo Table 1. Speciespresent at the beginningof the centuryand currentlyabsentfrom the studyregion accordingto their center of abundance, trophicgroup, relativeabundance,size class, and geographicrange. Common name Forest species Barred Forest-Falcon Yellow-eared Parrot Rufous-breasted Antthrush Russet-backed Oropendola Scarlet-rumped Cacique Red-bellied Grackle Vagrants Red-bellied Macaw Bar-bellied Woodpecker Tyrannine Woodcreeper Plain Xenops Black-capped Tyrannulet Slaty-backed Chat-Tyrant Long-billed Gnatwren Center of abundancea Scientific name Trophic groupb Relative abundancec Size classd Micrastur ruficollise Ognorbyncb.us icteroitsf Formicarius rttfipectuse Psarocolius angustifronse Cacicus uropygialise Hypopyrrbus pyrobypogasterf L HA SU SU SU SU R/D FR I FR-I FR-I FR-I M R U C C R 4 4 3 4 3 3 Ara severaeg Veniliornis nigricepse,b Dendrocincla tyranninae Xenops minzuttst'g Pbyllonij4as nigrocapillusf? Ocbtboeca cinnarnomeiventrisebi, Rampbocaenus melanuruseg L HA HA L HA HA L FR I I I I I I M M U M U M M 4 2 3 1 1 1 1 aCent.erof abundance: L, lowland; SU, subandean; HA, high Andean. bTJ)ophic group: R/D, raptor diurnal; I, insectivore; FR,frugivore; FR-I,frugivore-insectivore. cRelative abundance in the Neotropics: C, commton;M, moderately commnon;U, uncomnmon;R, rare. dSee textfor size classes. eLarge range, >50 000 kmn. fSmstallrange, ?50 000 km12. 'Iowland species usually found well belouwthe study area. "High Andeaan species usually found 'Associated with streams. well above the study) area. by Calvachi (1999). Of the 249 species, the original forest avifauna of the region was estimated at 139 species (Table 1; Appendix), with an additional 34 edge species, 35 nonforest species, and 41 species that were vagrants, nocturnal, or associated with aquatic habitats.The AMNH recorded by 7 species that seemed to be outside their usual elevational range (Table 1). The status of these species prior to fragmentation is not known, however, so I conservatively regarded them as vagrants rather than as extinct. Before assessing the relationship between traits and extinction, I tested the independence of some of these traits. Body size and membership in trophic groups were associated. Although insectivores, frugivores, and frugivore-insectivores overlapped broadly in body size, the relative distributions among size classes differed significantly (G = 42.04, p << 0.001); to match the test's assumptions I excluded other trophic groups (Fig. 2). Insectivores had more small-bodiedspecies and no species that reached 300 g, whereas frugivores had more large-bodied species, with 9 or 27 frugivores exceeding 300 g. Frugivore-insectivores were intermediate in body size. Not included in this analysiswere 12 species of nectarivores (all < 10 g), one vulture, and three forest raptors (all > 100 g). Trophic group and phylogenetic background were tightly correlated. For instance, nectarivores were Trochilidae; raptorswere Falconifornies;all Furnaridae,Formicariidae, Parulinae, and most Tyrannidae were insectivores; and nearly all Thraupidae were frugivore-insectivores (Ap- Conservation Biology Volume 13, No. 5, October 1999 pendix). Therefore, it was not possible to isolate the relative importance of trophic group from evolutionary history in determining vulnerabilityto fragmentation. RegionalExtinctions A relatively intact condition of the fauna within continuous forest in the region is indicated by the current pres- 70 EZ|1Insectivores Fru-insectiv. Frugivores 60 50 - < a,) U) 4.. 0 30- ~20- 10 < 25 g 25-50 g 50-100Og >lOO0g Size Classes Figure 2. Size-class distribution for the 63 insectivores, 33 frugivore-insectivores, and 2 7frugivores found in the study region. Long-Term Effectsof ForestFragmentation Renjifo ence of top predators, such as Black-and-chestnutEagles (Oroaetus isidori) and Collared Forest-Falcons (Micras- tur semitorquatus), and by large and scarce avian frugivores, such as Cauca Guans (Penelope perspicax) and the Andean Cock-of-the-Rock (Rupicola peruviana). This is corroborated by the presence of large mammals such as pumas (Puma concolor), spectacled bears, (Tremarctos ornatus), and mountain tapirs (Tapirus pinchaque) in continuous forest (L.M.R., unpublished data). Nevertheless, six bird species (4.3% of the original forest avifauna) were regionally extinct (Table 1). Regionally extinct species were on average larger than extant species (U test, p = 0.006; 6 extinct, 133 extant). None of the regionally extinct species weighed <50 g, whereas 67%of all forests species weigh < 50 g. Nevertheless, the largest species were still present in the region, including raptors and cracids. There were no regional extinctions among nectarivores, vultures, or NeotropicalNearctic migrants. Species outside their elevational centers of abundance yet within their usual distribution were not more likely to be regionally extinct than were species close to their centers of abundance (exact test, p = 0.59). For this analysis, I combined subandean (92 extant, 4 extinct) and foothill (18 extant, 0 extinct) for the category "close of center of abundance," and lowland (13 extant, 1 extinct) and high Andean (10 extant, 1 extinct) for the category "farfrom center of abundance." 1129 their capacity to survive in fragmented landscapes and were not included in the analysis: two hummningbirds (Schistes geoffroyi and Colibri delpbinae) were recorded once each in continuous forest and in forest fragments, and the Turquoise Dacnis-Tanager (Pseudodacnis hartlaubi) was recorded once in a forest fragment. Of the 41 species missing from fragments, two were Neotropical-Nearctic migrants: Cerulean Warblers (Dendroica cerulea) and Golden-winged Warblers (Vermivora chrysoptera). In contrast with regional extinctions, body size was not significantly associated with extinctions in fragmented forest when examined for all trophic groups combined (G = 2.02, df = 3, p = 0.56) or when ana- lyzed within insectivores and frugivore-insectivores (U tests, p > 0. 5). Only among frugivores was there a trend 90 - a) 80 70u) 60 .a:) 50 soa) U/) 40030 x 20 -35 Extinctionsin FragmentedLandscapes au 63 Forty-one forest species were extinct in fragmented landscapes (i.e., Salento-Filandia),which represent 30% of the original forest avifauna (Appendix). Three other species were too rare to allow any conclusion about R U MC C 10 90 b) 80- Table2. Incidenceof extinctions pertrophicgroupandguildof forestsin Salento-Filandia. forestspeciesin fragmented '1' ~70- 64 30 33 64 33 Mc C ui) 60- Trophic group and gutild All species* Diurnal raptors Vultures Nectarivores (hummingbirds) Insectivores Aerial Canopy - foliage Understory - foliage Bark Terrestrial Frugivores Large Small Frugivore-insectivores Extinction (%/,) Extant Extinct 95 0 1 9 43 3 41 3 0 1 0 29.9 100.0 0.0 10.0 31.7 0.0 13 16 8 8 38.1 4 5 4 7 7 0 10 20.0 38.5 57.1 25.9 35.0 0.0 31.3 3 20 13 7 22 20 *Three species were too rare to allow evaluation of their capacity to survive infragmentedforest and wverenot included in these nunmbers. bar) o50- U) 40030- -35 x 20 LU 10 0 1 R U Figure 3. Incidence of extinction within relative abuindance categories.-local relative abundance (a) and relative abundance in the Neotropics (b). R, rare; U, uncommon; MC, moder-ately common; C, commnon.Total nuimber of species in each category is inzdicatedinside bars. Conservation Biology Volume 13, No. 5, October 1999 1130 Long-Term EffectsofForestEragmentation Renjifo for large species to be more vulnerable, with no extinctions among small species (i.e., <50 g; Table 2). Body size was not associated with extinction when analyzed within six families with eight or more species (i.e., hummingbirds, woodcreepers, antbirds,flycatchers, warblers, tanagers; U tests, p > 0.1). Overall, the original forest avifauna was composed of 118 genera. Seventeen genera had two or more forest species. All species of Micrastur,Phyllomyias, and Diglossopis went extinct in fragments.All species of Pionus, Phaethornis, Colibri, Aulacorhynchus, Phylloscartes, Turdus, Piranga, and Basileuterus were present in fragments. Six genera had at least one species extinct and one extant in forest fragments (i.e., Grallaria, Pachyrhamphus, Chlorospingus, Columba, Tangara, and Dendroica) (Appendix). A paired-samplet test comparing mean weight of extant species versus mean weight of extinct species within a genus showed no association between body size and extinction (t = 0.378, df = 5, p > 0.5). Thus, body size per se was not a good predictor of extinction. Different scales of rarity were moderate to good predictors of extinction. Species with small geographic ranges had a greater proportion of extinct species in fragments (43%) than species with large geographic ranges (29%). Local relative abundance and extinction were strongly associated such that rare and uncommon species were more likely to be extinct than common or fairly common species (G = 12.34, df = 3,p < 0.01; Fig. 3). Relative abundance in the Neotropics and extinction were also strongly associated (G = 10.41, df = 2, p < 0.01 for rare and uncommon species combined). In contrast, species extinction was independent of position relative to elevational center of abundance (G = 4.84, df = 4, p > 0.15). Therefore, species out of their center of abundance but within the usual range were not more prone to extinction than species at or close to their elevational centers of abundance (Appendix). Table 3. Extinction was unequally distributed among trophic groups (Table 2). Only 1 in 10 hummingbird species but all three forest raptors were absent from fragments. Insectivores, frugivores, and frugivore-insectivores were evenly susceptible (G = 0.43, df = 2,p > 0.80). The majority of terrestrial insectivores were extinct in fragmented landscapes, whereas the majority of understory foliage insectivores were present in fragments. There were five families with 10 or more species (hummingbirds, antbirds, flycatchers, tanagers, warblers), of which only antbirds were more extinction prone in fragments than the rest of the avifauna (exact test, p = 0.04). Icterids were highly vulnerable, with all three forest species not only extinct in forest fragments but in the entire region; a fourth species associated with forest edge was regionally extinct as well. Cotingas were highly susceptible to forest fragmentation, with two of three species extinct in fragments and a third species found in only a few fragments (Appendix). Thirteen species from the original avifauna are of particular conservation concern because they are globally threatened or near-threatened (Baillie & Groombridge 1996; Stattersfield et al. 1998): 11 are associated with forest, 1 with forest edge, and 1 with forest rivers (Table 3). These species had little resilience to fragmentation; 8 were extinct in fragmented landscapes and 2 were regionally extinct. NonforestSpecies Before settlement, natural disturbances such as floods and landslides likely maintained some semi-open habitats and associated avifauna within the region. In fact, some open-habitat species such as Black-winged Saltators (Saltator atripennis) and Black-and-white Seedeaters (Sporophila luctuosa) are subandean elements. Natural occurrence of grasslands, however, was unlikely. Species of global conservation concern (Baillie & Groombridge 1996; Stattersfield et al. 1998). Common name Fasciated Tiger-Heron Black-and-chestnut Eagle Cauca Guan Wattled Guan Chestnut Wood-Quail Golden-plumed Parakeet Yellow-eared Parrot Black-billed Mountain-Toucan Moustached Antpitta Yellow-headed Manakin Multicolored Tanager Turquoise Dacnis-Tanager Red-bellied Grackle Scientific name Tigrisomafasciatum Oroaetus isidori Penelopeperspicax Aburria aburri Odontophorus hyperythrus Leptosittaca branickii Ognorhynchus icterotis Andigena nigrirostris Grallaria alleni Chloropipoflavicappilla Chlorochrysa nitidissima Pseudodacnis hartlaubi Hypopyrrhus pyrobypogaster Global statusa NT NT EN, NT NT, VU CR NT EN, NT, VU, VU, EN, SR SR SR SR SR SR SR aCR,critically endangered; EN, endangered; VU, vulnerable; NT, near threatened; SR, small geographic range. bEF,extinct in fragmented landscapes; PF,present in fragments; RE, regionally extinct. Conservation Biology Volume 13, No. 5, October 1999 Regional statusb RE EF PF EF PF EF RE EF EF PF PF PF RE Table4. 1131 Long-Term Effects of ForestEragmentation Renjifo Speciesassociatedwith edges and pasturesrecordedwithinthe studyregion. Presence in 191la Lowland Presence in colonizationb Edge Species 19 lja Lowland colonizationb Pasture Species Accipiter striatus Buteo magnirostris Buteo platypterus Columba cayennensis Leptotila verreauxi Nyctidromus albicollis Colibri coruscans Colibri thalassinus Amazilia franciae Acestrura mulsant Picumnus granadensis Melanerpesformicivorus Synallaxis albescens Synallaxis azarae Elaeniafrantzii Poecilotriccus ruficeps Todirostrum cinereum Catharus aurantiirostris Atlapetes gutturalis Pheucticus ludovicianus Saltator atripennis Pirangaflava Ramphocelus flammigerus Thraupis episcopus Thraupispalmarum Euphonia musica Tangara gyrola Chlorophanes spiza Pseudodacnis hartlaubi Diglossa albilatera Diglossa sittoides Dendroica castanea Icterus chrysater Amblycercus holosericeus Carduelis xanthogastra + + + + + + + + + + + + + + + + + + + + Bubulcus ibis Coragyps atratus Polyborusplancus Falco sparverius Vanellus chilensis Zenaida auriculata Columbina talpacoti Crotophaga ani Chlorostilbon melanorhynchus Amazilia tzacatl Elaeniaflavogaster Myiophobusfasciatus Pyrocephalus rubinus Pitangus sulphuratus Myiozetetes cayanensis Tyrannus m.elancholicus Notiochelidon cyanoleuca Stelgidopteryx ruficollis Troglodytes aedon Mimus gilvus Turdus ignobilis Zonotrichia capensis Sicalis citrinac Emberizoides berbicola Volatiniajacarina Sporophila luctuosd Sporophila nigricollis Sporophila minuta Tiaris olivacea Tangara vitriolina Tangara cyanicollis Tangara beinei Molothrus bonariensis Scaphidura oryzivora Carduelispsaltria + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + Nonforest vagrants Phimosus infuscatus Elanus leucurus Buteo swainsoni Leptotila plumbeicepsd Forpus conspicillatus Tapera naevia Amazilia saucerotteid Tyrannus savana Hirundo rustica Hemispingus melanotis Tachyphonus + rufusd Coereba flaveola Vireo flavifrons Leistes militaris aSpecies recorded in 1911 are marked; species not marked were recorded only during this study. bSpecies that colonized from the lowlands; these species were not recorded in the subandean regions of Colombia at the beginning of the century or were noted at that time to be expanding into subandean regions following deforestation, often following trails (Chapman 1917). cRecorded by Calvachi (1999). dRecorded by Naranjo (1994). Conservation Biology Volume 13, No. 5, October 1999 1132 Long-Term Effectsof ForestFragmentation The extent to which the region's nonforest avifauna has changed with deforestation is less documented than for the forest avifauna. There were already substantial clearings by 1911. Allen and Miller recorded 16 of the region's 31 edge species and 13 of the region's 36 species associated with pastures, including species such as the Southern Lapwing (Vanellus chilensis), which inhabits short pastures (Chapman 1917). Allen and Miller recognized that the avifauna of open areas was similar then to the open habitants in the Cauca Valley (lowlands) but with many species missing. Their failure to report colnspicuous species such as the Great Kiskadee (Pitangus sulphuratus) and the Gray-capped Flycatcher (Myfozetetes cayennensis) indicates that some species had not yet colonized the region following deforestation. This is likely given the expedition's purpose to record all species, including common and widespread ones (Chapman 1917). There was a marked asymmetry in the direction of colonization of deforested areas. Following deforestation, at least 23 species moved up into the region from the Cauca Valley lowlands following deforestation (Table 4). No species, however, or at most the Rufous-collared Sparrow (Zonotrichia capensis), moved from the extensive open habitats above timberline (i.e., paramo) down into the study region. This asymmetric colonization of deforested montane areas seems widespread in Colombia (L.M.R.,personal observation). In addition to the six regionally extinct forest species, there were six other species associated with habitats other than forest interior which were collected in 1911 and not found during this study. Three species are associated with streams or marshy vegetation: Fasciated TigerHeron (Tigrisoma fasciatum), Northern Waterthrush (Seiurus noveboracensis), and Subtropical Doradito (Pseudocolopteryx acutipennis). The habitatsof these species were not systematicallysampled duringmy study, so it is possible that a more detailed search might prove that they are not extinct. The other three missing species were found elsewhere at forest edges or pastures: Grayish Piculet (Picumnus granadensis), Bran-colored Flycatcher (Myiophobus fasciatus), and Yellow-billed Cacique (Amblycercus holosericeus); their absence likely means they are extinct in the region. Discussion Many patterns of species extinction found in other regions were revealed my study. For instance, forest interior raptors, terrestrialinsectivores, large frugivores, antbirds, and cotingas were extinction prone. Similarly, species with small geographic ranges and species that are locally scarce or rare throughout their range also were extinction-prone (Leck 1979; Willis 1979; Terborgh & Winter 1980; Kattan 1992). Hummingbirds were resilient (Stouffer & Bierregaard 1995b), as were Conservation Biology Volume 13, No. 5, October 1999 Renijifo migrants. Both migrants absent in fragments have also experienced long-term declines on their breeding grounds (Sauer & Droege 1992). More intriguing are those patterns not reported previously or not duplicated by this study: extinction in fragmented forest was independent of body size, species out of their center of abundance were not more likely to go extinct, forest icterids were highly extinction prone, and understory insectivores were moderately resilient. Body size per se was not a major determinant of vulnerability. Large species were not found to be more likely to go extinct when the entire avifauna was analyzed or genus, family, or trophic group were controlled for. Trophic group, pylogenetic background, and raritywere more important determinants of vulnerability. Other studies have found an association between evolutionary history and rarity (Kattan 1992; Goerck 1997). Although the six regionally extinct forest species were on average larger than extant species, their demise seems related to factors other than size: three were icterids, one was an antbird (also terrestrial insectivore), one was a parrot in critical danger of global extinction, and one was a small raptor, a forest-falcon (Table 1). Regional extinctions were likely to be driven by a reduction in the overall forest cover of the region, especially because forest cover was even less extensive during the 1950s and 1960s than it is presently (L.M.R.,unpublished data). The lack of extinction of species out of their center of abundance but within their usual distribution suggests that they were located in "source" habitat (Pulliam 1988). Therefore, if deforestation cut them off from other regions, they were nonetheless able to maintain local populations. Species at the very edge of their geographic range, however, are more likely to be located in "sink"habitat, and deforestation may prevent recolonization. The current absence of some "vagrant"species found in 1911 may result from loss of such sources at lower elevations or from a decrease at higher elevations. Continuous tracts of forest covering a broad elevational range can be important even for species that do not migrate elevationally on a regular basis (Winker et al. 1997). These species, perceived as vagrants, might have been more regular before deforestation because of greater connectedness in the landscape. Only the Yellow-backed Oriole (Icterus chrysater) remains of the icterids recorded in 1911 (although it was found in only 2 of 24 study sites). Russet-backed Oropendolas (Psarocolius angustifrons), Red-bellied Grackles (Hypopyrrbus pyrobypogaster), and Yellow-billed Caciques (Amblycercus bolosericeus) were common, whereas Scarlet-rumpedCaciques (Cacicus uropygialis) were uncommon. P. angustifrons was reported as one of the most characteristic subandean species on the western slope of the Central Andes (Chapman 1917). H. pyrobypogaster was recorded in Ucumari Regional Park as late as 1989 (Naranjo 1994), and a small flock of P. Renjifo angustifrons was seen there in November 1990 (L.M.R., personal observation). Although forest icterids were not previously regarded as a group vulnerable to fragmentation, they seem to be more susceptible to long-term fragmentation than previously acknowledged. This may be difficult to understand because they become more abundant at moderate levels of deforestation (S. Robinson, personal communication). It is unlikely a coincidence that P. angustifrons and P. decumanus have gone extinct in other Andean and inter-Andean regions following deforestation (Alvarez-L6pezet al. 1991; Kattan et al. 1994). H. pyrohypogaster has suffered a drastic geographic range contraction and is now a threatened species (Collar et al. 1992). Also, Willis (1979) reported the loss of one Cacicus in large fragments in eastern Brazil. A closer look at historical records elsewhere might provide further insights into this pattern. The social habits and colonial nesting of some Icterids may make them more vulnerable to extinction over the long term. Small nesting colonies often fail to produce fledglings because they are less capable of defending their nests from predators (Robinson 1985). Small forests likely harbor few flocks and small colonies; consequently, successive nesting failure may lead them to extinction. The best-documented long-term process of avian extinction in the Neotropics occurred on Barro Colorado Island (BCI;Willis 1974; Karr 1982, 1990). The most important driving forces of extinction for forest species on BCI were loss of wet microhabitats that could act as refuges during seasonal and aseasonal droughts (Karr 1982), low adult survival rates, high population variability(Karr 1990), and increased nest predation due to increased mesopredator populations (Terborgh & Winter 1980; Loiselle & Hoppes 1983; Sieving 1992). In general, local populations may fail to maintain themselves because of increased nest predation or parasitism (Robinson et al. 1995). Despite long-term forest fragmentation, there were 96 forest species in the fragments of Salento-Filandia.On average, 71 species were recorded in each fragment. Terborgh et al. (1997) recorded a mean of 21.5 species in forested islands of the same size in the Guri Lake in Venezuela after 7 years of isolation. Long-term extinctions have been documented in only one other subandean locality, namely San Antonio on the Cordillera Occidental of Colombia (Kattan et al. 1994). The original avifaunas of San Antonio and Salento-Filandiawere similar, as was the proportion of extinction, 31% and 30%, respectively. Understory insectivores were highly vulnerable in San Antonio, however, but were relatively resilient in Salento-Filandia.Also, 66.6% of large frugivores went extinct in San Antonio, whereas only 33.3% went extinct in my study. Several interacting factors may account for the differences found between Salento-Filandiaand other regions, including the availability of wet microhabitats, seasonal- Long-Term Effectsof ForestFragmentation 1133 ity, etective isolation, nesting success, anc numaninduced predation. Guri Lake'sislands and BCIwere created by impoundments. These islands are mountaintops with little or no wet microhabitats, which may serve as refuges during dry periods (Karr 1990; Terborgh et al. 1997). BCI and Guri also have a seasonal semideciduous forest (Leigh et al., 1990; Terborgh et al. 1997). In contrast, 15 or 16 fragments studied in Salento-Filandiahad permanent streams providing humid microhabitats. This region has mild seasonality. As a result, drought-driven extinctions are likely less frequent in Salento-Filandia. Isolation by anthropogenic land uses may represent less of a barrier than does water. Some weak fliers, such as toucanets and guans, cross pastures by using isolated tress as stepping stones, and the latter by walking (L.M.R., personal observation). Small open areas, however, represent a barrier to dispersal for some understory and terrestrialbird species (Bierregaardet al. 1992; Sieving et al. 1996). Few comparative studies document adult survivalrates of tropical and temperate birds. Among New World populations of Turdus, however, there is a strong negative correlation between survival rates and seasonality (as measured by temperature) and a weaker positive correlation between survivalrates and precipitation; survivalrates increase from the lowlands to montane regions within the tropics (Ricklefs 1997). If these patterns hold for other avian taxa, relatively h-igh annual survival rates and thus low extinction rates might be expected in Salento-Filandia, because it is a wet and mildly seasonal tropical montane region. Brood parasitism was not evaluated, yet it seems unlikely to be prevalent because few brood parasites were encountered. Shliny Cowbirds (Molothrus bonariensis) were recorded in small numbers in the region and never within study sites. The Giant Cowbird (Scaphidura oryzivora), a selective brood parasite of corvids and icterids (Alvarez-L6pez 1975; Stiles & Skutch 1989), was encountered only four times. Predation by humans, dogs, and cats is likely the cause of higher extinction rates of large frugivores and understory insectivores in San Antonio than in Salento-Filandia. Hunting is known to strongly affect large frugivores (Silva & Strahl 1991; Redford 1992). Fragmentsin Salento-Filandia were in landscapes with a low density of houses; hunting was infrequent. Fragments in San Antonio were surrounded by a rural and suburban matrix with a h-igher density of houses (Arango-V61ez& Kattan 1997) and were more likely to be affected by people and domestic animals. Kattanet al. (1994) attribute five extinctions in San Antonio to hunting, pet trade, and dog predation. ArangoVelez and Kattan (1997) documented artificial nest destruction by dogs in the area. Although cat predation was not reported, it is likely to be frequent in SanAntonio and to affect mainly small understory species. A large tract of forest and some large forest fragments in the region may serve as sources for recolonization. Conservation Biology Volume 13, No. 5, October 1999 1134 Long-Term Effectsof ForestFragmentation More intensive land use in the region would likely precipitate further avain extinctions. It is not known whether these fragments act as population sources or sinks, but the fact that some fragments still have terrestrial birds highly reluctant to cross open areas (e.g., Scytalopus) suggests that at least some species might be able to maintain isolated populations. Conclusion My results indicate a severe impact of fragmentation on this subandean avifauna. Of the 139 forest species recorded historically in Salento-Filandia,30%were extinct in fragments, including many species of global conservation concern. This figure would probably be greater in the absence of large forest tracts in the region. The future for the majority of subandean avifauna is only assured if large tracts of native forest are conserved. This is of concern considering the widespread forest fragmentation in the tropical Andes. For instance, Colombia has lost 73%of its continuous montane forest (Cavalier & Etter 1995), whereas the Cordillera Central has probably lost over 90%of its continuous subandean forests (Fig. 2 in Cavalier& Etter 1995). These figures are probably not too different from what would be found for other Andean regions. On the positive side, these fragments, especially if they contain mature forest, can still support a diverse avifauna after several decades of isolation, including small populations of globally endangered species. Large forest tracts of subandean forest should be given top priority for conservation wherever they exist. Nevertheless, fragments of mature forest could play an important role in the restoration of local avifaunas. Small forest fragments, however, are unlikely to maintain many species indefinitely. A good understanding of the mechanisms that allow persistence in such fragments and active management of their populations may prove essential for the conservation of a number of species for which no large tracts of habitat remain. Acknowledgments I thank B. Loiselle for invaluable advice through all the stages of this project. Discussions and comments by J. Blake, D. Clark, S. Robinson, W. Connett, C. M. Fisher, G. Graham,L. Griz,J. Goerck, I. Jimenez, E. Main,J. PerezEman, D. Saunders, G. Servat, and J. Tello contributed greatly to this paper. My colleagues S. Arango and W. Vargas collaborated in many valuable ways. F. G. Stiles, M. Isler, P. Isler, and T. Schulenberg identified some bird calls. I am thankful to R. Zapata, B. Calvachi, H. Zapata, H. Zuluaga, and R. Gutierrez for field assistance and to P. Sweet for help at the American Museum of Natural History. This study was made possible by funding and logis- Conservation Biology Volume 13, No. 5, October 1999 Renfifo tic support from Fundaci6n Herencia Verde, especially from J. C. Riascos, D. Uribe, J. Ospina, A. Solarte, L. Galvez, and G. Torres. I received generous funding from the MacArthurFoundation, the Wildlife Conservation Society, the National Science Foundation, the International Center for Tropical Ecology (Parker-GentryFellowship and Compton Fellowship), the American Museum of Natural History (Frank Chapman Fund), and the Graduate School of the University of Missouri-St. Louis (Summer Research Fellowship, three summers). I thank Carder, Corporaci6n Regional del Quindio, and Unidad Especial de Parques Nacionales (Ministry of the Environment, Colombia) for research permits and collaboration. These three institutions, Smurfit-Cart6nde Colombia, Bosquinsa, and numerous private landowners allowed me to work on their lands. 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Conservation Biology Volume 13, No. 5, October 1999 1136 Long-Term Effectsof ForestFragmentation Renjifo Appendix Forestbird species present in the studyregion, accordingto family,elevationalcenter of abundance,local relativeabundance,tropic group,and local status.a Family, common name, genus, species Cathartidae (American vultures) Cathartes aura Accipitridae (hawks, eagles) Chondrobierax uncinatus Ictinia plumbeaf Oroaetus isidori Falconidae (falcons) Micrastur ruficollis Micrastur semitorquatus Cracidae (guans) Penelope perspicaxg Aburria aburri Chamaepetes goudotii Odontophoridae (wood-quail) Odontophorus byperythrusg Columbidae (pigeons) Columbafasciata Columba subvinacea Geotrygonfrenata Psittacidae (parrots) Aratinga wagleri Leptosittaca branickii Ognorhynchus icterotis Bolborhynchus lineola Pionus tumultuosus Pionus chalcopterus Amazona mnercenaria Cuculidae (cuckoos) Coccyzus americanush Piaya cayana Strigidae (owls) Otus choliba Glaucidiumjardiniif Ciccaba virgata Nyctibiidae (Potoos) Nyctibius griseus Apodidae (swifts) Cypseloides rutilus Streptoprocne zonaris Chaetura cinereiventris Trochilidae (hummingbirds) Doryfera ludovicae Phaethornis guy Phaethornis syrmatophorus Colibri delphinae Adelomyia melanogenys Heliodoxa rubinoides Coeligena coeligena Coeligena torquata Boissonneauaflavescens Haplophaedia aureliae Ocreatus underwoodii Aglaiocercus kingi Schistes geoffroyi Trogonidae (trogons) Pharomachrus auriceps Trogon collaris Momotidae (Motmots) Momnotus momota Bucconidae (Puffbird) Malacoptila mystacalis Center of abundancd' Trophic groupd Local statuse R CA PF L L SU R SN I R/D V V EF L L U R/D R/D RE EF SU SU HA F R R FR FR FR PF EF PF SU M FR-I PF HA L SU U U U FR FR FR PF EF PF SU HA HA SU HA SU SU R R FR FR FR FR FR FR FR PF EF RE PF PF PF PF I V I PF L HA L R/N R/N R/N PF V PF L I PF L Local relative abundancef R U R U L L M SU SU F R R U I I I PF PF PF SU F SU SU SU SU SU HA SU SU SU SU SU R R R R M R U R R M R R NI NI NI NI NI NI NI NI NI NI NI NI NI PF PF PF EF PF PF PF V PF PF PF EF EF SU L M C FR FR-I PF PF SU F FR-I PF F U I PF continued Conservation Biology Volume 13, No. 5, October 1999 Long-Term Effects of Forest Fragmentation Renjifo 1137 Appendix(continued) Family, common name, genus, species Capitonidae (Barbet) Eubucco bourcierii Ramphastidae (Toucan) Aulacorbynchusprasinus Aulacorbynchus haematopygus Andigena nigrirostris Picidae (woodpeckers) Veniliornisfumnigatus Piculus rubiginosus Campephilus nmelanoleucos Dendrocolaptidae (woodcreepers) Sittasomus griseicapillus Glyphoryncbus spirurus Xiphocolaptes promneropirhynchus Dendrocolaptespicumnus Xiphorbynchus triangularis Lepidocolaptes caffinis Campylorhamphuspusillus Furnariidae (ovenbirds) Cranioleuca erythrops Premnornis guttuligera Premnoplex brunnescens Syndactyla subalaris Anabacerthia striaticollis Thripadectes holostictus Xenops rutilans Formicariidae (antbirds) Thamnophilus unicolor Dysithamnus mentalis Myrmotherula schisticolor Herpsilochmus aff: axilaris Dryrmophila caudata Terenura callinota Formicarious rufipectus Chbamaeza mollissimna Grallaria allenig Grallaria ruficapilla Rhinocryptidae (tapaculos) Scytalopus aff. spillmanni Tyrannidae (tyrant flycatchers) Phyllomnyias uropygialis Phyllomyiasplumbeiceps Phyllomyias cinereiceps Zimmerius viridiflavus Mionectes striaticollis Leptopogon rufipectus Phylloscartes ophthalmicus Phylloscartes poecilotis Pseudotriccuspelzelni Pseudotriccus ruficeps Lophotriccus pileatus Myiophobusflavicans Pyrrhomyias cinnarnomea Empidonax virescensh Myiarchus cephalotes AMyiodynastes chrysocephalus Pachyrazphuspolychopterus Pachyramphus versicolor Center of abundance" Local relative abundancef Trophic groupd Local statuse F U FR-I PF SU F HA M U R FR FR FR PF PF EF SU SU L R C U I I I PF PF PF L L SU R R M I I I EF EF PF SU SU SU F U U C R I I I I PF EF PF EF F SU SU SU SU SU SU M R C C C U U I I I I I I I PF EF PF PF PF PF PF SU F F F SU SU SU SU SU SU U M U M M U M M C I I I I I I I I I I EF PF PF EF PF EF RE EF EF PF SU C I PF SU SU SU SU SU SU SU SU SU HA F SU SU SU SU SU L SU R R U C U C C C M R U U C C M C M U I I I FR FR I I I I I I I I I I FR-I FR-I FR-I EF EF EF PF PF PF PF PF PF EF PF EF EF PF PF PF PF EF continuted Conservation Biology Volume 13, No. 5, October 1999 1138 Long-Term Effectsof ForestFragmentation Renjifo Appendix(continued) Family, common name, genus, species Pipridae (manakins) Chloropipo flavicapillag Masius chrysopterus Cotingidae (cotingas) Pipreola riefferii Pyroderus scutatus Rupicola peruviana Troglodytidae (wrens) Thryothorus genibarbis Henicorbina leucophrys Cyphorbinus thoracicus Turdidae (thrushes) Myadestes ralloides Catharus ustulatusb Platycichla leucops Turdusfuscater Turdus serranus Emberizidae (emberizids) Atlapetes schistaceusf Buarrem.on brunneinuchus Thraupidae (tanagers) Sericossypha albocristata Chlorospingus ophthalmicus Chlorospingus canigularis Hemispingusfrontalis Creurgops verticalis Habia cristatag Piranga rubra A Piranga leucoptera Anisognathusflavinucha Pipraeidea melanonota Euphonia xanthogaster Chlorophonia cyanea Chlorochrysa nitidissimaf Tangara arthus Tangara xanthocephala Tangara ruficervix Tangara labradorides Tangara nigroviridis Tangara vassorii Diglossopis caerulescens Diglossopis cyanea Parulidae (wood-warblers) Mniotilta variah Vermivora chrysopterah Vermivora peregrina b Parula pitiayumi Dendroica fusca " Dendroica cerulea" Setophaga ruticilla Wilsonia canadensish Myioborus miniatus Basileuterus coronatus Basileuterus tristriatus Vireonidae (vireos) Cyclarbis nigrirostris Vireo leucophrys Hylophilus semibrunneus Icteridae (blackbirds) Psarocolius angustifrons Cacicus uropygialis Hypopyrrhus pyrobypogaster Center of abundance" Local relative abundancec Trophic groupd Local statuge SU SU R U FR FR PF PF SU SU SU M M R FR FR FR EF PF EF SU SU SU R C C I I I PF PF EF SU SU SU HA SU C R M R U FR FR-I FR-I FR-I FR-I PF PF PF PF PF HA SU C FR-I FR-I V PF FR-I FR-I FR-I FR-I I I FR-I FR-I FR-I FR-I FR FR FR-I FR-I FR-I FR-I FR-I FR-I FR-I FR-I-N FR-I-N EF EF PF PF EF V PF PF PF PF PF PF PF PF EF EF PF PF PF EF EF I I I I I I I I I I PF EF V PF PF EF PF PF PF PF PF I I I PF PF PF FR-I FR-I FR-I RE RE RE HA SU SU SU SU F L SU SU SU L F F SU SU SU SU SU HA HA HA F F L F U R C M R U M M U C U U M R R M R M R U M R SU L SU SU SU F C C U R C C C C SU SU F C C M SU SU SU SU I continued Conservation Biology Volume 13, No. 5, October 1999 1139 Long-Term Effects of Forest Fragmentation Renjifo Appendix(continued) Family, common name, genus, species Center of abundancSP Corvidae (jays) Cyanocoraxyncas SU Local relative abundance' M Trophic groupd I Local statuse PF aTaxonomy follows that of Stotz et al. (1996). bElevational center of abundance: L, lowland (0-900 m ); F,foothill (900-1600 m); SU, subandean (1600-2600 m); HA, high Andean (above 2600( m). 'Local relative abundance: C, common; M, moderately common; U, uncommon; R, rare. dTrophic group; CA, carrion; SN, snails; RID, raptor diurnal; R/N, raptor nocturnal; FR,frugivore; FR-I,frugivore-insectivore; FR-I-N,frugivoreinsectivore-nectarivore; I, insectivore; NI, nectarivore. eLocal status: EF, extinct in fragments; PR, present in fragments; RE, regionally extinct; V, vagrant. fRecorded by Naranjo (1994). gSmall geographic range. bNeotropical-Nearctic migrant. I Conservation Biology Vololme 13, No. 5, October 1999