Contributed Paper Two Hundred Years of Local Avian in Eastern Amazonia

NARGILA´ G. MOURA,∗ ALEXANDER C. LEES,†‡‡ ALEXANDRE ALEIXO,† JOS BARLOW,†‡ SIDNEI M. DANTAS,† JOICE FERREIRA,§ MARIA DE FATIMA´ C. LIMA,† AND TOBY A. GARDNER¶∗∗†† ∗Curso de Pos-Graduac´ ¸˜ao de Zoologia, Universidade Federal do Par´a/Museu Paraense Em´ılio Goeldi, Caixa Postal 399, CEP 66040-170, Belem,´ Par´a, Brazil †Coordenac¸˜ao de Zoologia, Museu Paraense Em´ılio Goeldi, Caixa Postal 399, CEP 66040-170, Belem,´ Par´a, Brazil ‡Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, United Kingdom §Embrapa Amazoniaˆ Oriental, Trav. Dr. Eneas´ Pinheiro s/n, CP 48, CEP 66095–100 Belem,´ PA, Brazil ¶Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, United Kingdom ∗∗International Institute for Sustainability, Rio de Janeiro, CEP 22460-320, Brazil ††Stockholm Environment Institute, 87D Linegatan, Stockholm, Sweden

Abstract: Local, regional, and global extinctions caused by habitat loss, degradation, and fragmentation have been widely reported for the tropics. The patterns and drivers of this loss of species are now increasingly well known in Amazonia, but there remains a significant gap in understanding of long-term trends in species persistence and in anthropogenic landscapes. Such a historical perspective is critical for under- standing the status and trends of extant biodiversity as well as for identifying priorities to halt further losses. Using extensive historical data sets of specimen records and results of contemporary surveys, we searched for evidence of local extinctions of a terra firma rainforest avifauna over 200 years in a 2500 km2 eastern Amazonian region around the Brazilian city of Bel´em. This region has the longest history of ornithological fieldwork in the entire Amazon basin and lies in the highly threatened Bel´em Centre of Endemism. We also compared our historically inferred extinction events with extensive data on species occurrences in a sample of catchments in a nearby municipality (Paragominas) that encompass a gradient of past forest loss. We found evidence for the possible extinction of 47 species (14% of the regional species pool) that were unreported from 1980 to 2013 (80% last recorded between 1900 and 1980). Seventeen species appear on the International Union for Conservation of Nature Red List, and many of these are large-bodied. The species lost from the region immediately around Bel´em are similar to those which are currently restricted to well-forested catchments in Paragominas. Although we anticipate the future rediscovery or recolonization of some species inferred to be extinct by our calculations, we also expect that there are likely to be additional local extinctions, not reported here, given the ongoing loss and degradation of remaining areas of native vegetation across eastern Amazonia.

Keywords: avifauna, colonization, forest dependency, IUCN Red List, sighting record, urban conservation

Doscientos Anos˜ de Extinciones Locales de Aves en la Amazonia Oriental Resumen: Las extinciones locales, regionales y globales causadas por la p´erdida, degradacion´ y frag- mentacion´ de habitat´ se han reportado ampliamente para los tropicos.´ Los patrones y conductores de esta p´erdida de especies son ahora muy conocidos en la Amazonia, pero aun´ persiste un vac´ıo significativo en el entendimiento de las tendencias a largo plazo en la persistencia de las especies y la extincion´ en terrenos antropog´enicos. Dicha perspectiva historica´ es cr´ıtica para entender el estado y las tendencias de la biodiversidad existente as´ı como para identificar prioridades que detengan las p´erdidas futuras. Al usar

‡‡Address correspondence to A. C. Lees, email [email protected] Paper submitted October 30, 2013; revised manuscript accepted January 26, 2014. 1 Conservation Biology,Volume00,No.0,1–11 C 2014 Society for Conservation Biology DOI: 10.1111/cobi.12300 2 Avian Extinctions in Amazonia juegos de datos historicos´ extensivos de registros de espec´ımenes y resultados de sondeos contemporaneos,´ buscamos evidencias de extinciones locales de avifauna en una selva de tierra firme a lo largo de 200 anos˜ en una region´ de 2, 500 km2 en la Amazonia oriental, cerca de la ciudad brasilena˜ de Bel´em. Esta region´ tiene la mayor historia de trabajo de campo ornitologico´ en toda la cuenca del Amazonas y yace en el altamente amenazado Centro de Endemismo de Bel´em. Tambi´en comparamos nuestros eventos de extincion´ inferidos historicamente´ con los datos extensos de la ocurrencia de especies en una muestra de zonas de influencia en una municipalidad cercana (Paragominas) que engloba un gradiente de p´erdidas pasadas de bosque. Encontramos evidencias de la extincion´ posible de 47 especies (14% del acervo regional de especies) que no se reportaron de 1980 a 2013 (80% fue reportado por ultima´ vez entre 1900 y 1980). Diecisiete especies aparecen en la Lista Roja de la UICN, y muchas de estas son de gran tamano.˜ Las especies perdidas en la region´ inmediata a Bel´em son similares a aquellas que actualmente estan´ restringidas a zonas de influencia con bosques bien desarrollados en Paragominas. Aunque anticipamos el futuro redescubrimiento o recolonizacion´ de algunas especies que se infiere estan´ extintas de acuerdo a nuestros calculos,´ tambi´en esperamos que probablemente existan extinciones locales adicionales, no reportadas aqu´ı, dada la p´erdida y degradacion´ continua de las areas´ restantes de vegetacion´ nativa a lo largo de la Amazonia oriental.

Palabras Clave: avifauna, colonizacion,´ conservacion´ urbana, dependencia de bosque, Lista Roja de la UICN, registro de avistamientos

Introduction work has been conducted over long periods. Here, we present such a case study for the region around the city Determining if and when a species becomes locally, re- of Belem,´ the longest studied area of the entire Amazon gionally, or globally extinct is never easy because the basin. rarer a species gets, the more difficult it is to find Amazonia is subject to the highest absolute rates of and study. The ecological literature contains many cases loss of tropical forest on the planet (Hansen et al. 2013). whereby species once considered extinct have been re- Despite substantial reductions in deforestation rates in discovered decades or even centuries later (e.g., Crowley the Brazilian Amazon during the last decade (INPE 2013), 2011). Such cases indicate the necessity for thorough this loss and fragmentation of forests threaten many field surveys before declaring a species to be extinct (e.g., species with global extinction (e.g., et al. 2011). Butchart et al. 2006). These problems are most severe in Local extinctions caused by habitat loss, fragmentation, the tropics, where biodiversity is richest, extinction (and and disturbance from fire and logging are relatively well rediscovery) rates are highest (Costello et al. 2013), and studied in Amazonia (Peres et al. 2010), and the longest land-use change is currently most acute (e.g., Sodhi et al. running study, the Biological Dynamics of Forest Frag- 2004). Furthermore, a persistent lack of time-series data ments Project, dates back only to 1979 (Laurance et al. means that estimating extinction risk is often only pos- 2011). Thus, a major knowledge gap relating to the con- sible through a space-for-time substitution. For example, servation of Amazonian biota is an understanding of long- one might compare current species persistence in heavily term trends in species persistence and extinction in the forested areas with patterns of persistence in adjacent human-modified landscapes that increasingly character- recently deforested areas (Pickett 1989). However, it is ize the region. possible that many short-term studies may not be able Arguably the most threatened region of Amazonia is to capture long-term patterns of species survival because the 243,000 km2 Belem´ Center of Endemism (BCE) in extinction debts may be paid over a very long period for northeastern Par´a and W Maranh˜ao states. This area has species with long generation times and insulation from the longest history and highest proportion of forest loss of real-world threats (in experimental landscapes or over any Amazonian interfluve and retains 24% of its original short periods), such as hunting and trapping, may lead to primary forest cover (Almeida & Vieira 2010). Most of underestimates of extinction risk (e.g., Peres et al. 2010). this remaining forest is heavily fragmented and degraded Thus, understanding what constitutes the baseline of bio- by recurrent selective-logging and fire events, as well as diversity prior to recent large-scale landscape change and overextraction of game and other nontimber for- resource extraction by humans is fraught with difficultly est resources (Almeida & Vieira 2010; Amaral et al. 2012). for many parts of the world. Although 11 of the 160 threatened avian taxa on the cur- One of the most robust approaches to estimating past rent Brazilian Red List are strictly Amazonian, 10 of these extinctions and current extinction risk is to combine data are restricted to the BCE (Machado et al. 2008). A further from current field surveys with historical data from mu- 12 species occurring in but not necessarily restricted to seum specimens (e.g., Kattan et al. 1994; Patten et al. the BCE are also considered globally threatened (IUCN 2010). This powerful approach is only possible for re- 2013), of which 7 do not appear on the Brazilian Red List gions of the world where extensive natural history field- (Machado et al. 2008). Quantitative data on the responses

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Figure 1. (a) The state of Para´ in Brazil, (b) position of the study areas (1, metropolitan region of Bel´em (MRB); 2, Paragominas in Para),´ and (c) the extent of remaining forest cover in the MRB (black, forest; dark gray, secondary forest; light gray, urban; white agricultural; hatched, water). to land-use change and persistence in fragmented land- Methods scapes for many of these threatened taxa are generally lacking (Portes et al. 2011). Study Site The state capital Belem´ (Belem´ do Gr˜ao Par´a) was The 2537 km2 MRB (approximately 1°S, 48°ʹW, Fig. 1), founded by the Portuguese in 1616, and by 1752 it was a conurbation of 2.2 million people, is in northeastern a hub of Amazonian biodiversity research (Teixeira et al. Brazil at the mouth of the Guam´a River in Par´a state and 2010). Many renowned naturalists (including Henry Wal- is divided into 6 municipalities: Belem,´ Ananindeua, Mar- ter Bates, Alfred Russel Wallace, and Johann Baptist von ituba, Benevides, Santa Isabel, and Santa B´arbara do Par´a. Spix among others) collected thousands of bird (among Local soils are typically deep oxisoils, well-drained with other) specimens that were deposited in museums across low natural fertility, and the natural climax vegetation the world (Novaes & Lima 2009). This wealth of speci- is dense ombrophilous terra firma and varzea´ (season- men data has, until now, been untapped for use in con- ally flooded) forests (Novaes & Lima 2009). Local climate servation research, yet offers invaluable insights into the details are in Supporting Information. history of local avifaunal extinctions in this unique corner Since its founding on 12 January 1616 the city and its of Amazonia (e.g., Burgman et al. 1995). In stark contrast environs have undergone over 4 centuries of forest loss to most of Amazonia, where substantial forest losses have and degradation, catalyzed by the construction of the only occurred in the last 50 years, the Metropolitan re- Estrada Real from 1616 onward, a highway that connects gion of Belem´ (MRB) was already heavily deforested and Belem´ to S˜ao Lu´ıs in Maranh˜ao state, and later associated defaunated more than a century ago (Vieira et al. 2007). with the construction of the Braganc¸a railway, between Our goal was thus to investigate long-term trends in 1883 and 1908 aimed at developing eastern Par´a (Vieira local extinction and persistence of Amazonian in et al. 2007). Present day forest cover in the MRB is approx- a highly fragmented and degraded forest region (MRB) imately 43.5% of the original pre-Columbian extent (INPE that characterizes the BCE. We searched for evidence of 2013). There are 6 protected areas (6399 km2), most of local extinctions from 1812 to 1980 in the MRB by ex- which are severely degraded due to ongoing disturbance amining museum records and estimating the persistence events such as fire, selective-logging, and illegal hunting probabilities and likely extinction dates for species un- (Le˜ao et al. 2007). recorded since 1980. We compared these historical data with field data on local extinctions from the most exten- sively forested region left in the BCE—the municipality of Data Collection Paragominas, which was subject to a recent exhaustive biodiversity inventory (Lees et al. 2012; Gardner et al. Novaes and Lima (2009) list 490 bird species for the MRB, 2013; Moura et al. 2013). We then determined if current of which 329 (67%) are present in unflooded terra firma patterns of threat recognized at the regional, national, forest. We compiled a baseline list of those species re- and international levels agreed with our findings of which liably recorded in the region and represented either by species were most threatened with extinction in both our specimen records or archived documented observations historical and contemporary data sets. (voucher images or sound recordings). The principle

Conservation Biology Volume 00, No. 0, 2014 4 Avian Extinctions in Amazonia source of specimen data came from digitized records nas (2°S, 47°W), which is 307 km south of the MRB and of study skins deposited at the Museu Paraense Em´ılio has a baseline avifauna that is nearly identical to that of Goeldi (MPEG) and from 9 North American institutions the MRB (Lees et al. 2012; Gardner et al. 2013). The 18 with data from the MRB archived on the ORNIS database catchments studied were delineated using a digital eleva- (www.ornisnet.org). The databases of many avian collec- tion model and SWAT (Soil and Water Assessment Tool) tions are undigitized, so we also conducted an exhaustive for ARCGIS 9.3 and represented a gradient of accumu- search of secondary sources to locate additional historical lated forest loss (based on classified 2010 Landsat images records (e.g., Sclater & Salvin 1867; Hellmayr 1905; Stone [Gardner et al. 2013]) from 94% (6% remaining primary 1928) from which we extracted collection dates directly forest cover) to 0% (100% forest cover). Between 7 and or used to direct targeted visits to other collections (e.g., 12 (300 m) transects were stratified (forest, nonforest) the Natural History Museum at Tring). To ascertain the across each catchment. Three point count stations were contemporary presence of species in the region, in addi- allocated to each transect (see Lees et al. [2012] and tion to specimen data we also accepted digital voucher Gardner et al. [2013] for more details on experimental images and sound recordings (Supporting Information). design and avian survey protocols). Through the compilation of data from multiple sources, We compiled a list of avian taxa classified as threat- we compiled a sighting record for each species. A full ened on the state (Par´a) (Aleixo 2006), national (Brazilian) compilation of our data sources is listed in Supporting (Machado et al. 2008), and international (IUCN) red lists Information. (IUCN 2013) (evaluations at the state and national level also considered taxa below the species level, in some cases pending taxonomic upgrades) currently or histori- Data Analyses cally occurring in the MRB. We then compared all species that we inferred to be extinct in the MRB and all species We considered 1980, the cut-off year for analysis. Species listed as threatened on state, national, and international unrecorded since 1980 were candidates for local extinc- lists with the total number of records, catchment occu- tion because the last really rigorous inventories were fin- pancy, land-use breadth (number of land uses sampled ished in the 1970s (e.g., Lovejoy 1971; Novaes 1973). from primary and secondary forest, pasture, silviculture, To infer extinction dates, we used the formulas of Solow and mechanized agriculture), and the minimum percent- (1993, 2005). These formulas assume a uniform distri- age of forest cover within each occupied catchment in bution of sightings (nonstationary Poisson, which also Paragominas. To assess potential traits of birds vulnerable assumes the records are independent). We organized the to local extinction, we compared the threats compiled records as t1 < t2 < ... < tn,wheren represents the for each species and species’ life history attributes, such number of times a species was sighted during the study as mass and forest dependency, by Birdlife International period, ordered from the earliest to latest, starting with (2013). Finally, we adapted the framework of Butchart t1 = 0. To determine if a species was likely to be ex- et al. (2006) and used it to assess the tinct, we used the formula p = (tn/T) n−1,whereT is of species either already listed or deemed to be regionally the difference between the first sighting and the target threatened based on our analyses of species persistence year 2013 (which is the endpoint of the study period that in the MRB. For species last recorded quite recently, corresponds to the present time). If p < 0.05, then the there needs to be greater confidence that the last in- species was considered likely to be extinct (Solow 1993, dividual has died before the species can be considered 2005). We used the following equation to estimate extinc- extinct. tion dates:TˆE = (n + 1/n)tn, where the expected year of extinction is TˆE and the first record is t1 (for species with at least 4 independent records). The confidence interval Results for Tˆ was calculated as T U = t /α1/n,whereα = 0.05. E E n Possible Extinctions in the MRB Because the Solow equation is heavily dependent on the initial number of sightings (tn), calculating the sight- We traced 10,147 specimens of 329 terra firma species ing rate (sensu McInerny et al. 2006) is also useful because from 8 collections from which we were able to con- it allows for greater comparability between taxa if there is struct a sighting record. These indicated that 47 terra disparity in the period of initial sighting or discovery. The firma species (14%) were unrecorded in the MRB over (T −tn) sighting rate is calculated with p = (1 − (n/tn) ). We the last 33 years, a loss of 0.28 species/year. Probable present both measures for greater confidence in our in- extinctions were inferred to have occurred over the ferred candidates for extinction. course of the entire period 1800–2000. However, more To assess the generality of extinction patterns, we com- occurred in the 20th century; 80% of candidate extinc- pared them with the results of a 2010–2011 survey inves- tions were recorded between 1900 and 1980 (Table 1). tigating patterns of avian persistence in 18 catchments (of We were able to estimate extinction probabilities for 26 approximately 5000 ha) in the municipality of Paragomi- (for which number of records was ࣙ4). Ten species were

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Table 1. Species unrecorded in the last 33 years in the metropolitan region of Belem.´

Last Estimated Upper Sighting Mean a b c d e Scientific name English common name record n tn T Solow extinction year 95% bound rate weight (g) Penelope pileata White-crested Guan 1870 2 ------1260 Aburria cujubi Red-throated Piping-Guan 1835 1 ------1407 Pauxi tuberosa Razor-billed Curassow 1959 6 124 178 0.164 - - 0.108 2813 Odontophorus gujanensis Marbled Wood-Quail 1906 7 71 178 0.004 1918 1952 0.991 314 Sarcoramphus papa King Vulture 1898 1 ------3337 Accipiter poliogaster Gray-bellied Hawk 1915 3 ------420 Accipter superciliosus Tiny Hawk 1968 6 133 178 0.233 - - 0.178 104 Harpia harpyja Harpy Eagle 1894 2 ------6550 Spizaetus melanoleucus Black-and-white Hawk-Eagle 1962 1 ------751 Spizaetus ornatus Ornate Hawk-Eagle 1812 1 ------1215 Daptrius ater Black Caracara 1848 1 ------352 Micrastur mirandollei Slaty-backed Forest-Falcon 1835 1 ------517 Micrastur semitorquatus Collared Forest-Falcon 1968 2 ------631 Psophia obscura Dark-winged Trumpeter 1922 9 87 178 0.003 1931 1956 0.000 1071 Anodorhynchus hyacinthinus Hyacinth Macaw 1812 1 ------1565 Ara macao Scarlet Macaw 1900 4 88 201 0.084 - - 0.020 1245 Ara chloropterus Red-and-green Macaw 1906 6 94 104 0.523 - - 0.491 1479 Guarouba guarouba Golden Parakeet 1848 3 ------260 lepida Pearly Parakeet 1968 4 156 201 0.468 - - 0.417 75 Touit huetii Scarlet-shouldered Parrotlet 1969 4 71 115 0.235 - - 0.150 60 Deroptyus accipitrinus Red-fan 1912 4 100 201 0.123 - - 0.046 255 Neomorphus geoffroyi Rufous-vented Ground-Cuckoo 1912 4 100 201 0.123 - - 0.046 363 Lophornis gouldii Dot-eared Coquette 1967 9 55 101 0.008 1974 1992 0.001 2 Calliphlox amethystina Amethyst Woodstar 1926 1 ------2 Piculus chrysochloros Golden-green Woodpecker 1963 6 62 112 0.052 - - 0.015 66 Celeus torquatus Ringed Woodpecker 1968 1 ------124 Hylopezus macularius Spotted Antpitta 1968 6 133 178 0.233 - - 0.178 40 Sclerurus caudacutus Black-tailed Leaftosser 1967 5 42 88 0.052 - - 0.010 38 Sclerurus rufigularis Short-billed Leaftosser 1972 18 60 101 0.000 1976 1984 0.000 22 Dendrocincla merula White-chinned Woodcreeper 1968 6 5 50 0.00 1969 1972 0.00 53 Deconychura longicauda Long-tailed Woodcreeper 1968 3 ------26 Dendrexetastes rufigula Cinnamon-throated Woodcreeper 1936 1 ------70 Berlespchia rikeri Point-tailed Palmcreeper 1935 4 34 112 0.028 1946 1993 0.001 35 Philydor ruficaudatum Rufous-tailed Foliage-gleaner 1968 1 ------27 Philydor erythrocercum Rufous-rumped Foliage-gleaner 1965 6 86 134 0.109 - - 0.000 25 Myiobius atricaudus Black-tailed Flycatcher 1968 6 96 141 0.146 - - 0.090 10 Phoenicircus carnifex Guianan Red-Cotinga 1930 10 72 95 0.083 - - 0.046 84 Gymnoderus foetidus Bare-necked Fruitcrow 1912 1 ------283 Platyrinchus platyrhynchos White-crested Spadebill 1968 9 56 101 0.009 1975 1993 0.001 13 Platyrinchus saturatus Cinnamon-crested Spadebill 1972 12 60 101 0.003 1977 1981 0.000 13 Piprites chloris Wing-barred Piprites 1965 2 ------19 Corythopis torquatus Ringed Antpipit 1972 11 124 165 0.057 - - 0.032 17 Hylophilus ochraceiceps Tawny-crowned Greenlet 1969 8 66 110 0.028 1978 2004 0.007 15 Lamprospiza melanoleuca Red-billed Pied Tanager 1965 8 130 178 0.111 - - 0.070 35 Dacnis lineata Black-faced Dacnis 1926 6 47 134 0.005 1935 1965 0.000 11 Periporphyrus erythromelas Red-and-Black Grosbeak 1905 1 ------48 Euphonia minuta White-vented Euphonia 1960 3 ------9 aOur follows the checklist of Brazilian birds compiled by the Comitˆe Brasileiro de Registros Ornitologicos´ (CBRO 2011). bNumber of records. cThe interval between the first and last record. dThe time interval between the year of the first sighting and the target year (2013). eThe p values shown are based on the Solow equation (Solow 1993, 2005). considered likely to be extinct based on the Solow equa- highly likely to be extant based on the Solow equation tion; extinction dates ranged from 1918 to 1978 (95% (Table 1). confidence intervals between 1952 and 2004, Fig. 2), and 16 species were presumed to be still extant. Of the 21 species for which it was not possible to calculate the Forest Dependency of Threatened Species extinction probability, 9 were unrecorded after 1900. We were reasonably confident that these species have be- In comparing our historical analysis with contemporary come locally extinct (Fig. 2) because all are susceptible to avian surveys in the municipality of Paragominas, we local extinction following habitat loss and hunting (e.g., found that 8 species recorded as extinct (since 1980) Peres 2000) and all are large-bodied (> 350 g) easy to in the MRB were also unrecorded in Paragominas. Thirty- survey species which are very unlikely to have remained nine species considered extinct in the MRB persisted in undetected for over a century. The sighting rate calcula- Paragominas, although 5 of these are likely to be rare tions for 26 species suggested that 17 species were likely given that they were not recorded during our compre- to be extinct in the MRB, including 8 species that were hensive 2010 survey and reported only by Portes et al.

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Figure 2. Last record, extinction date (year), and confidence intervals for 47 species unrecorded in the Metropolitan region of Bel´em, Brazil, after 1980 (gray squares, last record of species presumed extinct but for which there are insufficient records to use the Solow equation (n < 4); white triangles, last record for species considered extant based on Solow equation; black circles, date of last record for species considered extinct based on Solow equation; white circles, extinction date inferred based on Solow equation; half-filled diamond, species extant based on Solow equation and extinct based on sighting rate; half-filled circle, species extinct based on Solow equation and extant based on sighting rate; crosses, 95% confidence interval for extinct species based on Solow equation).

(2011). Eight of 11 threatened (from any list) species number of catchments occupied ranged from 1 to 15 that were still extant in the MRB were also recorded in (of 18 catchments surveyed). The number of catchments Paragominas (Supporting Information). occupied in Paragominas and the date of the last record in Forest dependency of individual threatened or extinct the MRB were weakly and positively related (Fig. 3, non- species in Paragominas (measured as the minimum per- linear exponential model r2 = 0.16; p < 0.05). Species centage forest cover at the catchment scale from which recorded in fewer catchments were more susceptible a species was recorded) ranged from 34% to 100%; the to local extinction (last recorded longer ago). Among

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in old secondary forests [>50 years] elsewhere in the MRB). Nine other species were also recorded in sec- ondary forests, and 4 species considered likely to be extinct in the MRB and listed as endangered on the IUCN list were also threatened by hunting and the wild bird trade. Thirteen of the 15 species last recorded before 1900 were either large-bodied (>1 kg) game birds, rap- tors, or psittacids of high commercial value (Supporting Information). A combined analysis of sighting records, threat status, and estimates of the ease of detection revealed 15 ex- tinct species for which we are very confident of local extinction, 19 probably extinct species, and 13 possibly extinct species for which we have lower confidence in their extinction (Fig. 4). Figure 3. Relationship between inferred extinction date (year) in the Metropolitan region of Bel´em and number of catchments occupied in Paragominas, Discussion Brazil (r2 = 0.16, p < 0.05). We found evidence for the possible local extinction of 47 terra firma species in the MRB since 1812, all of which the 47 species with a high extinction probability in the remained undetected from 1980 to 2013. Gradual local MRB, 9 were recorded once in Paragominas, indicating and regional extinctions have been reported throughout parallel patterns of rarity. However, this was not the case the Neotropics (Table 2), but we conducted the first for all species. For example, the Red-billed Pied Tanager study illustrating the long-term (>160 years) erosion of an (Lamprospiza melanoleuca) was recorded on 37 occa- Amazonian bird community. Rate of loss was estimated at sions from 12 catchments in Paragominas (Supporting 0.28 species/year in the MRB. By comparison, Robinson Information). (2001) found that Barro Colorado Island, Panama, lost 13.5% of its avifauna in 25 years (1.1 species extinc- tion/year) and Patten et al. (2010) found that Palenque, Reassessment of Species Threat Status Mexico, lost 9.5% of its avifauna in 109 years (0.21 Fifteen (31%) of the 47 species unrecorded since 1980 extinctions/year). are categorized as threatened; 10 of these species are on These results suggest that short-term studies of avian the Par´a list, 6 are on the Brazilian list, and 10 are on the extinctions from Amazonian forest landscapes may yield IUCN list (Supporting Information). Ten species listed as very conservative results because extinction debts may regionally threatened are still extant in the MRB (Support- be paid over a long period and species present in the ing Information). All 47 species we considered to have a current landscape may not be part of viable populations high probability of extinction in the MRB, together with (e.g., Brooks et al. 1999; Metzger et al. 2009). Our results the species currently considered to be endangered in Par´a therefore reinforce the critical importance of establish- (12 species), are threatened by habitat loss, degradation, ing (when historical records are available) an accurate and fragmentation, and 19 of these species were only local baseline for a given biota to avoid underestimating recorded from primary forests in Paragominas, of which levels of species losses associated with cumulative land- 3 species were found exclusively in remnant fragments use change and synergistic interactions between multi- of undisturbed forests (Dark-winged Trumpeter [Psophia ple threats (Gardner et al. 2009; Lees et al. 2012). Our obscura], Guianan Red-Cotinga [Phoenicircus carnifex], results should also be viewed through a conservative and Tawny-crowned Greenlet [Hylophilus ochraceiceps lens, given potential historical collecting biases that we rubrifrons]). Fifteen species occupied both primary and believe makes it more likely that our analysis underesti- secondary forest and 3—Scarlet Macaw (Ara macao), mated rather than overestimated change. Many species Red-and-green Macaw (Ara chloropterus), and Golden may not have been represented in the predisturbance Parakeet (Guarouba guarouba)—were also recorded in samples that constituted our baseline due to the diffi- nonforest (agricultural) areas (Fig. 3). Of the species con- culty of collecting small-bodied canopy species relative sidered threatened in Par´a, only Black-spotted Bare-eye to understory species and the fact that collecting effort is (Phlegopsis nigromaculata paraensis) was restricted to neither temporally nor spatially constant (Burgman et al. primary forest around Paragominas (although it occurs 1995; McCarthy 1998).

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High Pauxi tuberosa Penelope pileata Psophia obscura* Aburria cujubi

Odontophorus gujanensis EXTINCT Sarcoramphus papa Harpia harpyja Spizaetus ornatus* Anodorhynchus hyacinthinus* Ara macao Guarouba guarouba* Neomorphus geoffroyi Gymnoderus foetidus Periporphyrus erythromelas Accipter superciliosus Accipiter poliogaster Daptrius ater Pyrrhura lepida* Spizaetus melanoleucus Micrastur mirandollei

Hylopezus macularius PROBABLY

Dendrexetastes rufigula* Deroptyus accipitrinus EXTINCT Confidence Sclerurus caudacutus Phoenicircus carnifexG ofE Sclerurus rufigularis Hylophilus ochraceiceps E extinction Dendrocincla merula Dacnis lineata Deconychura longicauda* Platyrinchus saturatus Corythopis torquatus Piprites chloris*

Micrastur semitorquatus Calliphlox amethystina Touit huetii

Piculus chrysochloros* POSSIBLY Lophornis gouldii EXTINCT Berlespchia rikeri Celeus torquatus* Euphonia minuta Philydor erythrocercum Phylidor ruficaudatum Myiobius atricaudus Platyrinchus platyrhynchos Lamprospiza melanoleuca Low ≈30 ≈50E >100E

Number of years since last record

Figure 4. Schematic of framework illustrating how time since last record interacts with confidence of extinction (bold, globally threatened species [IUCN 2013]; asterisk, included on the regional red list). The framework can be used to determine how species can be classified locally as possibly extinct, probably extinct, or extinct (adapted from Butchart et al. [2006]).

Table 2. Long-term species loss from Neotropical forest regions.

Number of extinct species, Period (years), total species richness, no. of community regionally Species Study Region Biome years extinct (%) loss/year

This study metropolitan region of Amazonia 1812–1980, 168 47, 360, 14.5 0.28 Belem,´ Par´a, Brazil Shaw et al. 2013 Sierra de Los Tuxtlas, Central America 1973–2004, 30 12, 122, 9.8 0.40 Veracruz, Mexico Patten et al. 2010 Palenque, Chiapas, Central America 1900–2009, 109 23, 240, 9.5 0.21 Mexico Robinson 2001 Barro Colorado Island, Central America 1970–1996, 25 27, 200, 13.5 1.08 Panama Renjifo 1999 west slope, Cordillera Andes 1911–1997, 86 6, 139, 4.3 0.06 Central, Colombia Ribon et al. 2003 Vic¸osa, Minas Gerais, Atlantic Forest 1932–1999, 67 28, 221, 13 0.42 Brazil Christiansen & Pitter 1997 Lagoa Santa, Minas Atlantic Forest 1870–1987, 117 13, 107, 12.1 0.11 Gerais, Brazil

Patterns of Local Extinction in the MRB Avifauna sistent with those of previous studies (e.g., Owens & Bennett 2000), which found that large-bodied species Extinction proneness in Amazonian birds is typically are particularly extinction prone. For example, we re- linked to life history characteristics such as body size, port the purported loss of 6 large-bodied (>1 kg) species feeding behavior, and dispersal ability (Lees & Peres from the MRB, of which 4—Dark-winged Trumpeter, 2009, 2010; Stouffer et al. 2011). Our findings are con-

Conservation Biology Volume 00, No. 0, 2014 Moura et al. 9

White-crested Guan (Penelope pileata), Red-throated Woodcreeper (Deconychura longicauda zimmeri)and Piping-Guan (Aburria cujubi), and Razor-billed Curas- terrestrial solitary species such as Spotted Antpitta (Hy- sow (Pauxi tuberosa)—are game birds highly sought lopezus [macularius] paraensis), which appear intoler- after for bushmeat (e.g., Peres 2000). Eight of the large- ant even to low-intensity selective-logging activities (Lees bodied species were unrecorded after 1900. The mean & Peres 2010; Moura et al. 2013). The potential lack of mass of species that went extinct from 1800 to 1900 was cavity trees could have contributed to population col- 1772 g, in contrast to a mean of 270 g after 1901. Given lapses in the MRB because many of the species inferred this information, the most parsimonious explanation for to be locally extinct are either primary (woodpeckers) this first wave of local extinctions from the MRB is hunt- or secondary cavity nesters (e.g., forest falcons, , ing of large-bodied species for food, although local forest and woodcreepers) for which habitat may be reduced loss also began to gain momentum in the same period in selectively logged and secondary forests (e.g., Cockle and was most severe after 1880 (Vieira et al. 2007). et al. 2010; Supporting Information). Trade and persecution may also have driven some species to extinction. For example, other large-bodied The Future of the MRB Avifauna species such as Scarlet Macaw, Red-and-green Macaw, and Hyacinth Macaw (Anodorhynchus hyacinthinus) Most studies documenting long-term extinctions in for- were harvested for the wild bird trade in the MRB (Alves merly forested tropical landscapes also report on colo- et al. 2013). The same is true of the Golden Parakeet, nization events by nonforest taxa (e.g., Patten et al. 2010). which we (N.G.M. and A.C.L.) found persisting in the However, these marginal gains in new species do not neighboring fragmented landscapes of Moju, Paragomi- compensate for the losses because the few colonizing nas, and Tailˆandia but which remains a target for the species are not of conservation concern. Thus, mainte- (now illegal) wild bird trade (Alves et al. 2013). Large nance and protection of well-preserved primary forest raptors, such as Harpy Eagle (Harpia harpyja), Crested habitats is a prerequisite for both local (Moura et al. 2013) Eagle (Morphnus guianensis), and Ornate Hawk-Eagle and global avian biodiversity conservation (Gibson et al. (Spizaetus ornatus) are also particularly threatened in 2011). fragmented landscapes from hunting, which may be trig- Future records of mobile large-bodied species may gered by human–wildlife conflicts when raptors are sus- more likely represent recolonization rather than low-level pected of killing small livestock (e.g., Trinca et al. 2008). persistence throughout the survey period (examples in Many of the other probable extinctions we found Supporting Information). Large-bodied (often frugivo- were more likely related to forest loss and disturbance rous) species with high dispersal capacity are more likely than direct persecution. A wave of extinctions of smaller to be recorded as occasional vagrants or colonizing in- bodied species occurred after 1900, and the mean dividuals than small-bodied (often insectivorous) species bodyweight of species assumed to go extinct between with lower dispersal capacity (Lees & Peres 2009). Al- 1900 and 1980 was 270 g (an 85% drop in body size though this could be grounds for guarded optimism, compared with losses observed during the previous biotic impoverishment driven by fragmentation, unsus- century). This second wave of extinctions may be tainable forest management, wildfires, and hunting is still linked to habitat loss and degradation associated with ongoing in the region (Amaral et al. 2012). Given these the construction of the railway in 1883–1908 (Vieira impacts, coupled with the lack of an adequate protected et al. 2007) and the subsequent increase in human area network in the MRB, we anticipate that the number population and the size of settlements in Belem´ after the of local extinctions will continue to rise and result in construction of the Belem–Bras´ ´ılia road in the 1960s. an ever more impoverished avifauna in this biologically The disappearance of both medium and small-bodied unique corner of the world’s largest remaining tropical primary-forest dependent frugivores such as the Guianan forest. Our ability to catalog the long-term erosion of Red-Cotinga and Wing-barred Piprites (Piprites chloris biological diversity in the MRB was made possible only griseicens) is consistent with results of other studies (e.g., due to the long history of natural history research in Lees & Peres 2008; Espanola˜ et al. 2013) and may reflect the region. It is likely that similar, hitherto unrecorded, loss of food resources or access to adequate nest sites. processes of erosion and species extinction are happen- The absence of many such species was observed by early ing elsewhere in Amazonian deforestation frontiers and naturalists. For example, in 1926 J. Bond failed to find across the tropics. Red-and-Black Grosbeak (Periporphyrus erythromelas) in the MRB, remarking that it was “found only in the virgin forest at Castanhal” 50 km from Belem´ (Stone 1928). Acknowledgments Insectivorous species have also been affected dispro- portionately by habitat loss, degradation, and fragmenta- We thank the Instituto Nacional de Cienciaˆ e tion, including both flock-following under and mid-story Tecnologia—Biodiversidade e Uso da Terra na Amazoniaˆ primary-forest dependent species such as Long-tailed (CNPq 574008/2008-0), the National Environment

Conservation Biology Volume 00, No. 0, 2014 10 Avian Extinctions in Amazonia

Research Council (NE/G000816/1), the Darwin Initia- Brooks, T. M., S. L. Pimm, and J. O. Oyugi. 1999. Time lag between tive (17-023), the Coordenac¸˜ao de Aperfeic¸oamento de deforestation and bird extinction in tropical forest fragments. Con- Pessoal de N´ıvel Superior-CAPES, Lancaster University, servation Biology 13:1140–1150. Burgman, M., R. Grimson, and S. Ferson. 1995. Inferring threat from Embrapa Amazonia Oriental (SEG: 02.08.06.005.00), and scientific collections. Conservation Biology 9:923–928. The Nature Conservancy for funding and The Nature Butchart, S. H. M., A. J. Stattersfield, and T. M. Brooks. 2006. Going Conservancy for access to detailed land-use maps of the or gone: defining “Possibly Extinct” species to give a truer picture municipality. We are very grateful to all the farmers of recent extinctions. Bulletin of the British Ornithologists’ Club and landowners of Paragominas for collaborating in the 126:7–24. Christiansen, M. B., and E. Pitter. 1997. 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