The role of alien plants in the composition of fruit-eating bird assemblages in Brazilian urban ecosystems

The role of alien plants in the composition of fruit-eating bird assemblages in Brazilian urban ecosystems Juan Carlos Guix Departament de Biologia Animal (Vertebrats), Facultat de Biologia, Universitat de Barcelona. Av. Diagonal 645, 08028 Barcelona, Spain. E-mail: [email protected] Manuscript received in September 2007 Abstract Between 1985 and 2004, 91 wild fruit-eating bird species were studied in 11 urban areas of Brazil: 78 of these species were seed dispersers and 13 were seed predators. The most representative families of fruit-eating birds in these areas were: Thraupidae with 46 species, Tyrannidae with 19 species, Psittacidae with 11 species and Turdidae with 6 species. Several of these avian species (or part of their populations) are vagrants or visitors (wanderers) and migrants. At least 19 fleshy-fruiting plant species usually dispersed by birds were found growing spontaneously in urban areas: at least 8 of these were indigenous (autochthonous) to the region in which they were found, and 11 were alien (allochthonous). A total of 383 fleshy-fruiting plants were found on 321 plots: 275 (71.8%) plants belonged to autochthonous taxa and 108 (28.2%) plants belonged to alien taxa. In these plots, the fleshyfruiting plants that most successfully colonized urban environments were those belonging to autochthonous taxa, all of them small-seeded: Ficus spp. (Moraceae), Rhipsalis spp. (Cactaceae), Struthanthus spp. (Loranthaceae) and Cereus spp. (Cactaceae). The alien fleshyfruiting plant species that most successfully colonized urban environments were: Ficus microcarpa, Morus nigra (Moraceae), Eriobotrya japonica (Rosaceae) and Pittosporum undulatum (Pittosporaceae). The present study indicates that many of the non-nesting birds that visit urban areas in Brazil are frugivores-insectivores. The results strongly suggest that such birds enter built-up areas to feed on fleshy fruits produced by allochthonous species of plants, especially during winter. The major ecological consequence of fruit-eating bird movements into urban areas is that most of these bird species can transport viable seeds of alien plants in the gut and disperse them in natural and semi-natural areas. Key words: alien species, birds, fleshy fruits, frugivory, plant colonization, seed dispersal, urban ecology, Brazil. Resumen. El papel de las plantas foráneas en la composición de los ensambles de aves frugívoras en ecosistemas urbanos brasileños Entre 1985 y 2004, 91 especies de aves frugívoras fueron estudiadas en 11 áreas urbanas de Brasil: 78 de estas especies eran diseminadoras de semillas y 13 eran depredadoras de semillas. Las familias de aves frugívoras más representativas en estas áreas fueron: Thraupidae, con 46 especies, Tyrannidae, con 19 especies, Psittacidae, con 11 especies y TurOrsis 22, 2007 87-104 didae, con 6 especies. Diversas de estas especies (o parte de ss poblaciones) de aves son divagantes o visitantes y migratorias. Como mínimo 19 especies de plantas que producen frutos carnosos, normalmente dispersadas por aves, fueron encontradas creciendo espontáneamente en áreas urbanas: como mínimo 8 de ellas eran especies indígenas (autóctonas) en la región donde fueron encontradas y 11 eran foráneas (alóctonas). Un total de 383 plantas que producen frutos carnosos fueron encontradas en 321 cuadrantes: 275 (71.8%) plantas pertenecieron a taxa autóctonos y 108 (28.2%) plantas pertenecieron a taxa foráneos. En estos cuadrantes, las especies de plantas que mejor colonizaron los ambientes urbanos fueron aquellas pertenecientes a taxa autóctonos, todas ellas productoras de semillas pequeñas: Ficus spp. (Moraceae), Rhipsalis spp. (Cactaceae), Struthanthus spp. (Loranthaceae) y Cereus spp. (Cactaceae). Las especies de plantas foráneas productoras de frutos carnosos que mejor colonizaron los ambientes urbanos fueron: Ficus microcapa, Morus nigra (Moraceae), Eriobotrya japonica (Rosaceae) y Pittosporum undulatum (Pittosporaceae). El presente estudio indica que muchas de las aves no nidificantes que visitan áreas urbanas en Brasil son frugívoro-insectívoras y los resultados sugieren que estas aves entran en los pueblos y grandes ciudades para alimentarse de frutos carnosos producidos por especies de plantas alóctonas, especialmente durante el invierno. La principal consecuencia ecológica de los movimientos de las aves frugívoras hacia las áreas urbanas es que muchas de estas especies de aves pueden transportar, en el trato digestivo, semillas viables de plantas foráneas y dispersarlas en áreas naturales y seminaturales. Palabras clave: aves, Brasil, colonización de plantas, dispersión de semillas, ecología urbana, especies foráneas, frugivoria, hábitos alimentarios. Introduction Human-related disturbances have been considered the major causes of avian extinction over the last few centuries. In addition to direct persecution for various purposes (e.g., hunting for meat supply and feathers), the human impact on natural vegetation and landscape have contributed to the decline of avian populations. Nevertheless, several species of birds around the world exploit (temporarily or on a long term basis) urban landscapes that show different degrees of anthropization (Beissinger & Osborne, 1982; Dickman, 1987; Sick, 1985, 1993;). This use of urban environments has long been a subject of interest to biologists (Beissinger & Osborne, 1982; Gavareski, 1976; Leveau & Leveau, 2006; Marzluff, 2001; Marzluff et al., 2001). Urbanization usually entails major disturbances to the environment, such as large impacts on landscape, natural vegetation, soil structure and animal communities. While former elements of the ecosystems are destroyed (e.g., rivers, wetlands, rock promontories) new elements are incorporated to the landscape (e.g., building structures, allochthonous vegetation, artificial lakes, new preys and predators) (Matarazzo-Neuberger, 1995). In tropical and subtropical regions of Brazil, major threats to forest birds include habitat loss, forest fragmentation and increase of interpatch distances. The effect of urbanization on bird communities have been poorly studied in the Neotropical region. In a recent review, Chace & Walsh (2006) identified a lack of information concerning the urban effects on native communities of birds from 88 Orsis 22, 2007 J. C. Guix regions of high avian diversities, such as tropical forests. The aim of this study is to describe and discuss the role of urban areas in the feeding habits of Brazilian fruit-eating birds. Materials and methods Between 1985 and 2004, observations of bird species were conducted in 11 urban areas of Brazil located in zones of tropical and subtropical forests (Fig. 1). Bird species were identified mainly through visualization with binoculars. Some species were also photographed and/or hand-examined. Bird species that eat fleshy fruits were divided into seed dispersers (i.e., species that defecate or regurgitate seeds able to germinate away from the mother plant) and seed predators (i.e., species that destroy seeds of fleshy fruits) (Guix, 1995). Alien plants and bird assemblages in Brazil Orsis 22, 2007 89 Fig. 1. Map of the north and central zones of South America indicating the location of the cities studied (represented by dot). Cities: 1. São Paulo; 2. São José do Rio Preto; 3. São Vicente and Santos; 4. Ilhabela; 5. Salvador; 6. Cachoeira; 7. Recife; 8. Olinda; 9. Manaus; 10. Novo Airão; 11. Carvoeiro. Food and feeding observations were conducted in these urban areas. The feeding bouts were based both on direct observations of food consumption and on the examination of feces and/or regurgitations of birds. The fleshy fruits consumed by birds were divided into indigenous (I: an autochthonous species in the region of each urban area according to Hoehne et al., 1941 and Hueck, 1956, 1972) and alien ones (A: an allochthonous species introduced by humans in the region of each urban area after the 15th century, when the first Europeans arrived in the region) (Guix, 2004). Data on feeding observations included in this study are only from the urban study areas. Seedlings and juvenile plants of fleshy-fruiting species usually dispersed by birds (see Guix, 1995) were sampled in gardens, parks, old and abandoned buildings and on the street, when growing spontaneously. Also, epiphytic plants found growing spontaneously on trees, walls, roofs and other urban structures were also sampled. Each seedling and juvenile plant up to a height of 0.50 m was counted in 321 plots of 1 ×1 m. Only plots with one or more seedlings and juvenile plant were considered. For the analysis of plant composition in plots the following mathematical descriptors were used: the numerical percentage of each plant genus in the collection of plots (%N), their percentage of occurrence in the plots (%OCC), and the Probabilistic Index (PI = ΣPi2, where Pi is the number of plants belonging to a given genus “i” in one plot divided by the total number of plants found in the same plot)(Ruiz, 1985; Jover, 1989). Also, the Use Index (UI) was used to describe the dominance of each plant genus in the total sample: UI = %Ni* %Ei, where: “n” is the total number of plots, “fj” the number of plants of each genus “i” in one plot, and “f*” the number of individuals belonging to one genus “i” in relation to the total number of plots (Jover, 1989). The Probabilistic Index and the UI combines both the numerical percentage and the percentage of occurrence to assess the relative importance of each genus found. In order to make the index values independent of sample size, they were calculated as PI’ = (PI/n) ×100 (where “n” is the total number of plots), and PI’’ = (PI’/ΣPI’) ×100 to give the values in percentage. The same procedure was applied for the UI (Ruiz, 1985). To estimate the diversity of plants in each plot, two indexes were used: athe Shannon-Weaver Index (H): H = -Σpi log2 pi(Shannon & Weaver, 1963); bthe Brillouin Index (BI): BI = (1/N) (log2N! – Σlog2Ni!), where N is the total number of plants in the collection and Ni is the number of plants of a given genus “i” in a plot (see Brillouin, 1956; Hurtubia, 1973; Ruiz, 1985). The diversity of plants in the collection of plots was calculated by the same index (BI), using the Jackknife procedure (Zahl, 1977). The values of population diversity (Shannon-Weaver Index and Brillouin Index) were obtained accumulating the diversity of plants of each plot in the maEi= - log Σ(fj/ f*)2 - log (1 / n) 90 Orsis 22, 2007 J. C. Guix trix; in the case of the Brillouin Index the Jackknife procedure was used to accumulate de diversity values (Heltshe & Forrester, 1983; Jover, 1989). Since not all seedlings and juvenile plants could be identified to species level, the analysis of dominance and diversity was based on genus. Nevertheless, native species of Ficus and alien ones belonging to a same genus were considered separately. Also, when one or more species in a genus may be involved, this information is indicated. In order to improve our assessment of the role of each bird species in seed dispersal/predation patterns (e.g., seed mobility), they were divided in: nestings (N: observations on nest construction and/or incubation of eggs and rearing), migrants (M: regular encounters in more than two years of species known to migrate) and vagrants or visitors (V: occasional findings, normally of few individuals, of species known to be wanderers). More than one category can appear associated with one species (e.g., nesting and migrant). This means that this species was detected both through nesting individuals or populations in the area, and also through migrant individuals or populations, which are not necessarily the same as the nesting populations (e.g., juvenile individuals). These categories were based on the observations performed in the 11 urban areas during the present study and on data from other authors who performed field studies in areas or regions located around or near these urban areas (see Borges et al., 2001; Isler & Isler, 1987; Mendonça-Lima & Fontana, 2000; Olmos, 1996; Sick, 1993; Willis, 1979; Willis & Oniki, 1981). “Migrant” and “vagrant/visitor” were considered as provisional categories for some species, since few studies with long-term bird banding programs were available in the study areas. Ecological studies of urban effects on avifauna have considered an urbanized center as a concentration of humans in residential and industrial settings containing more than 2500 people (see Chace & Walsh, 2006). Nevertheless, many Amazonian urban areas are smaller than eastern and southeastern Brazilian cities and towns. Thus, observations made at the small Amazonian village of Carvoreiro (located on the right margin of the Middle Negro river) was also included, due to the large number of fruit-eating bird species seen eating alien fruits in this area. Study areas The urban areas were chosen because of their location (both in relation to the latitude and longitude), their size (e.g., from small villages and town to large cities), and characteristics (coastal and inland areas), covering a wide range of altitudes: from sea level to 800 m high (Fig. 1). São Paulo megalopolis The city of São Paulo is located in south-eastern Brazil (23º 33’ S, 46º 39’ W; Altitude 650-800 m), and has about 11 million habitants. During the urban growth of São Paulo, this and other neighboring cities merged to form a megalopolis that hosts more than 18 million people. This megalopolis, locally called “A Grande São Paulo” (i.e., the Large São Paulo) includes several cities and urban areas of Alien plants and bird assemblages in Brazil Orsis 22, 2007 91 the municipalities of Osasco, Taboão da Serra, Diadema, São Bernardo do Campo, São Caetano do Sul, Santo André da Borda do Campo, Mauá and Guarulhos. Beside the city of São Paulo, there are two protected parks: the Parque Estadual da Cantareira, an area of 10000 ha mainly covered by secondary subtropical forests; and the Parque Estadual das Fontes do Ipiranga (former Parque do Estado), an area of 542 ha, which includes around 300 ha of a secondary forest composed by floral elements of both the Brazilian Atlantic rainforest and the subtropical forests (sensu Hueck, 1956; 1972). Both protected areas of native forests (separated from each other by 21 km of a continuous urban area) were not included in this study. São José do Rio Preto A city of about 330000 inhabitants located in north-western São Paulo state (20º 49’ S, 49º 22’ W ; Altitude: 489 m). The city is surrounded by farms (especially with sugarcane plantations), small forest fragments, woodlots, pastures, and Eucalyptus spp. plantations. São Vicente and Santos São Vicente (23058’ S, 46023’ W; Altitude: 2-30 m ) and Santos (23056’ S, 46020’ W; Altitude: 2-35 m) are two connected cities located on the eastern coast of the São Paulo state, in south-eastern Brazil. They are surrounded by some mangroves and mountains covered by the remains of secondary Atlantic rainforest, small banana plantations and several roads. These two cities together have about 740000 inhabitants. Ilhabela Town located at the São Sebastião Island in the northern coast of the São Paulo state (23050’ S, 45020’W; altitude: 2-60 m), south-eastern Brazil. This 33593 ha island is separated from the continent by a 1.76 km sea channel and it is located 5 km from the Serra do Mar, a mountain range of the coast of south-earten Brazil. The town of Ilhabela is beside the Parque Estadual de Ilhabela, a 25981 ha protected area mainly covered by native secondary Atlantic rainforest. Due to tourism, the population varies from 26000 (during winter) to 85000 (during summer). Salvador Large coastal city of more than 2600000 inhabitants located in eastern Bahia state (13004’ S; 38031’ W; Altitude: 2-60 m; NE Brazil), surrounded by pastures, plantations, small native forest fragments and woodlots. Cachoeira A town located 110 km inland from Salvador (12036’ S; 38058’ W; Altitude: 50 m; Altitude), north-eastern Brazil, on the left margin of the Paraguaçu river. This 92 Orsis 22, 2007 J. C. Guix town of about 16000 inhabitants is surrounded by extensive pastures, small native forests fragments and scant riparian vegetation. Recife Large coastal city of about 1400000 inhabitants located in eastern Pernambuco state (08004’ S; 34055’ W; Altitude: 4 m; Altitude), north-eastern Brazil. It is surrounded by plantations, pastures, some small native forest fragments, small farms and mangroves. There are also some small remnant mangroves in the city. Olinda A coastal city located in eastern Pernambuco state (08001’ S; 34051’ W; Altitude: 2-16 m), north-eastern Brazil, 6 km from center of the city of Recife. This city has about 350000 inhabitants and it is surrounded by native secondary forest fragments and farms with small pastures and plantations. As Olinda and Recife today are connected by urban areas, they could also be considered as part of a same large urban complex. Manaus A large city of about 1600000 inhabitants located on the left margin of the Negro river, close to it confluence with the Solimões river (03004’ S; 59001’ W; Altitude: 35-47 m), state of Amazonas (NW Brazil). This city is surrounded by large native forest fragments (e.g., the Reserva Florestal Adolpho Ducke, a 10072 ha protected Amazonian terra firme forest), large extensive forests and farmlands with pastures. The Reserva Florestal Adolpho Ducke and the Mata do Campus da Universidade Federal do Amazonas (a 546 ha of native forest located in the city) were not included in the present study. Novo Airão A town of about 7000 inhabitants located on the right margin of the Negro river (02040’ S; 61000’ W; Altitude: 37-42 m ), 200 km from Manaus, state of Amazonas (NW Brazil). This town is surrounded by extensive forests (mainly terra firme and igapó forests). Carvoeiro A village of about 800 inhabitants located on the right margin of the Negro river (01021’ S; 62007’ W; Altitude: 40-42 m ), close to its confluence with the Branco river, state of Amazonas (NW Brazil). This village is surrounded by large extensive forests (mainly terra firme and igapó forests). See also LANDSAT TM satellite images of these cities and towns and surrounding areas at EMBRAPA 2000-2003, and in GOOGLE-MAPS). Alien plants and bird assemblages in Brazil Orsis 22, 2007 93 94 Orsis 22, 2007 J. C. Guix Table 1. Bird species that disperse seeds of fleshy fruits in 11 urban areas of Brazil. 1. São Paulo; 2. São José do Rio Preto; 3. São Vicente and Santos; 4. Ilhabela; 5. Salvador; 6. Cachoeira; 7. Recife; 8. Olinda; 9. Manaus; 10. Novo Airão; 11. Carvoeiro. Categories: N: nestings (observations on nesting construction and/or incubation of eggs in these and other Brazilian urban areas), M: migrants (regular encounters in more than two years of species known to migrate in these and other Brazilian urban areas), V: vagrants or visitors (occasional findings, normally of few individuals, of species known to be wanderers in these and other Brazilian urban areas). Family, species and categories 1234567891011 CAPITONIDAE: Capito niger, V x x PICIDAE: Celeus elegans, V x Celeus flavus, V x Melanerpes cruentatus, N, V x x TYRANNIDAE: Elaenia flavogaster, V x x x Elaenia cf. parvirostris, V x Elaenia sp.3 x Elaenia sp.4 x Elaenia sp.5 x Empidonomus varius, V x x xxxx Megarynchus pitanga, V xxxxx Mionectes cf. oleagineus, V x x Myiarchus cf. swainsoni, M x x Myiarchus sp.2 x Myiarchus sp.3 x Myiodynastes maculatus, Mxxxxxx Myiozetetes cayenensis, V x xxx Myiozetetes similis, V xx x xxx x Pitangus sulphuratus, N xxxxxxxxxxx Tyrannus melancholicus, N, V xxxxxxxxxx Tyrannus savana, M x x xxx Tityra cayana, V x x x x x Tityra inquisitor, V x x COTINGIDAE: Laniisoma elegans, V x x Phibalura flavirostris, V x x TURDIDAE: Turdus albicollis, V xxx xxx Turdus amaurochalinus, N, V xxxxxx Turdus flavipes, N, V x x Turdus fumigatus, V xxxxx Turdus leucomelas, V x x x x x Turdus rufiventris, N, V xxxxx xx COEREBIDAE: Coereba flaveola, N, V x x x x Alien plants and bird assemblages in Brazil Orsis 22, 2007 95 Family, species and categories 1234567891011 THRAUPIDAE: Chlorophanes spiza, V x Chlorophonia cyanea, V x Dacnis cayana, V x x xxx Dacnis lineata, V x Euphonia cayennensis, V x Euphonia chalybea, V x Euphonia chlorotica, V x x x x x Euphonia chrysopasta, V x x Euphonia minuta, V x x Euphonia musica, V x Euphonia pectoralis, V xx Euphonia plumbea, V x x Euphonia rufiventris, V x Euphonia violacea, V x x x x Hemithraupis flavicollis, V x x Hemithraupis guira, V x Hemithraupis ruficapilla, V x Nemosia pileata, V x x Pipraeidea melanonota, V x x Piranga flava, V x Piranga rubra, V x x Ramphocelus carbo, V x xxx Ramphocelus bresilius, M, V x x x Tachyphonus coronatus, V x x x Tachyphonus cristatus, V x Tachyphonus luctuosus, V x Tachyphonus phoenicius, V x Tachyphonus rufus, V x x Tachyphonus surinamus, V x x Tangara cayana, V xx xxxx xx Tangara chilensis, V x x Tangara cyanocephala, V x Tangara cyanoventris, V x Tangara mexicana, V x Tangara peruviana, V x x Tangara punctata x Tangara seledon, V xxx Tangara varia, V x Tangara velia, V x x Tersina viridis, V x x Thlypopsis sordida xx Thraupis cyanoptera, V x x Thraupis episcopus, V xxx Thraupis ornata, V x xxx Thraupis palmarum, V x xxx xxxx Thraupis sayaca, N, V xxxxxxxx Acknowledgements I thank Sofia Cruz Alves Guix, Isabel Cruz Alves and Eduardo Mateos for their support and help. 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