DIVERSIDADE BETA DE PÁSSAROS (Passeriformes, Linnaeus, 1758) NA AMAZÔNIA MERIDIONAL

cab Ciência Animal Brasileira Ciênc. anim. bras. 1518-2797 1809-6891 Universidade Federal de Goiás Resumo Estimar a diversidade biológica e entender as mudanças acerca da especialização ecológica das espécies entre habitats em uma organização espacial é importante. A alta diversidade beta reflete numa pequena distância entre locais, mas que contêm alta incorporação de espécies, que geralmente possuem grande sensibilidade e não estão adaptadas ao estreitamento causado pelo desmatamento ou a presença de queimadas por ações antrópicas. Investigou-se a diversidade beta de pássaros (Passeriformes) na Amazônia Meridional em paisagens com coberturas vegetais mais heterogêneas: habitats de floresta alagada (iguapó), floresta de terra firme e buritis através de censo de audições, observações e fotografias. Marcaram-se pontos em equidistantes transectos. Em todo o estudo foram amostrados 126 pontos. Identificaram-se 148 espécies de pássaros da ordem Passeriformes, distribuídas em 27 famílias. A classificação sobre os habitats de forrageamento resultou em 97% das espécies que forrageiam em iguapó, 77% em floresta de terra firme e 18,1% em buritis, apenas 18% forragem nos três habitats. A análise de ordenação mostrou quais espécies estão mais relacionadas com cada habitat, a análise para a Beta diversidade Global certificou que a diversidade beta é alta (Whittaker: 7,7405). Como era esperado encontrou-se o mesmo padrão quando foi utilizada a medida de dissimilaridade por pares. Na análise de agrupamento, pode-se ver claramente a influência da distância espacial, mas em alguns pontos isto não ocorre. Estes pontos indicam o momento de transição e substituição de espécies. Na maioria dos casos, a influência da distância espacial é predominante e confirmou-se na análise de Mantel parcial. A influência da distância espacial entre o índice de dissimilaridade (diversidade beta) foi significante (r:0,0608, p:0,0049). Esta composição de espécies organizadas em pequenas populacões locais mas com alta diversidade beta não pode ser exposta ao desmatamento, corte seletivo de madeira e a caça furtiva como tem acontecido. Este estudo provê informações de habitats específicos de alta diversidade beta que estão correndo risco na estabilidade de suas populacões em face às mudanças ambientais contínuas nesta área de estudo. Introduction Ecologists have long been curious to understand how biological diversity changes with the environment, in particular species specialized in different ecologies in spatially-organized habitats(1). The smaller fraction of regional gamma diversity corresponds to the local alpha diversity and represents the number of species within small areas of similar and uniform habitats. Beta diversity represents the rate of species variation (turnover rate) between habitats(2). Beta diversity frequently measures the substitution of species without considering the relative abundance(3). However, the inclusion of the relative abundance or frequency index allows a more informative evaluation of species diversity, especially when it varies between habitats(4). Studies that compare variation in the number of species between local habitats are necessary to determine patterns, particularly in places in the world that are enriched in bird species(5). In these areas, deforestation and controlled burnings for agricultural expansion along with hunting pressure are decreasing species richness. High beta diversity along an environmental gradient reflect the specialization of species in habitats. The quantification of this parameter can be used to design strategies for protection of bird diversity in these areas(6). A high beta diversity within small distances reflects the presence of abundant species between neighboring habitats, which generally are locally specialized and highly susceptible to anthropogenic action(3). The spatial variation of birds composition with types of habitats is rarely measured, but it has shown to be important to define the area needed to protect some species(3). There are some studies on the changing of the composition of animal communities along altitudinal gradients, but beta diversity in tropical systems is particularly misunderstood(7,8). According to these studies, a gradual change in composition occurs with altitude, although some results may have been affected by the sampling method(9). Instead of using the total animal community, quantification of beta diversity using a specific taxonomic group, such as birds (order Passeriformes), may be easier in terms of research planning(10). Despite the apparent capacity for dispersion, many factors seem to influence variation of bird diversity or delimit their geographic distribution, for example the presence of rivers(4). Habitats created by rivers, such as floodplain forest, flooded habitats, and habitats with fluctuations in vegetation, present about 15% regional birds, suggesting that watercourses may have had a relevant role in the origin of different bird species in the current region of Southern Amazon. The present study investigated the change in the composition of bird species of the order Passeriformes along gradients in the Alto-Guaporé region, Southern Amazon, a region that presents an elevated richness of birds and has a constant substitution of species due to a high diversity of environments. We aimed to answer two questions: Are spatially closed habitats more similar in species composition (beta diversity)? Are there differences in species richness among the type of sampled habitats (flooded forest, dry forest, and marsh palm with palm tree fruits)? We used the observed patterns of variation in species composition obtained within a bird community and explored possible implications for conservation planning. Methods This study was performed from December 2011 to September 2012, in three large localities (A,B,C) in the region of Alto-Guaporé in Southern Amazon, a region characterized by a heterogeneous vegetation cover (180879.94S, 8331318.14W between 780708.00S, 8507364W; see Fig.1) Figure 1 Habitats sampled in three locations (A, B, C) in Alto-Guapore region Southern Amazon We sampled three types of local habitats: marsh palm, dry forest, and flooded forest. The marsh palms are habitats of planes in Southern Amazon with riparian areas dominated by Mauritia flexuosa, flooded during the rainy period and permanently humid in the dry periods (n: 18 points). In the dry forest there is no rainfall, the height of trees fluctuates between 30 and 60 m, with closed canopy and thick bush (n: 72 points). Flooded habitats occur along the banks of the rivers Alegre, Verde, and Guaporé. These habitats are always flooded and the trees present a maximum height of 20 m with lianas and aquatic plants, and without sub-woods (n: 36 points). The census procedures included the most efficient hearing census(11), and observational census with the utilization of binoculars and photographic equipment. Identification of each foraging bird species was accomplished with the collected photographs and recordings. We also referred to specific bibliography to associate the diet of each bird species with the food available in each sampled habitat(11-18), so that we could make inferences on each foraged habitat per bird species. We used the quantitative lifting method (adapted from Blondel et al.)(19). We sampled points in transects equidistant 5 km from each other. Each transect had six points located 200 m apart (this distance was adequate to avoid juxtaposition of territory between most species and allowed us to cover all habitats). In total, 126 points were sampled. The recordings in each point were done using audio digital equipment (96KHz), for 15 minutes during the morning (period of the day when birds are most active), three times in different days. The sampling effort consisted of 63 days of census and 31 hours and 50 minutes of recordings covering approximately 700 km in length, in total. The vocalizations were then edited and the species identified, and finally revised by a bird specialist (records were deposited in the Laboratory of Mammalogy, UNEMAT, Brazil). To investigate the presence of clustering of species relative to the type of sampled habitat, the PCA method was applied (Principal Components Analysis is a statistical procedure that uses an orthogonal transformation to convert a set of observations of possibly correlated variables into a set of values of linearly uncorrelated variables called principal components). We calculated the global β diversity to measure diversity between the sampled habitats(2). The Index quality of Jaccard (cc), a matrix of presence and absence for a dataset, represents the macrostructure of species distributed between the habitats, although application is restricted to habitats with more than seven species. This Index was calculated with the following formula: cc= c/ (a+b+c)*100(1), or cc=c/ (A+B-c)*100(2) where: “a” is the number of species unique to sample 1, “b” is the number of specie unique to sample 2, “c” is the number of species common to samples 1 and 2, “A” is the total number of species in sample 1, and “B” is the total number of species in sample 2. The distance values ​​are plotted as similarity dendograms, the lower the index the less the similarity, created through the UPGMA (Unweighted Pair Group Method with Arithmetic Mean). The correlation between two matrices of dissimilarity was evaluated: one matrix of spatial distance (Euclidean) and the other one of species dissimilarity (Bray-Curtis) utilized the Mantel Test (Number of permutatitons: 999) (20). All analyzes were performed using R version 2.14.0.2011 program(21). Results A total of 148 species of birds (order Passeriformes) were identified and distributed in 27 families. Of these, 97% (n= 145) of the species foraged in flooded forests, 77% (n= 114) in dry forests, and 18.91% (n= 28) in marsh palm. Only 18% (n= 27) of the bird species foraged in all three habitats. The habitat with the highest species richness was the flooded forest(7) (Table 1). The value of species richness per habitat and sampling areas can be seen in Table 2. The ordination showed that most species are highly associated with a habitat, for instance, Mimus saturninus is mainly observed within the flooded forest habitat, and Empidonomus varius, Onychorhynchus coronatus, Thamnomanes caesius, Myrmotherula menetriesii, and Dysithamnus mentalis in the dry forests (Figure 2). The analysis of the global beta diversities in total showed that substitution of species is predominant (Whittaker: 7.7405, Harrison: 0.14334, Cody: 554.5, Routledge: 0.700, Wilson-Shmida: 32.97, Mourelle: 0.610, Harrison2: 0.024, Williams: 0.5714). These values indicate that beta diversity is high. As expected, we found the same pattern when applying the measure of pairwise dissimilarity. In the cluster analysis (Figure 3), the effect of spatial distance is clear because in groups 1 and 2 the habitats closer to each other are very similar (according to the Jaccard similarity index; r= 0.872, p = 0,002). This is not observed with the points of groups 3 and 4; these points corresponded to the moment of transition and substitution of species. However, in the majority of cases, the influence of spatial distance was confirmed with the partial Mantel analysis. The influence of spatial distance on the dissimilarity index (beta diversity) was significant (Mantel statistic r: 0.0608, p (value): 0.0049) (Figure 4). Table I Composition of the list of birds (order Passeriformes) in Alto-Guapore region, Southern Amazon 2012 Name Taxon Passeriformes (order) Popular Name in Brazil English Name Habitats Thamnophilidae Microrhopias quixensis papa-fomiga-de-bando dot-winged antwren dry floo Myrmotherula axillaris choquinha-de-flanco- branco white-flanked antwren ma dry floo Myrmotherula menetiesii choquinha-de-garganta-cinza gray antwren ma dry floo Fomicívora grisea papa-formiga-pardo white-fringed antwren dry floo Thamnomanes caesius ipccuá cinereous antshrike ma dry floo Dysithamnus mentalis choquinha-lisa plain antvireo ma dry floo Herpsilochmus longirostris chorozinho-de-bico-comprido large-billed antwren dry floo Thamnophilus torquatus choca-de-asa-vermelha rufous-winged antshrike dry floo Thamnophilus schistaceus choca-de-olho-vermelho plain-winged antshrike dry floo Thamnophilus stictocephalus choca-de-natterer natterer's slaty-antshrike dry floo Thamnophilus aethiops choca-lisa white-shouldered antshrike dry floo Thanmophilus amazonicus choca-canela amazonian antshrike dry floo Taraba major choró-boi great antshrike dry floo Hypocnemoides maculicauda solta-asa band-tailed antbird dry floo Sclateria naevia papa-formiga-do-igarapé silvered antbird dry floo Myrmoborus myotherinus fonnigueiro-dc-cara-pma black-faced antbird ma dry floo Pyriglena leuconota papa-taoca white-backed fire-eye dry floo Cercomacra nigrescens chororó-negro blackish antbird dry floo Hypocnemis ochrogyna cantador-ocráceo rondonia warbling-antbird dry floo Willisornis poecilinotus rendadinho common scale-backed antbird dry floo Phlegopsis nigromaculata mãe-de-taoca black-spotted bare-eye dry floo Melanopareiidae Melanoparéia torquata tapaculo-de-colarinho collared crescentchest ma dry floo Formicariidae Formicarius colma galinha-do-mato rufous-capped antthrush dry floo Dendrocolaptidae Dendrocincla fuliginosa arapaçu-pardo plain-brown woodcreeper dry floo Sittasomus griseicapillus arapaçu-verde olivaceous woodcreeper dry floo Campylorhamphus trochilirostris arapaçu-beija-flor red-billed scythebill dxy floo Dendroplex picus arapaçu-de-bico-branco straight-billed woodcreeper dxy floo Xenopidae Xenops rutilans bico-virado-carijó streaked xenops dry floo Furnariidae Furnarius rufus joão-de-barro rufous hornero dry floo Certhiaxis cinnamomeus curutié yellow-chinned spinetail dry floo Synallaxis frontalis petrim sooty-fronted spinetail dry floo Synallaxis scutata esstrelinha-preta ochre-cheeked spinetail ma dry floo Pipridae Neopelma pallescens fruxu-do-cerradão pale-bellied tyrant-manakin dry floo Manacus manacus rendeira white-bearded manakin dry floo Heterocercus linteatus coroa-de-fogo flame-crowned manakin dry floo Machacropterus pyrocephalus uirapuru-cigarra fiery-capped manakin dry floo Xenopipo atronitens pretinho black manakm dry floo Oxyruncidae Oxyruncus cristatus araponga-do-horto sharpbill dry floo Onychorhynchidae Onychorhynchus coronatus maria-leque royal flycatcher ma dry floo Terenotriccus erythurous papa-moscas-uirapuru ruddy-tailed flycatcher dry floo Tityridae Schiffomis virescens flautim greenish schiffomis dry floo Schiffornis turdina flautim-marrom thrush-like schiffomis floo Tytyra inquisitor anambe-branco-de-bochecha-parda black-crowned tityra ma dry floo Tityra cayana anambé-branco-de-rabo-preto black-tailed tityra ma dry floo Tityra semifasciata anambé-branco-de-máscara-negra masked tityra floo Pachyramphus viridis caneleiro-verde greeu-backed becard ma dry floo Pachyramphus polychopterus caneleiro-preto white-winged becard dry floo Pachyramphus validus caneleiro-de-chapéu-preto crested becard ma dry floo Cotingidae Lipaugus vociferans cricrió screaming piha floo Gymnoderus foetidus anambé-pombo bare-necked fruitcrow floo Cotinga cayana anambé-azul spangled cotinga dry floo Cephalopterus omatus anambé-preto amazonian umbrellabird floo Platyrinchidae Platyrinchus mystaceus patinho white-throated spadebill dry floo Rhynchocyclidae Mionectes oleaginous abre-asa ochre-bellied flycatcher floo Corythopis delalandi estalador southern antpipit dry floo Tolmomyias sulphurescens bico-chato-de-ordha-preta yellow-olive flycatcher dry floo Todirostrum cinereum ferreirinho-relógio common tody-flycatcher ma dry floo Hemitriccuss margaritaceiventer sebinho-de-olho-de-ouro pearly-vented tody-tyrant ma dry floo Tyrannidae Inezia inornata alegrinho-do-chaco plain tyrannulet dxy floo Camptostoma obsoletum risadinha southern beardless-tyranuulet floo Elaenia flavogaster guaracava-de-barriga-amarela yellow-bellied elaenia dry floo Elaenia chilensis guaracava-de-crista-branca chilean elaenia dry floo Elaenia parvirostris guaracava-de-bico-curto small-billed elaenia dry floo Elaenia chiriquensis chibun 1esser elaenia dry floo Myiopagis caniceps guaracava-cinzenta gray elaenia dry floo Arttila cinnamomeus tinguaçu-ferrugem cinnamon attila dry floo Attila bolivianus bate-pára dull-capped attila floo Attila spadiceus captião-de-saira-amarelo bright-rumped attila floo Ramphotrigon ruficauda bico-chato-de-rabo-vermelho rufous-tailed flatbill dry floo Miyiarchus swainsoni irre swamson's flycatcher dry floo Sirystes sibilator gritador sirystes floo Casiomis rujus maria-ferrugem rufous casiornis dry floo Pitangus sulphuratus bem-te-vi great kiskadee floo Philohydor lector bentevizinho-do-brejo lesser kiskadee dry floo Machetornis rixosa suiriri-cavaleiro cattle tyrant floo Tyrannopsis sulphurea suiriri-de-garganta-rajada sulphury flycatcher floo Myiozetetes cayanensis bentevizinho-de-asa-ferrugínea rusty-margined flycatcher dry floo Tyrannus albogularis suiriri-de-garganta-branca white-throated kingbird ma dry floo Tyrannus savanna tesourinha fork-tailed flycatcher ma dry floo Griseotyrannus aurantioatrocristaus peitica-de-chapéu-preto crowned slaty flycatcher dry floo Empidonomus varins peitica variegated flycatcher dry floo Pyrocephalus rubinus príncipe vermilion flycatcher dry floo Arundinicola laucocephala freirinha white-headed marsh tyrant dry floo Lathrotriccus euleri enferrujado euler's flycatcher dry floo Vireonidae Vireo olivaceus juruviara-boreal red-eyed vireo ma dry floo Corvidae Cyanocorax cyanomelas gralha-do-panranal purplish jay dry floo Cyanocorax chrysops gralha-picaça plush-crested jay ma dry floo Hirundinidae Stelgidopteryx ruficollis andorinha-serradora southem rough-winged swallow floo Progne tapera andorinha-do-campo brown-chested martin floo Progne chalybea andorinha-doméstica-grande gray-breasted martin dry floo Tachycineta albiventer andorinha-do-rio white-winged swallow dry floo Riparia riparia andorinha-do-barranco bank swallow ma dry floo Troglodytidae Troglodytes musculus corruirá southern house wren dry floo Campylorhynchus turdinus catatau thrush-like wren dry floo Pheugopedius genibarbis garrinchão-pai-avó moustached wren floo Cantorchilus leucotis garrinchão-de-barriga- vermelha buff-breasted wren dry floo Cantorchilus guarayanus garrincha-do-oeste fawn-breasted wren dry floo Donacobiidae Donacobius atricapilla japacanim black-capped donacobius floo Polioptilidae Ramphocaenus melanurus bico-assovelado long-billed gnatwren dry Polioptila dumicola balança-rabo-de-máscara masked gnatcatcher floo Turdidae Turdus fumigatus sabiá-da-mata cocoa thrush dry floo Turdus rufiventrís sabiá-laranjeira rufous-bellied thrush floo Mimidae Mimus saturnimus sabiá-do-campo chalk-browed mockingbird dry floo Passerellidae Arremon taciturmus tico-tico-de-bico-preto pectoral sparrow dry floo Icteridae Psarocolius decumanus japu crested oropendola floo Procacicus solitaries iraúna-de-bico-branco solitary black cacique dry floo Cacicus haemorrhous guaxe red-rumped cacique dry floo Cacicus cela xexéu yellow-rumped cacique dry floo Icterus pyrrhopterus encontro vaiiable oriole floo Icterus croconotus joão-pinto orange-backed troupial dry floo Gnorimopsar chopi gmúna chopi blackbird dry floo Ambtyramphus holosericeus cardeal-do-banhado scarlet-headed blackbird floo Agelastieus cyanopus carretão unicolored blackbird ma dry Molothrus oryzivorus traúna-grande giant cowbird dry floo Molothrus bonaríensis vira-bosta shiny cowbird dry floo Thraupidae Coereba flaveola cambacica bananaquit dry floo Saltator maximus tempera viola buff-throated saltator nm dry floo Saltator coerulescens sabiá-gongá grayish saltator dry floo Saltator similis trinca-ferro-verdadeiro green-winged saltator floo Saltator grossus bico-encarnado slate-colored grosbeak dry floo Nemosia pileata saira-de-chapéu-preto hooded tanager dry floo Thlypopsis sordida sai-canário orange-headed tanager floo Ramphocelus carbo pipira-vermelha silver-beaked tanager floo Lanio versicolor pipira-de-asa-branca white-winged shriketanager ma dry floo Tangara gyrola saíra-de-cabeça-castanha bay-headed tanager floo Tangara chilensis sete-cores-da-amazônia paradise tanager floo Tangara sayaca sanhaçu-cinzento sayaca tanager dry floo Tangara palmarum sanhaçu-do-coqueiro palm tanager ma dry floo Tangam nigrocincta saíra-mascarada masked tanager floo Schistochlamys melanopis sanhaçu-de-coleira black-faced tanager ma dry floo Paroaria capitate cavalaria yellow-billed cardinal dry floo Daenis cayana sai-azul blue daenis dry floo Cyanerpes cyaneus saíra-beija-flor red-legged honeycreeper floo Chlorophanes spiza saí-verdc green honeycreeper floo Hemithraupis flavicollis saíra-galega yellow-backed tanager dry floo Conirostrum speciosum figuinha-de-rabo-castanho chestnut-vented conebill dry floo Sicalis flaveola canário-da-terra-verdadeiro saffron finch dry Volatinia jacarina tiziu blue-black grassquit ma dry floo Sporophila collaris coleiro-do-brcjo rusty-collared seedeater floo Sporophila lineola bigodinho lined seedeater floo Sporophila nigricollis baiano yellow-bellied seedeater floo Sporophila boitvreuil caboclinho cooper seedeater floo Sporophila angolensis curio chestnut-bellied seed-finch dry floo Cardinalidae Piranga flava sanhaçu-de-fogo hepatic tanager floo Pheucticus aureeventris rei-do-bosque black-backed grosbeak ma dry floo Fríngillidae Euphonia chlorotica fim-fim purple-throated euphonia ma dry floo Euphonia violacea gaturamo-verdadciro violaceous euphonia dry floo Family 27 Species 148 Legend: Habitats - ma: marsh palm, dry: dry forest, floo: flooded forest; Table II Characteristics of the sampling areas. Latitude and longitude are shown in UTM Codemap Habitnt Areas Latitude Longitude Passeriformes richness 1 Flooded forest A 180925 8331295 42 2 Flooded forest A 181142 8331279 41 3 Flooded forest A 181372 8331224 50 4 Flooded forest A 181021 8331896.89 20 5 Dry forest A 181299 8331786 24 6 Dry forest A 181531 8331695 1 7 Flooded forest A 181298 8333552 63 8 Flooded forest A 181210 8333807 41 9 Flooded forest A 181133 8334009 48 10 Flooded forest A 180970 8334329 40 11 Dry forest A 180869 8334506 34 12 Dry forest A 180743 8334696 34 13 Flooded forest A 180507 8335421 30 14 Flooded forest A 18O859 8335484 21 15 Flooded forest A 181109 8335564 19 16 Flooded forest A 181345 8335637 0 17 Flooded forest A 181644 8335637 1 18 Flooded forest A 181916 8335643 0 19 Marsh palm A 185524.73 8334058.32 3 20 Marsh palm A 185483 8334233 6 21 Marsh palm A 185408 8334423 9 22 Marsh palm A 185274 8334561 13 23 Marsh palm A 185131 8334699 9 24 Marsh palin A 184996 184996 1 25 Marsh palm A 186507.2 8333914.13 2 26 Marsh palm A 186719 8333932 9 27 Marsh palm A 186719 8333932 12 28 Marsh palm A 187144 8334029 7 29 Marsh palm A 187354 8334066 5 30 Marsh palm A 187554 8334110 2 31 Marsh palm A 185494.87 8333830.27 1 32 Marsh palm A 185700 8333887 9 33 Marsh palm A 185901 8333956 9 34 Marsh palm A 186077 8334058 8 35 Marsh palm A 186249 8334220 5 36 Marsh palm A 186402 8334340 2 37 Dry forest A 819055.33 8359824.1 14 38 Dry forest A 818975 8359651 9 39 Dry forest A 818817 8359468 4 41 Dry forest A 818493 8359114 7 42 Dry forest A 818255 8358369 8 43 Dry forest A 811167.56 8359219.72 9 44 Dry forest A 811318 8359025 9 45 Dry forest A 811433 8358841 6 46 Dry forest A 811602 8358642 2 47 Dry forest A 811854 8358500 2 48 Dry forest A 812095 8358369 5 49 Dry forest A 810624.6 8356568.87 8 50 Dry forest A 810867 8356679 7 51 Dry forest A 811116 8356721 1 52 Dry forest A 811397 8356733 1 53 Flooded forest A 811692 8356753 4 54 Flooded forest A 811981 8356764 3 55 Dry forest B 785583 8420492 13 56 Dry forest B 785329 8420504 4 57 Dry forest B 785110 8420518 1 58 Dry forest B 784857 8420483 3 59 Dry forest B 784609 8420485 3 60 Dry forest B 784418 8420524 2 61 Dry forest B 786562.51 8423589.41 6 62 Dry forest B 786356 8423564 1 63 Dry forest B 786159 8423565 2 64 Dry forest B 785941 8423609 5 65 Dry forest B 785736 8423655 4 66 Dry forest B 785535 8423743 3 67 Dry forest B 789791.98 8424305.24 3 68 Dry forest B 789985 8424198 0 69 Dry forest B 790212 8424129 3 70 Dry forest B 790422 8424038 2 71 Dry forest B 790681 8423946 5 72 Dry forest B 790951 8423856 3 73 Dry forest B 784229.14 8432586.27 2 74 Dry forest B 784437 8432581 4 75 Dry forest B 784660 8432583 1 76 Dry forest B 784888 8432615 3 77 Dry forest B 785113 8432621 1 78 Dry forest B 785331 8432631 1 79 Dry forest B 784048.69 8433618.56 2 80 Dry forest B 784208 8433773 4 81 Dry forest B 784428 8433825 2 82 Dty forest B 784658 8433875 0 83 Dry forest B 784878 8433895 2 84 Dry forest B 785122 8433926 0 85 Dry forest B 777628.65 8440405.58 3 86 Dry forest B 777927 8440412 4 87 Dry forest B 778204 8440352 3 88 Dry forest B 778535 8440404 2 89 Dry forest B 778829 8440401 1 90 Dry forest B 779083 8440399 2 91 Flooded forest B 788291 8447170 10 92 Flooded forest B 788500 8447253 1 93 Flooded forest B 788723 8447334 4 94 Flooded forest B 788940 8447398 7 95 Flooded forest B 789158 8447458 2 96 Dry forest B 789402 8447510 5 97 Flooded forest B 78738885 8447686.02 12 98 Flooded forest B 787651 8447772 6 99 Flooded forest B 787875 8447841 3 100 Flooded forest B 788140 8447970 6 101 Flooded forest B 788443 8448085 3 102 Dry forest B 788652 8448150 1 103 Flooded forest B 782787.56 8451826.06 11 104 Flooded forest B 782582 8451806 8 105 Flooded forest B 782381 8451887 6 106 Flooded forest B 782079 8451917 15 107 Flooded forest B 781864 8451969 3 108 Dry forest B 781666 8452017 3 109 Flooded forest C 775268 8503059 4 110 Flooded forest C 775018 8503202 9 111 Flooded forest C 774840 8503339 8 112 Flooded forest C 774682 8503490 18 113 Flooded forest C 774517 8503621 15 114 Dry forest C 774349 8503779 3 115 Dry forest C 778523.36 8504561.8 1 116 Dry forest C 778807 8504381 17 117 Dry forest C 778328 8504678 18 118 Dry forest C 778178 8504870 15 119 Dry forest C 777995 8505131 13 120 Dry forest C 777804 8505374 1 121 Dry forest C 781622.42 8506496.55 1 122 Dry forest C 781296 8506654 13 123 Dry forest C 781175 8506925 11 124 Dry forest C 781065 8507070 3 125 Dry forest C 780930 8507258 13 126 Dry forest C 780708 8507364 1 Figure 2 PCA-ordination diagram in correlation biplot scaling with birds species (Passeriformes) represented by arrows and habitats by points for data of birds from Southern Amazon, Brazil Figure 3 Dendogram of index similarity Jaccard (birds order Passeriformes) for habitats (r= 0.872, p= 0.002). Acronyms: h= habitats, see type of habitat according table I and G= Groups principals Figure 4 Mantel statistic based on Pearson’s product-moment correlation, relation between species dissimilarity and spatial distance in meters of birds (order Passeriformes) in Southern Amazon (r: 0.0608, p: 0.005). Each points represents one pair of compared habitats Discussion Silva(22) suggested that many amazon species penetrate the Brazilian savanna biome following the gallery forest or vice versa, both places presenting a high diversity of birds(23). In this study, the sampled places are very close to the transition between the Amazon and the Brazilian savanna, and this fact may explain the substitution of species that we observe. The high variability in the composition of species (unequally distributed) in the sampled points also contributed to the high species richness of birds Passeriformes. As suggested by Williams(24), the increased level of environmental heterogeneity in the sampled habitats may be very relevant in explaining the high species richness that we found. Cohn-Haft, Whitaker, and Stouffer(25) also proposed that habitat heterogeneity is the most important determinant for bird species richness inside the Amazon, and not primary productivity or level of rainfall as advocated by other authors. Concerning the preference for habitats, this study showed that, although some species revealed to be habitat specialists, most bird species of the order Passeriformes explored and foraged many types of habitats. The habitat that presented more species was the flooded forest (Table 2). In this type of habitat, birds may find suitable conditions that directly influence their life cycle, such as, water, food, shelter, and protection from predators(26,27). In the Amazon, many species, even residents, disperse according to water and food resources and these are abundantly present in the flooded forest habitat. Ferreira et al.(28) found more richness of species at flooded habitats, a finding that agrees with our own results. The species Mimus saturninus had the highest level of association with this type of habitat, though always with open grasslands with scattered trees and shrubs close-by. We believe this may be explained by the fact that this species lives in groups of thirteen individuals and they forage the river for reproduction and food (fruits). In the dry forest habitat there are many winged insects, which could explain the presence of Empidonomus varius, Dysithamnus mentalis, Onychorhynchus coronatus, Thamnomanes caesius, and Mymotherula menetriesii in this habitat, since they primarily feed in these insects. The high beta diversity that we found in this study is very important, particularly for strategic conservation plans. We provide specific points along an environmental gradient in the Amazon forest, where a high richness and high variation in species composition within different types of habitats may be found. More attention should be given to the importance of local conservation. High beta diversity should be taken into consideration when designing a natural reserve, particularly in including, placing and in the extension of contiguous heterogeneous habitats(29), which contrast with lowland habitats where species are widely distributed(11,30,31). The positive correlation between the species dissimilarity and geographic distance observed for Passeriformes in this study is in line with the Neutral Theory(32), which states that species similarity in a community decreases with increased geographic distance between different environments. This means that because of the limitation in species distribution, the more distant the habitats are, the more different they will be in terms of species composition(33). This author assumes that the limitation in species distribution is a function of immigration and local extinction, with species appearing and disappearing. Therefore, for species that have a small distribution, local and regional variation will impact their distribution the most. The analysis of the Jaccard similarity index revealed a major point where substitution of species is significant. Groups 3 and 4 appear on a point of transition and mixture of species close to the North Amazon, where in a small space, many different species may be found. 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