BETA DIVERSITY OF BIRDS (Passeriformes, Linnaeus, 1758) IN SOUTHERN AMAZON

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

Abstract

The importance of estimating the biological diversity and understanding how ecological specialization of species changes with spatially-organized habitats in undeniable. High beta diversity between neighboring places means an elevated number of species living within small distances, which usually are adapted to local conditions and highly vulnerable to anthropogenic actions as deforestation and burning. We investigated beta diversity of birds from the order Passeriformes in Southern Amazon, within landscapes with a large heterogeneous vegetation cover (habitats with flooded forest, dry forest, and marsh palm) through sound, observational, and photographic censuses. We marked 126 points in equidistant transects. A total of 148 species of birds were identified, distributed in 27 families. We found that 97% of the species foraged in flooded forest, 77% in dry forest and 19% in marsh palms, and only 18% foraged in the three habitats. An ordination analyses revealed which species showed the strongest preference to each habitat. The analysis for the Global beta diversity showed that this value is high (Whittaker: 7.7405), and the same pattern was obtained with the measure of pairwise dissimilarity. An influence of spatial distance was clearly observed in the cluster analysis and confirmed with a partial Mantel analysis; however, this was not observed at points that coincided with the transition and substitution of species. The influence of spatial distance in the dissimilarity index (beta diversity) was significant (r: 0.0608, p: 0.0049). The assemblage of species in small local populations with high beta diversity may be at risk if deforestation, selective logging, and poaching continue. In summary, this study provides important information on specific habitats with high beta diversity that may be at risk of destabilization of its populations due to continuing environmental changes imposed by humans.

Keywords:
Amazon birds; conservation; distance influence; high richness

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.

Palavras-chave:
conservação; influência da distância; pássaros da Amazônia; riqueza

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

Code map	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. This species composition is organized in limited local populations with high beta diversity that should be protected from the deforestation, selective logging, and poaching that have been occurring because this community is particularly vulnerable to disruption, and immediate recovery will most likely lead to reorganization of an unbalanced ecosystem. Thus, this study provides important information on specific habitats with high beta diversity whose stability is at risk in the face of continuing environmental challenges.

Acknowledgements

To the BioNorte Project - Knowledge, Sustainable Use and Bioprospecting of Biodiversity in the Southern Amazon for funding the project and to CAPES (Coordination for the Improvement of Higher Education Personnel) for the scholarship granted.

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Publication Dates

• Publication in this collection
  2017

History

• Received
  12 Apr 2016
• Accepted
  04 Oct 2016