Volume 7 1996 No.1

ORNITOWGIA NEOTROPICAL 7, 1-18, 1996@ The Neotropical Ornithological Society

DISTRIBUTION OF AMAZONIAN AND ATLANTIC BIRDS INGALLERY FORESTS OF THE CERRADO REGION, SOUTH AMERICA

José Mafia Cafdoso da Silva

Zoological Museum, University o! Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.

Resumo. As distribui~oes de aves que tem os seus centros de distribui~ao na Amazonia (Elementos AmazOnicos,202 taxa) e no sul da Floresta Atl~ntica (Elementos Atla.nticos, 79 taxa) nas florestas de galeria na regiao doCerrado, a maior regiao de savanas da América do Sul, sao analisadas. Em ambos os grupos, o número de espéciesdiminui com o aumento da dista.ncia em rela~ao a seus centros de distribui~o. Entretanto, elementos Atl~nticosestendem suas distribui~oes muito mais no interior da regiao do Cerrado que os elementos AmazOnicos. Há urnasepara~o altitudinal entre elementos AmazOnicos e Atl~nticos, com os primeiros ocorrendo, em média, emaltitudes mais baixas que os últimos. Elementos AmazOnicos sao restritos principalmente as depressoes periféricase planaltos baixos dentro da r~iao do Cerrado, enquanto elementos Atlanticos sao encontrados principalmenteem planaltos altos. Fatores historicos (efeitos das mudan~as climáticas durante o Quaternário sobre a estrutura ecomposi~o das florestas de galeria) e ecológicos (tolernncia das espécies a trocas abruptas de temperatura duranteo inverno) sao sugeridos como possíveis explic~oes para as diferen~ na distribui~ao dos elementos AmazOnicose Atl~nticos dentro da regiao do Cerrado.

Abstract. Distributions of Amazonian (202 taxa) and Atlantic (79 taxa) bird elements in the system of the galleryforests of theCerrado Region, the largest savanna region in South America, are analysed. In both categories, thenumber of species decreases with increasing distance from their source areas. However, more Atlantic elementsextend their ranges considerably deeper into the Cerrado Region than do Amazonian elements. There is analtitudinal separation between Amazonian and Atlantic elements, with Amazonian taxa occurring, on average,at lower altitudes than Atlantic ones. Amazonian elements are mainly restricted to the peripheral depressions andlow-altitude plateaus within the Cerrado Region, whereas Atlantic ones are found primarily at high plateaus. Bothhistorical (effects of the cyclic climatic changes during the Quaternary on the structure and composition of galleryforests) and ecological (tolerance to abrupt changes in temperature during the winter) factors are suggested to havecaused range differences between Amazonian and Atlantic elements within the Cerrado Region. Accepted 2 October1995.

Key words : Biogeography, Central Brazil, Cerrado, gallery forests, paleoecology, dispersion, South America, avifauna.

Modern historical biogeographers have fo-cused their efforts on reconstructing the tem-poral sequence of fragmentation of the range ofancient widespread species during cycles of vi-cariance as well as searching for congruence be-tween such sequences across different groups oforganisms (Nelson & Platnick 1981, Humphries& Parenti 1986, Humphries 1992). Nonetheless,cycles of species dispersion are as important asare cycles of vicariance from an evolutionaryviewpoint, as they promote biotal interchange

INTRODUCTIONBiogeographic patterns within continental biotasare produced by successive cycles of vicariance(i.e., range fragrnentation followed by differentia-tion) of widespread species, followed by cycles of

population dispersion (i.e., progressive rangeexpansion by occupying new areas that are suit-able across a landscape) of descendant speciesthat produce more widespread forms, followedby new cycles of vicariance (Cracraft 1988,Haffer 1993).

CARDOS( )A SILVA

1992) have all provided numerous examples ofAmazonian or Atlantic organisms whose rangeboundaries are located in the gallery forests with-in the Cerrado Region.

A point that still remains poorly investigatedin all groups of organisms is how these forest-adapted species are distributed throughout thesystem of gallery forests of the Cerrado Region.Are they widely distributed throughout thegallery forest system of this region? Have theyfollowed common pathways of colonization?What abiotic and biotic factors influence theranges of these organisms within the CerradoRegion? Two hypotheses related to these ques-tions have been proposed so far. The first sug-gests that Arnazonian and Atlantic forest ele-ments are not widely distributed within theCerrado Region, but that their numbers decreasewith increasing distance from the source areas(Cerqueira 1980, Silva & Oniki 1988). Thesecond suggests that there is an altitudinal segre-gation between Amazonian and Atlantic species,with the former mainly occurring at low-altitudeplateaus and peripheral depressions, and thelatter mainly occurring at high plateaus (Silva1989). Neither of these two hypotheses has beencritically evaluated for any group of organisms.

In this paper, I present a list of forest-adaptedbirds that have their centres of distribution inAmazonia or southern Atlantic Forest, andrange boundaries in the gallery forest system ofthe Cerrado Region. Thereafter, I shall evaluatehow the distance from the source areas and alti-tude influence the distribution of these birdswithin the Cerrado Region.

and ecological intermixing, phenomena thatplay important roles in augmenting the speciesrichness at a regional scale as well as in theevolution of biological comrnunities (Ricklefs &Schluter 1993).

A naturallaboratory to study the historicaland ecological factors involved in the promotionof biotal intermixing is the system of galleryforests within the Cerrado Region. The CerradoRegion is the second largest ecological region andthe largest savanna region in South America,comprising between 1.5 and 1.8 million km2(Ab'Saber 1977a). Together with Chaco andCaatinga, two predominantly xeric regions, theCerrado Region forms a broad open-vegetationcorridor (Fig. 1) separating the large blocks ofAmazonian and Atlantic forests (Vanzolini 1974,Ab'Saber 1977a). The development of this open-vegetation corridor during the Tertiary is gene-rally acknowledged as an important paleoecolo-gical event which determined the disjunctionand/or differentiation of several groups of forest-adapted species that currently have their centresof distribution in Amazonia or Atlantic Forest(Bigarella et al. 1975, Mori et al. 1981, Cracraft& Prum 1988).

The Cerrado Region is covered mainly by asavanna-like vegetation known as cerrado (Eiten1972), but evergreen forests occur as narrow beltsalong rivers and streams. These forests are termedgallery forests (Eiten 1990). Gallery forests seemto be expanding in the Cerrado Region followingthe improvement of the ecological conditions(e.g., soil, microclimate) caused by the gradualdessication of ancient plateaus by fluvial erosion(Ab'Saber & Costa Júnior 1950, Cole 1986).Because of that, several researchers have suggestedthat gallery forosts play an important role asmesic corridors, that open the way to the coloni-zation of the Cerrado Region by forest-depen-dent organisrns with ranges centered in theneighbouring Amazonian and Atlantic forests(Sick 1956, 1965, 1966; Rizzini 1979; Cerqueira1990; Redford & Fonseca 1986; Willis 1992).Studies on the distribution patterns of plants(Smith 1962, Ratter et al. 1973, Rizzini 1979,Prance 1987, Mori et al. 1981, Ratter 1987),butterflies (Brown & Mielke 1967, Brown 1987),mammals (Bishop 1974, Cerqueira 1982, Redford& Fonseca 1986) and birds (Silva & Oniki 1988;Silva 1989; Willis & Oniki 1990, 1991; Willis

THE CERRADO REGION AND ITS

GALLERY FORESTS

The Cerrado Region (see definition in Ab'Saber1977a, 1986, and Vanzolini 1988) includes mostof central Brazil and small extensions of north-east Paraguay and eastern Bolivia (Ab'Saber1977a). It has borders with Amazonia, southernAtlantic Forest, Caatinga and Chaco (Fig. 1).The estimated length of the border between theCerrado Region and Amazonia (7950 km) ismore than three times as long as that betweenthe Cerrado Region and southern Atlantic Forest(2630 km). The width of the transition zoneseparating the Cerrado Region from Amazonia

BIRDS OF GALLERY FORESTS

FIG. 1. Major South American morphoclimatic domains following Ab'Saber (1977a, 1986). Several small domainswere combined in a sing!e Andean Region. The domain of the plateaus with Araucaria has been merged withsouthern Atlantic Forest. The river dividing the Atlantic Forest in northern and southern regions is the sao

Francisco.

whose continuity is broken by a network ofperipheral or intermontane depressions (Ab'Sa-ber 1983, Brasil & Alvarenga 1989). The altitudeof these plateaus ranges from 500 to 1700 m.Most of the surface of the Cerrado Region pla-teaus was molded from the Upper Cretaceous tothe Mid.:rertiary, during the Sul-Americano cycleof erosion (Braun 1971, Cole 1986). The re-sulting pedeplain (Sul-Americana surface) was

(Fig. 1) ranges from 20 to 430 km (mean = 150km, s.d. = 30.5, n= 14 measuring points on

a map with scale of 1: l000000). The samemeasurement in the transition zone between theCerrado Region from Atlantic Forest (Fig. 1)varies from 38.4 to 269.2 km (mean = 82.0, s.d.= 70.0, n= 14).

Most of the Cerrado Region consists of largeblocks of crystalline or sedimentary plateaus,

3

CARDOSO DA SILVA

derstorey that harbors many ferns, epiphytes andpalms (Ribeiro et al. 1983). The floristic com-position of gallery forests is highly variable overthe Cerrado Region (Eiten 1990).

Gallery forests form a dense network withinthe Cerrado Region. This is mainly because theheadwaters of some of the major South Ameri-can rivers (e.g., sao Francisco, Tocantins, Ara-guaia, Paraguay) are located on the highest pla-teaus of the Cerrado Region (Innocencio 1989).From there, these rivers and their affluents flowin several directions (Fig. 3), making contactwith hydrographic systems of almost all neigh-bouring ecological regions. Little is knownabout the evolution of the present-day drainagesystem of the Cerrado Region. It has certainlyhad a long and dynamic history associated withthe geological changes in central Brazilian pla-teaus since the Paleozoic (Innocencio 1989).However, most of its modern features developedmore recently, possibly in association with thePlio-Pleistocene uplift (Braun 1971, Petri &Fúlfaro 1983).

then uplifted during the Plio-Pleistocene, withassociated subsidence leading to the formation ofthe peripheral depressions, whose altitudes varyfrom 100 to 500 m (Braun 1971, Brasil &Alvarenga 1989, Del'Arco & Bezerra 1989).Peripheral depressions have been modifiedduring the Quaternary by the recent cycles oferosion (Braun 1971). Geomorphological eviden-ce suggest that during the cyclic global climaticfluctuations in the Pleistocene and Holocene,peripheral depressions were much more unstableand underwent more drastic ecological changesthan the plateaus (Ab'Saber 1977b, 1983, 1988;Brasil & Alvarenga 1989).

On the plateaus, gallery forests occur asnarrow and well-defined strips (no more than100 m wide) along the rivers and streams (Fig. 2).On the peripheral depressions, gallery forests aregenerally wider than on the plateaus. In bothplateaus and depressions, gallery forests grow oncambisols or hydromorphic soils rich in organicmatter. Gallery forests are evergreen with treeson average 20-30 m tall, and a very humid un-

FIG. 2. Gallery forest on a high-plateau (ca. 1000 m) in the Cerrado Region. Notice the sharp separation betweengallery forest and the adjacent cerrado. Photo by R. Constantino near Brasília, Distrito Federal, Brazil.

4

BIRDS OF GALLERY FORESTS

The Cerrado Region has a tropical seasonalclimate with a dry period (May to August-Sep-tember) coincident with the coldest months ofthe year (Nimer 1979). The average annual rain-fall in this region varies between 1250 and 2000mm, and the average annual temperature bet-ween 20° and 26°C (Nimer 1979, Ab'Saber

1983).

boundaries within the Cerrado Region. I assumethat these species have expanded and/or areexpanding their ranges into th~ Cerrado Regionfrom their centres of distribution after a phase ofisolation caused by the fragmentation of anancient humid forest biota.

Among the selected species, 11 species orwell-marked subspecies (see Appendix) have dis-junct populations in Amazonia and southernAtlantic Forest and no differentiation at all inexternal morphology. For each of these lattertaxa, I measured the distance from its innermostrecord in the Cerrado Region to the nearestrecord in both Amazonia and southern AtlanticForest. Then, I used the criterion of minimumdistance between these points for determiningwhether populations in the Cerrado Region aremore parsimoniously (from a geographical pers-

METHODS

From a list of bird species that are known orassumed to breed in the Cerrado Region (Silva1995), I selected all those species or well-markedsubspecies that: (a) were recorded mainly in gal-lery forests, (b) have their centres of distributionin Amazonia (Amazonian elements, see Fig. 4)or southern Atlantic Forest (Atlantic elements,see Fig. 5), and, finally, (c) have their range

5

'ARDOSO DA SILVA

251-500 km, (c) 501-750 km, (d) 751-1000km, and (e) more than 1000 km. I tested the nullhypothesis that Amazonian and Atlantic ele-ments are similarly distributed across these fivedistance categories by using G-test.

To test the null hypothesis that Amazonianand Atlantic elements have similar altitudinalranges within the Cerrado Region, I listed alllocalities within this region where one or moretaxa of each of these two biogeographic cate-gories had been recorded. After that, I checkedthe altitude for each of these localities in Paynter& Traylor (1991). Finally, I compared the alti-tude of these two sets of localities by using thenon-parametric Mann-Whitney U-test.

To examine if the maximum distance reachedby Amazonian and Cerrado elements into theCerrado Region is associated with some of theirecological characteristics, I classified each taxonin broad categories of diet and habitat use. Dietcategories are as follows: (a) nectarivores, speciesthat feed mainly on nectar, perhaps includingsome arthropods in their diet; (b) frugivores,species whose diet is primarily based on fruits,with insects being included only rarely; (c)frugivores-insectivores, species whose diet may

pective) interpreted as expansions from Ama-zonian or Atlantic populations (see Fig. 4a foran example).

Some Atlantic taxa that occur in the CerradoRegion and have closest relatives in the AndeanRegion (e.g., 1igrisoma fasciatum, Otus atricapil-lus, Lochmias nematura, Philydor rufosupercilia.tus, Philydor rufus, Elaenia obscura, Todirostrumplumbeiceps, Pyroderus scutatus, Oxyruncus crista-tus, Pipraeida melanota, Euphonia musica) wereexcluded from this analysis, because their pre-sence in the gallery forests of the Cerrado Regionmight be as relicts of a pattern of distributioninvolving southern Atlantic Forest, part of theCerrado Region and the Andes (Remsen et al.1991) rather than due to comparatively recentrange expansion from southern Atlantic Forest

(Silva, unpubl.).I evaluated the maximum distance that Ama-

zonian and Atlantic elements extend into theCerrado Region by estimating for each taxon thedistance from its innermost record in the Cer-rado Region to the nearest point at the borderbetween the Cerrado Region and its centre ofdistribution. I classified each taxon in one of thefollowing distance categories: (a) 0-250 km, (b)

6

BIRDS OF GALLERY FORES~

}~ ¡( !\ , \

'--

-.r~'-,-

~--V~\

I,

[L-)-'

FIG. 5. Two examples of Atlantic Forest elemems recorded in the Cerrado Region: (A) Amazilia l. lactea, (B)

Lepidocolaptes f fuscus.

include similar proportions of fruits and insects(and other arthropods); (d) insectivores, specieswhich include only insects ( and other arthro-pods) in their diets; (e) others, a mixed categorycomposed of groups poorly represented in the setof species analysed, such as carnivores (raptors)and granivores (seedeaters). Habitat-use categoriesare the following: (a) species that concentratetheir activities mainly on the interior of galleryforests (understorey and sub-canopy); (b) speciesthat concentrate their activities on the externalregions of the gallery forests (canopy and/orborders); (c) species that use both internal andexternal regions of the gallery forests.

Data about the natural history of species werecollected during my field work in the CerradoRegion (several one-month expeditions from1985 to 1994). Distribution and taxonomy of thegallery forests birds in the Cerrado Region werebased on studies in museums (American Mu-seum of Natural History, New York, UnitedStates; Museu Paraense Emílio Goeldi, Belém,Brazil; Museu Nacional, Rio de Janeiro, Brazil;Museu de Zoologia da Universidade de saoPaulo, sao Paulo, Brazil; and Zoological Mu-seum, University of Copenhagen, Copenhagen,Denmark) supplemented by a literature survey.

RESULTS

A total of 276 species (278 taxa, because twospecies, Ciccaba huhula and Cissopis leveriana,are represented in the Cerrado Region by twosubspecies) were included in this analysis(Appendix). Amazonian elements include 200taxa whilst the Atlantic ones include 78 taxa

(Table 1).Eleven pairs of Amazonian and Atlantic

sister taxa were recorded within the CerradoRegion (Table 2). None of them are known tohave established a contact zone (e.g., a narrowzone of sympatry, hybridization or intergrada-tion) within this region.

The distributions of Amazonian and Atlanticelements in the categories of maximum distancereached within the Cerrado Region differ signi-ficantly (G= 61.2, df= 2, p < 0.001j three cate-gories with > 500 krn were grouped to avoidthe problem of categories with frequencies < 1).Most Amazonian elements (86%) do not extendmore than 250 km into the Cerrado Regionand no element extends more than 750 km(Table 1). In contrast, only 50% of the Atlanticelements are known to be restricted to the1-250 km distance category, and 14% extend

CARDOSO DA SILVA

TABLE 1. Distribution of Amazonian (AM) and Atlantic (AT) elements by categories of diet, habitat use, anddistance reached into the Cerrado Region. Diet categories are nectarivores (NE), frugivores (FR), frugivore-insecti-vores (FI), insectivores (IN) and others (OT). Distance categories are (A) 1-250 km, (B) 251-500 km, (C)501-750 km, (D) 751-1000 km, (E) > 1000 km.

Total AMAT

oo

116

II5

6222

2O

oo

132

23

10

132

4o

2313

52

67

the main plateaus in the western part of theCerrado Region (Fig. 6a). On the other hand,localities in which Atlantic elements have beenrecorded (n = 103) are mainly on the top of

plateaus, in the eastern part of the CerradoRegion (Fig. 6b). Altitudes of Amazonian loca-lities (mean = 396 m, s.d. = 213.4, n = 55) differfrom those of the Atlantic ones (mean = 705 m,s.d. = 279.8 m, n = 96). This difference is sta-tistically significant (Mann-Whitney U-test, U =

998.5, p < 0.001).

more than 1000 km into the Cerrado Region

(Table 1).No clear pattern of association between diet,

habitat use and distance reached into the CerradoRegion was found for Amazonian or Atlanticelements (Table 1). In general, most of thespecies assemblages formed by the combinationof diet and habitat-use categories have increas-ingly fewer species within the Cerrado Regionwith increasing distance from their centres ofdistribution.

Localities where Amazonian elements havebeen recorded (n = 58) are mainly within the

peripheral depressions or along the borders ofDlSCUSSION

Both distance from their centres of distributionand altitude influence the distribution of Ama-zonian and Atlantic elements over the galleryforest system of the Cerrado Region. The hypo-thesis that the number of these elements withinthe Cerrado Region decreases with increasingdistance from their centres of distribution(Cerqueira 1982, Silva & Oniki 1988) is sup-ported. Nonetheless, Atlantic elements extendtheir ranges significantly deeper into the CerradoRegion than do Amazonian ones (Table 1). Thehypothesis of differences in altitudinal distribu-tion between Amazonian and Atlantic elementswithin the Cerrado Region (Silva 1989) is alsosupported, bocause Amawnian elements occurat significantly lower altitudes than Atlanticones.

TABLE 2. Pairs of Amazonian and Atlantic allopatricsister taxa in the system of gallery forests of theCerrado Region.

AtlanticAmazonian

Tinamus taoCiccaba huhula huhulaBaryphthengus martiiSelenidera gouldiiMelanerpes cruentatusDendrocincla fuliginosapyriglena leuconota

Corythopis torquataMyiornis ecaudatusCissopis leveriana leveriana

Euphonia rufim¡tris

T solitariusc. h. albomarginatusB. ruficapilluss. maculirostrisM. flavifronsD. turdinaR leucopterac. delalandiM. auricularisc. I. majorE. pectoralis

8

BIRDS OF GALLERY FORE

500 km

FIG. 6. Distribution of alllocalities where Amazonian (A) and Atlantic (B) elements have been recorded withinthe Cerrado Region. Some dots in both maps may represent more than one locality. Stippled, areas with altitudeequal or more than 500 m.

9

CARDOSO DA SILVA

The reduction of number of species from themain source area toward the centre of the regionbeing colonized is the pattern expected if speciesare passively expanding their ranges in accordan-ce with the improvement of the ecological condi.tions (Udvardy 1969). The number of Amazo-nian and Atlantic forest species expanding theirranges into the Cerrado Region is only a fractionof the pool of species living in the source regions.The limited area covered by forest habitats, diffe-rences in floristic composition and structure, andpossibly the reduction of density of some keyresources (e.g., army ants swarms and fruits) inthe gallery forests of the Cerrado Region certain-ly constrain the range expansion of most of theAmazonian and Atlantic forest birds.

Amazonian and Atlantic elements followdifferent pathways to expand their ranges intothe Cerrado Region. Connections with the Ama-zonian forests are made mainly through thegallery forests that follow the channels of themajor rivers that flow toward the Amazon Basin(e.g., Araguaia, Tocantins, Guaporé). Theserivers, in turn, flow mainly in the peripheraldepressions. In contrast, links between the gal-lery forest system of the Cerrado Region andsouthern Atlantic Forest are made mainly bynarrow gallery forests on the plateaus as well asby a broad corridor of tall evergreen and semi-de-ciduous forests growing on rich soils along theParanaíba River and its tributaries (Brown &Ab'Saber 1979, Silva 1989).

Differences in the paleoecological history ofthese different pathways of colonization mightexplain the reason why more Atlantic elementsexpanded their ranges deeper into the CerradoRegion than Amazonian ones. Paleoecologicalinformation suggests that in the Cerrado Region,peripheral depressions were much more influ-enced by the drastic climatic fluctuations in theQuaternary than the plateaus (Ab'Saber 1977b,1983, 1988). Consequently, one can expect thathigh frequency climatic shifts and their associa-ted geomorphological and hydrological changeshave disturbed more frequently the galleryforests on the peripheral depressions than thegallery forests on the plateaus or those on richsoils. I suggest that connections with Amazonianforests following peripheral depressions mayhave broken down several times during un-

favourable climatic periods. This could have hada negative effect on populations of Amazonianforest birds that were expanding their ranges intothe Cerrado Region, promoting local extinctionsor range retraction toward the borders of thesource area. In contrast, gallery forests on theplateaus and those on rich soils were relativelymore stable during the Quaternary climaticfluctuactions (Ab'Saber & Brown 1979), pro-viding Atlantic forest birds with more oppor-tunities to expand and maintain their ranges intothe Cerrado Region.

In addition to historical factors, present-dayecological factors also may help to explain thedifferences in ranges found between Amazonianand Atlantic elements within the Cerrado Re-gion. Willis (1976) has documented that thedrastic falls in temperature, which are so com-mon during the winter of the Cerrado Region(Nimer 1979), affect negatively the behavior ofAmazonian forest birds in areas close to theirrange boundaries in the Cerrado Region. In con-trast, Atlantic elements seem to have developeddifferent strategies (long or local migrations,wanderings, diet shifts) to avoid such short-termclimatic changes (Willis 1990). If so, similaritybetween the climatic types of the CerradoRegion with parts of southern Atlantic Forest(Nimer 1979) may confer Atlantic elementsmore advantages for maintaining their rangeswithin the gallery forest system of the CerradoRegion than Amazonian ones.

Altitudinal segregation between Amazonianand Atlantic elements may be viewed as a conse-quence of the topographic distribution of theconnections between the gallery forest system ofthe Cerrado Region with the Amazonian andAtlantic forests as well as of the paleoecologicalhistories of these connections. One could suggestthat competition also might play an importantrole in the determination of this distribution

pattern. However, potential competitors, i.e.,pairs of closely related Amazonian and Atlantictaxa within the Cerrado Region (Table 2), onlyrepresent a small portion of the species identifiedas expanding their ranges into the CerradoRegion. In addition, the ranges of these closelyrelated taxa are known to be separated by largedistances, which makes any explanation based oncompetition unrealistic.

10

BIRDS OF GALLERY FORESTS

ACKNOWLEDGEMENTS

I thank J. Fjeldsa for guidance, support andreview of the first version of this paper. D. C.Oren, R. B. Cavalcanti, F. C. Novaes, andJ. Batesdiscussed with me different aspects of cerradobiogeography. For companionship and help dur-ing field work I thank D. C. P. Neto, S. F. Bal-bino, J. Ribeiro, M. S. Brígida and N. Guedes. D.M. Teixeira and J. B. Nacinovic (MNRJ), H. F.A. Camargo (MZUSP), and M. LeCroy and G.Barrowclough (AMNH) provided me with allfacilitiesto study the collections under their care.M. E. Petersen, J. Haffer, K.-L. Schuchmann, andan anonymous referee reviewed the manuscript,improving it very much. My studies were sup-ported by a doctoral scholarship of the ConselhoBrasileiro de Desenvolvimento Científico e Tec-nolÓgico (CNPq). Financial support for fieldwork and collection studies carne from NationalGeographic Society (Grant no.4964-93), TheFrank M. Chapman Memorial Fund, WorldWildlife Fund-US, The John D. and CatherineT. MacArthur Foundation, Danish NaturalScience Research Council (Grant J.nr. 11-0390),Museu Paraense Emílio Goeldi and Universida-de de Brasília. This paper is dedicated to the me-mory of Helmut Sick, who began the modernstudy on systematics, biogeography and evo-lution of the Cerrado Region avifauna.

Bigarella, J. J., Andrade-Lima, D., & P. J. Riehs. 1975.Consideras:Oes a respeito das mudans:as paleoam-bientais na distribuis:ao de algumas espécies vegetaisa animais no Brasil. An. Acad. brasil. Ci&nc. 47(supl.): 411-464.

Bishop, I. R. 1974. An annotated list of caviomorphrodents collected in north-eastern Mato Grosso,Brazil. Mammalia 38: 489-502.

Brasil, A. E., & S. M. Alvarenga. 1989. Relevo. Pp.53-72 in Duarte, A C. (ed.). Geografia do Brasil-Regiao Centro-Oeste. Rio de Janeiro.

Braun, O. P. G. 1971. Contribuis:ao a geomorfologia doBrasil Central. Rev. Bras. Geogr. 32: 3-39.

Brown, Jr., K. s. 1987. Biogeography and evolution ofNeotropical butterflies. Pp. 66-104 in Whitmore,T. C., & G. T. Prance (eds.). Biogeography andQuaternary history in tropical America. Oxford.

Brown, Jr., K. S., & 0. H. H. Mielke. 1967. Lepi.:doptera of the Central Brazil Plateau. I. Prelimi-nary list of Rhopalocera: Introduction, Nymphali-dae, Libytheidae. J. Lepid. Soc. 21: 77-106.

Brown,Jr., K. S., & A. N. Ab'Saber. 1979. Ice-age forestrefuges and evolution in the Neotropics: Corre-lation of paleoclirnatological, goomorphologicaland pedological data with modern biological en-demism. Paleoclimas 5: 1-30.

Cerqueira, R. 1980. South American landscapes andtheir mamrnals. Pp 53-75 in Genoways, H. H.(ed.). Mamrnalian biology in South America. Pitts-

burgh.Cole, M. M. 1986. The Savannas: Biogeography and

Geobotany. London.Cracraft, J. 1988. Deep-history biogeography: Re-

trieving the historical pattern of evolving continen-tal biotas. Syst. Zool. 37: 221-236.

Cracraft, J., & R. 0. Prum. 1988. Patterns and pro-cesses of diversification: Speciation and historicalcongruence in some Neotropical birds. Evolution42: 603-620.

Del'Arco, J. F., & P. E. L. Bezerra. 1989. Geologia. Pp.35-51 in Duarte, A. C. (ed.). Geografia do Brasil-Regiao Cemro-Oeste. Rio de Janeiro.

Eiten, G. 1972. The cerrado vegetation of Brazil. Bot.Rev. 38: 201-341.

Eiten, G. 1990. Vegetas:ao. Pp 9-65 in Pinto, M. N.(ed.). Cerrado: Caracterizas:ao, Ocupas:ao e Perspec-tiva. Bras¡lia.

Haffer, J. 1993. Times's cycle and time's arrow in thehistory of Amazonia. Biogeographica 69: 15-45.

Howard, R. & A Moore. 1991. A Complete Checklistof Birds of the World. Second Edition. San Diego.

Humphries, C. J. 1992. Cladistic biogeography. Pp.137-159 in Forey, P.L., Humphries, C. J., Kit-ching, I. L., Scotland, R. W., Siebert, D. J., & D. M.Williams (eds.). Cladistics: A pratical course in

systematics. Oxford.

REFERENCES

Ab'Saber, A. N. 1977a. Os Dominios morfoclimáticosda América do Sul. Primeira Aproxima~ao. Geo-

morfologia 52: 1-21.Ab'Saber, A. N. 1977b. Espa~os ocupados pela expan-

sao dos climas secos na América do Sul, por ocasiaodos períodos glaciais quaternários. Paleoclimas 3:

1-19.Ab'Saber, A. N. 1983. O domínio dos cerrados: ln-

trodu~o ao conhecimento. Revista do Servidor

Público 111: 41-55.Ab'Saber, A. N. 1986. Geomorfologia da regiao. Pp.

88-124 in Almeida Jr., J. M. G. (ed.). Carajás:Desafio político, ecologia e desenvolvimento. saoPaulo. ,

Ab'Saber, A. N. 1988. O Pantanal Mato-Grossense e a

teoria dos refúgios. Rev. Bras. Geogr. 50: 9-57.Ab'Saber, A. N., & M. Costa Júnior. 1950. Contri-

bui~o ao estudo do sudoeste goiano. Boletim

Paulista de Geografia 4: 3-26.

11

CARDOSO DA SILVA

Rizzini, C. T. 1979. Tratado de fitogeografia do Brasil.2 vols. sao Paulo.

Sick, H. 1956. O aspecto fitofisionomico da paisagemdo médio rio das Mortes, Mato Grosso, e a avi-fauna da regiao. Arquivos do Museu Nacional 42:

541-616.Sick, H. 1965. A fauna do cerrado. Arq. 2001. 12:

71-93.Sick, H. 1966. As aves do cerrado como fauna arbonco-

la. Anais Acad. bras. cienc. 38: 355-363.Silva, J. M. C. 1989. Análise biogeográfica da avifauna

de florestas do interflúvio Araguaia-Sao Francisco.Unpublished MSc. dissertation. Universidade deBrasilia, Brasilia.

Silva, J. M. C. 1995. Birds of the Cerrado Region,South America. Steenstrupia 21:69-92.

Silva, J. M. C., & Y. Oniki. 1988. Lista preliminar daavifauna da Esta~ao Ecológica Serra das Araras,Mato Grosso, Brasil. Bol. Mus. Para. EmilioGoeldi, sér. Zool. 4: 123-143.

Smith, L. B. 1 %2. Origins of the flora of southernBrazil. Contrib. U.S. Natl. Herb. 35: 215-249.

Udvardy, M. D. F. 1969. Dynamic wogeography, withreference to land animals. New York.

Vanwlini, P. E. 1974. Ecological and geographicaldistribution of lizards in Pernambuco, north-eastern Brazil (Sauria). Papéis Avulsos, 2001., saoPaulo 28: 61-70.

Vanwlini, P. E. 1988. Distributional patterns of SouthAmerican lizards. Pp. 245-274 in Vanwlini, P. E.,& W. R. Heyer (eds.). Proceedings of a workshopon NeotropK:al distribution patterns. Rio de Janeiro.

Willis, E. O. 1976. Effects of a cold wave on an Ama-zonian avifauna in the upper Paraguay drainage,western Mato Grosso, and suggestions on Oscine-Suboscine relationships. Acta Arnawnica 6: 379-394.

Willis, E. 0. 1990. Land-bird migration in sao Paulo,southeastern Brazil Acta XIX Congressus Inter-nationalis Ornithologici: 754-764.

Willis, E. 0. 1992. 20ogeographical origins of easternBrazilian birds. Orn. Neotrop. 3: 1-15.

Willis, E. 0., & Y. Oniki. 1990. Levantamento preli-minar das aves de inverno em dez áreas do sudoestede Mato Grosso, Brasil Ararajuba 1: 1-19-38.

Willis, E. 0., & Y. Oniki. 1991. Avifaunal transectsacross the open wnes of northern Minas Gerais,Brazil. Ararajuba 2: 41-58.

Humphries, C. J., & L. R. Parenti. 1986. Cladistic bio-

geography. Oxford.Innocencio, N. R. 1989. Hidrografia. Pp. 73-90 in

Duarte, A. C. (ed.). Geografia do Brasil- Regiao

Centro-Oeste. Rio de Janeiro.Mori, S. A., Boom, B. M., & G. T. Prance. 1981. Distri-

bution patterns and conservation of eastern Brazi-lian coastal forest tree species. Brittonia 33:

233-245.Nelson, G. J., & N. I. Platnick. 1981. Systematics

and biogeography: Cladistics and vicariance. New

York.Nimer, E. 1979. Climatologia do Brasil. Rio de Janeiro.Paynter, Jr., R. A., & M. A. Traylor, Jr. 1991. Ornitho-

logical gazetter of Brazil. 2 vols. Cambridge, Mass.Petri, S., & V. J. Fúlfaro. 1983. Geologia do Brasil

(Fanerozóico). sao Paulo.Prance, G. T. 1987. Vegetation. Pp. 28-45 in Whit-

more, T. C., & G. T. Prance (eds.). Biogeographyand Quaternary history in tropical America. Cam-

bridge.Ratter, J. A. 1987. Notes on the vegetation of the

Parque Nacional do Araguaia (Brnzil). Notes R.

bot. Gdn. Edinb. 44: 311-342.Ratter, J. A., Richards, P. W., Argent, G., & D. R.Gifford. 1973. Observations on the vegetation of north-

eastern Mato Grosso. I. The woody vegetationtypes of the Xavantina-Cachimbo Expedition area.Phil. Trans. R. Soc. Lond. B 266: 449-492.

Redford, K. H., & G. A. B. Fonseca. 1986. The role ofgallery forests in the zoogeography of the cerrado'snon-volant mammalian fauna. Biotropica 18:

126-135.Remsen, J. V. Jr., Rocha, O., Schmitt, C. G. & D. C.Schmitt. 1991. Zoogeography and geographical varia-

tion of Platyrinchus mystaceus in Bolivia and Peru,and the Cin:um-Amazonian distribution pattern.Orn. Neotrop. 2: 77-83.

Ribeiro, J. F., Sano, S. M., MacOOo, J., & J. A. Silva.1983. Os principais tipos fisionomicos da regiao dos

cerrados. Boletim de Pesquisa (EMBRAPA-CPAC)21: 1-28.

Ricklefs, R. E., & D. Schluter. 1993. Species diversity:regional and historical influences. Pp. 350-363 inRicklefs, R. E., & D. Schluter (eds.). Species diver-sity in ecological communities. Chicago.

12

BIRDS OF GALLERY FORESTS

APPENDIX. List of taxa included in this analysis (taxonomic sequence following Howard & Moore 1991).Pattern: (AM) Amazonian, (AT) Atlantic. Distance: (A) 1-250 km, (B) 251-500 km, (C) 501-750 km, (D)751-1000 km, (E) > 1000 km. Habitat Use: (I) Interior (understorey and sub-canopy), (E) Exterior (canopy andborders), (B) Both. Diet: (NE) Nectarivores, (FR) Frugivores, (FI) Frugivore-Insectivores, (IN) Insectivores, (OT)others, including carnivores and granivores. Species preceded by # have disjunct and undifferentiated populationsin Amazonia and southern Atlantic Forest.

Species Pattern Distance Habitat Diet

AMATAMAMAMATAMAT

BBAAACAA

IIIIIII

FIFIFIFIFIFI

FIFI

AMAM

BA

IB

OTIN

AT E E OT

AMAMAM

AAA

EBB

OTOTOT

AM

AM

AA

BI

FI

OT

AMAMAMAM

AAAA

BBBB

FRFRFRFR

AMATAM

AcA

FRFRFR

AT A IN

AM B IN

AM

AT

AA

EI

FRFR

AMAMAMATAMAMAMATAMAM

AAAcAAAcAA

EEEEEEEEEE

FRFRFRFRFRFRFRFRFRFR

TinamidaeTinamus taoTinamus solitariusTinamus majorTinamus guttatusCrypturellus cinereusCrypturellus obsoletus obsoletusCrypturellus strigulosusCrypturellus noctivagus noctivagusArdeidae

Agamia agamiZ2brilus undulatus

AnatidaeMergus octosetaa?Us

AccipitridaeLeucopternis kuhliLeucopternis albicollisSpizaetus tyrannus serus

FalconidaeDaptrius ater# Micrastur gilvicollis gilvicollis

CracidaeOrtalis guttata guttata

Penelope jacquacuPipile pipile nattereriMitu tuberosa

Phasianidae

Odontophorus gujanensisOdontophorus capueira capueiraOdontophorus stellatus

RallidaeEulabeornis saracura

EurypigidaeEurypyga helias

ColumbidaeColumba subvinaceaClaravis godefrida

PsittacidaeAra macaoAra severaAra manilata

Aratinga auricapillaAratinga wedelli

pyrrhura rhodogasterpyrrhura pictaBrotogeris tirica

Brotogeris cyanopteraPionus menstruus menstruus

OpisthocomidaeOpisthocomus hoazin AM B E OT

CARDOSO DA SILVA

Pattern Distance Habitat DietSpecies

AM

AM

AM

AcA

EEI

INININ

OTOTOTOTOT

AMAMATAMAT

AAAAA

BBBBB

ININ

ATAM

AA

II

BE

ININ

AMAM

AA

BBBBBBBBBBBBB

NENENENENENENENENENENENENP

AMAMAMATAMATAMATATATATATAM

AAAABcAAAAcAA

FIFIFIFIFIFI

FIFIFT

AMAMAMAMATAMAMATAM

BAAAAABEA

BBBBBBBBB

BAB

BBB

INININ

AMAMAM

ININININININININ

CuculidaePiaya melano?flSterPiaya minuta

Neomorphus geoffroyi geoffroyi

StrigidaeOtus watsoniiLophostrix cristataStrix virgata borellianaCiccaba huhula huhulaCiccaba huhula albomarginatus

NyctibiidaeNyctibius aethereus aethereus

Nyctiprogne leucopyga

Caprimulgidae# Caprimulgus maculicaudusChaetura cinereiventris sclateri

TrochilidaeThrenetes leucurusPhaethornis hispidusFlorisuga mellivoraMelanotrochilus fuscusAnthracothorax viridigulaLophornis magnij!caChlorostilbon mellisugusThalurania glaucopisÚ!ucochloris albicollisAmazilia lactea lacteaAphantochroa cirrochlorisHelioth1)X aurita auriculataHeliomaster longirostris

TrogonidaeTrogon melanurusTrogon viridis viridisTrogon collaris collaris

Trogon rufus rufusTrogon aurantiusTrogon violaceusElectron platyrhynchum

Baryphthengus mficapillusBaryphthengus martii

GalbulidaeGalbula cyanicollisGalbula leucogastraJacamerops aurea

BucconidaeNotharchus macrorhynchus hyperrhynchusNotharchus tectusBucco tamatiaNystalus striolatusMalacoptila striata striata

Malacoptila rufaNonnula ruficapillaMonasa morphoeus

CapitonidaeCapito dayi

AMAMAMAMATAMAMAM

AAAAAAAA

BBBBBBBB

FIAM A B

BIRDS OF GALLERY FORESTS

AMAMAMATATAM

AAAABA

EEEEEE

FIFIFI

FIFIFI

AMATATAMATATAMAMATAMAMAMAMAT

AAEBEAAAcAABBc

BBBBBBBBBBBBBB

IN

ININFIFIFIFI

FIFIFI

FIFIFIFI

AMATAMAMAMAMAMATAMAMAMATATAMAT

AEAAABAEAAAACAA

IIIBI1

INININININININININININININININ

IIIIIIB

ATATATAMATAMAMATAMATAMATAMAM

AcAAAAAEADADAA

BBBIBIIIIBIIBB

ININININININININININININININ

RamphastidaePteroglossus inscriptusPteroglossus bitorquatusSelenidera gouldiiSelenidera maculirostrisRamphastos dicolorusRamphastos tucanus

PicidaePicumnus auri/rons, Picumnus cirratus cirratus

Picumnus albosquamatus guttiferMelanerpes cruentatusMelanerpes flavi/ronsVeniliornis maatlifronsVeniliornis affinis ruficepsPiculus leucolaemusPiculus flavigula erythropisCeleus grammicusCeleus jlavus inornatusCeleus torquatus occidentalisCampephilus rubricollisCampephilus robustus

DendrocolaptidaeDendrocincla fuliginosaDendrocincla turdinaDendrocincla merulaGlyphorhynchus spirurus inornatusNasica longirostris

Hylexetastes perrotiiXiphocolaptes promeropirhynchusXiphocolaptes albicollisDendrocolaptes certhiaXiphorhynchus obsoletusXiphorhynchus elegansLepidocolaptes sguamatus squamatusLepidocolaptes juscus fuscusLepidocolaptes albolineatus

Campylorhamphus falcularius

Furnariidae

Synallaxis ruficapillaSynallaxis spixiSynallaxis cinerascensSynallaxis rutilansCranioleuca pallida

Philydor erythrocercusPhilydor erythropterusPhi{ydor lichtensteiniAutomolus ochrolaemusAutomolus leucophthalmusSclerurus rufigularisSclerurus scansor scansorXenops tenuirostrisXenops minutus genibarbis

FormicariidaeCymbilaimus lineatus

Hypoedaleus guttatusMackenziaena severaSakesphorus luctuosus

AMAT

ATAM

ABAB

ININININB

15

CARDOSO DA SILVA

DietDistance HabitatPatternSpecies

INININININININININININININININININININININININININININININININININININININININININ

EIII

AMAMAMAMATAMAMAMAMAMAMAMAMAMAMATAMAMATATATAMAMAMAMATAMAMAMAMAMATAMAMAMAMAMAMAMAMAM

AAAABAAAAAAAAAAEAAAAAAAABAAAAAAAABBABAAAA

IIIIIIBIIBIII

IIBIII

INAT E

BAACAEABAAAAAAAA

EIIIEI

FIINFRFRININININININININININININ

ATAMAMATATATAMATAMAMATAMAMAMAMAT

# Thamnophilus palliatus palliatus

Thamnophilus aethiops punctuligerThamnophilus schistaceus7bamnophilus amazonicusDysithamnus mentalis mentalisThamnomanes saturninus

Thamnomanes caesius persimilis

Mynnotherula brachyuraMynnotherula sclateri

Mynnotherula surinamensisMynnotherula hauxwelli

Mynnotherula leucophthalmaMynnotherula ornataMynnotherula axillaris axillarisMynnotherula menetriesii

Herpsilochmus longirostrisHerpsilochmus rufimarginatus frater

Microrhopias quixensisFormicivora serrana

Drymophila ferrugineaDrymophila ochromaDrymophila devilleiCercomacra cinerascens

Cercomacra nigrescenspyriglena leuconota

pyriglena leucopteraMynnoborus leucophrysMynnoborus m)VtherinusHypocnemis cantatorHypocnemoides maculicauda

Sclateria naeviaMynneciza loricataMynneciza hemimelaenaMynneciza atrothorax

Rhegmatorhina hoffinannsiHylophilax punctulataHylophilax poecilinotaPhlegopsis nigromaculataFormicarius colma amazonicus

Formicarius analis

Hylopezus berlepschi

ConopophagidaeConopophaga lineata

TyrannidaePhyllomyias virescens

# Ornithion inermeMionectes oleagineus chloronotus

Mionectes rufiventrisPhylloscartes ventralisCorythopis delalandi

Corythopis torquataMyiornis auricularisMyiornis ecaudatusHemitriccus minor

Hemitriccus diopsHemitriccus flammulatusHemitriccus zosteropsHemitriccus minimus# Hemitriccus striaticollis

Hemitriccus nidipendulum

IIIIBBIBB

16

BIRDS OF GALLERY FORESTS

Species Pattern Distance Habitat Diet

ATAMAMAMAMAMATAMATATAMAMAMAMAMAMAMATAMAM

AABAAAcAcAABAAABBBAA

BIIIEIIIIEEEEIIEBBBB

INININININININININININFIFIFIFIINFIFIFIFI

ATAMAMAMAMAMAMAMATAMATAMAM

EAAAAAcAAAAAA

FRFRFIFRFIFRFRFRFRFRFRFRFR

AMAMAM

AMAM

AAAAA

BEEEE

FIFRFRFRFR

AMAM

AA

EI

ININ

AMAM

BB

AA

FIFI

AM A B IN

AMATAMAMAMATATATAM

E OT

FI

FI

FI

FI

FI

FI

FI

FI

AcAABCCAA

BBBEEE

1bdirostrum poliocephalum

Ramphotrigon meEacephala megacephalaRamphotrigon rujicaudaRamphotrigon fuscicauda1blmomyias assimilis

Platyrinchus platyrhinchosOnychorhynchus coronatus swainsoniTerenotriccus erythrurusMyiobius barbatus mastacalisContopus cinereus cinereusKnipolegus orenocensisAttila bolivianusAttila spadiceus

Rhytipterna simplex frederici# Laniocera hypopyrra# Myiarchus tuberr:ulifer

Tyrannopsis sulphureaPachyramphus castaneus castaneusPachyramphus minor

Tityra semifasciata

PipridaeSchiffornis virescensSchiffornis turdinus amazonus > wallaciiPiprites chloris bolivianusTyranneutes stolzmanni

Neopelma sulphureiventerHeterocercus linteatus

Machaeropterus pyrocephalusManacus manacus subpurusIllicura militaris# Chiroxiphia pareola pareolaChiroxiphia caudataPipra nattereri# Pipra rubrocapilla

Cotingidae# Lipaugus vociferans

Xipholena puniceaGymnoderus foetidusQuerula purpurataCephalopterus ornatus

TroglodytidaeOdontorchilus cinereusMicrocerculus marginatus

Turdidae# Turdus fumigatusTurdus hauxwelli

PolioptilidaeRamphocaenus melanurus sticturus

EmberizidaeSporophila schistaceaArremon jlavirostris jlavirostris

Pitylus grossusCyanocompsa cyanoidesCissopis leveriana leverianaCissopis leveriana major

pyrrhocoma ruficepsHemithraupis ruficapillaHemithraupis jlavicollis centralis

17

CARDOSO DA SILVA

Pattern Distance Habitat DietSpecies

AMAMATATAMAMATAMAMAMATAMAMATATAMAMAMAMAMAMAM

EEEIIEEEEEEEEEEEEEEEEE

INFI

FIFIFI

FIFIFIFIFIFI

FIFIFI

FIFIFIFIFI

FIFIFI

AABcAcAAAABAAAAAAAAAAA

ATAMAM

AAA

IIB

INININ

AM

AMAMAM

AcAA

EEEE

ININININ

Lanio versicolorTachyphonus luctuosusTacbyphonus coronatus

Tricjjothraupis melanopsHabia rubica hesternaEuphonia laniirostris

Euphonia chalybeaEuphonia chrysopastaEuphonia minuta

Euphonia rufiventrisEuphonia pectomlisTangara mexicana bolivianaTangara chilensisTangara seledon

Tangara cyanaventrisTangara gyrolaTangara cyanicollis melanogasterTangara nigrocinctaDacnis lineataChlorophanes spiza caerulescensCyanerpes caeruleusCyanerpes cyaneus violaceus

ParulidaeBasileuterus leucoblepharusBasileuterus fulvicaudaGranatellus pelzelni

VireonidaeHylophilus thoracicus griseiventris

Hylophilus pectoralisHylophilus muscicapinusHylophilus hypoxanthusIcteridaePsarocolius bifasciatusCacicus cela

FIFI

AMAM

Ac

EE

18