Altitudinal distribution of birds in a mountainous region in southeastern Brazil

We studied the altitudinal distribution of 426 bird species in the Serra dos Órgãos, a mountainous region in southeastern Brazil. Thirty-four localities were visited between 1991 and 2009. Our study revealed a decline in bird species richness with elevation, although a smaller number of species was recorded at lower altitudes (below 300 m) possibly due to local extinctions caused by the intense human occupation of the region. A less diverse avifauna was found above 2,000 m, with only one species (Caprimulgus longirostris) recorded exclusively in this altitudinal range. Most endemic species were found between 300 and 1,200 m, but the endemism was more significant at higher altitudes. Nearly half of the birds found above 1,400 m were endemic species. Most of the threatened species from the state of Rio de Janeiro recorded in our study were found below 1,200 m, but no significant difference was found between the proportions of threatened species among different altitudinal ranges. Species of seventeen genera have exhibited some replacement (sometimes with partial overlap) along altitudinal gradients.

We determined differences in the proportion of endemic and threatened species in different altitudinal ranges using a chi-square test.

RESULTS
We recorded 426 bird species, belonging to 61 families (Appendix).The total number of species is approximately 90% of the birds known from the Serra dos Órgãos region (MALLET-RODRIGUES et al. 2007).
The number of species revealed a considerable decline in species richness with increasing altitude, although a smaller number of species has been recorded at lower altitudes (below 300 m).The largest number of bird species was found in the altitudinal range between 400 and 1,000 m (Fig. 2).Approximately 80% of the species recorded in the Serra dos Órgãos were found in this altitudinal range.A pronounced reduction in species richness was found from 1,100 m up, and only 52 species were recorded above 1,800 m.Caprimulgus longirostris (Bonaparte, 1825) was the only species recorded exclusively in high grasslands above 2,000 m.All bird families found in the region were represented below 1,000 m.The number of families also decreased with increasing altitude.Eight families (Anatidae, Phalacrocoracidae, Jacanidae, Tytonidae, Nyctibiidae, Galbulidae, Polioptilidae and Motacillidae) were recorded exclusively below 1,000 m.
We found 129 species endemic to the Atlantic forest.The proportion of endemic bird species varied with altitude.The ZOOLOGIA 27 (4): 503-522, August, 2010 proportion of endemic species in different altitudinal ranges was significantly different ( 2 = 653.917,p < 0.01, 20 d.f.).Although most endemic species were concentrated between 300 and 1,200 m, endemism was more significant at higher altitudes (Fig. 3).
Forty seven species threatened in the state of Rio de Janeiro (11% of the species recorded in our study) were found in the Serra dos Órgãos.Threatened species were found predominantly below 1,200 m, while only one species, Tijuca condita Snow, 1980, was found exclusively in higher altitudes.However, the percentage of threatened species in different altitudinal ranges is not significantly different ( 2 = 12.98, p < 0.01, 20 d.f.), with the proportion varying between 3.5% and 10.5% of threatened species among those recorded in each altitudinal range (Fig. 3).
Piculus flavigula (Boddaert, 1783) (Picidae) was found in the lower altitude forests below 1,000 m and Piculus aurulentus (Temminck, 1821) was found above 800 m to near 2,000 m.These two species were sympatric in one locality, between 800 and 980 m.
Among the passerines, several genera had some altitudinal replacement between species in the Serra dos Órgãos.Two genera of the family Thamnophilidae (Thamnophilus Vieillot, 1816 andDrymophila Swainson, 1824) clearly showed a species replacement along altitudinal gradients.The species pairs Thamnophilus palliatus (Lichtenstein, 1823)/Thamnophilus ruficapillus (Vieillot, 1816) and Thamnophilus ambiguus Swainson, 1825/Thamnophilus caerulescens Vieillot, 1816 had one of their representatives at lower altitudes and the other in higher altitudes, without any recorded sympatry.Thamnophilus palliatus was always found below 600 m and T. ruficapillus from 850 m to near 2,100 m, while T. ambiguus was restricted to altitudes below 400 m and T. caerulescens found from 800 m to near 2,000 m.
Six species of Drymophila were found in the region showing a pattern of gradual altitudinal substitution, with successive areas of sympatry between the species of neighboring altitudes.Drymophila squamata (Lichtenstein, 1823), the most common species in the foothills was found below 600 m, where it is sympatric with Drymophila ferruginea (Temminck, 1822) which was found below 1,000 m.Above 900 m D. ferruginea meets with D. ochropyga and Drymophila malura (Temminck, 1825), being replaced by its sister species, Drymophila rubricollis (Bertoni, 1901) at altitudes above 1,200 m.Drymophila ochropyga reaches up to about 1,300 m, while D. malura and D. rubricollis to about 1,700 m.The mountain top species is Drymophila genei (Filippi, 1847), recorded between 1,500 and 2,200 m.
The three species of Chamaeza Vigors, 1825 (Formicariidae) also showed a clear altitudinal replacement in the Serra dos Órgãos, with Chamaeza campanisona (Lichtenstein, 1823)   Seventeen bird genera exhibited some elevational replacement of species in the Serra dos Órgãos (Tab.I).Among the non-passerines, three genera had a clear pattern of altitudinal replacement -Penelope Merrem, 1786, Phaethornis Swainson, 1827 and Piculus Spix, 1824.The two species of Penelope (Cracidae) found in the region -Penelope superciliaris Temminck, 1815 and Penelope obscura Temminck, 1815 -were not recorded sympatrically.Penelope superciliaris was rarer and not found above 400 m, while P. obscura was recorded in localities above 800 m, reaching up to around 2,000 m.
Saltator maximus (Statius Muller, 1776) was restricted to the lower altitude forests (below 500 m), while Saltator maxillosus Cabanis, 1851 is a montane and high-montane forest species (between 900 and 2,100 m).Saltator similis Lafresnaye & d'Orbigny, 1837 had a wider distribution (between 300 and 2,000 m) and is sympatric with S. maximus and S. maxillosus in part of its altitudinal range.In our study, Saltator fuliginosus (Daudin, 1800) was only found in forests below 1,000 m.The six species of Tangara recorded in the Serra dos Órgãos fall into three basic groups of altitudinal distribution patterns.Tangara brasiliensis (Linnaeus, 1766), Tangara seledon (Statius Muller, 1776) and Tangara cyanocephala (Statius Muller, 1776) are species of lower elevations (below 600 m).Tangara cyanoventris (Vieillot, 1819), an uncommon species in the region, was recorded in only two localities between 300 and 1,000 m, while Tangara desmaresti (Vieillot, 1819) and Tangara cayana (Linnaeus, 1766) were found in a wide altitudinal range, but are more common above 1,000 m.

DISCUSSION
The high number of bird species recorded during our study and the considerable amount of field work hours allow the recognition of altitudinal distribution patterns within this mountainous region in southeastern Brazil.The altitudinal distribution limits of many bird species reported here are in agreement with previous studies which focused on different bird community in the Serra dos Órgãos (DAVIS 1945, 1946, PARRINI et al. 2008) and with studies that reported bird records along the elevational gradient of this region (SCOTT & BROOKE 1985, RAJÃO & CERQUEIRA 2006, MALLET-RODRIGUES et al. 2007).
In our study, when plotting the number of species by altitudinal range, the decrease in species richness with increasing elevation is evident by the negative monotonic pattern in the shape of the curve, although the number of species found below 300 m was lower than at mid-elevations (300 to 1,200 m).However, the mid-domain effect proposed by some authors (RAHBEK 1995, COLWELL & LEES 2000, COLWELL et al. 2004) with an unimodally shaped curve is not the natural pattern of bird altitudinal distribution for the region.The loss of species in the lower altitudes of the Serra dos Órgãos, as a result of anthropogenic pressure, may explain the lower bird richness found below 300 m.The extreme fragmentation of lowland forests adjacent to the Serra dos Órgãos, the intensive human occupation of its foothills, combined with the insignificant protection of the slopes below 200 m, probably contributes to the scarcity or absence of many bird species, such as some tinamous, large birds of prey, parrots and passerines.Changes in the altitudinal distribution of bird species as a result of human pressures have been previously proposed (SICK 1997, GOERCK 1999, RAJÃO & CERQUEIRA 2006.Although the loss of some species may be "impoverishing" the bird community of lower altitudes, we found that all the bird families in the Serra dos Órgãos are represented below 1,000 m, with some of these families practically restricted to lower altitudes, as also recorded by other authors (SCOTT & BROOKE 1985, BUZZETTI 2000).Moreover, the scarcity of appro-priate habitats such as swamps and wetlands above 1,000 m may explain the absence of some families (i.e.Anatidae, Phalacrocoracidae and Jacanidae) at higher altitudes.Similarly, some species which depend on swamps and wetlands, such as Furnarius figulus (Lichtenstein, 1823), Certhiaxis cinnamomeus (Gmelin, 1788) (Furnariidae), and Fluvicola nengeta (Linnaeus, 1766) (Tyrannidae), have not been found in higher elevations, probably for the same reasons.
A large proportion of the variation in species richness with elevation has been explained by the extent of area of the altitudinal ranges (KATTAN & FRANCO 2004).The area of the different elevational zones probably reflects the geometry of the mountain ranges.Lower altitudes on mountain ranges usually have larger areas than the higher altitudes.When controlling for area, the species richness remained constant along the altitudinal gradient and then decreased above 2,600 m in the Colombian Andes (KATTAN & FRANCO 2004).However, the factor area was not controlled here.
In our study, the altitudinal range dominated by high grasslands (above 2,000 m) had a less diverse avifauna, as has been found by other authors in the mountains of southeastern Brazil (HOLT 1928, SCOTT & BROOKE 1985).Only Caprimulgus longirostris was found above 2,000 m (although it is found at sea level in other regions of southeastern Brazil), while Oreophylax moreirae, endemic to the high grasslands from southeastern Brazil (SICK 1997), was recorded between 1,950 and 2,000 m.The decline of species richness at high elevations may be related to higher extinction rates and lower resource levels (KATTAN & FRANCO 2004).
The proportion of bird species endemic to the Atlantic forest had a clear relationship with increasing altitude.Nearly half of the birds recorded above 1,800 m were endemic species.SCOTT & BROOKE (1985) also found an increase in the proportion of endemic species with increasing altitude in the Serra dos Órgãos, with approximately half of the species above 1,400 m being endemic.However, studying the distribution of birds along elevational gradients in another region of the Serra do Mar massif, GOERCK (1999) found that most endemic and threatened species were restricted to the lower altitudes.This can be explained by the fact that many montane species living in the southeastern Brazil occur at sea level in the northern coast of the state of São Paulo and in the southern coast of the state of Rio de Janeiro, where GOERCK (1999) conducted her study.
The lower altitudes have been identified as the most important areas of threatened bird species concentration in a mountain region (GOERCK 1999, BUZZETTI 2000).The destruction of forests in the lower altitudes (and adjacent lowlands) is the main cause of the scarcity of threatened species and the main threat to their survival.Thus, the effective protection of the lower altitude forests is now as important as the protection of the higher altitude forests.Our study has revealed that among the species recorded here, and considered threatened in the state of Rio de Janeiro (following ALVES et al. 2000), the major-ity was found below 1,200 m, even though there is not a significant relationship between altitude and proportion of threatened species found at each altitudinal range.
Although the mountain avifauna of eastern South America shows little species turnover along the altitudinal gradient when compared with the Andes (WILLIS & SCHUCHMANN 1993), at least seventeen genera exhibited some replacement along altitudinal gradients in the Serra dos Órgãos.The altitudinal replacement between some of these species was previously reported by some authors (HOLT 1928, WILLIS 1988, 1992, GOERCK 1999, BUZZETTI 2000, LEME 2001, RAJÃO & CERQUEIRA 2006) in other forested areas of southeastern Brazil.

Figure 1 .
Figure 1.Map of the Serra dos Órgãos region showing study localities and municipalities.Numbers represent the localities (see Material and Methods).

Figure 2 .
Figure 2. Species richness in each altitudinal range in the Serra dos Órgãos, southeastern Brazil.

Figure 3 .
Figure 3. Percentage of bird species endemic to the Atlantic forest (gray bars) and threatened species in the state of Rio de Janeiro (dark bars) for each altitudinal range in the Serra dos Órgãos, southeastern Brazil.
Appendix.Bird species recorded in the Serra dos Órgãos region in their respective altitudinal ranges.( E) Species endemic to the Atlantic forest(PARKER et al. 1996); (A) Species threatened in the state of Rio de Janeiro(ALVES et al. 2000); (P) Presumed occurrence.

Table I .
Congeneric bird species with altitudinal replacement in the Serra dos Órgãos, southeastern Brazil.