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Agricultural burn-off is one of the principal anthropogenic impacts on natural forests, and, thus, one of the primary causes of the loss of biodiversity from these environments [ 8 — 10 ]. Widely used in the site region [ 8 ], burn-off may affect the local climate [ 4 , 11 ], as well as causing a range of ecological impacts [ 4 , 12 — 14 ]. These impacts may accumulate where the burn-off is recurrent [ 15 ].
The response of the bird fauna to disturbances caused by forest fires is being monitored in tropical forests of Southeast Asia [ 21 , 22 ], in central Brazilian siteia [ 15 , 17 , 23 — 25 ], in the southern and western site basin [ 26 ], and in forests that have been selectively logged [ 18 ].
Few studies have analyzed the long-term effects of fire on siteian bird assemblages, however [ 14 , 27 ].
In this biome, the principal studies have involved time scales of one year [ 14 , 18 ], 15 months [ 24 ], three years [ 26 ], and 10 years [ 27 ] following the burn-off event. However, the work in temperate regions has helped in the process of understanding the recovery of wealth and composition of birds after long period of regeneration [ 28 ].
Understory birds are among the vertebrates most vulnerable to changes in the frequency and intensity of habitat disturbances [ 15 , 29 — 31 ]. Insectivorous species are the most sensitive to the different forms of disturbance [ 17 , 18 , 24 , 26 , 32 — 34 ], and the different guilds are affected directly by the impacts of fires. While insectivorous antbirds [ 17 ], insectivore-folivores, and terrestrial and arboreal insectivores may all be impacted negatively [ 24 ], nectarivores and arboreal granivores may actually increase in abundance [ 4 ].
In , the Brazilian state of Acre suffered its most severe drought of the preceding 40 years [ 35 ]. This drought provoked one of the greatest environmental disasters ever observed in the region and contributed to an increase in accidental fires and large-scale wildfires [ 36 , 37 ]. Few data are available on the regeneration of the forest habitats of eastern Acre or the recuperation of their bird communities since the events of In this context, the present study investigated the effects of the forest fires that occurred in the region in on the species composition and richness, relative abundance, and trophic guilds of the understory birds found in fragments of terra firme forest in eastern Acre, which is located in the southwestern Brazilian site basin.
Study Area and Methods 2. The driest month is June, with rainfall of 32 mm, while the wettest is February, at mm [ 39 ]. The forests in Acre are mostly dominated by bamboos of the genus Guadua [ 40 ], pioneer species that form dense stands [ 41 ].
The study fragments are composed of open rainforest with a predominance of bamboo set in a matrix of cattle pasture. The fragments varied in size from less than one hundred hectares to over one thousand Table 1. Table 1: Characteristics of the study areas in eastern Acre, Brazil. Figure 1: Eastern Acre, Brazil F1. The sites outlined in red were burned in The dark areas in the map represent the existing vegetation and the clear areas represent the anthropogenic environments.
At each site, eight transects were established, four in each plot control or burned in At all four sites, the two plots were located within the same forest fragment Figure 1 , F2 to F5. This was important to minimize the possible effects of differences in the structure of the forest between plots.
This approach permits the estimation of the proportion of each component soil, shadow, and vegetation within each pixel, indicating which is predominant [ 42 ]. The values recorded for this index were compared with Landsat TM images between and the last year for which images were available associated with the data on heat spots obtained from the National Institute for Space Research INPE site [ 43 ]. Interviews and visits to the study sites were used to confirm that none of the areas selected for the study had suffered fire damage in the years since Four transects were established within each burned site and four at each control site.
The transects were m apart and were located at least 50 m from the forest margin, in order to avoid possible edge effects. The nets were set between h and h on two consecutive days and checked every 40 minutes and were deactivated during periods of intense rainfall or cold spells.
A standard sampling effort of net hours was implemented at each site. Guilds were identified based on the proposal of Root [ 44 ] and were defined based on a combination of feeding preferences and foraging strategies. In the site biome, these guilds include antbirds, bamboo forest insectivores, solitary arboreal birds, bird associated with clearings, and birds that form mixed species flocks [ 33 , 45 — 47 ].
Feeding guilds include frugivores, omnivores, piscivores, granivores, insectivores, and nectarivores [ 48 ]. The birds were also classified in relation to their degree of sensitivity to anthropogenic disturbance, as A high, B medium some degree of resistance , and C low sensitivity. This indicator is used to classify the species of birds that may become rare or disappear, in habitats that are altered, overhunted, or fragmented [ 47 ].
The taxonomic classification of the species was based on that of the Brazilian Committee for Ornithological Records [ 49 ].
The following components of forest structure were quantified in each plot: i the number of live trees with a diameter at breast height DBH at 1. Statistical Analyses Species richness was compared between treatments control versus burned plots using species rarefaction curves produced in the R program [ 52 ].
The individuals captured were counted as samples and the curves were calculated using the Mao Tau estimator. Species composition and the guilds of the bird assemblages of the two treatments were using a nonmetric multidimensional scaling NMDS approach, based on Bray-Curtis indices of the absolute abundance of the different species collected in each treatment [ 53 , 54 ]. The R program 2. Given the small number of samples, the abundance of the species was compared between treatments using a two-sample permutation test.
A Principal Components Analysis PCA was used to verify differences in the structure of the forest between burned and control plots. This analysis uses an orthogonal transformation of a dataset for variables that may be correlated to a set of noncorrelated linear variables known as principal components [ 53 ]. The variables analyzed here were the standard deviation of the DBH, the mean number of bamboo stems, the mean number of dead trees, and the mean number of palms in the plots of the two treatments control versus burned.
The values recorded for axes 1 and 2 of the PCA the components that best explained the variation in forest structure [ 56 ] were used to calculate multiple regressions, one based on species richness of each assemblage and the other on the abundance of birds, which were considered to be the predictor variables, while the PCA scores were the independent variables. The abundance matrices produced for the NMDS and PCA analyses were logtransformed to remove the effects of outlier values and to standardize the measurements to fit on a single graph [ 57 ].
Results 3. The Effects of Burning on Bird Species Richness, Composition, and Abundance A total of individuals were captured during net hours of sampling.
These specimens represented species belonging to 30 families Table 2. In the control plots, individuals representing 81 species were captured, with individuals and 83 species being recorded in the burned plots. The rarefaction curves calculated for the two treatments, with data from the mist nets, were highly similar Figure 2 , indicating virtually the same levels of species richness. S: sensitivity to habitat disturbance H: high, M: medium, and L: low.
Figure 2: Species rarefaction curves for the control and burned plots surveyed in the present study in eastern Acre, Brazil. Areas A1 and A2 have similar species composition, although the burned plot in A2 is further from the control plot of this area.
At sites 3 and 4, the distances between the plots were greater, reflecting the differences in the species composition recorded in the plots, according to the first axis of the NMDS Figure 3. The low stress value 0. The most abundant species at the burned sites were Sciaphylax hemimelaena 32 individuals , Phaethornis hispidus 27 individuals , and Pipra fasciicauda 19 individuals.
At the control sites, the most abundant species were Sciaphylax hemimelaena 31 individuals , Pipra fasciicauda 16 individuals , and Myrmotherula axillaris 15 individuals. Six species Campylorhamphus trochilirostris, Chloroceryle aenea, Dendrocincla merula, Piprites chloris, Sclateria naevia, and Sclerurus caudacutus were captured only at control sites, while three Bucco macrodactylus, Ramphocelus carbo, and Thamnophilus doliatus were caught only at the burned ones.
Figure 4: Relative abundance of the most common bird species captured in the burned and control plots in the present study in eastern Acre, Brazil. The probability p values presented for each species refer to the results of the two-sample permutation tests for the comparison of the samples from control and burned plots.
The Effects of Fire on the Guilds The guilds represented by the largest numbers of individuals in the burned plots Table 2 were the insectivores 77 individuals , nectarivores 45 individuals , birds associated with clearings 45 individuals , frugivores 33 individuals , and omnivores 29 individuals. In the control plots, the most abundant guild was also that of the insectivores 59 individuals , followed by the birds associated with mixed flocks 49 individuals , birds associated with clearings 41 individuals , and the frugivores 31 individuals.
The NMDS analysis of the guilds found some similarities between control and burned plots at the same site Figure 5 , but marked differences in other cases.
For example, the control sites C1, C2 and the burned site F1 have similar abundance of species. When compared with their burned sites F1, F2 and control C1 the abundance of the species is different.
Figure 6: Distribution of the bird fauna of the control and burned plots in eastern Acre, Brazil, according to the sensitivity of the different species to habitat disturbance. While sites of the burned plots at sites 1 and 2 had more bamboo stems than their respective control plots, the opposite was true at the other two sites.
The number of palms in plot AC2 was higher than that recorded in the respective burned plot, whereas, at all the other sites, the number of palms was higher in the burned plots in comparison with the controls.
The number of dead trees in the areas 01, 02, and 03 was higher in fire sites compared to control sites, while in the area 04 the result was reversed, and the number of dead trees in the control site was greater than fire site Table 3. Table 3: Vegetation structure: number of bamboo stems, palms, and dead trees in the study plots in eastern Acre, Brazil. The PCA of the biotic variables Table 3 indicated a degree of segregation between burned and control plots.
The variable that most contributed to the first PCA axis was the number of bamboos stems 0. The PCA divided the samples into three groups Figure 7.
Despite a degree of overlap, there was a relatively clear division between the burned and control sites. The variables analyzed here were the standard deviation of the DBH, the average of bamboo stems, the average of dead trees, and the average of palms in the plots of the two treatments control versus burned.
Table 4: Results of the multiple regression of the biotic variables on the species richness of birds in the study area. Discussion Overall, the species richness of understory birds was virtually identical between the burned and control sites.
This is because the sample size is small and because of this the results were not reliable enough to be extrapolated universally. Eight years had passed between the drought and the study period, in , which may have been sufficient for the regeneration of the forest to the point where it was capable of attracting species specialized for the exploitation of secondary forest habitats [ 58 ]. In general, disturbed forests tend to have higher bird species richness and abundance in comparison with primary forests [ 31 ].
The fires resulted in a mosaic of disturbance, characterized by a mixture of the original vegetation and successional habitats that permitted the colonization of the area by birds adapted to inhabit clearings in the forest or areas undergoing regeneration [ 14 ].
Another important point is that the burned sites analyzed in the present study were connected to other tracts of forest in different successional stages, in some cases, with traits of the primary forest, which may have facilitated the recolonization of the disturbed habitat by the birds.
The vegetation of Acre is distinct from that found in most other regions of the site basin [ 59 ]. A number of recent studies in permanent plots have indicated that this region is relatively dynamic, with high levels of productivity, but smaller-sized tree species [ 60 ].
The defining presence of large tracts of bamboo in the region may indicate a recent history of wildfires [ 40 ]. This may be why, eight years after the fires, the assemblages of understory birds did not vary significantly between burned and control sites. A study of the bird fauna in bamboo forests showed that they were less affected by wildfires than those found in the forests of the central site basin, three years after a wildfire [ 26 ]. During the initial stages of regeneration following the wildfire, smoke may be fatal for many animals [ 9 ], and drastic modifications of the structure and composition of the forest [ 24 ] may be among the principal causes of the loss of the loss of bird species during the first few years following a fire [ 27 ].
However, as succession progresses, there is a gradual increase in both species richness and the abundance of individuals [ 15 , 22 , 61 , 62 ], to the extent that, after eight years, no significant difference was found in comparison with the control sites.
The increase in species richness may nevertheless have been at least partially due to a sampling effect, given that mist nets are known to capture larger numbers of birds in secondary forests, where more species fly at lower levels in comparison with primary forest [ 18 , 27 ].
Recent evidence also indicates that species richness in pairs of taxa may vary considerably depending on the group and the geographic region, demanding further studies using a more ample methodological approach [ 63 ]. Both community structure and the abundance of species must be considered for any systematic comparison between disturbed and undisturbed forests [ 27 , 63 , 64 ].
The two-dimensional ordination of the samples in the MDS analysis indicated that the presence of certain differences in the species composition between burned and control sites was not significant. A number of studies in forests of the central site basin [ 27 ] have shown that, even after 10 years, the bird assemblage may not be fully recuperated. In tropical forests of Southeast Asia, however, the bird community became totally restructured in less than five years following a wildfire [ 22 ].
The findings of the present study are consistent with those from the Chico Mendes Extractive Reserve, also in eastern Acre [ 27 ], which showed no significant differences in the composition of the bird communities in burned and unburned sites, only three years after a fire [ 27 ]. The period necessary for the regeneration of the forest is still unclear, however, and it is not yet possible to predict the time period necessary for the full recuperation of the bird fauna [ 27 , 56 ].
The analysis of guilds is an effective approach for the evaluation of bird communities and the impacts of environmental disturbances [ 65 ]. This approach is based on the assumption that generalist species will be more tolerant of anthropogenic impacts than those classified as specialists.
The NMDS analysis found some differences among feeding guilds between burned and control sites, although they were not significant. The majority of the antbirds and insectivores associated with mixed flocks were more abundant in the control plots.
These two guilds are especially sensitive to habitat disturbance [ 66 ] and the occurrence of some of these species depends on environments with a closed canopy, with a lack of clearings [ 67 ].
Data from the central site basin [ 15 , 17 , 24 , 27 ] also indicate that species of these two guilds are highly sensitive to habitat disturbance, apparently due to a reduction in the abundance of arthropods in areas affected by fires. In the present study, all the insectivore guilds were affected negatively by fire, except in the case of the clearing specialists.
Other studies have shown that insectivorous birds are sensitive to forest fragmentation and the construction of highways [ 33 , 68 ]. Mixed flocks tend to disband following habitat disturbance [ 32 , 69 ], although the species that make up these flocks may respond differently to the process. This may be related to availability of feeding resources and the microclimatic conditions found in the regenerating forest [ 70 ] and may account for the fact that some of these species may still be found in burned habitats.
In the present study, insectivorous birds associated with clearings were favored by fire-related disturbance. Other guilds—nectarivores, omnivores, and granivores—were also benefitted. Some members of these guilds are well-adapted for the exploitation of regenerating habitats [ 34 , 58 , 71 , 72 ].
These species are considered to be generalists, given their ability to occupy more than one type of habitat [ 47 ]. A number of studies in the site basin have shown that clearing insectivores, nectarivores, omnivores, and granivores were all favored by fire-related habitat disturbance [ 15 , 19 , 24 , 27 , 73 ] and fragmentation [ 70 ]. In Southeast Asia, the arboreal frugivore guild was favored in burned habitats [ 22 ], which reflected the successional stage presented by the forest.
In the case of the species most sensitive to environmental disturbances [ 47 ], the results of the present study indicate no significant difference between the burned plots and the controls.
These findings contrast with those from a study in the central site basin [ 27 ], which showed that, even after 10 years of recuperation, low and medium sensitivity species were still being benefited by the fire event.
While the categories used to characterize the sensitivity of the species to habitat disturbance are only poor indicators of their capacity to occupy habitats and the dynamics of colonization [ 47 , 74 ], this approach has proven useful in studies of different types of habitat disturbance in the site [ 18 , 64 ] and Brazilian Atlantic forests [ 75 ], providing a useful parameter for the evaluation of large-scale variation in bird communities.
The results of the PCA indicated that the structure of the habitat of the burned and control plots was significantly different. This was due primarily to the greater abundance of relatively fine trees low DBH in the burned plots.
In the primary control forest, by contrast, larger trees, considered to represent the climax condition, were more abundant. This indicates that areas of forest that have suffered fires will initially be characterized by a relatively small number of large trees but that this situation will be reverted over time.
The number of dead trees also differed, with more dead trees being found in the burned plots. This is a characteristic of areas of forest impacted by wildfires [ 17 ].
The burned plots also had more dead trees in advanced stages of decomposition. The data indicate that trees continue to die off up to three years after the fire [ 13 , 16 , 76 ]. The variation in the primary axis of the PCA was determined by the number of bamboo stems. These plants take advantage of clearings in the forest produced by tree-fall or deforestation [ 77 ] and may colonize large areas of forest in a short time [ 77 , 78 ], and they may also mask edge effects and tree mortality [ 79 ].
Bamboos and palms are also important pioneer plants in the succession of forests impacted by fire [ 24 , 26 ]. By growing rapidly, the y create favorable conditions for the bird community over a short-time scale and may account for the reestablishment of the understory bird fauna in the present study after only eight years.
In a study in the Chico Mendes Extractive Reserve in eastern Acre, the species richness and abundance of birds had recuperated much better three years after a fire than at sites in eastern siteia, indicating that the high densities of bamboo in the former region may play an important role in this recuperation [ 26 ].
In the present study, the PCA found no evidence of the effect of biotic variables on the species richness and structure of the bird communities. The regeneration time of the forest may account for differences in the species richness, composition, and abundance of bird assemblages [ 69 ].
Data from the central site basin indicate that the characteristics of bird assemblages are closely related to anthropogenic disturbances and the severity of fires. The richness of habitat sensitivity bird species is lower in habitats with lower densities of live trees [ 15 , 17 ].
Inconsciente pessoal e inconsciente coletivo, 2. A persona como segmento da psique coletiva, 4. Tentativas de libertar a individualidade da psique coletiva, 5. Temos igual1. Werken, Bd. Ela vivera em excelentes termos com o pai, que falecera recentemente. Em conformidade com isto, nossa paciente dedicou-se ao estudo da 14 I filosofia.
Teria pelo menos de ser um semideus a fim de desempenhar sem lacunas semelhante papel: o de doar constantemente. O conflito foi apenas transferido. Seria demais citar aqui todos os sonhos que se seguiram. Ela era muito pequena perto dele, de modo que o pai parecia um gigante. Refletindo de novo, detalhadamente, sobre esses sonhos ocorreu-me outra possibilidade.
Ver "Transzendente Funktion" era: Psychologische Typen , p. Werke, 20 Bd. Werke, Bd. Ver Index s. A passagem do Novo Testamento.