Climate stability and the current patterns of terrestrial vertebrate species richness on the Brazilian Cerrado

Quaternary International 222 (2010) 230–236

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Climate stability and the current patterns of terrestrial vertebrate species richness on the Brazilian Cerrado Matheus de Souza Lima-Ribeiro a, *, Jose´ Alexandre Felizola Diniz-Filho b, Maira Barberi c a

´s, Rua Riachuelo, no. 1530, Cx. Postal 03, Setor Samuel Graham, Jataı´, GO 75804-020, Brazil ˜o de Cieˆncias Biolo ´gicas, Campus Jataı´, Universidade Federal de Goia Coordenaça ´ s, Cx. Postal 131, Goia ˆnia, GO 74001-970, Brazil Departamento de Biologia Geral, ICB, Universidade Federal de Goia c ´s, Cx. Postal 86, Goia ˆ nia, GO 74605-010, Brazil ´ rio de Paleoecologia, MCAS, Universidade Cato ´ lica de Goia Laborato b

a r t i c l e i n f o

a b s t r a c t

Article history: Available online 21 October 2009

New indices of the historical environmental stability that underlies palynological data presented here show how much the climate and vegetation has changed over the late Quaternary, and tests the relationships between climate stability and the current patterns of terrestrial vertebrate species richness on the Brazilian Cerrado. Three historical environmental stability indices have been developed from palynological studies available in the primary literature. Correlation analyses were used to quantify the strength of the relationships among the three historical stability indices, as well as between the indices, species richness, and the latitudes of pollen-based records. The three historical stability indices are positively related to one another in that they have strong and significant correlations in all cases. However, there is no meaningful correlation among the historical stability indices, species richness and latitude. The new indices are spatially concordant throughout the Brazilian Cerrado, revealing that palynological data are efficient datasets with which to assess the climate stability during the late Quaternary, but they do not support the historical hypothesis that higher environmental stability allows a greater accumulation of species. Environmental stability as an underlying mechanism responsible for the maintenance of the broad-scale latitudinal gradients in species richness is not supported for the terrestrial vertebrates of the Brazilian Cerrado. Ó 2009 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction Diversity gradients between tropical and temperate-polar regions are among the most prominent patterns in ecology and biogeography, and multiple processes have been implicated in their origin and maintenance (Brown and Maurer, 1989; Blackburn and Gaston, 2003; Willig et al., 2003). Empirical analyses of large-scale species richness patterns have shown that both current factors such as the water-energy dynamic, plant productivity, and topographic relief, and historical factors such as climate changes (glaciations), evolutionary processes (speciation and extinction), and geological changes (tectonic uplift and sea-level change), are important mechanisms in explaining the origin, maintenance, and distribution of species diversity in the world (Gaston and Blackburn, 2000; Willis and Whittaker, 2002; Hawkins and Porter, 2003; Willig et al., 2003; Hawkins et al., 2005; Arau´jo et al., 2008).

* Corresponding author. Tel.: þ55 064 3632 1510; fax: þ55 064 3632 0002. E-mail addresses: [email protected] (M. de Souza Lima-Ribeiro), [email protected] (J.A. Felizola Diniz-Filho), [email protected] (M. Barberi). 1040-6182/$ – see front matter Ó 2009 Elsevier Ltd and INQUA. All rights reserved. doi:10.1016/j.quaint.2009.10.003

The influence of the present-day climate (e.g., the water-energy hypothesis) on large-scale patterns of species richness has been firmly established (Kerr and Currie, 1999; Allen et al., 2002; Willig et al., 2003; Hawkins et al., 2003a, 2005; Diniz-Filho et al., 2004; Kaspari et al., 2004), but the historical factors have been poorly incorporated into analyses. Although researchers have used a number of approaches to assess the influence of historical factors, these analyses have been generally insufficient in explaining the global patterns of species richness (Kerr and Currie, 1999; Diniz-Filho et al., 2004; Hawkins et al., 2005, 2006). However, few studies have tested the relationship between the historical events linked with past climate changes and current patterns of diversity (Hawkins and Porter, 2003; Arau´jo et al., 2008). This is expected because the contemporary climate is a cumulative result of the events that occurred in the past (Crowley and North,1991) and is a good predictor of species richness (Willig et al., 2003). Nevertheless, the possibility of conducting such a comparative test has been hampered by difficulties in generating quantitative estimates of past climate events with which to undertake analyses (Arau´jo et al., 2008). Hawkins and Porter (2003) used the historical pattern of glacial retreat during the most recent ice age to quantify the length of time

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during which different regions of the northern half of North America were exposed for potential recolonization by terrestrial organisms, and to test the influence of the historical climate in the current species richness of mammals and birds on the northern Nearctic. Arau´jo et al. (2008) used climate simulations for the Last Glacial Maximum (LGM) and the contemporary climate to test the hypothesis that the gradients of richness of European reptiles and amphibians can be determined by past climate changes. Both studies found that, although contemporary energy inputs explain much of the variance, there is a detectable historical sign in the diversity gradients of these groups (Hawkins and Porter, 2003; Arau´jo et al., 2008). One advantage of the historical analyses conducted by Hawkins and Porter (2003) is that there is solid evidence, rather than a possibly inaccurate model, for where and when different areas were deglaciated and colonized. However, these analyses were restricted to a short span of history (the last 20 ka) and to parts of the world where the land was completely buried under ice during the most recent glacial maximum. Even so, more analyses are necessary to examine the effects of climate change operating over longer time periods than 20 ka and in tropical lands that were not buried under ice sheets during the last glaciation. These analyses can be made with palaeoecological data, which can support analyses that may be useful in establishing the historical factors that drove the origin and still drive the maintenance of diversity patterns (Tallis, 1991; Behrensmeyer et al., 1992). Palaeoecological reconstructions can provide data about past climate and environment (Delcourt and Delcourt, 1991), particularly the vegetational and climatic shift sequence through the Quaternary (Faegri et al., 1989), and can reveal the level of environmental stability in this time period (Crowley and North, 1991). This paper considers how the level of environmental stability through the late Quaternary (ca. 50 ka to present) can be revealed through palynological data and whether the current patterns of species richness of terrestrial vertebrates in tropical areas can be explained by past climate change. The focus is on the part of South America covered by the Cerrado biome in Central Brazil in order to develop new indices of the historical environmental stability that underlies palynological data. The indices developed show quantitatively and qualitatively how much the climate and vegetation has changed over time. These indices’ relationships with the current patterns of species richness of terrestrial vertebrates are tested in order to test the hypothesis that the richness and historical stability indices are spatially concordant. More specifically, some studies have shown that areas that are climatically stable over time (e.g., tropical areas) are often characterized by high levels of contemporary energy and water-energy (Fjeldsa¨ and Lovett, 1997; Willig et al., 2003; Hawkins et al., 2005), so these regions have higher species richness in the present (Willig et al., 2003). The validity of this hypothesis for the terrestrial vertebrates of Brazilian Cerrado is assessed by investigating the correlation among historical climate stability, latitude, and species richness. The validity of this test depends on the accuracy of the palynological data in representing the historical environmental stability. In the first instance, the climate changes of the last 50 ka do not reflect the full cycle of the more recent ice age and are not relevant for speciation (Mayr, 1954) or sufficiently representative of the much longer period during which diversity was developed (Blackburn and Gaston, 2003). However, the time period that includes the late Quaternary is relevant because it comprises an amount of taxa migration events and the geographical rearrangement of species already existent in South America in response to prolonged climate changes (Salgado-Labouriau, 1997; Colinvaux et al., 2000, 2001), and is sufficiently representative for assessing the influence of the historical climate on the species richness on a longer time period than only the LGM (the last 20 ka). Moreover, pollen records longer

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than 50 ka that would allow assessments of the environmental stability (or climate changes) are not available in the Brazilian Cerrado. However, the present exercise reflects a first effort to develop indices of historical environmental stability from palynological records for a tropical region. 2. Materials and methods 2.1. Regional setting The Cerrado biome, located in tropical South America between 3 –24 S and 41 –63 W, covers about 22% of the Brazilian territory, corresponding to 2 million km2 on the Neotropical biogeographic region. This region is characterized by several phytophysiognomies, including forest, savanna and shrub-grassland vegetation. Eiten (1972, 1986) explained that the Cerrado biome as a whole is not a savanna, but that savannic physiognomies are present. Thus, in spite of structural similarity to savannic physiognomies, the Brazilian Cerrado has faunal and floral composition and ecological relationships different from other known savannas, such as the African savanna and the Venezuelan Llanos (see Eiten, 1986 and Ribeiro and Walter, 1998 for more details about the terminology of the phytophysiognomies) The large variety of phytophysiognomic forms in the Brazilian Cerrado is due to various biotic and abiotic factors: grazing, seasonal precipitation, soil fertility, moisture and drainage, fire regime (Eiten, 1972) and the climatic fluctuations of the Quaternary (Salgado-Labouriau, 1997). In addition, its central position in South America favors contact with other large biomes that constitute an important ecological corridor (Meio´ et al., 2003). These biomes include the Amazon forest to the north; Caatinga, the deciduous xerophytic vegetation of the semiarid region, to the northeast; the Atlantic forest to the south–southeast and along the Atlantic Ocean coast; and the Araucaria forest to the south. Climate changes of the late Quaternary appear to have favored the dispersion of typical species of these geographically adjacent biomes, forming a phytophysiognomic mosaic in Central Brazil (Salgado-Labouriau, 1997). In addition to its wide latitudinal and longitudinal range, the Brazilian Cerrado varies in elevation from 100 m in the pantanal (wet plains on the western border) to 1500 m above sea level in some of the more elevated tablelands of the Central Plateau (Motta et al., 2002). There is a remarkable variation in the average annual temperature across the region, ranging from 18 to 28  C. Rainfall also varies widely, from 800 to 2000 mm, with a strong dry season during the southern winter (approximately April–September) (Nimer, 1989). 2.2. Sampling The current species richness of terrestrial vertebrates and the palynological data for the Brazilian Cerrado were compiled from various sources, mainly primary literature. The data on the vertebrate species richness of the Brazilian Cerrado range categorizes the richness of mammals, birds, reptiles and amphibians into 181 equal-area cells with spatial resolution of 1 grid cells (Fig. 1) (see http://www.ecoevol.ufg.br/laboratorios/lets/; Diniz-Filho et al., 2006, 2008 for details about the richness data). The palaeoclimatic data were obtained from 15 reports of palynological studies with emphasis on palaeoecological reconstruction in the late Quaternary of the Brazilian Cerrado and its boundary areas (Fig. 1). These pollen-based records were used to estimate three Historical Environmental Stability Indices (HESIs). The HESIs indices are not interpolated over grid cells that lacked any direct historical record because of the relatively few palynological records available for the Brazilian Cerrado. Therefore, the five pollen-based records outside

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Fig. 1. Distribution of the 181 cells used to analyze the spatial richness of terrestrial vertebrate and the geographical location of the 15 pollen-based records in the Brazilian Cerrado. These pollen-based records are: 1. Icatu´ River (BA) – De Oliveira et al., 1999 – (10 240 S/43 130 W); 2. Lagoa da Confusa˜o (TO) – Behling, 2002 – (10 380 S/49 430 W); 3. A´guas Emendadas (DF) – Barberi et al., 2000 – (15 340 S/47 350 W); 4. Lagoa Bonita (DF) – De Oliveira et al., 2005 – (15 350 S/47410 W); 5. Meia Ponte River (GO) – Lima-Ribeiro et al., 2004 – (16 200 S/49 300 W); 6. Cromı´nia (GO) – Ferraz-Vicentini and Salgado-Labouriau, 1996 – (17 170 S/49 250 W); 7. Lago do Pires (MG) – Behling, 1995 – (17 570 S/42 130 W); 8. Serra Negra (MG) – De Oliveira, 1992 – (18 490 S/46 150 W); 9. Lagoa dos Olhos (MG) – De Oliveira, 1992 – (19 200 S/43 370 W); 10. Lagoa Santa (MG) – Parizzi et al., 1998 – (19 380 S/43 540 W); 11. Serra do Salitre (MG) – Ledru, 1993 – (19 430 S/46 190 W); 12. Catas Altas (MG) – Behling and Lichte, 1997 – (20 050 S/43 220 W); 13. Morro de Itapeva (SP) – Behling, 1997a – (22 470 S/ 45 320 W); 14. Jacareı´ (SP) – Garcia et al., 2004 – (23 170 S/45 580 W); 15. Serra de Campos Gerais (PR) – Behling, 1997b – (24 400 S/50 130 W).

the Cerrado biome grid, as shown in Fig. 1, were used in this analysis to maximize information for the HESIs indices. 2.3. Historical Environmental Stability Indices The first Historical Environmental Stability Index (HESI1, hereafter) measures the relative frequency of climatic changes in the late Quaternary. The climate of the late Quaternary is divided into the five classes established by Salgado-Labouriau (1997): cold/dry, warm/dry, cold/wet, warm/current wet and warm/wettest. Then, the sequence of climatic change is systematized on a linear timescale for each pollen-based record (see climate change sequence for all pollen-based records in Supplementary Material, Fig. S1). The HESI1 index was obtained by dividing the number of climate changes by the time periods of the respective pollen-based record, where the timescale was gauged per thousand years. Therefore, this index represents only the frequency (quantitative measurement) of climatic changes through time for the 15 pollen-based records of the Brazilian Cerrado and does not consider the productivity of the five past climatic types. The second Historical Environmental Stability Index (HESI2, hereafter) was also developed to evaluate the sequence of climatic changes, but it uses a qualitative measurement of productivity of the climatic types that occurred in the late Quaternary. For this task, the productivity mean for each climate type was determined, as previously established for HESI1 index (see Supplementary

Material, Fig. S1). The analyses used the actual evapotranspiration (AET), a widely recognized measure of productivity balance that represents the joint availability of energy and water in the environment (see Currie, 1991; Diniz-Filho et al., 2003; Hawkins et al., 2003a, b) as an estimation of productivity. The average AET for the various current climatic domains of South America was estimated, and the productivity of the Quaternary’s climate types (cold/dry, warm/dry, cold/wet, warm/current wet and warm/wettest) compared to the productivity of the Ko¨ppen climate types BWk (on eastern Patagonia and northern Chile), BSh (on Caatinga biome, northeast Brazilian), Cfa (on northeast Argentinean and southern Brazilian), Aw (on Cerrado biome, Central Brazil) and Af/Am (on Amazonian forest, northern South American), respectively (see the synthesis of Ko¨ppen–Geiger climate classification in Peel et al., 2007.) From this comparison and based on the tropical geographic localization of Brazilian Cerrado, productivity is more influenced by the water regime than by energy. According to Hawkins et al. (2003b) and Whittaker et al. (2007), energy is the limiting component of the ecological interactions in high latitudes, whereas, in lower latitudes, water is the key limiting component. In fact, the productivity of the Quaternary’s climate types follows this criterion, as shown in the AET values: cold/dry (AET ¼ 240), warm/dry (AET ¼ 814), cold/wet (AET ¼ 1021), warm/current wet (AET ¼ 1139) and warm/wettest (AET ¼ 1453). This quantitative classification indicates that the warm/wettest climate is more

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productive than any other climatic type, and it has a productivity level approximately six times higher than the cold/dry climate. After establishing the expected productivity (AET value) for each Quaternary climate type, the sequence of the past climate types (as shown in Fig. S1, Supplementary Material) was classified under the productivity for each pollen-based record in the Brazilian Cerrado, and obtained an amount of productivity for each climate phase over time by multiplying its AET value by time period in which it occurred. Next, the HESI2 index was calculated from the coefficient of variation among the climate productivity measurements in each pollen-based record on the Brazilian Cerrado, divided by the time period of the respective pollen record, where the timescale was gauged per thousand years. Thus, this index represents an estimate, independent of the unit of measurement, of the amount of productivity variation through time, in terms of environmental changes among very different climatic types (see Sokal and Rohlf, 1995, for details on coefficients of variation). In other words, if a pollen-based record presents climatic types that vary widely based on the productivity classification, the coefficient of variation (and, consequently, the HESI2 index) should be higher as a result of the greater differences among the productivity classes. The third Historical Environmental Stability Index (HESI3, hereafter) was obtained directly from pollen diagrams, without a previous palaeoecological/palaeoclimatic interpretation of palynological data, such as the sequence of climatic changes over time that were previously established in the papers with pollen records (Fig. S1, Supplementary Material) and used here for the two previous indices (HESI1 and HESI2). The pollen percentage diagrams were used to obtain the relative frequency of pollen taxa every thousand years along the stratigraphic profile for each pollen-based record analyzed. Pollen taxon that reflect the local vegetation (such as aquatics), that do not indicate a specific vegetation or climate type, or that are poorly represented in the diagrams (low total pollen) were often excluded from the analyses. Using pollen percentage diagrams may appear to be a dangerous and inaccurate way to access the representation of the pollen taxa over time and, consequently, to estimate the HESI3 index because the relative frequency curve of any pollen taxa shows significant noise (see Faegri et al.,1989 for details). As a result of the ‘‘percentage effect’’, a noise on the curve of any pollen taxon is transplanted to all other pollen taxa, and the relative frequency curve of all pollen taxa may include a significant part of the noise from each pollen taxon. This noise transplant does not occur in the pollen concentration diagrams because each pollen taxon is represented independently of others. Nevertheless, pollen percentage diagrams were used because most papers with pollen-based records in the Brazilian Cerrado have not presented pollen concentration diagrams. The relative frequency of pollen taxa over time was then ordered by a detrended correspondence analysis – DCA (Hill and Gauch, 1980), and the dispersal of scores along DCA axes was used to estimate the local environmental stability for each pollen-based record. This estimation is valid because the climate changes drive the extinction, migration and/or spatial reorganization of biological populations, including changes in the composition of the plant community (Colinvaux et al., 2000, 2001). Pollen-based records wherein the floristic composition shows greater oscillation among different plant taxa through time, that is, where the environment is more unstable, tend to show larger dispersion scores, and pollen records where the environment is more stable show smaller dispersion scores (Legendre and Legendre, 1998). Therefore, the HESI3 index was calculated from the coefficient of variation of the scores of each pollen-based record on the first axis of DCA ordination, divided by the time period of the respective pollen record, where the timescale was gauged per thousand years. Unlike HESI1 and HESI2 indices, which were based on a priori palaeoecological

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interpretations of palynological data, HESI3 index is based on plant composition oscillations over the late Quaternary. The HESI3 index is free of the previous interpretations made by various authors, which interpretations may be unreliable in terms of their estimations of the numbers and sequences of climate changes because of unclear procedures. In particular, what is considered a ‘‘climate change’’ in a pollen record? How is it defined? On the other hand, the HESI3 index was derived from pollen percentage diagrams, rather than from pollen concentration diagrams. In spite of these technical problems, the three HESIs indices show the magnitude of climate and vegetational shifts over time and can be identically interpreted, that is, smaller HESIs indices indicate environments that are climatically more stable. 2.4. Statistical analyses Because the HESIs indices are an inverse metrics for environmental stability, that is, smaller HESIs indices indicate environments that are climatically more stable, we employed a simple transformation in the HESIs values to make them more intuitive (transformation: HESI’ ¼ 1  (HESI/HESImax), where HESI is the value of index for each pollen-based record, and HESImax is the largest value of HESI among the pollen-based records). Correlation analyses were used to quantify the relationship among the three HESIs indices themselves and between the HESIs indices and the current species richness of mammals, birds, reptiles and amphibians in the grid cells that correspond to the geographic coordinates of the pollen-based records. The species richness related to five pollen-based records in the designated boundary areas were estimated within the grid of the Brazilian Cerrado range, once that species richness showed strongly structured in the space, that is, high spatial autocorrelation (Diniz-Filho et al., 2008). In these cases, the nearest cell in the Brazilian Cerrado grid to each pollen-based record in the boundary areas was used to estimate the species richness and was included in the analysis. Thus, the correlation analyses were based on 15 data points. Because of spatial autocorrelation in the richness data, the probabilities associated with these analyses are too liberal, but the focus of the analysis is on the ability of HESIs indices to explain the variation in the terrestrial vertebrate species richness, rather than on fixing significance levels (although the standard 0.05 significance level was used as the threshold for correlation analyses.) Because it is expected that environments in lower latitudes (tropical regions) to be more stable than those in higher latitudes (subtropical regions), a correlation analysis was also performed between the three HESIs indices and the latitude of each pollen-based record. 3. Results and discussion Results show that the correlations among the three HESIs indices are strong, positive, and significant in all cases (Table 1). This result indicates that the new HESIs indices are spatially Table 1 Correlation coefficient matrix among the three Historical Environmental Stability Indices (HESIs). HESI1

HESI2

HESI3

HESI1

r ¼ 1.0 p¼–

– –

– –

HESI2

r ¼ 0.6235 p ¼ 0.013

r ¼ 1.0 p¼–

– –

HESI3

r ¼ 0.6669 p ¼ 0.007

r ¼ 0.6834 p ¼ 0.005

r ¼ 1.0 p¼–

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concordant, that is, that the three HESIs indices lead to similar values of long-term climate stability throughout the Brazilian Cerrado (Table S1, Supplementary Material). Positive correlations, but not statistically significant, were found between the HESIs indices and the current species richness of four terrestrial vertebrate classes across the 15 nested quadrats (except the relationship between HESI3 index and mammal species richness) (Table 2). Likewise, the coefficients of correlation of relationships between HESIs indices and latitude were also all non-significant, but negative (Table 2). Thus, the null hypothesis that there is no correlation between the variables cannot be rejected. Although these correlations are usually non-significant, it is difficult to evaluate the causal relationship as the number of pollen-based records analyzed is too lowdonly 15 data points were used for correlation analysesdand there is relatively low statistical power. However, while high correlations do not imply direct causation, weak correlations can be used to support the conditional dismissal of a causal relationship (Shipley, 2000). In other words, although positive correlations would indicate that a more stable environment would support more terrestrial vertebrate species (Table 2), the non-significance of the correlations reveal no causal relationship between late Quaternary climate stability and current richness patterns of terrestrial vertebrates for the Brazilian Cerrado. That is, the non-significant correlations do not support the historical hypothesis that greater environmental stability leads to greater accumulation of vertebrate species in the Brazilian Cerrado range. An influence of climate stability on current patterns of species richness has been reported in some studies of various biological groups, especially vertebrates. However, the studies that have defined the influence of long-term climate change on species richness have been carried out mainly in the northern hemisphere, in the northern Nearctic and Palearctic biogeographic regions (see study of Hawkins and Porter, 2003 in North America; and Arau´jo et al., 2008 in Europe). The historical climate stability hypothesis proposes that species are differentially excluded from areas that experience the most severe climate changes, whereas persistence and speciation are favored where there is climate stability over time (McGlone, 1996; Dynesius and Jansson, 2000; Stephens and Wiens, 2003; Wiens and Donoghue, 2004; Jablonski et al., 2006; Ricklefs, 2006). Thus, a question arises regarding whether similar influences from historical climates can be found in the northern hemisphere as well as in the southern hemisphere, which was not glaciated during the Pleistocene. However, at least one piece of evidence suggests that the results are unique to the southern hemisphere (or at least for Brazilian Cerrado). The northern hemisphere as a wholedparticularly the northern Nearctic and Palearcticdwas extensively glaciated during the LGM, and the species ranging in these regions were forced to migrate to the more stable regions in the southeast, where they remained isolated in small areas that were not covered by ice sheets (Lessa et al., 2003; Waltari et al., Table 2 Coefficients of correlation among the three Historical Environmental Stability Indices (HESIs) and vertebrate species richness (mammals, birds, reptiles, amphibians) and latitude in the Brazilian Cerrado, Central Brazil. Vertebrate group

Latitude

Mammals

Birds

Reptiles

Amphibians

HESI1

r ¼ 0.3212 p ¼ 0.243

r ¼ 0.0451 p ¼ 0.873

r ¼ 0.4318 p ¼ 0.108

r ¼ 0.2203 p ¼ 0.430

r ¼ 0.2382 p ¼ 0.393

HESI2

r ¼ 0.4626 p ¼ 0.083

r ¼ 0.0472 p ¼ 0.867

r ¼ 0.4033 p ¼ 0.136

r ¼ 0.3319 p ¼ 0.227

r ¼ 0.2742 p ¼ 0.323

HESI3

r ¼ 0.6969 p ¼ 0.004

r ¼ 0.0993 p ¼ 0.725

r ¼ 0.5005 p ¼ 0.057

r ¼ 0.3783 p ¼ 0.164

r ¼ 0.2640 p ¼ 0.342

2007; Nogue´s-Bravo et al., 2008). These areas were used as refuges for various populations that then differentiated over time by vicariance (Hewitt, 2000; Lessa et al., 2003). When the post-Pleistocene global warming commenced and glaciers retreated, many species were able to expand their geographical ranges and return to the northern Nearctic and Palearctic (Graham et al., 1996; Lessa et al., 2003; Martı´nez-Meyer and Peterson, 2006; Waltari et al., 2007; Nogue´s-Bravo et al., 2008). Thus, the species richness in the southeast is greater than that of the northern Nearctic because of the time-for-speciation effect (Hawkins and Porter, 2003; Stephens and Wiens, 2003). In the southern hemisphere, the Pleistocene climatic changes occurred as a response to the cold of the northern hemisphere in the last glacial period (Salgado-Labouriau, 1997), but the southern hemisphere was not covered by ice sheets in the LGM (Delcourt and Delcourt, 1991). Colinvaux et al. (2000, 2001) proposed that shifts in the plant assemblage over the late Quaternary in South America are related to migration of many plant taxa from high altitudes, such as the Andes Mountains, and high latitudes, such as the Araucaria forest, in response to decreasing temperatures. Therefore, it was not surprising that the analyses found no causal relationship between historical climate and the current species richness of terrestrial vertebrate in the Brazilian Cerrado and showed no historical signature of climate change through the late Quaternary in the structuring of the current richness pattern. The available evidence suggests that ‘‘habitat tracking’’ was a more influential phenomenon in the South American biota than was ‘‘biome replacement’’ (Colinvaux et al., 1996a, b, 2000, 2001; De Oliveira, 1996; Colinvaux and De Oliveira, 2000), for which there is evidence in the northern hemisphere during the last glacial cycle (Lessa et al., 2003; Rowe et al., 2004). Further, the results do not support the suggestion that regions of the Brazilian Cerrado in the lower latitudes are more stable than those in the high latitudes, which finding indicates that there was similar climate stability in the regions near to and distant from the equator. Thus, environmental stability as an underlying mechanism responsible for the maintenance of the broad-scale latitudinal gradients in species richness is not supported for the terrestrial vertebrates of Brazilian Cerrado. Although the findings failed to demonstrate the validity of historical climate predictions for the Brazilian Cerrado and contained no evidence of a causal relationship among the current species richness of terrestrial vertebrates, latitude and climate stability, the three HESIs indices developed here are satisfactorily concordant and highlight that palynological data are efficient datasets with which to access the climate stability in the late Quaternary. However, these findings require several important caveats. First, the limited availability of pollen-based records in the study area results in degrees of freedom that are too low for a correlation analysis to be efficient and robust. If more pollen-based records were considered, the relative influence of each data point in the correlation analysis would be less, increasing then the degrees of freedom and the statistical power of the analysis. Second, the five pollen-based records outside the Brazilian Cerrado grid included here in order to maximize the information for the HESIs indices may also have influenced the explanatory power of the relationships among species richness, latitude and climate stability. Third, the greater number of the pollenbased records is placed on the central–southeastern regions of the Brazilian Cerrado. The northern Brazilian Cerrado has only two pollen-based records and the western region as a whole has no record. Fourth, the use of pollen concentration diagrams, when available, can be more auspicious than percentage diagrams for access the representation of the pollen taxa over time and consequently to estimates of the HESIs indices. In the pollen percentage diagrams, the representation curve of the pollen taxa often includes noise that is transplanted to all other pollen taxa curves, which effect does not occur in pollen concentration diagrams.

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4. Conclusions Although this study has been restricted to a relatively small spatial and temporal scale, it used a comparatively simple, but fine test to access the relative magnitude of climate change and to test its influence on modern-day species richness patterns. This is the first time that such tests have been employed to assess palynological data as an indicator of environmental stability and to develop indices of historical environmental stability using pollenbased records, considering a time period longer than glacial maximum. The three HESIs indices were spatially concordant themselves, indicating that the different uses of palynological data presented here lead us to similar conclusions about the historical environmental stability of the Brazilian Cerrado. Thus, we conclude that pollen records are an adequate dataset for accessing historical climate stability. Further, our findings do not support the suggestion that greater environmental stability leads to greater accumulation of vertebrate species in the Brazilian Cerrado range. Acknowledgements We thank Luis Mauricio Bini for suggestions that improved the Historical Environmental Stability Indices, and Paulo Eduardo de Oliveira, Fabrizio D’Ayala Valva and two anonymous reviewers for discussion and comments on an early version of the manuscript. This research was supported, in part, by CNPq/SECTEC-GO (PRONEX project no. 23234156) and the authors received graduate (M.S. Lima-Ribeiro) and productivity (J.A.F. Diniz-Filho) fellowships from CAPES and CNPq, respectively. Appendix. Supplementary Material The supplementary data associated with this article can be found in the on-line version at doi:10.1016/j.quaint.2009.10.003 References Allen, A.P., Brown, J.H., Gilloly, J.F., 2002. Global diversity, biochemical kinetics and the energetic-equivalence rule. Science 297, 1545–1548. Arau´jo, M.B., Nogue´s-Bravo, D., Diniz-Filho, J.A.F., Haywood, A.M., Valdes, P.J., Rahbek, C., 2008. Quaternary climate changes explain diversity among reptiles and amphibians. Ecography 31, 8–15. Barberi, M., Salgado-Labouriau, M.L., Suguio, K., 2000. Paleovegetation and paleoclimate of ‘‘Vereda de A´guas Emendadas’’, central Brazil. Journal of South American Earth Sciences 13, 241–254. Behling, H., 1995. A high resolution Holocene pollen record from Lago do Pires, SE Brazil: vegetation, climate and fire history. Journal of Palaeolimnology 14, 253–268. Behling, H., 1997a. Late Quaternary vegetation, climate and fire history from the tropical mountain region of Morro de Itapeva, SE Brazil. Palaeogeography, Palaeoclimatology, Palaeoecology 129, 407–422. Behling, H., 1997b. Late Quaternary vegetation, climate and fire history in the Araucaria forest and campos region from Serra Campos Gerais (Parana´), South Brazil. Review Palaeobotany Palynology 97, 109–121. Behling, H., 2002. Late quaternary vegetation and climatic dynamics in southeastern Amazonia inferred from Lagoa da Confusa˜o in Tocantins state, northern Brazil. Amazoniana 17, 27–39. Behling, H., Lichte, M., 1997. Evidence of dry and cold climatic conditions at glacial times in tropical southeastern Brazil. Quaternary Research 48, 348–358. Behrensmeyer, A.K., Damuth, J.D., Dimichele, W.A., Potts, R., Sues, H.D., Wing, S.L. (Eds.), 1992. Terrestrial Ecosystems Through Time: Evolutionary Paleoecology of Terrestrial Plants and Animals. University of Chicago Press, Chicago. Blackburn, T.M., Gaston, K.J., 2003. Introduction: why macroecology? In: Blackburn, T.M., Gaston, K.J. (Eds.), Macroecology: Concepts and Consequences. Blackwell, London, pp. 1–14. Brown, J.H., Maurer, B.A., 1989. Macroecology: the division of food and space among species on continents. Science 243, 1145–1150. Colinvaux, P.A., De Oliveira, P.E., 2000. Paleoecology and climate of the Amazon basin during the last glacial cycle. Journal of Quaternary Science 15, 347–356. Colinvaux, P.A., De Oliveira, P.E., Moreno, J.E., Miller, M.C., Bush, M.B., 1996a. A long pollen record from Lowland Amazonia: forest and cooling in glacial times. Science 274, 85–88.

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