Structure of Small Mammal Assemblages Across

BIOTROPICA 45(4): 489–496 2013

10.1111/btp.12027

Structure of Small Mammal Assemblages Across Flooded and Unflooded Gallery Forests of the Amazonia-Cerrado Ecotone Maria Ramos Pereira1,4, Rita G. Rocha1,2, Eduardo Ferreira1,2,3, and Carlos Fonseca1 1

Biology Department and Centre for Environmental and Marine Studies, University of Aveiro, Campus de Santiago, 3810-193, Aveiro, Portugal

2

Federal University of Tocantins, 109 Norte, Av. NS 15, ALCNO 14, 77001-090, Palmas, Tocantins, Brazil

3

Department of Engineering and Sea Science, University of Cape Verde, Mindelo, Cape Verde

ABSTRACT Habitat heterogeneity may affect the structure of animal assemblages even within apparently homogenous landscapes. Gallery forests of the Amazonia-Cerrado ecotone have a small-scale patchiness that is induced by river system dynamics. Gallery forests that never flood are located in upper areas of watercourse margins, whereas seasonally flooded gallery forests are located at lower ground along those margins. We tested the prediction that the assemblage structure of small non-volant mammals of these two types of forests is distinct and arises from the ecological heterogeneity induced by seasonal floods. We found that species composition differed between forest types, with arboreal species dominating in the seasonally flooded forests and a more balanced distribution of arboreal and terrestrial species in unflooded forests. We found no differences in species abundance between habitats, but species richness was higher in unflooded forests. We hypothesize that this difference is due to decreased resource availability for strictly terrestrial species in seasonally flooded forests. Relative biomass of seasonally flooded forests was more than twice that of unflooded forests due to the dominance of largebodied didelphid species in that assemblage. Our results suggest that the ecological heterogeneity created by seasonal floods is central to maintaining diverse assemblages in this region. The preservation of both unflooded and flooded gallery forests, which are under high human pressure from deforestation, agricultural conversion, and implementation of dams, may be crucial to preserving small mammal diversity at the landscape scale. Abstract in Portuguese is available in the online version of this article. Key words: Araguaia; habitat heterogeneity; marsupials; river dynamics; rodents.

THE FOREST-DOMINATED AMAZONIA AND SAVANNA-DOMINATED Cerrado ecosystems merge along an ecotonal region that extends several thousand kilometers across central Brazil. In this region, the Amazonia and Cerrado ecosystems overlap, with several large savanna patches occurring within the Amazonian forests (Ratter et al. 2006), while gallery forests extend the Amazonian influence along the watercourses in the Cerrado (Oliveira-Filho & Ratter 2002). Although only representing a small percentage of the habitats of the Amazonia-Cerrado ecotone, these gallery forests function as environmental buffers, playing key ecological and hydrological functions by protecting the river banks, preventing silting, and ensuring the quality and quantity of water in the riverbeds (Felfili & Silva Junior 1992). According to one of the major paradigms in community ecology, spatially heterogeneous conditions provide a greater diversity of potentially suitable niches for the array of species present, thus creating richer assemblages or communities (MacArthur & MacArthur 1961, Pianka 1966). So, gallery forests may function as a primary contributor to the species pool in the transitional region between Amazonia and

Received 12 March 2012; revision accepted 24 October 2012. 4

Corresponding author; e-mail: [email protected]

Cerrado because riparian areas tend to increase the variety of microhabitats within the landscape (Salo et al. 1986, SuazoOrtu~ no et al. 2011). Gallery forests, however, are not all alike. Along the mid-Araguaia River Basin in central Brazil, the watercourse margins located in upper areas are mostly characterized by gallery forests that never flood, whereas seasonally flooded gallery forests grow on those margins located on lower ground. Here, the landscape is not only shaped by the ‘tension zone’ resulting from the contact between the vast and extremely diverse Amazonia and Cerrado biomes (Myers et al. 2000, Cardoso Da Silva & Bates 2002, Laurance et al. 2011) but also by the seasonality of the Araguaia flooding regime. As a consequence, the dynamics of the river system may play a central role in shaping the structure of animal communities in the riverine areas of this ecotonal region. In lowland Amazonian rain forests, seasonal floods influence forest structure, floristic composition, and tree phenology (Kubitzki 1989, Junk 1993, Haugaasen & Peres 2005a). This leads to a marked structuring of Amazonian assemblages of medium to large non-volant mammals (Haugaasen & Peres 2005b), birds (Borges & Carvalh~aes 2000, Haugaasen & Peres 2008, Beja et al. 2009), and bats (Ramos Pereira et al. 2009). When compared with the effects of seasonal floods in lowland Amazonia, the patchiness of gallery forests in the

ª 2013 The Author(s) Journal compilation ª 2013 by The Association for Tropical Biology and Conservation

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Ramos Pereira, Rocha, Ferreira, and Fonseca

Amazonia-Cerrado ecotone is at a much smaller scale. It is reasonable to assume, however, that flooding also plays a similar role here, at least concerning the assemblages of animals with limited dispersal abilities and high habitat selectivity, such as small rodents and marsupials (Emmons 1984, Mares et al. 1986, Sutherland et al. 2000, Lacher & Alho 2001). Seasonal floods may be an additional source of environmental heterogeneity, thus promoting a more diverse regional species pool. On the other hand, they may also decrease habitat availability and create adverse conditions and physical barriers to dispersal (Diniz-Filho et al. 2008), thus resulting in lower levels of local diversity in the seasonally flooded habitats. We hypothesize that the small non-volant mammal fauna of this ecotonal region are strongly affected by the flooding regime, as suggested by Bezerra et al. (2009). Specifically, we hypothesize that the assemblages of small rodents and marsupials of the gallery forests that never flood differ significantly from those that suffer seasonal floods because: (1) species composition is distinct between the two forest types, with a dominance of arboreal species in the seasonally flooded gallery forests contrasting with a more balanced distribution of arboreal and strictly terrestrial species in unflooded forests; and (2) seasonally flooded gallery forests have lower levels of mammal richness and abundance due to decreased habitat availability for strictly terrestrial non-volant mammals. To test these hypotheses, we sampled small non-volant mammals in gallery forests that suffer seasonal floods and in gallery forests that never flood.

METHODS STUDY AREA.—The study area was located mainly in the Cant~ao State Park (Parque Estadual do Cant~ao, PEC, 80,000 ha), state of Tocantins, central Brazil (Fig. S1). Only one sampling point (U1) was located in the Bananal/Cant~ao Environmental Protection Area, state of Tocantins, and three sampling points were located in a private ranch (U6, U7, F3), state of Para. This area constitutes an ecotonal region between Amazonia and Cerrado and is markedly influenced by the Araguaia River, a natural border between the states of Tocantins and Para. Araguaia is an anabranching river consisting of multiple channels separated by vegetated semipermanent alluvial islands excised from preexisting floodplain or formed by within-channel or deltaic accretion (Nanson & Knighton 1996, Latrubesse 2008). The landscape is characterized by a mosaic of seasonally flooded and unflooded gallery forests located along the margins of the streams and channels. In well-drained areas, vegetation physiognomies more typical of the Cerrado occur (OliveiraFilho & Ratter 2002), such as dry and humid grasslands and savanna dominated by shrubs and/or trees. The climate is tropical, with a rainy season lasting from October to April and a dry season from May to September (INMET 2011). SAMPLING OF SMALL NON-VOLANT MAMMALS.—We used a standardized trapping protocol to sample small non-volant mammals in upland and floodplain gallery forests. Two trapping methods— pitfalls with plastic drift fences and live traps—were set at 18

sampling points; seven in unflooded gallery forests (U1 to U7) and 11 in gallery forests that suffer seasonal floods (F1 to F11) (Fig. S1). To ensure spatial independence, and considering the limited dispersal abilities of small non-volant mammals (Sutherland et al. 2000, Bowman et al. 2002), sampling locations were at least 2 km apart. At each location, the sampling design consisted of: (1) a line of sixteen 30 L pitfalls (diameter 32 cm/height 38 cm) with drift fences (50 cm height and 5 m long) between buckets; (2) a line of ten 60 L pitfalls (diameter 38 cm/height 54 cm) with drift fences (50 cm height and 5 m long) between buckets; (3) a line of 22 Sherman traps (45 9 12.5 9 14.5 cm) and ten Tomahawk traps (45 9 21 9 21 cm) placed on the ground; and (4) a line of four Sherman traps (45 9 12.5 9 14.5 cm) and four Tomahawk traps (45 9 21 9 21 cm) placed in the understory. Lines were placed at least 150 m apart. We placed a small piece of wood or stone inside the buckets to provide a dry surface for captured animals. Excess water was removed after heavy rain. We baited live traps with peanut butter and pineapple, which was replaced every 2 days. We checked all traps daily in the early morning so that captured animals would not spend the hottest hours of the day inside traps. Whenever possible, we identified all captured small mammals to species level. The first individuals of each species were collected and deposited at the Colecß~ao de Mamıferos of the Universidade Federal do Espırito Santo (UFES). All other individuals were measured, weighed with a digital scale (0.1 g precision) or with a spring scale (20 g precision), individually marked with ear tags, and were then subsequently released in the same location but away from the trap lines. Sampling was carried out between June 2007 and November 2008. All areas were sampled in 2007, except for five that were sampled in 2008 due to logistic constraints (three corresponding to seasonally flooded gallery forests – F5, F6, and F11; and two to unflooded gallery forests – U6 and U7). Three sampling periods averaging seven nights (between five and nine nights) were performed: (1) at the end of the rainy season (June–July 2007 and May–June 2008); (2) during the dry season (August–September 2007 and August–September 2008); and (3) at the beginning of the following rainy season (October–November 2007 and October–November 2008). At the end of the 2 years of fieldwork, the sampling effort was equal for all the sampling points, with 20 nights sampled at each location. During the three sampling periods, the ground of the seasonally flooded gallery forests was still accessible for small mammals. Due to flooding, sampling did not take place in the rainy season. At the end of each sampling period, we closed all buckets and removed the live traps. DATA ANALYSIS.—Species richness patterns were investigated using individual-based rarefaction curves (Coleman 1981, Gotelli & Colwell 2001). Comparisons across forests were made by truncating the rarefaction curves at the minimum number of individuals recorded in the samples.

Small Mammal Assemblages in Gallery Forests

We compared Shannon diversity indices, number of captures and relative biomass between habitats using general linear modeling (GLM). The distributions of diversity and relative biomass were somewhat skewed when adjusted to a gamma distribution, so we used a GLM with a gamma-distributed error function and a log link (Crawley 1993). We used a GLM with a poisson-distribution error function and a log link for the number of captures. We graphically evaluated the Bray–Curtis dissimilarity between the assemblages of the two forests using non-metric multidimensional scaling (NMDS), which plots assemblages that are more similar more closely together in a two-dimensional space. We used the logarithm of abundance to normalize the distribution of the variable and to stabilize the variance, followed by a square-root transformation to offset the influence of dominant taxa (Clarke 1993). We tested for significant differences in assemblage structure by means of a permutational multivariate analysis of variance (Anderson 2001, Oksanen et al. 2008, 2010) on the community matrix incorporating small mammal abundances. This analysis tends to be less sensitive to differences in point dispersal than analysis of similarities (ANOSIM) or the multiresponse permutation procedure (MRPP; Oksanen et al. 2010). The permutational multivariate analysis of variance was done using the adonis function implemented in the R package vegan. The distance matrices were constructed using the Bray–Curtis index, and P-values were generated using F-tests based on sequential sums of squares from 10,000 permutations of the raw data. The presence of spatial patterns in assemblage structure was investigated by comparing the Bray–Curtis similarity matrix and the matrix of Euclidean distances between sampling sites using a ranked Mantel test. Ranking the data in this way helps to linearize otherwise nonlinear relationships between dissimilarity matrices (Legendre & Legendre 1998). To assess if arboreal species were more common in flooded forests, species frequencies were compared in a cross-classified table. We used a similarity percentage (SIMPER) analysis to assess the relative contribution of species to the dissimilarity between seasonally flooded gallery forests and unflooded gallery forests. All analyses were performed in R software (Ihaka & Gentleman 1996), including the packages ade4, ecodist, epiR, stats, and vegan.

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between-habitat variation in species richness, with a higher number of species overall being captured in unflooded gallery forests. Our sampling effort appears to have been sufficiently intensive because species rarefaction curves are close to an asymptote in both forest types (Fig. 1). We found no significant differences in Shannon diversity indices (GLM z-value = 0.082; P = 0.9374) or in the number of captures between habitats (GLM z-value = 0.5081; P = 0.6120). Relative biomass (measured as the ratio between total biomass and the number of captures), however, was significantly higher in seasonally flooded gallery forests (GLM z-value = 2.6134; P = 0.0182; Fig. 2). Sampling points were clustered according to habitat type, with NMDS revealing a well-defined separation of the species assemblages of seasonally flooded and unflooded gallery forests (Fig. 3). Indeed, small mammal community structure based on abundance was significantly different between forest types (F = 3.2128; R2 = 0.1515; P = 0.0021). Arboreal species were significantly more common in flooded forests than in unflooded forests (Contingency coefficient = 0.61; P < 0.0064). Spatial structure did not significantly affect assemblage similarity, as similarity did not vary with distance between sampling sites, irrespective of forest type (ranked Mantel test = 0.0274; P = 0.5830). Over 60 percent of the dissimilarity among seasonally flooded and unflooded forests was due to differences in the capture rate of just four taxa: Oecomys sp. and Didelphis marsupialis were more frequently captured in seasonally flooded forests, whereas Marmosa murina and P. roberti were more often captured in unflooded forests (Table 1).

RESULTS We captured a total of 406 individuals from 19 species (eight marsupials and 11 rodents), of which 206 were trapped in seasonally flooded forest and 200 in unflooded forests. Thirteen species were caught in seasonally flooded forests, three of which were exclusive to that habitat (Gracilinanus agilis, Holochilus sciureus, and Makalata didelphoides). Sixteen species were caught in unflooded forests, including six that were exclusive (Metachirus nudicaudatus, Oecomys paricola, Oligoryzomys fornesi, Pseudoryzomys simplex, Rhipidomys ipukensis, and Proechimys roberti) (Table S1). After controlling for differences in numbers of individuals captured using rarefaction curves (Fig. 1), we found a significant

FIGURE 1. Individual-based species-rarefaction curves (solid lines) with 95% confidence intervals (dashed lines), based on captures for unflooded and seasonally flooded gallery forests.

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FIGURE 2. Shannon diversity index, number of captures, and relative biomass in seasonally flooded and unflooded gallery forests. Vertical lines correspond to 95% confidence intervals. Asterisk indicates a significant difference at alpha = 0.05 (see text for values).

DISCUSSION Several studies have shown that the Amazonian rain forest influences the Cerrado through the presence of gallery forests, which act as refuges and dispersal corridors for rain forest mammal species (e.g., Redford & Fonseca 1986, Costa 2003). Few studies, however, have been carried out in riparian areas along the ecotonal belt between the Amazonia and Cerrado biomes (but see Lacher & Alho 2001, Bezerra et al. 2009, Rocha et al. 2011). In this study, we showed that flooding patterns are important abiotic factors that determine spatial variations in the structure of small non-volant mammal assemblages between gallery forests along the mid-Araguaia River Basin that never flood and those that suffer seasonal floods.

FIGURE 3. Non-metric multidimensional scaling (NMDS) plot of small non-volant mammal assemblage variation among unflooded and seasonally flooded gallery forests. NMDS ordination clearly separated unflooded and seasonally flooded gallery forests, reducing the number of meaningful dimensions to three. In two dimensions, our NMDS solution attained a minimum stress of 0.17, while a minimum stress of 0.13 was reached in three dimensions. Crosses and rectangles represent, respectively, arboreal and terrestrial taxa that contribute the most to the dissimilarity between unflooded and seasonally flooded gallery forests. Species codes as in Table S1.

DIFFERENCES IN SPECIES COMPOSITION BETWEEN FOREST TYPES.—As hypothesized, species composition differs between forest types, with a dominance of arboreal species such as Oecomys sp., D. marsupialis, and M. didelphoides in the seasonally flooded forests, and a more balanced distribution of arboreal and terrestrial species in unflooded forests (Table S1). Some strictly terrestrial species, such as P. roberti and O. fornesi, were never caught outside unflooded areas (Table S1). Differences between assemblage composition of flooded and unflooded forests have also been recorded for other animal groups in Amazonia such as medium to large non-volant mammals, including primates (Haugaasen & Peres 2005c), and bats

TABLE 1. Small non-volant mammal species contributing > 5 percent to habitat dissimilarity between seasonally flooded and unflooded gallery forests of the mid-Araguaia basin. av

av

Species

av.contr

sdi

sdi.av

Flooded

Unflooded

Cum

Oecomys sp.

15.8043

0.1360

0.0086

7.2700

0.5000

18.4575

P. roberti

14.5411

0.2120

0.0146

0.0000

6.7500

35.4397

D. marsupialis M. murina

12.6158 11.3676

0.1213 0.1374

0.0096 0.0121

5.4500 0.2730

1.5000 6.1300

50.1733 63.4493

P. opossum

8.2689

0.0754

0.0091

1.1800

3.6300

73.1064

M. didelphoides

5.5880

0.0506

0.0091

1.1800

2.1300

79.6325

av.contr: average contribution to overall similarity; sdi: standard deviation of contribution; sdi.av: ratio mean/SD = sdi/av.contr.; av Flooded: average abundance in flooded forests; av Unflooded: average abundance in unflooded forests; cum: cumulative contribution. Rows highlighted in pale gray represent species with higher average abundances in seasonally flooded forests, while white rows represent species with higher average abundances in unflooded forests.


(Ramos Pereira et al. 2009), and also for birds (Borges & Carvalh~aes 2000, Haugaasen & Peres 2008, Beja et al. 2009). Our second hypothesis was partially corroborated: we did not find significant differences in abundance between the two forest types, but we found significant differences in species richness, with seasonally flooded forests being poorer than unflooded forests. Although there are more species present in unflooded gallery forests, the absence of strictly terrestrial species in seasonally flooded habitats seems to have been partly offset by the presence of additional arboreal (M. didelphoides) and semiaquatic (H. sciureus) species that are absent from unflooded forests. Indeed, there was no statistical difference between the Shannon diversity indices of the two forest types. THE ROLE OF FLOODS IN ASSEMBLAGE STRUCTURING.—Both historical and ecological factors influence species richness at a site (Zobel 1992, Ricklefs & Schluter 1993, Hortal et al. 2008). Local species richness is limited by the available species pool, i.e., richness at a given community or site is determined by the number of available species at the next largest scale (Zobel 1997), and is also a function of productivity (although that relationship can be positive, negative, or unimodal; for a review see Mittelbach et al. 2001, Cornwell & Grubb 2003). In our study, however, the two forest types are supplied by the same regional species pool and both are located in nutrient-depleted soils, drained by clearwaters (Junk et al. 2011), and are likely to present similar levels of productivity. So, differences in species richness must be mainly determined by other ecological factors acting at a smaller scale. Some species in our sample thrived well in both flooded and unflooded gallery forest, whereas others were restricted to one or the other. A close assessment of the species absent from seasonally flooded forests suggests that the difference in the number of species between the two forest types is mostly due to the decreased area available to strictly terrestrial small non-volant mammals in seasonally flooded forests. Therefore, our results add to the growing evidence that the species assemblage of a given site is finely tuned by the ecological and behavioral features of the species that can potentially occupy the area, and support the idea that flooding is a primary environmental filter (sensu Poff 1997). In fact, although all our captures were made during nonflooding periods, our results suggest that, at least for some species, the influence of flooding persists year-round. This indicates that its influence is not only direct, by constraining access to the ground or to resources near the ground during floods, but also indirect, by affecting forest structure and floristic diversity. In fact, small mammals seem to be strongly dependent on ground and understory vegetation to feed on or shelter in (Emmons & Feer 1997). Because this vegetation is much less developed and less diverse in seasonally flooded habitats due to long periods of hypoxia (Gentry 1982, Worbes 1997), such mammals probably avoid these forests, not only during the floods, but year-round due to the absence or scarcity of understory plants (Haugaasen & Peres 2006). Our findings are supported by Beja et al. (2009), who demonstrated that many abundant ground-dwelling birds in

493

Amazonian terra firme forests were absent or rare in floodplain forests all year-round. A similar result was obtained by Haugaasen and Peres (2005b), who showed that flooding led to a reduction in mammal richness in varzea (forests seasonally flooded by nutrient-rich water)—in comparison with terra firme forests (upland forests that never flood)—because floods in that habitat prevented terrestrial and understory medium-sized non-volant mammals from accessing the ground. Haugaasen and Peres (2007), however, indicate that terrestrial vertebrates moved into varzea as soon as dry land appeared. SPECIES-SPECIFIC PATTERNS.—The restricted occurrence of P. roberti in unflooded forests is related to its strictly terrestrial habitat requirements and limited dispersal ability (Bonvicino et al. 2002). In fact, these spiny rats are most common in dense undergrowth, around fallen trees and complex tree roots and they rarely climb, except onto low fallen logs (Emmons & Feer 1997). They also show a preference for microhabitats associated with the presence of babacßu palms Attalea speciosa (Johnson et al. 2004). These palms do not occur in seasonally flooded gallery forests, thereby limiting the occurrence of P. roberti in these habitats even during the dry season. Indeed, this affinity of P. roberti for drier gallery forests has also been reported elsewhere in the Cerrado (Fonseca & Redford 1984, Johnson et al. 2004). Some arboreal species also seem to prefer unflooded forests. This is the case of M. murina, known to be associated with terra firme and its transition to igapo forests (forests seasonally flooded by nutrient-poor water; Patton et al. 2000). Based on our study, M. murina seems to avoid gallery forests that flood. In fact, murine mouse opossums are known to search the understory and forest floor, exploring the undersurfaces of leaves for invertebrate prey (Emmons & Feer 1997); a foraging strategy impossible to accomplish when the forest floor remains below water for several months a year, as occurs in seasonally flooded forests. Other species, such as M. demerarae and P. opossum, were also more frequently captured in unflooded habitats, although they also use seasonally flooded forests to some extent. These predominantly arboreal species often search the ground for arthropods and small vertebrates on which they primarily feed (Charles-Dominique et al. 1981, Emmons & Feer 1997, Pinheiro et al. 2002), which may explain their preference for unflooded areas. Although flooded forests may provide important food resources when their availability in unflooded forests is low (Haugaasen & Peres 2007), the use of seasonally flooded habitats by M. demerarae and P. opossum, at least during the dry season, may be due to the fact that the ground is still moist and is a suitable habitat for amphibians and crustaceans. Didelphis marsupialis is well established in the flooded forests of this ecotonal area between the Cerrado and Amazonia biomes, whereas in Amazonia, this species appears to occur primarily in upland, unflooded forests (Patton et al. 2000). Nevertheless, it should be noted that D. marsupialis and another large-bodied and, closely related species, D. albiventris, are sympatric in the Amazonia-Cerrado ecotone (Gardner 2008, Rocha et al. 2011), but they rarely coexist in the same habitat (Emmons & Feer

494


1997). Didelphis marsupialis is more common in Amazonian environments, whereas D. albiventris seems to replace it in dryer and more open environments (Gardner 2008). We hypothesize that the pattern found in our study area is a result of competitive exclusion, with D. marsupialis favouring seasonally flooded gallery forests to avoid competition with D. albiventris in dryer forests. Makalata didelphoides is strictly arboreal, feeding on leaves (Patton et al. 2000) and immature seeds of Inga and Virola plants (Charles-Dominique et al. 1981). Some species of these plant genera do well on poorly drained or periodically flooded sites (Lieberg & Joly 1993), which may explain the strict association of M. didelphoides with seasonally flooded forests in our study area. Specimens of Oecomys sp. could not be allocated to any described species (Rocha et al. 2011), and the reasons for the observed patterns thus remain unknown. The relative biomass of seasonally flooded forests was, on average, more than twice of the biomass of unflooded forests. This was not due to differences in the abundance of individuals, but to the dominance of large-bodied didelphid species in the flooded forests. As mentioned above, D. marsupialis, averaging 1 kg of body mass, was the most common species in flooded forests. In unflooded areas, the assemblage is more diverse in terms of body mass; here medium-sized species like P. roberti, P. opossum, and M. demerarae, averaging 100–300 g of body mass, were the more common species. CONSERVATION IMPLICATIONS.—The Cant~ao State Park and its surroundings harbor a patchy environment of upland and alluvial riparian forests. Evidence of associations between some species and one forest type corroborate the hypothesis that this mosaic of habitats promotes rich regional (gamma) animal communities (Lacher & Alho 2001). These riparian areas are highly susceptible to deforestation and the consequential impacts of human disturbance and agricultural conversion (Morton et al. 2006), and they are also seriously threatened by the implementation of new hydroelectric dams (Brand~ao & Ara ujo 2008). Conservation efforts should thus be focused on the creation of new or the extension of existing protected areas in this region, combining a sufficiently large mosaic of habitats and providing conditions for a large number of species with different habitat requirements.

ACKNOWLEDGMENTS We thank Andrea Serafini, Sr. Ant^ onio Messias, Roberto, Sr. Joaquim, Sr. Lucimar and all field assistants who helped with logistics and fieldwork. We thank A.P. Carmignotto for valuable suggestions on the sampling design for pitfall lines. We also thank staff from Parque Estadual do Cant~ao, Fazendas Santa Fe e Aguas do Papagaio, and the following institutions: Ecotropical (a partnership between Instituto Ecol ogica and Universidade de Aveiro), Universidade Federal do Tocantins/Fundacß~ao de Apoio Cientıfico e Tecnologico do Tocantins (UFT/FAPTO), Universidade Luterana do Brasil (ULBRA-TO) and NATURATINS, for all logistical support. All procedures were performed according to

Brazilian national laws and guidelines. Fieldwork was carried out with permits from the federal (ICMBIO, permits: 200/2006 and 14307-1) and state (NATURATINS, permits: 019/2006 and 001/2008) conservancy agencies. MJRP, RGR, and EF were funded by Fundacß~ao para a Ciência e Tecnologia, through grants SFRH/BPD/72845/2010, SFRH/BD/24767/2005, SFRH/BD/23191/2005 and SFRH/ BPD/72895/2010.

SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: FIGURE S1. Map of the study area, showing the approximate location of the unflooded and flooded sample sites, within the Cant~ao Environmental Protection Area. TABLE S1. List of small non-volant mammal species with corresponding forest level and number of captured individuals in seasonally flooded and unflooded gallery forests in the mid-Araguaia River Basin.

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