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Interactions between land use, taxonomic group and aspects and levels of diversity in a Brazilian savanna: implications for the use of bioindicators

The study was carried out in the Triângulo Mineiro region of Minas Gerais state, covering the municipalities of Uberlândia, Monte Alegre, and Nova Ponte, in south-eastern Brazil. We conducted the study in five habitat types, comprising two natural habitats (savanna and semideciduous forest), and three anthropogenic land-uses: cattle pastures (planted with introduced Urochloa grasses), soy fields (where sampling took place when plants were at the vegetative phase) and  plantations of Eucalyptus trees (≥ 6 yrs old). Ants and beetles were sampled at the same 40 sites (8 replicates per land use), and birds at 30 sites (6 replicates per land use), only some of which were the same as for ants and beetles.  Ants that forage on ground and dung beetles were sampled using pitfall traps. Sampling took place in November and December (early wet season) 2017. In each site, eight traps were installed with traps located at the corners of a 100×100 m square, and at the mid-points of the sides of the square, keeping a minimum distance of 50 m between any two traps. All traps were at least 75 m distant from the edge of the respective land use. Traps were plastic containers (19 cm diam, 11 cm height) filled with 150 ml of a saline solution and detergent. Each trap had a wire hoop suspended over it to accommodate a small (4 cm diam, 4 cm height) plastic container for holding a dung bait. We used a 20 cm diameter plastic cover supported by three sticks to protect traps from rain. Traps were baited with ~40 g of a mixture of pig dung and human faeces (4:1 proportion) and left in the field for 48-hrs. Birds were surveyed using 20-min point counts in the rainy season (November 2017 to March 2018). At each site, five sampling points were established, 200 m distant from each other. All surveys started at sunrise (about 6 a.m.), and all species seen or heard from each point were recorded. Each sampling site was re-surveyed in the following dry season (April to October to 2018); however, for logistic reasons we were unable to re-survey the plantation sites.  Ant and dung beetle species were identified to species or morphospecies by comparison with named species in the Zoological Collection at the Federal University of Uberlândia (UFU) or with specialist assistance from Fernando Vaz de Mello, respectively. Vouchers of all species have been deposited at UFU´s Zoological Collection. Birds were identified directly in the field and species names follow the checklist produced by the Brazilian Ornithological Records Committee. We classified species functionally based on primary diet, foraging location and/or behaviour, and body size, as these traits are known to be sensitive to habitat modifications and of importance for the ecosystem services provided by ants, birds, and dung beetles. Ant species were classified according to their diet as predators, fungivores, nectarivores or omnivores, and according to their main foraging location as arboreal, epigeal (aboveground) or hypogeal (in soil and litter), based on information provided by Brown (2000) and Silvestre et al. (2003). Species were further classified into four body size categories based on our measurements of body length (Weber´s length; Brown, 1953) of 1-5 ant workers per species: 1 (< 0.75 mm), 2 (0.75-1.74 mm), 3 (1.75-3 mm), and 4 (> 3 mm). Dung beetles were classified as coprophagous, necrophagous, frugivore, generalist or predator, according to the type of food resource each species is most often attracted to. This classification was based on over 30 years of field experience throughout Brazil by one of the authors of this study (FVM), who used multiple types of baits (e.g., carcasses, fruits, faeces) to attract and collect dung beetles, and/or on literature information. Although information about the “attractiveness” of different types of baits to dung beetles (used here as a proxy for primary diet) was not obtained directly in the sites of the present study, it is importat to note that we are not aware of any evidence of geographic or habitat variation in bait preference among tropical species of dung beetles. Dung beetles were also classified according to their foraging behaviour as: telecoprid (species that make a dung ball and roll it away for burial), paracoprid (species that store dung in tunnels dug immediately below the dung source), or endocoprid (species living within or immediately below the dung, without moving it). For this, we used the database of the Zoological Collection of the Federal University of Mato Grosso (UFMT). Whenever sample sizes allowed, 30 individuals from each species were weighed for determination of body mass (following Almeida et al., 2011), and species were classified according to the following ordinal scale: 1 (< 10 mg); 2 (10-99 mg); 3 (100-300 mg); and 4 (>300 mg). Each bird species was classified according to its primary diet as frugivores granivore, insectivore, nectarivore, carnivore, detritivore, or omnivore, and according to the main foraging location as ground, understory/shrubby vegetation, or tree canopy, based on the Wilman et al. (2014) database and our own field experience. Using these same sources, we obtained information on mean body weights of each species and assigned them to one of five size categories: 1- (<15 g); 2 (15-39 g); 3 (40-199 g); 4 (200-599 g); and 5 (> 600 g).

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Figure 3 in Woody species distribution across a savanna-dry forest soil gradient in the Brazilian Cerrado

Figure 3. Proportional occurrence of 51 woody species across 30 plots ordinated by the soil gradient of aluminum saturation and base saturation (RDA axis 1, see Figure 1) in a savanna-dry forest transition. Grey and black bars correspond to cerrado stricto sensu and dry forest plots, respectively.

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Figure 2 in Woody species distribution across a savanna-dry forest soil gradient in the Brazilian Cerrado

Figure 2. Topography and the gradients of aluminum saturation, base saturation, and phosphorus across 30 plots (rectangles, 10×40 m) in a 4.5 ha area of contact between the cerrado stricto sensu (SA) and dry forest (DF) physiognomies.

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Figure 1 in Woody species distribution across a savanna-dry forest soil gradient in the Brazilian Cerrado

Figure 1. Biplot of tb-RDA for woody species composition, and relationships with edaphic (P = phosphorous; A = aluminum saturation; B = base saturation) and spatial (M1 and M2) variables, among plots in cerrado stricto sensu (gray) or dry forest (black) physiognomies.

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Fig. 2 in Interseasonal variation of Chrysodeixis includens (Walker, [1858]) (Lepidoptera: Noctuidae) populations in the Brazilian Savanna

Fig. 2. Population variation of Chrysodeixis includens (bars) sampled through light traps, compared to monthly normal rainfall (mm/month) (dotted line), monthly accumulated rainfall (mm/month) (continuous line) and period of corn and soybean cultivation (grey area) during five nights each month (new moon), in the 'Estação Experimental da Embrapa Cerrados', Planaltina, DF, Brazil.

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Fig. 1 in Interseasonal variation of Chrysodeixis includens (Walker, [1858]) (Lepidoptera: Noctuidae) populations in the Brazilian Savanna

Fig. 1. Monthly abundance of Chrysodeixis includens moths during three crop seasons. Vectors angles represents circular mean abundance while vectors length represents how clustered is the abundance data around the average.

FIGURE 4 in Land-use changes affect the functional structure of stream fish assemblages in the Brazilian Savanna

FIGURE 4 | Structural equation model diagrams showing the effects of landscape degradation (CDI) on the functional structure of stream fish assemblages from the Araguari River basin. CDI influenced functional diversity mediated by alterations in habitat heterogeneity and stability (A. Model fit: X2 = 32.8, df = 25, p = 0.51). CDI also influenced functional identity, mediated by changes in habitat type (B. Model fit: X2 = 44.9, df = 18, p = 0.13). Arrows indicate positive (black) and negative (gray) significant direct effects (p <0.05; *p <0.10), with thickness proportional to their power (standardized path coefficients along arrows). Biodiversity metrics – FRic: Functional Richness; FDiv: Functional Divergence; FEve: Functional Evennes; FSpe: Functional Specialization; FOri: Functional Originality; CWM1-3: Functional Identity. For physical-habitat codes, calculation and ecological meaning, see Tab. 1.

FIGURE 5 in Land-use changes affect the functional structure of stream fish assemblages in the Brazilian Savanna

FIGURE 5 | Ecomorphological space showing the position of each fish species (36) from the Araguari River basin. Each plot represents two axes of a principal component analysis (PCA), where species are plotted according to their respective trait values. Codes at the ends of the arrows are the most important ecomorphological traits for each PCA axis. For trait and species codes, see Tab. 2 and Tab. S3, respectively).

FIGURE 2 in Land-use changes affect the functional structure of stream fish assemblages in the Brazilian Savanna

FIGURE 2 | Examples of landscape and local-habitat conditions of the streams sampled across a degradation gradient in the Cerrado: A. Streams with a small strip of riparian forests in landscapes dominated by mechanized agriculture; B. Stream with relatively well-preserved local conditions, including forest on both banks; C. Stream surrounded by intermediate riparian cover; and D. Stream running in pasture areas without any forest.

FIGURE 3 in Land-use changes affect the functional structure of stream fish assemblages in the Brazilian Savanna

FIGURE 3 | Predictions tested using structural equation modeling, indicating the expected pathways (arrows) for the effects of catchment degradation (CDI) on stream physical habitat and, consequently, on the functional structure of the fish assemblages. Land use is expected to influence the functional diversity mediated by alterations in habitat heterogeneity and stability (A), and to influence functional identity, mediated by changes in habitat type (B). Arrows indicate expected effects between predictive and response variables, which can be positive (black continuous line), negative (gray continuous line) or non-directional (dashed lines). For physical-habitat codes, calculation and ecological meaning, see Tab. 1.

FIGURE 1 in Land-use changes affect the functional structure of stream fish assemblages in the Brazilian Savanna

FIGURE 1 | Headwater streams (N = 40; black dots) sampled for fish and local physical habitat. All sites drain to Nova Ponte Reservoir in the Araguari River basin, Upper Paraná River, Minas Gerais, Brazil.

Fig. 6 in Trophic structure of a fish community in Bananal stream subbasin in Brasília National Park, Cerrado biome (Brazilian Savanna), DF

Fig. 6. Proportion of autochthonous feeding items (black) and allochthonous (gray) with respect to the rainy (C) and dry (S) seasons for the fish species that presented this significant variation. Species abbreviations: Aspidoras fuscoguttatus (aspfus), Astyanax sp. (astsp), Characidium xanthopterum (chaxan), Hasemania sp. (hassp), Hyphessobrycon balbus (hypbal), Heptapterus sp. (hepsp), Knodus moenkhausii (knomoe), Kolpotocheirodon theloura (kolthe), Moenkhausia sp. (moesp), Phalloceros harpagos (phahar), Planaltina myersi (plamye), Rhamdia quelen (rhaque) and Rivulus pictus (rivpic)..

Fig. 1 in Trophic structure of a fish community in Bananal stream subbasin in Brasília National Park, Cerrado biome (Brazilian Savanna), DF

Fig. 1. Localization of the Brasília National Park in the Distrito Federal and distribution of sampling sites in the Bananal stream subbasin, Paranoá Lake basin, DF.

Fig. 5 in Trophic structure of a fish community in Bananal stream subbasin in Brasília National Park, Cerrado biome (Brazilian Savanna), DF

Fig. 5. Feeding items distributed according to the frequency of fish species occurrence (axis X) and relative abundance (axis Y), based upon the method proposed by Amundsen et al (1996): Moenkhausia sp., Phalloceros harpagos, Planaltina myersi, Rhamdia quelen and Rivulus pictus. The number of analyzed stomachs is shown in parentheses.

Fig. 4 in Trophic structure of a fish community in Bananal stream subbasin in Brasília National Park, Cerrado biome (Brazilian Savanna), DF

Fig. 4. Feeding items distributed according to the frequency of fish species occurrence (axis X) and relative abundance (axis Y), based upon the method proposed by Amundsen et al (1996): Aspidoras fuscoguttatus, Astyanax sp., Characidium xanthopterum, Hasemania sp., Hyphessobrycon balbus, Heptapterus sp., Knodus moenkhausii and Kolpotocheirodon theloura. The number of analyzed stomachs is shown in parentheses.

Fig. 2 in Trophic structure of a fish community in Bananal stream subbasin in Brasília National Park, Cerrado biome (Brazilian Savanna), DF

Fig. 2. General view of sites 1 to 7 sampled at the Bananal stream subbasin, Paranoá Lake basin, DF.

Fig. 3. Non-metric multidimensional scaling analysis for the 13 in Trophic structure of a fish community in Bananal stream subbasin in Brasília National Park, Cerrado biome (Brazilian Savanna), DF

Fig. 3. Non-metric multidimensional scaling analysis for the 13 more abundant fish species' diet found in the Bananal stream subbasin, Paranoá Lake basin, DF. Indication of four groups A, B, C and D. Species abbreviations: Aspidoras fuscoguttatus (aspfus), Astyanax sp. (astsp), Characidium xanthopterum (chaxan), Hasemania sp. (hassp), Hyphessobrycon balbus (hypbal), Heptapterus sp. (hepsp), Knodus moenkhausii (knomoe), Kolpotocheirodon theloura (kolthe), Moenkhausia sp. (moesp), Phalloceros harpagos (phahar), Planaltina myersi (plamye), Rhamdia quelen (rhaque) and Rivulus pictus (rivpic).

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Fig. 2 in Influence of the riparian zone phytophysiognomies on the longitudinal distribution of fishes: evidence from a Brazilian savanna stream

Fig. 2. Two-dimension ordinations based on Jaccard similarity coefficient (a) and on Bray-Curtis (b), considering the ten samples from the wet and dry seasons from the Correntes stream, central west Brazil.

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Fig. 1 in Influence of the riparian zone phytophysiognomies on the longitudinal distribution of fishes: evidence from a Brazilian savanna stream

Fig. 1. Map showing localization of the sampled reaches of Correntes stream in the plateau region of the Paraguay basin, Mato Grosso do Sul State, Brazil.