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Implications of an agricultural mosaic in small mammal communities
Journal Pre-proof Implications of an agricultural mosaic in small mammal communities ˜ Maria Adelia ´ B. de Oliveira, Mart´ın Alejandro Montes Marina Falcao,
PII:
S1616-5047(19)30031-X
DOI:
https://doi.org/10.1016/j.mambio.2019.09.010
Reference:
MAMBIO 41141
To appear in:
Mammalian Biology
Received Date:
12 February 2019
Accepted Date:
24 September 2019
˜ M, de Oliveira MAB, Montes MA, Implications of an Please cite this article as: Falcao agricultural mosaic in small mammal communities, Mammalian Biology (2019), doi: https://doi.org/10.1016/j.mambio.2019.09.010
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Implications of an agricultural mosaic in small mammal communities
Marina Falcãoa*, Maria Adélia B. de Oliveirab, Martín Alejandro Montesc *[email protected]
a
Graduation Program in Ecology, Biology Department, Federal Rural University of Pernambuco,
Rua Dom Manoel de Medeiros, s/n, CEP: 52171-900, Recife/Pernambuco, Brazil. Correspondent author. b
Laboratory of Ecophysiology and Animal Behavior, Department of Animal Morphology and
Physiology, Federal Rural University of Pernambuco.
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Laboratory of Genetics, Department of Biology, Federal Rural University of Pernambuco.
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c
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Abstract
The ideas that larger fragments have greater species richness and abundance, when compared to smaller fragments and altered environments, and that assemblage composition is different, was
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tested in an agricultural mosaic using data on small mammals. To achieve this, we sampled ten forest fragments of different sizes, small and large, as well as five areas in a sugarcane matrix,
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through the capture-mark-recapture method. The study was conducted in a sugarcane plantation (Usina São José, Igarassu, Pernambuco, Brazil) from January to October 2016. There was a significant difference when comparing richness between small fragments (eight species) and the sugarcane matrix (four species). Abundance differed significantly between all areas, being
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influenced by fragment size and habitat type. We found that abundance was positively influenced by forested environments and, among them, larger fragments. The composition of assemblages in the forest fragments and the sugarcane matrix differed clearly for NMDS,
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MANOVA and SIMPER analyses. Between the habitats, assemblage parameters were also distinct. Lower abundance and richness were found in the sugarcane matrix, where the presence of rodents was associated with food availability and less competition; and higher abundance and richness was measured in forest fragments, where there was a strong association between
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marsupials and forest strata. The landscape configuration in an agricultural mosaic can compromise the level of interspecific interactions of small mammals, which negatively impacts the ecological processes of forested areas. In this case, the conservation of a matrix permeable to most species and the preservation of all fragments are necessary, since small and large fragments have different functions in the maintenance of species.
Keywords: Atlantic Forest, sugarcane, richness, abundance, composition and assemblage.
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Introduction The conversion of landscapes from natural to anthropogenic ones brings with it drastic biological consequences, especially in the tropics (Ranganathan et al., 2008), i.e. regions with high biodiversity and accelerated degradation (Laurance, 2010). This process of conversion is responsible for the loss in vegetation cover and deforestation, both of which are associated with fragmentation (Nagendra et al., 2004). Historically, habitat loss was caused by the growth of urban areas, industrial growth, construction of highways and agriculture (Geist and Lambin, 2002; Butler and Laurance, 2008), driving approximately 65% of deforestation in the planet’s tropical regions (Geist and Lambin, 2002). Between 1990-2010, agricultural expansion stimulated a loss of vegetation cover of two million 2
km in the neotropics, among it Africa (including Madagascar) and southeast Asia regions (Estrada et al., 2017). In the same period, in Brazil, agricultural areas grew by 34 million hectares and approximately 7%
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of native forested areas were converted into agricultural land over a period of 11 years (OECD/FAO, 2015). Within agricultural production we can highlight farming of sugarcane, of which Brazil is the
largest producer in the world (OECD/FAO, 2015), and was one of the main causes of the fragmentation
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of the Atlantic Forest (Silveira et al., 2003).
The Atlantic Forest is categorized for its high heterogeneity, species richness and endemism (Tabarelli et al., 2005; Ribeiro et al., 2009). However, the biome has lost approximately 88% of its
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original cover (Ribeiro et al., 2011), leaving 87.5% of the forest remnants labeled as small (<50ha) (SOS Mata Atlântica and INPE, 2018) and less than 3% as larger than 250ha (Ribeiro et al., 2009). In the Center of Endemism Pernambuco – CEPE, a biogeographic sub-region of the Brazilian Atlantic Forest,
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there is only 11.5% of forest remnants, presenting one of the biome’s largest examples of destruction (Ribeiro et al., 2009).
The high level of environmental degradation has varied effects on ecological parameters across
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the world, with records of anthropogenic landscape interference being made about the richness of species (Remsen and Parker, 1983; Jullien and Thiollay, 1996; Nupp and Swihart, 2000; Pardini et al., 2005;
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Holland and Bennett, 2007), as well as interfering in species composition (Vivian-Smith, 1997; Pardini, 2004; Bonecker et al., 2009; Gheler-Costa et al., 2012) and abundance, particularly in agricultural areas (Rappole and Morton, 1985; Heroldová et al., 2007; Bonecker et al., 2009; Verdade et al., 2012). Pardini et al (2005) stated that the size of the fragments positively influenced the abundance
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and richness of small mammals proportionally, while Nupp and Swihart (2000) found the same for richness. The correlation between the size of fragments and richness and abundance of small mammals has been shown to be positive according to Flinday and Houlahan (1997) and Fonseca and Robinson (1990). Even more so about richness when there are conglomerates or other fragments in the surroundings within a radius of 2 km, as in the mosaics (Flindlay and Houlahan, 1997). This would lead to the assumption that species loss would be related to habitat area and landscape configuration. In spite of the consequences of degradation on biological communities, mammals’ elevated species richness, endemism (Bonvicino et al., 2002) and population abundance stand out in the Atlantic
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Forest. Within this class, small mammals as rodents and marsupials are the land representatives with the greatest richness and abundance (Paglia et al., 2012), and two of the three orders with the highest level of endemism in the Atlantic Forest (Costa et al., 2000). The species of these groups act as seed dispersers and plant and small animal populations controllers (Sanchez-Cordero and Martinez-Gallargo, 1998; Cáceres and Monteiro-Filho, 2007). They also act as prey for larger mammals, snakes and birds (RochaMendes et al., 2010) as well as provide other important contributions for the maintenance and recuperation of forests and their ecological interactions (Jordano et al., 2006). In this study we investigated how the richness, abundance and composition of small mammal assemblages responded to fragment size and to the habitats present in the studied landscape. In this way, two predictions were tested: I – the richness and abundance of small mammals will be lower in the sugarcane plantation than in the forest, increasingly so from small forest fragments to large forest
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fragments; II – the composition of species will differ between the environments (the two forest fragments
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and the sugarcane plantation).
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Methods
This study was carried out in the Usina São José (USJ) plantation, with 28000 hectares
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belonging to the Cavalcanti Petribu group, based on the state highway PE-41, km 10.7, Igarassu, Pernambuco, Northeastern Brazil (São José Agroindustrial, 2017). The plantation is located in the Atlantic Forest area in the Center of Pernambuco Endemism (CEPE) and the classification of the forest in
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the region is Dense Ombrophilous Forest (Veloso and Góes-Filho, 1982). The climate is classified as type As’ (Köppen) and there are two well defined seasons, dry and rainy (Alvares et al., 2014). The landscape is organised into three categories: sugarcane plantations, other anthropogenic
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areas (urban, livestock farms, forest plantations, etc.) and fragments of Atlantic Forest, representing 55.59%, 14.24% and 30.17% respectively (Silva, 2015), comprising the largest part of the CEPE territory. We sampled the most representative habitats of the landscape: five large forest fragments (G, between
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284.38 ha and 410.463 ha), five small fragments (P, from 13.8 ha to 36 ha) and five points in the sugarcane matrix (C), with an average distance of 200 meters from the fragments (Fig. 1, Table 1). Although secondary forests were present in the USJ landscape, all the fragments included in this study were categorized as mature forest (Lins and Silva, 2010). The edge effect in the USJ area corresponds to a
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range of 40 - 60 meters in the perimeter of the fragments (Silva et al., 2008). In the sugarcane matrix, samples were taken from plots that had a plantation height of more than one meter and the presence of small shrubbery and herbaceous vegetation.
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A 1 0
C
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Fig.1–Areas sampled for rodents and marsupials between January and October 2016 in the Usina São
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José, Igarassu (Pernambuco, Northeastern Brazil). A – map of Brazil highlighting the state of Pernambuco; B – the state of Pernambuco, highlighting the municipality of Igarassu; C – the municipality of Igarassu; D – partial view of the municipality of Igarassu, highlighting the study areas. The matrix in light grey with triangles represents the sample sites in the sugarcane plantations (C1 to C5), small forest
Small mammal captures
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fragments (P1 to P5) are in dark grey and large forest fragments in light grey (G1 to G5).
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The capture of small mammals was performed between January and October 2016, during five
months of the dry period and five months of the rainy period, always during the new Moon (Read and Moseby, 2001). In all areas, three campaigns were carried out for six consecutive days, totalizing 45 days per category (G, P and C) for each seasonal stage (dry and rainy). This totalled 90 days of capture per
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habitat category, being the samples taken simultaneously from each habitat in each campaign. We captured animals using Tomahawk (17cm x 17cm x 44cm) and Sherman traps (14cm x 11.5cm x 43cm; 7.5cm x 9.5cm x 30.5cm). Forty-five traps were placed in each area a transect of 230m, in the bordercenter direction, starting from 50m after the edge of the fragment. Two traps (one Tomahawk and one Sherman) were positioned along the transect every ten meters, alternating ground and understory (from 1m to 1.5m in height). In the sugarcane plantation, all the traps were positioned on the ground. The traps remained open during the day and night, holding baits with a mixture of pineapple with crushed peanuts, and were visited once a day.
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The captured animals were identified and marked at the research base and were freed the following day at the same location where they were captured. Marking was achieved through tattooing the animals’ left ear, using a letter to represent each area of capture and a number referring to the individual. For this, we used surgically sterilized and disposable needles with vegetable-based pigments: black color for paler skin tones and pink color for darker ones. All the proceedings were authorized by federal license SISBIO N° 53991-1/2016. The identification of each animal was achieved using external characteristics, following Gardner (2007) and Patton et al. (2015). Only when necessary (e.g. for Sigmodontinae family), one individual from each morphotype was euthanized, following the recommendations of the Board of Veterinary Medicine, and identified by a specialist through the analysis of the skull. Data Analysis
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Data normality was verified by the Shapiro-Wilk K test. The richness and abundances
observed were recorded for data analysis. For each area, the expected richness was calculated using the bootstrap as estimator by the program Estimates 9.10, as well as the absolute number of registered
species. The Analysis of Variance (ANOVA) was used to test if there were differences in the data of
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species abundance and richness between the dry and rainy seasons. ANOVA was also used to verify the statistical difference of richness and abundance between large and small forest fragments and sugarcane
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crops. When there was significant difference between the three categories, Tukey's comparison test was performed in pairs. The ranking/abundance graph (Whittaker’s Graph) with geometric distribution, was generated to evaluate the abundance of each studied category: large forests, small forests and sugarcane
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crops. To better describe the assemblages, the Relative Abundance (AR) of species per assemblage was associated with richness, in accordance with Paglia et al. (2012). The visual analysis of small mammal community composition between the categories (G, P and C) was carried out using a Non-Metric Multidimensional Scaling (NMDS) analysis and by using the Bray-Curtis Coefficient (Hammer et al.,
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2001). The relation between the environmental descriptors (habitat category and the size of forest fragments) and the compositions of assemblages was made through the canonical correspondence
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analysis (CCA). To evaluate the significance of differences between the composition of the three categories, we used one-way Multivariate Analysis of Variance (MANOVA) also using the Bray-Curtis Coefficient (Hammer et al., 2001). The percentage of similarity between the formed groups and the identification of the most densely grouped species in the fragments were analysed using SIMPER
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(Hammer et al., 2001). The statistical tests were performed using “Past 2.17” (Hammer et al., 2001).
Results
For the whole USJ agricultural mosaic, 10 species of small mammals were found, three of which were rodents and the other seven marsupials (Table 2). We registered 129 captures, with 100 individuals, of which the majority was represented by the order Didelphimorphia (89.2%). Of the 29 recaptures, 22.48% of the total number of captures, only one individual was found to move to another
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habitat (one Didelphis albiventris individual was captured in the forest and then in the sugarcane plantation). These data were the result of 12.150 traps-day with a Capture Success (SC) of 1.06%. Since richness, abundance and composition did not present a significant difference between seasons (F = 0.29; p = 0.6 and F = 1.11; p = 0.3; F = 0.33, p = 0.56, respectively), we chose to analyse the data as a single set. The normality of the collected data was confirmed by the Shapiro-Wilk K test with 0.79 and p = 0.68 to G, 0.88 and p = 0.31 to P, and 0.98 and p = 0.94 to C. The richness observed came from four species for the sugarcane plantation, five species for the large forest fragments and eight species for the small forest fragments (Table 2). We found a significant difference when comparing the richness between small fragments and the sugarcane matrix (F = 6.081; p = 0.023) however, there was no significant difference between the size of forest fragments (F = 1.796; p = 0.176), nor between the sugarcane matrix and the large fragments (F = 0.782; p = 0.388). The order Rodentia presented two representatives in the
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sugarcane plantation and one in the forest fragments. We registered seven species of Didelphimorphia in
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the forest fragments and only two in the sugarcane crops. Based on the bootstrap estimator (SD=0), our
samples reached 95%, 94.8% and 80% of the richness expected (corresponding to 9.62, 5.27 and 4.99 in terms of estimated richness) for the small fragments, large fragments and the sugarcane plantation
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respectively.
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Abundance differed significantly among the three categories (F=6.32 and p= 0.0039), between forest categories based on size, large and small fragments (T = 0.024) and between habitats, large forest
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fragments and the sugarcane plantation (T = 0.005). However, when this same analysis was performed for small fragments and the sugarcane plantations, there was no significant difference (T=0.814). Besides the greater abundance, the assemblages of the larger forest fragments (FG) showed a greater dominance, revealed by the extremely steep curved line in the ranking/abundance graph, in
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comparison with the more uniform assemblages of the smaller forest fragments (FP) and sugarcane crops (Fig. 2). In this way, the abundance of species found in the sugarcane plantation and in the small
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fragments is similar, whereas in the large fragments one species was considered more dominant over the other less frequent species.
In the two forest categories, G and P, the most abundant species was Marmosa demerarae,
with a relative abundance (AR) of 61% and 40% respectively, followed by Didelphis albiventris (G-17%
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and P- 11%) and Didelphis aurita (G-12% and P-26%). Monodelphis americana (3.37%) was only registered once, in a small fragment, and it was the least represented of the species. In the sugarcane plantation, 61.1% of the species captured were rodents and 38.9% were marsupials. In this habitat, half of all captured animals were of the most abundant species, Necromys lasiurus (50%), followed by Monodelphis domestica (33.3%).
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Fig. 2 – The geometric distribution of ranking/abundance of the study areas in the Usina São José, Igarassu – PE, Northeastern Brazil. Subtitle: G, large fragments; P, small fragments; and C, sugarcane
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plantation.
The analysis of assemblage composition grouped the forest fragments (Fig. 3) due to the large number of shared species between the two environments, and it separated these species from those found
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in the sugarcane plantation (Table 2). For the composition analysis, the fourth area investigated in the sugarcane plantation (C4) was excluded, due to the absence of captures. The MANOVA demonstrated a significant difference between the three categories (F = 2.733; p = 0.0012). When we performed the
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pairwise test, we did not find a significant difference between the forest categories (P and G), however we found a significant difference between the sugarcane plantations and the forest fragments (P x C, p =
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0.0073 and G x C, p = 0.015). The SIMPER presented high dissimilarity between the sugarcane plantation and the large and small forest fragments, 98.36% and 97.48% respectively, however, the difference between the fragments was smaller, 76.38%. The species that contributed to the difference
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between the sugarcane plantation and the forest fragments was Marmosa demerarae.
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F10P
F7P
F9G
C1 F6G
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F5P F2G
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F4P
C4
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F3P
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Fig. 3– NMDS axis 1 + NMDS axis 2 formed by a cluster analysis, based on the Bray-Curtis coefficient, which separated the habitats by clusters based on assemblage composition, overlapping the forest areas. Subtitle – C, sugarcane plantation areas, F, forest fragments followed by the number corresponding to
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Table 1; G, large fragments and P, small fragments.
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Discussion During the evaluation of the effects of habitat structure on small mammals, the abundance and richness parameters were found to be negatively influenced by environmental quality of the habitat. Land use changes in the natural environments lead to the reduction in biodiversity parameters (Dixon et al., 2009; Fahrig et al., 2011 and Hass et al., 2018). The richness registered in this study was within the expected values for agricultural mosaics in Atlantic Forest enclaves, according to Gheler-Costa et al. (2012). The richness observed in the USJ – 1% of the CEPE area, represents 40% of the total of 25 species of rodents and marsupials registered in the CEPE (Oliveira and Langguth, 2004; Asfora and Mendes Pontes, 2009; Dantas-Torre et al., 2012). According to the percentage reached by the richness estimator, we obtained a great representativeness of species sampled in the region where the landscape is inserted.
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The lowest richness found was in the sugarcane plantation, and it supports Wijesinghe and
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Brooke’s (2005) results, who found a difference in richness between forests and anthropogenic habitats. Although Gheler-Costa et al. (2012) also registered a difference in the richness of small mammals
between the study habitats, in their samples the greatest number of species was found in the sugarcane
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plantation. This inversion of values is due to the higher number of representatives of the order Rodentia in the work of Gheler-Costa et al. (2012) compared to the unexpected greater number of marsupials registered in this study. Despite the increased number of species found in the small fragments in relation
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to the larger ones, there was no significant difference between the forest fragments, which was similar to the results found by Pardini (2004) in the Atlantic Forest. Our data show that the type of habitat interferes
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with richness, with a decrease in the number of species in the sugarcane. However, in the landscape configuration, the difference between fragment sizes does not significantly interfere with richness. It is essential to emphasize the role of small fragments in the management of species, where three more species were found compared to the large fragments, as well as their role in acting as
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functional corridors. Turner and Corllet (1996), pointed out that small fragments such as these are functionally effective in acting as refuges for fauna and flora, allowing for the management of species at
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risk of extinction. However, this role of safeguarding biodiversity may be at its limit, since Estavillo et al. (2013) demonstrated that below 30% of forest cover there is a decline in small mammal richness. The richness registered in our study areas, together with the fact that the USJ is found close to the aforementioned limit, reinforces the necessity of fauna management. This situation can be modified by
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small changes in landscape (such as ecological corridors), due to the proportion of forested area in the USJ (30.17%). In anthropogenic landscapes, such as agricultural mosaics, its components have a greater value for conservation when considered together, compared to the value of each component individually (Pardini, 2004).
Three factors are important in explaining the richness observed in this study. Firstly, in tropical forests some taxa have complex patterns of endemism and grouped distributions. We agree with Laurance and Vasconcelos (2009) who concluded that the absence of species in a given location may represent a natural pattern. Secondly, despite the tendency of the matrix to act as a barrier for more sensitive species,
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it allowed the establishment of species from other biomes. This can be exemplified by the presence of Calomys expulsus in this study, which has a natural distribution in the Cerrado and the Caatinga (Oliveira and Langguth, 2004). Finally, the smaller fragments actually acted as shelter and safe passageways for the fauna. As so, our results agree with Dunn (2004) who suggests that in regenerating forests, some taxa tend to have a greater richness in smaller fragments even if only temporarily. The pattern of abundance in the study area, with significant differences between forest and plantations, was also observed by Gheler-Costa et al. (2012). The lower number of individuals found in the sugarcane plantation, predominantly rodents, was also found by Verdade et al. (2012). Since sugarcane farming is an intensive activity, the environmental patterns in these habitats are distinct from those of the forest, with poorer air, soil and water quality (Stoate et al., 2009), as well as the absence of canopy and strata coverage and decreased food variability. Thus, the influence of habitat type on the
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abundance of small mammals could be altered by the resource availability and the degree of disturbance
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along the categories, which gradually decreased from great forest fragments to small ones, followed by sugarcane plantations.
Regarding the size of forest fragments, abundance was significantly greater in the larger
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fragments when compared to the smaller fragments, which corroborates the findings of Laurance (1994) and Pardini et al. (2005). Notably, in these environments there are ecological characteristics that are
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fundamental in determining the abundance of assemblages and that explain the greater adaptation of these assemblages to larger fragments. We agree with Laurance et al. (1998), who highlight the fact that in small fragments there is a decrease in environmental quality with modifications in the microclimate and
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an increase in tree mortality. Additionally, we agree with Uezu et al. (2005), when they state that larger fragments house more stable populations long-term. Smaller assemblages are more susceptible to stochastic events (Brito, 2009; Laurance and Vasconcelos, 2009), highlighting the importance of communication between fragments of different sizes in such a way that allows for the migration and
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establishment of species in these environments, particularly for species which avoid the matrix. The composition of assemblages was not explained by fragment size, but rather by the types of
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habitat sampled – forest and sugarcane matrix. This result is in agreement with studies developed in the Atlantic Forest on small mammals by Bonvicino et al. (2002), who analysed data from from forests and altered matrices, and by Umetsu and Pardini (2007) and Gheler-Costa et al. (2012), who compared forested and agricultural areas. The species that contributed the most to the difference found in this study
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had a restricted distribution, as well as a greater abundance in the forest (M. demerarae). Species tolerant to the open areas were registered in the sugarcane plantation, agreeing with Benedek and Sirbu (2018) who have suggested that species less tolerant to tree cover are more abundant in agricultural areas. Thus, the abundance of assemblages in the forest and in the sugarcane plantation associated with the presence/absence of the species in the environments was determinant in differentiating the compositions of the assemblages. The ecological causes that explain the results of the abundance and composition of the small mammal assemblages are closely intertwined. The dominance observed in the forest assemblages
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indicates the success of M. demerarae in competing for available resources in this habitat. This species, despite using different forest strata, is essentially arboreal (Vieira and Monteiro-Filho, 2003; Paglia et al., 2012). The greater abundance of this species in larger forest fragments (62.2%) is justified by its dependence on more structured forests, as observed by Castro and Fernandez (2004). The authors emphasised that mammals with a strong dependence on mature forests, decreased in abundance or disappeared in small fragments (Castro and Fernandez, 2004). It is worth noting, that despite D. aurita being considered a habitat specialist (Cáceres et al., 2016), its greater relative abundance found in the smaller study fragments may be a strategy for the maintenance of the species in highly fragmented environments, which increases its adaptive power. In the sugarcane plantation, only two marsupials were registered and M. domestica was the second most abundant mammal. Due to its terrestrial habitat, this species does not suffer from the loss of
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vertical stratification. We found a greater abundance of rodents in the sugarcane plantation, a result which
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has also been found by Verdade et al. (2012) and Santos et al. (2016), who explained this result as a
consequence of the greater availability of food in sugarcane plantations. We found that this availability was due not only to the sugarcane itself, but also to the herb vegetation associated with sugarcane, serving
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as an alternative source of food. The most abundant species in the sugarcane habitat was N. lasiurus, which was also the most abundant species in a study by Gheler-Costa et al. (2012). All the species present in the sugarcane plantation were essentially terrestrial, except for D. albiventris, initially recorded in the
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forest.
The observed distribution of species in the study habitats is a reflection of the adaptation of
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species to their environments, with the sigmodontinae exclusively inhabiting the sugarcane plantation and five of the seven marsupial species being restricted to the forested areas. Marsupial adaptation to the upper strata of their environment makes it impossible to establish certain species in the sugarcane matrix due to the absence of their niche. Of the marsupials found in the sugarcane plantation, D. albiventris was
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found once in this habitat. Its generalist behaviour favours the occupation of agricultural areas due to the greater availability of food with higher energy content and reduced competition. However, the use of the
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sugarcane matrix temporarily annuls its scansorial behaviour due to the absence of upper strata. Gheler-Costa et al. (2012) registered less complex communities of small mammals in landscapes with an agricultural matrix and forest fragment remnants when compared to untouched forests. However, our results demonstrated that forested areas house species with a greater diversity which occupied
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different niches. Even within the agricultural mosaic, the forest fragments presented more complex assemblages compared to the modified matrix. Our results are in accordance with Luza et al. (2016) who recorded simplified assemblages in disturbed sites, like sugarcane plantations. The association of small mammals with their habitats, restricted the majority of the collected marsupials to the forests and the rodents to the sugarcane matrix. However, this does not completely prevent interspecific ecological interactions between these orders of mammals. The exclusivity of the six species found in the forest fragments reinforces the importance of the conservation of these environments, considering the affirmation of Gascon et al. (1999), stating that species that avoid modified matrices tend
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to decrease in number or disappear. In this way, the sugarcane matrix acts by selecting the species with the greatest environmental plasticity and not as an insurmountable barrier. This restricts the distribution of species dependent on forests, increasing the distribution and abundance of more environmentally flexible species, such as exotic ones, to the detriment of the native species. The complexity of the ecological responses of assemblages as a result of anthropogenic modifications in the study environments reiterates the importance of forest fragment conservation, regardless of size. The large fragments are essential for the viability of populations long-term, whereas the smaller fragments safeguard species in anthropogenic scenarios, and act as connections between the fragments. Despite the importance of the conservation of forest corridors in the face of habitat fragmentation, in heavily anthropic areas where there is no possibility of forest restoration, land uses that allow the maintenance of native species in the landscape and / or those whose characteristics are similar
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to the natural environment, are essential for the dynamics of the mammalian populations.
'Declarations of interest: none'
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Funding: This study was supported by CAPES
Acknowledgements: Petribu-Cavalcanti/Grupo Usina São José for permission and Pedro Aguilar Cescon
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for revising the English language of the manuscript.
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species of small mammals and birds in a tropical rain forest in Sri Lanka. J Trop Ecol 21:661–668
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Table 1: Locations of rodent and marsupial samples between January and October 2016, in the Usina São José (Igarassu, Pernambuco, Northeaster of Brazil), names of locations; coordinates; area size and
Coordinates (UTM)
Area (ha)
Sample site code
FG
Avião
S 07°49’13.5” W 034°59’14.8”
410.46
G1
FG
Macacos
S 07°46’53.9” W 035°00’30.6”
356.94
G2
FG
Piedade
S 07°50’19.6” W 034°59’46.3”
308.98
G3
FG
Vizinho de Dedo de Deus
S 07°45’27.8” W 035°00’34.1”
322.71
G4
FG
Vizinho do Avião
S 07°44’59.4” W 034°58’51.8”
284.38
FP
Chico Dias
S 07°49’14.96” W 034°59’37.0”
15.5
FP
Paô
S 07°48’36.1” W 034°59’16.3”
FP
Córrego da Carniça
S 07°48’21.9” W 034°59’10.6”
FP
Pezinho
S 07°47’56.3” W 035°01’24.6”
FP
Vizinho de Vespa
C
Cana Pezinho
C
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Habitat / Location Category
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corresponding sample site codes – FP, small fragments, FG, large fragments, and C, sugarcane plantation.
G5
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P1 P2
36
P3
29.8
P4
S 07°44’58.4” W 034°58’51.9”
14
P5
S 07°47'56.1" W 035°01'26.2"
-
C1
Cana Piedade
S 07°50’00.6” W 034°59’44.6”
-
C2
Cana Vizinho de Avião
S 07°47'43.5" W 034°57'42.4"
-
C3
C
Cana Vizinha a S 07°45’46.8” Dedo Deus W 035°00’43.8”
-
C4
C
Cana do Paô
S 07°48’44.6” W 034°59’13.5”
-
C5
Pr
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C
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13.8
19
Table 2: Rodent and marsupial taxa, abundance and richness for the studied categories at Usina São José, Igarassu – PE, Northeastern Brazil. Habitat Use according to Paglia et. al (2012). Taxa
Habitat Use
Large Fragments Small Fragments Sugarcane G P C
DIDELPHIMORPHIA Didelphidae Didelphis aurita (Wied-Neuwied, 1826)
Sc
Didelphis albiventris Lund, 1840
Sc
Marmosa murina (Linnaeus, 1758)
Sc
Marmosa (Micoreus) demerarae Thomas, 1905
Ar
Metachirus nudicaudatus (É. Geoffroy, 1803)
Te
Monodelphis americana (Muller, 1776)
Te
Monodelphis domestica (Wagner, 1842)
Te
3
1
3
0
50
11
0
1 3
Sigmodontinae
Pr
Te
1
e-
0
1
0
Te
0 0
pr
0
f
5
Echimydae
6
2
0
0
9
0
2
al
0
Te
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Necromys lasiurus (Lund, 1838) Calomys expulsus (Lund, 1841)
0
oo
14
RODENTIA Thricomys laurentius Thomas, 1904
7 10
0
82
29
18
Richness
5
8
4
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Abundance
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PII:
S1616-5047(19)30031-X
DOI:
https://doi.org/10.1016/j.mambio.2019.09.010
Reference:
MAMBIO 41141
To appear in:
Mammalian Biology
Received Date:
12 February 2019
Accepted Date:
24 September 2019
˜ M, de Oliveira MAB, Montes MA, Implications of an Please cite this article as: Falcao agricultural mosaic in small mammal communities, Mammalian Biology (2019), doi: https://doi.org/10.1016/j.mambio.2019.09.010
This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier.
Implications of an agricultural mosaic in small mammal communities
Marina Falcãoa*, Maria Adélia B. de Oliveirab, Martín Alejandro Montesc *[email protected]
a
Graduation Program in Ecology, Biology Department, Federal Rural University of Pernambuco,
Rua Dom Manoel de Medeiros, s/n, CEP: 52171-900, Recife/Pernambuco, Brazil. Correspondent author. b
Laboratory of Ecophysiology and Animal Behavior, Department of Animal Morphology and
Physiology, Federal Rural University of Pernambuco.
f
Laboratory of Genetics, Department of Biology, Federal Rural University of Pernambuco.
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c
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Abstract
The ideas that larger fragments have greater species richness and abundance, when compared to smaller fragments and altered environments, and that assemblage composition is different, was
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tested in an agricultural mosaic using data on small mammals. To achieve this, we sampled ten forest fragments of different sizes, small and large, as well as five areas in a sugarcane matrix,
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through the capture-mark-recapture method. The study was conducted in a sugarcane plantation (Usina São José, Igarassu, Pernambuco, Brazil) from January to October 2016. There was a significant difference when comparing richness between small fragments (eight species) and the sugarcane matrix (four species). Abundance differed significantly between all areas, being
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influenced by fragment size and habitat type. We found that abundance was positively influenced by forested environments and, among them, larger fragments. The composition of assemblages in the forest fragments and the sugarcane matrix differed clearly for NMDS,
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MANOVA and SIMPER analyses. Between the habitats, assemblage parameters were also distinct. Lower abundance and richness were found in the sugarcane matrix, where the presence of rodents was associated with food availability and less competition; and higher abundance and richness was measured in forest fragments, where there was a strong association between
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marsupials and forest strata. The landscape configuration in an agricultural mosaic can compromise the level of interspecific interactions of small mammals, which negatively impacts the ecological processes of forested areas. In this case, the conservation of a matrix permeable to most species and the preservation of all fragments are necessary, since small and large fragments have different functions in the maintenance of species.
Keywords: Atlantic Forest, sugarcane, richness, abundance, composition and assemblage.
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Introduction The conversion of landscapes from natural to anthropogenic ones brings with it drastic biological consequences, especially in the tropics (Ranganathan et al., 2008), i.e. regions with high biodiversity and accelerated degradation (Laurance, 2010). This process of conversion is responsible for the loss in vegetation cover and deforestation, both of which are associated with fragmentation (Nagendra et al., 2004). Historically, habitat loss was caused by the growth of urban areas, industrial growth, construction of highways and agriculture (Geist and Lambin, 2002; Butler and Laurance, 2008), driving approximately 65% of deforestation in the planet’s tropical regions (Geist and Lambin, 2002). Between 1990-2010, agricultural expansion stimulated a loss of vegetation cover of two million 2
km in the neotropics, among it Africa (including Madagascar) and southeast Asia regions (Estrada et al., 2017). In the same period, in Brazil, agricultural areas grew by 34 million hectares and approximately 7%
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of native forested areas were converted into agricultural land over a period of 11 years (OECD/FAO, 2015). Within agricultural production we can highlight farming of sugarcane, of which Brazil is the
largest producer in the world (OECD/FAO, 2015), and was one of the main causes of the fragmentation
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of the Atlantic Forest (Silveira et al., 2003).
The Atlantic Forest is categorized for its high heterogeneity, species richness and endemism (Tabarelli et al., 2005; Ribeiro et al., 2009). However, the biome has lost approximately 88% of its
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original cover (Ribeiro et al., 2011), leaving 87.5% of the forest remnants labeled as small (<50ha) (SOS Mata Atlântica and INPE, 2018) and less than 3% as larger than 250ha (Ribeiro et al., 2009). In the Center of Endemism Pernambuco – CEPE, a biogeographic sub-region of the Brazilian Atlantic Forest,
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there is only 11.5% of forest remnants, presenting one of the biome’s largest examples of destruction (Ribeiro et al., 2009).
The high level of environmental degradation has varied effects on ecological parameters across
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the world, with records of anthropogenic landscape interference being made about the richness of species (Remsen and Parker, 1983; Jullien and Thiollay, 1996; Nupp and Swihart, 2000; Pardini et al., 2005;
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Holland and Bennett, 2007), as well as interfering in species composition (Vivian-Smith, 1997; Pardini, 2004; Bonecker et al., 2009; Gheler-Costa et al., 2012) and abundance, particularly in agricultural areas (Rappole and Morton, 1985; Heroldová et al., 2007; Bonecker et al., 2009; Verdade et al., 2012). Pardini et al (2005) stated that the size of the fragments positively influenced the abundance
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and richness of small mammals proportionally, while Nupp and Swihart (2000) found the same for richness. The correlation between the size of fragments and richness and abundance of small mammals has been shown to be positive according to Flinday and Houlahan (1997) and Fonseca and Robinson (1990). Even more so about richness when there are conglomerates or other fragments in the surroundings within a radius of 2 km, as in the mosaics (Flindlay and Houlahan, 1997). This would lead to the assumption that species loss would be related to habitat area and landscape configuration. In spite of the consequences of degradation on biological communities, mammals’ elevated species richness, endemism (Bonvicino et al., 2002) and population abundance stand out in the Atlantic
2
Forest. Within this class, small mammals as rodents and marsupials are the land representatives with the greatest richness and abundance (Paglia et al., 2012), and two of the three orders with the highest level of endemism in the Atlantic Forest (Costa et al., 2000). The species of these groups act as seed dispersers and plant and small animal populations controllers (Sanchez-Cordero and Martinez-Gallargo, 1998; Cáceres and Monteiro-Filho, 2007). They also act as prey for larger mammals, snakes and birds (RochaMendes et al., 2010) as well as provide other important contributions for the maintenance and recuperation of forests and their ecological interactions (Jordano et al., 2006). In this study we investigated how the richness, abundance and composition of small mammal assemblages responded to fragment size and to the habitats present in the studied landscape. In this way, two predictions were tested: I – the richness and abundance of small mammals will be lower in the sugarcane plantation than in the forest, increasingly so from small forest fragments to large forest
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fragments; II – the composition of species will differ between the environments (the two forest fragments
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and the sugarcane plantation).
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Methods
This study was carried out in the Usina São José (USJ) plantation, with 28000 hectares
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belonging to the Cavalcanti Petribu group, based on the state highway PE-41, km 10.7, Igarassu, Pernambuco, Northeastern Brazil (São José Agroindustrial, 2017). The plantation is located in the Atlantic Forest area in the Center of Pernambuco Endemism (CEPE) and the classification of the forest in
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the region is Dense Ombrophilous Forest (Veloso and Góes-Filho, 1982). The climate is classified as type As’ (Köppen) and there are two well defined seasons, dry and rainy (Alvares et al., 2014). The landscape is organised into three categories: sugarcane plantations, other anthropogenic
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areas (urban, livestock farms, forest plantations, etc.) and fragments of Atlantic Forest, representing 55.59%, 14.24% and 30.17% respectively (Silva, 2015), comprising the largest part of the CEPE territory. We sampled the most representative habitats of the landscape: five large forest fragments (G, between
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284.38 ha and 410.463 ha), five small fragments (P, from 13.8 ha to 36 ha) and five points in the sugarcane matrix (C), with an average distance of 200 meters from the fragments (Fig. 1, Table 1). Although secondary forests were present in the USJ landscape, all the fragments included in this study were categorized as mature forest (Lins and Silva, 2010). The edge effect in the USJ area corresponds to a
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range of 40 - 60 meters in the perimeter of the fragments (Silva et al., 2008). In the sugarcane matrix, samples were taken from plots that had a plantation height of more than one meter and the presence of small shrubbery and herbaceous vegetation.
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A 1 0
C
B
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D
Fig.1–Areas sampled for rodents and marsupials between January and October 2016 in the Usina São
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José, Igarassu (Pernambuco, Northeastern Brazil). A – map of Brazil highlighting the state of Pernambuco; B – the state of Pernambuco, highlighting the municipality of Igarassu; C – the municipality of Igarassu; D – partial view of the municipality of Igarassu, highlighting the study areas. The matrix in light grey with triangles represents the sample sites in the sugarcane plantations (C1 to C5), small forest
Small mammal captures
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fragments (P1 to P5) are in dark grey and large forest fragments in light grey (G1 to G5).
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The capture of small mammals was performed between January and October 2016, during five
months of the dry period and five months of the rainy period, always during the new Moon (Read and Moseby, 2001). In all areas, three campaigns were carried out for six consecutive days, totalizing 45 days per category (G, P and C) for each seasonal stage (dry and rainy). This totalled 90 days of capture per
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habitat category, being the samples taken simultaneously from each habitat in each campaign. We captured animals using Tomahawk (17cm x 17cm x 44cm) and Sherman traps (14cm x 11.5cm x 43cm; 7.5cm x 9.5cm x 30.5cm). Forty-five traps were placed in each area a transect of 230m, in the bordercenter direction, starting from 50m after the edge of the fragment. Two traps (one Tomahawk and one Sherman) were positioned along the transect every ten meters, alternating ground and understory (from 1m to 1.5m in height). In the sugarcane plantation, all the traps were positioned on the ground. The traps remained open during the day and night, holding baits with a mixture of pineapple with crushed peanuts, and were visited once a day.
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The captured animals were identified and marked at the research base and were freed the following day at the same location where they were captured. Marking was achieved through tattooing the animals’ left ear, using a letter to represent each area of capture and a number referring to the individual. For this, we used surgically sterilized and disposable needles with vegetable-based pigments: black color for paler skin tones and pink color for darker ones. All the proceedings were authorized by federal license SISBIO N° 53991-1/2016. The identification of each animal was achieved using external characteristics, following Gardner (2007) and Patton et al. (2015). Only when necessary (e.g. for Sigmodontinae family), one individual from each morphotype was euthanized, following the recommendations of the Board of Veterinary Medicine, and identified by a specialist through the analysis of the skull. Data Analysis
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Data normality was verified by the Shapiro-Wilk K test. The richness and abundances
observed were recorded for data analysis. For each area, the expected richness was calculated using the bootstrap as estimator by the program Estimates 9.10, as well as the absolute number of registered
species. The Analysis of Variance (ANOVA) was used to test if there were differences in the data of
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species abundance and richness between the dry and rainy seasons. ANOVA was also used to verify the statistical difference of richness and abundance between large and small forest fragments and sugarcane
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crops. When there was significant difference between the three categories, Tukey's comparison test was performed in pairs. The ranking/abundance graph (Whittaker’s Graph) with geometric distribution, was generated to evaluate the abundance of each studied category: large forests, small forests and sugarcane
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crops. To better describe the assemblages, the Relative Abundance (AR) of species per assemblage was associated with richness, in accordance with Paglia et al. (2012). The visual analysis of small mammal community composition between the categories (G, P and C) was carried out using a Non-Metric Multidimensional Scaling (NMDS) analysis and by using the Bray-Curtis Coefficient (Hammer et al.,
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2001). The relation between the environmental descriptors (habitat category and the size of forest fragments) and the compositions of assemblages was made through the canonical correspondence
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analysis (CCA). To evaluate the significance of differences between the composition of the three categories, we used one-way Multivariate Analysis of Variance (MANOVA) also using the Bray-Curtis Coefficient (Hammer et al., 2001). The percentage of similarity between the formed groups and the identification of the most densely grouped species in the fragments were analysed using SIMPER
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(Hammer et al., 2001). The statistical tests were performed using “Past 2.17” (Hammer et al., 2001).
Results
For the whole USJ agricultural mosaic, 10 species of small mammals were found, three of which were rodents and the other seven marsupials (Table 2). We registered 129 captures, with 100 individuals, of which the majority was represented by the order Didelphimorphia (89.2%). Of the 29 recaptures, 22.48% of the total number of captures, only one individual was found to move to another
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habitat (one Didelphis albiventris individual was captured in the forest and then in the sugarcane plantation). These data were the result of 12.150 traps-day with a Capture Success (SC) of 1.06%. Since richness, abundance and composition did not present a significant difference between seasons (F = 0.29; p = 0.6 and F = 1.11; p = 0.3; F = 0.33, p = 0.56, respectively), we chose to analyse the data as a single set. The normality of the collected data was confirmed by the Shapiro-Wilk K test with 0.79 and p = 0.68 to G, 0.88 and p = 0.31 to P, and 0.98 and p = 0.94 to C. The richness observed came from four species for the sugarcane plantation, five species for the large forest fragments and eight species for the small forest fragments (Table 2). We found a significant difference when comparing the richness between small fragments and the sugarcane matrix (F = 6.081; p = 0.023) however, there was no significant difference between the size of forest fragments (F = 1.796; p = 0.176), nor between the sugarcane matrix and the large fragments (F = 0.782; p = 0.388). The order Rodentia presented two representatives in the
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sugarcane plantation and one in the forest fragments. We registered seven species of Didelphimorphia in
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the forest fragments and only two in the sugarcane crops. Based on the bootstrap estimator (SD=0), our
samples reached 95%, 94.8% and 80% of the richness expected (corresponding to 9.62, 5.27 and 4.99 in terms of estimated richness) for the small fragments, large fragments and the sugarcane plantation
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respectively.
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Abundance differed significantly among the three categories (F=6.32 and p= 0.0039), between forest categories based on size, large and small fragments (T = 0.024) and between habitats, large forest
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fragments and the sugarcane plantation (T = 0.005). However, when this same analysis was performed for small fragments and the sugarcane plantations, there was no significant difference (T=0.814). Besides the greater abundance, the assemblages of the larger forest fragments (FG) showed a greater dominance, revealed by the extremely steep curved line in the ranking/abundance graph, in
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comparison with the more uniform assemblages of the smaller forest fragments (FP) and sugarcane crops (Fig. 2). In this way, the abundance of species found in the sugarcane plantation and in the small
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fragments is similar, whereas in the large fragments one species was considered more dominant over the other less frequent species.
In the two forest categories, G and P, the most abundant species was Marmosa demerarae,
with a relative abundance (AR) of 61% and 40% respectively, followed by Didelphis albiventris (G-17%
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and P- 11%) and Didelphis aurita (G-12% and P-26%). Monodelphis americana (3.37%) was only registered once, in a small fragment, and it was the least represented of the species. In the sugarcane plantation, 61.1% of the species captured were rodents and 38.9% were marsupials. In this habitat, half of all captured animals were of the most abundant species, Necromys lasiurus (50%), followed by Monodelphis domestica (33.3%).
G
P
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Fig. 2 – The geometric distribution of ranking/abundance of the study areas in the Usina São José, Igarassu – PE, Northeastern Brazil. Subtitle: G, large fragments; P, small fragments; and C, sugarcane
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plantation.
The analysis of assemblage composition grouped the forest fragments (Fig. 3) due to the large number of shared species between the two environments, and it separated these species from those found
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in the sugarcane plantation (Table 2). For the composition analysis, the fourth area investigated in the sugarcane plantation (C4) was excluded, due to the absence of captures. The MANOVA demonstrated a significant difference between the three categories (F = 2.733; p = 0.0012). When we performed the
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pairwise test, we did not find a significant difference between the forest categories (P and G), however we found a significant difference between the sugarcane plantations and the forest fragments (P x C, p =
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0.0073 and G x C, p = 0.015). The SIMPER presented high dissimilarity between the sugarcane plantation and the large and small forest fragments, 98.36% and 97.48% respectively, however, the difference between the fragments was smaller, 76.38%. The species that contributed to the difference
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between the sugarcane plantation and the forest fragments was Marmosa demerarae.
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F10P
F7P
F9G
C1 F6G
C3
F5P F2G
C5
F4P
C4
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F1G
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F8G
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F3P
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Fig. 3– NMDS axis 1 + NMDS axis 2 formed by a cluster analysis, based on the Bray-Curtis coefficient, which separated the habitats by clusters based on assemblage composition, overlapping the forest areas. Subtitle – C, sugarcane plantation areas, F, forest fragments followed by the number corresponding to
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Table 1; G, large fragments and P, small fragments.
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Discussion During the evaluation of the effects of habitat structure on small mammals, the abundance and richness parameters were found to be negatively influenced by environmental quality of the habitat. Land use changes in the natural environments lead to the reduction in biodiversity parameters (Dixon et al., 2009; Fahrig et al., 2011 and Hass et al., 2018). The richness registered in this study was within the expected values for agricultural mosaics in Atlantic Forest enclaves, according to Gheler-Costa et al. (2012). The richness observed in the USJ – 1% of the CEPE area, represents 40% of the total of 25 species of rodents and marsupials registered in the CEPE (Oliveira and Langguth, 2004; Asfora and Mendes Pontes, 2009; Dantas-Torre et al., 2012). According to the percentage reached by the richness estimator, we obtained a great representativeness of species sampled in the region where the landscape is inserted.
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The lowest richness found was in the sugarcane plantation, and it supports Wijesinghe and
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Brooke’s (2005) results, who found a difference in richness between forests and anthropogenic habitats. Although Gheler-Costa et al. (2012) also registered a difference in the richness of small mammals
between the study habitats, in their samples the greatest number of species was found in the sugarcane
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plantation. This inversion of values is due to the higher number of representatives of the order Rodentia in the work of Gheler-Costa et al. (2012) compared to the unexpected greater number of marsupials registered in this study. Despite the increased number of species found in the small fragments in relation
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to the larger ones, there was no significant difference between the forest fragments, which was similar to the results found by Pardini (2004) in the Atlantic Forest. Our data show that the type of habitat interferes
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with richness, with a decrease in the number of species in the sugarcane. However, in the landscape configuration, the difference between fragment sizes does not significantly interfere with richness. It is essential to emphasize the role of small fragments in the management of species, where three more species were found compared to the large fragments, as well as their role in acting as
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functional corridors. Turner and Corllet (1996), pointed out that small fragments such as these are functionally effective in acting as refuges for fauna and flora, allowing for the management of species at
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risk of extinction. However, this role of safeguarding biodiversity may be at its limit, since Estavillo et al. (2013) demonstrated that below 30% of forest cover there is a decline in small mammal richness. The richness registered in our study areas, together with the fact that the USJ is found close to the aforementioned limit, reinforces the necessity of fauna management. This situation can be modified by
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small changes in landscape (such as ecological corridors), due to the proportion of forested area in the USJ (30.17%). In anthropogenic landscapes, such as agricultural mosaics, its components have a greater value for conservation when considered together, compared to the value of each component individually (Pardini, 2004).
Three factors are important in explaining the richness observed in this study. Firstly, in tropical forests some taxa have complex patterns of endemism and grouped distributions. We agree with Laurance and Vasconcelos (2009) who concluded that the absence of species in a given location may represent a natural pattern. Secondly, despite the tendency of the matrix to act as a barrier for more sensitive species,
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it allowed the establishment of species from other biomes. This can be exemplified by the presence of Calomys expulsus in this study, which has a natural distribution in the Cerrado and the Caatinga (Oliveira and Langguth, 2004). Finally, the smaller fragments actually acted as shelter and safe passageways for the fauna. As so, our results agree with Dunn (2004) who suggests that in regenerating forests, some taxa tend to have a greater richness in smaller fragments even if only temporarily. The pattern of abundance in the study area, with significant differences between forest and plantations, was also observed by Gheler-Costa et al. (2012). The lower number of individuals found in the sugarcane plantation, predominantly rodents, was also found by Verdade et al. (2012). Since sugarcane farming is an intensive activity, the environmental patterns in these habitats are distinct from those of the forest, with poorer air, soil and water quality (Stoate et al., 2009), as well as the absence of canopy and strata coverage and decreased food variability. Thus, the influence of habitat type on the
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abundance of small mammals could be altered by the resource availability and the degree of disturbance
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along the categories, which gradually decreased from great forest fragments to small ones, followed by sugarcane plantations.
Regarding the size of forest fragments, abundance was significantly greater in the larger
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fragments when compared to the smaller fragments, which corroborates the findings of Laurance (1994) and Pardini et al. (2005). Notably, in these environments there are ecological characteristics that are
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fundamental in determining the abundance of assemblages and that explain the greater adaptation of these assemblages to larger fragments. We agree with Laurance et al. (1998), who highlight the fact that in small fragments there is a decrease in environmental quality with modifications in the microclimate and
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an increase in tree mortality. Additionally, we agree with Uezu et al. (2005), when they state that larger fragments house more stable populations long-term. Smaller assemblages are more susceptible to stochastic events (Brito, 2009; Laurance and Vasconcelos, 2009), highlighting the importance of communication between fragments of different sizes in such a way that allows for the migration and
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establishment of species in these environments, particularly for species which avoid the matrix. The composition of assemblages was not explained by fragment size, but rather by the types of
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habitat sampled – forest and sugarcane matrix. This result is in agreement with studies developed in the Atlantic Forest on small mammals by Bonvicino et al. (2002), who analysed data from from forests and altered matrices, and by Umetsu and Pardini (2007) and Gheler-Costa et al. (2012), who compared forested and agricultural areas. The species that contributed the most to the difference found in this study
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had a restricted distribution, as well as a greater abundance in the forest (M. demerarae). Species tolerant to the open areas were registered in the sugarcane plantation, agreeing with Benedek and Sirbu (2018) who have suggested that species less tolerant to tree cover are more abundant in agricultural areas. Thus, the abundance of assemblages in the forest and in the sugarcane plantation associated with the presence/absence of the species in the environments was determinant in differentiating the compositions of the assemblages. The ecological causes that explain the results of the abundance and composition of the small mammal assemblages are closely intertwined. The dominance observed in the forest assemblages
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indicates the success of M. demerarae in competing for available resources in this habitat. This species, despite using different forest strata, is essentially arboreal (Vieira and Monteiro-Filho, 2003; Paglia et al., 2012). The greater abundance of this species in larger forest fragments (62.2%) is justified by its dependence on more structured forests, as observed by Castro and Fernandez (2004). The authors emphasised that mammals with a strong dependence on mature forests, decreased in abundance or disappeared in small fragments (Castro and Fernandez, 2004). It is worth noting, that despite D. aurita being considered a habitat specialist (Cáceres et al., 2016), its greater relative abundance found in the smaller study fragments may be a strategy for the maintenance of the species in highly fragmented environments, which increases its adaptive power. In the sugarcane plantation, only two marsupials were registered and M. domestica was the second most abundant mammal. Due to its terrestrial habitat, this species does not suffer from the loss of
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vertical stratification. We found a greater abundance of rodents in the sugarcane plantation, a result which
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has also been found by Verdade et al. (2012) and Santos et al. (2016), who explained this result as a
consequence of the greater availability of food in sugarcane plantations. We found that this availability was due not only to the sugarcane itself, but also to the herb vegetation associated with sugarcane, serving
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as an alternative source of food. The most abundant species in the sugarcane habitat was N. lasiurus, which was also the most abundant species in a study by Gheler-Costa et al. (2012). All the species present in the sugarcane plantation were essentially terrestrial, except for D. albiventris, initially recorded in the
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forest.
The observed distribution of species in the study habitats is a reflection of the adaptation of
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species to their environments, with the sigmodontinae exclusively inhabiting the sugarcane plantation and five of the seven marsupial species being restricted to the forested areas. Marsupial adaptation to the upper strata of their environment makes it impossible to establish certain species in the sugarcane matrix due to the absence of their niche. Of the marsupials found in the sugarcane plantation, D. albiventris was
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found once in this habitat. Its generalist behaviour favours the occupation of agricultural areas due to the greater availability of food with higher energy content and reduced competition. However, the use of the
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sugarcane matrix temporarily annuls its scansorial behaviour due to the absence of upper strata. Gheler-Costa et al. (2012) registered less complex communities of small mammals in landscapes with an agricultural matrix and forest fragment remnants when compared to untouched forests. However, our results demonstrated that forested areas house species with a greater diversity which occupied
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different niches. Even within the agricultural mosaic, the forest fragments presented more complex assemblages compared to the modified matrix. Our results are in accordance with Luza et al. (2016) who recorded simplified assemblages in disturbed sites, like sugarcane plantations. The association of small mammals with their habitats, restricted the majority of the collected marsupials to the forests and the rodents to the sugarcane matrix. However, this does not completely prevent interspecific ecological interactions between these orders of mammals. The exclusivity of the six species found in the forest fragments reinforces the importance of the conservation of these environments, considering the affirmation of Gascon et al. (1999), stating that species that avoid modified matrices tend
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to decrease in number or disappear. In this way, the sugarcane matrix acts by selecting the species with the greatest environmental plasticity and not as an insurmountable barrier. This restricts the distribution of species dependent on forests, increasing the distribution and abundance of more environmentally flexible species, such as exotic ones, to the detriment of the native species. The complexity of the ecological responses of assemblages as a result of anthropogenic modifications in the study environments reiterates the importance of forest fragment conservation, regardless of size. The large fragments are essential for the viability of populations long-term, whereas the smaller fragments safeguard species in anthropogenic scenarios, and act as connections between the fragments. Despite the importance of the conservation of forest corridors in the face of habitat fragmentation, in heavily anthropic areas where there is no possibility of forest restoration, land uses that allow the maintenance of native species in the landscape and / or those whose characteristics are similar
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to the natural environment, are essential for the dynamics of the mammalian populations.
'Declarations of interest: none'
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Funding: This study was supported by CAPES
Acknowledgements: Petribu-Cavalcanti/Grupo Usina São José for permission and Pedro Aguilar Cescon
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for revising the English language of the manuscript.
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Table 1: Locations of rodent and marsupial samples between January and October 2016, in the Usina São José (Igarassu, Pernambuco, Northeaster of Brazil), names of locations; coordinates; area size and
Coordinates (UTM)
Area (ha)
Sample site code
FG
Avião
S 07°49’13.5” W 034°59’14.8”
410.46
G1
FG
Macacos
S 07°46’53.9” W 035°00’30.6”
356.94
G2
FG
Piedade
S 07°50’19.6” W 034°59’46.3”
308.98
G3
FG
Vizinho de Dedo de Deus
S 07°45’27.8” W 035°00’34.1”
322.71
G4
FG
Vizinho do Avião
S 07°44’59.4” W 034°58’51.8”
284.38
FP
Chico Dias
S 07°49’14.96” W 034°59’37.0”
15.5
FP
Paô
S 07°48’36.1” W 034°59’16.3”
FP
Córrego da Carniça
S 07°48’21.9” W 034°59’10.6”
FP
Pezinho
S 07°47’56.3” W 035°01’24.6”
FP
Vizinho de Vespa
C
Cana Pezinho
C
oo
f
Habitat / Location Category
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corresponding sample site codes – FP, small fragments, FG, large fragments, and C, sugarcane plantation.
G5
pr
P1 P2
36
P3
29.8
P4
S 07°44’58.4” W 034°58’51.9”
14
P5
S 07°47'56.1" W 035°01'26.2"
-
C1
Cana Piedade
S 07°50’00.6” W 034°59’44.6”
-
C2
Cana Vizinho de Avião
S 07°47'43.5" W 034°57'42.4"
-
C3
C
Cana Vizinha a S 07°45’46.8” Dedo Deus W 035°00’43.8”
-
C4
C
Cana do Paô
S 07°48’44.6” W 034°59’13.5”
-
C5
Pr
Jo
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C
e-
13.8
19
Table 2: Rodent and marsupial taxa, abundance and richness for the studied categories at Usina São José, Igarassu – PE, Northeastern Brazil. Habitat Use according to Paglia et. al (2012). Taxa
Habitat Use
Large Fragments Small Fragments Sugarcane G P C
DIDELPHIMORPHIA Didelphidae Didelphis aurita (Wied-Neuwied, 1826)
Sc
Didelphis albiventris Lund, 1840
Sc
Marmosa murina (Linnaeus, 1758)
Sc
Marmosa (Micoreus) demerarae Thomas, 1905
Ar
Metachirus nudicaudatus (É. Geoffroy, 1803)
Te
Monodelphis americana (Muller, 1776)
Te
Monodelphis domestica (Wagner, 1842)
Te
3
1
3
0
50
11
0
1 3
Sigmodontinae
Pr
Te
1
e-
0
1
0
Te
0 0
pr
0
f
5
Echimydae
6
2
0
0
9
0
2
al
0
Te
ur n
Necromys lasiurus (Lund, 1838) Calomys expulsus (Lund, 1841)
0
oo
14
RODENTIA Thricomys laurentius Thomas, 1904
7 10
0
82
29
18
Richness
5
8
4
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Abundance
20