Mammalia 2017; aop
Matheus R.J. Corrêa*, Yuri M. Bellagamba, Adriele P. de Magalhães, Joice P.V. Martins, Antônio J. do R. Cruz, Alessandra R. Kozovitz, Maria C.T.B. Messias and Cristiano S. de Azevedo*
Microhabitat structure and food availability modelling a small mammal assemblage in restored riparian forest remnants https://doi.org/10.1515/mammalia-2017-0026 Received March 7, 2017; accepted October 4, 2017
Abstract: Small mammal populations respond to environmental changes in secondary riparian forest remnants in different ways, depending on the influences of biotic and abiotic variables. The present study evaluated how habitat/microhabitat structure and food availability influence small mammal assemblages in restored riparian forest remnants. Pitfall traps disposed in three linear transects were used to collect small mammals during 9 months of field work. General linear models were built to test the hypothesis that microhabitat structure (litter biomass and type – leaves and branches) and food availability (richness of zoochoric tree species and arthropods) influence species richness and abundance of small mammals. Three hundred and eighty-two individuals belonging to 14 species were captured. Biomass and type of litter (leaves or branches) provided greater structural to microhabitats, allowing the coexistence of morphologically similar species. Besides, food availability influenced foraging strategies of marsupials, forcing them to use the forest floor when zoochoric plants were rare. Thus, litter structure and food availability, allowing spatial segregation of the small mammal species using the forest fragments. We concluded that the maintenance of small mammals and their ecosystem services in restored riparian forests are
*Corresponding authors: Matheus R.J. Corrêa and Cristiano S. de Azevedo, Programa de Pós-graduação em Ecologia de Biomas Tropicais, Biodiversidade, Evolução e Meio Ambiente, Instituto de Ciências Exatas e Biológicas, Universidade Federal de Ouro Preto, Campus Morro do Cruzeiro, CEP: 35400.000, Ouro Preto, Minas Gerais, Brazil, e-mail:
[email protected] (M.R.J. Corrêa);
[email protected] (C.S. de Azevedo) Yuri M. Bellagamba, Adriele P. de Magalhães, Joice P.V. Martins, Antônio J. do R. Cruz, Alessandra R. Kozovitz and Maria C.T.B. Messias: Programa de Pós-graduação em Ecologia de Biomas Tropicais, Biodiversidade, Evolução e Meio Ambiente, Instituto de Ciências Exatas e Biológicas, Universidade Federal de Ouro Preto, Campus Morro do Cruzeiro, CEP: 35400.000, Ouro Preto, Minas Gerais, Brazil
dependent on habitat structure and food availability, thus, litter and zoochoric plants should be conserved in riparian forest fragments, especially those reforested. Keywords: conservation; fragmentation; litter; marsupials; rodent.
Introduction The Cerrado and the Atlantic Forest are the most biodiverse and threatened Brazilian biomes. The large-scale deforestation, as well as the high incidence of endemic and threatened species has placed these biomes among the world’s “hotspots” (Mittermeier et al. 2005). Riparian forests of the Cerrado share faunistic and floristic elements with the Atlantic Forest (Redford and Fonseca 1986, Mares and Ernest 1995, Johnson et al. 1999, Marinho-Filho and Gastal 2000, Costa 2003, Oliveira-Filho and Ratter 2009). Many endemic mammal species of the A tlantic Forest have resident populations in riparian forests (Costa 2003, Cáceres et al. 2008, Naxara 2008) and use these forests as corridors between remnant fragments of forested habitats (Naxara 2008). Besides, riparian forests are worldwide important corridors for animal dispersion, allowing gene flow and preventing local extinctions (Lees and Peres 2007, Smiley and Cooper 2013). In spite of the importance of the conservation of riparian forests for animals, these habitats are being deforested and suffering from anthropogenic threats in Brazil, especially in areas of Cerrado and Atlantic forests, historically explored by humans (Klink and Machado 2005, Ribeiro et al. 2009, Galetti et al. 2010). Most of the forest into the Atlantic Forest and the Cerrado domains are disturbed and found in secondary successional stages (Brown and Lugo 1990, Wright 2010). Their forest remnants present substantial modifications in the biotic and abiotic structures, resulting in loss of ecological interactions (Tabarelli and Peres 2002, Pardini et al. 2009, Pinotti et al. 2012). Moreover, anthropogenic modifications in the biotic structure, as habitat fragmentation, are reducing small mammal populations both in Brought to you by | Universidade Federal de Ouro Preto UFOP Authenticated |
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2 M.R.J. Corrêa et al.: Small mammals in restored riparian forests the Cerrado and in the Atlantic Forest (Malcolm 1995, Williams et al. 2002, Figueiredo and Fernandez 2004, Pardini et al. 2005, Puttker et al. 2008, Cáceres et al. 2010). Forest habitat description (habitat defined as the area where the animal lives; Tagliapietra and Sigovini 2010), like forest horizontal and vertical structure modelling animal diversity, has been widely acknowledged. However, the importance of the forest microhabitat in the ecosystem functions, especially as a predictor of mammal biodiversity, is still under investigation. Microhabitat can be defined as a discrete fraction of the habitat, with specific niche requirements, directly or indirectly influencing the distribution of species (Morris 1987). Forest litter is an example of microhabitat, and litter depth, humidity and food availability are examples of characteristics of the microhabitat that can influence small mammals. Changes in the microhabitat also influence survivorship of small mammals in riparian forest fragments (Pardini et al. 2005, Lambert et al. 2006, Naxara et al. 2009). Many studies have demonstrated that habitat microstructures influence directly or indirectly the abundance and distribution of small mammals, both in temperate and tropical regions (Dueser and Shugart 1978, Brannon 2000, 2002, Naxara et al. 2009, Pinotti 2010). Small mammals can be defined as non-flying mammal species weighing less than 1 kg (Barnett and Dutton 1995). Vertical stratification, different activity period and the exploration of different food items allow the coexistence of ground-dwelling, arboreal and scansorial small mammal species (Vieira and Monteiro-Filho 2003, Oliveira-Santos et al. 2008, Melo et al. 2013). The Neotropical small mammals occupy different strata of the habitat, such as through arboreal habitat (animals that spend most of their lives above ground), scansorial (animals that spend part of their lives climbing on plants) and terrestrial (Eisenberg and Redford 1999). This spatial segregation diminishes niche overlap, avoiding competition among the species (Schoener 1974, Melo et al. 2013, Zhong et al. 2016). However, in restored riparian forests, depending on their characteristics (tridimensional structure, food availability, size, plant diversity, etc.), this niche overlap could be increased (Vieira and Paise 2011), leading the animals to expand their home ranges to search for food (Acevedo et al. 2007). It remains to be tested whether species coexistence is stabilised/equalised by variation in litter structure and biomass. Litter structure and biomass, such as the biomass of leaves and branches, are microhabitat variables that ground-dwelling small mammals use as shelter against predators, as locomotion structures, as hunting areas (to capture invertebrates) and as water resources
(Drickamer and Stuart 1984, Harmon et al. 1986, Naxara et al. 2009, Pinotti 2010). Thus, variation in litter structure and biomass would control the abundance and richness of these species (Drickamer and Stuart 1984, Harmon et al. 1986, McCay 2000, Brannon 2002, Bernard 2004, Naxara et al. 2009, Pinotti 2010). Food availability is also an important factor influencing forest small mammal communities. Invertebrates and fruits are the most abundant items in the diets of tropical small mammals (Vieira and Pizo 2003, Vieira et al. 2006, Leiner and Silva 2007, Lessa and Geise 2010, Camargo et al. 2011). Alterations in these resources entail direct changes in the abundance and distribution of the mammal species (Malcolm 1995, 1997, Bergallo and Magnusson 1999, Naxara et al. 2009). Fruit biomass availability is influenced by the richness of zoochoric species (Kuhlmann and Ribeiro 2016, Moore et al. 2016), and arthropod biomass is influenced by microhabitat structure and by the amount of habitat (Gardner et al. 1995, Travassos-de-Britto and Rocha 2013). Thus, ecological restoration projects always plan the use of this functional group in reforestation. However, in newly restored riparian forests, food items can be very rare and/or scatter, forcing the small mammals to expand foraging areas, which can end up with increased competition and niche overlapping (arboreal species foraging on the ground, etc.) (Lessa and Paula 2014, Galetti et al. 2016). In general, anthropogenic alterations in food availability can lead to bottom up effects (Pace et al. 1999), i.e. an increase in food availability can favor recruitment and populational growth of some small mammal species (Malcolm 1995, 1997, Pardini et al. 2005). In turn, these species can promote alterations in rates of arthropod predation (Malcolm 1997), seed predation and seed dispersal (Vieira et al. 2006, Leiner and Silva 2007, Camargo et al. 2011), directly influencing the regeneration and succession in these forest fragments (Terborgh et al. 2001). How parameters of habitat/microhabitat structure influence small mammal populations in restored riparian forest remnants, however, remains rarely evaluated (Wike et al. 2000, Smiley and Cooper 2013). The present study aimed to evaluate the influences of environmental variables over small mammal populations in secondary fragments of restored riparian forests around the Grande River Reservoir, located at the border of Minas Gerais and São Paulo States, Southeastern Brazil. We tested the hypothesis that small mammal abundance and richness are influenced by the microhabitat structure and food availability. We predicted that there are increases in ground-dwelling small mammal abundance and richness with an increase of the biomass of litter (leaves and Brought to you by | Universidade Federal de Ouro Preto UFOP Authenticated |
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M.R.J. Corrêa et al.: Small mammals in restored riparian forests 3
branches) due to an increase in the habitat complexity. We also predicted that an increase in food availability (abundance of invertebrates and richness of zoochoric plants) will lead to increases in the abundance and richness of ground-dwelling small mammal species. We evaluated whether the locomotion habitat (arboreal, scansorial, terrestrial) and diet (frugivorous or insectivorous), have been correlated to marsupial and rodent abundances.
Materials and methods Study site Five riparian forest fragments of the Grande River were studied. Four of them were originated from restoration efforts (with 10–20 years after planting) and one fragment
was formed by natural vegetation regrowth after disturbance provoked by the building of a hydroelectric dam (for more details see Table 1). The fragments were located at Conceição das Alagoas, Água Comprida, Igarapava and Miguelópolis Municipalities, in the border of the states of Minas Gerais and São Paulo (Figure 1). The vegetation of the studied areas is classified as semideciduous seasonal forest (Filardi et al. 2007). The mean temperature varied between 22°C and 24°C yearly, and the region presents an annual pluviometric mean of 1550 mm, with two distinct seasons: a dry season from April to September and a rainy season from October to March, being climate classified as Cwa (Humid subtropical climate) in the Köppen System (Álvares et al. 2013). The matrix surrounding the fragments was very diverse, but mostly consisted of sugar cane besides other crops like pasture, rubber and soybean, in different proportions.
Table 1: Location (UTM) and characteristics of the five riparian forest fragments studied. Fragment
Vegetation
UTM
Location
Municipality
1 2 3 4 5
Native Reforestation Reforestation Reforestation Reforestation
22 k 22 k 22 k 23 k 23 k
791531/7783262 798082/7775015 800294/7768027 205429/7786874 208838/7787209
Conceição das Alagoas/MG Água Comprida/MG Miguelópolis/SP Igarapava/SP Igarapava/SP
Age (years)
Area (km2)
30 10 20 20 10
0.232 0.08 0.129 0.18 0.12
MG, Minas Gerais State; SP, São Paulo State.
Figure 1: Border between Minas Gerais and São Paulo states, showing the five riparian forest fragments studied, being fragments 1 formed by natural vegetation regrowth and fragments 2 to 5 from restoration efforts.
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4 M.R.J. Corrêa et al.: Small mammals in restored riparian forests
Small mammal sampling
Litter structure and botanical variables
Pitfall traps were used to collect small mammals (Barros et al. 2015, Rocha et al. 2015). Thirty 60-l buckets were disposed in three linear transects of 50 m; 10 buckets, 5 m equidistant, were disposed in each transect. Pitfall traps stood open for four nights per month in each area, and they were checked daily to remove any captured animals. Nine months of field work were carried out (March 2013 to January 2014), 4 months during the dry season and 5 months during the rainy season (no sampling was carried out in August and September 2013 due to logistical difficulties). Captured individuals received earrings (National Band and Tag Co., Newport, KY, USA) and were released at the same location of capture. Capture and individual manipulation were carried out according to the guidelines of the Committee of Animal Care and Use of the American Society of Mammalogists (Sikes and Gannon 2011). Specimens were collected, taxidermised and deposited in the mastozoology collection of the Laboratory of Vertebrate Zoology of the Federal University of Ouro Preto (LZV-UFOP; 287 individuals). Taxonomic classifications followed Wilson and Reeder (2005), except for the Oryzomyni tribe, which followed Weksler et al. (2006), and for the marsupials, which followed Rossi et al. (2012). Paglia et al. (2012) was used to classify marsupials and rodents according to their locomotor and food habit (terrestrial, arboreal or scansorial, and insectivorous or frugivorous). The study was approved by the Brazilian System of Authorization and Information on Biodiversity (SISBIO license n° 37067-1) and by the Animal Ethics Committee of the Federal University of Ouro Preto (#2012/55).
Botanical sampling was approved by the Brazilian System of Authorization and Information on Biodiversity (SISBIO license n° 29311-1). Botanical data were collected during the same period of time of the mammal survey. The species composition and structure of the vegetation were carried out with phytosociological studies, using the plot method (Mueller-Dombois and Ellenberg 1974). Twelve plots (10 × 10 m) in each fragment were systematically arranged along the three 50 m transects where pitfall traps were installed (six plots 10 m-spaced, along each side of the transects). All individual trees with circumference at breast weight (CBH) equal to or greater than 10 cm were sampled, allowing the identification and evaluation of abundance and richness of plant species in the different areas. Specimens were collected, identified, herborised and deposited in the Professor José Badini herbarium (OUPR) of the Federal University of Ouro Preto. Lorenzi (2002a,b) and Kuhlmann (2012) were used to classify plant species according to their dispersal syndrome; only the abundance and richness of zoochoric species data were used in the analyses. To quantify litter, 20 litter traps (50 × 50 cm, 2 mm mesh) per area were installed in parallel with the small mammal pitfall traps. Litter production was monthly collected during the study period. In the laboratory, litter was separated into leaves and branches fractions and the material were oven-dried for 72 h and weighed. The dry biomass of leaves and branches litter was used in the analyses.
Invertebrate sampling Pitfall traps were also used to sample terrestrial invertebrates (Holway 2005). Ten 400 ml plastic cups, filled with a mixture of alcohol 70% and detergent, were disposed laterally to the small mammal pitfall trap transects. As done for small mammals sampling, pitfall traps stood open for four nights per month in each area. Nine months of field work were carried out (March 2013 to January 2014), 4 months during the dry season and 5 months during the rainy season. Samples were analysed in the laboratory, and the abundance of arthropod orders was determined. Invertebrate sampling was approved by the Brazilian System of Authorization and Information on Biodiversity (SISBIO license n° 37067-1).
Data analyses Sampling effort was evaluated by the construction of the observed and expected richness accumulation curves (jackknife 1) using the software EstimateS Win 8.20 (Colwell 2009). Sampling success was evaluated dividing the number of individual registers by the trapping/night effort and multiplying by 100 (Bezerra et al. 2009). Comparisons between the abundance and composition of the small mammal assemblages of the five areas were run using Contrast Analysis (multicomp package; Hothorn et al. 2008) and Permanova (Vegan package; Dixon 2003) (Anderson 2006, Anderson et al. 2006, Novais et al. 2015), using the software R (R Development Core Team 2012). The Shannon-Wiener diversity index was used to estimate the diversity of the small mammal assemblages. To this, it were estimated the relative abundances of each species based on the Brought to you by | Universidade Federal de Ouro Preto UFOP Authenticated |
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M.R.J. Corrêa et al.: Small mammals in restored riparian forests 5
Results
total number of individuals sampled (Magurran 2004). Species richness and the presence of rare species on the studied sites exert great influence on this index (Hurlbert 1971). Pielou’s J index was used as a measure of evenness, calculated based on the degree of equality in the species’ abundances found for each taxon recorded in each studied area. This index is mainly influenced by the species’ dominance, which is determined by the high abundance of one species over the other taxa in the assemblage (Magurran 2004). Pearson correlations were used to evaluate and exclude multicollinearity among the variables (Mac Nally 2002). In addition, to insert the order of the variables in the general linear model (GLM), a principal component analysis (PCA) was run to evaluate the variables distribution in the multivariate space of the PCA. Both analyses were run using the Vegan package (Dixon 2003). GLMs, with Poisson and quasiPoisson errors, were built to evaluate if the independent microhabitat variables (litter biomass – leaves and branches; and food availability – abundance of invertebrates and richness of zoochoric plants) influenced the small mammal assemblages (species richness and abundance of small mammals, rodents and marsupials as dependent variables) (Crawley 2002, Novais et al. 2015). GLMs were run using R Studio software (R Development Core Team 2012). A significance level of 5% was set for all statistical tests employed in this study.
Community structure The present study employed a sampling effort of 5400 trapping/night, capturing 382 individuals of 14 species, with seven recaptures, eight species of which belonged to the order Rodentia and six species to the order Didelphimorphia, and a sampling success of 7.07%. Due to taxonomic difficulties, some cryptic species were identified as morphotypes, to better match the data in the analysis (Table 2). Oligoryzomys spp. Bangs, 1900. was the most abundant species (64%), followed by Calomys gr. expulsus Lund, 1841 (11.78%) and Gracilinanus agilis Burmeister, 1854 (8.37%), the most abundant marsupial species (Table 2). Area 4 presented the greatest abundance of rodents (117 individuals; Table 2; F = 34.5; p = 0.01) and area 5 presented the greatest abundance of marsupials (19 individuals; Table 2; F = 4.87; p = 0.02). The sampling areas, in general, presented similar values for the Shannon-Wiener and the Pielou’s J indexes. Only the area 5 presented the value of the Pielou’s J index more accentuated when compared to the others. The small mammal assemblage, considering all areas together, was low in diversity and equitability (Table 3). Richness curves estimated 13.68 species for area 1, 10.92 species for area 2 and 3, 11.92 species for area 4, and 5.55 species for area 5 (Figure 2). No statistical differences
Table 2: Small mammals’ species, habitat of locomotion and abundance, captured by pitfall traps in five areas of riparian forests of the Grande River, border of Minas Gerais and São Paulo States, Southeastern Brazil. Species
Diet
Locomotion
Number of individuals 1
2
3
4
5
All areas together
Order Didelphimorphia Caluromys lanatus Cryptonanus sp. Didephis albiventris Gracilinanus agilis Gracilinanus microtarsus Monodelphis kunsi
Fr/On In/On Fr/On In/On In/On In/On
Arboreal Arboreal Scansorial Arboreal Arboreal Terrestrial
0 0 1 1 0 2
0 0 1 3 1 4
0 0 3 3 1 5
1 4 0 8 0 0
0 0 2 17 0 0
1 4 7 32 2 11
Order Rodentia Calomys expulsus Calomys tener Necromys lasiurus Oecomys sp1 Oecomys sp2 Oecomys sp3 Oligoryzomys sp. Rhipidomys sp.
Fr/Gr Fr/Gr Fr/On Fr/Se Fr/Se Fr/Se Fr/Gr Fr/Se
Terrestrial Terrestrial Terrestrial Arboreal Arboreal Arboreal Scansorial Arboreal
14 4 2 1 1 0 48 0
4 0 1 0 0 0 27 3
2 1 1 1 0 0 68 0
11 2 10 0 1 1 92 0
14 0 6 0 0 0 10 0
45 7 20 2 2 1 245 3
Total
74
44
85
130
49
382
Fr/Gr, frugivore/granivore; Fr/On, frugivore/omnivore; Fr/Se, frugivore/seed predator; In/On, insectivore/omnivore (Paglia et al. 2012).
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6 M.R.J. Corrêa et al.: Small mammals in restored riparian forests Table 3: Values of the Shannon-Wiener and the Pielou’s J index for the abundance and richness of small mammals represented in five areas of riparian forests of the Grande River, border of Minas Gerais and São Paulo States, Southeastern Brazil. Areas
Species richness
Species richness Total individuals Shannon-Wiener Pielou’s J
18 16 14 12 10 8 6 4 2 0
1
2
3
4
5
All areas together
9 74 1.181 0.5376
8 44 1.36 0.654
9 85 0.8785 0.3998
9 130 1.106 0.5035
5 49 1.437 0.893
14 382 1.347 0.510
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35
Figure 5A, B, respectively), but not small mammal richness. Biomass of leaves and branches also positively influenced the abundance of arboreal and scansorial species (Table 5; Figure 5C). The richness of zoochoric plants was negatively associated with the abundance of marsupials (Table 5; Figure 5C). There was no influence of the microhabitat variables and food availability on the small mammal richness, rodent abundance and terrestrial species.
Sampling effort Figure 2: Estimated species richness of small mammals for the five riparian forest areas of the Grande River. Area 1: ○; area 2: □; area 3: ◊; area 4: x; and area 5: ∆.
were found among the five sampled areas in the composition of the small mammal assemblages [permutational multivariate analysis of variance (PERMANOVA: R2 = 0.40, p = 0.06)].
Small mammals, microhabitats structure and food availability Among the independent variables, five were significantly correlated (Table 4). Thus, four variables not correlated were chosen for the construction of the PCA. Regarding the dependent variables, it was observed that the rodent abundances were significantly correlated with the scansorial habit and the frugivore diet, while the marsupial abundances were significantly correlated to the arboreal habit and insectivorous diet (Table 4). The first two axes of PCA explained 82% of data variation related the independent variables to the richness of small mammals (Figure 3). Similarly, for marsupial and rodent abundances, 85% of data variation was explained by the two principal component axes (Figure 4). Biomass of branches and leaves presented the highest values of the eigenvectors in the first and second components, respectively, for the richness and small mammal abundances (marsupial and rodent). Biomass of leaves and branches in litter positively influenced rodent and marsupial abundances (Table 5;
Discussion Community structure The diversity and evenness indexes found in the present study were considered low (H′ = 1.37; J′ = 0.51, respectively) when compared to other areas surveyed in the Cerrado biome (Carmignotto and Aires 2011, Carmignotto et al. 2014). However, our results are in accordance with others run in restored riparian forest in the Cerrado, where nonvolant small mammal assemblages were characterised by a dominant species (e.g. Oligoryzomys sp.), some species with intermediate abundance (e.g. Calomys expulsus; Gracilinanus agilis) and many rare species (e.g. Caluromys lanatus Oifers, 1818; Oecomys spp. Thomas, 1906) (Cáceres et al. 2010, Bonvicino et al. 2014). The estimated curve of species richness for the small mammals did not reach the asymptote, presenting subtle variations among the studied restored riparian forest fragments. This pattern is common in tropical regions, where biodiversity is very high and habitats very heterogeneous (Voss and Emmons 1996, Magurran et al. 2010); the same pattern was observed in other studies in the Brazilian Cerrado (Bonvicino et al. 2014, Carmignotto et al. 2014). Area 5 presented lower species richness when compared to all other areas, and the curve of estimated richness quickly reached the asymptote, with few samples. Probably, the human presence, added to its short time of regeneration (10 years), was responsible for this result. Time of regeneration is an important variable to the maintenance of small mammal species richness in forest fragments Brought to you by | Universidade Federal de Ouro Preto UFOP Authenticated |
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−0.142 0.820 0.962 0.009a 0.081 0.897 0.333 0.583 0.999 0.000a −0.126 0.840
– – −0.220 0.722 0.855 0.065 0.191 0.758 −0.174 0.779 0.988 0.002a
Abun. of marsupials
– – −0.403 0.501 −0.898 0.039a −0.819 0.090 −0.947 0.015a −0.893 0.041a
Biomass of branches
– – – – −0.101 0.871 0.068 0.913 0.972 0.006a −0.234 0.705
Abun. of scansorial
– – – – 0.631 0.253 0.608 0.276 0.219 0.723 0.274 0.655
Abun. of invert.
Number in the first row corresponds to the number of variables in the first column. Spearman correlation was performed (ap
