Use of microhabitats affects butterfly assemblages in a rural landscapeAbstract
Landscapes composed of small rural properties may support highly heterogeneous habitat, because they often cover distinct types of land uses adjacent to surrounding forest fragments. Many butterfly species may benefit from this kind of landscape, as very distinct microhabitats can be found in a very restricted spatial scale. To better understand how different microhabitats are related to fragmentation in rural landscapes the present study collected the butterfly fauna in 18 sampling point sites, representing distinct types of forest edges and forest interiors. Although closely located, these sites showed no spatial autocorrelation. Instead, a major distinction in species richness and composition was found among forest interior and edge habitats while no significant difference was found in species composition among distinct edge types. Therefore, the high segregation of butterfly assemblages found in a very restricted geographic scale suggests the presence of two different groups of butterflies that respond independently to forest fragmentation, the forest interior assemblages and forest edge assemblages. This distinction of butterfly assemblages related to forest interior and forest edges were already reported, but our results highlights that these differences are found mostly due to species turnover between those habitats. In other words, both microhabitat types present a high number of specialized species compared to a smaller fraction of generalist species that may occurs in both microhabitats. In the case of Atlantic Forest, the species of special conservation concern are those true specialized in forest interior habitats and not those specialized in forest edges, thus the present study corroborates the importance of sampling different microhabitats when studying fragmentation processes, both inside and outside of fragments. Although forest edges may present different kinds of habitat types, species present along border tend to be as heterogeneous as species present in different locations inside the forest. This information should be considered in sampling designs of biodiversity essays that focus on a more consistent representation of local diversity.
Key-Words.
Atlantic Rainforest; Landscape fragmentation; Host plants; Species list
INTRODUCTION
The increase in land exploitation for agricultural use have been identified as one of the main causes of habitat fragmentation (Foley, 2005; Foley et al., 2011). This phenomena increases the isolation and the number of small habitat patches, as well as decreases the original area size of natural habitats (Fahrig, 2003), thus affecting the organisms diversity and distribution (Prugh et al., 2008; Foley et al., 2011; Gibson et al., 2013; Ibáñez et al., 2014; Haddad et al., 2015). All these effects however, are dependent of how different landscape variables change across geographical scales (Brown Jr. & Hutchings, 1997; Driscoll et al., 2013; Prugh et al., 2008; Verbeylen et al., 2003).
Studies using butterflies as models have demonstrated that local habitat fragmentation can affect their abundance, richness, composition, and diversity (Brown Jr. & Hutchings, 1997; Bobo et al., 2006; Uehara-Prado et al., 2007; Ribeiro et al., 2008; Uehara-Prado et al., 2009; Bonebrake et al., 2010; Collier et al., 2010; Ribeiro et al., 2012; Robinson et al., 2014; Filgueiras et al., 2016). Most importantly, local butterfly distribution is closely associated with habitat conditions as impacted by habitat fragmentation, such as fragment interior vs. fragment edges (Ribeiro et al., 2012; Brito et al., 2014; Filgueiras et al., 2016). This occurs because species that feed as adults on fruits, decomposing matter or bird excrement, find these resources mainly inside the forest, while nectarivorous species find most of the food resources in the canopy, on the edges or in open areas (Brown Jr. & Hutchings, 1997; Devries & Walla, 2001; Hill et al., 2001; Brown Jr. & Freitas, 2002). As distinct types of matrices surrounding fragments may influence the availability of food resources to butterflies, more complex landscapes may offer greater resource diversity (Tews et al., 2004). Therefore, it is expected that rural landscapes under predominance of small farms can harbour more rich and complex assemblages when compared to the extensive monocultural and urban landscapes (Fahrig et al., 2015; Iserhard et al., 2018). This is because small rural properties tend to have different kinds of land occupations, promoting peculiar characteristics, which enable population maintenance and species interaction (Fahrig et al., 2011, 2015).
In addition, the transition area between the fragment and the surrounding matrix may provide differentiated food resources for some groups of insects, relative to those found within the fragment and in the matrix (Landis et al., 2000; Poggio et al., 2010). These areas, the fragment edges, usually have pioneering plant species (Rigueira et al., 2012) and unique micro-climates (Lawson et al., 2014) that form peculiar microhabitats, attracting not only nectarivores, but also predators and other herbivorous insects (Didham et al., 1996; Jokimäki et al., 1998; Albrecht et al., 2010). Fragments surrounded by matrices composed of different occupations (e.g., abandoned areas, crop lands, or roads) present these differentiated transition areas, which form microhabitats at different levels of complexity (e.g., different types of resources). Several butterfly species, for example, are recognized for inhabiting these environments, from where they extract food, both at the larval and adult stages (Brown Jr. & Hutchings, 1997; Brown Jr. & Freitas, 2002).
This study aimed to verify whether the butterfly species richness and composition in a rural fragmented landscapes is influenced by these kinds of microhabitat, thus testing the following hypotheses: (1) Despite of their close proximity, the butterfly assemblages have distinct species richness and composition in different microhabitats present in a fragmented landscape; (2) forest edges and interior have distinct butterfly richness and composition, because butterfly species usually prefer for a particular microhabitat type and (3) different edges types presents distinct butterfly richness and composition.
MATERIALS AND METHODS
Study site
The study was conducted in the municipality of Joaçaba (27°10’41.0”S, 51°30’17.0”W), in the western region of Santa Catarina State, southern Brazil (Fig. 1a). This region is broadly characterized by its rural landscape, with small urban areas (Maté et al., 2015). Small farms predominate in the rural landscape, some of them raising livestock such as cattle, pigs, and poultry, while the others grow corn, beans, rice, tobacco, soy, apple, and oranges (Begnini & Almeida, 2016). The forest fragments are relicts from a transition area (ecotone) between the Araucaria forest and Deciduous forest (Vibrans et al., 2012). The climate is mesothermal humid with a hot summer (according to Köppen-Geiger climatic classification), the average annual temperature is 18°C, annual rainfall of about 2,000 mm, relative annual humidity average is 76% (Alvares et al., 2013), and an altitude of range 700-830 m (Google Earth, 2016).
Location of the study area in the Joaçaba Municipality, Santa Catarina State, Brazil. (a) Fragments sampled; (b-c) Distribution of collection points of A, B and C fragments.
Sampling
Butterfly assemblages were measured in 18 sample sites representing four microhabitat types: forest interiors (n = 6); road edges: edge of the fragment closer to the road (n = 4); farmland edges: crops of soybean and corn and cattle ranching (n = 4); and abandoned edges: early-regrowth vegetation areas (n = 4) (Fig. 2). The focus of the present study was to measure distribution of these butterfly assemblages in a very fine geographical scale. Therefore, these 18 sample sites were choosen in three fragments, being some of them more closely located to each other than to others (Fig. 1b-d, Appendix I). Sample sites in the same fragment were distant from each other by a minimum of 50 m meters distance when representing distinct microhabitats, or at least 100 m distance when representing the same microhabitat. Inside the forest, butteflies were captured in a radius up to 10 m, while in forest edges the butterflies were sampled in a transect up to 30 m.
Characterization of the sampled microhabitats in a rural landscape in Southern Brazil. (a, b) forest interior; (c, d) abandoned edge; (e, f) farmland edge; (g, h) road edge.
Sampling was conducted with an entomological net between 08:30 AM and 04:00 PM between January 2016 and March 2017, except in April, June, July, and August, totaling 15 replicates for each sample site. Butterfly sampling was performed at each site for 01:15 hours, following a rotation, resulting a total of 337.5 h/net per site. Therefore, all sites were equally sampled during different times of the day in the same period of the year. Only the butterfly captured and euthanized were considered in the samples. The specimens were identified based on photographs of type series available in Warren et al. (2013) and/or confirmed by specialists. Voucher specimens are deposited in the “Coleção Entomológica Padre Jesus Santiago Moure (DZUP)”.
Statistical analyses
Considering that butterflies can easily move among the sample sites and use more closely located food resources, the samples in this study are potentially subject to spatial autocorrelation. To determine if this was the case, a Mantel test was employed using a Euclidean distance matrix to represent the geographic distances between samples and a similarity matrix based on Bray-Curtis index to represent species composition.
Later, we measured the richness and composition of butterfly assemblages at each sample site. The butterfly richness was estimated using the interpolation and extrapolation methodology proposed by Chao & Jost (2012), available in the iNEXT package (Hsieh et al., 2016). This method is particularly efficient to estimates the differences in species richness estimated from communities with distinct structure (e.g., abundances distribution). Non-metric multidimentional scaling (NMDS) based on the Bray-Curtis similarity index was used to access assemblage composition at different microhabitats. This method generates a scatter plot in which closely localized samples (e.g., clustered) exhibit similar fauna composition. Thus, distances between sample sites can be used as surrogates of composition dissimilarity (Melo & Hepp, 2008). A PERMANOVA test (n = 999 permutations) was performed to test the significance of microhabitat type in shaping the butterfly species composition. The PERMANOVA was performed for two distinct datasets in our study, since the fragment interior showed a very distinct species composition when compared to all other microhabitat types. Therefore, after testing the whole dataset, a subsequent analysis was performed after removing the forest interior samples.
Additionally, we partitioned the Bray-Curtis coefficient into two measurements to test if any of the microhabitat types are distinct in terms of species turnover (βturn-diversity) and nestedness (βnest-diversity) (Baselga, 2013). These results were used to infer whether the differences in species compostion are due to the segregation of different species at different microhabitats (turnover) or because one microhabitat have only a smaller amount of the same species as the other (nestedness). Therefore, if all microhabitats have a large amout of specialists butterflies a higher βturn-diversity is expected. On the contrary, when most of the species in a microhabitat are generalists (e.g., found across other microhabitats) a higher βnest-diversity is expected. Also to complement this goal, we employed the INDVAL test to verify how many butterfly species present close ecological affinities with any microhabitat type. The INDVAL yields a maximum value when all specimens of a given species are recorded in only one type of habitat and in all samples representing this habitat, despite other species abundances (Dufrene & Legendre, 1997). Since all forest edges revealed no significant changes in the species composition, we only scored microhabitats as forest edges or forest interior. In this test, we considered only species with ≥ 10 individuals, thus totalling 190 species tested. The species that presented significant value were compared with the literature’s observations regarding adult habits and larvae host plants. All analyses were performed in the R environment (R Core Team, 2015) using the package vegan (Oksanen et al., 2017), betapart (Baselga, 2013) and labdsv (Roberts, 2016).
RESULTS
A total of 7,941 butterflies belonging to 431 species were recorded. Twenty-nine species were later recorded during occasional collects totalling 460 species; these species were attached to the species list, but not accounted in the statistical analyses (Appendix II). The Mantel test showed no correlation between species composition and the geographical proximity of sample sites (R = 0.07, p > 0.05), indicating that sample sites are not spatial autocorrelated.
Comparisons among butterfly richness revealed that different microhabitat types do play a role on butterfly species richness patterns (Fig. 3). Assemblages are richer in forest edges than the forest interiors, with the abandoned edges being the richest, followed by the road edge and the farmland edge (Fig. 4, Appendix III). Also a major distinction in species composition is found among forest interior and edges (R² = 0.36476, p < 0.001, Fig. 5a), but in this case the different types of edges revealed no significant differences between each other, even when the samples from the forest interior were removed from the analyses (R² = 0.14894, p = 0.909, Fig. 5b). In both types of microhabitats, beta-diversity is mostly represented by species turnover (Forest interior: βturn = 0.5; Forest edges: βturn = 0.56; p = 0.58) instead of nestedness (Forest interior: βnest = 0.03; Forest edges: βnest = 0.04; p = 0.67), showing that the differences between habitat types is mostly represented by specialists species instead of generalists species. By comparing microhabitat types, the fragment edges show a much larger number of indicator species (n = 68), than the forest interior (n = 20) (Appendix IV).
Results of integrated coverage-based rarefaction-extrapolation (Chao & Jost, 2012) of butterfly richness between microhabitat types in a rural landscape in Southern Brazil (confidence interval = 95%). Continuous lines (rarefaction), dotted lines (extrapolation).
Results of integrated coverage-based rarefaction-extrapolation (Chao & Jost, 2012) of butterfly richness between 18 sampled points in a rural landscape in Southern Brazil (confidence interval = 95%). Continuous lines (rarefaction), dotted lines (extrapolation).
Non-metric multidimensional scaling (NMDS), plots representing butterfly assemblages composition measured in distinct types of microhabitats (abandoned edge, road edge, farmland edge and forest interior) in a rural landscape in Southern Brazil. a) Including forest interior sampled sites (Stress = 0.11); b) Excluding forest interior sampled sites (Stress = 0.14). Forest interior butterfly communities are distinct from all edge communities, but all edge habitats support similar butterfly communities despite microhabitat differences (even when interior samples are removed from the data analysis).
DISCUSSION
The fragmentation impacts of natural environments have been extensively studied in different animal and botanical groups (Uehara-Prado et al., 2007; Buchmann et al., 2013; Sancha et al., 2014; Filgueiras et al., 2016; Justino et al., 2016). In general, several studies already demonstrated how the type of matrix surrounding a fragmented landscape may influence on species richness and composition (Gascon et al., 1999; Steffan-Dewenter, 2003; Vieira et al., 2009; Öckinger et al., 2012; Driscoll et al., 2013). The phenomena associated with these patterns are mostly related to species dispersal, colonization and extinction. However, few studies tested how the use of distinc microhabitat in a fragmented landscapes may influence on the assemblage structure of highly mobile organisms. Considering, for example, that sites inside fragments and sites along fragment border present very distinct habitats traits over a narrow geographical distance, highly mobile organisms such as winged insects could easily make use of both microhabitat types. Our study results showed, using distinct assemblage measurements, that this is not the case of butterfly assemblages.
Butterflies are widely known to have special preference for specific microhabitats (Brown Jr. & Hutchings, 1997; Devries & Walla, 2001; Hill et al., 2001; Brown Jr. & Freitas, 2002; Uehara-Prado et al., 2007; Ribeiro et al., 2012), such as shady environments (Hill et al., 2001; Brown Jr. & Freitas, 2002), hilltops (Prieto & Dahners, 2006; Carneiro et al., 2014); or to fly very close to their host plants (Rutowski, 1991). Most frequently (although not always) this association with microhabitats is based on the presence and abundance of adult and/or larval food resources (Hamer et al., 2006). According to our data, the assemblages sampled within microhabitats are more similar when compared among microhabitats. Therefore, the structure and distribution of butterfly assemblages in a fragment may be very heterogeneous, even when this fragment is deeply reduced in size (Ribeiro et al., 2008).
This pattern cannot be explained by their geographical proximity between sample sites. Actually, even delimiting sample sites in a very narrow distance between each other (< 100 m), we could not find a spatial bias in our assemblages. In general, forest edges concentrated greater species richness than the forest interior, and consequently a higher number of significant indicator species. This difference could occur due to the higher concentration of food resources offered to butterflies at the forest borders. The abundance of flowers attractive to butterflies inside the forest is scarce when compared to the forest edges, where several pioneering plant species bloom mainly from the Asteraceae and Rubiaceae family (Silberbauer-Gottsberger & Gottsberger, 1988; Andersson et al., 2002; Brown Jr. & Freitas, 2002; Ramírez, 2004). Such phanerogams are concentrated to a greater or lesser abundance around fragments, depending on which type of edge is found. For example, while abandoned edges are occupied by pioneer vegetation, farmers extend their crop fields closer to the fragment edge, thereby reducing the abundance of pioneer vegetation. Therefore, a greater richness is likely to be found in the abandoned habitat due to the greater abundance and diversity of flowers of this pioneer vegetation richness. Brown & Hutchings (1997) observed a similar pattern in the Amazon forest fragments, that is, small fragments surrounded by homogeneous areas (burned or pasture) and interiors of large fragments presenting low richness when compared with fragments that contained areas in regrowth and flowers in abundance. Similarly, Öckinger et al. (2012) found that butterfly species’ richness is higher in fragments surrounded by matrixes whose vegetation was more similar to the forest fragment. Hence, the quality of forest edges is of great relevance in order to maximize the species richness in fragmented landscapes.
Nevertheless, it is important to highlight that butterfly species richness is not always a good descriptor of habitat quality (Shuey et al., 2017). Instead, species composition has shown to be more sensitive measurement to detect differences between habitat types (Uehara-Prado et al., 2007; Truxa & Fiedler, 2012; Filgueiras et al., 2019). Although we could not find a significant difference in the species composition between different types of edges, (despite of their difference in species richness), the differences between forest interior and edges are remarkable. This distinction of butterfly assemblages related to forest interior and forest edges were already reported, including those of fruit-feeding butterfly (Brown Jr. & Hutchings, 1997; Uehara-Prado et al., 2007; Ribeiro et al., 2012; Filgueiras et al., 2016). Moreover, our results highlights that these differences are found mostly due to species turnover between those habitats. In other words, both types of microhabitat have a larger fraction of specialized species and only a smaller set of species can be found inhabiting forest interior and forest edges. This pattern is the opposite to those found in the Northern Hemisphere, in which the structure of butterfly assemblages across fine scale habitat use is mostly nested (Summerville et al., 2002; Trivellini et al., 2016). Most likely, the higher turnover rate observed here was produced by the behavior of butterflies. The species commonly found around the fragment hardly perch or forage inside the forest, or when they do, they should use the canopy stratum instead (Hill et al., 2001). The opposite behavior is observed to forest interior species, who usually avoids flying in habitats with high luminosity rates. These species are known to be adapted to shady and humid microclimates, frequently presenting cryptic behaviours and/or coloration (Uehara-Prado & Freitas, 2009, Iserhard et al., 2018).
Evidently, in the case of Atlantic Forest the species of special conservation concern are those specialized in forest interior habitats and not those specialized in forest edges (Brown Jr. & Hutchings, 1997; Ribeiro et al., 2012; Filgueiras et al., 2016). However, not all of them are reliable indicators of habitat quality. The abundance of some Ithomiini species for example, respond only to the presence of small pockets of humidity generated inside the fragments, instead of habitat quality (Brown Jr. & Freitas, 2002). The same could occur with some Satyrinae species whose larvae feed on grasses that invades the understory of strongly modified fragments. On the contrary, species such as Celaenorrhinus eligius punctiger (Burmeister, 1878) may indicate habitat quality because both larvae and adults feed on typical understory food resources (De Jong, 1982; Brown, 1992). Although our results pointed to a relevant number of interior forest indicators, we believe it is possible that several forest specialists are no longer present in the region due to their sensitiveness to disturbances (Hill et al., 2001; Cleary & Genner, 2004, Filgueiras et al., 2019). This hypothesis would also explain the lower number of species found in forest interiors when compared to forest edges.
The present study corroborates the importance of sampling different microhabitats when studying fragmentation processes, both inside and outside of fragments. Although forest edges may present different kinds of habitat types, species present along border tend to be as heterogeneous as species present in different locations inside the forest. This information should be considered in sampling designs of biodiversity essays that focus on a more consistent representation of local diversity.
ACKNOWLEDGEMENTS
We would like to thank Diego Rodrigo Dolibaina, Fernando Maia Silva Dias, Marlon Paluch, Mirna Martins Casagrande, Olaf Hermann Hendrik Mielke, Thamara Zacca Bispo Taumaturgo and Wildio Ikaro da Graça Santos for help with species identification.
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APPENDIX I
Geographic coordinates of sampled sites in the studied area.
F = Fragments (A, B, C); T = Microhabitat types (I = forest interior, F = farmland edge, R = road edge, Ab = abandoned edge)
APPENDIX II
List of butterflies (Papilionoidea) sampled in the sites studied, Joaçaba, Santa Catarina, Brazil.
Fragments (A, B, C). * Indicates species sampled by chance
APPENDIX III
Butterflies richness and abundance in the studied site
F = Fragments (A, B, C)
T = Microhabitat types (I = Forest interior, F = Farmland edge, R = Road edge, Ab = Abandoned edge)
APPENDIX IV
Butterflies species indicators in the studied area (only species with n ≥ 10 were included)
H: Habitat = E: edge, I: forest interior
Habits and Host plants information were obtained from literature cited below this table
