Conservation of mayflies (Insecta, Ephemeroptera) in Espírito Santo, southeastern Brazil

BIOLOGY, ECOLOGY AND DIVERSITY

Conservation of mayflies (Insecta, Ephemeroptera) in Espírito Santo, southeastern Brazil

Fabiana Criste Massariol^I,*; Elaine Della Giustina Soares^II,III; Frederico Falcão Salles^II

^IPrograma de Pós-graduação em Biodiversidade Tropical, Laboratório de Sistemática e Ecologia de Insetos, Universidade Federal do Espírito Santo, Rodovia BR-101 Norte Km 60, Bairro Litorâneo, 29932-540 São Mateus-ES, Brazil

^IIDepartamento de Ciências Agrárias e Biológicas, Centro Universitário Norte do Espírito Santo, Universidade Federal do Espírito Santo, Rodovia BR-101 Norte Km 60, Bairro Litorâneo, 29932-540 São Mateus-ES, Brazil. [e-mail]

^IIIPresent address: Instituto Latino-Americano de Ciências da Vida e da Natureza, Universidade Federal da Integração Latino-Americana, Foz do Iguaçú, Paraná, Brazil. [e-mail]

ABSTRACT

Conservation of mayflies (Insecta, Ephemeroptera) in Espírito Santo, southeastern Brazil. Ephemeroptera exhibits great diversity among bodies of freshwater in the Atlantic Forest, a biome that is suffering from massive human impact. Within this context, the creation of conservation units using biological information is more recommended than economic, cultural, or political criteria. The distribution pattern of 76 Ephemeroptera species was analyzed using the biogeographical methods Parsimony Analysis of Endemicity and Network Analysis Method in order to infer relevant areas for conservation of the mayfly community in Espírito Santo. The results obtained from both analyses were largely congruent, and pointed out four relevant areas for conservation: two in the south of the state, where conservation units or priority areas for conservation are well established; and two in the north, a region in the state where little conservation efforts have been historically done. Therefore, based on our analyses on mayflies, we recommend the expansion of the existing APCs or the creation of new APCs on the north of Espírito Santo.

Keywords: Atlantic Forest; biodiversity; distribution pattern; endemism; macroinvertebrates.

Conservation units are created by public managers and are of great importance to the in situ conservation of species, populations, and ecosystems. In addition to ensuring the preservation of biodiversity, conservation units are an important means of guaranteeing the quality and quantity of the water supply (Medeiros et al. 2011). Approximately 45% of threatened or endangered species depend on aquatic habitats and wetlands (Clark 1999). Therefore, to delimit and create a conservation unit, it is important to consider the hydrographical basin in which it is located (Clark 1999; Moulton & Souza 2006). Besides that, despite the above mentioned dependence on aquatic ecosystems, many studies have been conducted based on charismatics species (usually vertebrates), leading to a potentially problematic taxonomic bias in conservation (Clark & May 2002). In this sense, the use of macroinvertebrates in these kinds of studies is very important.

For the establishment of a conservation unit, economic, cultural, and political factors are more decisive than ecological principles, which are merely one among many criteria for the selection of a preservation site; moreover, there are several biological factors that should be considered (Soulé & Simberloff 1986). Accordingly, many conservation units have been created in Brazil and also in Espírito Santo without taking into consideration the most appropriate criteria.

The criterion of endemism is utilised to indicate a specific location as a priority for conservation (Carvalho 2004; Chen & Bi 2007; Löwenberg-Neto 2011). Although there are many concepts used to define areas of endemism, most authors agree that these areas have a significant number of exclusive species (Nelson & Platnick 1981). Indeed, areas of endemism are biogeographic elements that are used to indicate areas to be conserved because of unique features of biodiversity (Löwenberg-Neto 2011).

The Atlantic Forest is one of the most biodiverse and endangered ecosystems in the world, occupying the fourth position on the hottest hotspots in the world (Myers et al. 2000). It includes a large region that extends over the coastal mountain range along the Atlantic Ocean, in the northeast, southeast, and south regions of Brazil, also including eastern Paraguay and northern Argentina (IPEMA 2005). This biome that originally occupied approximately 90% of the State of Espírito Santo (southeastern Brazil) was reduced to only 9% after drastic environmental changes (IPEMA 2005; Passamani 2007). Fragmentation and habitat loss are the largest factors regarded as responsible for the loss of biodiversity and are the main processes contributing to landscape change (Fischer & Lindenmayer 2007).

Mayflies (Ephemeroptera) exhibit a high diversity and abundance in rivers of various sizes in the Atlantic Forest (Crisci-Bispo et al. 2007; Salles et al. 2010), and play an indispensable role in the food chain participating in the nutrient cycling, providing a food source for fish, birds, and other invertebrates (Waltz & Burian 2008). This order is the oldest group among winged insects (Britain & Sartori 2003) and have been widely used as bioindicators of water and ecological integrity (Baptista et al. 2007; Buss & Salles 2007), mainly because they exhibit significant variation in sensitivity to various contaminants including ammonia, nitrite, nitrate, metal, and other chemicals (Hickey & Clements 1998; Beketov 2004).

The aim of this paper, therefore, is to investigate relevant areas for conservation of the mayfly community in Espírito Santo, Brazil. Besides that, the aim is also to check if the existing conservation units or priority areas for conservation in the state encompass the relevant areas found in this work.

MATERIAL AND METHODS

Study area. Espírito Santo has an area of 45,597 km² and is located in southeastern Brazil, bounded by the states of Bahia, Minas Gerais, and Rio de Janeiro in the north, west, and south, respectively (Fig. 1). The topography is mountainous, with elevations ranging from sea level to 2897 m (IPEMA 2005). The state has 20 ottobasins, at level 04 (Fig. 2): 10 are basins (basins of the São Mateus, São José, Pancas, Santa Maria do Rio Doce, Guandu, José Pedro, Santa Maria da Vitória, Jucu, Itapemirim, and Itabapoana rivers), and 10 are interbasins (interbasins of the Itaúnas, Barra Seca, Norte, Bananal, Córrego do Ouro, Santa Joana, Piraquê-Açu, Aribiri, Benevente, and Córrego São Salvador rivers) (IJSN 2009). The state has 14 federal conservation units and 17 state conservation units, for a total of 31 conservation areas (Fig. 3) occupying 2.66% of the state area (119,559.8 ha). Most of the conservation units comprise less than 2,500 ha, and only four contain more than 10,000 ha: Reserva Biológica de Sooretama, Parque Nacional do Caparaó, Parque Nacional dos Pontões Capixabas, and Parque Estadual Paulo César Vinha. The first two units together represent the largest continuous forest remnants of the state and have great importance for the conservation of biodiversity (IPEMA 2005).

Projects sponsored by the Ministério do Meio Ambiente (MMA), part of the executive branch of the federal government, have indicated 182 priority areas for conservation (APCs) in Brazil (MMA 2000). Twenty-six APCs are in Espírito Santo (concentrated in the south): 12 of extreme biological importance, 13 of very high importance, and only one of high importance (Fig. 4).

Sampling and identification. We collected nymphs from 48 sampling sites between October 2011 and August 2012 (Fig. 1, Table I) in Espírito Santo and along its border with Minas Gerais. The sampling points were distributed in a standardised way—three in each ottobasin at different elevations and river widths. This standardisation was employed to obtain a more complete sampling, as these factors directly influence the composition of Ephemeroptera fauna (Domínguez & Valdez 1992; Baptista et al. 2001; Gallardo-Mayenco 2003). Only four ottobasins were not sampled (interbasins of the Norte, Aribiri, Córrego São Salvador, and Córrego do Ouro rivers) because they are influenced by seawater or have a reduced size (Fig. 2).

In Brazil, hydrographic basins are defined as operating territorial units for management of water resources, according to the law nr. 9433 (BRASIL 1988), and the classification in ottobasins has been used by Conselho Nacional de Recursos Hídricos. Therefore, the choice to work at ottobasins level was because this geographic information system is more appropriate to make decisions on water resources (ANA 2006). Besides, the rapid assessment approaches are enough to show the diversity profile of Ephemeroptera, due to the availability of the immature stages during most of the time (Edmunds et al. 1976) and the easy and inexpensive identification of specimens (Lenat & Barbour 1994; Resh 1994).

Collections were performed in 50-m stretches in rivers with small to medium widths and in 100-m stretches in large rivers. Ten samples in each section were collected with the aid of D-shaped net (aperture of 0.5 mm) in which a sweeping of the shadow area of net was performed. The sampling distribution in each stretch was made according to substrate availability, these included slabs, stone, gravel, sand, root, macrophytes, marginal vegetation, bottom litter, riffle litter. The samples were collected in this way to prevent the sampling effort from influencing the results.

All samples collected were fixed in 80% ethanol. The identifications were made based on Domínguez et al. (2006) and Salles (2006), assisted when necessary by articles relevant to each taxon. Morphotypes, i.e. Paracloeodes species 1, Paracloeodes species 2, were used for those specimens that did not fit into any species concept. They may represent species new to science or undescribed stages of previously described species. The specimens are deposited in the Coleção Zoológica Norte Capixaba (CZNC) of the Universidade Federal do Espírito Santo (UFES), in São Mateus.

Data analysis. Two methods of historical biogeographic were used to analyse the data: Parsimony Analysis of Endemicity (PAE) and Network Analysis Method (NAM), both can be used to delimitate areas of endemism. PAE (Morrone 2014) has also been used to indicate priority areas for conservation (e.g., Caviers et al. 2002; Chen & Bi 2007; Huang et al. 2010) and NAM, recently developed by Dos Santos et al. (2008, 2012), to date has not been used for this propose. However, NAM has many advantages when compared to PAE, such as: 1) independence on predefined areas; 2) considers earth's curvature; 3) evaluates the randomness in data structure; and 4) has a high relative stability of results to scale change (Dos Santos et al. 2008).

Although the collections were conducted quantitatively, the data were analysed qualitatively. After specimen identifications, matrices of presence and absence were constructed for PAE, and a set of species and its respective geographical coordinates were constructed for NAM. The areas resulting from these analyses were not denominated areas of endemism because the species whose geographic distribution extends outside the Espírito Santo area were not excluded from the analyses, so only the distribution within the state was taken into consideration.

Parsimony Analysis of Endemicity. We performed two separate analyses using localities as the operational geographical units: PAE by collection point and PAE by ottobasin. The data matrix was generated in Microsoft® Office Excel 2010, and the taxa were coded as absent (0) or present (1). A hypothetical area coded with zeros was used to root the cladogram; thus, the endemic areas were grouped by the presence of taxa. The matrices were analysed with TNT (Goloboff et al. 2004) using traditional search with 500 replicates. A strict consensus cladogram of the resulting trees was obtained using Winclada 1.0 (Nixon 1999) with fast optimization. The collection points and ottobasins with two or more exclusive species in Espírito Santo were mapped using the programme DIVA-GIS 7.5.0 (Hijmans et al. 2005).

Network Analysis Method. The distribution patterns of species of Ephemeroptera were analysed through NAM based on sympatry inference (Dos Santos et al. 2008, 2012). The analysis was performed using the software R 2.14.2 (R Development Core Team 2011) and the packages SyNet (Dos Santos et al. 2012) and TKRplot (Tierney 2010).

The data were managed to estimate the minimum spanning tree for each species, and the orthodromic distances were calculated. From this result, two matrices of spatial association were inferred: the cost of spatial homogenisation (ACSH) and the topological resemblance (MST). The analysis involved only UCs and diads that satisfied both thresholds, and those that were absent from one of the matrices were discarded. The next step was to choose the cut-off value (maximum distance between the two points considered to be sympatric) used to calculate the basal network. The basal network was achieved from the reweighted topological resemblance > 0.886 and ACSH < 26.091 km. The binary matrix generated corresponded to the basal network to be analysed by NAM.

UCs are presents in a large network, and existing intermediate species are typically associated with these UCs. Thus, the removal of intermediate species segregates UCs and diads. The resulting cleavogram shows the spatial relationship among the species in a net context and represents a simplified technique to illustrate the division of groups with the removal of intermediate species. The spatial expression patterns of UCs and diads were mapped using the software DIVA-GIS 7.5.0 (Hijmans et al. 2005).

RESULTS

A total of 76 species (Appendix 1) were found in 48 sampling sites, for a total of 658 distribution records from Espírito Santo and its borders with Minas Gerais and Rio de Janeiro.

PAE by collection point. The analysis of the data matrix (Table II) produced 34 equally parsimonious trees with 432 steps, a consistency index of 17, and a retention index of 19. The strict consensus cladogram (Fig. 5) showed at the base of the cladogram the presence of six species widely distributed in the state: Americabaetis alphus Lugo-Ortiz & McCafferty, 1995; Camelobaetidius billi Thomas & Dominique, 2000; Camelobaetidius rufiventris Boldrini & Salles, 2009; Paracloeodes eurybranchus Lugo-Ortiz & McCafferty, 1996; Paracloeodes waimiri Nieto & Salles, 2006; and Farrodes carioca Dominguez, Molineri & Peters, 1996. Furthermore, some points or groups showed only one exclusive species: PT 10 (Tricorythopsis rondoniensis Dias, Cruz & Ferreira, 2009), PT 16 (Lachlania sp. 2), PT 21 (Lachlania sp. 1), PT 35 (Adebrotus lugoi Salles, 2010), PT 37 (Baetodes liviae Polegatto & Salles, 2008), PT 41 (Paracloeodes sp. 2), PT (26+19(10+27)) (Traverella insolita Nascimento & Salles, 2013), and PT (10+27) (Harpagobaetis gulosus Mol, 1986).

Four points (Fig. 6) with two or more exclusive species each resulted from the analyses: PT 02 def ined by Paracloeodes sp. 1 and Leptohyphodes inanis (Pictet, 1843); PT 08 defined by Callibaetoides caaigua Cruz, Salles & Hamada, 2013 and Miroculis sp. 1; and PT 42 defined by Spiritiops sp. 1 and Thraulodes sp. 1. Sample site PT 27 showed the highest number of exclusive species, Camelobaetidius juparana Boldrini & Salles, 2012; Tricorythopsis spongicola Limas, Salles & Pinheiro, 2011; and Oligoneuria amandae Salles, Soares, Massariol & Faria, 2014, plus two: Ha. gulosus shared with PT 10 and Ta. insolita shared with PT 16 and 26.

PAE by ottobasin. The analysis of the data matrix (Table III) produced six equally parsimonious trees with 182 steps, a consistency index of 41, and a retention index of 42. The strict consensus cladogram (Fig. 7) showed ten ottobasins and groups of them (Figs. 8-9) with two or more exclusive species each. The resulting ottobasins exhibited a nested pattern, with some groups subordinate to others.

All the ottobasins analysed were grouped by eight species: Am. alphus; Americabaetis labiosus Lugo-Ortiz & McCafferty, 1996; Cm. billi; P. eurybranchus; P. waimiri; Waltzoyphius fasciatus Lugo-Ortiz & McCafferty, 1995; Tricorythopsis minimus (Allen, 1973); and F. carioca. The basins and interbasins of the Pancas (7614), São Mateus (7598), São José (7612), Guandu (7618), Santa Maria do Rio Doce (7616), Santa Joana (7617), Santa Maria da Vitória (7712), Piraquê-Açu (7711), Bevente (7715), Jucu (7714), Itabapoana (7718), José Pedro (7624), and Itapemirim rivers (7716) were grouped by five exclusive species: Baetodes iuaquita Salles & Nessimian, 2011; Cm. rufiventris; Leptohyphes plaumanni Allen, 196; Tricorythopsis sp. 1; and Ta. insolita. All the thirteen ottobasins mentioned above jointly with the interbasin of the Bananal river (7613) were defined by three exclusive species: Callibaetis sp. 1; Camelobaetidius francischettii Salles, Andrade & Da-Silva, 2005; and Cloeodes sp. 1.

In the north of the state, the interbasin of the Itaúnas river (7597) showed Cl. caaigua and Miroculis sp. 1 as exclusive species. The basin of the São José river (7612) presented three exclusive taxa: Cm. juparana, Ti. spongicola, and O. amandae. These basins in conjunction with the basin of the São Mateus river (7598) were grouped by the presence of the exclusive species Ha. gulosus and Hylister obliquus Nascimento & Salles, 2013.

The resulting ottobasins in the south of the state had a little more complex hierarchical pattern. The basin of the Itabapoana river (7718) presented two exclusive taxa (Paracloeodes sp. 1 and L. inanis), that together with the ottobasins of Itapemirim (7716) and José Pedro (7624) rivers had the unique taxa Americabaetis titthion Lugo-Ortiz & McCafferty, 1996; Baetodes sp. 2; Cloeodes itajara Massariol & Salles, 2011; Tupiara ibirapitanga Salles, Lugo-Ortiz, Da-Silva & Francischetti, 2003; and Askola froehlichi Peters, 1969. The basins mentioned above, i.e. (7716+7624+7718), along with the Jucu river basin (7714) shared two exclusive species: Americabaetis sp. 1 and Baetodes sp. 1. Furthermore, in the Jucu river basin (7714) three exclusive taxa were found: Paracloeodes sp. 2, Spiritiops sp. 1, and Thraulodes sp. 1.

Network Analysis Method. After the analyses of 658 records, NAM recognised four UCs and six diads (Table IV, Figs. ^10-20) after the removal of 31 intermediary species and eight isolated species.

 

UC1 is composed of the distribution area of eight species: As. froehlichi; Am. titthion; Baetodes serratus Needham & Murphy, 1924; Baetodes sp. 2; Co. itajara; L. inanis; Paracloeodes sp. 1; and Tu. ibirapitanga. The spatial expression of this unit matches the Parque Nacional do Caparaó, including the collection points PT 01, 02, 03, 14, and 15 (Fig. 17).

UC2 comprises the distribution areas of four species: Americabaetis sp. 1, Spiritiops sp. 1, Thraulodes sp. 1, and Tricorythodes santarita Traver, 1959. This unit is in the central, north coast, and northwest regions of Espírito Santo and encompasses the collect points PT 26, 27, 31, 42, and 46 (Fig. 18).

UC3 encompasses the distribution area of seven species: Ad. lugoi, Hy. obliquus, Cm. juparana, O. amandae, Ti. spongicola, Ti. rondoniensis, and Ha. gulosus. This unit is in the north coast and northwest regions and encompasses the collection points PT 10, 19, 24, 27, and 35 (Fig. 19). UCs 2 and 3 overlap at one point, PT 27 (Sooretama, São José river), which has exclusive taxa of the two units.

UC4 is composed of the distribution area of six species: Baetodes santatereza Salles & Polegatto, 2008; Callibaetis sp. 1; Cm. francischettii; Tricorythopsis gibbus (Allen, 1967); Tricorythopsis araponga Dias & Salles, 2005; and W. fasciatus. This unit has a very broad spatial expression, with points from north to south (Fig. 20).

Diads 2, 3, and 5 showed a broad spatial expression in the state (Figs. 12, 13, and 15) and are composed of the distribution area of Cloeodes hydation McCafferty & Lugo-Ortiz, 1995 - Thraulodes itatiajanus Traver & Edmunds, 1967; Hylister plaumanni Dominguez & Flowers, 1989 - Tricorythopsis baptistai Dias & Salles, 2005; and Hydrosmilodon gilliesae Thomas & Péru, 2004 - Zelusia sp. 1, respectively. The remaining diads have a more restricted spatial expression: diad 1 with spatial expression at only one point in the northern state with exclusive taxa Cl. caaigua, and Miroculis sp. 1 (Fig. 11); diad 4 (Fig. 14) and 6 (Fig. 16) both restricted to the south with exclusive taxa Rivudiva trichobasis Lugo-Ortiz & McCafferty, 1998 - Leptohyphes sp. 1, and Lachlania sp. 1 - Paracloeodes sp. 2, respectively.

DISCUSSION

The results of the three analyses were largely congruent, particularly the results of the two approaches using PAE. Considering the total congruence in at least two of the three analyses, the following four relevant areas for conservation of the mayfly community in Espírito Santo were inferred (Fig. 21). Area 1: In the extreme north, this area corresponds to PT 08, ottobasin 7597 (interbasin of the Itaúnas river), and diad 10 and comprises the distribution of two exclusive species: Cl. caaigua and Miroculis sp. 1. Area 2: On the north coast and in the northwest region, this area corresponds to PT 27 and ottobasin 7612 (basin of the São José river) and encompasses the distribution of three exclusive species: Cm. juparana, Ti. spongicola, and O. amandae. Although there was no total congruence between the results of PAE and NAM for this area, PT 27 in the Network Analysis was a point of overlap for two UCs (UC2 and UC3). Area 3: In the central region, this area corresponds to PT 42 and ottobasin 7714 (basin of Jucu river) and is composed of the distribution of three exclusive species: Paracloeodes sp. 2, Spiritiops sp. 1, and Thraulodes sp.1. Area 4: In the south along the border with Minas Gerais, this area corresponds to ottobasins 7718, 7624, and 7716 (the basins of the Itabapoana, José Pedro, and Itapemirim rivers, respectively), containing PT 02 and UC1. This area includes eight exclusive species: As. froehlichi, Am. titthion, B. serratus, Baetodes sp. 2, Co. itajara, L. inanis, Paracloeodes sp. 1, and Tu. ibirapitanga.

The inferred areas for conservation 1 and 4 have the largest number of previously protected areas, with six conservation units each (Fig. 22). Area 1 presents units with a small size (not exceeding 3,000 ha), whereas area 4 contains Parque Nacional do Caparaó, the second largest unit of conservation in Espírito Santo and five other small units. Area 1 is located in the north of the state, a region with few forest fragments due to the severe deforestation occurred in the 19th century by wood exploration and actually by vast eucalyptus plantations (IPEMA 2005; Paula 2006). It is noteworthy that the spatial expression of UC1 corresponds to the region of Parque Nacional do Caparaó. Area 2 encompasses only a small part of Parque Nacional dos Pontões Capixabas, and area 3 contains only the Parque Estadual de Pedra Azul (Fig. 22); both areas present three exclusive taxa, but the number as well as the size of conservation units area are minimal (not exceeding 1,300 ha). The point PT 27 located in area 2 (corresponding to ottobasin 7612), showed the highest number of exclusive species, besides in NAM analyses PT 27 was a point of contact between UCs 2 and 3, so this area has a high complexity. Despite the ottobasin 7612 being an area that suffer intense anthropogenic pressure (ANA 2001) and be recognized (through PAE and NAM) as one of the relevant areas for conservation, it is unprotected, with only a small part set as a conservation unit in western state. When we compared the inferred areas for conservation (Fig. 21) with APCs of MMA (Fig. 4), we observed that most APCs are in areas 3 and 4 in the southern part of state (Fig. 22). Although area 3 has four APCs all are located marginally. The area 4 is extensive (ottobasins 7624, 7716 and 7718), however the points of exclusive taxa are concentrated in a small area, so the methods showed that this area can be a natural unit. The APCs in area 4 seem to be sufficient and necessary to preserve the biodiversity of the studied group, because they are well distributed spatially, and covers the points of exclusive taxa resulting by PAE and NAM analyses. The contact area between areas 3 and 4 was previously indicated as extremely high priority for conservation. In this work the data suggested that this area is complex, because it is a transition between two areas, so our data corroborate the status given by the MMA assessment.

Unlike the southern portion of the state, northern Espírito Santo is poorly represented by APCs. In this work two areas were pointed out in the north of the state, however only one APC was indicated by MMA, and it is located on area 1. Despite the area 2 being indicated in this study as a relevant area for conservation of the mayfly community and with a high complexity, the MMA did not pointed out any area within this region as APC. This fact occurs because of two historical and probably dependent reasons: little effort has been done in the north of the state in order to uncover its biodiversity; and, except for Reserva Biológica de Sooretama and Reserva da Vale, only small fragments of forest persist in this area due to agricultural activities. So, this situation makes the region to receive less interest from researches (Moreira et al. 2008).

The north coast of the state is widely suggested as having high priority for conservation according to MMA, however the western portion is unprotected by both the lack of conservation units and APCs. Furthermore, the point of contact between UCs 2 and 3 (PT 27) is unprotected by conservation units, and it is not identified as a priority for conservation by MMA. All areas resulting from the analyses present at least one conservation unit or one portion of APC with the exception of point PT 27 in the north of Espírito Santo. Therefore, it is recommended that the existing APCs be expanded to integrate the relevant areas for conservation of the mayfly community inferred in this work, or the creation of new APCs particularly on the north of Espírito Santo.

ACKNOWLEDGMENTS

We are grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, grants 402939/2012-3, 245924/2012-4) and Fundação de Apoio à Ciência e Tecnologia do Espírito Santo (FAPES, grants 54689627/ 2011, 511187434/2010) for financial support; IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis) for collecting permits; Ezinete Moreira do Rozário for her invaluable support with the fieldwork; to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for scholarship provided to the first author and to CNPq for research scholarship provided to the third author (grant 306670/2012-7). To Carlos Molineri for his help with biogeographic methods, and to Luisa Maria Soares Porto and Mateus Pepinelli for their contributions to dissertations that originated this work.

Received 31 March 2014; accepted 22 October 2014

Associate Editor: Gustavo Graciolli

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Appendix 1

   

Publication Dates

• Publication in this collection
  12 Jan 2015
• Date of issue
  Dec 2014

History

• Received
  31 Mar 2014
• Accepted
  22 Oct 2014