Faunistic Catalog of the Caddisflies (Insecta: Trichoptera) of Parque Nacional do Itatiaia and its Surroundings in Southeastern Brazil

The Atlantic Forest is considered one of the world's biological diversity hotspots, and is increasingly threatened by the rapid destruction and fragmentation of its natural areas. The caddisflies (Trichoptera) of Itatiaia massif, an Atlantic Forest highland area, are inventoried and cataloged here. The catalog is based on examination of bibliographies, field work on many localities of Itatiaia massif (including Parque Nacional do Itatiaia — PNI), and the entomological collection Professor José Alfredo Pinheiro Dutra (DZRJ), Universidade Federal do Rio de Janeiro. A total of 92 species are recorded, representing about 17% of the known Brazilian Trichoptera fauna. Leptoceridae, Hydropsychidae, and Philopotamidae are the families most represented. The high species richness, as well as the remarkable patterns of species distribution, may be related to the characteristics of Mantiqueira mountain range.


Introduction
Caddisflies (Trichoptera) comprise more than 13,500 extant species described from all faunal regions, arranged in about 610 genera and 47 families (Morse 2011). However, Schmid (1984) claimed that world fauna may contain approximately 50,000 species, which leads to the conclusion that only about 25% of world species of caddisflies have been described. Even limited to the diversity currently known, Trichoptera constitutes the 7th-largest insect order and the most diverse among orders of primary aquatic insects Holzenthal et al. 2007).
The Neotropical Region is divided into two distinct faunal subregions: the Chilean subregion (southern Chile and adjacent Argentina) and the Brazilian subregion (southern Mexico, Central America, Antilles, and remnant South America) (Flint 1976). de Moor and Ivanov (2008) proposed an alternative biogeographic pattern for Trichoptera distribution, considering 12 biogeographical regions. According to them, the Neotropical region sensu Wallace (1876) is divided into Patagonian and Neotropical regions, corresponding respectively to the Chilean and Brazilian subregions, as determined by Flint (1976). Chilean fauna is highly endemic and closely related to the fauna of the Australian region. Furthermore, the northern Andes, the Amazon basin, and the mountains of southern and southeastern Brazil can be considered areas with great concentrations of endemic species and with high numbers of non-endemic species (Flint et al. 1999).
There are about 2,200 species described from the Neotropical region, where diversity and distribution of Trichoptera are little-known (Flint et al. 1999). In Brazil, a recent inventory of the fauna reported 378 species for the country ). Currently, this number has increased significantly to approximately 550 species, distributed in 70 genera and 16 families (Santos et al. 2011), indicating that the diversity of the order in Brazil is underestimated. In such case, there are many new species remaining to be discovered and described . There are over 300 new species deposited in Brazilian and in foreign entomological collections waiting to be described (Calor 2009). Besides that, many species are only known from their typelocalities .
The order Trichoptera is divided into three suborders: Annulipalpia (net-spinning or fixed-retreat makers), Integripalpia (portablecase makers), and Spicipalpia (Hydrobiosidae and Rhyacophylidae (free-living), Glossosomatidae (saddle-case makers), and Hydroptilidae (purse-case makers)) ). However, Spicipalpia is not monophyletic in either morphological or molecular phylogenetic analyses (Morse 1997;Kjer et al. 2001Kjer et al. , 2002. Some phylogenetic works recognize to a fourth suborder called Protomeropina, composed of fossil families from the Permian. This suborder is sometimes considered part of the ancestral Amphiesmenoptera lineage (de Moor and Ivanov 2008;Calor 2009). Immature caddisflies stages are exclusively aquatic, being important in aquatic assemblages.
Larvae are important components of energy flow and nutrient dynamics in freshwater environments (Resh and Rosenberg 1984). Trichoptera larvae are capable of spinning silk from modified salivary glands. Silk is used in many ways by caddis larvae to construct portable cases, fixed retreats, shelters, and capture nets, and probably is an asset in their ecological and taxonomic diversification (Wiggins 1996). Immature caddisflies can be found in all types of freshwater environments, being especially diverse in running waters like rivers and streams. Furthermore, larvae of Trichoptera have distinct responses to pollution and other environmental impacts. For this reason, caddisflies are widely used in water quality monitoring programs (Morse 1997;Paprocki et al. 2004). Adult caddisflies resemble small moths, generally drab in color, and are found in riparian and shoreline vegetation (Angrisano 1995a;Holzenthal et al. 2007). In contrast to larvae, ecology and behavior of adult Trichoptera are poorly known (Flint et al. 1999).
The Brazilian Atlantic Forest is among the five most important biodiversity hotspots in the world. Less than 8% of the original forest now remains, and it occurs mostly in isolated topographically remnants scattered throughout a landscape dominated by agricultural uses and urbanization. Despite these disturbances, the Atlantic Forest is still extremely rich in biodiversity, sheltering a significant proportion of the Brazilian fauna and flora with high levels of endemism (Joly and Bicudo 1998;Myers et al. 2000). The Itatiaia massif, on which the Parque Nacional do Itatiaia (PNI) exists, is among one of the most important protected areas of Atlantic Forest due to different forest formations with welldefined climatic and vegetation bands (Ururahy et al. 1983). Trichoptera species recorded from the Itatiaia massif were derived from isolated species descriptions and general checklists for southeastern Brazil. However, a comprehensive checklist was not available for the Itatiaia massif, highlighting the gaps in our knowledge of this group in the area. Furthermore, collection events were concentrated in the lower portion of PNI. Therefore, herein we present a catalog aiming to update the list of caddisfly species found in the Itatiaia massif. This catalog is based on recently collected specimens, specimens previously deposited in the Coleção Entomológica Prof. José Alfredo Pinheiro Dutra, UFRJ, Brazil (DZRJ), and literature data until 2011, providing a taxonomic overview of the Trichoptera species known to occur in the Itatiaia massif. New Brazilian state records and distribution data are also given here.

Study area
The Itatiaia massif is situated in Mantiqueira mountain range, an extensive area of highlands in southeastern Brazil. The massif is located on the border of three Brazilian states: Minas Gerais (Alagoa, Bocaina de Minas and Itamonte municipalities), Rio de Janeiro (Itatiaia and Resende municipalities), and São Paulo (a small portion of Queluz municipality).
The highlands of Itatiaia massif are a Pre-Cambrian outcrop of metamorphic nephelinesyenite rocks (IBDF 1982). One of the most important Brazilian geological areas, the massif possesses the seventh-highest mountain of the country -the Itatiaiaçuwhich stands at 2,787 m, located in Agulhas Negras complex. Other important peaks, such as Pedra do Couto (2,682 MASL) and Prateleiras (2,515 MASL) also belong to the massif (Magro 1999).
Itatiaia massif has four vegetation types that follow an altitudinal gradient: lower montane forest (from 400 to 499 MASL) montane forest (from 500 to 1,499 MASL) (Figure 1),  upper montane forest (from 1,500 to 1,999 MASL) (Figure 2), and high-altitude grasslands (more than 2,000 MASL) ( Figures  3 and 4) (Ururahy et al. 1983). According to The Conservation International of Brazil (2000), this region is characterized as a nucleus of the Atlantic Forest Biosphere Reserve, one of the biggest conservation units in the world.
The climate is mesothermic, markedly seasonal, with cold and dry winters and very wet summers (Cwa according Köppen's classification). Mean annual temperature is about 14 °C, with lower temperatures falling below -10 °C during the rigorous winter. Annual rainfall is about 2,400 mm, concentrated in the summer months (Ribeiro et al. 2007). At the end of April and beginning of October the rainfalls become uncommon, which causes a relatively dry winter (Barros 2003 (IBDF 1982). Rivers and streams of Itatiaia massif have regular discharges during the winter, receiving a large amount of water during the summer period. The rivers usually have a tumbling flow, forming rapids along sloping rocky beds, mainly at the south portion (turned to Paraíba do Sul valley), where the topography is more pronounced (Magro 1999). At the high area of the massif, there are highland lakes formed by flowing water of marshes. These may become frozen during the winter (IBAMA 1994).
PNI is located on the border between Rio de Janeiro and Minas Gerais states, between 22º 19' -22º 45' S and 44º 15' -44º 50' W. The protected area was established in 1937 and is the oldest national park in Brazil. Currently, PNI comprises an area of 30,000 ha, covering 20% of Itatiaia massif (Barros 2003 Mantiqueira) which provides an ecological buffer zone for the park ( Figure 5).

Sampling
The catalog of species is based mainly on specimens collected from many localities of the Itatiaia massif between 1990 and 2009. Additional records from previous published articles are also provided here. Sampled area was divided into five major drainage subbasins (  Figure 11). In addition, the specimens deposited at Coleção Entomológica Professor José Alfredo Pinheiro Dutra (DZRJ) of the Universidade Federal do Rio de Janeiro were examined. Taxonomic bibliography that includes data of Itatiaia massif is also included here to complement this inventory.
Larvae and pupae were collected with Surber and Brundin nets (125 m and 180 m mesh), sieves, and manually in several kinds of substrate, in rapids, and pools of rivers and streams. The specimens were preserved in 80% ethanol. Adults were collected with light traps (white sheet and Pennsylvania light trap), which were placed near streams and lightened at dusk, remaining switched on during the night. At daytime the adults were collected in activity with entomological nets and aspirators. The specimens were also preserved in 80% ethanol and few ones were pinned.
Immature stages were identified to generical level based on keys by Angrisano (1995a), Wiggins (1996), and Pes et al. (2005). Some larvae were identified to species level according to descriptions given for manuscripts of immature association (Holzenthal 1997;Huamantinco and Nessimian 2004a;Huamantinco et al. 2005;Dumas and Nessimian 2006;Calor and Froehlich 2008;Nessimian and Dumas 2010). Adult identification was based on the morphology of male genitalia. In order to observe the genital structures, the abdomen was removed and cleared in a heated solution of 10% KOH (Beten 1934

Discussion
Itatiaia massif caddisfly fauna represents a significant proportion of Brazilian known fauna.
Considering that Brazil has approximately 550 described species (Santos et al. 2011), the fauna of Itatiaia massif comprises about 17% of the total number of species known from the country. This species richness is even more significant considering the minute surface area of Itatiaia massif and the total number of species found in comparison with other South American countries (Argentina, 250 spp.; Venezuela, 240 spp.; Peru, 224 spp.; Chile, 214 spp.; Colombia, 205 spp.; Surinam, 124 spp.) (Angrisano 1995b;Flint 1974b;Flint 1996;Johanson and Holzenthal 2004;Muñoz-Quesada 2000;Rojas 2006). However, it is important to emphasize that several of these countries have deficient knowledge of caddisflies fauna, with most biomes poorly sampled.
Such high species richness present in Itatiaia massif may be explained by the singular features of Mantiqueira mountain range. The mountaintops of Mantiqueira present a cold, temperate climate within a tropical zone and a temperate vegetation island surrounded by a tropical rain forest. Besides that, rocky outcrops abruptly raised from surrounding plains (inselbergs) have a strong influence on the distribution and abundance of biodiversity worldwide, being biological hotspots and supporting unique biotic communities. Moreover, these areas are characterized by high levels of endemism (Porembski et al. 1997;Porembski and Barthlott 2000). This may be attributed to three main factors that have acted at different time scales: biotic evolution in response to climatic and geological history; species adaptations to environmental constraints; and biotic exchanges with the surrounding lowlands (Sarmiento 2002).
Furthermore, 13 species are endemic to Itatiaia massif. This notable mark may reflect the fact that most distributional records of Neotropical caddisflies species are represented by incidental collections, with many species known only from the original site where they were described ). However, some of these endemisms are remarkable.
A few conclusive empirical works have focused on the Southern Hemisphere biogeographical patterns (Sanmartín and Ronquist 2004;Giribet and Edgecombe 2006;Daugeron et al. 2009). Two climatic biotic provinces are recognized within Gondwana: the northern Tropical Gondwana, which includes northern South America, Africa, Madagascar, India, New Guinea, and northern Australia; and the southern Temperate Gondwana, which includes southern South America, South Africa, Australia, Antarctica, New Caledonia, and New Zealand (Sanmartín and Ronquist 2004). In the Neotropical Trichoptera, some of these affinities are discussed by de Moor and Ivanov (2008) and Holzenthal and Blahnik (2010).
Some interesting patterns of species distribution occur in Itatiaia massif and other areas of Mantiqueira mountain range. Some endemic species encountered do not seem to be related to any other species in South America, being ancient relicts of prerupture Gondwanan fauna (Flint 1976). The genus Neoatriplectides Holzenthal, 1997 contains two species, one in the Mantiqueira mountain range -N. desiderata Dumas and Nessimian, 2009 -and other in tropical Andes -N. froehlichi Holzenthal, 1997. The other genera of Atriplectididae, Atriplectides Mosely, 1936 andHughscottiella Ulmer, 1910, possess representatives in Australia and the Seychelles Islands, respectively (Holzenthal 1997). Therefore, the family Atriplectididae contains Tropical Gondwana components. Likewise, the monobasic genera Neoathripsodes Holzenthal, 1989 (Leptoceridae) and Barypenthus Burmeister, 1839 (Odontoceridae) show affinities with South African genera (Holzenthal 1989;de Moor 1997). In contrast, Holzenthal and Blahnik (2010) Blahnik, 2010 andN. ecuadorensis Holzenthal andBlahnik, 2010, respectively -may represent an older occurrence in the region, followed by recent dispersal from southern South America to north and its subsequent diversification (Holzenthal and Blahnik 2010).
Some other curious distributional patterns can be observed in Antarctoecia brasiliensis , the single species of Limnephilidae recorded from Brazil. The genus Antarctoecia Ulmer, 1907 shows a disjunct distribution, with A. nordenskioeldii (Ulmer, 1907), described from the Puna de Jujuy (Argentina) in elevations above 4,500 m, and A. brasiliensis, found only at Itatiaia plateau above 1,800 m. Biogeographical affinities have been recognized between the fauna and flora of southeastern Brazilian mountains and the Andean-Patagonian region (Illies 1969;Sick 1985;Safford 1999;Behling 2002). It is assumed that Brazilian southeastern mountains were colonized by Andean elements during Pleistocene glaciations, when climatic-vegetational connections between both regions were similar (Simpson-Vuilleumier 1971). During interglacial periods, those montane habitats would have retreated to cooler upland areas, explaining the isolated occurrence of some Andean-Patagonian taxa on southeastern Brazilian mountaintops (Simpson 1979;Safford 1999). Holzenthal and Blahnik (2010) claim that the distributional pattern of Notidobiella and Antarctoecia, like other with Patagonian and Neotropical distribution, are probably one and the same.
de Moor and Ivanov (2008) propose five biogeographical patterns. One of them is a two-way exchange of Neotropic and Neartic faunas. It may be the case of Anastomoneura guaybae Huamantinco and Nessimian, 2004 (Odontoceridae), the only species within the genus, which larvae share more similarities with the North American genus Nerophilus Banks, 1899and Namamyia Banks, 1905(Dumas and Nessimian 2006.! Itatiaia massif is located in the Atlantic Forest biome, which is classified as one of the 25 biodiversity hotspots around the world. However, less than 8% of the original forest of this biome now remains, and it occurs mostly in isolated remnants scattered throughout a landscape dominated by agricultural uses. Despite these disturbances, Atlantic Forest is still extremely rich in biodiversity, sheltering a significant proportion of total national fauna and flora, with high levels of endemism (Dean 1997;Joly and Bicudo 1998;Myers et al. 2000). Although part of Itatiaia massif is inserted in protected areas -Parque Nacional do Itatiaia and Área de Proteção Ambiental da Mantiqueira -there are constant losses of its vegetation and fauna by anthropic pressures, such as fire and livestock grazing.
The results of this study, allied with other faunistic and floristic works (Geise et al. 2004;Sendas and Araújo 2004;Ribeiro et al. 2007;Monné et al. 2009; among others), emphasize the importance of better efforts to preservation and conservation of Itatiaia massif. Furthermore, considering the degree of threat in the Atlantic Forest in this area and its high biological diversity, including that of Trichoptera, the conservation of these remnants and incentives to continue studying native species of fauna and flora are therefore highly recommended. The creation of new conservation units, or the enlargement of existing ones, is necessary to better preserve the biodiversity and to help prevent further deforestation.

Acknowledgements
We would like to thank Dr. Ralph Holzenthal and Dr. Roger Blahnik for their very important contribution to this manuscript, providing some new species records included here; two anonymous referees for constructive suggestions; Léo Nascimento and his staff at Parque Nacional do Itatiaia (PNI)