Aquatic Insects from the Caatinga: checklists and diversity assessments of Ubajara (Ceará State) and Sete Cidades (Piauí State) National Parks, Northeastern Brazil

Abstract Background Diversity and distribution of Neotropical aquatic insects is still poorly known, with many species to be recorded and many others to be described, due to the small number of taxonomists and sparse faunistic studies. This knowledge is especially poor in the Caatinga Domain in Northeastern Brazil, even though, this region may have played an important historical role in the spatial evolution of faunas of forested areas in northern South America. New information Aquatic insect checklists of 96 species from Parque Nacional de Ubajara (Ceará State, Brazil) and 112 species from Parque Nacional de Sete Cidades (Piauí State, Brazil) are presented, representing the following taxa: Elmidae, Epimetopidae, Hydrophilidae, and Torridincolidae (Coleoptera), Hemerodromiinae (Diptera: Empididae), Ephemeroptera, Gerromorpha and Nepomorpha (Hemiptera), Odonata, Plecoptera, and Trichoptera. Because of the scarce number of biological inventories in Northeastern Brazil, several new distributional records (of species, genera, and families) for Brazil, Northeastern Brazil, and Ceará and Piauí states are provided. In addition, several undescribed species were detected, being 26 from Ubajara and 20 from Sete Cidades. Results represent a significant increase to the known fauna of these states, ranging from 13%-70% increase for Ceará and 41% to 91% increase for Piauí. Although both parks are relatively close to each other and within the Caatinga domain, their aquatic fauna display a very high complementarity (89% species), possibly due to structural differences of water bodies sampled in each park. Rarefaction curves based on quantitative light trap samples suggest a much higher expected species richness of aquatic insects at Sete Cidades than at Ubajara National Park. Discussion on biogeographical affinities of this sample of the Caatinga fauna is provided.


Introduction Aquatic insects
Insects constitute the most diverse animal group and represent one of the earliest lineages occupying the terrestrial habitat (Grimaldi and Engel 2005). Although they are mostly terrestrial, insects usually dominate inland waterbodies in terms of species number and biomass. Many terrestrial insects are resilient to eventual submersion in water (Chapman 1998), but true aquatic insects inhabit freshwater or marine environments at least for one life stage and have several morphological, physiological, and behavioural adaptations. Aquatic insects are usually abundant and important components of energy flow in freshwater habitats, and thus have been the focus of many ecological studies, as well as, the most frequent macroinvertebrate group used in biomonitoring (Rosenberg andResh 1993, Merritt andCummins 1996).
The diversity of aquatic insects is a result of several independent invasions of aquatic habitats by terrestrial lineages (more than 50 separate invasions, according to Dijkstra et al. (2014). Marine insects are relatively rare, most of them living in coastal areas and only very few species in the open sea (Cheng 1976). On the other hand, insects inhabiting freshwater are close to 100,000 described species, in twelve insect orders, five of them primarily aquatic: Ephemeroptera, Odonata, Plecoptera, Megaloptera, and Trichoptera (Dijkstra et al. 2014).
Regional knowledge of the aquatic insect fauna is essential to ecological surveys or biomonitoring. In the Neotropics, diversity and distribution of aquatic insects is still poorly known, with many species to be recorded and many others to be described, especially because of the small number of taxonomists and sparse faunistic studies, even near large urban areas. Currently, there are approximately 7,000 described species of aquatic insects in Brazil (Boeger et al. 2016), representing approximately 8% of known species in the world. Amongst these groups, only Odonata and Psychodomorpha reach numbers higher than 14% of the world's fauna ( Table 1). The number of species of some aquatic taxa recorded from Brazil, e.g., Trichoptera, is far below the average of 8% of the world fauna, very likely due to the many undescribed species waiting to be formally named or recorded from the country. Undersampling is one of the major biases for richness evaluations studies and conservation actions such as recently demonstrated for Brazilian dragonflies (Vianna and De Marco Júnior 2012). Therefore, local inventories should remain a priority, particularly in those poorly sampled areas, such as Northeastern Brazil. Number of described species in the major aquatic insect groups in the world and in Brazil, and percentage of Brazilian fauna in relation to the world's biota.
Odonata, and Trichoptera recorded from Brazilian states of Ceará (CE) and Piauí (PI) are given in Table 2. This table includes species records previously published based on material collected during this project. Previous to this study, there were no records of Elmidae, Epimetopidae, and Torridincolidae (Coleoptera), Leptophlebiidae (Ephemeroptera), Gelastocoridae, Naucoridae, and Pleidae (Hemiptera), and Ecnomidae, Polycentropodidae, and Xyphocentronidae (Trichoptera) for these Brazilian states. Part of distributional data were initially compiled based on available information at Moreira et al. (2011), Moreira (2016), , and . Curiously, the first record of an aquatic insect from either state was of Nephepeltia phryne from Piauí described by Perty (1834) (Fig. 2) and, amazingly, a second dragonfly species was only recorded to this state after 160 years in 1994. Map of Brazilian states colored by four major phytogeographical domains: Amazon forest, Cerrado, Atlantic forest, and Caatinga; the last one including Ubajara (blue star) and Sete Cidades (green star) National Parks. Table 2.
Species list of Coleoptera (Hydrophilidae), Ephemeroptera, Hemiptera (Gerromorpha and Nepomorpha), Odonata, and Trichoptera recorded from Ceará (CE) and Piauí (PI) states. Species marked with a "#" were described or firstly recorded to these states based on material sampled in this project.
Aquatic Insects from the Caatinga: checklists and diversity assessments ...  Takiya D et al. In this paper, we provide a preliminary checklist of selected taxa of aquatic insects from Ubajara and Sete Cidades National Parks in Northeastern Brazil ( Fig. 1), an undersampled region in terms of biological inventories. Additionally, species richness was compared between the two National parks. As far as we know, this is the first published aquatic insect inventory of the selected National Parks.

Focal taxa of aquatic insects
Identification of aquatic insects depended on the availability of specialists, therefore we focused on Ephemeroptera; suborders Nepomorpha and Gerromorpha of Hemiptera; families Elmidae, Epimetopidae, Hydrophilidae, and Torridincolidae of Coleoptera; Hemerodromiinae (aquatic Empididae) of Diptera; Odonata; Plecoptera; and Trichoptera. These focal taxa were identified at least in genus level, given that in some cases specieslevel identification was not possible because collected individuals were not adult males (immatures, subimagoes, or adult females), and, in other cases, because of the lack of comprehensive taxonomic revisions for particular genera. Higher-level classification followed the "Catálogo Taxonômico da Fauna do Brasil" , Monné Detail of plate 25 modified from Joseph Anton Maximilian Perty's work from 1834, with a water color illustration of the holotype of the small skimmer dragonfly Libellula phryne (Fig. 3, Odonata: Libellulidae; currently Nephepeltia phryne) described by him from "Provincia Piauhiensi", Brazil. et al. 2016, Pinto 2016, Rafael and Câmara 2016.

Study areas
Material examined in this paper were obtained during two collecting expeditions to the study areas, from April 18 to 21 of 2012 and February 7 to 13 of 2013 at Parque Nacional de Sete Cidades (PNSC, Piracuruca municipality, PI) and from Abril 21 to 25 of 2012 and February 13 to 20 of 2013 at Parque Nacional de Ubajara (PNU, Ubajara municipality, CE). Although both parks are included in the Caatinga Domain ( Fig. 1), areas sampled within these parks seem to represent islands dominated by Cerrado (PNSC) or montane humid forest (PNU). The two parks are distant by approximately 110 km.
Sampling localities within these parks were in or very close (less than 100 m) to bodies of water and are listed in Table 3. Bodies of water ranged from lentic and lotic systems and some streams sampled during the 2012 expedition to PNSC were completely dry in 2013 (see Figs 3,4).
Aquatic Insects from the Caatinga: checklists and diversity assessments ...    Aquatic Insects from the Caatinga: checklists and diversity assessments ...   Suspended intercept trap over stream at Parque Nacional de Ubajara, CE, Brazil.

Figure 15.
Manual collecting using white-sheet light trap at Parque Nacional de Ubajara, CE, Brazil.
Aquatic Insects from the Caatinga: checklists and diversity assessments ...

Data analyses
Species complementarity index for the two National parks were calculated with Cjk = Ujk/ Sjk, where Ujk is the number of unique species in both sites and Sjk total richness in both sites combined (Colwell and Coddington 1994).
During the expeditions 27 samples (14 at PNSC and 13 at PNU) of Pennsylvania light traps placed over streams were collected. Each sample was the result of an approximately 6-8 hour effort of 15W fluorescent or UV light turned on at dusk. All individuals of Ephemeroptera, Plecoptera, Trichoptera, and Hydrophilidae (Coleoptera) were identified or morphotyped and counted. Adult females or subimagoes impossible to be identified into species level were treated as conspecific as males identified of the same genus on the sample (6 morphotypes from PNSC and 8 morphotypes from PNU of Ephemeroptera and Trichoptera). However, in cases where more than one species of the same genus was identified from the same sample (Helicopsyche and Oxyethira from PNU and Chimarra, Neotrichia, Smicridea, and Oxyethira from PNSC), the number of female individuals were equally divided among different species.
Quantitative samples of Pennsylvania light traps totalled 227 individuals of 23 species from PNU and 511 individuals of 54 species from PNSC of Ephemeroptera, Plecoptera, Trichoptera and Hydrophilidae (Coleoptera). Quantitative data served for comparisons of species richness between the two National Parks based on a rarefaction curve by individuals calculated in PAST 3.0 (Hammer et al. 2001).

Data resources Data for species checklists of Parque Nacional de Ubajara (PNU) e Parque Nacional de Sete Cidades (PNSC)
Approximately 7,000 individuals of focal taxa were identified, being 5,472 from PNU and 1,539 from PNSC (Fig. 17).
These individuals were identified into 96 species from PNU and 112 species from PNSC, while 20 of these species were found in both parks (Fig. 18). Species complementarity between both parks was of 89%.
The number of species per insect order in PNU and PNSC, respectively were: Coleoptera, 16 and 20; Diptera 10 and 1; Ephemeroptera, 1 and 9; Hemiptera, 9 and 20; Odonata, 21 and 21; Plecoptera, 1 and 1; and Trichoptera, 38 and 40. Species checklists for both National Parks are given below. Species marked with an asterisk (*) were found in both National Parks and distributional records (country or state) marked with and exclamation mark (!) are new records published herein. Species described or first taxa records based on material collected during this project are cited under Notes. Number of individuals of aquatic insects identified from Ubajara (PNU, blue) and Sete Cidades (PNSC, green) National Parks.
Aquatic Insects from the Caatinga: checklists and diversity assessments ...  Lateral habitus of male holotype of Hemerodromia brevicercata collected at PNU-07 (CZMA), species described based on material collected during this project.  Lateral habitus of male holotype of Hemerodromia mourai collected at PNU-07 (CZMA), species described based on material collected during this project.

Genus Metachela Coquillett, 1903
Notes: New genus record for CE.  Lateral habitus of male holotype of Hemerodromia ubajaraensis collected at PNU-07 (CZMA), species described based on material collected during this project.

Genus Neoplasta Coquillett, 1895
Notes: New genus record for CE.  Teneral adult specimen of Anacroneuria calori collected at PNU-02. This species was also recorded from PNSC, representing the first record of Plecoptera for Piauí.   diagonal vegetation, including currently the Cerrado and Chaco formations, or during the Plio-Pleistocene through forested areas in the Caatinga Domain (see references in Batalha-Filho et al. 2013). Furthermore, wet period intervals every 20,000-200,000 years during at least 2 million years created intermittent corridors of between forested areas in Brazil (Wang et al. 2004) and can explain the mixing of fauna among Amazonia-Caatinga-Atlantic Forest. At least the PNU can be considered an island of humid forest surrounded by savannah-like formation and studies focusing the aquatic insect assemblages can strongly help understand the spatial evolution of these forested patches in the Northeastern Brazil and past connections between the two largest tropical forest domains in South America.

New distributional records and notes on species records
Based on the collected material during this project, one caddisfly species was firstly recorded from Brazil, Phylloicus pirapo (Calamoceratidae) previously known from Argentina and Paraguay. Eighteen species collected at PNU and 21 at PNSC (5 species shared between parks) represent their first record for Northeastern Brazil.
Several new state records are made based on this material, especially for Piauí State. Thirty and 56 species are firstly recorded from Ceará and Piauí states, respectively. These exclude records previously published, but based on material collected during this project, which add other 10 new species records for these states (see Table 2). Herein, it is also recorded 25 and 47 new genera and 9 and 14 aquatic insect families from Ceará and Piauí states, respectively.
Some of these new records are for widespread species in South America, such as for many dragonflies (see below), however, others significantly expand species ranges in Brazil. For example, the caddisflies Helicopsyche monda (Helicopsychidae) and Chimarra calori (Philopotamidae) previously known from Southeastern and/or Southern Brazil have their ranges expanded for over 1,000 km.
The knowledge of stoneflies from Northeastern Brazil is still very scarce, when compared to the other aquatic insects studied. In the Neotropical Plecoptera catalogue, only two species, Anacroneuria lacunosa (Navás, 1926) and A. parilobata Klapálek, 1922, from this Brazilian Region was recorded (Froehlich 2010), both from Bahia State. In the last ten years, following an increase of local taxonomists and inventories, species number boosted from two to 27 stoneflies (Lecci and Froehlich 2011, Righi-Cavallaro et al. 2013, Duarte and Lecci 2014, Duarte and Lecci 2016. However, most sampling localities are still concentrated in some regions of Bahia State. Nevertheless, stonefly diversity still seems higher in the Atlantic forest, than in the Caatinga. A single Anacroneuria species has been recently described fom PNU (Duarte and Lecci 2016) and was recorded herein from both National parks, thus representing the first record of Plecoptera from Piauí State.
Except by few Amazonian and Atlantic Forest representatives, most dragonflies correspond to common species and are now firstly recorded mainly due to undersampling. Thus, field surveys must be one of the priority efforts for assessment of the diverse dragonfly fauna of tropical South America (e.g., Pinto and Lamas 2010). Amongst the new records, the known distribution of Acanthagrion jessei (Coenagrionidae) was extended considerably from previous localities at Brazilian Amazonia and Pantanal. Another unexpected occurrence is of the South American emerald Neocordulia setifera (Anisoptera, incertae sedis), a species apparently confined to ombrophilous forested areas in the Atlantic Forest Domain with several misidentified specimens cited in the literature, including records from Brazil (MT, GO, MG), and Ecuador (APP, in prep.). Other specimens need further studies, such as, a possible new species of the Oxyagrion basale-group (Coenagrionidae) from PNSC; a single female with mesostigmal plate and mesepisternal fossae similar to that of the Central American Acanthagrion quadratum (not a well preserved specimen) from PNU; and specimens of Argia, a genus of difficult species identification, which are broken or smashed, thus were determined doubtfully ("cf."). Specimens from PNU of the Amazonian Castoraeschna corbeti (Aeshnidae) and Hetaerina indeprensa (Calopterygidae), species previously only known from their type localities in Pará State (Brazil) are slightly distinct from typical specimens and need further studies to investigate if they only represent geographical variation.
Several published records of dragonfly species from the states of CE and PI are old, based on misidentifications or wrong localities, or for names currently under a different taxonomic status, and as a result, some of them should be ignored or are pending confirmation. Such cases are discussed below.
The Amazonian damselflies Mnesarete cupraea (Selys, 1853) and Metaleptobasis bicornis (Selys, 1877) were recorded from Ceará State (Garrison 2006: 21, von Ellenrieder 2013: 20; respectively) based on a misinterpretation of the locality of "Canindé" on the Rio Gurupi Basin at the border of Pará and Maranhão states (see Pinto and Lamas 2011). The occurrence of M. cupraea in Ceará was recently proven to be true for Serra da Ibiapaba (  Table 2).
Belle 1983: 170-171), in his revision of Zonophora, provided a map where Zonophora calippus calippus Selys, 1869 and Zonophora batesi Selys, 1869 are apparently recorded from Piauí State, however it is clear that their location was based on the material from Maranhão cited by Belle 1972: 236-236). This mistake was reproduced by Garrison et al. 2006: 131) in their thumbnail map. Additionally, several other thumbnail maps for genera (Garrison et al. 2006) show ranges of distribution in both Ceará and Piauí States (e.g., Phyllogomphoides, Aeschnosoma, and Ypiranthemis), however, we have not located references for these records and they should be considered potential distributions rather than actual occurrences. Even considering that species of some of these genera are common and widespread in South America, they are pending confirmation based on voucher specimens.
In the first published list of dragonflies from Ceará State, Navás (1924) cited currently considered dubious or questionable names due to changes in species concepts and very likely also based on misidentifications. These species were not included in Table 2. Navás (1924) cited Erythrodiplax connata (Burmeister, 1839), which likely refers to E. fusca since the former is restricted to Chile (Paulson 2003). Erythrodiplax nigricans was mentioned dubiously in the generic revision by Borror (1942), and based on its distribution in southern South America with the northernmost record from Rio de Janeiro State (Anjos- Santos and Costa 2006), it seems unlikely that it occurs in Northeastern Brazil. Three other species recorded by Navás (1924), Micrathyria eximia Kirby, 1897, Orthemis ferruginea (Fabricius, 1775, and Perithemis domitia (Drury, 1773), are very likely misidentifications. While reviewing M. eximia, Westfall (1992) observed that almost all specimens identified as this species were misidentified, including most Brazilian ones, as they indeed correspond to four species. Orthemis ferruginea is a largely North and Central American species with southernmost records to Costa Rica (Donnelly 1995), and its occurrence in South America is very unlikely. Material in which this record was based represent at least five species of the O. ferruginea group (see Pinto 2010). Finally, P. domitia is a Caribbean and Central America species with southernmost records in Venezuela and Colombia. Costa et al. (2006) considered all records of the latter species from Brazil as records of P. mooma and we agree with these authors.

Increase of the known aquatic insect diversity of Ceará and Piauí states
Besides the high number of taxa recorded for the first time from Ceará and Piauí, effectively increasing the knowledge of aquatic insect diversity for these states, several undescribed species were detected. Twenty-six and 20 undescribed species from PNU and PNSC, respectively, were detected based on the material collected during this project, of those 12 from PNU (  Number of previously recorded species of Trichoptera, Odonata, Hemiptera, Ephemeroptera, and Hydrophilidae (Coleoptera) for Ceará (blue) and Piauí (green). Dark blue or green represent the number of previously recorded species based on the literature. Light blue and green represent the number of species recorded for the first time in its respective state based on material collected at Ubajara (CE) and Sete Cidades (PI) National Parks. Number of undescribed species collected in these parks are given in red.
Many more aquatic insect species (except of Ephemeroptera) have been recorded from Ceará than Piauí (see Table 2). Our results represent an increase of approximately 16% in the number of known species for Ceará State, except for Trichoptera (Fig. 29). Caddisflies (the most diverse of groups sampled) seem to be understudied in both Brazilian states, with our sampling including a high proportion of species still to be described and results representing an increase of approximately 70% in the number of species known for Ceará and of 91% for Piauí. This increase for Piauí State is especially evident in other groups, such as, for Coleoptera, Ephemeroptera, and Hemiptera, which increased in approximately 51% of known species. This increase is even higher (86%) for dragonflies (Odonata) in Piauí, which is surprising given that they are possibly the most well-studied of focal groups.

Species richness comparison between Parque Nacional de Ubajara (PNU) and Parque Nacional de Sete Cidades (PNSC)
There are no published lists of insect species for neither Parque Nacional de Ubajara (PNU) nor Parque Nacional de Sete Cidades (PNSC). In PNU's management plan it is cited the occurrence of five orders and 14 insect families, with 6 genera and 9 species identified. However, these names were not made available. In another study, Silva and Ferreira (2009) list 26 families of 9 insect orders, including the identification solely of the genera Conicera (Phoridae), Lutzomyia (Psychodidae), and Endecous (Phalangopsidae), as part of a cave invertebrate inventory of PNU. The only insect faunal study published involving the two parks is a list of Lutzomyia (Diptera: Psychodidae) species by Martins et al. (1989), with five species occurring at PNU and seven species ate PNSC, while only Lutzomyia ( L.) longipalpis (Lutz & Neiva, 1912) occurred in both parks. Thus, this preliminary list of aquatic insect taxa already represents a good sampling of insect diversity for these parks and a baseline for further monitoring and conservation strategies of freshwater macroinvertebrate fauna.
Considering all focal taxa, only 11% of species were found in both National Parks (Fig. 18), their species composition displaying very high complementarity (89% species). Although both parks are relatively close to eachother and within the Caatinga Domain, they drastically differ in phytophysiography. Specifically in the case of aquatic insects, the low complementary is more probably explained by the structural differences of water bodies sampled available in the different parks. At PNSC most part of aquatic insects (67 species) were collected at Cachoeira do Riachão (Fig. 3), a (supposedly) permanent stream with broad humid gallery forest and high diversity of microhabitats (sand, litter, and rocks), and in some temporary streams in open savannah vegetation (Fig. 4), which were partially dry during the second expedition and with lentic characteristics. The majority of water bodies sampled at PNU were very homogeneous, bedrock rapid streams and low diversity of microhabitats.
Although for some groups, e.g. Trichoptera, the number of species collected in each National Park was similar, rarefaction curves based on individuals sampled (Fig. 30) surprisingly suggest much higher expected richness of aquatic insect species at PNSC than at PNU, thus much more sampling is needed at PNSC to have a better estimate of total species richness. This is certainly the result of a higher range of aquatic microhabitats sampled at PNSC, as discussed above. However, it is still surprising that such a high diversity was found at PNSC in this study, given that the second expedition to these parks was conducted at the start of the rainy season, when some bodies of water sampled in the first expedition to PNSC (e.g., stream below Cachoeira do Riachão) were completely dry and resulted in the collection of a low number of individuals. Insect abundances in general seem to conspicuously peak during the rainy season and follow a very strong seasonality in Caatinga areas (Vasconcellos et al. 2010), which probably affected our effective sampling of a much higher richness from PNSC.