Ichthyofauna of the humid forest enclaves in the tablelands of Ibiapaba and Araripe , Northeastern Brazil

Humid highland forest enclaves are remnants of Atlantic Forest found in tablelands within the Caatinga biome (Northeastern Brazil), which emerged during interglacial periods in the Pleistocene. These ecosystems have a highly diverse and endemic fish fauna. Most earlier surveys have focused on the tableland of Borborema (Pernambuco and Paraíba States). In this study we surveyed the fish fauna of the humid forest enclaves in the tablelands of Ibiapaba and Araripe, based on samples collected in the rainy season (March and April) between 2009 and 2014. The 45 sampling points covered rivers, streams and reservoirs in five river basins belonging to three ecoregions. The species were listed according to drainage divide, and endemism was determined for each ecoregion and for the Caatinga. Our area was more species-rich (n=59) than Borborema (n=27). The samples included five introduced species and 29 species endemic to the Caatinga (49.1% of the sampled species). The distribution of Parotocinclus haroldoi was expanded to the Mid-Northeastern Caatinga ecoregion (Timonha river basin, Ceará State). Our study intends to make a significant contribution to current knowledge of the ichthyofauna in humid highland forest enclaves of semiarid Northeastern Brazil, identified as a priority in the conservation of the biodiversity in the Caatinga.


Introduction
The Brazilian territory may be divided into six large morphoclimatic zones, each with its own climatic, pedological, hydrological and phytogeographic characteristics (Ab'Sáber 2003).One of these, the Caatinga, a predominantly Northeast Brazilian biome, is characterized by a semiarid climate with a relatively short rainy season (four months) of sporadic and unevenly distributed rainfalls.Due to the paucity of rain (240-800 mm annually) and high evaporation rate (Tabarelli & Santos 2004), most aquatic systems are intermittent.This probably results in a smaller fish diversity than that observed in other tropical aquatic systems (Medeiros & Maltchik 2001).However, the Caatinga features minor contrasting areas, such as humid highland forest enclaves locally referred to as 'brejos de altitude ' (Ab'Sáber 2003).Acting as drainage divides between the main hydrographic ecoregions of Northeastern Brazil (Maranhão-Piauí, Mid-Northeastern Caatinga, São Francisco and Northeastern Atlantic Forest), these highland enclaves receive more rain than the surrounding Caatinga due to orographic rainfalls, favoring the maintenance of aquatic systems throughout the year.Moreover, the expansion and posterior recession of the Atlantic and Amazon forest in Northeastern Brazil due to climate changes in the Pleistocene (Andrade-Lima 1982, Santos et al. 2007) resulted in the emergence of unique ecosystems with high levels of diversity and endemism, which serve as refuges for regional fauna and flora (Andrade-Lima 1982).
Unfortunately, little is known about the aquatic biota of the Brazilian semiarid region and how fish assemblages and richness are impacted by environmental degradation and the introduction of exotic species (Santos et al. 2011, Botero et al. 2014).In addition, efforts at freshwater fish conservation have been feeble at best (Lévêque et al. 2008, Abell et al. 2008).Fish fauna surveys not only help define biogeographic regions, but also provide important subsidies for environmental policy decisions (especially with regard to the establishment and effectiveness of conservation areas) and serve as an important first step for research in related fields (Albert et al. 2011).Rosa & Groth (2004) published the first comprehensive study on fish assemblages in humid highland forest enclaves.The study covered the Borborema tableland which drains into the Paraíba do Norte and Mamanguape river basins (Paraíba State) and the Ipojuca river basin (Pernambuco State) located in the eastern part of the Mid-Northeastern Caatinga ecoregion.Other initiatives, such as the PROBIO Project for Conservation and Sustainable Use of Brazilian Biological Diversity (Projeto de Conservação e Utilização Sustentável da Diversidade Biológica Brasileira) and the PPBio Program for Research in Biodiversity (Programa de Pesquisa em Biodiversidade), are helping expand current knowledge on fish diversity in the region.In addition, Ramos et al. (2014) recently evaluated the richness of the ichthyofauna of the Parnaíba river basin (a semiarid region shared by Ceará, Piauí and Maranhão States) and identified 146 species of freshwater fishes, 54 (36.9%) of which were endemic to the basin.Their survey added significantly to the list of 95 species of Albert et al. (2011) for the Maranhão-Piauí ecoregion, highlighting the need for additional inventories.Nevertheless, many gaps remain in the knowledge of the ichthyofauna of the São Francisco and Mid-Northeastern Caatinga ecoregions, especially with regard to humid forest enclaves (Rosa & Groth 2004, Langeani et al. 2009).Thus, the purpose of this study was to provide a list of fish species from forest enclaves and streams in the tablelands of Ibiapaba (between Piauí and Ceará States) and Araripe (between Ceará and Pernambuco States) which drain into the Parnaíba, Coreaú, Timonha, Jaguaribe and São Francisco river basins.

Study area
The surveys were conducted in humid forest enclaves in two tablelands, Ibiapaba and Araripe, which act as drainage divides between the Maranhão-Piauí, São Francisco and Mid-Northeastern Caatinga ecoregions (Rosa et al. 2003, Albert et al. 2011) (Figure 1).The two tablelands make up the Araripe-Ibiapaba complex, which extends along the confines from Northwestern Ceará to Northeastern Piauí and from Southern Ceará to Central Piauí.The complex displays great altitude variations between the highlands and the central lowlands (depressão sertaneja).In the highlands, soils (latosols) tend to be deep, sandy and poor, and surface water is scarce.In Ibiapaba, water infiltrating the soil drains mainly towards Piauí State.In Araripe, water drains towards Ceará State.
Araripe and Ibiapaba have a maximum elevation of 900-1,000 m (Claudino-Sales & Lira 2011), average rainfalls of 1,000 mm in the rainy season (Sá et al. 2004) and perennial or intermittent streams.The humid forests of Ibiapaba drain westward into the Parnaíba basin (Maranhão-Piauí) in Piauí and eastward into the Coreaú basin (Mid-Northeastern Caatinga) in Ceará, whereas Araripe drains northward into the Jaguaribe basin (Mid-Northeastern Caatinga) in Ceará and southward into the São Francisco basin (Rosa et al. 2003) in Pernambuco State (Figure 1).
The eastern slope of the Ibiapaba tableland intercepts the humid coastal wind producing orographic rainfalls and making this region the wettest (mean annual rainfall: ~1000 mm) and coolest (mean annual temperature: 22-26°C) in Ceará.On the other hand, Araripe has 8,000 km 2 of highland forest and elevations up to 1,000 m (Köppen type BSh'), with mean annual temperatures around 25ºC (MME 1996, SRH 2005).These enclaves were previously considered a remnant of the Atlantic Forest (due to the geographic proximity), but recent studies have shown the flora to be more akin to that of the Amazon Forest (Santos et al. 2007).

Sampling
Fish were sampled in the rainy season (March-April) during six surveys from 2009 to 2014, covering 45 sampling points-24 in Araripe and 21 in Ibiapaba (Table 1, Figure 2).The sampling sites included first to third-order rivers (n=9), streams (n=27) and small reservoirs (n=9) (100-1,000 m 2 ).The sampling points in Araripe were located within the Jaguaribe river basin (n=7) and the São Francisco river basin (n=17), while the sampling points in Ibiapaba were located within the Coreaú river basin (n=12), the Parnaíba river basin (n=8) and the Timonha river basin (n=1) (Table 1).Each sampling site was georeferenced using a portable GPS and later plotted on a map to avoid errors of attribution in areas near drainage divides.Using the definition of Rosa et al. (2003), only species restricted to a single ecoregion (Albert et al. 2011) were considered endemic.
Seventeen of the 45 sampling points were located inside conservation units.Thus, seven of the sampling points in the Jaguaribe river basin and one in the São Francisco river basin were located inside the Chapada do Araripe Environmental Protection Area (EPA) (1,063,000 ha).In Ibiapaba, one sampling point in the Timonha river basin was located in the Serra da Ibiapaba EPA microbacia do rio Timonha, no Estado do Ceará.Este estudo pretende contribuir com informações inéditas para o conhecimento ictiofaunístico dos ecossistemas aquáticos dos brejos de alitude do semiárido brasileiro, apontadas como prioritárias para conservação da biodiversidade da Caatinga.
(1,592,550 ha) and eight sampling points in the Coreaú river basin were located in the Ubajara National Park (NP) (6,271 ha).
The fish were captured with casting nets (5.3 m 2 ; 14 mm between opposing knots), sieves (0.7 m 2 ; 1 mm between opposing knots) and seines (1.3 m 2 ; 2 mm between opposing knots) in all accessible habitats (aquatic macrophytes, ponds, pools, rapids and waterfalls) with a fishing effort of four man-hours, under licenses (#26174-2, #32656 and #32921-4) issued by the Ministry of the Environment (MMA) and the Chico Mendes Institute of Biodiversity Conservation (ICMBio).The ichthyological material was deposited in the fish collection of the Universidade Federal do Rio Grande do Norte (UFRN) and the Universidade Federal da Paraíba (UFPB).Vouchers for each species are included in the appendix.

Ichthyofauna and endemism
Fifty-nine fish species, belonging to 38 genera, 16 families and five orders, were identified in our samples from the two tablelands (Table 2).This is more than twice the number of species ( 27) reported by Rosa & Groth (2004) for nine humid forest enclaves in the tableland of Borborema (Mid-Northeastern Caatinga ecoregion).As pointed out by the authors, the low diversity observed in that study, when compared to that of larger regional river basins, may be the result of sampling or logistic limitations.We do not intend to have fully overcome the difficulties described over a decade ago (for example, not all stretches of the sampled tributaries were accessible due to steep banks, dense riparian vegetation and fast-flowing waters), but with the help of new research teams from several universities in semiarid Northeastern Brazil and taxonomic advances, we believe to have produced a comprehensive and fairly accurate list of the fish species in these ecosystems.
Current knowledge of fish diversity and endemicity in the Caatinga is mainly based on surveys conducted in the largest basins of Northeastern Brazil (Rosa et al. 2003, Rosa & Groth 2004).Miranda-Ribeiro (1937) were the first to describe the fish fauna of humid highland forests in the region (Granjeiro river basin, Araripe).Nijssen and Isbrüker (1976) identified species of Aspidoras in highland streams in Northeastern Brazil (mostly in Ceará).More recently, Rosa & Groth (2004) published a seminal study on humid highland forest fish fauna, with emphasis on the question of endemicity and the urgent need for conservation.
In addition to harboring a large number of fishes of the Caatinga (~56% endemicity), humid forest enclaves play a crucial role in the maintenance and conservation of the regional ichthyofauna (Rosa & Groth 2004).In this study, the most species-rich river basin was Parnaíba (n=26), followed by São Francisco (n=24), Jaguaribe (n=20), Coreaú (n=16) and Timonha (n=11) (Table 2).When analyzed according to ecoregion, Jaguaribe and Parnaíba both yielded five endemic species, followed by São Francisco (n=4), Coreaú (n=1) and Timonha (n=0) (Figure 3).The introduced species registered in this study (Cichla sp., Coptodon rendalli, Oreochromis niloticus, Poecilia reticulata and Xiphophorus helleri) (Table 2) have a potentially negative impact on native fish diversity mainly through taxonomic homogenization of assemblages and species extinction (Vitule et al. 2009, Villéger et al. 2014).The introduced species (except the last one) were also observed by Rosa & Groth (2004) in the humid forest enclaves of Borborema.The introduction of species into humid forest enclaves in Northeastern Brazil is of particular concern in view of the high level of endemism, the scarcity of information and related anthropic impacts (e.g., removal of riparian vegetation, building of reservoirs and use of agricultural pesticides) (Rosa & Groth 2004).For example, due to the predominance of small fishes in the local assemblage, the abundance and wide distribution of P. reticulata may lead to the competitive exclusion of native species, especially poeciliids (Rosa & Groth 2004), as Poecilia sp., observed in the Timonha river basin.

Expansion of distribution
In this study, Parotocinclus haroldoi is for the first time reported for the Mid-Northeastern Caatinga ecoregion based on individuals captured in Passagem, a stream in the Timonha river basin (Granja, Ceará State).A small detritivorous catfish, P. haroldoi lives in small groups, with a preference for shallow streams with clear or slightly turbid water and a substratum of rocks, twigs, sand and mud.The present report expands the distribution of the species, previously considered endemic to the Maranhão-Piauí ecoregion (Ramos et al. 2014), although the river mouth of the Timonha basin is close to the small coastal basins of the Maranhão-Piauí ecoregion (Figure 1).The occurrence of the species in this stream may be explained by the geomorphological slope northwest of Ibiapaba, which may have formed as a result of headwater capture during intense neotectonic activity in the region (Claudino-Sales & Lira 2011) or during periods of marine regression in the Pleistocene when the basins were connected.The new occurrence of Poeciliidae (Poecilia sp.) was registered in the only basin (Timonha) where the exotic species P. reticulata was not observed.Despite the limited sampling in this basin (a single point), 11 species were registered, three (27.2%) of which endemic to the Caatinga (Table 2).

Conservation perspectives
Approximately 38% (n=17) of the sampling points were located inside conservation units (Table 1).These points accounted for 45.7% (n=27) of the captured species.Eleven of these species (37.9%) were considered endemic to the Caatinga (Table 3).Chapada do Araripe EPA harbored the greatest number of species (n=20), corresponding to 51.5% of all non-introduced species registered in Araripe, nine (45.0%) of which were endemic to the Caatinga.The two CUs in Ibiapaba accounted for 16 species (48.4% of all non-introduced species registered in Ibiapaba), six (11.1%) of which were endemic to the Caatinga.More specifically, the Serra da Ibiapaba EPA yielded 11 species, of which four were endemic and seven were native (none were introduced), whereas the Ubajara NP yielded nine species, of which four were endemic, four were native and one was introduced (Table 3).
Interestingly, seven of the endemic (Caatinga) species captured in the three conservation units were observed in one unit only (in Chapada do Araripe EPA = Aspidoras menezesi, Hypostomus carvalhoi, Hypostomus jaguaribensis, Parotocinclus jumbo and Trachycorystes cf.cratensis; in Ubajara NP = Aspidoras spilotus; in Serra da Ibiapaba EPA = Parotocinclus haroldoi), while only two species occurred in all three units: Characidium bimaculatum and Cichlasoma orientale (Table 3).In general, the conservation units in the study area protected a relatively small proportion of the total number of species, and even fewer endemic species, whereas more than 60% of the introduced species were observed at sampling points inside the units (Table 3).The low representativeness of native and endemic species inside these units may be explained by inadequate CU design: most of the headwaters streams which flow through the units are located in urbanized areas where they are exposed to adverse environmental impacts (removal of riparian vegetation, contamination with agricultural pesticides and fertilizers, etc.) and possibly the introduction of non-native species (Blackburn et al. 2015).
The highland forest enclaves of Northeastern Brazil not only represent important remnants of rain forest (Tabarelli et al. 2005, Santos et al. 2007), but boast a highly endemic fauna and flora.The enclaves in Borborema (Pernambuco and Paraíba) have been comprehensively surveyed, revealing high levels of endemism for bromeliads (33% in a single enclave), birds (13%) and mammals (7%) (Siqueira-Filho 2004, Souza et al. 2004).Some of these species have a limited geographical distribution and are endemic to the Caatinga, making them more vulnerable to extinction, especially when populations are small (Gaston et al. 1998).The swift and relentless degradation of the Caatinga and the processes of desertification and climate change which threaten the local biodiversity highlight the need for greater efforts at protecting both terrestrial and aquatic ecosystems (Maltchik & Medeiros 2012).
The present study provides new information on the fish assemblages of humid highland forest enclaves in two tablelands (Araripe and Ibiapaba) in semiarid Northeastern Brazil which serve as drainage divides between the ecoregions Maranhão-Piauí (Parnaíba river basin), Mid-Northeastern Caatinga (Timonha, Coreaú and Jaguaribe river basins) and São Francisco.Nearly half the sampled species (29/59) were considered endemic to the Caatinga, and five were introduced.Only 11 of the species endemic to the Caatinga were captured in conservation units, but it should be kept in mind that the study was not specifically designed to evaluate the diversity of these units (with the exception of Ubajara NP).Most sampling points inside the units were located in basins of the Mid-Northeastern Caatinga ecoregion (n=16; 94.1%).Thus, further studies are necessary to determine the ability of these units to protect the fish fauna of the Caatinga, especially in the São Francisco and Parnaíba river basins.
In addition, the distribution of P. haroldoi was expanded to include the Timonha river basin in the westernmost reaches of the Mid-Northeastern Caatinga ecoregion.The fact that all samplings were carried out in the rainy season leaves unanswered questions about the impact of drought periods on the dynamics of the fish fauna in these ecosystems.According to Rosa & Groth (2004), humid highland forest enclaves serve as permanent refuges.Future research may shed light on the role of these ecosystems in the maintenance of the local and regional fish fauna.
The diversity of endemic species and the singularity of these highland enclaves justify the creation of new conservation units (or the expansion of existing ones) in order to include important areas of aquatic ecosystems, such as riverheads, thereby reducing upstream anthropic impacts.
The present study provides new taxonomic information to subsidize future investigations into such fields as biogeography, ecology, conservation, bioinvasion and macroecology, and evidences the need for greater efforts to protect the highly endemic fish fauna of the highland forest enclaves of Northeastern Brazil.
Table 3 .Total number of endemic, native and introduced species of the Caatinga sampled in the tablelands of Araripe and Ibiapaba and in the three conservation units (CU) (1=Chapada do Araripe EPA; 2=Ubajara NP; 3=Serra da Ibiapaba EPA), with an indication of the number of units in which each was observed. Total