Abstract
The humid forest zones of northeastern Brazil are recognized as endemic hotspots for pseudothelphusid crabs. In this study, we report new occurrence records of the pseudothelphusids, Fredius ibiapaba and Kingsleya attenboroughi, in humid soil and streams within humid forests of the semi-arid region of northeastern Brazil. These new records expand the geographical distribution of these crabs, highlighting their potential to inhabit humid forests throughout this region. Furthermore, this information indicates that these crabs, especially K. attenboroughi, are not confined to slopes and patches of humid forests in highland swamps but can also extend to springs in other areas of the Brazilian semi-arid region.
Keywords Freshwater crabs; Endemic species; Humid forest Brazilian semi-arid; Neotropical crabs
INTRODUCTION
Pseudothelphusidae Ortmann, 1893, comprises a family of freshwater crabs widely distributed throughout the Neotropical region, typically associated with mountainous environments ranging in altitude from 300 to 3,000 meters (Rodríguez & Magalhães, 2005; Acevedo-Alonso & Cumberlidge, 2021). With an estimated 290 species, these crabs inhabit a wide variety of habitats, such as rivers, streams, lakes, swamps, waterfalls, and caves (Magalhães & Türkay, 2010). In Brazil, the majority of pseudothelphusid species are concentrated in the northern region, primarily within the Amazon basin (Magalhães, 2003, 2016; Cumberlidge et al., 2014).
However, recent studies conducted in northeastern Brazil have revealed that the Pseudothelphusidae fauna in this region is underestimated (Pinheiro & Santana, 2016; Pralon et al., 2020; Santos et al., 2020a). Additionally, geographic distribution studies and descriptions of new species have expanded the eastern limits of pseudothelphusid distribution into the states of Ceará (Magalhães et al., 2005; Pinheiro & Santana, 2016; Santos et al., 2020a) and Piauí (Pralon et al., 2020).
Similar to other pseudothelphusid crabs, the species described from northeastern Brazil exhibit restricted distributions and a high degree of endemism. Currently, Kingsleya attenboroughi Pinheiro & Santana, 2016 and Fredius ibiapaba Santos, Tavares, Silva, Cervini, Pinheiro & Santana, 2020 are found in limited areas along the eastern portions of the Chapada do Araripe and Serra da Ibiapaba, respectively (Pinheiro & Santana, 2016; Santos et al., 2020a, b; Araújo et al., 2022), with the exception of a recent record suggesting the probable occurrence of F. ibiapaba in Bragança, Pará (Mantelatto et al., 2022). Furthermore, Kingsleya parnaiba Pralon, Pinheiro & Santana, 2020 has been recorded only at its type locality (Pralon et al., 2020).
The restricted geographic distribution and anthropogenic pressures indicate a favorable scenario for the extinction of freshwater crab species (Vogt, 2013; Magalhães, 2016). Dalu et al. (2017) suggest that establishing the actual distribution area of a species is crucial for conservation actions. Therefore, the present study reports new occurrence records of Pseudothelphusidae freshwater crabs in the semi-arid region of northeastern Brazil, thereby expanding their distributional range.
MATERIAL AND METHODS
Sampling was carried out between June 2021 and November 2022 in poorly explored humid forest areas located in the states of Ceará and Piauí, in the semi-arid region of northeastern Brazil. These two states were explored due to previous records of pseudothelphusid species (Magalhães et al., 2005; Pinheiro & Santana, 2016; Pralon et al., 2020; Santos et al., 2020a, b; Araújo et al., 2022) and the presence of humid forest areas that have been under-explored for freshwater crabs.
During field sampling, crab specimens were collected during the day using the active search method, inspecting small streams on humid forest slopes, as well as soils with litter, characteristic environments where Pseudothelphusidae occur in northeastern Brazil (Magalhães et al., 2005; Pinheiro & Santana, 2016; Pralon et al., 2020; Santos et al., 2020a, b). The sex was determined by the presence (males) or absence (females) of gonopods, according to Magalhães (2003). Subsequently, the crabs were individually placed in plastic containers and euthanized by cooling on crushed ice. Then, we packed the crabs in a thermal box and transported them to the Laboratório de Crustáceos do Semiárido (LACRUSE) at the Universidade Regional do Cariri (URCA), in the municipality of Crato, Ceará, Brazil.
In the laboratory, the specimens were identified as Fredius ibiapaba and Kingsleya attenboroughi according to Santos et al. (2020a) and Pinheiro & Santana (2016), respectively, based on the morphology of male gonopods (Figs. 1, 2). Subsequently, specimens were measured using a digital caliper (precision of 0.01 mm) for carapace width (CW = distance between the lateral margins of the carapace), pleon width (PW = width of the 4th pleon somite for females and the 3rd for males), and length of the larger propodus (LP = distance between the base and the distal portion of the larger propodus). Finally, specimens were preserved in 70% ethanol and deposited in the LACRUSE carcinological collection.
Right gonopod (G1) of Fredius ibiapaba Santos, Tavares, Silva, Cervini, Pinheiro & Santana (2020) in external, lateral, mesial and pleon views respectively. (A D) Gonopod of F. ibiapaba collected in the Parque Estadual das Carnaúbas in the municipality of Granja (LACRUSE 304); (E H) Gonopod of F. ibiapaba collected at Fonte do Caranguejo in the city of Viçosa do Ceará (LACRUSE 305); (I K) Gonopod of F. ibiapaba collected at sítio Caranguejo in the municipality of Ipu (LACRUSE 151). Scale bar = 2 mm.
Right gonopod (G1) of Kingsleya attenboroughiPinheiro & Santana (2016) (LACRUSE 306) in external, lateral, mesial and pleon views, respectively. (A D) Gonopod of K. attenboroughi collected in the riacho Jacaré, municipality of São João da Canabrava, state of Piauí; (E H) gonopod of K. attenboroughi collected in the district of Arajara, municipality of Barbalha, state of Ceará. Scale bar = 2 mm.
RESULTS
Family Pseudothelphusidae Ortmann, 1893 Subfamily Kingsleyinae Bott, 1970 Genus Fredius Pretzmann, 1967
Fredius ibiapaba Santos, Tavares, Silva, Cervini, Pinheiro & Santana, 2020 (Fig. 1).
New records: BRAZIL - Ceará: Parque Estadual das Carnaúbas, municipality of Granja, district of Timonha; 03°18′14.11″S, 041°09′56.74″W; 760 m altitude; 19.VII.2021; J.G. Araújo, C.A.M. Martins, C.A. Nascimento & P.H.P. Nobre; 2 males e 1 female (LACRUSE 304).
Additional material: Fonte do caranguejo, in the city of Viçosa do Ceará; 03°33′39.35″S, 041°05′14.60″W; 600 m; 20.VII.2021; J.G. Araújo, C.A.M. Martins, C.A. Nascimento & P.H.P. Nobre; 1 male (LACRUSE 305).
Distribution: Brazil, state of Ceará.
Previous records: Planalto da Ibiapaba, municipality of Ipu, state of Ceará, in the following localities: sítio Gameleira (04°17′42.00″S, 040°44′48.00″W), sítio Gameleira Quintal (04°17′042.00″S, 040°44′43.00″W); cachoeira do sítio Ipuçaba (04°17′56.00″S, 040°44′35.00″W); olho d’água do sítio Ipuçaba (04°18′05.00″S, 040°44′43.00″W); olho d’água da Cinta (04°18′34.00″S, 040°44′48.00″W); sítio Caranguejo (04°18′51.00″S, 040°44′48.00″W); Santa Cruz I (04°19′40.00″S, 040°45′09.00″W); Santa Cruz II (04°19′40.00″S, 040°45′09.00″W); olho d’água da Taperinha (04°20′18.00″S, 040°45′23.00″W); riacho da Taperinha (04°20′33.00″S, 040°45′32.00″W); and Santa Luzia (04°22′11.00″S, 040°45′52.00″W) (Santos et al., 2020a). Planalto da Ibiapaba, municipality of Viçosa do Ceará, state of Ceará, fonte do Caranguejo (03°33′43.20″S, 041°5′9.06″W) (Magalhães et al., 2005; Santos et al., 2020a). Municipality of Bragança, state of Pará (Mantelatto et al., 2022).
Remarks: Three specimens of F. ibiapaba were found in Parque Estadual das Carnaúbas inside burrows approximately 50 centimeters deep (Fig. 3A, B), constructed in a small forested area with humid soil at approximately 760 m above sea level (Fig. 3C E). This new occurrence area is approximately 29.9 km north of the nearest recorded occurrence point (Fig. 4B), located at Fonte do Caranguejo in the municipality of Viçosa do Ceará, and approximately 122.17 km north of the type locality at Sítio Santa Cruz, municipality of Ipu. Among the collected specimens, two are males (male 1: CW = 43.42 mm, PW = 13.20 mm, LP = 34.47 mm; male 2: CW = 46.12 mm, PW = 14.24 mm, and LP = 37.55 mm) and one female (CW = 39.66 mm, PW = 17.62 mm, and LP = 29.01 mm) LACRUSE 304 (Fig. 5C, D).
Habitat of Fredius ibiapaba in Parque Estadual das Carnaúbas. (A) Adult of F. ibiapaba; (B) burrow of F. ibiapaba built in moist soil; (C) litter in the soil at the place of occurrence; (D, E) panoramic view of the park.
(A) Distribution of Pseudothelphusidae in northeastern Brazil; (B) previous records and new occurrences of Fredius ibiapaba; (C) previous occurrence of Kingsleya attenboroughi; (D) new occurrence of K. attenboroughi; (E) previous occurrence of Kingsleya parnaiba. (B E) Digital Elevation Model (DEM) showing the altimetry of the Pseldothelphusidae areas of northeastern Brazil (warm colors indicate higher elevations). Map created in Qgis free software 3.16.14.
Dorsal view of specimens of Fredius ibiapaba and Kingsleya attenboroughi. (A) Adult male of K. attenboroughi from riacho Jacaré (LACRUSE 306); (B) adult female K. attenboroughi from riacho Jacaré (LACRUSE 306); (C) adult male of F. ibiapaba from Parque Estadual das Carnaúbas (LACRUSE 304); (D) adult female of F. ibiapaba from Parque Estadual das Carnaúbas (LACRUSE 304); (E) adult male of F. ibiapaba da Fonte do Caranguejo in the municipality of Viçosa do Ceará (LACRUSE 305). Scale bar = 1 cm.
The new site showed few signs of anthropic intervention, with dense vegetation, humid soil rich in organic matter, and well shaded conditions, favoring the occurrence of the species. However, all these factors were present only in a small area, limiting the distribution of specimens around a headwater. Additionally, this area exhibits few signs of anthropic pressures.
At Fonte do Caranguejo, we found only one male specimen LACRUSE 305 (CW = 35.05 mm, AW = 11.34 mm, and LP = 26.64 mm) of F. ibiapaba (Fig. 5E) inside a burrow approximately 40 cm deep (Fig. 5B, C), constructed under rocks in the humid soil of a small forested area around the spring near the rocky wall (Fig. 6A). Due to its proximity to the urban area, the site shows strong evidence of human presence, such as solid waste (Fig. 6D-F).
Habitat of Fredius ibiapaba at Fonte do Caranguejo in the municipality of Viçosa do Ceará. (A) Panoramic view of the place of occurrence; (B) juvenile by F. ibiapaba; (C) burrow of F. ibiapaba built in damp soil; (D, F) traces of strong human presence at Fonte do Caranguejo.
Despite the small number of specimens collected, we observed the presence of several burrows in the humid soil of the visited sites, with openings of various diameters, indicating the presence of other crabs. We also collected some juvenile specimens that were later released.
Genus Kingsleya Ortmann, 1897
Kingsleya attenboroughiPinheiro & Santana, 2016 (Fig. 6).
New record: BRAZIL - Piauí: Riacho Jacaré, municipality of São João da Canabrava; 06°47′5.00″S, 041°22′25.00″W; 346 m altitude; 16.XI.2022; J.G. Araújo, C.A.M. Martins, C.A. Nascimento, W.M. Nascimento, P.H.P. Nobre; 1 male 1 female (LACRUSE 306).
Distribution: Brazil, states of Ceará and Piauí.
Previous records: Chapada do Araripe, municipality of Barbalha, state of Ceará, in the following localities: district of Arajara (07°20′07.60″S, 39°23′58.80″W) and sítio Cocos (07°22′28.30″S, 39°16′21.90″W) (Pinheiro & Santana, 2016). Chapada do Araripe, municipality of Missão Velha, state of Ceará, district of Missão Nova (07°23′27.71″S, 39°12′45.80″W) (Araújo et al., 2022).
Remarks: Two specimens of Kingsleya attenboroughi were found in Riacho Jacaré. The specimens were hidden among leaves and rocks, within water puddles in a small spring area (Fig. 7). This new occurrence area is approximately 227.17 km east of the nearest recorded occurrence point (Fig. 4D), located in the Arajara district, municipality of Barbalha, state of Ceará (Fig. 4C) (Pinheiro & Santana, 2016; Araújo et al., 2022). A male (CW = 56.94 mm, AW = 15.41 mm, LP = 54.25 mm) and a female (CW = 46.09 mm, PW = 24.24 mm, and LP = 31.16 mm; LACRUSE 306) were collected (Fig. 5A, B).
Habitat of Kingsleya attenboroughi in the riacho Jacaré. (A) Stony creek bed; (B, C) vegetation on the banks of the creek; (D, E) small puddles of standing water; (F) panoramic view of the site of occurrence of the K. attenboroughi.
Riacho Jacaré has tall and dense riparian vegetation, making the creek well shaded and rich in organic matter, important factors for the presence of the species. However, the occurrence of K. attenboroughi in Piauí is restricted to a small area of stream sources in the midst of the caatinga, an environmental characteristic of the Brazilian semi-arid region, with several shrubs, twisted trees, and medium-sized trees. This likely contributes to the small population of K. attenboroughi present in this area as it presents a situation sensitive to anthropic pressures.
DISCUSSION
The new records of Fredius ibiapaba and Kingsleya attenboroughi in the semi-arid region of northeastern Brazil presented in this study expand their distributional range. Fredius ibiapaba is found in humid forest enclaves of the Serra da Ibiapaba, in patches of humid soil where they can construct their burrows (Santos et al., 2020a). This type of environment is present in other unexplored locations in the Brazilian semi-arid region, known as humid forests (Ab’Sáber, 1999; Tabarelli & Santos, 2004).
The new occurrence record of F. ibiapaba in Parque Estadual das Carnaúbas, on the northern limit of Serra da Ibiapaba, shares similar characteristics with the previously reported occurrence area by Santos et al. (2020b). Therefore, our results emphasize the importance of forest zones with humid soil for this species. We believe that the actual geographical distribution of F. ibiapaba may be wider than currently known, as such environments are abundant along the eastern slope of Serra da Ibiapaba (Souza & Oliveira, 2006). Additionally, the new occurrence area of F. ibiapaba is highly restricted, indicating a likely small population, making it vulnerable to any environmental disturbance. Thus, the importance and necessity for the conservation of Parque Estadual das Carnaúbas are underscored, as other populations, including the population of Sítio Caranguejo in the municipality of Ipu, occur in areas with significant environmental disturbances (Santos et al., 2020b). Therefore, as well as in other successful examples highlighted by Dalu et al. (2016), the preservation of Parque Estadual das Carnaúbas is crucial for the conservation of the population of F. ibiapaba in the municipality of Granja.
Prior to this study, K. attenboroughi was considered an endemic species of the state of Ceará, occurring only in the narrow strip of humid forest on the slopes of Chapada do Araripe (Pinheiro & Santana, 2016; Araújo et al., 2022), with a strong association with areas near springs, always found in shaded streams with clear water, rich in organic matter and rocks (Pinheiro & Santana, 2016; Lima, 2018; Araújo et al., 2022). However, the records presented here reveal a new occurrence of K. attenboroughi in a small stream near the headwaters of riacho Jacaré, municipality of São João da Canabrava, in the state of Piauí. This area is not located on slopes of elevations with humid forests, implying new and important aspects for the species. Therefore, K. attenboroughi can no longer be considered endemic to the state of Ceará or to the slopes of highland swamps. This might represent a substantial increase in the potential area of occurrence of K. attenboroughi, making its geographic distribution likely underestimated. Another significant aspect of this new occurrence area is its environmental characteristics, similar to the environments present in already known occurrence points (Araújo et al., 2022), reinforcing the idea that such environmental characteristics are essential resources for the presence of these crabs, as well as consolidating the type of environment of the species.
The present results underscore the importance of biological surveys for freshwater crabs in northeastern Brazil. However, they also reveal that the population of K. attenboroughi from riacho Jacaré, as well as those of F. ibiapaba from Ceará, face significant anthropic pressures. The main issues encountered by Pseudothelphusidae crabs in northeastern Brazil include deforestation in areas adjacent to springs and streams, the presence of domestic animals such as pigs inside the rivers where the species occurs, and the presence of garbage and other pollutants in the areas where crabs are found, exerting strong anthropic pressure.
ACKNOWLEDGMENTS:
We thank the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) for the financial support and scholarship for APP and PHPN (#BP4-00172 00173.01.00/20; #BMD 0008-02422.01.08/22), to Coordenação de Apefeiçoamento de Pessoal de Nível Superior (CAPES) for granting a scholarship to CAN, CAMM, JGA and WMN (88887.637365/2021-00; 88887.717864/2022-00; 88887.717871/2022-00; 88887.511078/2020-00), and to the Universidade Regional do Cariri (URCA) for supporting studies on decapod crustaceans. We also thank João Rafael, Gustavo Alves, Joldam Fortuna, Edimar Machado, Dionísio Ecologista and Djanilson Ecologista for the information about the existence of crabs and for the great support in the field.
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FUNDING INFORMATION:
Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico - FUNCAP (#BP4-00172 00173.01.00/20; #BMD 0008-02422.01.08/22); Coordenação de Apefeiçoamento de Pessoal de Nível Superior - CAPES (88887.637365/2021-00; 88887.717864/2022-00; 88887.717871/2022-00; 88887.511078/2020-00).
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Published with the financial support of the “Programa de Apoio às Publicações Científicas Periódicas da Universidade de São Paulo”
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Edited by
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Edited by:
Marcos Domingos Siqueira Tavares
Publication Dates
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Publication in this collection
22 Nov 2024 -
Date of issue
2024
History
-
Received
12 June 2023 -
Accepted
24 June 2024 -
Published
09 Aug 2024