An integrative taxonomy study of cave-dwelling aeglids (Decapoda: Anomura: Aeglidae) from Natural Protected Areas in south-eastern Brazil, with description of three new species
Sérgio Luiz de Siqueira Bueno A * , Alexandre Lopes Camargo B , Heros Augusto Santos Lobo C D , Ana Luiza Vera-Silva E , Marcos Tavares F and Fernando Luis Mantelatto EA
B
C
D
E
F
Abstract
Three new cave-dwelling aeglid species from the Alto Ribeira karst region, south-eastern Brazil, are described. Morphological descriptions are based on traits traditionally used in aeglid taxonomy. Molecular phylogeny reconstruction based on the partial fragments of the 16S ribosomal RNA (16S rDNA) and the cytochrome oxidase subunit I (COI) revealed that: (1) dispersal of epigean aeglids toward the Alto Ribeira karst area occurred at two separate events in the evolutionary history of freshwater aeglids; (2) extant cave-dwelling aeglid species form two distinct subclades, each of which originated from a distinct ancestral epigean lineage; and (3) successful adaptation to subterranean habitats, as seen in extant cave-dwelling aeglid species from the Alto Ribeira karst area, developed independently within each subclade, as each one of them comprised an exclusive group of both stygobitic and stygophilic species.
ZooBank: urn:lsid:zoobank.org:pub:3F2D0A63-B86E-421F-9B29-DD605BF7B4E7
Keywords: Aegla, biodiversity, conservation units, dispersal, new species, stygobites, stygophiles, subterranean habitat.
References
Abell R, Thieme ML, Revenga C, Bryer M, Kottelat M, Bogutskaya N, Coad B, Mandrak N, Balderas SC, Bussing W, Stiassny MLJ, Skelton P, Allen GR, Unmack P, Naseka A, Ng R, Sindorf N, Robertson J, Armijo E, Higgins JV, Heibel TJ, Wikramanayake E, Olson D, López HL, Reis RE, Lundberg JG, Pérez MHS, Petry P (2008) Freshwater ecoregions of the world: A new map of biogeographic units for freshwater biodiversity conservation. BioScience 58, 403-414.
| Crossref | Google Scholar |
Alvarez F, Villalobos JL (2018) A new species of stygobitic freshwater crab of the genus Rodriguezia Bott, 1969 (Crustacea: Decapoda: Trichodactylidae) from Tabasco, Mexico. Zootaxa 4378, 137-143.
| Crossref | Google Scholar | PubMed |
Anker K (2008) A worldwide review of stygobiotic and stygophilic shrimps of the family Alpheidae (Crustacea, decapoda, Caridea). Subterranean Biology 6, 1-16.
| Google Scholar |
Arantes T, Souza-Shibatta L, Teixeira GM (2024) Description of a new species of Aegla (Decapoda, Anomura) from the Paraná 3 hydrographic basin, Brazil. Zootaxa 5418, 371-384.
| Crossref | Google Scholar | PubMed |
Baldari F, Mejía-Ortíz LM, López-Mejía M (2010) A new cave species of Chyphiops (Crustacea: Decapoda: Palaemonidae) from southern Mexico. Zootaxa 2427, 47-54.
| Crossref | Google Scholar |
Bond-Buckup G, Buckup L (1994) A Família Aeglidae (Crustacea, Decapoda, Anomura). Arquivos de Zoologia do Museu de Zoologia da Universidade de São Paulo 32, 159-346 [In Portuguese].
| Crossref | Google Scholar |
Bond-Buckup G, Jara CG, Buckup L, Pérez-Losada M, Bueno AAP, Crandall KA, Santos S (2010) New species and new records of endemic freshwater crabs from the Atlantic Forest in southern Brazil (Anomura: Aeglidae). Journal of Crustacean Biology 30, 495-502.
| Crossref | Google Scholar |
Bueno SLS, Shimizu RM, Rocha SS (2007) Estimating the population size of Aegla franca (Decapoda: Anomura: Aeglidae) by mark-recapture technique from an isolated section of Barro Preto stream, County of Claraval, State of Minas Gerais, southeastern Brazil. Journal of Crustacean Biology 27, 553-559.
| Crossref | Google Scholar |
Bueno SLS, Shimizu RM, Moraes, JCB (2016a) A remarkable anomuran: the taxon Aegla Leach, 1820. Taxonomic remarks, distribution, biology, diversity and conservation. In ‘A Global Overview of the Conservation of Freshwater Decapod Crustaceans’. (Eds T Kawai, N Cumberlidge) pp. 23–64. (Springer: Cham, Switzerland) 10.1007/978-3-319-42527-6_2
Bueno SLS, Camargo AL, Moraes JCB (2017) A new species of stygobitic aeglid from lentic subterranean waters in southeastern Brazil, with an unusual morphological trait: short pleopods in adult males. Nauplius 25, e201700021.
| Crossref | Google Scholar |
Bueno SLS, Wolf MR, Shimizu RM (2021) Reassessing the Current Conservation Status of the Freshwater Aeglid, Aegla jaragua Moraes, Tavares and Bueno, 2016 (Decapoda: Anomura: Aeglidae) as Critically Endangered. A Ten-Year Case Study. In ‘Recent Advances in Freshwater Crustacean Biodiversity and Conservation’. (Eds T Kawai, DC Rogers) Advances in Crustacean Research 22, pp. 347–380. (CRC Press: Boca Raton, FL, USA)
Christman MC, Culver DC (2001) The relationship between cave biodiversity and available habitat. Journal of Biogeography 28, 367-380.
| Crossref | Google Scholar |
Colavite J, Bueno SLS, da Silva AR, Tavares M (2024) A new species of Aegla (Decapoda, Anomura, Aeglidae) from the Paranapanema watershed, southeastern Brazil. Crustaceana 97, 659-675.
| Crossref | Google Scholar |
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| Crossref | Google Scholar | PubMed |
De Grave S, Pentcheff ND, Ahyong ST, Chan TY, Crandall KA, Dworschak PC, Felder DL, Feldmann RM, Fransen CHJM, Goulding LYD, Lemaitre R, Low MEY, Martin JW, Ng PKL, Schweitzer CE, Tan SH, Tshudy D, Wetzer R (2009) A classification of living and fossil genera of decapod crustaceans. Raffles Bulletin of Zoology Supplement 21, 1-109 Available at http://hdl.handle.net/10088/8358.
| Google Scholar |
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792-1797.
| Crossref | Google Scholar | PubMed |
Edgar RC (2022) Muscle5: high-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny. Nature Communications 13(1), 6968.
| Crossref | Google Scholar |
Feldmann RM (1984) Haumuriaegla glaessneri n. gen. and sp. (Decapoda; Anomura; Aeglidae) from Haumurian (late Cretaceous) rocks near Cheviot, New Zealand. New Zealand Journal of Geology and Geophysics 27, 379-385.
| Crossref | Google Scholar |
Feldmann RM, Vega FJ, Applegate SP, Bishop GA (1998) Early Cretaceous arthropods from the Tlayúa formation at Tepexi de Rodríguez, Puebla, Mexico. Journal of Paleontology 72, 79-90.
| Crossref | Google Scholar |
Fenolio DB, Niemiller ML, Gluesenkamp AG, McKee AM, Taylor SJ (2017) New distributional records of the stygobitic crayfish Cambarus cryptodytes (Decapoda: Cambaridae) in the Floridan Aquifer System of southwestern Georgia. Southeastern Naturalist 16, 163-181.
| Crossref | Google Scholar |
Fernandes CS, Bichuette ME (2013) Shape variation of Aegla schmitti (Crustacea Decapoda, Aeglidae) associated to superficial and subterranean stream reaches. Subterranean Biology 10, 17-24.
| Crossref | Google Scholar |
Fernandes CS, Bueno SLS, Bichuette ME (2013) Distribution of cave-dwelling Aegla spp. (Decapoda: Anomura: Aeglidae) from the Alto Ribeira karstic area in southeastern Brazil based on geomorphological evidence. Journal of Crustacean Biology 33, 567-575.
| Crossref | Google Scholar |
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294-299.
| Google Scholar | PubMed |
Gilbert J, Deharveng L (2002) Subterranean ecosystems: a truncated functional biodiversity. BioScience 52, 473-481.
| Crossref | Google Scholar |
Hobbs HH, Jr, Hobbs HH, III, Daniel MA (1977) A review of the troglobitic decapod crustaceans of the Americas. Smithsonian Contributions to Zoology 244, 1-154.
| Crossref | Google Scholar |
Jara CG (1980) Dos nuevas especies de Aegla Leach (Crustacea, Decapoda, Anomura) del sistema hidrografico del rio Valdivia. Anales del Museo de Historia Natural 13, 255-266 Available at https://bibliotecadigital.ciren.cl/handle/20.500.13082/18407 [In Spanish].
| Google Scholar |
Jara CG (1989) Aegla denticulata lacustris, new subspecies, from Lake Rupanco, Chile (Crustacea: Decapoda: Anomura: Aeglidae). Proceedings of the Biological Society of Washington 102, 385-393 Available at https://biostor.org/reference/74605.
| Google Scholar |
Karmann I, Ferrari JA (2002) Carste e cavernas do Parque Estadual Turístico do Alto do Ribeira (PETAR), SP. In ‘Sitios Geológicos e Paleontológicos do Brasil’. (Eds C Schobbenhaus, DA Campos, ET Queiroz, M Berbert-Born) pp. 401–413. (Departamento Nacional de Produção Mineral, RNPM: Brasília, Brazil) Available at https://rigeo.sgb.gov.br/handle/doc/19846 [In Portuguese]
Lobo HAS (2012) Espeleoclima e suas aplicações no manejo do turismo em cavernas. Revista do Departamento de Geografia da USP 23, 27-54 [In Portuguese].
| Crossref | Google Scholar |
Lundberg JG, Marshall LG, Guerrero J, Horton B, Malabarba MCSL, Wesselingh F (1998) The stage for Neotropical fish diversification: a history of tropical South American rivers. In ‘Phylogeny and classification of neotropical fishes, part 1 – fossils and geological evidence’. (Ed. LR Malabarba) pp. 13–48. (Edipucrs: Porto Alegre, Brazil)
Maia KP, Bueno SLS, Trajano E (2013) Ecologia populacional e conservação de eglídeos (Crustacea: Decapoda: Aeglidae) em cavernas da área cárstica do Alto Ribeira, em São Paulo. Revista da Biologia 10, 40-45 [In Portuguese].
| Crossref | Google Scholar |
Mammola S, Piano E, Cardoso P, Vernon P, Domínguez-Villar D, Culver DC, Pipan T, Isaia M (2019) Climate change going deep: the effects of global climatic alterations on cave ecosystems. The Anthropocene Review 6, 98-116.
| Crossref | Google Scholar |
Mantelatto FL, Pardo LM, Pileggi LG, Felder DL (2009) Taxonomic re-examination of the hermit crab species Pagurus forceps and Pagurus comptus (Decapoda: Paguridae) by molecular analysis. Zootaxa 2133, 20-32.
| Crossref | Google Scholar |
Mantelatto FL, Terossi M, Negri M, Buranelli RC, Robles R, Magalhães T, Tamburus AF, Rossi N, Miyazaki MJ (2018) DNA sequence database as a tool to identify decapod crustaceans on the São Paulo coastline. Mitochondrial DNA Part A 29, 805-815.
| Crossref | Google Scholar | PubMed |
Marçal IC, Páez FP, Souza-Shibatta L, Sofia SH, Teixeira GM (2020) Taxonomic revision of Aegla lata Bond-Buckup & Buckup, 1994 (Decapoda: Anomura: Aeglidae), with the description of a new species of Aegla Leach, 1820 from the Upper Paraná Ecoregion, Brazil. Journal of Crustacean Biology 40, 425-434.
| Crossref | Google Scholar |
Marçal IC, Páez FP, Souza-Shibatta L, Sofia SH, Teixeira GM (2021a) Aegla buenoi n. sp. (Decapoda: Anomura): first record of aeglid crab from Cinzas River basin, Brazil. Zootaxa 5005, 291-303.
| Crossref | Google Scholar |
Marçal IC, Páez FP, Da Silva PF, Souza-Shibatta L, Teixeira GM (2021b) Cryptic diversity among populations of Aegla Leach, 1820 (Decapoda: Anomura: Aeglidae) from Tibagi River basin, Paraná state, Brazil, with descriptions of three new species. Journal of Natural History 55, 2145-2171.
| Crossref | Google Scholar |
Martin JW, Abele LG (1988) External morphology of the genus Aegla (Crustacea: Anomura: Aeglidae). Smithsonian Contributions to Zoology 453, 1-46.
| Crossref | Google Scholar |
Mejía-Ortíz LM, Hartnoll RG (2005) Modifications of eye structure and integumental pigment in two cave crayfish. Journal of Crustacean Biology 25, 480-487.
| Crossref | Google Scholar |
Mejía-Ortíz LM, Hartnoll RG, López-Mejía M (2006) Progressive troglomorphism of ambulatory and sensory appendages in three Mexican cave decapods. Journal of Natural History 40, 255-264.
| Crossref | Google Scholar |
Mejía-Ortíz LM, Baldari F, López-Mejía M (2008) Macrobrachium sbordonii (Decapoda: Palaemonidae), a new stygobitic species of freshwater prawn from Chiapas Mexico. Zootaxa 1814, 49-57.
| Crossref | Google Scholar |
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE)’, 14 November 2010, New Orleans, LA, USA. INSPEC Accession Number 11705685. (IEEE) doi:doi:10.1109/GCE.2010.5676129
Moraes JCB, Terossi M, Buranelli RC, Tavares M, Mantelatto FL, Bueno SLS (2016) Morphological and molecular data reveal the cryptic diversity among populations of Aegla paulensis (Decapoda, Anomura, Aeglidae), with descriptions of four new species and comments on dispersal routes and conservation status. Zootaxa 4193, 1-48.
| Crossref | Google Scholar |
Moraes JCB, Tavares M, Bueno SLS (2017) Taxonomic review of Aegla marginata Bond-Buckup & Buckup, 1994 (Decapoda, Anomura, Aeglidae) with description of a new species. Zootaxa 4323, 519-533.
| Crossref | Google Scholar |
Oyanedel A, Valdovinos C, Sandoval N, Moya C, Kiessling G, Salvo J, Olmos V (2011) The southernmost freshwater anomurans of the world: geographic distribution and new records of Patagonian aeglids (Decapoda: Aeglidae). Journal of Crustacean Biology 31, 396-400.
| Crossref | Google Scholar |
Palumbi SR, Martin A, Romano S, Mcmillan WO, Stice L, Grabowski G (2002) ‘The simple fool’s guide to PCR’, ver. 2. (University of Hawaii Press: Honolulu, HI, USA) Available at https://library.oarcloud.noaa.gov/noaa_documents.lib/NOAA_related_docs/SimpleFoolsMaster.pdf
Pérez-Losada M, Jara CG, Bond-Buckup G, Crandall KA (2002) Phylogenetic relationships among the species of Aegla (Anomura: Aeglidae) freshwater crabs from Chile. Journal of Crustacean Biology 22, 304-313.
| Crossref | Google Scholar |
Pérez-Losada M, Bond-Buckup G, Jara CG, Crandall KA (2004) Molecular systematics and biogeography of the southern South American freshwater “crabs” Aegla (Decapoda: Anomura: Aeglidae) using multiple heuristic tree search approaches. Systematic Biology 53, 767-780.
| Crossref | Google Scholar | PubMed |
Potter PE (1997) The Mesozoic and Cenozoic paleodrainage of South America: a natural history. Journal of South American Earth Sciences 10, 331-344.
| Crossref | Google Scholar |
Ribeiro AC (2006) Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: An example of faunal evolution associated with a divergent continental margin. Neotropical Ichthyology 4, 225-246.
| Crossref | Google Scholar |
Rocha SS, Bueno SLS (2004) Crustáceos decápodes de água doce com ocorrência no Vale do Ribeira de Iguape e rios costeiros adjacentes, São Paulo, Brasil. Revista Brasileira de Zoologia 21, 1001-1010.
| Crossref | Google Scholar |
Rocha SS, Bueno SLS (2011) Extension of the known distribution of Aegla strinatii Türkay, 1972 and a checklist of decapod crustaceans (Aeglidae, Palaemonidae and Trichodactylidae) from the Jacupiranga State Park, South of São Paulo State, Brazil. Nauplius 19, 163-167.
| Crossref | Google Scholar |
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539-42.
| Crossref | Google Scholar | PubMed |
Sallun Filho W, Ferrari JA, Hiruma ST, Sallun AEM, Karmann I (2010) O carste no plano de manejo do Parque Estadual Intervales e zona de amortecimento, Estado de São Paulo, Brasil. Revista da Escola de Minas 63, 441-448 [In Portuguese].
| Google Scholar |
Santos S, Bond-Buckup G, Buckup L, Bartholomei-Santos ML, Pérez-Losada M, Jara CG, Crandall KA (2015) Three new species of Aeglidae (Aegla Leach, 1820) from Paraná state, Brazil. Journal of Crustacean Biology 35, 839-849.
| Crossref | Google Scholar |
Sociedade Brasileira de Espeleologia (2023) Cadastro Nacional de Cavernas. (SBE) Available at https://sbecnc.org.br/ [In Portuguese, verified February 2023]
Schmitt WL (1942) The species of Aegla, endemic South American fresh-water crustaceans. Proceedings of the United States National Museum 91, 431-524.
| Crossref | Google Scholar |
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Molecular Biology and Evolution 28, 2731-2739.
| Crossref | Google Scholar | PubMed |
Trevisan A, Masunari S (2010) Geographical distribution of Aegla schmitti Hobbs III, 1979 (Decapoda Anomura Aeglidae) and morphometric variations in male populations from Paraná State, Brazil. Nauplius 18, 45-55.
| Google Scholar |
Trevisan A, Marochi MZ, Costa M, Santos S, Masunari S (2016) Effects of the evolution of the Serra do Mar mountains on the shape of the geographically isolated populations of Aegla schmitti Hobbs III, 1979 (Decapoda: Anomura). Acta Zoologica 97, 34-41.
| Crossref | Google Scholar |
Türkay M (1972) Neue Höhlendekapoden aus Brasilien (Crustacea). Revue Suisse de Zoologie 79, 415-419.
| Crossref | Google Scholar |