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Diversity and conservation status of Aegla spp. (Anomura, Aeglidae): an update

Abstract

The speciose genus Aegla Leach, 1820 is the only valid extant genus of the anomuran family Aeglidae, bearing 83 known species. This diversity may be even greater since there is some evidence for cryptic speciation. The genus is endemic to southern South America, occurring in freshwater habitats. We assessed the conservation status of 82 species of Aegla and found almost 70% of them under some level of threat, which represents a concerning proportion. Major threats to the group include freshwater pollution with urban, agricultural and industrial effluents, habitat modification and fragmentation, riparian forest removal, among others. Conservation measures are required to mitigate the major threats to freshwater ecosystems along rivers where the group occurs.

Key words
Anomuran crabs; Decapoda; freshwater crabs; South American creeks

Introduction

Taxonomically, the family Aeglidae was formerly included within the anomuran superfamily Galatheoidea, but morphological and molecular evidence ( Martin and Abele, 1986Martin, J.W. and Abele, L.G. 1986. Phylogenetic relationships of the genus Aegla (Decapoda, Anomura, Aeglidae), with comments on anomuran phylogeny. Journal of Crustacean Biology , 6: 576-616.; Tudge and Scheltinga, 2002Tudge, C.C. and Scheltinga, D.M. 2002. Spermatozoal morphology of the freshwater anomuran Aegla longirostris Bond-Buckup and Buckup, 1994 (Crustacea: Decapoda: Aeglidae) from South America. Proceedings of the Biological Society of Washington , 115: 118-128.; Pérez-Losada et al., 2002aPérez-Losada, M., Jara, C.G.; Bond-Buckup, G.; Porter, M.L. and Crandall, K.A. 2002a. Anomuran phylogenetic relationships: on the taxonomic positioning of Aeglidae freshwater crabs. Journal of Crustacean Biology , 22: 670-676.; Ahyong and O’Meally, 2004Ahyong, S.A. and O’Meally, D. 2004. Phylogeny of the Decapoda Reptantia: resolution using three molecular loci and morphology. The Raffles Bulletin of Zoology, 52: 673-693.) questioned this position. A reappraisal by McLaughlin et al. (2007McLaughlin, P.A.; Lemaitre, R. and Sorhannus, U. 2007. Hermit crab phylogeny: a reappraisal and its “fall-out”. Journal of Crustacean Biology , 27: 97-115.) elevated Aeglidae to superfamily rank (Aegloidea).

Aegla Leach, 1820 is the only extant genus of the family Aeglidae and can be found in rivers, streams, and lakes of southern South America, occurring from the Rio Grande basin, on the border of São Paulo and Minas Gerais states, Brazil ( Bueno et al., 2007Bueno, S.L.S.; Shimizu, R.M. and Rocha, S.S. 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. ), to Duque de York Island, South River basin, Chile ( Oyanedel et al., 2011Oyanedel, A.; Valdovinos, C.; Sandoval, N.; Moya, C.; Kiessling, G.; Salvo, J. and 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.). This genus includes 83 described species ( Bond-Buckup et al., 2008Bond-Buckup, G.; Jara, C.G.; Pérez-Losada, M.; Buckup, L. and Crandall, K.A. 2008. Global diversity of crabs (Aeglidae: Anomura: Decapoda) in freshwater. Hydrobiologia, 595: 267-273.; 2010aBond-Buckup, G.; Jara, C.G.; Buckup, L.; Bueno, A.P.; Perez-Losada, M. and Crandall, K.A. 2010a. Description of a new species of Aeglidae, and new records of related species from river basins in Argentina (Crustacea, Anomura). Zootaxa, 2343: 18-30. ; 2010bBond-Buckup, G.; Jara, C.G.; Buckup, L.; Pérez-Losada, M.; Crandall, K.A. and Santos, S. 2010b. 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.; Santos et al., 2012Santos, S.; Bond-Buckup, G.; Buckup, L.; Pérez-Losada, M.; Finley, M. and Crandall, K.A. 2012. Three new species of Aegla (Anomura) freshwater crabs from the Upper Uruguay River hydrographic basin in Brazil. Journal of Crustacean Biology , 32: 529-540. ; 2013Santos, S.; Jara, C.G.; Bartholomei-Santos, M.L.; Pérez-Losada, M. and Crandall, K.A. 2013. New species and records of the genus AeglaLeach, 1820 (Crustacea, Anomura, Aeglidae) from the West-Central region of Rio Grande do Sul, Brazil. Nauplius , 21: 211-223 .; 2015Santos, S.; Bond-Buckup, G.; Buckup, L.; Bartholomei-Santos, M.L.; Pérez-Losada, M.; Jara, C.G. and Crandall, K.A. 2015. Three new species of Aeglidae ( AeglaLeach, 1820) from Paraná State, Brazil. Journal of Crustacean Biology , 35: 839-849.; Moraes et al., 2016Moraes, J.C.; Terossi, M.; Buranelli, R.C.; Tavares, M.; Mantelatto, F.L. and Bueno, S.L.S. 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.) and probably new species will be uncovered in the next years ( Fig. 1).

Figure 1
Cumulative number of know species of the genus Aegla Leach, 1820, since 1900.

The use of molecular techniques together with traditional systematics has helped to confirm several new species, as the number of morphological characters for taxonomic use is limited by the conservative morphotype of the group ( Bond-Buckup and Buckup, 1994Bond-Buckup, G. and Buckup, L. 1994. A família Aeglidae (Crustacea, Decapoda, Anomura). Arquivos de Zoologia, 32: 159-347.; Pérez-Losada et al., 2004Pérez-Losada, M. , Bond-Buckup, G.; Jara, C.G. and Crandall, K.A. 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.; Santos et al., 2009Santos, S.; Bond-Buckup, G.; Pérez-Losada, M.; Bartholomei-Santos, M.L. and Buckup, L. 2009. Aegla manuinflata, a new species of freshwater anomuran (Decapoda: Anomura: Aeglidae). Zootaxa , 2088: 31-40.; 2010Santos, S.; Bond-Buckup, G.; Pérez-Losada, M.; Jara, C.G.; Crandall, K.A. and Buckup, L. 2010. New records and description of a new species of Aeglidae (Crustacea: Anomura) from river basins in Southern Brazil. Nauplius , 18 : 79-86.; 2012Santos, S.; Bond-Buckup, G.; Buckup, L.; Pérez-Losada, M.; Finley, M. and Crandall, K.A. 2012. Three new species of Aegla (Anomura) freshwater crabs from the Upper Uruguay River hydrographic basin in Brazil. Journal of Crustacean Biology , 32: 529-540. ; 2013Santos, S.; Jara, C.G.; Bartholomei-Santos, M.L.; Pérez-Losada, M. and Crandall, K.A. 2013. New species and records of the genus AeglaLeach, 1820 (Crustacea, Anomura, Aeglidae) from the West-Central region of Rio Grande do Sul, Brazil. Nauplius , 21: 211-223 .). Moreover, the existence of cryptic species cannot be ruled out since molecular markers and geometric morphometrics have already pointed to this possibility ( Bartholomei-Santos et al., 2011Bartholomei-Santos, M.L.; Roratto, P.A. and Santos, S. 2011. High genetic differentiation of Aegla longirostri (Crustacea, Decapoda, Anomura) populations in southern Brazil revealed by multi-loci microsatellite analysis. Genetics and Molecular Research, 10: 4133-4146. ; Marchiori et al., 2014Marchiori, A.B.; Bartholomei-Santos, M.L. and Santos, S. 2014. Intraspecific variation in Aegla longirostri(Crustacea: Decapoda: Anomura) revealed by geometric morphometrics: evidence for ongoing speciation? Biological Journal of the Linnean Society , 112: 31-39.; 2015Marchiori, A.B.; Fornel, R. and Santos, S. 2015. Morphometric variation in allopatric populations of Aegla platensis(Crustacea: Decapoda: Anomura): possible evidence for cryptic speciation. Zoomorphology, 134: 45-53.). This level of diversity is greater than that observed for crayfishes of the family Parastacidae ( Almerão et al., 2015Almerão, M.; Rudolph, E.; Souty-Grosset, C.; Crandall, K.A.; Buckup, L.; Amouret, J.; Verdi, A.; Santos, S. and Araújo, P.B. 2015. The native South American crayfishes (Crustacea, Parastacidae): state of knowledge and conservation status. Aquatic Conservation: Marine and Freshwater Ecosystems, 25: 288-301.) and brachyuran crabs of the genus Trichodactylus Latreille, 1828 ( Yeo et al., 2006Yeo, D.C.; Ng, J.P.K.L.; Cumberlidge, N.; Magalhães, C.; Daniels, S.R. and Campos, M.R. 2006. A global assessment of freshwater crab diversity (Crustacea: Decapoda: Brachyura). Hydrobiologia , 595 : 275-286.), other crustacean groups inhabiting southern South American continental waters. Bond-Buckup et al. (2008)Bond-Buckup, G.; Jara, C.G.; Pérez-Losada, M.; Buckup, L. and Crandall, K.A. 2008. Global diversity of crabs (Aeglidae: Anomura: Decapoda) in freshwater. Hydrobiologia, 595: 267-273. estimated that 36.5% of the 63 species described at that time were under threat of extinction. Pérez-Losada et al. (2009)Pérez-Losada, M., Bond-Buckup, G.; Jara, C.G. and Crandall, K.A. 2009. Conservation assessment of southern South American freshwater ecoregions on the basis of the distribution and genetic diversity of crabs from the genus Aegla. Conservation Biology, 23: 692-702. assessed the conservation status of 66 aeglid species and found that 32% of them were threatened, that is, species falling within the International Union for Nature Conservation (IUCN) categories Vulnerable (VU), Endangered (EN), and Critically Endangered (CR). Many factors contribute to threat the group along its distribution in southern South America, such as decline in habitat quality, water contamination by extensive use of pesticides in agriculture or by urban sewage, silvicultural practices, construction of hydroelectric plants, among others ( Pérez-Losada et al., 2002bPérez-Losada, M., Jara, C.G.; Bond-Buckup, G.; and Crandall, K.A. 2002b. Conservation phylogenetics of Chilean freshwater crabs Aegla (Anomura, Aeglidae): assigning priorities for aquatic habitat protection. Biological Conservation , 105: 345-353.; Bond-Buckup et al., 2008Bond-Buckup, G.; Jara, C.G.; Pérez-Losada, M.; Buckup, L. and Crandall, K.A. 2008. Global diversity of crabs (Aeglidae: Anomura: Decapoda) in freshwater. Hydrobiologia, 595: 267-273.; Baumart and Santos, 2010Baumart, J.S. and Santos, S. 2010. The impact of herbicides on benthic organisms in flooded rice fields in southern Brazil. p. 369-382. In: A. Kortekamp (ed), Herbicides and Environmental. 1st ed.: InTech, Rijeka, Croatia.; Santos et al., 2012Santos, S.; Bond-Buckup, G.; Buckup, L.; Pérez-Losada, M.; Finley, M. and Crandall, K.A. 2012. Three new species of Aegla (Anomura) freshwater crabs from the Upper Uruguay River hydrographic basin in Brazil. Journal of Crustacean Biology , 32: 529-540. ). The presence of some species in restrict areas, as in headwaters, several of them with a few records of occurrence, highlights even more the level of threat to the group’s conservation ( Magris et al., 2010Magris, R.A.; Bond-Buckup, G.; Magalhães, C.; Mantelatto, F.L; Reid, J.W.; Loureiro, L.M.A.E.; Coelho, P.A.; Santana, W.; Buckup, L.; Rocha, S.S.; Bueno, S.L.S.; Pinheiro, M.A.A.; D’Incao, F.; Ivo, C.T.C.; Dias Neto, J.; Rodrigues, E.S.; Araujo, P.B.; Boos Jr, H. and Duarte L.F.A. 2010. Quantification of extinction risk for crustacean species: an overview of the National Red Listing process in Brazil. Nauplius, 18: 129-135.).

In this study, we present data on the diversity of species of the genus Aegla, as well as updated information on the distribution of these species in different South American hydrographic basins. Moreover, based on data from several scientific collections and from years of work and experience of the authors, we evaluated the conservation status of the aeglid species and discussed the main threats to the genus diversity.

Material and Methods

We assessed and updated the distribution of 82 species of Aegla. Based on the updated distribution data, we revised the conservation status for each species previously assessed until 2016, according to the rules established by the International Union for Conservation of Nature ( IUCN, 2012IUCN (International Union for Conservation of Nature). 2012. IUCN Red List Categories and Criteria: Version 3.1. Second edition. IUCN, Gland, Switzerland and Cambridge, UK. ). There are five quantitative criteria (A - E) to be applied in order to evaluate if a taxon is under threat, and in which category the taxon should be included (EX - extinct; EW - extinct in wild; CR - critically endangered; EN - endangered; VU - vulnerable; NT - near threatened; LC - least concern; DD - deficient data; and NE - not evaluated; CR, EN and VU represent threat categories). The assessment employs sub-criteria to justify the assignment of a taxon to a certain category. Each species was evaluated in relation to its Extent Of Occurrence (EOO; sub-criterion B1) and Area Of Occupancy (AOO; sub-criterion B2), using data from literature ( Bond-Buckup and Buckup, 1994Bond-Buckup, G. and Buckup, L. 1994. A família Aeglidae (Crustacea, Decapoda, Anomura). Arquivos de Zoologia, 32: 159-347.; Jara and Palacios, 1999Jara, C. and Palacios, V.L. 1999. Two new species of Aegla Leach (Crustacea: Anomura: Aeglidae). Proceedings of the Biological Society of Washington, 112: 106-109.; Jara et al., 2003Jara, C.G.; Pérez-Losada, M. and Crandall, K.A. 2003. A new species of freshwater anomuran crab of the genus Aegla (Crustacea: Decapoda: Aeglidae) from the Nahuelbuta Coastal Range, Chile. Proceedings of the Biological Society of Washington , 116: 933-942.; Galves et al., 2007Galves, W.; Jerep, F.C. and Shibatta, O.A. 2007. Estudo da condição ambiental pelo levantamento da fauna de três riachos da região do Parque Estadual Mata dos Godoy (PEMG), Londrina, PR, Brasil. Pan-American Journal of Aquatic Sciences, 2: 55-65.; Santos et al., 2009Santos, S.; Bond-Buckup, G.; Pérez-Losada, M.; Bartholomei-Santos, M.L. and Buckup, L. 2009. Aegla manuinflata, a new species of freshwater anomuran (Decapoda: Anomura: Aeglidae). Zootaxa , 2088: 31-40.; 2010Santos, S.; Bond-Buckup, G.; Pérez-Losada, M.; Jara, C.G.; Crandall, K.A. and Buckup, L. 2010. New records and description of a new species of Aeglidae (Crustacea: Anomura) from river basins in Southern Brazil. Nauplius , 18 : 79-86.; 2012Santos, S.; Bond-Buckup, G.; Buckup, L.; Pérez-Losada, M.; Finley, M. and Crandall, K.A. 2012. Three new species of Aegla (Anomura) freshwater crabs from the Upper Uruguay River hydrographic basin in Brazil. Journal of Crustacean Biology , 32: 529-540. ; 2013Santos, S.; Jara, C.G.; Bartholomei-Santos, M.L.; Pérez-Losada, M. and Crandall, K.A. 2013. New species and records of the genus AeglaLeach, 1820 (Crustacea, Anomura, Aeglidae) from the West-Central region of Rio Grande do Sul, Brazil. Nauplius , 21: 211-223 .; 2014Santos, S.; Bond-Buckup, G.; Buckup, L.; Loureiro, T.G.; Gonçalves, A.S.; Verdi, A.; Scarabino F. and Clavijo, C. 2014. The Aeglidae of Uruguay (Decapoda, Anomura), with the description of a new species of Aegla. Crustaceana Monographs, 19: 195-205.; 2015Santos, S.; Bond-Buckup, G.; Buckup, L.; Bartholomei-Santos, M.L.; Pérez-Losada, M.; Jara, C.G. and Crandall, K.A. 2015. Three new species of Aeglidae ( AeglaLeach, 1820) from Paraná State, Brazil. Journal of Crustacean Biology , 35: 839-849.; Bond-Buckup et al., 2010aBond-Buckup, G.; Jara, C.G.; Buckup, L.; Bueno, A.P.; Perez-Losada, M. and Crandall, K.A. 2010a. Description of a new species of Aeglidae, and new records of related species from river basins in Argentina (Crustacea, Anomura). Zootaxa, 2343: 18-30. ; 2010bBond-Buckup, G.; Jara, C.G.; Buckup, L.; Pérez-Losada, M.; Crandall, K.A. and Santos, S. 2010b. 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.; César and Damborenea, 2010César, I.I. and Damborenea, C. 2010. Type and non-type specimens of Aegla (Decapoda: Anomura: Aeglidae) housed in the Museo de La Plata, Argentina. Zootaxa , 2337: 31-46.; Oyanedel et al., 2011Oyanedel, A.; Valdovinos, C.; Sandoval, N.; Moya, C.; Kiessling, G.; Salvo, J. and 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.; Rocha and Bueno, 2011Rocha, S.S. and Bueno, S.L.S. 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. 2011. Nauplius , 19: 163-167.; Boos et al., 2012Boos, H.; Bond-Buckup, G.; Buckup, L.; Araujo, P.B.; Magalhães, C.; Almerão, M.P.; dos Santos, R.A. and Mantelatto, F.L. 2012. Checklist of the Crustacea from the state of Santa Catarina, Brazil. Check List, 8: 1020-1046.; Satterlee et al., 2012Satterlee, S.A.; Zuercher, G.L.; Kuhle, C.W.; Ramírez-Pinto, F.; Fernández, S.; Jackson, L.; Velázquez, M.C. and Kochalka, J.A. 2012. Rediscovery of aeglid crabs in the Rio Jejuí watershed, Paraguay. Journal of Crustacean Biology , 32: 541-543.; Giri and Collins, 2014Giri, F. and Collins, P. 2014. Clinal variation in carapace shape in the South American freshwater crab, Aegla uruguayana (Anomura: Aeglidae). Biological Journal of the Linnean Society, 113: 914-930.; Moraes et al., 2016Moraes, J.C.; Terossi, M.; Buranelli, R.C.; Tavares, M.; Mantelatto, F.L. and Bueno, S.L.S. 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.) and from sampling records in scientific collections (Universidade Federal do Rio Grande do Sul, Universidade Federal de Santa Maria, Pontifícia Universidade Católica do Rio Grande do Sul, Fundação Zoobotânica do Rio Grande do Sul, Universidade Regional do Alto Uruguai e das Missões - Campus Erechim, Universidad Austral de Chile). We determined the AOO for species with less than four records, using an area measure unit (each pixel corresponds to an area of 1 km2). In this case, AOO ranged from 1 to 3 km2. For species with four or more records, we calculated the EOO. We assessed data for land-use classification for the whole occurrence area of Aeglidae from the Harmonized World Soil Database ( http://webarchive.iiasa.ac.at/Research/LUC/External-World-soil-database/HTML/), from the World Land Use - Land cover from Food and Agriculture Organization of the United Nations (FAO) ( http://www.fao.org/geonetwork/srv/en/metadata.show?id=12749&currTab=simple), as well as from SOS Mata Atlântica and Instituto Nacional de Pesquisas Espaciais, 2011 ( http://mapas.sosma.org.br).

Results

The list of species, with author(s) and year of description, as well as their distributions, are presented in Tab. 1. Records indicate the presence of aeglids in rivers, lakes and streams in catchments in Argentina (14 species), Bolivia (1 species), Brazil (52 species), Chile (22 species, considering Aegla intermedia Girard, 1855), Paraguay (1 species) and Uruguay (4 species), some species occurring in more than one country ( Figs. 2, 3).

Table 1
Known species of the genus Aegla Leach, 1820, distribution, previous and current conservation status assessments according to IUCN (2012) Red List categories (CR - critically endangered; EN - endangered; VU - vulnerable; NT - near threatened; LC - least concern; DD - deficient data; EX - extinct and NE - not evaluated). The numbers in parentheses, after the name and author of the species, indicate their location in the maps of figures 2 and 3.

Figure 2
Distribution of Aegla Leach, 1820 in Argentina, Bolivia, Chile, and Paraguay (see Tab. 1 for the corresponding species number). In areas with less species diversity, we used a larger font size to facilitate the localization in the map. However, where diversity is high, to avoid overlapping the numbers, we reduced the font size, and if necessary we used a point with a line indicating the respective number.

Figure 3
Distribution of Aegla Leach, 1820 in Brazil and Uruguay (see Tab. 1 for the corresponding species number). In areas with less species diversity, we used a larger font size to facilitate the localization in the map. However, where diversity is high, to avoid overlapping the numbers, we reduced the font size, and if necessary we used a point with a line indicating the respective number.

Based on our assessment, 17 species were classified as critically endangered (CR), 21 as endangered (EN), 19 as vulnerable (VU), one as near threatened (NT), 21 as least concern (LC), three had deficient data (DD), and one was not evaluated (NE). Current and previous conservation status and the criteria used to assign each species to an IUCN category are also shown in Tab. 1.

Discussion

There are currently 83 known species of the genus Aegla, although the existence of A. intermedia is questioned. This species was described based upon specimens collected by the “U. S. N. Astronomical Expedition”, in tributaries of Maipu River, near to Santiago, Chile. Despite the effort of various researchers, the species has never been found again in nature and its type-series has disappeared ( Bond-Buckup and Buckup, 1994Bond-Buckup, G. and Buckup, L. 1994. A família Aeglidae (Crustacea, Decapoda, Anomura). Arquivos de Zoologia, 32: 159-347.). Hence, the conservation status of this species was not evaluated.

Using updated data from the species distribution, we found 57 species of Aegla under threat or almost 70% of the 82 species evaluated. This proportion represents a significant increase in relation to previous assessments for the genus Aegla, which estimated nearly half of the present value ( Bond-Buckup et al., 2008Bond-Buckup, G.; Jara, C.G.; Pérez-Losada, M.; Buckup, L. and Crandall, K.A. 2008. Global diversity of crabs (Aeglidae: Anomura: Decapoda) in freshwater. Hydrobiologia, 595: 267-273.; Pérez-Losada et al., 2009Pérez-Losada, M., Bond-Buckup, G.; Jara, C.G. and Crandall, K.A. 2009. Conservation assessment of southern South American freshwater ecoregions on the basis of the distribution and genetic diversity of crabs from the genus Aegla. Conservation Biology, 23: 692-702.). Considering the most recent conservation status assessment for each species, from the 32 species previously assessed as LC, only 20 kept the same status; nine species changed the category to some level of threat and three have deficient data. Twenty-nine species kept the same threat category, but seven previously threatened species raised the threat level. Only one species changed from a threat category to NT status ( Tab. 1).

Eighteen new species were described in the last decade (see Tab. 1). It is noteworthy that all the recently described species are under some level of threat ( Santos et al., 2009Santos, S.; Bond-Buckup, G.; Pérez-Losada, M.; Bartholomei-Santos, M.L. and Buckup, L. 2009. Aegla manuinflata, a new species of freshwater anomuran (Decapoda: Anomura: Aeglidae). Zootaxa , 2088: 31-40.; 2010Santos, S.; Bond-Buckup, G.; Pérez-Losada, M.; Jara, C.G.; Crandall, K.A. and Buckup, L. 2010. New records and description of a new species of Aeglidae (Crustacea: Anomura) from river basins in Southern Brazil. Nauplius , 18 : 79-86.; 2012Santos, S.; Bond-Buckup, G.; Buckup, L.; Pérez-Losada, M.; Finley, M. and Crandall, K.A. 2012. Three new species of Aegla (Anomura) freshwater crabs from the Upper Uruguay River hydrographic basin in Brazil. Journal of Crustacean Biology , 32: 529-540. ; 2013Santos, S.; Jara, C.G.; Bartholomei-Santos, M.L.; Pérez-Losada, M. and Crandall, K.A. 2013. New species and records of the genus AeglaLeach, 1820 (Crustacea, Anomura, Aeglidae) from the West-Central region of Rio Grande do Sul, Brazil. Nauplius , 21: 211-223 .; 2014Santos, S.; Bond-Buckup, G.; Buckup, L.; Loureiro, T.G.; Gonçalves, A.S.; Verdi, A.; Scarabino F. and Clavijo, C. 2014. The Aeglidae of Uruguay (Decapoda, Anomura), with the description of a new species of Aegla. Crustaceana Monographs, 19: 195-205.; 2015Santos, S.; Bond-Buckup, G.; Buckup, L.; Bartholomei-Santos, M.L.; Pérez-Losada, M.; Jara, C.G. and Crandall, K.A. 2015. Three new species of Aeglidae ( AeglaLeach, 1820) from Paraná State, Brazil. Journal of Crustacean Biology , 35: 839-849.; Bond-Buckup et al., 2010aBond-Buckup, G.; Jara, C.G.; Buckup, L.; Bueno, A.P.; Perez-Losada, M. and Crandall, K.A. 2010a. Description of a new species of Aeglidae, and new records of related species from river basins in Argentina (Crustacea, Anomura). Zootaxa, 2343: 18-30. ; 2010bBond-Buckup, G.; Jara, C.G.; Buckup, L.; Pérez-Losada, M.; Crandall, K.A. and Santos, S. 2010b. 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.; Moraes et al., 2016Moraes, J.C.; Terossi, M.; Buranelli, R.C.; Tavares, M.; Mantelatto, F.L. and Bueno, S.L.S. 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.). Two species previously considered extinct in the wild, Aegla expansa Jara, 1992 ( Pérez-Losada et al., 2002aPérez-Losada, M., Jara, C.G.; Bond-Buckup, G.; Porter, M.L. and Crandall, K.A. 2002a. Anomuran phylogenetic relationships: on the taxonomic positioning of Aeglidae freshwater crabs. Journal of Crustacean Biology , 22: 670-676.) and Aegla lata Bond-Buckup & Buckup, 1994 ( Pérez-Losada et al., 2009Pérez-Losada, M., Bond-Buckup, G.; Jara, C.G. and Crandall, K.A. 2009. Conservation assessment of southern South American freshwater ecoregions on the basis of the distribution and genetic diversity of crabs from the genus Aegla. Conservation Biology, 23: 692-702.), have been found again ( Galves et al., 2007Galves, W.; Jerep, F.C. and Shibatta, O.A. 2007. Estudo da condição ambiental pelo levantamento da fauna de três riachos da região do Parque Estadual Mata dos Godoy (PEMG), Londrina, PR, Brasil. Pan-American Journal of Aquatic Sciences, 2: 55-65.; Ministerio del Medio Ambiente, Chile, 2013Ministerio del Medio Ambiente, Chile. 2013. Available at http://www.mma.gob.cl/clasificacionespecies/fichas10proceso/fichas_10_pac/Aegla_expansa_10RCE_04_PAC.pdf
http://www.mma.gob.cl/clasificacionespec...
) and are currently categorized as endangered and critically endangered, respectively.

The high rate of endemism presented by many aeglid species, in association with habitat loss/fragmentation or even climatic events, has led many populations to decline ( Maia et al., 2013Maia, K.P.; Bueno, S.L.S. and 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.; Bueno et al., 2014Bueno, S.L.S.; Takano, B.F.; Cohen, F.P.A.; Moraes, J.C.B.; Chiquetto-Machado, P.I.; Vieira, L.C.M. and Shimizu, R.M. 2014. Fluctuations in the population size of the highly endemic Aegla perobae (Decapoda: Anomura: Aeglidae) caused by a disturbance event. Journal of Crustacean Biology , 34: 165-173.). Forty years ago, many species were found in several streams and rivers within a basin, but currently, most of them are restricted to low order creeks ( Bond-Buckup and Buckup, 1994Bond-Buckup, G. and Buckup, L. 1994. A família Aeglidae (Crustacea, Decapoda, Anomura). Arquivos de Zoologia, 32: 159-347.).

Threats to conservation of aeglids and other freshwater organisms in southern South America derive from different sources: removal of riparian forest, causing siltation ( Magris et al., 2010Magris, R.A.; Bond-Buckup, G.; Magalhães, C.; Mantelatto, F.L; Reid, J.W.; Loureiro, L.M.A.E.; Coelho, P.A.; Santana, W.; Buckup, L.; Rocha, S.S.; Bueno, S.L.S.; Pinheiro, M.A.A.; D’Incao, F.; Ivo, C.T.C.; Dias Neto, J.; Rodrigues, E.S.; Araujo, P.B.; Boos Jr, H. and Duarte L.F.A. 2010. Quantification of extinction risk for crustacean species: an overview of the National Red Listing process in Brazil. Nauplius, 18: 129-135.); habitat modification, fragmentation and destruction ( Cumberlidge et al., 2009Cumberlidge, N.; Ng, P.K.L.; Yeo, D.C.J.; Magalhães, C; Campos, M.R.; Alvarez, F.; Naruse, T.; Daniels, S.R.; Esser, L.J.; Attipoe, F.Y.K.; Clotilde-Ba, F.-L.; Darwall, W.; McIvor, A.; Baillie, J.E.M.; Collen, B. and Ram, M. 2009. Freshwater crabs and the biodiversity crisis: Importance, threats, status, and conservation challenges. Biological Conservation, 142: 1665-1673.; Reid et al., 2013Reid, G. McG., Contreras McBeath, T. and Csatádi, K. 2013. Global challenges in freshwater fish conservation related to public aquariums and the aquarium industry. International Zoo Yearbook, 47: 6-45.); freshwater contamination with agricultural pesticide ( Magris et al., 2010Magris, R.A.; Bond-Buckup, G.; Magalhães, C.; Mantelatto, F.L; Reid, J.W.; Loureiro, L.M.A.E.; Coelho, P.A.; Santana, W.; Buckup, L.; Rocha, S.S.; Bueno, S.L.S.; Pinheiro, M.A.A.; D’Incao, F.; Ivo, C.T.C.; Dias Neto, J.; Rodrigues, E.S.; Araujo, P.B.; Boos Jr, H. and Duarte L.F.A. 2010. Quantification of extinction risk for crustacean species: an overview of the National Red Listing process in Brazil. Nauplius, 18: 129-135.; Negro et al., 2015Negro, C.L.; Senkman, L.E.; Marino, F.; Lorenzatti, E. and Collins, P. 2015. Pesticide effects on crabs: how environmental concentrations of endosulfan and chlorpyrifos affect embryos. Journal of Environmental Science and Health, Part B, 50: 261-265.; Stehle and Schulz, 2016Stehle, S. and Schulz, R. 2016. Agricultural insecticides threaten surface waters at the global scale. Proceedings of the National Academy of Sciences, USA, 112: 5750 -5755.); construction of dams that alter the flow and sometimes the temperature of the water as well ( Olsson, 2015Olsson, G. 2015. Water and energy: threats and opportunities. Second Edition. London, IWA Publishing, 496p. ); urban and agricultural activities which modify the physical and chemical characteristics of water bodies and freshwater biota composition ( Milesi et al., 2008Milesi, S.V.; Biasi, C.; Restello, R.M. and Hepp, L.U. 2008. Efeito de metais Cobre (Cu) e Zinco (Zn) sobre a comunidade de macroinvertebrados bentônicos em riachos do sul do Brasil. Acta Scientiarum - Biological Sciences, 30: 283-289.; Hepp and Santos, 2009Hepp, L.U. and Santos, S. 2009. Benthic communities of streams related to different land uses in a hydrographic basin in southern Brazil. Environmental Monitoring and Assessment, 157: 305-318.; Hepp et al., 2010Hepp, L.U.; Milesi, S.V.; Biasi, C. and Restello, R.M. 2010. Effects of agricultural and urban impacts on macroinvertebrates assemblages in streams (Rio Grande do Sul, Brazil). Zoologia, 27: 106-113.; Magris et al., 2010Magris, R.A.; Bond-Buckup, G.; Magalhães, C.; Mantelatto, F.L; Reid, J.W.; Loureiro, L.M.A.E.; Coelho, P.A.; Santana, W.; Buckup, L.; Rocha, S.S.; Bueno, S.L.S.; Pinheiro, M.A.A.; D’Incao, F.; Ivo, C.T.C.; Dias Neto, J.; Rodrigues, E.S.; Araujo, P.B.; Boos Jr, H. and Duarte L.F.A. 2010. Quantification of extinction risk for crustacean species: an overview of the National Red Listing process in Brazil. Nauplius, 18: 129-135.); invasive species ( Palaoro et al., 2013Palaoro, A.V.; Dalosto, M.M.; Costa, G.C. and Santos, S. 2013. Niche conservatism and the potential for the crayfish Procambarus clarkiito invade South America. Freshwater Biology, 58: 1379-1391.; Loureiro et al., 2015Loureiro, T.G.; Anastácio, P.M.; Bueno, S.L.S.; Araujo, P.B.; Souty-Grosset, C. and Almerão, M.P. 2015. Distribution, introduction pathway, and invasion risk analysis of the North American crayfish Procambarus clarkii (Decapoda: Cambaridae) in Southeast Brazil. Journal of Crustacean Biology, 35: 88-96.), among others.

Threats to the family Aeglidae, specifically, have been identified and listed, as the use of biocides in wine and fruit farms in Chile, silviculture of exotic species, large-scale cultivation of potatoes and apples with extensive use of pesticides, and hog raising activities along southern rivers in Brazil ( Bond-Buckup et al., 2008Bond-Buckup, G.; Jara, C.G.; Pérez-Losada, M.; Buckup, L. and Crandall, K.A. 2008. Global diversity of crabs (Aeglidae: Anomura: Decapoda) in freshwater. Hydrobiologia, 595: 267-273.), beyond severe deforestation in Paraguay ( Satterlee et al., 2012Satterlee, S.A.; Zuercher, G.L.; Kuhle, C.W.; Ramírez-Pinto, F.; Fernández, S.; Jackson, L.; Velázquez, M.C. and Kochalka, J.A. 2012. Rediscovery of aeglid crabs in the Rio Jejuí watershed, Paraguay. Journal of Crustacean Biology , 32: 541-543.). Irrigated rice crops are responsible for the entrance of great amount of pesticides into the hydric systems ( Bhuiyan and Castañeda, 1995Bhuiyan, S.I. and Castañeda, A.R. 1995. The impact of ricefield pesticides on the quality of freshwater resources. p. 181-202. In: P.L. Pingali and P.A. Roger (eds) Impact of pesticides on farmer health and the rice environment. Kluwer Academic Publishers, Norwell.), what may constitute a threat to aeglids in southern Brazil, Uruguay, Paraguay and northwestern Argentina. These activities, although doubtless important, negatively impact the aquatic environment, and it is imperative that they respect the principle of sustainability ( Santos et al., 2012Santos, S.; Bond-Buckup, G.; Buckup, L.; Pérez-Losada, M.; Finley, M. and Crandall, K.A. 2012. Three new species of Aegla (Anomura) freshwater crabs from the Upper Uruguay River hydrographic basin in Brazil. Journal of Crustacean Biology , 32: 529-540. ). In Argentina, the exotic golden mussel Limnoperna fortunae Dunker, 1857 was reported to settle on Aegla platensis Schmitt, 1942 affecting its populations ( Darrigran and Damborenea, 2006Darrigran, G. and Damborenea, C. 2006. Características de la especie. p. 53-70. In: G. Darrigran and C. Damborenea (Eds) Bio-invasión del mejillón dorado en el continente Americano. La Plata, Univ. Nacional de La Plata. ). In Bolivia, anthropic activity and indiscriminate extraction by local people affect populations of Aegla septentrionalis Bond-Buckup & Buckup, 1994 ( Flores, 2010Flores, V.G.B. 2010. Identificación de factores que afectan la estructura poblacional del cangrejo de río ( Aegla septentrionalis) en dos vertientes del Municipio de Tupiza (Dpto. Potosí). Facultad de Agronomia, Universidad Mayor de San Andrés, La Paz, Bolívia, Graduation thesis. 104p. [Unpublished].), the only aeglid species occurring in that country.

It should also be taken into account that many aeglid species present a narrow distribution, and two species with a relatively wide distribution, Aegla longirostriBond-Buckup & Buckup, 1994Bond-Buckup, G. and Buckup, L. 1994. A família Aeglidae (Crustacea, Decapoda, Anomura). Arquivos de Zoologia, 32: 159-347. and Aegla platensis, may represent a complex of cryptic species as supported by genetic and morphogeometric evidence ( Bartholomei-Santos et al., 2011Bartholomei-Santos, M.L.; Roratto, P.A. and Santos, S. 2011. High genetic differentiation of Aegla longirostri (Crustacea, Decapoda, Anomura) populations in southern Brazil revealed by multi-loci microsatellite analysis. Genetics and Molecular Research, 10: 4133-4146. ; Marchiori et al., 2014Marchiori, A.B.; Bartholomei-Santos, M.L. and Santos, S. 2014. Intraspecific variation in Aegla longirostri(Crustacea: Decapoda: Anomura) revealed by geometric morphometrics: evidence for ongoing speciation? Biological Journal of the Linnean Society , 112: 31-39.; 2015Marchiori, A.B.; Fornel, R. and Santos, S. 2015. Morphometric variation in allopatric populations of Aegla platensis(Crustacea: Decapoda: Anomura): possible evidence for cryptic speciation. Zoomorphology, 134: 45-53.). If this is true, so the distribution area of each cryptic species will be narrower than the “grouped” species, which can result in different conservation status for each cryptic species, the reason for which data were considered deficient for these two current recognized species.

Our assessment of the conservation status of all the currently known species of Aeglidae is worrisome, with 70% of the species under some level of threat and 20% critically endangered. Measures to protect the aeglid fauna are urgent, such as the frequent monitoring of water quality in systems where the threatened species occur, following-up the species to obtain information on possible population fluctuation or decline, protecting and restoring habitats, and information spreading among the population on the importance of water courses for conserving the native fauna, as well as encouraging agricultural practices that do not harm the water quality.

Aeglids live preferentially in clean waters ( Bond-Buckup and Buckup, 1994Bond-Buckup, G. and Buckup, L. 1994. A família Aeglidae (Crustacea, Decapoda, Anomura). Arquivos de Zoologia, 32: 159-347.), presenting a high demand for oxygen ( Dalosto and Santos, 2011Dalosto, M. and Santos, S. 2011. Differences in oxygen consumption and diel activity as adaptations related to microhabitat in Neotropical freshwater decapods (Crustacea). Comparative Biochemistry and Physiology, Part A, 160: 461-466.), and thus making these crustaceans potential good indicators of water quality. Policies for continental water quality control will help to protect not only the aeglids but also the limnetic fauna as a whole.

Acknowledgements

We are grateful to Dr. Nilton Hebling, the first author's "scientific grandfather", for his wise teachings and wonderful legacy. We would like to thank CNPq for the productivity grant for SS (311142/2014-1).

References

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  • 1
    This article is part of the special series offered by the Brazilian Crustacean Society in honor to Nilton José Hebling in recognition of his dedication and contributions to the development of carcinology in Brazil.
  • 2
    Guest Editors: Maria Lúcia Negreiros-Fransozo and Adilson Fransozo

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    10 Mar 2016
  • Accepted
    01 Oct 2016
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
E-mail: editor.nauplius@gmail.com