Research Article |
Corresponding author: Fernando Luis Mantelatto ( flmantel@usp.br ) Academic editor: Ingo S. Wehrtmann
© 2014 Fabrício Lopes Carvalho, Célio Magalhães, Fernando Luis Mantelatto.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Carvalho FL, Magalhães C, Mantelatto FL (2014) Molecular and morphological differentiation between two Miocene-divergent lineages of Amazonian shrimps, with the description of a new species (Decapoda, Palaemonidae, Palaemon). In: Wehrtmann IS, Bauer RT (Eds) Proceedings of the Summer Meeting of the Crustacean Society and the Latin American Association of Carcinology, Costa Rica, July 2013. ZooKeys 457: 79-108. https://doi.org/10.3897/zookeys.457.6771
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Palaemon carteri (Gordon, 1935) and P. ivonicus (Holthuis, 1950) are morphologically similar species of South American freshwater shrimps. Past studies have questioned the taxonomic status of both species, which are supposed to have partially sympatric geographic distributions in the Amazon basin. We analyzed a 550 bp fragment of the mitochondrial 16S rRNA gene from these Amazonian Palaemon species as well as from 11 palaemonids as the outgroup. Additionally, we checked diagnostic characters of the genus and family as well as other morphological characters that have been little explored before. Palaemon carteri and P. ivonicus are allocated in two sister lineages, with wide genetic divergence and little morphological differentiation. The divergence time between these lineages was estimated as approximately 10 million years ago. Both molecular and morphological data support the taxonomic validity of both Palaemon carteri and P. ivonicus, refuting the hypothesis of synonymy. In addition, a new species, Palaemon yuna sp. n., closely related to P. ivonicus, is described. Our findings indicate that these species can be differentiated using the projection of the anterolateral margin and anterolateral spine of the first antennular segment, shape of the rostrum, and relative size of the appendix masculina.
Amazon basin, divergence time, freshwater shrimp, Palaemon yuna , taxonomy
The genus Palaemon Weber, 1795 comprises 84 marine, estuarine and freshwater species in tropical and subtropical regions, including Palaemonetes Heller, 1869, which was recently considered to be a junior synonym of Palaemon by
Palaemon carteri and P. ivonicus are freshwater species with abbreviated larval development (see
A multivariate morphometric approach was applied in order to confirm whether the two species constitute separate biological entities in the Amazon basin, and a wide plasticity and overlap in these characters among populations was found (
The occurrence of P. ivonicus in the Amazon, Orinoco and Paraguay/lower Paraná basins, however, might indicate a Miocene origin for these lineages. In this period the Orinoco and Amazon basin were widely connected and different sequences of capture of headwater might have resulted in dispersal of species across boundaries of the Amazon and Paraguay basins during the Tertiary (see
Regarding the morphological variability of this group, our study aimed to test the taxonomic status of P. ivonicus and P. carteri, as well as to verify the presence of a new species from the Negro River basin, on the basis of partial sequences of the large ribosomal subunit 16S and morphological analyses.
CCDB Crustacean Collection of the Biology Department, Faculty of Philosophy, Sciences and Letters at Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil.
CL Carapace length (measured from the posterior margin of the orbit to the posterior margin of the carapace).
CNCR National Crustacean Collection of the Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico.
INPA Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil.
OUMNH-ZC Zoological Collections of the Oxford University Museum of Natural History, Oxford, England.
MNRJ National Museum of the Federal University of Rio de Janeiro, Rio de Janeiro, Brazil.
MPEG Museu Paraense Emilio Goeldi, Belém, Brazil.
MV Museum of Victoria, Melbourne, Australia.
MZUSP Museum of Zoology of the University of São Paulo, São Paulo, Brazil.
NHM Natural History Museum, London, England.
USNM National Museum of Natural History (United States National Museum), Smithsonian Institution, Washington, D.C., USA.
MZUCR Universidad de Costa Rica, Museo de Zoología, San José, Costa Rica.
♂: male, ♀: female, ♀ov: ovigerous female.
Specimens from several localities were obtained from field collections as well as from visits to and loans from the above-mentioned carcinological collections (Fig.
Sample sites of Palaemon carteri, P. ivonicus and P. yuna sp. n. c1–Bragança, Pará; c2–Santa Maria do Pará, Pará; c3–National Forest of Amapá, Amapá; c4–Belém, Pará; i1–Solimões River, near Manaus, Amazonas; i2–Xingu River, Altamira, Pará; i3 and i4–Itacoatiara, Amazonas; AC-Acre; AM-Amazonas; AP-Amapá; MS-Mato Grosso do Sul; MT-Mato Grosso; PA-Pará and RO-Rondônia.
DNA extraction, amplification and sequencing protocols followed
Specimens of Palaemonidae used for the phylogenetic analyses. CCDB: Crustacean Collection of the Department of Biology of the Faculty of Philosophy, Sciences and Letters at Ribeirão Preto, University of São Paulo; CNCR: National Crustacean Collection of the Instituto de Biología, Universidad Nacional Autónoma de México; MPEG: Museu Paraense Emilio Goeldi; MV: Museum Victoria; MZUCR: Museo de Zoología, Universidad de Costa Rica.
Taxon | Locality | Collection accession number | GenBank |
---|---|---|---|
Creaseria morleyi (Creaser, 1936) | Yucatan Peninsula, Mexico | --- | EU448997 |
Palaemon carteri (Gordon, 1935) | (c1) Jequiri, Bragança, Pará, Brazil | MPEG 0787 | KF923721 |
Palaemon carteri (Gordon, 1935) | (c2) Santa Maria do Pará, Pará, Brazil | CCDB 4339 | KF923720 |
Palaemon carteri (Gordon, 1935) | (c3) Japim stream, National Forest of Amapá, Amapá, Brazil | MPEG 1108 | KF923727 |
Palaemon carteri (Gordon, 1935) | (c4) Mocambo, Belém, Pará, Brazil | MPEG 0628 | KF923730 |
Palaemon gracilis (Smith, 1871) | Pacific coast, Costa Rica | CCDB 3402 | KF923714 |
Palaemon hancocki Holthuis, 1950 | Golfo Dulce, Puntarenas, Pacific coast, Costa Rica | MZUCR 2477-02 | KF923715 |
Palaemon intermedius (Stimpson, 1860) | Victoria, Australia | MV J60843 | KF923725 |
Palaemon ivonicus (Holthuis, 1950) | (i1) Solimões River, Manaus, Amazonas, Brazil | CCDB 1435 | KF923717 |
Palaemon ivonicus (Holthuis, 1950) | (i2) Xingu River, Altamira, Pará, Brazil | MPEG 0715 | KF923726 |
Palaemon ivonicus (Holthuis, 1950) | (i3) Poranga, Itacoatiara, Amazonas, Brazil | CCDB 4632 | KF923728 |
Palaemon ivonicus (Holthuis, 1950) | (i4) Itacoatiara, Amazonas, Brazil | CCDB 4716 | KF923729 |
Palaemon kadiakensis (Rathbun, 1902) | Convent, Louisiana, USA | CCDB 1600 | KF923718 |
Palaemon longirostris H. Milne Edwards, 1837 | Guadiana River, Portugal | CCDB 2750 | KF923724 |
Palaemon northropi (Rankin, 1898) | Mamanguape River, Paraíba, Brazil | CCDB 4332 | KF923722 |
Palaemon pandaliformis (Stimpson, 1871) | Ilha Comprida, São Paulo, Brazil | CCDB 813 | KF923713 |
Palaemon pugio (Holthuis, 1949) | River Delta, Gautier, Mississippi, USA | CCDB 3804 | KF923723 |
Palaemon ritteri Holmes, 1895 | Bahía Wafer, Puntarenas, Pacific coast, Costa Rica | MZUCR 2396-04 | KF923719 |
Palaemon suttkusi (Smalley, 1964) | Salado River, Zaragoza, Mexico | CNCR 25864 | KF923712 |
Palaemon yuna sp. n. | Lago Tupé beach, Negro River, Manaus, Amazonas, Brazil | CCDB 4866 | KF923716 |
Sequence alignments were conducted in MAFFT alignment software (version 7.058) with default settings (
We performed four phylogenetic reconstructions: two by Bayesian inference, one by maximum likelihood and one by parsimony. All analyses were conducted using Creaseria morleyi (Creaser, 1936) as the outgroup. A consensus tree of the two Bayesian and maximum likelihood analyses was constructed by 50% majority-rule in the Mesquite package (2.75, build 566). Only posterior probabilities and bootstrap values above 50% are shown. All other software settings not mentioned below were maintained as default.
The Bayesian inferences were performed in the MrBayes software (version 3.2.2) (
The maximum likelihood (ML) analysis was conducted in the RAxML program (7.6.3) (
The maximum parsimony analysis was performed using the branch-and-bound algorithm in PAUP (version 4.0 for Unix/Linux). We conducted a bootstrap analysis with 1,000 replicates. Gaps, missing and ambiguous characters were excluded in this analysis.
The likelihood ratio test (LRT) was used to test the null hypothesis that the data evolved under a molecular clock. The likelihoods for the molecular trees, under the GTR+Γ+I model, with and without an imposed molecular clock were compared using the LRT calculator in jModelTest. The assumption of a molecular clock could not be rejected (P = 0.51). We used both a strict molecular clock and a relaxed molecular clock with independent gamma rates (IGR) in MrBayes, under the settings mentioned above, in order to estimate an approximate divergence time between the P. carteri and P. ivonicus / P. yuna lineages. We assumed the rate of 0.0083 substitutions per site per million years to corrected divergence values for the 16S rRNA gene. This rate was estimated for neotropical palaemonid species of Palaemon, assuming that the isolation of the transisthmian estuarine sibling species P. ritteri Holmes, 1895 and P. paivai Fausto Filho, 1967 (CCDB 4334) occurred about three million years ago (Carvalho et al. unpublished data), as demonstrated for other estuarine carideans (
Once the phylogenetic relationships based on molecular data were known, we analyzed adult morphological characters of South American species of Palaemon in order to verify the morphological support for the clades obtained, as well as provide new diagnoses for the P. carteri / P. ivonicus / P. yuna group.
We checked out the diagnostic characters that were traditionally used to differentiate P. carteri from P. ivonicus: position of the branchiostegal tooth, number of rostral teeth, and rostral shape (
The search for morphological differences among species was conducted using the optimized comparison method described below. Initially, all pairwise differences found between the specimens from each clade in the tree were listed. Those differences with more than 80% constancy were chosen for further validation, using the remaining specimens from the same lots used in the molecular analyses. The consistency of each difference was evaluated step-by-step, analyzing blocks of 10 specimens from each clade. Characters with less than 80% constancy were discarded and no longer analyzed in the following blocks. Additional blocks of specimens from lots that were not included in the molecular analyses were used for a final check.
The diagnostic characters found were verified in the original descriptions (
The two Bayesian analyses, maximum likelihood and parsimony analyses indicated the same topology. The mean standard deviation of the split frequencies after 107 generations was less than 0.003 for both GTR+Γ+I and HKY+Γ models. No important differences were found between the two Bayesian inferences using each model, since only slight differences were noted in the posterior probabilities of the clades and branch lengths, indicating that there is no perceptible effect of model overfitting. Similarly, only dissimilarities in the values of node support were observed between the maximum likelihood and the Bayesian inferences, with the GTR+Γ+I implemented in both analyses.
Of the 435 aligned positions (after exclusion of gaps, missing and ambiguous characters), 193 sites were variable, of which 54 (28%) were parsimony-informative. The parsimony reconstruction also showed more than 50% bootstrap values for all clades indicated by the previous analyses, with high support for most of them.
The monophyly of the P. carteri / P. ivonicus / P. yuna group was indicated in all analyses, although this clade had weak bootstrap support in the parsimony and maximum-likelihood methods. All analyses supported the existence of two sister lineages for the specimens of this group (Fig.
Bayesian (GTR+Γ+I and HKY+Γ models) and maximum likelihood 50% majority-rule consensus tree. Numbers in the nodes represent posterior probabilities (GTR+Γ+I and HKY+Γ, respectively), and bootstrap value for maximum likelihood and parsimony analyses, respectively. c1–Bragança, Pará; c2–Santa Maria do Pará, Pará; c3–National Forest of Amapá, Amapá; c4–Belém, Pará; i1–Solimões River, near Manaus, Amazonas; i2–Xingu River, Altamira, Pará; i3 and i4–Itacoatiara, Amazonas. MYBP–million years before present.
The wide genetic dissimilarity between the “Carteri” and “Ivonicus/yuna” lineages (from 10.6% to 13.7%), compared among the representative members of the genus used here (from 3.5% to 23.0%; data not shown), also supports the hypothesis that P. carteri and P. ivonicus are valid species, as well as clearly genetically divergent (Fig.
The divergence time between the “Carteri” and “Ivonicus/yuna” lineages, based on the 16S rRNA gene, was estimated as approximately 10 million years ago. This mean value varied between ~9 and ~11 Ma in our analysis, depending on the molecular-clock model used, as well as other parameter settings such as node constraints. The 95% credible intervals (highest posterior density–HDP) were 5.5–14.3 Ma using a relaxed clock, and 8.2–14.0 Ma using a strict clock.
Morphological characters supported these lineages. The morphological analysis (including the type series of all three species) of 122 specimens of P. carteri, 333 specimens of P. ivonicus and 125 specimens of P. yuna sp. n. indicated that the projection of the anterolateral margin and the anterolateral spine of the first antennular segment were useful characters to differentiate these lineages, as long as adult specimens were considered. The “Carteri” lineage had the projection of the anterolateral margin of the first antennular segment slightly shorter, not reaching the dorsal distal margin of the second segment. Additionally, the anterolateral spine of the first antennular segment usually reached the middle of the projection of the anterolateral margin (Fig.
The rostral characters (shape, relative size and number of ventral teeth of the rostrum) were helpful to differentiate P. ivonicus from P. yuna sp. n. (Fig.
Once the validity of P. ivonicus and the new species for the Negro River basin were corroborated, we provide illustrations, diagnoses, identification key as well as a description of P. yuna sp. n. in order to differentiate the three species from each other as well as from other South American species of Palaemon.
Palaemonetes carteri Gordon, 1935: 324, fig. 12;–
Palaemonetes (Palaemonetes) carteri–
Guyana, upper Cuyuni River, ♂, col. GS Carter (NHM 1935.5.20.19).
Karow Creek, 2 m NE of Penal Settlement, Mazaruni, 1 ♂; River Cuyuni, 1♀ov; Forest Swamp, upper Cuyuni, 1♂; same data as holotype, 7♂ 3♀ 1♀ov 1 juvenile (NHM 1935.5.20.20-29).
Suriname.Nickerie. Lower Naui Kreek, Southern Niew, 10♂ 10♀, col. DC Geijskes, 18 March 1971 (INPA 176). Brazil.Amapá. Floresta Nacional do Amapá, igarapé Japim, 5♂ 5♀, col. CRM Santos and JEM Nanzelor, 27 October 2009 (MPEG 1108); Porto Grande, Floresta Nacional do Amapá, tributary of rio Araguari, 1♂ 4♀, col. CRM Santos, 28 October 2009 (CCDB 2755); Macapá, stream in the home of Sr. Marcondes, 1♂ 4♀ov, col. J Cunha, 6 March 2005 (MZUSP 17676). Pará. Barcarena, Vila do Conde, 5♂ 2♀ 3♀ov, col. B Mascarenhas, 23 March 2002 (MPEG 739); Belém, Mocambo, 5♂ 5♀ov, col. FR Pimentel and R Maia, January 9 1998 (MPEG 528); Belém, Mocambo, Reserva Mocambo, 4♂ 6♀, col. FR Pimentel and J Dias, 18 June 1999 (MPEG 628); Bragança, Jequeri, Sítio Anacuã, 7♂ 9♀, 23 October 2002 (MPEG 787); Ilha do Marajó, cachoeira do Arari, 1♀, col. J Cunha and J Zuanon, 16 May 2008 (MZUSP 22753); Castanhal, 1♀ov, col. FL Carvalho et al., 14 December 2012 (CCDB 4338); Ilha de Marajó, cachoeira do Arari, rio Arari, igarapé Popudas, 1♂ 1♀, col. J Cunha and J Zuanon, 17 May 2006 (MZUSP 23224); Laranjal do Jari, igarapé Arapiranga, 2♀ 1♀ov, col. Moreira et al., 25 March 2008 (MZUSP 23225); Melgaço, Floresta Nacional de Caxiuanã, 5♂ 4♀, 8 November 1999 (MPEG 717); Santa Maria do Pará, 3 juveniles, col. FL Carvalho et al., 15 December 2012 (CCDB 4339); Tucuruí, rio Tocantins basin, igarapé Santos, 2♀, col. W Zuink and LCF Alvarenga, 16 September 1984 (MNRJ 23382).
Mandibular palp absent. Rostrum slender, curved upward, reaching or just overreaching the tip of the scaphocerite; dorsal margin with 6 to 10 teeth; ventral margin with 3 to 7 teeth, usually 4 or more. Projection of the anterolateral margin of the first antennular segment overreaching the middle of the second segment, but not reaching, sometimes almost reaching, the dorsal distal margin of the second segment; anterolateral spine of the first antennular segment usually reaches the middle of the projection of the anterolateral margin. Appendix masculina up to 1.1 the length of the appendix interna, measured from their junction. Telson carrying 2 plumose setae between the inner distal stout setae; inner distal stout setae overreaching the distal tip of the telson.
Venezuela (Amazonas, Bolívar, Delta Amacuro, Monagas), Guyana, Suriname, French Guiana, Brazil (eastern Amazon: Amapá, Pará).
Usually associated with riparian vegetation, leaf litter and similar microhabitats in lakes, streams and rivers, in areas with low flow. At least in the Amazon river basin, its occurrence is usually associated to clear water river systems.
Palaemonetes ivonicus Holthuis, 1950a: 98;–
Palaemonetes carteri–
Palaemonetes (Palaemonetes) ivonicus–
Palaemonetes (Palaemonetes) carteri–
Bolivia, Beni, Ivon, Beni River, ♀ (CL 7.5 mm), col. WM Mann, February 1922 (USNM 85234).
same data as holotype, 1♀ (CL 6.6 mm) (USNM 85234).
Brazil.Acre. Bujari, igarapé Mapinguari, 2♂ 18♀, col. LR Malabarba et al., 8 August 2001 (UFRGS 3179). Amazonas. Itacoatiara, canal Irandiba, 3♂, col. GY Hattori, April 2008 (CCDB 2753); Itacoatiara, igarapé Aeroporto, 2♂ 18♀ (CCDB 4725); Itacoatiara, Poranga, 7♂ 23♀ (CCDB 4632); Itacoatiara, 3♂ 15♀ (CCDB 4716); rio Madeira, Borba, 1♂ 9♀ (MNRJ 1078); rio Solimões, igarapé do Xiboreno, 1♂ 1♀, col. FL Carvalho and EA Souza-Carvalho, 28 January 2012 (CCDB 1435); rio Solimões, lago Janauacá, 1♀, col. J Donnath, 18 March 1978 (MZUSP 8183); rio Solimões, lago do Jacaré, 2♀, col. H Reichardt, 29 March 1967 (MZUSP 6405); Tefé, igarapé da Aeronáutica, 12♂ 8♀, col. JO Chaves, 21 March 1979 (INPA 128). Pará. Almeirim, rio Arraiolos, pesqueiro São Paulo, 7♂ 5♀, col. J Carvalho Júnior, 26 July 1999 (MPEG 689); Altamira, rio Xingu, 4♀, col. RM Sousa and Dionísio, 18 December 2000 (MPEG 715); Porto de Moz, rio Xingu, 1♂ 1♀ov, col. R Robles et al., 25 September 2013 (CCDB 4867); rio Tapajós, near the rio Cupari’s mouth, downstream Itaiatuba, 1♀, col. C Magalhães and LH Py-Daniel, 27 October 1991 (INPA 1176); Santarém, igarapé do Juá, 2♀, col. LM Sousa and JL Birindelli, 13 November 2006 (MZUSP 28358). Rondônia. Rio Guaporé, 1♂ 2♀, col. JC Malta, 25 September 1985 (INPA 326). Mato Grosso. Acorizal, 17♂ 6♀, col. Sebastiana, 28 August 1987 (MNRJ 1151); Acorizal, 9♂ 5♀ 4 juveniles, col. Sebastiana (MNRJ 1153); baía do Pio, Pantanal, 5♂ 15 juveniles, col. Sebastiana (MNRJ 1152); Poconé, baía do Pio, 14♂ 33♀ 19 juveniles (INPA 328). Mato Grosso do Sul. Rio Negro, córrego Anhumas, 9♂ 11♀, col. C Magalhães et al., 28 August 1998 (CCDB 4667). Peru.Loreto. Lago Urcococha, rio Amazonas, 10♂ 5♀, col. C García-Dávila, 10 January 1999 (INPA 883); Quistococha, río Itaya, 12♂ 7♀ov, col. C García-Dávila, 13 July 1998 (INPA 882).
Mandibular palp absent. Rostrum high, straight or slightly curved upward, not overreaching the scaphocerite; dorsal margin with 6 to 10 teeth; ventral margin with 1 to 4 teeth, usually 3 or fewer. Projection of the anterolateral margin of the first antennular segment reaching or overreaching the dorsal distal margin of the second segment; anterolateral spine of the first antennular segment almost reaching or overreaching the first third of the projection of the anterolateral margin. Appendix masculina up to 1.5 the length of the appendix interna, measured from their junction. Telson carrying 2 plumose setae between the inner distal stout setae; inner distal stout setae overreaching the distal tip of the telson.
Venezuela? (Delta Amacuro, Monagas), Colombia? (Amazonas, Arauca, Casanare, Guainía, Meta, Vichada), Brazil (Acre, Amazonas, Mato Grosso, Mato Grosso do Sul, Pará), Bolívia (Beni, Cochabamba, Pando), Peru (Loreto, Madre de Díos), Paraguay.
Usually associated with riparian vegetation, leaf litter and similar microhabitats in lakes, streams and rivers with white or clear water, in areas with low flow. In the western portion of the Amazon river basin it is commonly found in the floodplains of the white water river systems.
Palaemonetes (Palaemonetes) carteri–
Palaemonetes carteri–
Palaemonetes ivonicus–
Lago Tupé beach, lower Rio Negro tributary, Manaus, Amazonas, Brazil (003°02'42"S, 060°15'10"W), ♂, col. FL Carvalho and EA Souza-Carvalho, 27 January 2012 (CCDB 4865).
same data as holotype, 28♂ 8♀ 17♀ov (CCDB 4866); same data as holotype, 10♂ 3♀ 3♀ov (INPA 2016); same data as holotype, 1♂ 1♀ 1♀ov (OUMNH-ZC 2013-08-001).
Brazil.Amazonas. Parque Nacional de Anavilhanas, lake near the rio Apuaí’s mouth, 1♂ 1♀, col. J Zuanon, 20 August 2005 (INPA 1432); Manaus, Rio Negro basin, Igarapé do Camarão, 20♀ov, col. O Odinetz-Collart et al., 28 February 1989 (CCDB 4726); Rio Negro basin, igarapé Alagadiço, 20♂, col. O Odinetz-Collart et al., 17 January 1989 (CCDB 4727); São Gabriel da Cachoeira, igarapé Barixia, right bank of the Rio Negro, 4♀, col. J Cunha et al., 14 December 2005 (MZUSP 16907); Santa Izabel do Rio Negro, 2♀, 24 October 1972 (MZUSP 13645); rio Uatumã, near the igarapé do Miriti’s mouth, 1♂ 3♀, col. C Magalhães, 12 July 1985 (INPA 173).
Mandibular palp absent. Rostrum slender, slightly curved upward at the distal half, overreaching the scaphocerite; dorsal margin with 6 to 10 teeth; ventral margin with 2 to 5 teeth, usually 3 or 4. Projection of the anterolateral margin of the first antennular segment reaching the dorsal distal margin of the second segment; anterolateral spine of the first antennular segment not overreaching the first third of the projection of the anterolateral margin. Appendix masculina up to 1.1 the length of the appendix interna, measured from their junction. Telson carrying 2 plumose setae between the inner distal stout setae; inner distal stout setae overreaching the distal tip of the telson.
Carapace glabrous. Sub-orbital lobe and pterygostomial angle rounded. Branchiostegal suture located approximately with a half of the distance between the antennal and branchiostegal tooth. Branchiostegal tooth almost as strong as the antennal, placed behind the anterior margin of the carapace.
Rostrum slender, slightly curved upward at the distal half, overreaching the scaphocerite (Fig.
Palaemon yuna sp. n. Figure a holotype; figures b–n paratype (CCDB 4866, male, CL 5.5 mm). a anterior part of the carapace b right eye, dorsal view c left scaphocerite, ventral view d left mandible, ventral view e left maxillula, ventral view f left maxilla, ventral view g left second maxilliped, ventral view h left first maxilliped, ventral view i left first maxilliped, dorsal view j right third maxilliped, ventro-lateral view k right second pereiopod, ventro-lateral view l right first pereiopod, ventro-lateral view m right first chela, mesial view n right second chela, mesial view. Scale bar: a, c, k equal to 1 mm; others equal to 0.5 mm.
Eye well developed with pigmented cornea (Fig.
Antennular peduncle not reaching the distal margin of the scaphocerite; first antenular segment with outer margin slightly convex and projection of the anterolateral margin rounded, reaching the dorsal distal margin of the second segment (Fig.
Scaphocerite slender (Fig.
Mandibular palp absent; incisor process with three teeth on both sides (Fig.
Thoracic sternal armature sexually similar. First thoracic sternite with an acute tooth and a conspicuous transverse ridge; second without tooth, bearing a triangular transverse ridge. Third to fifth without tooth and ridge incomplete.
First pereiopod slender (Fig.
Second pereiopod slender (Fig.
Third pereiopod (Fig.
Palaemon yuna sp. n. Figures i and m holotype; figures a–e, g, h, j–l paratype (CCDB 4866, male, CL 5.5 mm); figure f paratype (CCDB 4866, female, CL 5.5 mm). a left third pereiopod, lateral view b left fourth pereiopod, lateral view c distal portion of the left fifth pereiopod, lateral view d left fifth pereiopod, lateral view e left first pleopod, posterior view f left first pleopod, posterior view g left second pleopod, posterior view h left appendix masculina and appendix interna, posterior view i right posterior part of the abdomen, lateral view j pre-anal fig, ventral view k telson and uropods, dorsal view l distal part of the telson, dorsal view m left distal portion of the exopod of the uropod, dorsal view. Scale bar: a, b, d–g, i, k equal to 1 mm; c, j, m equal to 0.5 mm; h, l equal to 0.25 mm.
Fourth pereiopod slender (Fig.
Fifth pereiopod slender (Fig.
First pleopod without appendix interna and sexually dimorphic in proportions; males with endopod 0.5 the length of exopod (Fig.
Abdominal sternal armature sexually dimorphic; males with first and second sternites bearing median process; second more acute and bigger than the first process; females with median process less develop than males.
Abdominal pleura furnished with plumose setae on ventral margin; fifth pleuron elongated and disto-ventrally rounded (Fig.
Telson as long as sixth pleonite; dorsal surface with two pairs of cuspidate setae (Fig.
Uropods overreaching the telson by 0.3 of the length of exopod; exopod 1.25 times the length of endopod; mobile distolateral setae of exopod weak, reaching about the middle of the fixed tooth (Fig.
Brazil (Amazonas, Pará?), Venezuela? (Apure).
Usually associated with riparian vegetation, leaf litter and similar microhabitats in lakes, streams and rivers of black or clear water river systems, in areas with low flow.
The specific epithet is derived from the Tupi, the general language of the Brazilian indigenous people: y = water, river + úna = black, alluding to the environment where the species was first found (Fig.
1 | Projection of the anterolateral margin of the first antennular segment not overreaching the middle of the second segment | other South American Palaemoninae |
– | Projection of the anterolateral margin of the first antennular segment overreaching the middle of the second segment | 2 |
2 | Mandibular palp present | other South American Palaemoninae |
– | Mandibular palp absent | 3 |
3 | Projection of the anterolateral margin of the first antennular segment not reaching, rarely almost reaching, the dorsal distal margin of the second segment; anterolateral spine of the first antennular segment usually reaching the middle of the projection of the anterolateral margin (Fig. |
Palaemon carteri |
– | Projection of the anterolateral margin of the first antennular segment reaching or overreaching the dorsal distal margin of the second segment; anterolateral spine of the first antennular segment not reaching the middle of the projection of the anterolateral margin (Fig. |
4 |
4 | Rostrum high, straight or slightly curved upward, not overreaching the scaphocerite; rostrum with 1 to 4 ventral teeth (usually 3 or fewer) (Fig. |
Palaemon ivonicus |
– | Rostrum slender, slightly curved upward, overreaching the scaphocerite; rostrum with 2 to 5 ventral teeth (usually 3 or 4) (Fig. |
Palaemon yuna sp. n. |
Both molecular and morphological data support the validity of P. ivonicus, refuting the hypothesis that this species is a junior synonym of P. carteri. The two species are allocated in two sisters Amazonian lineages, with great genetic divergence and morphological support. Additionally, a third species closely related to P. ivonicus is described.
The projection of the anterolateral margin and anterolateral spine of the first antennular segment seems to be an important character in this group, although we have found some specimens with a state of character close to an intermediate form, making difficult a clear distinction between these lineages. Additionally, there is an ontogenetic variation, which needs to be considered in the analyses. Some large specimens of the “Carteri” lineage have the antennular projection almost reaching the dorsal margin of the second segment. On the other hand, some small specimens of the “Ivonicus/yuna” lineage also have the projection almost reaching the dorsal margin of the second segment. However, even considering those limitations, the antennular character was the most constant one to distinguish the “Carteri” and “Ivonicus/yuna” lineages. Therefore, we suggest that this character must be evaluated in further morphological analyses within the Palaemon genus.
The wide intraspecific morphological variability and interspecific similarity between P. carteri and P. ivonicus as well as the presumptive synonymy have been reported by previous studies since the 1970s (
The overlapping of several morphological characters demonstrated by
The wide genetic dissimilarity between the “Carteri” and “Ivonicus/yuna” lineages shows that they have no recent divergence, as one could expect based only on their morphological similarity. The approximately 10 million years of divergence estimated for these lineages, based on the 16S rRNA gene, may be associated with marine incursion as well as colonization of different environments in western Amazonia during the Middle Miocene (~16 to 11.6 Ma) and Late Miocene (~11.6 to 5.3 Ma) (Fig.
The specimens from the Negro River (P. yuna sp. n.) have considerable genetic divergence from the specimens collected in the Solimões-Amazon and Xingu rivers, being allocated outside the P. ivonicussensu stricto clade. The specimens from the Negro River also show some differences in the rostrum, in the antennular characters and in the appendix masculina compared to specimens from the type locality of P. ivonicus as well as other basins (Figs
Specimens from the upper Orinoco River basin have antennular characters similar to those of P. yuna sp. n. Nevertheless, some specimens fail to have a curved upward rostrum overreaching the scaphocerite. The connection between the Negro and Orinoco river basins through the Casiquiare River opens the possibility of the existence of a conspecific group occurring in the Negro and Orinoco rivers. A similar biogeographical pattern has been reported for fish species, using molecular data (
The occurrence of P. ivonicus in the Paraguay/lower Paraná River basin is an issue that needs further analyses in order to verify the phylogenetic relationships of these populations. As discussed by
An additional record of P. ivonicus from the São Francisco River basin, state of Minas Gerais, Brazil (
The fact that our target group seems to be closer related to three neotropical species of Palaemon (P. gracilis, P. hancocki and P. pandaliformis) than to other species of the genus require further studies.
Our study is part of a project aiming to investigate the American species of Palaemon, and this is the first one which uses a multidisciplinary approach aiming to clarify this taxonomic issue. Our data clearly show that there are at least two morphologically and genetically distinct lineages, which might have diverged ~10 Ma. A multilocus approach is needed to provide more molecular support for this estimated divergence time. The possibility of hybridization cannot be rejected and must be deeply investigated in further studies. Moreover, the morphological variability found in some populations still assigned to P. ivonicus as well as the molecular variability found within the “Carteri” lineage need to be further investigated to verify whether there are other morphologically similar species not yet described.
The present study is part of a long-term project to evaluate the taxonomy of freshwater decapods in Brazil, and was supported by scientific grants provided to FLM by the São Paulo Research Foundation–FAPESP (2002/08178-9, 2009/54931-0 and 2010/50188-8) and the Conselho Nacional de Desenvolvimento Científico e Técnológico–CNPq (472746/2004-9, 491490/2004-6, 473050/2007-2, 471011/2011-8, 504322/2012-5; Research Scholarships PQ 301261/2004-0, 301359/2007-5, 302748/2010-5), and to CM by CNPq (Research Scholarships PQ 304468/2009-6, 303837/2012-8). FLC is supported by PhD fellowship from CNPq (140199/2011-0) and “Sandwich” PhD fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–CAPES (7711-13-1). We are grateful to the Department of Biology and Postgraduate Program in Comparative Biology of the FFCLRP/USP and Instituto Nacional de Pesquisa da Amazônia–INPA for partial financial and logistic support, to the Xingu Project funded by the U.S. National Science Foundation (DEB-1257813) and CNPq (Proc. N° 1300.001303/2011-2) for providing some specimens from the Xingu River, and to many colleagues and friends (Cléverson Santos, Darryl Felder, Edinaldo Nelson dos Santos-Silva, Edvanda Souza-Carvalho, Emmanoela Ferreira, Fernando Alvarez, Gary Poore, Ingo Wehrtmann, Irene Cardoso, José Luis Villalobos, José Montoya, Joana Palma, Marcos Tavares, Mariana Terossi, Natalia Rossi, Rafael Robles, Ray Bauer, Tatiana Magalhães) for helping in collections, making available some essential specimens and information, lending material from collections used in our research, and for critical discussion during the preparation of this manuscript. Special thanks to all members of LBSC for their assistance during the development of this study, to Dr. Janet Reid (JWR Associates) for providing the English review service, to anonymous reviewers and Ingo Wehrtmann for all comments and suggestions.