Snapping shrimps of the genus Alpheus Fabricius, 1798 from Brazil (Caridea: Alpheidae): updated checklist and key for identification

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The genus Alpheus includes 296 valid species worldwide (De Grave and Fransen, 2011;Anker, 2012;Anker and De Grave, 2012;Almeida et al., 2013;Anker and Pachelle, 2013), the most of any genus of caridean shrimps.However, this number represents an underestimate of the actual diversity of the taxon.Empirical evidence and molecular studies point to the existence of cryptic diversity in Alpheus (Anker et al., 2006;
A total of 52 species of Alpheus have been recorded in the western Atlantic (Anker, 2012;Almeida et al., 2013), and most of them have been reported for the Brazilian coast.However, some of the Brazilian records need to be confirmed because many taxa belong to species complexes as mentioned above, but also because some records were published in general lists of species from certain localities and regions, without morphological descriptions and illustrations of diagnostic characters or color patterns [e.g., A. armatus Rathbun, 1901, A. belli Coutière, 1898, A. candei Guérin-Méneville, 1855 and A. macrocheles (Hailstone, 1835) (Coelho et al., 1983;Guterres et al., 2005;Coelho Filho, 2006;Alves et al., 2008)].Confirmation of some doubtful records is difficult because in some cases the reported material was not deposited in any carcinological collection or is no longer available (damaged).Other species are indeed rare, and it is difficult to obtain new samples for analysis.
Studies of the species of Alpheus from Brazil began in the mid-19th century.Dana (1852), describing A. malleator based on material collected by the U.S. Exploring Expedition, mentioned that the type material was probably from Rio de Janeiro.Spence Bate (1888) described A. intrinsecus from off Salvador, based on a specimen collected during the Challenger Expedition.Pocock (1890) and Coutière (1898) described A. ridleyi Pocock, 1890 (a junior synonym of A. websteri Kingsley, 1880) and A. belli Coutière, 1898 [possible junior synonym of A. malleator (see Anker and Pachelle, 2013)], respectively, from Fernando de Noronha Archipelago.Rathbun (1900), studying the material obtained by the Branner-Agassiz Expedition in northeastern Brazil, attributed the new name A. cristulifrons to material from Fernando de Noronha reported by Pocock (1890) as Alpheus obeso-manus Dana, 1852. Christoffersen (1979) studied the taxonomy of the Alpheoidea collected during the Calypso Expedition, which carried out sampling along the Brazilian coast in 1961, and also included other material from the western Atlantic in his analyses.His study included 11 species of Alpheus from Brazil, and descriptions of the new taxa A. maxilliplanus Christoffersen, 1979, A. pouang Christoffersen, 1979 andA. puabeba Christoffersen, 1979; the type localities of the first two are on the coasts of Sergipe and São Paulo, respectively.Christoffersen (1984), revising a group of species morphologically similar to A. heterochaelis Say, 1818, described A. estuariensis Christoffersen, 1984 (type locality: estuary of the Potengi River, Rio Grande do Norte), and considered A. maxilliplanus a junior synonym of A. chacei Carvacho, 1979.Besides these major taxonomic works, species of Alpheus from Brazil have been recorded in several lists of species (e.g., Coelho and Ramos, 1972;Fausto Filho, 1974;Christoffersen, 1998;Coelho et al., 2006;Coelho Filho, 2006;Santos et al., 2012), some of them of great historical importance (e.g., Smith, 1869;Moreira, 1901;Luederwaldt, 1919).A few ecological and biological studies (Mossolin et al., 2006;Pavanelli et al., 2008Pavanelli et al., , 2010;;Rodrigues et al., 2009) or larval descriptions (Pires et al., 2008) have been published.
In recent years, several new species were described from the western Atlantic, some of which have been reported from the Brazilian coast, such as A. brasileiro Anker, 2012 (type locality: Fortaleza area and Camocim, Ceará), A. carlae Anker, 2012, A. christofferseni Anker, Hurt andKnowlton, 2007 (type locality: Cemitério Island, Atol das Rocas) and A. rudolphi Almeida and Anker, 2011 (type locality: off Alagoas) (Anker et al., 2007a(Anker et al., , 2009;;Almeida and Anker, 2011;Anker, 2012).Some recent descriptions of new taxa are the product of taxonomic revisions of complexes of cryptic species (Anker et al., 2007a(Anker et al., , 2009;;Anker, 2012;Almeida et al., 2013).Alpheus vanderbilti Boone, 1930, which until recently was believed to be a junior synonym of A. cylindricus Kingsley, 1878a, was resurrected after revision (Anker et al., 2008d).Alpheus cylindricus is currently restricted to the eastern Pacific, and the previous records of this species from Brazil (e.g., Coelho and Ramos, 1972;Christoffersen, 1998) correspond to A. vanderbilti (Anker et al., 2008d).On the other hand, A. agilis Anker, Hurt andKnowlton, 2009 andA. buckupi Almeida, Terossi, Araújo-Silva andMantelatto, 2013 (type locality: Timbó River, Pernambuco) were recognized as new species of amphi-Atlantic distribution.Finally, species that have long been recorded along the Brazilian coast, such as A. heterochaelis and A. armillatus H. Milne Edwards, 1837 (see Christoffersen, 1984), may not occur in Brazil.New evidence suggests that A. heterochaelis is a species complex (A.O.Almeida, under study).The A. armillatus complex was recently revised, and the occurrence of the sensu stricto form was not confirmed in Brazil (see Anker, 2012).
The process of identifying species of Alpheus is difficult, not only because it is a taxonomically complex group, including several cryptic lineages as mentioned above, but also because of the scarcity of keys for identification and illustrations of the diagnostic characters for regional faunas.Therefore, our present objective is to provide an updated list of members of the shrimp genus Alpheus from Brazil, including all recent changes regarding species composition, as well as a key for their identification, with illustrations of the main characters of taxonomic significance and photographs of color patterns of some species.

MATERIAL AND METHODS
The Brazilian coast is about 8,500 km long (Lavrado, 2007).The checklist contains species recorded from coastal areas extending from Cape Orange, northern Amapá State (04°17'N / 51°32'W) to the mouth of Chuí Stream, southern Rio Grande do Sul State (33°45'S / 53°23'W) (Fig. 1).Oceanic areas include: (1) the seamounts of the North Chain (= seamounts off Ceará) (01°00'-04°00'S / 37°00'-39°00'W) (Coelho Filho, 2006); (2) the Atol das Rocas (03°45'-03°56'S / 33°37'-33°56'W), 260 km east of Natal, Rio Grande do Norte State (Kikuchi, 2000); (3) the Fernando de Noronha Archipelago (03°45'-03°57'S / 32°19'-32°41'W), located 345 km east off the coast of Rio Grande do Norte (Leão and Dominguez, 2000); and (4) the seamounts of the Vitória-Trindade Chain, which extends over about 1,000 km (approx.20-21°S / 28-38°W) off the coast of Espírito Santo State, southeastern Brazil (Ferrari and Riccomini, 1999).The eastern limits of this chain are Trindade Island (20°28'-20°32' / 29°17'-29°20'W) and the Martin Vaz Archipelago (20°30'-20°31' / 28°51'-29°20'W), located about 1,100 and 1,145 km off the Espírito Santo coast, respectively (Castro and Antonello, 2006) (Fig. 1).The key for identification was developed taking as a starting point the adaptation of the keys proposed by Chace (1972) for species of Alpheus from the Caribbean Sea, by Christoffersen (1984) for species related to A. heterochaelis, and by Anker (2012) for the A. armillatus complex.Morphological characteristics of each taxon were also obtained through examination of the available material, complemented with descriptions of the species obtained in the literature.Illustrations of the main diagnostic characters are provided to facilitate the identification process (Figs. 2,  3).Color photographs of 16 species collected by the authors on the coast of Bahia are also provided to facilitate the identification of fresh specimens, since some taxa listed in this study can only be distinguished by analysis of their coloration in life.For each species, we provide the reference to the original description and the distribution, as well as a list of previous records for the Brazilian coast.Comments on dubious records or taxonomic remarks are provided.The existence of illustrations based on Brazilian material, when available, is also mentioned.The species marked with an asterisk had material examined in this study.We used the status cf.(e.g., Alpheus cf.floridanus Kingsley, 1878a) to designate a taxon belonging to a species complex which has not been taxonomically revised and the identity of the Brazilian material remains unknown.
The longitudinal and latitudinal distribution patterns (see discussion) were classified based on the proposal of Melo (1985).In the western Atlantic, the species are treated as having disjunct distributions where the gap in their range corresponds at least to the Guyana region (Guyanas, Amapá, and Pará) (Coelho and Ramos, 1972).
Remarks: In the western Atlantic, A. agilis is presently known only from Atol da Rocas (Anker et al., 2009).
Remarks: Due to their similarity, part of the western Atlantic records of A. macrocheles (Hailstone, 1835) may refer to A. amblyonyx (see also remarks on A. macrocheles).The only published illustrations of the Brazilian material were provided by Christoffersen (1979;Bahia: fig.1).
Remarks: Material reported by Coelho et al. (1983) and subsequently by Coelho et al. (1990Coelho et al. ( , 2006) ) may correspond to A. rudolphi (see Almeida and Anker, 2011).For this reason, the occurrence of A. armatus in Brazil remains to be confirmed.
Remarks: Alpheus buckupi (type locality: Timbó River, Pernambuco), distributed in the western and eastern Atlantic, was recently recognized as new based on morphological and molecular data.The resemblance between that species and members of the A. lobidens De Haan, 1850 complex indicated they are cryptic taxa (Almeida et al., 2013).Illustrations, including drawings and colour photographs, from Brazilian material were provided by Almeida et al. (2013;Pernambuco  Distribution: Western Atlantic -Florida (Dry Tortugas), Cuba, Dominica?, Colombia, and Brazil (Seamounts of the North Chain) (Chace, 1972;Martínez-Iglesias et al., 1997;Coelho Filho, 2006).
Remarks: Alpheus candei has only been recorded from Brazil in listings (Coelho and Ramos, 1972;Coelho Filho, 2006).Actually, the record of Coelho and Ramos (1972) from Rio de Janeiro consists of a misidentification (= A. puapeba, see Christoffesersen, 1979).For this reason, Christoffersen (1998) did not include the species in his list of Brazilian species of Alpheus.A new record of A. candei was provided by Coelho Filho (2006) from the seamounts of the North Chain, although with no reference to morphological characters or illustrations.
Remarks: The only illustrations of this species from Brazil were provided by Christoffersen (1979, figs. 11-13), when describing A. maxilliplanus, a junior synonym of A. chacei (see Christoffersen, 1984), described by him from Sergipe.
Remarks: Illustrations of the type material from Atol das Rocas were provided by Anker et al. (2007a, figs. 1-3).
Remarks: Alpheus macrocheles is very similar to A. amblyonyx, and its occurrence in the western Atlantic has long been discussed.In fact, some authors considered all western-Atlantic material as belonging to the latter species (e.g., Chace, 1972;Christoffersen, 1979).On the other hand, possible morphological differences between material of A. macrocheles from Brazil and A. amblyonyx were also observed (Ramos-Porto, 1979).According to Anker and De Grave (2012), all records of A. macrocheles in the western Atlantic must be treated with caution because they may actually represent A. amblyonyx or other species of the complex present in the western Atlantic.Drawings of the Brazilian material from Maranhão ("Estampas" 1-3, 5, 6) and Amapá ("Estampa" 4) were provided by Ramos-Porto (1979).
Remarks: According to Dana (1852a), the type locality of A. malleator is probably Rio de Janeiro.Drawings of the holotype were published by Dana (1852b;pl. 35, fig.9a-h).In a recent revision of the A. malleator species complex, A. malleator was recognized as the species occurring in the Atlantic basin and a full specific status was given to the eastern Pacific form (A. wonkimi Anker and Pachelle, 2013) (Anker and Pachelle, 2013).Moreover, those authors also tentatively synonymized A. belli and A. malleator.Alpheus belli was described by Coutière (1898) from Fernando de Noronha and, since then, it has been reported from Brazil only from that archipelago (Christoffersen, 1998;Coelho et al., 2006;Alves et al., 2008;Souza et al., 2011).Unfortunately, the holotype of A. belli is apparently no longer available and the synonymy proposal was based on drawings and comments provided by Coutière (1998) in the original description (see Anker and Pachelle, 2013).Analysis of material from the type locality is highly desirable in order to confirmate the status of that species.
Remarks: Most Brazilian records of A. packardii were given as A. normanni, an eastern-Pacific species (see Kim and Abele, 1988), or as A. beanii, a junior synonym of A. packardii (see Christoffersen, 1979).However, the taxonomy of A. normanni and A. packardii remains unsettled due to the presence of cryptic taxa on both sides of the Americas (Williams et al., 2001;A. Anker, under study).Currently, the true identity of the material from Brazil remains unknown.Santos et al. (2012, fig. 3H) provided a color photograph of material from Bahia.
Remarks: Color-pattern analyses as well as preliminary molecular data indicate that A. paracrinitus is a species complex (Knowlton and Mills, 1992;Anker, 2001;Williams et al., 2001;Almeida et al., 2012;A. Anker, under study).For this reason, the true identity of the Brazilian material remains uncertain and all records of this species from Brazil must be treated with caution (Almeida et al., 2012).Color photographs of material from Bahia were provided by Almeida et al. (2012, fig. 2D) and Santos et al. (2012, fig. 3I).
Remarks: The original description of A. pouang contains illustrations of the holotype, from off São Paulo and of a paratype from Rio Grande do Sul (Christoffersen, 1979, figs. 14 and 15 respectively).
Remarks: The only illustrations available are those in the original description, of the holotype and a paratype from Argentina (Christoffersen, 1979, figs. 16-18).
Remarks: Alpheus cf.rostratus may represent a new species of the A. paracrinitus complex.The occurrence of this form, recognized by its color pattern, has only been documented from Bahia [see color photographs provided by Almeida et al. (2012, fig. 2E) and Santos et al. (2012, fig. 4A)], but it is possibly widespread along the northeastern Brazilian coast where suitable hard substrata are available.For more details, see Almeida et al. (2012) and Santos et al. (2012).Distribution: Western Atlantic -Brazil (Alagoas) (Almeida and Anker, 2011).
Remarks: Line drawings and a color photograph of Brazilian material were provided by Bezerra and Almeida (2008, fig.2) and Santos et al. (2012, fig. 4B), respectively.
Remarks: The occurrence of A. cylindricus, previously believed to be distributed in the Atlantic and the eastern Pacific, now appears to be restricted to the latter basin (see Anker et al., 2008d).
Remarks: Anker (2012) pointed out that the status of the Brazilian material requires confirmation, based on minor morphological and color-pattern differences observed by him.A color photograph of a specimen from São Paulo was provided by Anker (2012, fig. 18D).
Remarks: The record from Alagoas, which would be the current southern limit of the distribution of A. websteri in the western Atlantic, needs confirmation because of a possible mistaken identification of A. thomasi (see Anker et al., 2008b).Drawings of the material from Atol das Rocas were provided by Anker et al. (2008b, fig. 2).

DISCUSSION
Of the 33 species of Alpheus recorded from Brazil, 31 occur in shallower waters (less than 100 m deep) and two at depths over 100 m (A.pouang from 120 to 268 m and A. puapeba from 45 to 175 m; see Christoffersen, 1979).The former group comprises tropical species ranging, in the western Atlantic, mostly from North Carolina, Florida or the West Indies to southern Brazil; whereas the latter group includes subtropical species ranging from southeastern Brazil to Uruguay (A. pouang) or Argentina (A. puapeba) (sensu Christoffersen, 1982).
A more accurate analysis of the geographic distribution of certain shallow-water caridean groups is difficult at present, mainly because of factors such as the existence of areas or habitats that are still underexplored, the little-known ranges of some recently described species (e.g., A. agilis, A. christofferseni, A. rudolphi), the difficulty of collecting some small-sized and (ecologically) cryptic or symbiotic taxa, and the existence of a number of (morphologically) cryptic species complexes, especially in the Alpheidae (Almeida et al., 2012).
Twenty-one of the 33 species currently known from Brazil are restricted to the western Atlantic, and eight are amphi-Atlantic (Table 1).The remaining four taxa treated here for which the status still needs to be confirmed were not included in this classification.According to Melo's (1985) patterns of latitudinal distribution, the group of western Atlantic species comprises 14 Antillean, 2 Carolinian, 2 Argentinian, 1 Virginian, and 2 species that are presently endemic to Brazil (Table 1).Regarding the amphi-Atlantic species, eastern-and western-Atlantic populations of A. intrinsecus, A. pontederiae and A. macrocheles have not been examined for possible cryptic biodiversity.

A. bouvieri
A. paracrinitus species complex; identity unknown (Williams et al., 2001;Almeida et al., 2012;A. Anker, pers. com 1. Snapping shrimps of the genus Alpheus Fabricius, 1798 from the Brazilian coast the northern and southern limits of their geographic ranges in the western Atlantic Ocean, patterns of distribution according to Melo (1985), and taxonomic observations.
to the oceanographic conditions in that coastal area, which is mainly characterized by low salinity and predominance of soft bottoms (Coelho, 1969;Coelho and Ramos, 1972).
In fact, several of the species with disjunct distributions usually inhabit intertidal and/ or shallow-water hard bottoms, including coral reefs; examples include A. cristulifrons, A. formosus, A. peasei and A. simus.With increased collection effort in these gap regions, it may be observed that some of these alpheids actually have continuous distributions, when there are suitable habitats.However, in some cases, some of these populations may represent different cryptic taxa.
Of the 33 species recorded from the Brazilian coast, at least 26 are members of complexes (see observations in Table 1).Cryptic speciation occurs through a wide genetic differentiation, which is not expressed in the same proportion morphologically (see Mathews et al., 2002).This process has generated extensive cryptic biodiversity in the Alpheidae, especially in the genera Alpheus and Synalpheus Spence Bate, 1888 (Mathews and Anker, 2009).The existence of cryptic species complicates the identification of the taxa and may lead to misidentifications.
Currently, the largest species complex in terms of number of intertidal/shallowsubtidal species in Brazil is the A armillatus complex (Anker, 2012).Alpheus armillatus was considered one of the most common species in rocky intertidal coastal habitats along the Brazilian coast (see discussion in Christoffersen, 1984).Following a revision of the western-Atlantic species within this complex, the distribution of the sensu stricto form is presently understood to extend only from southern Florida to Venezuela (Anker, 2012).Some of the previous records of this shrimp in Brazil have been assigned to A. angulosus (Coelho and Ramos, 1972;Christoffersen, 1998;Coelho et al., 2006, in part) and A. carlae (Holthuis, 1956;Mossolin et al., 2006;Pavanelli et al., 2008) (see Anker, 2012).The material reported by Almeida et al. (2006Almeida et al. ( , 2007aAlmeida et al. ( , 2012) ) from the coast of Bahia was re-examined by us and corresponds to A. carlae and A. angulosus.However, most records of A. armillatus in Brazil lack morphological accounts or information about color (e.g., Gomes Corrêa, 1972;Fausto Filho, 1978, 1979;Sampaio and Fausto Filho, 1984;Coelho et al., 1986;Austregésilo-Filho and Ramos-Porto, 1995;Sousa et al., 1998;Young and Serejo, 2005), preventing the determination of the material's identity.These records may represent either of the Brazilian species in this complex, and were ignored here because of the impossibility of determining the true species involved.
Alpheus paracrinitus is another large species complex (A.Anker, pers. com.), represented in Brazil by at least two forms, A. cf.paracrinitus and A. cf.rostratus (see Almeida et al., 2012;Santos et al., 2012).Both forms are, at the moment, only distinguishable by the color pattern (see Figs. 6B, E).However, if these two forms actually represent distinct species, as strongly suggested by their different color patterns, this can only be confirmed after a comprehensive review of this widely distributed complex.Inclusion of both forms in this contribution and the publication of photographs of the color pattern of the material examined as provided by Almeida et al. (2012) and Santos et al. (2012) will aid in mapping the geographic distribution of the forms.Except for the species pair A. cf.paracrinitus -A.cf.rostratus, all other taxa treated here can be separated based on the morphological characters presented in the key.
We believe that the actual diversity of Alpheus from the Brazilian coast, as well as of the entire family Alpheidae, is still far from being understood, and the number of species known today is certainly underestimated.Thus, the Brazilian alpheid fauna is still awaiting a major taxonomic revision.With increasing research and collection efforts directed at this group, especially in regions and microhabitats that have been little explored (e.g., crevices in dead and living corals and coralline algae, in association with other marine invertebrates, deep sea, etc.) and the revision of species complexes that have not been studied, the number of species present on the Brazilian coast is expected to increase.

Figure 7 .Figure 9 .
Figure 7. Morphology of snapping shrimps of the genus Alpheus Fabricius, 1798 from Brazil: types of configuration of anterior region of carapace in dorsal (A-D, F) and lateral (E) views.(A) Anterior region emarginated between the orbits (arrow), with no rostral projection; (B) anterior region with rostrum short (arrow); (C) anterior region with rostrum flat and ocular hoods toothed, teeth arising from anterior slope (arrows); (D) anterior region with rostrum flat and ocular hoods toothed, teeth arising from mesial slope (arrows); (E) anterior region with rostrum carinate in dorsal midline, ocular hoods unarmed (arrow); (F) anterior region with rostrum carinate in dorsal midline, with V-shaped post-rostral plate (contour indicated by arrows), typical of A. armillatus complex.Scale bars = 1 mm.