Freshwater shrimps ( Crustacea , Decapoda , Caridea , Dendrobranchiata ) from Roraima , Brazil : species composition , distribution , and new records

This work provides an update on the species composition and distribution of freshwater shrimps from the state of Roraima, Brazil, based on material deposited in the Brazilian collections of the Instituto Nacional de Pesquisas da Amazônia (Manaus) and the Museu Integrado de Roraima (Boa Vista). A total of 12 species (1 Sergestidae, 3 Euryrhynchidae, and 8 Palaemonidae) are listed, of which 7 (Acetes paraguayensis Hansen, 1919; Euryrhynchus amazoniensis Tiefenbacher, 1978; E. burchelli Calman, 1907; E. wrzesniowskii Miers, 1877; Palaemon yuna Carvalho, Magalhães & Mantelatto, 2014; Pseudopalaemon chryseus Kensley & Walker, 1982; and Ps. gouldingi Kensley & Walker, 1982) are recorded for the first time from the state of Roraima. Maps of geographic distribution for all species known from the state are offered.


Introduction
Despite the number of studies addressing the taxonomy and geographic distribution of the Amazonian freshwater shrimps (Holthuis 1951, 1952, 1966, Omori 1975, Tiefenbacher 1978, Kensley and Walker 1982, D'Incao and Martins 2000, Magalhães 2002, Melo 2003, García-Dávila and Magalhães 2004, Pileggi et al. 2013, Pimentel and Magalhães 2014), the diversity of these decapods in the state of Roraima is still poorly known in the carcinological literature.Ramos-Porto and Coelho (1998) made the first mention of a species of shrimp in Roraima by simply listing the state in the geographical distribution of Macrobrachium nattereri (Heller, 1862) in a faunistic catalogue.However, this record cannot be confirmed as the authors did not document it; that is, the specific locality and other collecting data as well as the repositories of the voucher material were not informed.Melo (2003) did not relate voucher material when listing the state as part of the geographic distribution of M. ferreirai Kensley & Walker, 1982, and M. nattereri.The first documented record was published only recently by Pileggi et al. (2013) for Macrobrachium amazonicum (Heller, 1982), from the lower Branco River basin.Shortly thereafter, Castro and Silva (2013) recorded M. brasiliense (Heller, 1862), M. inpa Kensley and Walker, 1862 (= M. brasiliense), and M. nattereri, in addition to 3 morphospecies of Macrobrachium, from the "igarapé" Perdido, in the municipality of Mucajaí.Later, Cavalcante and Castro (2014) found M. jelskii Miers, 1877 in fish culture reservoirs in the municipality of Alto Alegre.
In Roraima, the rapid deterioration of aquatic environments due to deforestation and siltation of water bodies has increased, especially in areas of forests and savannahs located outside the boundaries of protected areas (Fearnside 1997, Barbosa et al. 2007), contributing to a possible loss of decapod diversity due to habitat degradation.The purpose of this study is to update the information on the taxonomic composition and geographical distribution of freshwater shrimps from Roraima, as well as to report new records from the state and to provide baseline information for future studies or eventual conservation actions.

Methods
Study site.The state of Roraima (225,116 km²), in northern Brazil between the geographic coordinates 05°16ʹ N and 01°25ʹ S, and 058°55ʹ W and 064°48ʹ W (Ferreira et al. 2007), is part of the Amazon-Orinoco interfluvium (Franco et al. 1975) and is characterized by 2 main vegetation types, savannah (open areas) and forest areas (Barbosa 1997).
The main drainage system in Roraima is the Branco River, a tributary of the left bank of the Negro River, with a watershed of 187,540 km 2 (of which 12,310 km² are situated in Guyana), comprising 83% of the state territory (Carvalho 2015).The confluence of the Uraricoera and Tacutu rivers gives rise to the Branco River, and most of their respective tributaries originate in the Parima-Pacaraima mountainous complex along the Venezuelan-Brazilian border.The 566-km-long Branco River flows through the state in a northeast-southwest direction.Its main tributaries are: the Cauamé, Mucajaí, Água Boa, and Catrimani rivers on the right bank; and the Quitauau and Anauá rivers, as well as their tributary, the Baruana River, on the left bank.The Xeruini, Jauaperi, and Jatapu rivers cover the remainder of the south and southeastern portion of Roraima's territory (Santos et al. 1985, Ferreira et al. 2007, Carvalho 2015).
Data collection.The list of species was based both on unpublished data from material previously deposited in the Brazilian carcinological collections of the Instituto Nacional de Pesquisas da Amazônia, Manaus (INPA), and the Museu Integrado de Roraima, Boa Vista (MIRR), as well as material collected during field trips carried out between April 2014 and April 2015 in several municipalities in the state of Roraima: Alto Alegre, Amajarí, Boa Vista, Bonfim, Cantá, Caracaraí, Caroebe, Iracema, Mucajaí, Normandia, Pacaraima, Rorainópolis, São João da Baliza, and São Luís do Anauá.Fresh material was preserved in 70% ethanol.All sampling was made according to the permit issued by ICMBio (SISBIO # 47494-1).
Taxonomic and distributional analysis.Generic and specific identifications were made according to the morphological descriptions and keys in Holthuis (1951Holthuis ( , 1952)), Omori (1975), Tiefenbacher (1978), Kensley andWalker (1982), D'Incao andMartins (2000), Melo (2003), and García-Dávila and Magalhães (2004), and by comparison with identified material of the INPA collection.The "identification characters" listed under each species apply for adult specimens; these characters must be considered with great care regarding juveniles or subadults specimens.Suprageneric classification follows Ahyong et al. (2011), and the taxa are organized alphabetically.The distributional maps are based on geographical coordinates obtained from a GPS receiver during the sampling and from the labels of the collection lots.The geographic coordinates informed between brackets represent the municipality for lots lacking specific site location.The maps were obtained using the QGIS software, v. 2.14.16 (Quantum GIS Development Team 2017) according to the instructions presented in the second part of the tutorial by Calegari et al. (2016).For generating the maps, coordinates were all converted to decimal degrees using WGS84 datum (the same used in the GPS receiver employed during the sampling) according to the calculator provided by INPE (2017).

Material
Remarks.The morphology of our specimens agrees quite well with the description provided by Omori (1975), although the number of segments in the lower antenullar flagellum of the females are smaller than that found by Omori (1975) (13-17 segments).However, this difference might represent intraspecific variation and needs to be further investigated.Suborder Pleocyemata Burkenroad, 1963Infraorder Caridea Dana, 1852Family Euryrhynchidae Holthuis, 1950 Genus Euryrhynchus Miers, 1877 1F-J, 7)

Euryrhynchus amazoniensis Tiefenbacher, 1978 (Figs
Identification characters (Fig. 1F-J).Rostrum triangular, depressed, unarmed, usually not reaching distal margin of cornea.Carapace smooth, antennal tooth present; abdomen smooth, pleura of second somite enlarged and overlapping pleuron of first and third somites.Telson with posterior margin convex, its posterolateral angles with 2 pair of spines, inner pair distinctly larger than outer one.P2 (second pair of chelipds) similar in shape, not in size; merus spineless, carpus with small, sharp spine on inner distal margin.Male Plp2 with endopod shorter than exopod, with short row of setae on inner margin starting near to appendix interna, apex flattened, provided with a few setae subdistally on outer margin.7. Remarks.The morphology of our specimens agrees quite well with the description provided by Kensley and Walker (1982), García-Dávila and Magalhães (2003) and Melo (2003).No significative intraspecific variability was noticed.2A-E, 6) Identification characters (Fig. 2A-E).Rostrum triangular, depressed, unarmed, usually not reaching distal margin of cornea.Carapace smooth, antennal tooth present; abdomen smooth, pleura of second somite enlarged and overlapping pleuron of first and third somites.Telson with posterior margin convex, its posterolateral angles with 2 pair of spines, inner pair distinctly larger than outer one.P2 (second pair of chelipds) similar in shape, not in size; merus with 2 spines on inner margin, carpus with 1 subterminal, sharp spine on inner distal margin.Male Plp2 with endopod longer than exopod; endopod bearing 2 rows of setae on inner margin distally to reduced appendix interna.Remarks.The morphology of our specimens agrees quite well with the description provided by Holthuis (1951) and Melo (2003).No significative intraspecific variability was noticed.

Material
Euryrhynchus wrzesniowskii Miers, 1877 (Fig. 2F-J, 7) Identification characters (Fig. 2F-J).Rostrum triangular, depressed, unarmed, usually not reaching distal margin of cornea.Carapace smooth, antennal tooth present; abdomen smooth, pleura of second somite enlarged and overlapping pleuron of first and third somites.Telson with posterior margin convex, its posterolateral angles with 2 pair of spines, inner pair distinctly larger than outer one.P2 (second pair of chelipeds) similar in shape, not in size; both merus and carpus without subterminal spines on inner distal margin.Male Plp2 with endopod longer than exopod; endopod bearing 2 rows of setae on inner margin distally to reduced appendix interna.Remarks.The morphology of our specimens agrees quite well with the description provided by Holthuis (1951) and Melo (2003).No significative intraspecific variability was noticed.
Remarks.The morphology of our specimens agrees quite well with the description provided by Holthuis (1952Holthuis ( , 1966)), García-Dávila and Magalhães (2003), and Melo (2003).In juveniles the inner pair of posterolateral spines can exceed the tip of telson, which still shows a rather distinct posterior margin.Pileggi et al. (2013) listed this species from the municipality of Caracaraí, in the lower rio Branco region.The records presented here extend its distribution northwards as far as the rio Tacutu basin, in the northeastern part of the rio Branco basin (Fig. 8).The species also occurs in the rio Jatapu, a tributary of the rio Uatumã basin.3D-G, 9) Previous records.Castro and Silva (2013: as M. inpa in p. 41, and M. brasiliense in p. 42).
Macrobrachium brasiliense was first recorded in Roraima by Castro and Silva (2013) from the municipality of Mucajaí, and some of their specimens were misidentified as M. inpa.The records presented here show that the species is widely distributed in the state of Roraima (Fig. 9).3H-K, 8) Previous records.Melo (2003, in list and map).

Macrobrachium ferreirai Kensley & Walker, 1982 (Figs
Identification characters (Fig. 3H-K).Rostrum straight, short, slightly directed downwards, reaching (or failing short of reaching) distal margin of scaphocerite; rostral formula: 9-10(2-3 post-orbital teeth)/1-2.Carapace with antennal and hepatic teeth present, anterolateral portion smooth; abdomen smooth, pleura of second somite enlarged and overlapping pleuron of first and third somites.Telson with posterior margin distinct, ending in a small acute point, usually overreached by inner pair of posterolateral spines.P2 (larger cheliped) similar in shape, slightly unequal in size, larger than entire body in full grown adults; palm subcylindrical in cross-section, fingers a little less than half the length of palm, cutting edges without tubercles.Distribution.Colombia, Brazil (Amazonas, Mato Grosso, Rondônia, Roraima) (see Pileggi et al. 2013 for references; present study).The distribution in Roraima is depicted in Figure 8.

Material
Remarks.The morphology of our few specimens agrees very well with the description provided by Kensley and Walker (1992).Macrobrachium ferreirai closely resembles M. brasiliense and their juveniles and subadult specimens are almost impossible to distinguish.Adult specimens can be identified by the morphology of the second pair of chelipeds, especially the spinulation (fewer and longer spinules in M. brasiliense; denser and smaller in M. ferreirai) and the presence (in M. brasiliense) or absence (in M. ferreirai) of tubercles in the cutting edges of the fingers.
Ramos-Porto and Coelho (1998) and Melo (2003) listed M. ferreirai as occurring in the state of Roraima, but did not specify the localities or document the record with voucher specimens.Pileggi et al. (2013) discussed that the occurrence of the species in the state was probable since M. ferreirai is present in the Negro River basin and the Branco River is its main tributary.The records presented here confirm its occurrence in Roraima (Fig. 8).3L-N, 8) Previous records.Cavalcante and Castro (2014).
Remarks.The morphology of our specimens agrees very well with the description provided by Holthuis (1952), García-Dávila and Magalhães (2003), andMelo (2003).Adult specimens of M. jelskii and M. amazonicum can be easily distinguished by the shape of the rostrum and telson, although juveniles and subadults are somewhat difficult to separate.Vera-Silva et al. (2017) presented a set of characters to differentiate both species.4A-D, 10) Previous records.Ramos-Porto and Coelho (1998, in list); Melo (2003, in list); Castro and Silva (2013).

Macrobrachium nattereri (Heller, 1862) (Figs
Identification characters (Fig. 4A-D).Rostrum straight, short, slightly directed downwards, reaching distal margin of scaphocerite; rostral formula: 8-11(2-3 post-orbital teeth)/1-4.Carapace with antennal and hepatic spines present, anterolateral portion roughened by numerous spinules; abdomen also roughened by spinules, pleurae of second somite enlarged and overlapping pleuron of first and third somites.Telson with posterior margin distinct, ending in a small acute point, usually overreached by inner pair of posterolateral spines.P2 (larger cheliped) similar in shape, unequal in size; larger cheliped overreaching scaphocerite with large part of the length of carpus, palm pear-shaped in cross-section with distinct longitudinal sulcus on outer surface, fingers approximately 0.6 times the length of palm, with row of tubercles on cutting edges.Distribution.Venezuela, Colombia, French Guiana, Brazil (Amazonas, Amapá, Bahia, Ceará, Pará, Roraima), Peru (see Pimentel and Magalhães 2014 for references; present study).The distribution in Roraima is depicted in Figure 10.
Remarks.The morphology of our specimens agrees very well with the description provided by Holthuis (1952).Macrobrachium nattereri closely resembles M. brasiliense and M. ferreirai, and their juveniles and subadult specimens are very difficult to distinguish (Kensley and Walker 1992).
Ramos-Porto and Coelho (1998) and Melo (2003) listed M. nattereri as occurring in the state of Roraima, but without specifying the localities.The records presented here confirm its occurrence in Roraima (Fig. 10).4E, F, 11) Identification characters (Fig. 4E, F).Rostrum slender, slightly curved upwards distally, overreaching distal margin of scaphocerite; rostral formula: 6-10(1 post-orbital tooth)/2-5.First antennular segment with projection of its anterolateral margin reaching the distal margin of second segment; anterolateral spine of first antennular segment not overreaching one third of the projection of the anterolateral margin.Carapace smooth, with antennal and branchiostegal teeth present, branchiostegal suture situated between both teeth; abdomen with pleura of second somite enlarged and overlapping pleuron of first and third somites.Telson with posterior margin distinct, ending in a small acute point, overreached by inner pair of posterolateral spines.P2 similar in shape and size, overreaching scaphocerite with approximately half of the distal part of carpus.Distribution.Brazil (Amazonas, Roraima [new record]) (Carvalho et al. 2014;this study).The distribution in Roraima is depicted in Figure 11.

Genus
Remarks.The morphology of our specimens agrees with the description provided by Carvalho et al. (2014).
Until recently, Palaemon carteri (Gordon, 1935) was considered to be distributed in the Negro River basin (Magalhães and Pereira 2007).However, in a study on the morphological and molecular differentiation of two species of Palaemon from the Amazon basin, Carvalho et al. (2014) concluded that the populations distributed in the Negro River basin were distinct and described a new species, Palaemon yuna, from this basin.The records presented herein indicate that the distribution of this species also encompasses the Branco River basin.
Remarks.In general, the morphology of our specimens agrees well the description provided by Kensley and Walker (1992).However, the curvature of the rostrum over the eyes (Fig. 5D) seems to be a little less pronounced in the specimens from Roraima than those from the Negro River basin (see Kensley and Walker 1982: 18, fig. 20)

Discussion
With a total of 12 species documented herein from the Branco River drainage system, the basin exhibits the highest species richness among the sub-basins of the Amazon River where inventory is available.The number of species in the Branco River basin is higher than the number documented for the Uatumã River basin (8 spp.), Trombetas River basin (7 spp.), Pastaza River basin (6 spp.) (Magalhães 2005, Magalhães andPereira 2007), and the Xingu River basin (11 spp.; C. Magalhães et al., unpubl. data); it is only smaller than that verified for the Negro River basin (16 species) by Magalhães and Pereira (2007).The richness found in the Branco River basin is 75% similar to that verified for the Negro River basin.With the exception of E. wrzesniowskii, all species herein listed from the Branco River basin were also listed from the Negro River basin, considering that the record of Palaemonetes carteri in Magalhães and Pereira (2007) currently refers to P. yuna (see Carvalho et al. 2014).
Acetes paraguayensis was found in the Jauaperi River, a left bank tributary of the lower Branco River (Fig. 1).The occurrence of 3 species of Euryrhynchus in Roraima was somewhat expected due to their distribution  in the Amazon (Figs 6, 7).Both E. amazoniensis and E. burchelli are widely distributed in the Amazon Basin and have already been recorded in the Negro River basin (Magalhães 1988, Melo 2003, Magalhães and Pereira 2007).Euryrhynchus wrzesniowskii also occurs in contiguous hydrographical basins in Guyana (Tiefenbacher 1978) and in the Uatumã River basin, in Brazil (Magalhães 1988).
Macrobrachium is the most diversified genus of Palaemonidae worldwide (De Grave and Fransen 2011) and this is, to a certain extent, reflected in the shrimp fauna of Roraima: with 5 species, the genus is more diverse than Pseudopalaemon (2 spp.) and Palaemon (1 sp.).Macrobrachium nattereri and M. brasiliense are the most widespread species in the state, although M. nattereri seems to be restricted to the Branco River drainage whereas M. brasiliense is also found in the Jatapu River, a tributary of the Uatumã River, in the southeastern portion of the state (Fig. 9).Macrobrachium amazonicum is also present in both Branco River and Jatapu River basins, but its distribution is mainly in the lowland parts, not occurring in the more elevated areas along the mountainous areas in the northern and western part of the state (Fig. 8).According to the present study, M. jelskii and M. ferreirai have more restricted distribution along or close to the Branco River main channel (Fig. 3).This could be reflective of greater sample efforts in this more easily accessible area as well as a habitat preference for the periodically flooded marginal areas along the lowland course of the river.Pseudopalaemon chryseus is widely distributed along the lowland areas of the Branco River drainage (Fig. 12), in contrast to Ps. gouldingi which was found only in a tributary of the Tacutu River, near the border with Guyana (Fig. 11).However, Ps. gouldingi must have a much wider distribution along the Branco River, as the species is also present in the middle and lower reaches of the Negro River (Kensley and Walker 1982).
Four species of the genus Palaemon occur in the Amazon basin (Carvalho et al. 2014).According to these authors, the lineage occurring in the Negro River basin is P. yuna, whose distribution was herein extended into the Branco River basin (Fig. 11).
Although the data presented in this study significantly raised the number of species of shrimps with documented occurrences in the state of Roraima from 3 to 12, this number certainly does not encompass the actual richness of the shrimp fauna in the state.Large areas of Roraima are either conservation units or indigenous reserves (EPE   2010), and are therefore relatively inaccessible for biological surveys without proper permits and adequate, expensive logistics for the fieldwork.These difficulties are reflected in the distributional maps of the species presented herein , where extensive gaps can be noticed, especially in the northern and western portions of the state, encompassing most of the Uraricoera River basin and mainly the right bank tributaries of the Branco River.Figures 6 to 12 show that the occurrences are distributed close to or along the Branco River, in the center and northeastern portions of Roraima, and a few others are distributed in the southeastern portion, thus indicating that collecting efforts are concentrated around the most populated areas, where collecting material is somewhat easier.Taking into account the variety of environments still to be explored in these large areas, it is still premature to have a concrete idea of the richness and distribution of shrimp species in Roraima.Kensley & Walker, 1982 (star) in the state of Roraima, Brazil.Some symbols may represent more than one record.
anonymous reviewer for their valuable comments and suggestions that greatly improved the manuscript.

Figure 7 .
Figure 7. Map showing the distribution of the records of Eyryrhynchus amazoniensis Tiefenbacher, 1978 (circle) and E. wrzensiowski Miers, 1877 (star) in the state of Roraima, Brazil.Some symbols may represent more than one record.

Figure 6 .
Figure 6.Map showing the distribution of the records of Acetes paraguayensis Hansen, 1919 (circle) and Eyryrhynchus burchelliCalman, 1907 (star)  in the state of Roraima, Brazil.Some symbols may represent more than one record.

Figure 9 .
Figure 9. Map showing the distribution of the records of Macrobrachium brasiliense (Heller, 1862) in the state of Roraima, Brazil.Some symbols may represent more than one record.

Figure 10 .
Figure 10.Map showing the distribution of the records of Macrobrachium nattereri (Heller, 1862) in the state of Roraima, Brazil.Some symbols may represent more than one record.

Figure 12 .
Figure 12.Map showing the distribution of the records of Pseudopalaemon chryseus Kensley & Walker, 1982 in the state of Roraima, Brazil.Some symbols may represent more than one record.

Figure 11 .
Figure 11.Map showing the distribution of the records of Palaemon yuna Carvalho, Magalhães & Mantelatto, 2014 (circle) and Pseudopalaemon gouldingiKensley & Walker, 1982 (star)  in the state of Roraima, Brazil.Some symbols may represent more than one record.