Shrimps of genus Lysmata Risso, 1816 (Caridea: Lysmatidae) from Queimada Grande Island region, southeastern Brazil

Abstract

The objective of this study is to report the first occurrences of three species from the genus Lysmata Risso, 1816 in an area of the Queimada Grande Island (QGI), a conservation unit on the southern coast of São Paulo, southeastern Brazil. The specimens were sampled manually in August 2018 from a small rocky formation from the QGI region. The species Lysmata bahia Rhyne and Lin, 2006, Lysmata uncicornis Holthuis and Maruin, 1952, and Lysmata vittata (Stimpson, 1860) are reported, of which the last two are not native to the Western Atlantic waters. The present study reports L. uncicornis for the first time on the coast of São Paulo State. The records informed herein not only provide more information about biodiversity, but can also help in the development of management plans and conservation.

Keywords
Aquarium trade; Decapoda; Geographical distribution; Peppermint shrimp; Western Atlantic

INTRODUCTION

The genus LysmataRisso, 1816, which belongs to the family Lysmatidae Dana, 1852b, is composed of widely distributed species with distinct behavior (social and sexual) and life habits in different marine environments (Bauer, 2000; Rhyne and Lin, 2006; Baeza, 2009; Soledade et al., 2013). Currently, the genus includes 47 species distributed worldwide (Pachelle et al., 2020), with 18 reported in the Atlantic (Chace, 1972; Rhyne and Lin, 2006; Baeza and Anker, 2008; Anker and Cox, 2011; De Grave and Fransen, 2011; Rhyne et al., 2012; Soledade et al., 2013; Gan and Li, 2016; Pachelle et al., 2016; Prakash and Baeza, 2017; Wang and Sha, 2018; De Grave and Anker, 2018; González-Ortegón et al., 2020) and 11 of these on the Brazilian coast in which three of them, Lysmata lipkeiOkuno and Fiedler, 2010, Lysmata uncicornisHolthuis and Maruin, 1952, and Lysmata vittata (Stimpson, 1860), are exotic (Pachelle et al., 2020).

The genus Lysmata has species that are highly valuable in the ornamental aquarium industry (Calado et al., 2003; Baeza and Behringer, 2017; Giraldes et al., 2018; González-Ortegón et al., 2020) because they help control pests (anemones of the genus AiptasiaGosse, 1858) in aquariums, and are visually appealing due to their vivid color patterns (Karplus, 2014; Giraldes et al., 2018). Due to the popularity of Lysmata in the aquarium trade, the demand for them has grown among marketed marine invertebrates (Wabnitz et al., 2003; Calado et al., 2007; Rhyne et al., 2017). Therefore, areas where Lysmata species occur are targeted for the commercialization of these organisms, including the southeastern coast of Brazil.

Queimada Grande Island (QGI) is part of an Area of Relevant Ecological Interest (AREI) encompassing Queimada Grande and Queimada Pequena Islands; a “sustainable use” marine protected area on the southern coast of São Paulo State, Brazil (Pivetta et al., 2012). Additionally, QGI is part of the Marine Environmental Protected Area “Litoral Centro”, and this area has different types of zones, according to the zoning protocol - version 18/12/2018 - measuring the level of permission for human activity (APAMLC, 2018). Queimada Pequena Island is inside a Zone of Special Protection (ZSP), forbidding any human activity in a radius of 1 km from the island coast. QGI is inside a Zone for Low-Scale Uses (ZLSU) within a radius of 3 km from the island coast and a Zone of Intensive Use (ZUI) beyond this 3 km, allowing some fisheries activities. Studies on the fauna of the subtidal region in QGI have already been reported, including on reef fish (Pivetta et al., 2012) and coral reefs (Pereira-Filho et al., 2019). Despite this, the biodiversity of crustaceans has not yet been studied in this area. Thus, the aim of the present study is to register the occurrence of Lysmata bahiaRhyne and Lin, 2006, L. uncicornis, and L. vittata at Queimada Grande Island, using an integrative approach (morphological and molecular analysis). In addition, we expanded the knowledge about the distribution of two invasive species in the Western Atlantic, with a relevant record of these species in a conservation unit area.

MATERIAL AND METHODS

Sampling of Lysmata shrimps

Sampling was accomplished by artisanal collectors who catch ornamental marine organisms. The shrimps were removed from areas near the Queimadas Area of Relevant Ecological Interest (AREI) (Fig. 1) by free divers who collected the shrimps using a hand net from a small rocky formation with biogenic substrate at 6 to 12 m deep (C.H.A. Marques, artisanal fisherman, personal communication). The collection information and the shrimps were voluntarily transferred to one of us (AC-B) to be used in the present study. The sampled specimens were individually stored in plastic bags, kept in insulated boxes with ice and transported to the laboratory. Individuals were identified according to an identification key (Pachelle et al., 2020) and deposited in the carcinological collection of the Museum of Zoology at the University of São Paulo (MZUSP).

Figure 1.
Sampling region in the Area of Relevant Ecological Interest (AREI) Queimada Grande and Queimada Pequena Islands and the Marine Environmental Protected Area “Litoral Centro” in the Zone of Special Protection (Queimada Pequena Island) and Zone for Low-Scale Use (Queimada Grande Island), southeastern Brazil.

Morphology analysis

Each shrimp was measured and sexed. The carapace length (CL, the distance from the posterior orbital margin to the posterior margin of the carapace) was measured with a Vernier caliper (accuracy 0.01 mm). Due to protandric hermaphroditism reported in many species of the genus Lysmata (see Bauer, 2006; Alves et al., 2019), individuals were simply divided into ovigerous (ov.) and non-ovigerous (non-ov.) specimens. For identification shrimps were examined using a Leica MZ12S stereomicroscope equipped with a camera lucida. The following morphological characters were analyzed: [1] armature of the rostrum, [2] presence or absence of sharp tooth on pterygostomial margin, [3] number of free articles on accessory ramus of lateral antennular flagellum, [4] reach of rostrum in relation to distal margin of third article of antennular peduncle, [5] reach of stylocerite in relation to row of spiniform setae on dorsal surface of first article of antennular peduncule, [6] length of carpus of first pereopod in relation to height in lateral view, [7] number of subdivisions on carpus of second pereopod, [8] length of merus of second pereopod in relation to ischium length, [9] number of fused articles on lateral antennular flagellum before bifurcation with accessory ramus, [10] number of subdivisions on merus of second pereopod, and [11] intraorbital process form. These characters were used because of their importance in the previous identification of Lysmata species (Rhyne and Lin, 2006; Giraldes et al., 2018; Pachelle et al., 2020).

Molecular analysis of Lysmata shrimps

Molecular analysis was based on the 16S rRNA mitochondrial DNA segment following the protocols provided by Schubart et al. (2000). The analysis was carried out to genetically compare the specimens received, with 27 species of Lysmata and ExhippolysmataStebbing, 1915 (Tab. 1).

Table 1.
Details of specimens and sequences used in the phylogenetic analyses in this study. The new sequences obtained in this study are highlighted. CCDB = Crustacean Collection of Biology Department of FFCLRP, University of São Paulo; IEO-CDCAD = Decapoda and Stomatopoda Crustacean Collection of Spanish Institute of Oceanography in Cadiz; CNCR = National Crustacean Collection of the Universidad Nacional Autónoma de México; LCP/UFSC = Laboratory of Crustaceans and Plankton Collection of Santa Catarina Federal University; MNRJ = Crustacean Collection of National Museum of Rio de Janeiro; MZUSP = Zoological Collection of Museum of Zoology of the University of São Paulo; RMNH = Naturalis Biodiversity Center (formerly Rijksmuseum van Natuurlijke Historie); SMF = Collection of the Senckenberg Natural History Museum; UMML = Collection of The Marine Laboratory, University of Miami.

Species	Catalogue Number	Sampling locality	GenBank 16S
Lysmata amboinensis De Man, 1888	UMML 32.9451	Philippines	EU861488
Lysmata ankeri Rhyne and Lin, 2006	CCDB 4715	Ubatuba, São Paulo, Brazil	KU312981
Lysmata ankeri Rhyne and Lin, 2006	UMML 32.9452	USA	EU861501
Lysmata argentopunctata Wicksten, 2000	CNCR 20998	Mexico	GQ227814
Lysmata bahia Rhyne and Lin, 2006	UMML 32.9453	Panama	EU861503
Lysmata bahia Rhyne and Lin, 2006	MZUSP 37511	Sergipe, Brazil	MH102006
Lysmata bahia Rhyne and Lin, 2006	MZUSP 37511	Sergipe, Brazil	MH102007
Lysmata bahia Rhyne and Lin, 2006	MZUSP 41122	Peruíbe, São Paulo, Brazil	MT459816
Lysmata bahia Rhyne and Lin, 2006	MZUSP 41122	Peruíbe, São Paulo, Brazil	MT459817
Lysmata boggessi Rhyne and Lin, 2006	UMML 32.9454	USA	EU861505
Lysmata californica (Stimpson, 1866)	UMML 32.9455	USA	EU861498
Lysmata debelius Bruce, 1983	UMML 32.9456	Philippines	EU861492
Lysmata galapagensis Wicksten, 2000	UMML 32.9457	Panama	EU861480
Lysmata grabhami (Gordon, 1935)	UMML 32.9459	Haiti	EU861489
Lysmata gracilirostris Wicksten, 2000	UMML 32.9458	Panama	EU861502
Lysmata hochi Baeza and Anker, 2008	UMML 32.9460	USA	EU861507
Lysmata holthuisi Anker, Baeza and De Grave, 2009	UMML 32.9466	Panama	EU861483
Lysmata intermedia (Kingsley, 1878)	UMML 32.9461	Panama	EU861484
Lysmata intermedia (Kingsley, 1878)	Not vouchered	USA	HQ315580
Lysmata intermedia (Kingsley, 1878)	MZUSP 37512	Sergipe, Brazil	MH102008
Lysmata lipkei Okuno and Fiedler, 2010	Not vouchered	Okinawa, Japan	HQ315574
Lysmata lipkei Okuno and Fiedler, 2010	MZUSP 37513	Sergipe, Brazil	MH102009
Lysmata lipkei Okuno and Fiedler, 2010	MZUSP 37513	Sergipe, Brazil	MH102010
Lysmata moorei (Rathbun, 1901)	UMML 32.9462	Panama	EU861481
Lysmata nayaritensis Wicksten, 2000	UMML 32.9463	Panama	EU861506
Lysmata nilita Dohrn and Holthuis, 1950	SMF 32005	Italy	EU861482
Lysmata olavoi Fransen, 1991	SMF 32006	Portugal	EU861494
Lysmata pederseni Rhyne and Lin, 2006	UMML 32.9464	Belize	EU861504
Lysmata rafa Rhyne and Anker, 2007	UMML 32.9465	Haiti	EU861495
Lysmata seticaudata (Risso, 1816)	UMML 32.9614	Portugal	GQ227827
Lysmata udoi Baeza et al., 2009	UMML 32.9603	Venezuela	GQ227815
Lysmata uncicornis Holthuis and Maurin, 1952	MNRJ 27976	Florianópolis, Santa Catarina, Brazil	MH142085
Lysmata uncicornis Holthuis and Maurin, 1952	LCP/UFSC-106	Florianópolis, Santa Catarina, Brazil	MH142086
Lysmata uncicornis Holthuis and Maurin, 1952	RMNH D.7812	Casablanca, Morocco	MT002801
Lysmata uncicornis Holthuis and Maurin, 1952	IEO-CDCAD18/2464	Cadiz, Spain	MN294751
Lysmata uncicornis Holthuis and Maurin, 1952	MZUSP 41123	Peruíbe, São Paulo, Brazil	MT459814
Lysmata uncicornis Holthuis and Maurin, 1952	MZUSP 41123	Peruíbe, São Paulo, Brazil	MT459815
Lysmata vittata (Stimpson, 1860)	RMNH D 35616	Thailand	GQ227828
Lysmata vittata (Stimpson, 1860)	RMNH D 35616	Thailand	GQ227829
Lysmata vittata (Stimpson, 1860)	Not vouchered	Bahia, Brazil	JX912539
Lysmata vittata (Stimpson, 1860)	Not vouchered	Bahia, Brazil	JX912540
Lysmata vittata (Stimpson, 1860)	MZUSP 37509	Sergipe, Brazil	MH102011
Lysmata vittata (Stimpson, 1860)	MZUSP 37509	Sergipe, Brazil	MH102012
Lysmata vittata (Stimpson, 1860)	MZUSP 41124	Peruíbe, São Paulo, Brazil	MT459818
Lysmata wurdemanni (Gibbes, 1850)	CCDB 5510	Ubatuba, São Paulo, Brazil	KU312984
Lysmata wurdemanni (Gibbes, 1850)	UMML 32.9468	USA	EU861500
Exhippolysmata ensirostris (Kemp, 1914)	UMML 32.9602	China	GQ227819
Exhippolysmata oplophoroides (Holthuis, 1948)	UMML 32.9469	Ubatuba, São Paulo, Brazil	EU861510

Total genomic DNA was extracted from abdominal muscle tissue using the Wizard® Genomic DNA Purification Kit (Promega, Madison, WI, USA) following the manufacturer’s protocol. For amplification of the 16S gene segment, we used primers 16 L2 (5′-TGCCTGTTTATCAAAAACAT-3′) and 1472 (5′-AGATAGAAACCAACCTGG-3′) (Schubart et al., 2000; 2002). PCR reactions were performed in a Veriti® Thermal Cycler (Applied Biosystems, Foster City, CA, USA) and included 12.5 mL of PCR Buffer Go Taq Green (Promega, Madison, WI, USA), 1.0 mL of each primer, 8.5 mL of Milli-Q water (Milipore, Billerica, MA, USA) and 2 mL of each sample at a final volume of 25 mL. PCR cycles proceeded as follows: initial denaturation at 95 °C for 5 min; 40 cycles of 95 °C for 45 sec, 52 °C for 45 sec, and 72 °C for 1 min; and final extension at 72 °C for 5 min. Negative controls (sterile water) were used in all reactions. The results were checked on a 1.5 % agarose gel stained with GelRed. The PCR products were purified using the Wizard® SV Gel and PCR Clean-Up System (Promega) and sequenced on an ABI 3500 Genetic Analyzer (Applied Biosystems) in the Bioinformatics and Evolutionary Biology Laboratory in the Genetics Department at the Federal University of Pernambuco, Brazil.

Forward and reverse sequences were aligned to obtain the consensus sequence in BioEdit v.7.0.5 (Hall, 1999). Consensus sequences alignment was performed using ClustalW (Thompson et al., 1994) enforcement in BioEdit v.7.0.5 (Hall, 1999). The selection of an optimal model of base substitution, based on AICc and conducted in MEGA 7 (see Kumar et al., 2016), identified an HKY + G + I evolutionary model (-lnL = -3914.411). Phylogenetic analysis was estimated via the Maximum Likelihood (ML) method in MEGA 7. The robustness of the ML tree topologies was assessed by bootstrap resampling of the observed data 1000 times. To verify intra- and interspecific genetic divergence among the studied sequences, a matrix of genetic divergence was calculated in MEGA 7 based on the p distance (Kumar et al., 2016).

RESULTS

In the present study, five individuals of Lysmata were collected from areas around Queimada Grande Island, with two L. bahia, two L. uncicornis, and one L. vittata.

Systematics

Order Decapoda Latreille, 1802

Infraorder Caridea Dana, 1852a

Family Lysmatidae Dana, 1852b

Lysmata Risso, 1816

Lysmata bahia Rhyne and Lin, 2006

Lysmata bahiaRhyne and Lin, 2006: 191, figs. 16-18, pls. 1F, 2; Barros-Alves et al., 2015: 3, figs. 1C, 3; Pachelle et al., 2016: 16, tab. 1; Pachelle et al., 2020: 60, figs. 3-4.

Hyppolysmata (Hippolysmata) wurdemanni: Fausto Filho, 1970: 56; Coelho and Ramos, 1972: 153 (partim?) [not L. wurdemanni (Gibbes, 1850), see Rhyne and Lin, 2006]

Lysmata wurdemanni: Chace, 1972: 129 (remarks on São Paulo material); Coelho et al., 2006: 121, tab. 3 (partim?) [not L. wurdemanni (Gibbes, 1850)]

Material examined. 1 ov. specimen (10.86 mm CL), 1 non-ov. specimen (10.26 mm CL), MZUSP 41122, Queimada Grande Island, Peruíbe, São Paulo State, Brazil, collector Marques, C.H.A. (artisanal fisherman), 01.viii.2018.

First record for São Paulo. Santos harbor (Rhyne and Lin, 2006).

Distribution. Western Atlantic: Panama and Brazil (Ceará, Sergipe, Bahia, Rio de Janeiro, São Paulo) (Rhyne and Lin, 2006; Barros-Alves et al., 2015; Pachelle et al., 2016; Terossi et al., 2018; Pachelle et al., 2020; present study).

Remarks. Lysmata bahia was first reported from Brazil by Fausto Filho (1970) as Hippolysmata wurdemanniGibbes, 1850, followed by the first occurrence in São Paulo as Lysmata wurdemanni (Gibbes, 1850) by Chace (1972), which were later considered paratypes of L. bahia by Rhyne and Lin (2006). It is also one of the three species that belongs to the L. wurdermanni complex in Brazil, along with Lysmata ankeriRhyne and Lin, 2006 and L. wurdermanni (see Pachelle et al., 2020). The analyzed specimens presented all the diagnostic characteristics of L. bahia, according to Pachelle et al. (2020). The two specimens presented long stylocerites, almost reaching the distal margin of the first article of the antennular peduncle, which is a characteristic that differentiates L. bahia from L. ankeri and L. wurdemanni (which have a comparatively shorter stylocerite) (Pachelle et al., 2020). However, the two specimens presented the carpus of the first pereiopod about 4 times longer than tall, instead of 4.5 times, as indicated by Pachelle et al. (2020).

Lysmata uncicornis Holthuis and Maurin, 1952

Lysmata uncicornisHolthuis and Maurin, 1952: 198, figs. 1-2; Lagardère, 1971: 99, figs. 232-235; González-Ortégon et al., 2020: 26, figs. 1-4.

Lysmata arvoredensisGiraldes, Macedo, Brandão, Baeza and Freire, 2018: 5, figs 1-4F.

Material examined. 2 ov. specimens (10.09, 10.12 mm CL), MZUSP 41123 (Fig. 1), Queimada Grande Island, Peruíbe, São Paulo State, Brazil, collector Marques, C.H.A. (artisanal fisherman), 01.viii.2018.

First record for São Paulo. Present study.

Distribution. Eastern Atlantic: from Morocco to Congo; Gulf of Cadiz (between Spain and Portugal). Western Atlantic: Brazil (Santa Catarina [as L. arvoredensis] and São Paulo) (Holthuis and Maurin, 1952; Lagardère, 1971; Giraldes et al., 2018; González-Ortegón et al., 2020; present study).

Remarks. Lysmata uncicornis was recently classified as a senior synonym of L. arvoredensis (see González-Ortégon et al., 2020). The record of L. uncicornis in São Paulo mentioned by Pachelle et al. (2020) was made via photographic register from a mussel farm in 2012, but was not tracked and remained an uncertain record. Therefore, the present study offers the first documented record of the occurrence of this species on the coast of São Paulo State, based on morphological and molecular analysis, and is the northern limit for the species in Western Atlantic waters. The occurrence of L. uncicornis in Brazilian waters may be associated with the introduction of non-native species by anthropogenic influence related to the marine aquarium trade (González-Ortégon et al., 2020). Both specimens presented all diagnostic characteristics and expected morphological variation for L. uncicornis, according to Pachelle et al. (2020) (Fig. 2). The species differs from L. bahia by the proportion of the length and height of the carpus of the first pereiopod (longer in L. bahia); by the number of subdivisions in the carpus of the second pereiopod (22-24 versus 29-32 in L. bahia); and the length of the free portion of the accessory ramus of the antennular flagellum (shorter in L. uncicornis).

Figure 2.
Lysmata uncicornisHolthuis and Maurin, 1952. A, Specimen collected in the area near to the border of the protected area of Queimada Grande Island, lateral view; B, lateral view, rostrum details and absence of pterogostomial spine; C, dorsal view, reach of rostrum in relation to distal margin of third article of antennular peduncle; D, dorsal antennular flagellum with trace of accessory branch; E, dactyl of pereopod 3, lateral view; F, second pereopod, lateral view, number of subdivisions on carpus; G, first pereopod, lateral view, length of carpus in relation to height. Scale bars, A = 1cm; B-F = 1mm. Photographs by R. C. Santos.

Lysmata vittata ( Stimpson, 1860 )

Hippolysmata vittataStimpson, 1860: 26.

Nauticaris unirecedensSpence Bate, 1888: 608, pl. 110, fig. 1

Hippolysmata vittata var. subtilisThallwitz, 1891: 22.

Lysmata vittata: Bruce, 1990: 601, figs. 23-28; Soledade et al., 2013: 67; Alves et al., 2018: figs. 1B, 3; Terossi et al., 2018: 83.

Hippolysmata durbanensisStebbing, 1921: 20, pl. 5.

Lysmata rauliLaubenheimer and Rhyne, 2010: 299, figs. 1-3; Soledade et al. 2013: 67, fig. 2C.

Material examined. 1 non-ov. specimen (7.02 mm CL), MZUSP 41124, Queimada Grande Island, Peruíbe, São Paulo State, Brazil, collector Marques, C.H.A. (artisanal fisherman), 01.viii.2018.

First record for São Paulo. São Vicent Estuary (Soledade et al., 2013).

Distribution. Indo-West Pacific: from Mozambique to Hong Kong; Philippines, Japan, Russia, Australia, and New Zealand. Mediterraean Sea. Western Atlantic: Brazil (Sergipe, Bahia, Rio de Janeiro, São Paulo) (Barnard, 1955; Chace, 1997; Ahyong, 2010; Laubenheimer and Rhyne, 2010; Marin et al., 2012; Soledade et al., 2013; Abdelsalam, 2018; Alves et al., 2018; Pachelle et al., 2018; Terossi et al., 2018; Present study).

Remarks. It is the first non-native species of Lysmata reported on the Brazilian coast (Soledade et al., 2013), followed by L. lipkei (see Pachelle et al., 2016). Recently recognized as a senior synonym of L. rauli (see Laubenheimer and Rhyne, 2010) and due to its wide distribution and diverse color patterns may be considered a species complex (Marin et al. 2012; Soledade et al., 2013; Anker and De Grave 2016; Pachelle et al., 2018; 2020). The analyzed specimen was very damaged, with several broken appendages. However, despite the damage the identification by morphological characteristics was possible, since the rostrum and some appendages were still intact. Thus, it was possible to verify: [1] the presence of a sharp tooth on the pterygostomial margin; [2] seven dorsal and three ventral teeth on the rostrum; [3] a single short free article in the accessory ramus of the antennular flagellum; [4] stylocerite longer, overreaching distal margin of cornea; [5] intraorbital process of carapace longer than wide in lateral view; and [6] first pereopod carpus short, about three times as long as wide in lateral view. These characteristics can be used as morphological evidence, allowing the analyzed specimen to be identified according to the key proposed by Pachelle et al. (2020). The proposition of L. vittata as a senior synonym of L. rauli may be carefully checked using more extensive material and through morphological and molecular analysis because of the possibility of L. vittata being a species complex (Marin et al., 2012; Soledade et al., 2013; Terossi et al., 2018; Pachelle et al., 2018; 2020).

Molecular analysis

The two sequences obtained for L. bahia from QGI (Brazil) matched with the sequence from a L. bahia specimen from Sergipe State (Brazil) and Panama (Fig. 3). The genetic divergence among these three L. bahia specimens varied from 0 to 0.004 (p distance). The two sequences obtained for L. uncicornis specimens from QGI (Brazil) matched with the sequences of L. uncicornis from Florianópolis, Santa Catarina State, Brazil (Fig. 3). There were no differences among the four sequences of this species (p distance = 0). The sequence of L. vittata from Ilha da Queimada Grande matched with the sequences of L. vittata from Thailand and Sergipe and Bahia States (Brazil) (Fig. 3). The genetic divergence among the five L. vittata specimens varied from 0 to 0.007 (p distance).

Figure 3.
Phylogenetic tree of genus Lysmata (Risso, 1816), including Lysmata bahiaRhyne and Lin, 2006, Lysmata uncicornisHolthuis and Maurin, 1952, and Lysmata vittata (Stimpson, 1860) from Queimada Grande Island, Brazil (indicated in red), constructed via Maximum Likelihood analysis of the 16S DNA gene. Numbers are support values for 1000 bootstraps; values < 50 % were not included.

DISCUSSION

Through morphological and molecular analyses, the present study confirms the first record of three species from the genus Lysmata in areas surrounding the Queimada Grande Island, southern coast of São Paulo State, of which two species are non-native to the Western Atlantic. Integrative techniques, such as DNA (16S) and morphological characters, contributed and complemented the identification process of Lysmata, which had already proven to be arduous due to ambiguous morphological characteristics, and consequently, by the presence of species complexes (Rhyne and Lin, 2006; Baeza, 2010; Soledade et al., 2013; Baeza and Behringer, 2017; Wang and Sha, 2018; González-Ortegón et al., 2020; Pachelle et al., 2020).

Lysmata bahia is widely distributed on the Brazilian coast since its description by Rhyne and Lin (2006). The present record is the southern-most limit of this species occurrence in the Western Atlantic, after the occurrence record in Santos Bay, São Paulo State (Rhyne and Lin, 2006; Alves et al., 2018; Terossi et al., 2018). Regarding the non-native species found in the QGI area, L. vittata has already been well established in Brazilian waters (Soledade et al., 2013; Alves et al., 2018; 2019), while there have been few occurrence records for L. uncicornis on the coast of Brazil (Giraldes et al., 2018; Gonzáles-Ortegón et al., 2020; Pachelle et al., 2020).

Our results confirm the presence of L. uncicornis on the coast of São Paulo State. This species was previously recorded in São Paulo by Pachelle et al. (2020), however, this record could not be confirmed because the specimen was lost. Thus, the present study extends the range of L. uncicornis in the Western Atlantic (from 27°25’ S to 24°29’ S of latitude) (Giraldes et al., 2018, González-Ortégon et al., 2020; Pachelle et al., 2020). Lysmata uncicornis is the sixth species of Lysmata to be confirmed on the São Paulo State coast, along with L. ankeri, L. bahia, Lysmata intermedia (Kingsley, 1878), L. vittata, and L. wurdemanni, and is the second non-native species to be recorded there (Soledade et al., 2013; Pachelle et al., 2016; Barros-Alves et al., 2016; Terossi et al., 2018; Pachelle et al., 2020).

The dispersal vector responsible for the presence of exotic Lysmata species on the São Paulo coast is still uncertain, nevertheless, ballast water transportation, as previously registered for other Decapoda crustaceans, as well as the high demand of Lysmata specimens for the marine aquarium trade are the most likely causes (Mantelatto and Dias, 1999; Calado, 2009; Pachelle et al., 2011; Tavares, 2011; Soledade et al., 2013; Barros-Alves et al., 2016). The increased demand for these shrimps may result in deregulated exploitation, as well as inappropriate trade, which can lead to the introduction of exotic species, as is the case for L. lipkei, L. uncicornis, and L. vittata on the Brazilian coast, which are originally from Indo-West Pacific (Alves et al., 2018).

The introduction of non-native species by the ornamental aquarium trade needs to be explored (González-Ortegón et al., 2020; Alves et al., 2021). According to Mainka and Howard (2010), the occurrence of invasive species is currently one of the largest causes of biodiversity loss on the planet along with climate change. The ecological consequences of this introduction can be direct, with the loss of native species, or indirect, through the transmission of pathogens (Rodríguez and Suárez, 2001; Tavares, 2003; Almeida et al., 2012).

The present study is the first to report crustacean species in areas near to Queimada Grande Island AREI, but is limited to the genus Lysmata. We highlight the importance of carrying out new studies that use new sampling techniques in this area in order to more effectively determine the local diversity in different substrates, as well as mechanisms that may evaluate the process of non-native species introduction and how it occurs; such as molecular analysis. This information could facilitate management and conservation measures that decrease the possible impacts that invasive species have on native species in this conservation unit.

ACKNOWLEDGEMENTS

The authors thank MSc. Isabela R.R. Moraes and Dra. Jessica Colavite for help with the figure 2 construction. The authors thank the anonymous reviewers that improved the quality of the manuscript and the free divers who collected and donated the specimens used in the study. This research was financed by “Fundação de Amparo à Pesquisa do Estado de São Paulo-FAPESP/SP” (scholarship Nº 2018/00739-0, granted to RCS).

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Publication Dates

• Publication in this collection
  21 July 2021
• Date of issue
  2021

History

• Received
  25 Nov 2020
• Accepted
  31 Mar 2021