Lysmata arvoredensis nov. sp. a new
species of shrimp from the south coast
of Brazil with a key to species of Lysmata
(Caridea: Lysmatidae) recorded in the
southwestern Atlantic
Bruno W. Giraldes1, Thais P. Macedo2, Manoela C. Brandão2,3,
J. Antonio Baeza4,5,6 and Andrea S. Freire2
1
Environmental Science Centre, Qatar University, Doha, Qatar
Laboratório de Crustáceos e Plâncton, Departamento de Ecologia e Zoologia, Universidade
Federal de Santa Catarina, Florianópolis, Santa Catarina, Brazil
3
Observatoire Océanologique de Villefranche-sur-Mer, Villefranche-sur-Mer, France
4
Department of Biological Sciences, Clemson University, Clemson, SC, USA
5
Smithsonian Marine Station at Fort Pierce, Fort Pierce, FL, USA
6
Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte,
Coquimbo, Chile
2
ABSTRACT
Submitted 22 April 2018
Accepted 9 August 2018
Published 5 September 2018
Corresponding authors
Bruno W. Giraldes,
bweltergiraldes@qu.edu.qa
J. Antonio Baeza,
baeza.antonio@gmail.com
Lysmata arvoredensis sp. nov. inhabits temperate waters in the south coast of Brazil
and is named in tribute to the Marine Protected Area REBIO Arvoredo. This is
the fourth species belonging to the genus Lysmata recorded for the region and the
ninth for Brazil. L. arvoredensis sp. nov. can be distinguished from other species of
Lysmata by the presence of a nearly completely fused accessory branch with a single
free unguiform segment on the outer antennular flagellum; a rostrum with seven
dorsal (2+5) and three ventral teeth; a stylocerite with a pointed tip bearing mesial
setae; a second pereiopod with 22–24 carpal subsegments and 14–16 subsegments in
the merus; a merus of the third pereiopod with five ventrolateral and 12 ventral
spines on the propodus; and its color pattern, with red bands and patches in pleonites
2–3 that resemble a mask in dorsal view. Molecular characters demonstrate that
L. arvoredensis sp. nov. is most closely related to other species of Lysmata belonging
to the Neotropical and Cleaner clades. To support future ecological studies in the
region, identification keys to the species of Lysmata recorded in the southwestern
Atlantic Ocean are provided.
Academic editor
Antonina Dos Santos
Additional Information and
Declarations can be found on
page 17
Subjects Biodiversity, Genetics, Marine Biology, Taxonomy
Keywords Marine biodiversity, Peppermint shrimp, Maare project, REBIO do Arvoredo, Phylogeny
and taxonomy, Santa Catarina, Decapod
DOI 10.7717/peerj.5561
Copyright
2018 Giraldes et al.
Distributed under
Creative Commons CC-BY 4.0
INTRODUCTION
Shrimps belonging to the genus Lysmata Risso, 1816 are commonly traded in the
aquarium industry (Calado et al., 2003; Baeza & Behringer, 2017) because of their beautiful
coloration, ability to remove ectoparasites from reef fishes (Karplus, 2014), and capability
to control pests in aquaria (Rhyne, Lin & Deal, 2004). In the last decade, the genus
How to cite this article Giraldes et al. (2018), Lysmata arvoredensis nov. sp. a new species of shrimp from the south coast of Brazil with a
key to species of Lysmata (Caridea: Lysmatidae) recorded in the southwestern Atlantic. PeerJ 6:e5561; DOI 10.7717/peerj.5561
has received considerable attention: several new species have been described (Rhyne,
Calado & Dos Santos, 2012; Gan & Li, 2016) and complexes of cryptic species have been
partially resolved (Rhyne & Lin, 2006; Baeza & Behringer, 2017). Furthermore, a series
of studies focusing on the phylogeny of the genus coupled with behavioral experiments
have improved our understanding regarding the evolution of hermaphroditism in caridean
shrimps (Baeza, 2009, 2010, 2013; Fiedler et al., 2010; Baeza & Fuentes, 2013; De Grave
et al., 2014). Currently, a total of 45 species are recognized worldwide (De Grave &
Fransen, 2011; Rhyne, Calado & Dos Santos, 2012; Soledade et al., 2013; Gan & Li, 2016;
Prakash & Baeza, 2017; De Grave & Anker, 2018) and eight of them have been recorded in
Brazil: L. ankeri Rhyne & Lin, 2006 and L. bahia Rhyne & Lin, 2006 previously
misidentified as L. wurdemanni (Gibbes, 1850) (Rhyne & Lin, 2006); L. grabhami
(Gordon, 1935) previously misidentified as L. amboinensis (de Man, 1888) (Kassuga,
Diele & Hostim-Silva, 2015); L. moorei (Rathbun, 1901) (Coelho et al., 2006; Coelho Filho,
2006); L. jundalini Rhyne, Calado & Dos Santos, 2012 previously misidentified as L. cf.
intermedia (Kingsley, 1878) (Rhyne, Calado & Dos Santos, 2012; Terossi et al., 2018);
the Indo-Pacific L. vittata (Stimpson, 1860) improperly described as a new species (i.e.,
L. rauli Laubenheimer & Rhyne, 2010) (Laubenheimer & Rhyne, 2010; Soledade et al.,
2013); Lysmata cf. lipkei Okuno & Fiedler, 2010, described from Japan (Okuno & Fiedler,
2010) and likely representing a second nonindigenous species in the region (Pachelle et al.,
2016); and L. wurdemanni (Gibbes, 1850) (Terossi et al., 2018).
In this study, we describe a new species of Lysmata from the south coast of Brazil.
To support future ecological studies in the southwestern Atlantic Ocean, identification
keys to species belonging to the genus Lysmata present in Brazil are provided. One key is
based on morphology and a second key is based on color pattern.
MATERIAL AND METHODS
Specimens were collected in the SW Atlantic Ocean, close to Calhau de São Pedro Islet,
Santa Catarina, Brazil (27 25′37.39″S 48 40′11.15″W). A group of specimens of different sizes
was captured from an Acoustic Doppler Current Profiler (ADCP) which was deployed at
20 m depth for a few months at the collection site, therefore acting as an artificial reef.
Collected specimens were transported alive to the Laboratory of Crustáceos e Plâncton (LCP),
Department of Ecologia e Zoologia, Universidade Federal de Santa Catarina (UFSC) for
detailed observation of their coloration and color pattern (Fig. 1). Specimens were then
preserved in ethanol and studied under a stereomicroscope. The holotype and paratypes were
deposited in the National Museum of Rio de Janeiro (MNRJ) and in the Zoological Collection
of UFSC (LCP/UFSC). Postorbital carapace length (pocl) and carapace length, including
rostrum (cl), were used as measurements of body size and expressed in millimeters.
We were interested in revealing the phylogenetic position of the new species within the
genus Lysmata. Thus, we conducted molecular phylogenetic analyses using a portion
of the 16S mitochondrial DNA fragment. A total of 28 sequences; two sequences from two
specimens of Lysmata arvoredensis sp. nov. and 27 sequences each from other species
belonging to the Neotropical, Cosmopolitan, Cleaner, and Morpho-variable clades of
peppermint shrimps were included in the present phylogenetic analyses. Total genomic
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Figure 1 Colors of L. arvoredensis sp. nov. (A) holotype (CL+R: 16.2) (MNRJ 27976) after some days in
the aquarium; (B) lateral view of paratype 1 fixed just after captured (CL+R 16.60) (LCP/UFSC- 100).
Photograph was taken a few days after collection; (C) specimens attached to artificial reef structure
(ADCP) immediately before collection. Photographic Credits: (A) Bruno W. Giraldes, (B) Andrea S.
Freire and Thais P. Macedo, (C) Alejandro D. Varella. Full-size DOI: 10.7717/peerj.5561/fig-1
DNA extraction, PCR amplification with specific 16S rRNA DNA primers (16Sar
[5′-CGCCTGTTATCAAAAACAT-3′] and 16Sbr [5′-CCGGTCTGAACTCAGATCACGT3′] Palumbi, 1996) product cleanup, and sequencing were conducted as described in
Baeza et al. (2009). In short, all PCR reactions had a final volume of 20 mL, and contained
one mL of the DNA template, one mL of each primer (forward and reverse), and 17 mL
of Promega GoTaq Green Master Mix. PCR conditions were initial 95 C denaturation
for 2 min; then 40 cycles of 95 C denaturation for 30 s, 47 C annealing for 1 min,
and 72 C extension for 1 min, and a final extension at 72 C for 5 min. The size and
quality of PCR products were visualized on 1.5% agarose gels. PCR products were then
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purified using SephadexTM G-50 spin columns. Samples were sequenced using BigDye
3.1 with an automatic sequencer ABI3500 at the Universidade Federal do Paraná
(Laboratório de Dinâmica Evolutiva e Sistemas Complexos). Both strands of each sample
were sequenced, and then proofread and compiled in Geneious 10.1.3 (Biomatters,
Auckland, New Zealand). Alignment of each set of sequences was conducted in
MUSCLE (Edgar, 2004) as implemented in MEGA 7.0 (Kumar et al., 2016). The aligned
sequences did contain various indels. Thus, we identified positions that were highly
divergent and poorly aligned in this 16S gene segment using the software GBlocks v0.91b
(Castresana, 2000) and we omitted them from the analyses. After highly divergent
positions were pruned, the 16S consisted of 513 bp (88% of the original 582 positions).
Next, the aligned gene fragments were analyzed with the software jModelTest 2.1.10
(Guindon & Gascuel, 2003; Darriba et al., 2012) that compares different models of
DNA substitution in a hierarchical hypothesis–testing framework to select a base
substitution model that best fits each dataset. The optimal model identified by jModelTest
(selected with the corrected Akaike Information Criterion, Akaike, 1974) was TPM3uf+G
(-lnL = 4280.3454). The calculated parameters were as follows: assumed nucleotide
frequencies A = 0.3214, C = 0.1332, G = 0.2067, T = 0.3388; substitution rate matrix
with A–C substitution = 0.4427, A–G = 4.7502, A–T = 1.000, C–G = 0.4427, C–T = 4.7502,
G–T = 1.0, and rates for variable sites assumed to follow a gamma distribution (G)
with shape parameter = 0.2350. Next, we used the webserver W-IQ-TREE (Trifinopoulos
et al., 2016, http://iqtree.cibiv.univie.ac.at/) for maximum likelihood (ML) analysis and the
software MrBayes (Huelsenbeck & Ronquist, 2001) for Bayesian inference (BI) analysis.
As the model selected by jModelTest2 was not available on the webserver W-IQ-TREE
(Trifinopoulos et al., 2016, http://iqtree.cibiv.univie.ac.at/), we conducted the ML analysis
with the GTR+G evolutionary model that was included within the 95% confidence interval
calculated by JModelTest2. All the parameters used for the ML analysis in W-IQ-TREE
server were those of the default options. In MrBayes, the analysis was performed for
6,000,000 generations. Every 100th tree was sampled from the MCMC analysis obtaining
a total of 60,000 trees and a consensus tree with the 50% majority rule was calculated
for the last 59,900 sampled trees. The robustness of the ML tree topologies was assessed by
bootstrap reiterations of the observed data 1,000 times. Support for nodes in the BI tree
topology was obtained by posterior probability values.
The electronic version of this article in portable document format will represent a
published work according to the International Commission on Zoological Nomenclature
(ICZN), and hence the new names contained in the electronic version are effectively
published under that Code from the electronic edition alone. This published work and
the nomenclatural acts it contains have been registered in ZooBank, the online
registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can
be resolved and the associated information viewed through any standard web
browser by appending the LSID to the prefix http://zoobank.org/. The LSID for
this publication is: (L. arvoredensis sp. nov. urn:lsid:zoobank.org:act:16D1C1E5-DED245CF-856F-06A7C167370A; and the publication under urn:lsid:zoobank.org:
pub:5ECAB752-E712-42E8-100 8FCA-5C3386D7F7F9). The online version of this
Giraldes et al. (2018), PeerJ, DOI 10.7717/peerj.5561
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work is archived and available from the following digital repositories: PeerJ, PubMed
Central, and CLOCKSS.
RESULTS
Systematics
Family Lysmatidae Dana, 1852
Lysmata arvoredensis sp. nov.
Figures 1–4
Material examined.
Type material. Holotype. adult ovigerous (pocl 11.30, cl 16.20); May 25, 2014; Calhau de
São Pedro Island-Santa Catarina, (27 25′37.39″S 48 40′11.15″W), 20 m depth, hidden in a
moored current profiler (MNRJ 27976). Paratypes. One hermaphrodite (pocl 10.50,
cl 16.60); May 25, 2014; six males (pocl 3.90–6.30, cl 5.60–9.75); two males (pocl 6.00, 4.65,
cl 9.00, 7.00) (muscle extracted for genetic analysis); Calhau de São Pedro Island-Santa
Catarina, (27 25′37.39″S 48 40′11.15″W), 20 m depth, hiding in a moored current profiler
(LCP/UFSC- 101–107).
Description of holotype. Rostrum (Figs. 2A and 2B) short, reaching middle of
second segment of antennular peduncle, convex and slightly curved upwards near
tip; rostral tip simple, dorsal carina with seven teeth (2+5), posterior-most tooth
situated on carapace, with considerable gap between first and second tooth, both
anterior to postorbital margin with the second tooth ending just above the
postorbital margin; stiff setae among dorsal teeth. Ventral margin with three teeth,
proximal ventral tooth not reaching the end of first antennular peduncle, in line with
sixth distal dorsal tooth; rostrum length (tip to base of orbit) about 0.46 times that
of carapace length. Carapace (Figs. 2A and 2B) smooth, with rounded posteroventral
margin; antennal tooth stout, acute, somewhat separated from ventral angle of
orbit; pterygostomial angle rounded, pterygostomial tooth absent. Eyes moderately
large (Fig. 2B).
Antennular peduncle shorter than scaphocerite blade (Fig. 2B); first segment 0.5 times
the length of all antennular peduncle segments, with small setae forming a semicircle
located before the distal edge (Fig. 2H). Stylocerite with pointed tip and mesial setae, nearly
reaching end of first antennular segment (Figs. 2F and 2H). Second segment of antennular
peduncle almost as long as wide; third segment as long as second segment (Fig. 2H).
Distomesial angles of antennular segments with spinules (Figs. 2B and 2H). Outer
antennular flagellum with aesthetascs extending from first segment to accessory branch;
accessory branch nearly completely fused with the outer antennular flagellum bearing
only a single free unguiform segment (Figs. 2E and 4E); about 37 joined/fused segments
prior to the free unguiform segment.
Antenna with basicerite bearing acute distolateral tooth. Scaphocerite (Figs. 2B and 2I)
subrectangular, about 2.7 times as long as wide distally, distolateral tooth stout, acute,
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Figure 2 Morphological illustrations of L. arvoredensis sp. nov. (A) Frontal region, lateral view; (B)
frontal region, dorsal view; (C) total carapace, lateral view; (D) variation of rostrum, lateral view; (E)
details of accessory branch in the outer antennular flagellum, lateral view; (F) stylocerite, dorsal view; (G)
telson and uropods, dorsal view; (H) antennular peduncle and (I) scaphocerite in same scale, dorsal view;
(J) abdominal segments and telson, lateral view; (K) telson, details of posterior margin, dorsal view; (L)
second right pleopod, lateral view. Holotype (MNRJ 27976) (A–C, E, G, J–L); Paratype 4 (LCP/UFSC104) (D); Paratype 1 (LCP/UFSC- 100) (F, H, I). Scale size, (A–C) five mm; (D, G–J, L) three mm; (E, F,
K) one mm. Drawings by Bruno W. Giraldes.
Full-size DOI: 10.7717/peerj.5561/fig-2
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falling short of blade distal margin. Scaphocerite slightly longer than antennular peduncle,
exceeding distal segment by ~0.25 times its length.
Mouthparts (Figs. 3A, 3I and 3K–3P) as is typical for the genus (Chace, 1972, 1997;
Rhyne & Lin, 2006) including unequal but similar mandibles armed with three large incisor
teeth on masticatory edge; right with more teeth than left (Figs. 3O and 3P). All maxillipeds
with a well-developed exopod (Figs. 3A, 3I, 3K and 3L). Third maxilliped (Figs. 3A
and 3I) with dense serrate setae compared to pereiopods, especially on distal segment;
overreaching scaphocerite by 1/2 of distal segment; exopod about 0.5 times the length of
antepenultimate segment (Fig. 3A); tip of terminal segment armed with stout spines (Fig. 3I).
First pereiopod (P1) (Figs. 3B and 3J) short and robust, overreaching the end of the
third maxilliped penultimate segment or reaching the distal margin of scaphocerite.
Chela 0.8 times length of carpus, with subcylindrical palm, 1.4 times as long as dactylus
(Fig. 3J). Dactylus with corneous tip. Carpus with oblique row of distomesial long setae
and ventral surface with sparse setae. Merus 1.5 times as long as carpus and obliquely
articulated with ischium (Fig. 3B).
Second pereiopods (P2) (Fig. 3C) long, slender, multi articulated with merus and carpus
segmented, right and left subequal in length, ending in simple chela. Chela 5.7 times as
long as carpus, with palm 1.4 times as long as dactylus. Carpus 2.0 times as long as merus;
and ischium as long as merus. Merus of right and left P2 with 16 and 14 subsegments,
respectively; carpus of right and left P2 with 24 and 22 subsegments, respectively; and
ischium with three subsegments.
Third to fifth pereiopods similar, decreasing in length from third to fifth. Third
pereiopod (Fig. 3D) overreaching distal margin of scaphocerite by proximal third of
propodus; merus about six times as long as wide, with five stout ventrolateral spines
distally (Fig. 3E), and less than twice as long as carpus; propodus slightly shorter than
merus (Fig. 3D), with line of 12 setae on ventral margins; dactylus biunguiculate, about
0.18 times the length of propodus, flexor margin with three spines increasing in size
distally (Fig. 3G). Fourth pereiopod similar to third. Fifth pereiopod with merus distinctly
shorter than propodus, with three stout ventrolateral spines distally (Fig. 3E); propodus
with line of 10 setae on ventral margin (Fig. 3F).
Abdomen (Figs. 2J and 4A) 4.3 times longer than wider (including telson), second
pleonite two times wider than sixth; first three pleura with rounded margins laterally, fourth
with protruding posterolateral round margin, fifth with sharp posterolateral tooth, sixth
with acute posteroventral tooth plus acute posterior tooth on each side of telson (Fig. 2J);
sixth segment 1.8 times longer than fifth segment and 1.1 times longer than wider (Fig. 2J).
Second and third pleopods with appendix interna (Fig. 2L); endopod in second pleopod
lacking appendix masculina (Fig. 4B). Uropod with short protopodite and posterolateral lobe
pointed; exopod with diaeresis bearing acute tooth laterally, adjacent to distolateral spine
(Fig. 2G); endopod and exopod overreaching the posterior end of telson; exopod slightly
longer than endopod, both with plumose setae in lateral and posterior margins.
Telson (Fig. 2G) 1.5 times as long as sixth abdominal somite; tapering posteriorly,
about 1.7 times as long as wide at base; dorsal surface with two pairs of stout spines,
anterior and posterior pair at ~0.36 and 0.67 of telson length, respectively; longitudinal
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Figure 3 More illustrations of L. arvoredensis sp. nov. Lateral/superior view of (A) third maxiliped, (B)
first pereiopod, (C) second pereiopod, and (D) third pereiopod; (E) spines in the merus of pereiopods 3,
4, and 5, inferior view; (F) propodus of pereiopod 3, inferior view; (G, H) dactyls of pereiopod 3, lateral
view; (I) tip of ultimate segment of the third maxiliped, dorsal view; (J) chela of first pereiopod, inferior
view; (K) second maxilliped; (L) first maxilliped; (M) maxilla; (N) maxilulla; (O) right mandible; (P) left
mandible. Holotype (MNRJ 27976) (A–G, I–J); Paratype 4 (LCP/UFSC- 104) (H, K–P). Scale size, (A–F)
three mm; (G–P) one mm. Drawings by Bruno W. Giraldes. Full-size DOI: 10.7717/peerj.5561/fig-3
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Figure 4 Photography of details of L. arvoredensis sp. nov. (A) Abdomen of the hermaphrodite
holotype (MNRJ 27976) with details of the (B) endopod of second pleopod (left) and third pleopod
(right) lacking appendix masculina; (C, D) second pleopod from small male paratypes 4 and 5 (LCP/
UFSC- 104–105) with appendix masculina; (E) the fused segments of the accessory branch with a free
unguiform segment in the antennular flagellum. Comparison of color pattern between (F) L. arvoredensis
sp. nov. and (G) L. nayaritensis. Color pattern (H) in dorsal and (I) lateral view of L. moorei. Photographic credits: (A, B, F) Bruno W. Giraldes; (C–E) Andrea S. Freire and Thais P. Macedo; (G) J. Antonio
Full-size DOI: 10.7717/peerj.5561/fig-4
Baeza; (H, I) Thais P. Macedo.
middle-dorsal line with tufts of setae (Fig. 2G); posterior margin subacute, with pair
of longer mesial setae each flanked by shorter lateral setae; lateral and posterior margin of
telson with plumose setae (Fig. 2K).
Variation in paratypes. Number of dorsal rostral teeth range from 6 to 7, including
two postorbital ones. One specimen also exhibited two ventral teeth (Fig. 2D). The number
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of carpal subsegments in the second pereiopod ranges from 22 to 24. One small
specimen with two spines on ventral margin of fifth pereiopod. Propodus in pereiopods 3,
4, and 5 bearing 10–12, 9–12, and 9–12 ventral spines, respectively. Dactyl of
pereiopods 3–5 with two spines proximal to biunguiculate tip in two specimens (Fig. 3H).
Smaller specimens with appendix interna and appendix masculina in second pleopods
(Figs. 4C and 4D). Larger specimens without appendix masculina.
Color in life. Color pattern is based on the holotype after remaining a few days in an
aquarium (Fig. 1A). Entire body and appendices with semitransparent background and red
colored details. Antennas, antennules, and pereiopods red. Antennular scale with red
margin. Carapace with irregular oblique bands and patches. No longitudinal red lines in
abdomen. Each abdominal segment with narrow transversal band occupying less than
half of the surface in dorsal view. Second and third abdominal segments with a dorsal
ornament in the shape of a mask formed by chromatophores located immediately anterior
to the transversal band. Sixth abdominal segment with a red hexagon in dorsal view.
Tail fan ornamented with three transversal bands; uropods with red margins; telson with a
red tip (Fig. 1A).
Type locality. Calhau de São Pedro Island (27 25′37.39″S 48 40′11.15″W), Santa Catarina,
southern Brazil.
Etymology. The new species is named after the REBIO Arvoredo, a Marine Protected
Area from which the studied specimens were collected.
Distribution. Presently known only from the type locality.
Habitat. Natural habitat unknown. All specimens were collected from an ADCP, deployed
at 20 m for 2 months, acting as an artificial reef substrate. The above suggests that the
new species inhabit cavities in hard bottoms.
Behavior. That large and small animals were collected together suggests that this species is
gregarious.
Phylogenetic results. The molecular data matrix comprised a total of 513 characters,
of which 175 were parsimony informative, for a total of 28 terminals. The analyses
conducted with different molecular phylogenetic inference methods (ML and BI)
resulted in similar tree topologies (Fig. 5). The new species L. arvoredensis sp. nov.
(two specimens) clustered together into a monophyletic clade with other species of
Lysmata belonging to the Neotropical and Cleaner clades (Baeza & Fuentes, 2013).
Remarks. This new species increases to 46 the total number of species belonging
to the genus Lysmata described worldwide (De Grave & Fransen, 2011; Rhyne,
Calado & Dos Santos, 2012; Soledade et al., 2013; Gan & Li, 2016; Prakash & Baeza, 2017;
De Grave & Anker, 2018) and increases to nine the number of species recorded in Brazil
(Chace, 1972; Coelho et al., 2006; Rhyne & Lin, 2006; Soledade et al., 2013; Kassuga,
Diele & Hostim-Silva, 2015). L. arvoredensis sp. nov. is the fourth species of the genus
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Figure 5 Phylogenetic tree for shrimps from the genus Lysmata. Trees were obtained using (A) Bayesian inference (BI) and (B) maximum
likelihood (ML) phylogenetic analyses of the partial 16S rRNA mitochondrial DNA gene. Numbers above and/or below the branches represent the
bootstrap values obtained from ML and the posterior probability values from the BI analysis (ML/BI). GenBank accession numbers are provided
immediately after the species names. Analysis conducted by J. Antonio Baeza and illustrated by Bruno W. Giraldes.
Full-size DOI: 10.7717/peerj.5561/fig-5
reported for the temperate waters of Santa Catarina in the south of Brazil (Christoffersen,
1998; Bond-Buckup & Buckup, 1999; Boos et al., 2012; Giraldes & Freire, 2015).
In our phylogenetic analyses, L. arvoredensis sp. nov. clustered together and formed
a monophyletic clade with other species belonging to the previously recognized
Neotropical and Cleaner clades (Baeza et al., 2009). Furthermore, the tree topologies
supported a sister relationship between L. arvoredensis sp. nov. and congeneric species
belonging to the Cleaner clade. However, this relationship was not well supported by both
ML and BI analyses. Importantly, L. arvoredensis sp. nov. differs considerably both in
terms of morphology and coloration from species belonging to the Cleaner clade.
All cleaner shrimps exhibit conspicuous color patterns; L. debelius Bruce, 1982 has a
deep scarlet red coloration in the entire body (Bruce, 1982) while L. amboinensis and
L. grabhami are yellow and possess dorsal longitudinal red and white bands (Hayashi,
1975; Chace, 1997; Baeza, 2010; Kassuga, Diele & Hostim-Silva, 2015). The color pattern of
the new species is rather dull in comparison. Furthermore, L. debelius has a relatively
long rostrum that reaches beyond the intermediate segment of the antennular peduncle,
has a dorsal formula of 2+3 teeth, the scaphocerite extends far beyond the antennular
peduncle, and the second pereiopod exhibits two subsegments in the merus and 16 in the
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carpus (Bruce, 1982). In turn, L. arvoredensis sp. nov. has a shorter rostrum (just reaching
the middle of the intermediate segment of the antennular peduncle), has a dorsal formula
of 2+5 teeth, the scaphocerite slightly extends beyond the antennular peduncle, and the
second pereiopod has 11–16 subsegments in the merus and 22–24 subsegments in the
carpus. L. debelius is the only congener recorded with a longitudinal middle-dorsal line of
setae on the telson (Bruce, 1982), similar to L. arvoredensis sp. nov. (Fig. 2G).
L. amboinensis and L. grabhami are very similar, having a relatively long rostrum (~0.8
times the carapace length), a pterygostomial spine, a very long antennular peduncle with a
first segment ~0.5 as long as the carapace and a second segment twice as long as the third.
Also, the stylocerite in L. amboinensis and L. grabhami is very short, not nearly reaching
midlength of the basal segment, and the carpus of the second pereiopod has 19–21
subsegments (Hayashi, 1975; Chace, 1997). In L. arvoredensis sp. nov., the rostrum is
shorter than in L. amboinensis and L. grabhami (~0.48 times the carapace length), the
pterygostomial spine is absent, the first segment of the antennular peduncle is ~1/3 as long
as the carapace, the second segment is short, almost as long as the third segment, the
stylocerite reaches the end of the basal segment, and the carpus of the second pereopods
have 22–24 subsegments.
L. nayaritensis and L. californica also exhibit several morphological similarities with the
new species, including the accessory branch nearly completely fused with the outer
antennular flagellum (Wicksten, 2000). Furthermore, the color pattern of L. nayaritensis is
very similar to that of L. arvoredensis sp. nov. (Fig. 4G). However, L. nayaritensis has a
relatively long rostrum (0.6 times its carapace length, exceeding the second segment of the
antennular peduncle) and a short stylocerite (~0.75 times the length of the first segment of
antennular peduncle). In L. nayaritensis, the dorsal rostrum formula is 1+5–6, the exopod
of the third maxilliped is less than 0.5 times the length of the antepenultimate segment, and
the second pereiopod has 15–18 subsegments in the merus. By contrast to L. nayaritensis,
L. arvoredensis sp. nov. has a rostrum (0.48 times the carapace length) that does not reach
the end of the second segment of the antennular peduncle. The dorsal rostrum formula is 2
+4–5, the stylocerite is relatively long, almost reaching the distal end of the first segment of
the antennular peduncle, the exopod of the third maxilliped is 0.5 times the length of the
antepenultimate segment, and the second pereiopod has 11–16 subsegments in the merus.
With respect to color pattern, L. arvoredensis sp. nov. features relatively thin reddish dorsal
bars (1/3 of each pleuron) in the second and third abdominal segments, forming a mask
(Fig. 4F). In turn, L. nayaritensis exhibits thicker dorsal bands in the abdominal segments.
Dorsally, in pleonites 2–5, L. nayaritensis features two short longitudinal lines of
chromatophores located anterior to the band that forms a shape similar to the letter “U” in
each segment (Fig. 4G).
L. californica presents a pterygostomial tooth, the scaphocerite overreaches
the antennular peduncle by nearly the length of the last segment, the spine in the
scaphocerite strongly overreaches the blade, and the second pereiopod has more than
25 (25–32 or 27–29) subsegments in the carpus (Chace, 1997; Wicksten, 2000). By
contrast to L. californica, L. arvoredensis sp. nov. does not have a pterygostomial tooth,
the scaphocerite slightly overreaches the antennular peduncle, the spine in the
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scaphocerite does not overreaches the blade, and the second pereiopod has less than 25
(22–24) subsegments in the carpus. The color pattern of L. californica is also different
from that of L. arvoredensis. While L. arvoredensis sp. nov. exhibits transversal
abdominal bands, L. californica bears longitudinal abdominal bands/lines (Wicksten,
2012: 294 plate 2).
Lysmata arvoredensis sp. nov. is superficially similar both in terms of color pattern
(red abdominal transversal bands) and morphology (unguiform free segment in the
accessory branch at the antennular flagellum) to species belonging to the unguiform
clade (sensu Fiedler et al., 2010) or morpho-variable clade (sensu Baeza et al., 2009; Baeza,
2010; Baeza & Fuentes, 2013), including L. hochi Baeza & Anker, 2008, L. kuekenthali
(de Man, 1902), and L. anchisteus Chace, 1972. Importantly, our phylogenetic analyses
demonstrated that L. arvoredensis sp. nov. is genetically dissimilar from the species above.
L. hochi, L. kuekenthali, and L. anchisteus can be easily distinguished from L. arvoredensis
sp. nov. using a combination of various morphological traits, but most importantly,
the dorsal rostral formula (Kubo, 1951; Chace, 1972, 1997; Baeza & Anker, 2008; Soledade
et al., 2013). For instance, the dorsal rostrum formula is 2+3 in L. hochi, 1+3–4 in
L. kuekenthali, and 1+4–5 in L. anchisteus. By contrast to the species above, the rostral
formula is 2+4–5 in L. arvoredensis sp. nov.
Lastly, L. arvoredensis sp. nov. is similar to L. uncicornis Holthuis & Maurin, 1952,
a species for which no genetic information exist (Baeza & Anker, 2008; Chace, 1972).
However, L. uncicornis differs from the new species with respect to the stylocerite
that exhibit a series of denticules in the outer margin; the longer first pereiopod that
exceeds the scaphocerite by nearly the length of the dactylus; the ventral margin of the
propodus in pereiopods 3 and 4 with 6–8 setae, the ventral margin of the propodus in
pereiopods 5 with 5 setae, the second pereiopod with a maximum of 14 and 28
subsegments in the merus and carpus, respectively, and the accessory branch of the
antennular flagellum that is not fused (not distinguishable) before the unguiform free
segment (Holthuis & Maurin, 1952). In L. arvoredensis nov. sp., the stylocerite is flat in
the outer margin and exhibits mesial setae in the inner margin; the first pereiopod
does not exceed the scaphocerite; the ventral margin of the propodus in pereiopods
3, 4, and 5 has 10–12, 9–12, and 9–12 setae, respectively; the second pereiopod has a
maximum of 16 and 25 subsegments in the merus and the carpus, respectively, and the
accessory branch of the antennular flagellum is fused (distinguishable) before the
unguiform free segment.
Key to species of Lysmata from the Southwestern Atlantic Ocean
For L. vitatta (senior synonym of L. rauli), L. cf lipkei, L. jundalini, and L. wurdemanni,
morphological characteristics from specimens collected in the southwestern Atlantic
Ocean were used to develop a dichotomous key. Also, the color pattern of L. moorei has
not been officially described. Here, we used the color pattern observed in specimens
collected from tidepools in Atol da Rocas, an oceanic island off the Brazilian coast (Figs. 4H
and 4I). These specimens were collected and identified by Thais P. Macedo and are
deposited at the Zoological Collection of the UFSC (LCP/UFSC- 113). The color
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pattern exhibited by other species present in Brazil was taken from Gordon (1935),
Hayashi (1975), D’Acoz (2000), Rhyne & Lin (2006), Coelho et al. (2006), Baeza (2010),
Okuno & Fiedler (2010), Fiedler et al. (2010), Laubenheimer & Rhyne (2010), Rhyne,
Calado & Dos Santos (2012), Soledade et al. (2013), Barros-Alves et al. (2015), Giraldes &
Freire (2015), Kassuga, Diele & Hostim-Silva (2015), and Terossi et al. (2018). It must be
highlighted that the color pattern of most species likely becomes less intense when
specimens are subject to high intensity illumination (Wear & Holthuis, 1977; Calvo et al.,
2016). As pointed before, we have noticed changes in color intensity depending upon
illumination conditions in L. arvoredensis sp. nov. (Figs. 1A and 1C).
Key based on morphology
1—Outer antennular flagellum with accessory branch consisting either of a single
unguiform segment or a short segment (two or less articles). . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1—Outer antennular flagellum with accessory branch consisting of more than two free
articles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
2—Outer antennular flagellum with accessory branch consisting of an unguiform free
segment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2—Outer antennular flagellum with accessory branch consisting of a short segment
(two or less articles) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
3—Stylocerite short, just reaching to midpoint of proximal segment of antennular
peduncle, slightly beyond cornea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3—Stylocerite well developed, overreaching the mid length of proximal segment of
antennular peduncle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4—Second pereiopod with 29–30 subsegments on carpus and 11 on merus. Only one
dorsal rostral teeth posterior to the orbit. Antennular peduncle with short second and
third segment (Slightly longer than wider). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. wurdemanni
4—Second pereiopod with 15–19 subsegments on carpus and 5–9 on merus. Between
2–4 dorsal rostral teeth posterior to the orbit. Antennular peduncle with longer second
and third segments (distinctively much longer than wider) . . . . . . . . . . . . . . . . . . . . L. vittata
5—Pterygostomial tooth absent. Second pereiopod with 22–24 subsegments
on carpus and 11–16 on merus. Short pereiopods, with third pair overreaching
the scaphocerite by lengths of dactylus and proximal third of propodus.
Shorter scaphocerite, little overreaching distal margin of antennular
peduncle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. arvoredensis sp. nov.
5—Pterygostomial tooth present. Second pereiopod with 27–32 subsegments on carpus
and 23–27 on merus. Long pereiopods, with third pair overreaching the scaphocerite
by lengths of dactylus, propodus and distal fourth of carpus. Longer scaphocerite
distinctively overreaching distal margin of antennular peduncle . . . . . . . . . . . . . . . . . L. lipkei
6—Antennular peduncle shorter than scaphocerite; short second segment of antennular
peduncle, half-length of first segment. Carpus of second pereiopod with more than
25 subsegments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
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6—Antennular peduncle overreaching the scaphocerite; long second segment of
antennular peduncle, as long as first segment. Carpus of second pereiopod with 17–23
subsegments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. grabhami
7—Longer rostrum 0.6–0.8 times as long as carapace, reaching middle or rarely past the
end of third segment of antennular peduncle. Short stylocerite reaching just beyond distal
margin of eye, falling well short of end of first segment of antennular peduncle. Carpus
of second pereiopod with 33–41 (usually 35–37) subsegments . . . . . . . . . . . . . . . . . . L. ankeri
7—Shorter rostrum (about 0.5 times as long as carapace), reaching the middle of second
segment of antennular peduncle. Longer stylocerite reaching well beyond level of eye,
falling just short of distal margin of first segment of antennular peduncle. Carpus of
second pereiopod with 29–31 subsegments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. bahia
8—Rostrum and carapace with 6–7 dorsal teeth. Two or three median spines on
carapace posterior to rostrum. Carpus of second pereiopod with 28
subsegments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. jundalini
8—Rostrum and carapace with 4–5 dorsal teeth. One median spine on carapace
posterior to rostrum. Carpus of second pereiopod with 17 subsegments . . . . . . . L. moorei
Key based on color in life
1—Color conspicuous consisting of yellow background, two broad dorsolateral bands of a
brilliant red separated by a middorsal stripe of white along the entire length of the
body. Flagellum of antennae and antennules white. . . . . . . . . . . . . . . . . . . . . . . . . . . L. grabhami
1—Without conspicuous pattern. Transparent or semitransparent background body
with red lines and bands. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2—Abdomen with the presence of several longitudinal lines/bands in the
abdomen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2—Abdomen with transversal red bands dorsally in the abdomen; with virtual absence
of longitudinal lines in the abdomen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3—Broad transversal bands in the abdomen, covering most of each
pleuron . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. moorei
3—Narrow transversal bands in the abdomen, occupying less than half of each
pleuron . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. arvoredensis sp. nov.
4—At least one solid transversal band (visible dorsally) in the abdomen among the
longitudinal lines/bands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4—Without defined transversal bands (visible dorsally) in the abdomen; only
longitudinal lines/bands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
5—Several large transversal bands dorsally in the abdomen (one per segment); three
irregular longitudinal bands running through posterior half of carapace to sixth
abdominal somite . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. lipkei
5—Larger transversal band mainly in the third pleuron; absent in most
segments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
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6—Third pleuron with a broad transverse curved band with a u-shape (dorsal view),
forming with the longitudinal lines u-shapes dorsally; several solid and well-defined
longitudinal lines in the abdomen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. ankeri
6—Third pleuron with a straight transverse band not directly connected with the
longitudinal lines (not forming a u-shape in the dorsal view); with longitudinal lines,
but not all solid lines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
7—Longitudinal lines are spotted (general spotted look). Lateral view of abdomen with
only longitudinal lines (not diagonal) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. vittata
7—Longitudinal lines are solid. Lateral view of abdomen with diagonal lines
connecting with the basal longitudinal line . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. wurdemanni
8—Abdomen with broad irregular sublongitudinal bands and patches; lateral view of
abdomens with diagonal bands ventrally . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. bahia
8—Abdomen with longitudinal lines and spotted longitudinal bands; the ventral
band in the lateral view is continuous and follow the spotted pattern of other
bands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. jundalini
DISCUSSION
The dichotomous keys either based on morphological traits or color patterns herein developed
aim to support future ecological studies in the south-western Atlantic Ocean. Only a few in situ
studies has explored the ecology of the genus Lysmata in the region although most species are
often observed by scuba divers (Baeza et al., 2016). The genus Lysmata exhibits remarkable
disparity in terms of ecology, social behavior, and mating systems (Chace, 1997; Rhyne & Lin,
2006; Baeza & Anker, 2008; Baeza et al., 2009; Baeza, 2010; Laubenheimer & Rhyne, 2010;
Rhyne, Calado & Dos Santos, 2012; Baeza & Fuentes, 2013; Giraldes, Coelho Filho & Smyth,
2015). Furthermore, species that belong to the Cleaner clade have the ability to remove fish
parasites (Rhyne, Lin & Deal, 2004; Karplus, 2014). The above suggests that species in the genus
Lysmata can serve as bioindicators in reef ecosystems. We argue in favor of additional studies
on the ecology and systematics of the species in the south-western Atlantic Ocean to set a
baseline with which to monitor environmental health in the region.
ACKNOWLEDGEMENTS
Data and images included in this work were obtained within the framework of the Project
MAArE (Monitoramento Ambiental do Arvoredo e Entorno). The carrying out of the
project MAArE is a condition set by the ICMBio in the context of IBAMA’s environmental
licensing process. We are grateful to the MAArE team Barbara S. Ramos, Márcio Soldatelli,
and Ana Flora S. de Oliveira and the ICMBio team Ricardo C. Vieira and Adriana
Carvalhal from planning to fieldwork procedures. Special thanks to Alejandro D. Varella
for sampling shrimps from the ADCP; and for André Olivotto Agostinis and Marcio R. Pie
for sequencing the samples. We also thank researchers of the Crustacean and Plankton
Laboratory and Maritime Hydraulics Laboratory for sampling specimens and aquarium
maintenance. Sincere thanks are specially extended to Dr. Sammy De Grave for offering
his expert advice and comments during earlier versions of this manuscript.
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ADDITIONAL INFORMATION AND DECLARATIONS
Funding
This work was supported by Project MAArE (Monitoramento Ambiental do Arvoredo e
Entorno) and funded by the Brazilian oil company PETROBRAS. This work was also
supported by the grant from the National Counsel of Technological and Scientific
Development—CNPq (312644/2013-2, 311994/2016-4) to Andrea S. Freire. The funders
had no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Grant Disclosures
The following grant information was disclosed by the authors:
Project MAArE (Monitoramento Ambiental do Arvoredo e Entorno).
Brazilian oil company PETROBRAS.
National Counsel of Technological and Scientific Development—CNPq: 312644/2013-2,
311994/2016-4.
Competing Interests
The authors declare that they have no competing interests.
Author Contributions
Bruno W. Giraldes conceived and designed the experiments, performed the
experiments, analyzed the data, contributed reagents/materials/analysis tools,
prepared figures and/or tables, authored or reviewed drafts of the paper, approved
the final draft.
Thais P. Macedo conceived and designed the experiments, performed the experiments,
analyzed the data, contributed reagents/materials/analysis tools, prepared figures and/or
tables, approved the final draft.
Manoela C. Brandão conceived and designed the experiments, performed the
experiments, analyzed the data, contributed reagents/materials/analysis tools, prepared
figures and/or tables, approved the final draft.
J. Antonio Baeza analyzed the data, contributed reagents/materials/analysis tools,
prepared figures and/or tables, authored or reviewed drafts of the paper, approved the
final draft, English corrections.
Andrea S. Freire conceived and designed the experiments, performed the experiments,
contributed reagents/materials/analysis tools, authored or reviewed drafts of the paper,
approved the final draft.
DNA Deposition
The following information was supplied regarding the deposition of DNA sequences:
GenBank:
BankIt2027186 Seq1 MF380416.
BankIt2027186 Seq2 MF380417.
Giraldes et al. (2018), PeerJ, DOI 10.7717/peerj.5561
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Data Availability
The following information was supplied regarding data availability:
The holotype was deposited in the Natural History Museum of Rio de Janeiro, Brazil
(ID: MNRJ 27976).
New Species Registration
The following information was supplied regarding the registration of a newly described
species:
Publication LSID: urn:lsid:zoobank.org:pub:5ECAB752-E712-42E8-8FCA5C3386D7F7F9.
Lysmata arvoredensis: urn:lsid:zoobank.org:act:16D1C1E5-DED2-45CF-856F06A7C167370A.
Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/10.7717/
peerj.5561#supplemental-information.
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