J OURNAL OF C RUSTACEAN B IOLOGY, 34(6), 848-861, 2014
MOLECULAR AND MORPHOLOGICAL RESURRECTION OF CLIBANARIUS
SYMMETRICUS (RANDALL, 1840), A CRYPTIC SPECIES HIDING UNDER
THE NAME FOR THE “THINSTRIPE” HERMIT CRAB C. VITTATUS
(BOSC, 1802) (DECAPODA: ANOMURA: DIOGENIDAE)
Mariana Negri 1 , Rafael Lemaitre 2 , and Fernando L. Mantelatto 1,∗
1 Laboratory
of Bioecology and Crustacean Systematics, Post-graduate Program in Comparative Biology,
Department of Biology, Faculty of Philosophy, Sciences and Letters at Ribeirão Preto (FFCLRP),
University of São Paulo (USP), Av. Bandeirantes 3900, CEP 14040-901, Ribeirão Preto (SP), Brazil
2 Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution,
4210 Silver Hill Road, Suitland, MD 20746, USA
ABSTRACT
Analysis of the barcode region of the COI gene has unmasked a cryptic hermit crab species confounded under the name Clibanarius
vittatus (Bosc, 1802), long applied to a common littoral, striped-colored species presumed to range broadly in the western Atlantic
from the southeastern United States and Gulf of Mexico to Brazil. Molecular and morphological (color) data from recently collected
specimens distinctly show that Bosc’ name should be restricted to populations in the southeastern coast of the United States and Gulf of
Mexico, although the extent of its southern distribution remains uncertain. The two species have a genetic divergence ranging from 5.18 to
7.29% for the molecular marker analyzed. Based on a comparative study of syntypes of three taxa previously considered synonyms of C.
vittatus, and examination of museum specimens, together with recent field observations, we conclude that the confounded species should
be assigned the name C. symmetricus (Randall, 1840). A lectotype is selected for this resurrected name, with Suriname as type locality.
The distribution of C. symmetricus has been found to include with certainty the western and southern Caribbean, and coast of Venezuela to
Brazil, although it is possible that it may occur more broadly in the Caribbean, the Antilles, or southern Gulf of Mexico. Morphologically,
the two species differ only in color pattern of the lateral surface of carpi of the second and third pereiopods. A redescription of C.
symmetricus is presented, including illustrations, photographs, and discussion of taxonomy, coloration, and distribution. A phylogram is
included showing relationships with selected species of Clibanarius.
K EY W ORDS: Barcoding COI, Clibanarius, mitochondrial genes, taxonomy, western Atlantic
DOI: 10.1163/1937240X-00002277
I NTRODUCTION
The diogenid genus Clibanarius Dana, 1852 includes 59
species worldwide (McLaughlin et al., 2010), the majority
of which are found in the intertidal to shallow waters of
the littoral zone of tropical and subtropical regions, where
they often occur abundantly and are ecologically important (Southward and Southward, 1977; Lowery and Nelson,
1988; Gherardi and Vannini, 1993; Kelly and Turner, 2011).
Clibanarius was briefly diagnosed by Dana (1852), and even
to this day species of this genus can be characterized by only
a few shared characters, such as: presence of 13 pairs of
biserial gills; elongate, subrectangular shield, and short rostrum; ocular acicles close together; antennal flagella usually
but not always, with short setae; endopodite of first maxilliped with a well-developed recurved lobe; chelipeds equal
or subequal, with fingers opening horizontally and ending
in spoon-shaped corneous tips; and both sexes with four left
biramous pleopods on each of pleonal somites 2-5 (Forest
and de Saint Laurent, 1968; Rahayu and Forest, 1993). Many
species of Clibanarius, however, are anatomically so similar
∗ Corresponding
that they can only be separated by using their often subtle
color differences while alive or freshly preserved, as all vestiges of coloration eventually disappear after preservation.
In the western Atlantic, five species of Clibanarius
are currently recognized: C. antillensis Stimpson, 1859,
C. foresti Holthuis, 1959, C. sclopetarius (Herbst, 1796),
C. tricolor (Gibbes, 1850) and C. vittatus (Bosc, 1802).
One other western Atlantic species formerly assigned to
Clibanarius, C. anomalus A. Milne-Edwards and Bouvier,
1893, was shown by Forest (1989) not to fit the diagnosis
and typical shallow water distribution of species of this
genus, and was placed in his new genus Bathynarius Forest,
1989 along with a closely related eastern Atlantic species,
C. albicinctus Alcock, 1905. The five western Atlantic
species that remained in Clibanarius have been considered
valid at least since Forest and de Saint Laurent (1968)
who synonymized a number of names with one or more
of these five species. Most notably, they considered C.
cubensis de Saussure, 1858, a name often still used in the
literature of western Atlantic hermit crabs (e.g., Schmitt,
1935, 1936; Provenzano, 1959; Sánchez and Campos, 1978;
author; e-mail: [email protected]
© The Crustacean Society, 2014. Published by Brill NV, Leiden
DOI:10.1163/1937240X-00002277
NEGRI ET AL.: RESURRECTION OF CLIBANARIUS SYMMETRICUS
Rodríguez, 1980; Martínez Campos et al., 2012), as a junior
synonym of C. sclopetarius. Of the five western Atlantic
species of Clibanarius, C. vittatus or “thinstriped” hermit
crab (Williams et al., 1989; McLaughlin et al., 2005),
has been by far the most studied, and a large number
of studies have focused on various biological aspects of
this abundant species throughout its traditionally presumed
broad geographic range from the southeastern coast of the
United States to Brazil (e.g., Hazlett, 1966, 1981; Lowery
and Nelson, 1988; Ruppert and Fox, 1988; Harvey, 1996;
Turra and Leite, 2001, 2004, 2007; Hess and Bauer, 2002;
Sant’Anna et al., 2006, 2009; Mantelatto et al., 2010; Kelly
and Turner, 2011).
The similarity in morphology between C. vittatus and C.
sclopetarius was discussed by Holthuis (1959) who proposed that the two could be differentiated based on shape of
rostrum, length of ocular peduncles relative to shield width,
fifth antennal segment width, and differences in coloration
of stripes of ambulatory legs. However, except for color differences, Forest and de Saint Laurent (1968) considered all
these characters variable and useful only in distinguishing
specimens of intermediate size. Recently, Negri et al. (2012)
used molecular methods to test whether the subtle but clear
differences in striped coloration pattern of the ambulatory
legs traditionally used to separate these two species, actually
supported their separation into distinct species. While their
genetic analysis confirmed conclusively that C. sclopetarius is a separate species, they also found that the specimens
used of C. vittatus separated into two subgroups, one from
Brazil and another from the Gulf of Mexico. Negri et al.
(2012) found high molecular divergences for two mitochondrial genes (cytochrome oxidase I and 16S rDNA) between
these two subgroups, suggesting the existence of a cryptic
species confounded under the name C. vittatus. Negri et al.
(2012) did not formally take taxonomic action to divide the
latter species, and instead suggested that more specimens
and samples from intermediate regions between the northwestern and southwestern Atlantic were needed in order to
confirm the existence of a taxon confounded under the name
C. vittatus. In this study, we now use a geographically expanded specimen and molecular database to retake the Negri
et al. (2012) analysis of populations of C. vittatus traditionally considered under that name, and test further whether
indeed those populations represent two species.
Three names have so far been considered synonyms
of Bosc’s (1802) C. vittatus, a species described based
on specimens from the Carolinas (“côtes de la Caroline”)
on the southeastern coast of the United States: Pagurus
symmetricus, Randall, 1840 (transferred by Dana (1852) to
Clibanarius), C. speciosus Miers, 1877, and C. cayennensis
Miers, 1877 (Holthuis, 1959; Forest and de Saint Laurent,
1968; McLaughlin et al., 2010). Here we argue, based
on molecular and morphological (coloration) evidence and
using phylogenetic methods, that Bosc’ name should apply
to northern populations of C. vittatus sensu lato from at
least the southeastern coast of the United States and Gulf of
Mexico, whereas Randall’s name, C. symmetricus, should be
resurrected and applied to southern populations of C. vittatus
sensu lato ranging from at least Belize in the southwestern
Caribbean to Brazil. A redescription of C. symmetricus,
849
the sixth western Atlantic species in the genus, is provided
even though its morphology is highly variable and similar
to other congeners from the region, along with a taxonomic
discussion, illustrations, and photographs to document color
differences between this species, and C. vitattus sensu
stricto. The distributions of C. symmetricus and C. vittatus
sensu stricto are ascertained based on genetically sampled
specimens, taxonomic reports that have included sufficient
information on coloration, unreported specimens deposited
in museums with color patterns still visible, and our own
collections.
M ATERIALS AND M ETHODS
Specimens and Taxonomy
In order to find stronger support for the molecular findings by Negri et al.
(2012), we studied the morphology and molecular genetics of specimens
recently collected by us or supplied by our colleagues from Venezuela to
Brazil, and deposited in the Crustacean Collection, Department of Biology,
Faculty of Philosophy, Sciences and Letters at Ribeirão Preto, University
of São Paulo, São Paulo, Brazil (CCDB). We compared the morphology
of our recently collected specimens with those historically identified as
C. vittatus from northern to southern localities, deposited in the National
Museum of Natural History, Smithsonian Institution, Washington DC, USA
(USNM), and examined photographic records of specimens in the holdings
of the University of Louisiana at Lafayette Zoological Collection, Lafayette,
LA, USA (ULLZ). We examined syntypes of C. symmetricus, deposited in
the General Invertebrates Collection of the Academy of Natural Sciences,
Drexel University, Philadelphia, PA, USA (ANSP); and also the syntypes
of C. cayennensis Miers, 1877 and C. speciosus Miers, 1877, which
remain deposited in the National History Museum, London, UK (NHM).
Specimens listed in Table 1 have come from: CCDB; Natural History
Museum and Institute, Chiba, Japan (CBM ZC); National Taiwan Ocean
University, Keelung, Taiwan (NTOU); and Instituto de Ciencias del Mar,
Universitad de Barcelona, Barcelona, Spain (ICM UB). We follow Schram
and Koenemann (2004) in the use of “pleon” instead of “abdomen.” Shield
length (sl) was measured from the tip of the rostrum to the midpoint of the
posterior margin of the cephalothoracic shield. Other abbreviations used
are: USFC, United States Fish Commission; sta, station. Photographs were
taken using a stereomicroscope with a camera Leica® DFC295.
In the synonymy of C. symmetricus, only taxonomic references are
considered. No attempt has been made to elucidate the true identity of
specimens used in the numerous studies that have been published on
ecological or other biological aspects of C. vittatus sensu lato, in part
because the deposition of specimens is unknown or not extant, or if extant,
have lost their coloration and cannot be reliably identified, although identity
assumptions can sometimes be made based on the geographical origin of the
samples.
Molecular Phylogenetic Analysis
A phylogram based on the barcode region of the mitochondrial gene
cytochrome oxidase subunit I (COI) was generated with 24 sequences of
C. symmetricus and 13 of C. vittatus sensu stricto, from 9 and 4 different
localities, respectively, and 14 sequences of 13 other species of Clibanarius.
We used 10 sequences of individuals from one paguroid (Pagurus) and two
lithodoid genera (Lithodes, Paralithodes) to serve as the outgroup (Table 1).
DNA was extracted and the region of interest was amplified and sequenced following protocols of Schubart et al. (2000), with modifications
according to Mantelatto et al. (2006, 2007, 2009), Pileggi and Mantelatto (2010) and Vergamini et al. (2011). Most of the sequences were
generated by the Laboratory of Bioecology and Crustacean Systematics
(LBSC), Department of Biology, Faculty of Philosophy, Sciences and Letters at Ribeirão Preto (FFCLRP), University of São Paulo (USP), as part
of a long-term study on the molecular taxonomy of hermit crabs. Additional sequences, including those of the outgroup, were retrieved from
GenBank.
First, DNA was extracted from muscle tissues extracted from cheliped
articulations. Muscle was ground and incubated for 24 h in 600 μl of lysis
buffer and 200 μl of proteinase K at 65°C; proteins were separated by the
addition of 200 μl of 7.5 M ammonium acetate prior to centrifugation. DNA
850
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
Table 1. List of specimens used for molecular analysis, with date and collection site, voucher number and GenBank accession numbers. Superscript
numbers refer to areas sampled along São Paulo coast, each indicating a locality (also indicated in Fig. 1A). JSDN is not an institute code. Superscript letters
after GenBank acccession numbers indicate publications: a, Hirose et al. (2010); b, Hall et al. (unpublished); c, Yanagimoto, T. (unpublished); d, Ahyong
and Chan (2010); e, Grant and Cheng (2012); f, García-Merchán et al. (2012); g, Kelly and Palumbi (2010); h, Young et al. (2002); i, Matzen da Silva et al.
(2011). Country state abbreviations: BA, Bahia; FL, Florida; PA, Pará; PR, Paraná; RJ, Rio de Janeiro; SC, Santa Catarina; SP, São Paulo.
Species
Collection site, date
Catalogue No.
Clibanarius corallinus (H. Milne Edwards, 1848)
Clibanarius demani Buitendijk, 1937
Clibanarius erythropus (Latreille, 1818)
Clibanarius eurysternus (Hilgendorf, 1879)
Clibanarius lineatus (H. Milne Edwards, 1848)
Clibanarius longitarsus (De Haan, 1849)
Clibanarius merguiensis De Man, 1888
Clibanarius symmetricus (Randall, 1840)
Okinawa, Japan
Okinawa, Japan
Cadiz, Spain, Oct 2001
Okinawa, Japan
Porosi, Nicaragua, Nov 2001
Okinawa, Japan
Okinawa, Japan
Isla Margarita, Venezuela, May 2006
Clibanarius symmetricus (Randall, 1840)
Bragança, PA, Brazil, May 2010
Clibanarius symmetricus (Randall, 1840)
Ilhéus, BA, Brazil, Mar 2009
Clibanarius symmetricus (Randall, 1840)
Clibanarius symmetricus (Randall, 1840)
Clibanarius symmetricus (Randall, 1840)
Clibanarius symmetricus (Randall, 1840)
Paraty, RJ, Brazil, Aug 2007
Ubatuba, SP, Brazil, Apr 20113
São Sebastião, SP, Brazil, Jun 20022
Ilha Comprida, SP, Brazil, Apr 20111
Clibanarius symmetricus (Randall, 1840)
Guaratuba, PR, Brazil, Feb 2008
Clibanarius symmetricus (Randall, 1840)
Florianópolis, SC, Brazil, Jul 2003
Clibanarius rhabdodactylus Forest, 1953
Clibanarius sclopetarius (Herbst, 1796)
Clibanarius sclopetarius (Herbst, 1796)
Clibanarius striolatus Dana, 1852
Clibanarius signatus Heller, 1861
Clibanarius tricolor (Gibbes, 1850)
Clibanarius virescens (Krauss, 1843)
Clibanarius vittatus sensu stricto (Bosc, 1802)
Okinawa, Japan
Bocas del Toro, Panama, Aug 2011
São Sebastião, SP, Brazil, May 2010
Okinawa, Japan
Qeshm Island, Iran, Feb 2006
Cozumel, Mexico, Oct 2010
Okinawa, Japan
Island Sanctuary, FL, USA, Sep 20114
Clibanarius vittatus sensu stricto (Bosc, 1802)
Choctawhatchee Bay, FL, USA, Jul 20015
Clibanarius vittatus sensu stricto (Bosc, 1802)
Clibanarius vittatus sensu stricto (Bosc, 1802)
Texas, USA, Sep 2001
Mecoacan, TC, Mexico, Feb 2011
Lithodes confundens Macpherson, 1988
Lithodes longispina Sakai, 1971
Lithodes formosae (Ahyong and Chan, 2010)
Paralithodes camtschaticus (Tilesius, 1815)
Pagurus alatus Fabricius, 1775
Pagurus hirsutiusculus (Dana, 1851)
Pagurus longicarpus Say, 1817
Pagurus pubescens Kröyer, 1838
Pagurus samuelis (Stimpson, 1857)
Pagurus venturensis Coffin, 1957
Not available
Not available
Yilan County, Taiwan, Jun 1998
Not available
Not available
Alaska, USA, 2007
Mohane Bay, Nova Scotia, Canada
Barents Sea, Norway, Oct 2004
Santa Barbara, USA, 2007
Santa Barbara, USA, 2008
AB507374a
AB496940a
JN671592
AB496942
JN671594
AB496944a
AB496945a
KM101462
KM101463
CCDB 2944
JN671540 JN671541
JN671542 JN671543
JN671544
CCDB 2907
JN671550 JN671545
JN671546
CCDB 2237
JN671548
CCDB 1651
JN671547
CCDB 2947
JN671549
CCDB 3363
JN671551 JN671552
JN671553 JN671554
JN671555
CCDB 2262
JN671556 JN671557
JX238505
CCDB 2946
JN671558 JN671559
JN671560
CBM ZC 9593
AB496946a
CCDB 3563
JQ805895
CCDB 2961
JN671584
CBM ZC 9624
AB507376a
CCDB 3694
JN671590
CCDB 504
JN671593
CBM ZC 9621
AB507377a
CCDB 3783
JX238506
JX238507
JX238508
CCDB 1189
JN671530 JN671531
JN671532
CCDB 1185
JN671533
CCDB 3364
JN671534 JN671535
JN671536 JN671537
JN671538 JN671539
Not available
HM020901b
Not available
AB476814c
NTOU A01090
GU289678d
Not available
JF738248e
ICM UB Pala01_01 JN564864f
Not available
GU442450g
Not available
AF483113h
JSDN 22
JQ305956i
Not available
GU443074g
Not available
GU442190g
was precipitated by the addition of 600 μl of cold absolute isopropanol,
followed by centrifugation; the resulting pellet was washed with 70%
ethanol, dried, and resuspended in 20 μl of TE buffer. The final DNA
concentration was measured using NanoDrop® 2000 Spectrophotometer
(Thermo Scientific).
GenBank accession
No. (COI)
CBM ZC 9622
CBM ZC 9585
CCDB 488
CBM ZC 9588
CCDB 2444
CBM ZC 9583
CBM ZC 9592
CCDB 4531
Polymerase chain reaction (PCR) was used to amplify a fragment of
approximately 700 base pairs of the COI in a PxE0.2 (Thermo Electron
Corporation) or a Veriti 96-Well (Applied Biosystems) Thermal Cyclers
(thermal cycles: initial denaturing for 2 min at 94°C; annealing for 35
cycles: 30 s at 94°C, 30 s at 46-50°C, 1 min at 72°C; final extension
NEGRI ET AL.: RESURRECTION OF CLIBANARIUS SYMMETRICUS
2 min at 72°C). Two pairs of primers were used: COH6 (5 -TADACTTCD
GGRTGDCCAARAYCA-3 ) and COL6b (5 -ACAAATCATAAAGATAT
YGG-3 ) (Schubart and Hubert, 2006); LCO-1490 (5 -GGTCAACAAATC
ATAAAGATATTG-3 ) and HCO-2198 (5 -TAAACTTCAGGGTGACCAA
AAAATCA-3 ) (Folmer et al., 1994). PCR products were purified using the
kit SureClean Plus® and then a second PCR using the same primer set was
run with the ABI BigDye® Terminator Mix (Applied Biosystems, Carlsbad,
CA, USA) and the products of this second PCR were sequenced (forward
and reverse directions) in an ABI Prism 3100 Genetic Analyzer® (Applied
Biosystems automated sequencer) following Applied Biosystems protocols.
Sequences were assembled, cleaned and edited from two strands
sequences to obtain a consensus sequence using the computational program
BioEdit 7.0.5 (Hall, 2005). Multiple sequences aligning were performed
with the aid of Clustal W (Thompson et al., 1994) with an interface to
BioEdit (Hall, 2005) with default parameters.
The molecular tree was constructed using a Maximum Likelihood (ML)
analysis conducted in the RAxML v.7.0.4 program (Stamatakis, 2006)
through the online version of the Cyber Infrastructure for Phylogenetic
Research (CIPRES) website (Stamatakis et al., 2008; Miller et al., 2010).
The default parameters of RAxML were used to perform the analysis for
the GTR model of evolution. To measure the consistency of the topology,
we selected the option to automatically determine the number of bootstraps
to be run in RAxML. Consequently, 950 bootstrap pseudo-replicates were
run, and only values > 50% were reported.
R ESULTS
Molecular Analysis
The final multiple sequence alignment included 595 bp. The
nucleotide frequencies were: A = 0.291596, C = 0.194360,
G = 0.174043, T = 0.340001; the substitution rates were:
A-C = 4.029421, A-G = 31.580560, A-T = 13.918809,
C-G = 2.225914, C-T = 89.881667, G-T = 1.000000;
the proportion of invariable sites I = 0.565802; and alpha
parameter α = 1.289298. When the genetic relationships of
C. vittatus sensu lato with other congeners were analyzed
in a phylogram (Fig. 1A), a clear separation was shown
in the tree between specimens from the Gulf of Mexico
(indicated as C. vittatus sensu stricto), and those from
Venezuela to Brazil (indicated as C. symmetricus), with a
genetic divergence ranging from 5.18 to 7.29%, and a strong
bootstrap value of 91. Thus, based on this molecular data
and phylogenetic analysis, it is clear that one species, C.
vittatus sensu stricto, occurs in the northern portions of the
western Atlantic, at least in the Gulf of Mexico, whereas
another species previously confounded under the name C.
vittatus sensu lato, herein assigned to C. symmetricus, occurs
in the southern portions of the western Atlantic, at least from
Venezuela to Brazil (Table 1, Fig. 1).
Systematics
Diogenidae Ortmann, 1892
Clibanarius symmetricus (Randall, 1840)
Figs. 1A-C, 2B, C, 3-5
Pagurus symmetricus Randall, 1840: 133 (type locality: Suriname,
restricted by lectotype selection).
Clibanarius symmetricus – Dana, 1852: 464.
Clibanarius vittatus – Smith, 1869: 18, 39; Rathbun, 1900: 144;
Moreira, 1901: 28; Alcock, 1905: 160; Holthuis, 1959: 141,
Figs. 26a, b, 27; Williams, 1965: 120 (in part), Fig. 97 (see
Remarks); Forest and de Saint-Laurent, 1968: 104; Coelho and
Ramos, 1972: 170; Sánchez and Campos, 1978: 32, Fig. 9;
Williams, 1984: 195 (in part), Fig. 135 (see Remarks); Coelho
and Ramos-Porto, 1986: 52; Abele and Kim, 1986: 339 (in part),
unnumbered fig. e, d (see Remarks); Coelho-Santos and Coelho,
1995: 163, 169, Fig. 2b, 170; Rieger, 1997: 422; Melo, 1999: 56,
851
Fig. 14; Nucci, 2002: 29, Figs. 13, 14; Batista-Leite et al., 2003:
227; Almeida et al., 2006: 11; Coelho et al., 2007: 9; Martínez
Campos et al., 2012: 248, tbl. 4; Negri et al., 2012: 563, Figs. 1,
2, tbls. 1-3 (in part), Fig. 4 (see Discussion).
Clibanarius cayennensis Miers, 1877: 657, pl. 66, Fig. 1 (type
locality by monotypy: Cayenne, French Guiana).
Clibanarius speciosus Miers, 1877: 658, pl. 66, Fig. 3 (type locality
by lectotype selection herein: Rio de Janeiro, Brazil).
?Clibanarius vittatus – Ives, 1891: 208, pl. 5, Fig. 3; Provenzano,
1959: 367, Fig. 5d; Rodríguez, 1980: 224; Voss, 1976: 92, 93
(unnumbered fig.); Gómez Hernández and Pérez P., 1984: 30;
Gómez Hernández and Martínez-Iglesias, 1986: 26; Williams et
al., 1989: 29; Markham et al., 1990: 425; Hernández Aguilera et
al., 1996: 47; Strasser and Price, 1999: 37; Raz-Guzman et al.,
2004: 628; Rodríguez-Almaraz and Zavala-Flores, 2005: 275,
not Fig. 7, lam. 8B; McLaughlin et al., 2005: 241; Felder et al.,
2009: 1068 (see Discussion).
Type Material.—Lectotype herein selected (dry, sex undetermined due to damaged condition of ventral part of thorax and missing pleon) sl 11.2 mm, Suriname, no other data,
coll. Dr. Herring (ANSP 3229); paralectotype, 1 dry specimen (sex undetermined) sl 9.5 mm, “East Indies,” [no other
data], coll. J. Longstreth (ANSP 3229).
Holotype of Clibanarius cayennensis Miers, 1877: 1
male (dry) sl 10.2 mm, Cayenne, French Guyana (NHM
1879.21.1).
Lectotype herein selected of Clibanarius speciosus Miers,
1877: 1 male (dry) sl 9.5, mm, Rio de Janeiro, Brazil, no
other data (NHM 1850.7).
Additional Material Examined.—Caribbean. Belize: 3 males
(sl 9.6-14.3 mm), near Belize City, USNM 21380. Panama:
Smithsonian Biological Survey of Panama Canal: 1 male
(sl 11.3 mm), Fox Bay, Canal Zone, Colón, 3 January
1911, coll. Meek & Hildebrand, USNM 44195; 1 male (sl
6.3 mm), [same locality as previous], 22 January 1912,
USNM 1076269; 1 ovig. female (sl 4.5 mm), Canal Zone,
Colon, 31 March 1911, coll. Meek & Hildebrand, USNM
44196; 1 male (sl 5.4 mm), Bahía de Portobelo, 24 April
1911, coll. Meek & Hilderbrand, USNM 44197; 2 males
(sl 4.8, 5.6 mm), 2 females (sl 3.8, 4.1 mm), Gatún Locks,
lower east chamber wall, sta. 177, 9°16 40 N, 79°55 30 W,
5 March 1974, coll. M. Jones, USNM 1249512; 2 males (sl
5.8, 5.9 mm), 2 females (sl 4.7, 4.9 mm), 5 ovig. females
(sl 5.0-5.9 mm), [same sta and date as previous], USNM
1249513; 2 males (sl 4.2, 6.8 mm), 3 females (sl 4.14.3 mm), [same sta and date as previous], USNM 1249510;
6 males (sl 4.5-7.2 mm), 1 female (sl 5.2 mm), 3 ovig.
females (sl 4.6-5.4 mm), Gatún Locks, lower W chamber
outer sill, sta. 81-9 P, 20 March 1972, coll. M. Jones,
USNM 1249511. Colombia: 1 ovig. female (sl 7.8 mm),
Bahia Cispata, Gulf of Morrosquillo, 0.5 mile into channel
to Ciénaga de Soledad, ∼3 m, 6 January 1995, coll. R.
Lemaitre & D. L. Felder, USNM 1093268; 10 males (sl 5.711.7 mm), Sabanilla [Puerto Colombia], USFC Albatross,
[shore collection], 16 March 1884, USNM 7572. Venezuela:
2 males (sl 8.9, 11.3 mm), Isla Margarita, Punta Pescadores,
09°53 N, 61°35 W, 18 May 2006, coll. Julian Mora-Day,
CCDB 4531 (DNA voucher). Trinidad and Tobago: 16 males
(sl 5.3-11.9 mm), 12 females (sl 5.2-6.9 mm), 2 ovig.
females (sl 6.8, 6.9 mm), 7 in shells (not sexed or measured),
Trinidad, USFC Albatross, [shore collection], [no day,
852
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
Fig. 1. A, Phylogram showing relationships among selected species of Clibanarius Dana, 1852, inferred from ML analysis of COI sequences. Numbers
below branches are bootstrap values (950 replicates); only values higher than 50% are shown and only for largest clades (superscript indicates locality of
specimen, see also Table 1; country state abbreviations: USA: FL, Florida; TX, Texas; Mexico: QR, Quintana Roo; Brazil: AL, Alagoas; BA, Bahia; CE,
Ceará; ES, Espírito Santo; PA, Pará; PE, Pernambuco; PI, Piauí; PR, Paraná; RJ, Rio de Janeiro; RN, Rio Grande do Norte; SC, Santa Catarina; SP, São
Paulo). B, C: Clibanarius symmetricus (Randall, 1840), male sl 8.0 mm, Trincheira Beach, Ilha Comprida, São Paulo, Brazil, CCDB 3363. D, E: Clibanarius
vittatus sensu stricto (Bosc, 1802), male sl 16.0 mm, Barrier Island Sanctuary, Florida, USA, CCDB 3695. B, D: right chela, dorsal view; C, E: carpus of
third pereiopod, lateral view. Scales: B, C, 2 mm; D, E, 5 mm.
month] 1884, USNM 7644. Atlantic coast of South America.
French Guyana: 3 males (sl 5.5-7.1 mm), Cayenne, Rémiré
Beach, 04°53 S, 52°15 W, 25 September 2000, collector
not informed, MZUSP 16171. Brazil: Pará State: 5 males
NEGRI ET AL.: RESURRECTION OF CLIBANARIUS SYMMETRICUS
Fig. 2. Right chela, dorsolateral view. A, Clibanarius vittatus sensu stricto
(Bosc, 1802): male, sl 10.9 mm, Choctawhatchee Bay, Florida, USA,
CCDB 1189. B, C, Clibanarius symmetricus (Randall, 1840): B, lectotype,
sex undetermined, sl 11.2 mm, Suriname, ANSP 3229; C, male, sl 11.6 mm,
Macapá Mangrove, Piauí, Brazil, CCDB 2905. Scale: 6 mm.
(sl 6.1-8.5 mm), Urujuçuaba Beach, Bragança, 00°49 S,
46°36 W, 27 May 2010, coll. F. Abrunhosa, CCDB 2944
(DNA voucher); Piauí State: 1 male (sl 11.6 mm), Macapá
Mangrove, Macapá, 02°54 S, 41°26 W, November 2004,
coll. L. C. Fernandes-Góes and J. M. de Góes, CCDB 2905;
Paraiba State: 1 male (sl 7.3 mm), Mamanguape stone reef,
Branner-Agassiz Expedition, 23 June 1899, USNM 25771;
6 males (sl 3.1-5.2 mm), Rio Paraiba do Norte, Cabedelo,
Branner-Agassiz Expedition, on mangroves, 20 June 1899,
USNM 25773; Alagoas State: 1 male (sl 6.4 mm), Maceió,
Branner-Agassiz Expedition, coral reef, [no date], USNM
25772; Bahia State: 3 males (sl 5.5-6.8 mm), Maramata
Beach, Ilhéus, 14°48 S, 39°02 W, 31 March 2009, coll. A. O.
Almeida and F. L. Mantelatto, CCDB 2907 (DNA voucher);
Rio de Janeiro State: 1 male (sl 11.9 mm), Rio de Janeiro,
[no other precise locality or date], USNM 48307; 1 male
(sl 8.1 mm), Pontal Beach, Paraty, 23°12 S, 44°42 W, 17
August 2007, coll. F. L. Mantelatto, CCDB 2237 (DNA
voucher); São Paulo State: 1 male (sl 8.6 mm), Itaguá
Beach, Ubatuba, 26°27 S, 45°03 W, 04 April 2004, coll.
R. Robles, CCDB 1651; 8 males (sl 6.8-9.2 mm), Araçá
mangrove, São Sebastião, 23°48 S, 45°24 W, June 2002,
coll. F. L. Mantelatto, CCDB 2947 (DNA voucher); 3 males
(sl 9.0-10.0 mm), Araçá mangrove, São Sebastião, 23°48 S,
45°24 W, 17 December 2002, coll. F. L. Mantelatto, CCDB
1427; 6 males (sl 6.0-8.0 mm), Trincheira Beach, Ilha
Comprida, 24°54 S, 47°45 W, 17 April 2011, coll. F. L.
Mantelatto, M. Negri, N. Rossi, and R. Buranelli, CCDB
3363 (DNA voucher). Paraná State: 2 males (sl 8.1, 8.8 mm),
Brava Beach, Guaratuba, 25°21 S, 48°34 W, 20 February
2008, coll. F. L. Mantelatto and E. C. Mossolin, CCDB 2277
(DNA voucher); Santa Catarina State: 1 male (sl 6.2 mm),
Sambaqui Beach, 27°29 S, 48°32 W, 16 April 2007, coll.
F. L. Mantelatto, E. C. Mossolin, L. A. G. Pileggi and L. S.
Torati, CCDB 1889 (DNA voucher).
Comparative Material of Clibanarius vittatus Sensu
Stricto.—Southeastern United States. Delaware: 2 males (sl
13.0, 16.3 mm), coast of Delaware, [no date], USNM 56474;
Virginia: 1 male (sl 5.3 mm), 1 female (sl 5.7 mm), Gunston, Potomac River, 24 June 1881, coll. M. Mcdonald,
USNM 4138; 2 males (sl 10.9, 15.2 mm), R/V Fish Hawk,
853
Lynnhaven Inlet, Virginia Beach, 15 July 1916, USNM
56473; North Carolina: 5 males (sl 5.4-15.9 mm), 5 females
(sl 5.5-10.4 mm), Carteret County, Beaufort, USNM 42547;
South Carolina: 3 males (sl 7.9-11.8 mm), 6 females (5.211.6 mm), Charleston Harbor, 32°45 00 N, 79°52 59 W,
coll. M. Mcdonald, USNM 4141; Georgia: 1 female (sl
6.0 mm), Black Beard Creek, Sapelo Island, [no month, day]
1962, coll. M. Gray, USNM 150237; Florida: 3 males (sl
13.2-15.9 mm), 1 female (sl 7.2 mm), Indian River Lagoon,
Barrier Island Sanctuary, 27°54 N, 20°28 W, 20/21 September 2011, coll. B. O’Neill, CCDB 3783; 4 males (sl 8.812.3 mm); 1 male (sl 6.7 mm), Coral Gables, [no date], coll.
J. Pearson, USNM 77413. Gulf of Mexico. Florida: Florida
Keys: 2 males (sl 9.5, 9.8 mm), 1 female (sl 11.2 mm),
Dry Tortugas, Bush Key Reef, Tortugas Expedition Carnegie
Lab, sta 46-32, 15 July 1932, coll. R. Stone & W. Schmitt,
USNM 265325; Choctawhatchee Bay, 30°27 N, 86°21 W,
20 July 2001, coll. F. L. Mantelatto and R. Robles, CCDB
1189; 3 males (sl 15.6-16.1 mm), Eagle Harbor, Cape Saint
Joe, 29°46 N, 85°24 W, 01 April 2011, coll. D. Peiró and J.
Rasch, CCDB 3695; Mississippi: 3 males (sl 10.4-11.8 mm),
mouth of Mississippi River, [no day, month] 1891, coll. H.
Ward, USNM 42546; Louisiana: 92 males (sl 3.5-10.3 mm),
54 females (sl 5.6-7.6 mm), Grand Terre Island, <1 m, 2 November 1999, coll. G. Hess, USNM 1009413; Texas: 2 males
(sl 9.1, 9.8 mm), jetty rocks, Port Aransas, 25 November
1945, coll. J. Hedgpeth, USNM 1249514. Mexico: Tabasco
State: 1 male (sl 7.7 mm), Puerto Cieba, intertidal, 5 July
2002, coll. D. L. Felder et al., ULLZ 10292 (photo voucher);
6 males (sl 10.3-16.0 mm), Mecoacan Lagoon, Mecoacan,
18°23 N, 93°08 W, 25 February 2011, coll. E. Barba, CCDB
3364.
Redescription.—Gills biserial. Shield (Figs. 3A, 5) about as
long as broad or slightly longer than broad (on average 1.1 as
long as broad). Rostrum short, acutely or bluntly triangular,
slightly exceeding lateral projections. Lateral projections
broadly triangular, terminating in small blunt or sharp spine.
Ocular peduncles (Figs. 3A, 5) length distinctly greater
than shield width, corneas weakly dilated. Ocular acicles
(Fig. 3A, B) subtriangular, nearly approximate at base, with
corneous-tipped spines (1 terminal, 1-3 supplemental spines
on lateral margin).
Antennular peduncles (Fig. 3A) reaching or sometimes
slightly exceeding distal margins of corneas when fully
extended. Ultimate and penultimate segments unarmed.
Basal segment with spine on inner ventrodistal margin, and
row of 2-4 spines on laterodistal angle.
Antennal peduncles (Fig. 3A, C) reaching or sometimes
slightly exceeding distal margins of corneas. Fifth and
fourth segments unarmed except for few tufts of setae.
Third segment with simple or bifid ventrodistal spine.
Second segment with strong spine on dorsodistal angle. First
segment with strong ventrodistal spine. Antennal flagella
short, reaching to about tips of dactyls of ambulatory
legs, with minute, short setae. Antennal acicles (Fig. 3A,
C) subtriangular, reaching or slightly overreaching distal
margin of fourth segment; with 3-7 mesial spines, of which
usually 1-3 terminal and sometimes 1 or 2 on outer margin.
Chelipeds equal or weakly subequal. Chelae (Figs. 1B, C,
3D, E, 5) each about 2 times longer than broad (on average
854
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
Fig. 3. Clibanarius symmetricus (Randall, 1840): male, sl 8.0 mm, Trincheira Beach, Ilha Comprida, São Paulo, Brazil, CCDB 3363. A, shield and cephalic
appendages (ocular, antennal and antennular peduncles), dorsal view; B, distal half of right ocular acicle, dorsal view; C, right antennal peduncle, dorsal
view; D, right cheliped, mesial view; E, right chela, dorsal view. Scales: A, D, E, 5 mm; B, 0.5 mm; C, 2 mm.
NEGRI ET AL.: RESURRECTION OF CLIBANARIUS SYMMETRICUS
855
Fig. 4. Clibanarius symmetricus (Randall, 1840): male, sl 8.0 mm, Trincheira Beach, Ilha Comprida, São Paulo, Brazil, CCDB 3363. A, right third
pereiopod, lateral view; B-E, merus (E), carpus (D), propodus (C), and dactyl (B) of same, lateral view; F, right fourth pereiopod, lateral view; G, right fifth
pereiopod, lateral view; H, telson, dorsal view. Scales: A, 10 mm; B-E, G, 2 mm; F, 4 mm; H, 1 mm.
2.2 as long as broad), dorsal surfaces with numerous small
spines and tubercles denser on fingers and distal portion
of palm, and scattered tufts of short setae; ventral surface
with few, well-spaced blunt spines or tubercles. Fingers
terminating in spoon-shaped corneous tips. Carpus with
dorsal and lateral surfaces armed similarly to chela but not
as dense, dorsodistal margin with 1 or 2 strong, corneoustipped spines on mesial angle, and few tufts of short setae;
856
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
Fig. 5. Clibanarius symmetricus (Randall, 1840): male, sl 10.0 mm, Araçá mangrove, São Sebastião, São Paulo, Brazil, CCDB 4900. Photo by Buranelli,
R. C. and L. G. Pileggi. Scale: 10 mm.
ventral surface unarmed. Merus with small tubercles and
few tufts of short setae on dorsal margin; ventrolateral and
ventromesial margins with row of small blunt spines; ventral
face unarmed. Ischium with ventromesial margin armed with
row of tiny spines.
Second and third pereiopods (ambulatory legs, Figs. 4AE, 5) subequal left from right; with tufts of short setae
on dorsal, dorsolateral and dorsomesial surfaces. Dactyl
(Figs. 4A, B, 5) about 1.1 (second pereiopod) or 1.3
(third pereiopod) as long as propodus, terminating in sharp,
curved, corneous claw; with ventrodistal row of corneous
spines. Propodus (Figs. 4A, C, 5) about 1.5 times (second
pereiopod) or 1.6 times (third pereiopod) as long as carpus;
with 2 or 3 blunt spines on ventrodistal margin. Carpus
(Figs. 4A, D, 5) about 0.7 (second pereiopod) or 0.8
(third pereiopod) length of merus, with 1 or 2 corneoustipped dorsodistal spines. Merus (Fig. 4A, E) armed with
row of small spines throughout ventral margin (second
pereiopod), or with few spines distally on ventral margin
(third pereiopod).
Fourth pereiopod (Fig. 4F) semichelate, with numerous
tufts of long setae. Dactyl terminating in corneous claw, with
ventrolateral row of small corneous spinules. Propodal rasp
well developed, with 10 or more rows of ovate scales. Carpus
with strong, corneous-tipped dorsodistal spine.
Fifth pereiopod (Fig. 4G) chelate; with numerous tufts of
long setae; propodal rasp well developed (occupying about
one-third to half of lateral surface of propodus).
Uropods markedly asymmetrical, left distinctly larger
than right; exopodal and endopodal rasps well developed.
Telson (Fig. 4H) asymmetrical, left lobe distinctly larger
than right; distal margins of posterior lobes strongly rounded,
each with row of spines and long setae, lobes separated by
distinct median cleft; lateral indentations distinct.
Color (Fresh Specimens).—Shield (Fig. 5) olive-green mottled with lightly colored small spots, and with brownish areas on anterior and lateral regions. Ocular peduncles
(Figs. 3A, 5) lightly colored except for darker, olive-green
dorsomesial surfaces. Antennal (Figs. 3A, C, 5) peduncles
olive green, with whitish longitudinal stripe on dorsal sur-
NEGRI ET AL.: RESURRECTION OF CLIBANARIUS SYMMETRICUS
faces of fourth and fifth segments; antennal flagella olive
green, each with orange stripe. Chelipeds (Fig. 5) overall
olive-green with lightly colored spines or tubercles; carpi
and meri less darkly colored than chelae, carpi each with
two whitish stripes dorsally. Second and third pereiopods
(ambulatory legs, Figs. 4A, 5) with distinct, straight white
stripes on olive-green background; dactyls, propodi and
carpi (Figs. 1C, 4B-D, 5) each with three white stripes (one
dorsolateral, and two on lateral surface, the latter two in
propodi curving sharply at one or both ends and joining to
form elongated rectangle), and lightly colored ventral margin; meri (Fig. 4E) each with white dorsomesial stripe extending throughout segment, and two (second pereiopod) or
three (third pereiopod) more or less slightly oblique white
stripes not covering entire segment.
Distribution.—Western Atlantic, in the Caribbean from at
least Belize, Panama, Colombia, Venezuela, Trinidad and
Tobago, and northeastern coast of South America from
French Guyana to Santa Catarina, Brazil. Usually intertidal
or in shallow waters less the 1 m, infrequently ranging to
22 m. Most frequently found in estuarine and mangrove
areas.
D ISCUSSION
Based on molecular and coloration data, C. vittatus sensu
stricto can herein be applied with certainty to northern
populations from the southeastern coast of the United States
and Gulf of Mexico, whereas the species confounded under
C. vittatus sensu lato occurs at least in the Caribbean (Belize,
Panama, Colombia, Venezuela, Trinidad and Tobago), and
northeastern coast of South America from French Guyana to
Brazil. As previously mentioned, there are three names that
were considered in the past to be synonyms of Bosc’ (1802)
C. vittatus and that morphologically could apply to the
confounded species: C. symmetricus, C. cayennensis and C.
speciosus, all described based on specimens from Suriname,
French Guiana and Brazil, respectively (see Holthuis, 1959;
Forest and de Saint Laurent, 1968; McLaughlin et al.,
2010). We have examined the types of these three taxa,
studied the original albeit brief original descriptions, and
conclude that, despite inconsistencies or incompleteness in
color descriptions and the poor, dry and virtually colorless
condition of these type specimens, the most senior name,
Randall’s (1940) C. symmetricus, should be adopted for the
species previously confounded under C. vittatus sensu lato.
Randall (1940) mentioned the color of his species only as
“yellowish” and did not indicate any stripes, although it
is unclear if he observed fresh or faded, dry specimens.
In other respects, Randall’s syntypes exhibit a large body
size (sl 9.5, 11.5 mm) and cheliped spination pattern
consistent with that observed by us in the genetically
analyzed specimens from Venezuela to Brazil. Randall
(1940) used two syntype specimens, one from Suriname
and another smaller specimen (found severely damaged)
from the “East Indies”; in order to fix the name, we herein
choose the former syntype specimen as the lectotype for C.
symmetricus.
We have studied the literature and collections from
numerous localities in Venezuela to Brazil, and have not
found any specimens from this extense coastline that can be
857
identified genetically or using color patterns, as Clibanarius
vittatus sensu stricto, and conclude that this species does
not occur along the Atlantic coast of South America. Thus,
we are confident that a number of taxonomic studies from
that coast of South America that have previously reported
C. vittatus sensu lato, are assignable to C. symmetricus
(see synonymy entry: C. vittatus). Williams (1965, 1984)
and Abele and Kim (1986) did focus on decapods from
Florida and the southeastern coast of the United States, but
reproduced or used a modified illustration from Holthuis’
(1959) report of C. vittatus from Suriname, which actually
represents C. symmetricus. In their genetic analysis of C.
vittatus sensu lato, Negri et al.’s (2012) used specimens from
the Gulf of Mexico and Brazil, and the latter represent as
well C. symmetricus.
While it is clear from our genetic analysis that Clibanarius
vittatus sensu lato contains two species, C. vittatus sensu
stricto and C. symmetricus, it is difficult to determine
precisely the extent of their distributions. Because many
earlier reports of C. vittatus sensu lato lack information
on coloration or the species name is only listed as part
of faunistic inventories, and most collections upon which
those reports were based are unavailable or if available
the specimens have lost coloration, it is not possible to
ascertain their true identity. Furthermore, the scarcity of
reports or collections of Clibanarius from many areas in
the Caribbean and the Antilles (except for Cuba), hinders
understanding of the exact ranges of these two species, and
whether their ranges overlap or not in those areas. Herein we
can confirm, based on color data in USNM specimens, that
C. symmetricus occurs at least as far north in the western
Caribbean as the coast of Belize. Several studies that have
reported C. vittatus sensu lato from the southern portions of
the Gulf of Mexico to the Caribbean coast of Yucatán, or the
Gulf and Atlantic coasts of southern Florida (Provenzano,
1959; Voss, 1976; Williams et al., 1989; Markham et al.,
1990; Hernández Aguilera et al., 1996; Strasser and Price,
1999; Raz-Guzmán et al., 2004; McLaughlin et al., 2005;
Felder et al., 2009), and Cuba (Gómez Hernández and Pérez
P., 1984; Gómez Hernández and Martínez-Iglesias, 1986),
could conceivably include C. symmetricus. Therefore, in
our synonymy we consider as questionable (see entry:
?Clibanarius vittatus) a number of reports of C. vittatus
sensu lato, as those reports could potentially represent in full
or in part, C. symmetricus. However, Rodríguez-Almaraz
and Zavala-Flores (2005: Fig. 7, lam. 8B) clearly illustrated
a specimen of C. vittatus sensu stricto from Tamaulipas,
although they listed numerous specimens from Tamaulipas
to Campeche, and thus it is possible that some of their most
southerly collected specimens could represent instead C.
symmetricus.
The study of morphology and molecular analyses using
16S rDNA and barcode COI (Negri et al., 2012 and present
study) show that Clibanarius symmetricus and C. vittatus
sensu stricto are different but closely related species. The
morphology is so similar, however, that the only reliable
morphological character that can be used to separate C.
symmetricus from C. vittatus sensu stricto, is the coloration
pattern on the lateral face of the carpi of the ambulatory
legs, although unfortunately the coloration in specimens
858
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
disappears completely after some time in preservative.
Holthuis (1959: 145) actually was the first to point out color
differences between specimens of C. vittatus sensu lato from
Suriname and those from Florida, when he briefly noted that
the “bands” [stripes] on the legs in specimens from Suriname
were narrower than in those from Florida, although he did
not suggest that two species might be involved. We have
found that the carpi of the ambulatory legs in C. symmetricus
each have three straight, whitish longitudinal stripes, two on
the lateral face and one on the dorsal or dorsolateral margin
(Fig. 1C). In contrast, the carpi of the ambulatory legs in
C. vittatus sensu stricto have four stripes on the lateral face:
one straight lateroventral, two submedian and approximate
of which the lower stripe is slightly curved proximally and
together with the upper stripe form the top of a blunt,
posteriorly schewed triangle, and one straight dorsolateral
(Fig. 1E). When comparing the morphology of these two
species, we observed in some specimens differences in
density and sharpness of spines on the dorsal surfaces of the
chelae. The spines and tubercles tend to be denser, larger,
and usually blunt in C. symmetricus, whereas the spines
are not as dense or as large, and are usually sharp, in C.
vittatus sensu stricto (Figs. 1B, D, 2A, C). Unfortunately, the
difference in spination is of limited value as a differentiating
character because of the considerable interspecific overlap
in spination of chelae between these two species depending
on size of specimens and geographic area.
Clibanarius symmetricus resembles C. sclopetarius, from
which it differs in telson morphology, chela ornamentation,
and color pattern of ambulatory legs. In C. symmetricus,
the distal margins of the posterior lobes of the telson are
distinctly rounded and divided (Fig. 4H); the dorsal surface
of the chelae have dense spines and tubercles (Fig. 1B,
2B, C, 5); and the white stripes on the lateral face of the
ambulatory legs are thin, with one median stripe on propodus
and two on the dactyl (Fig. 1C, 4A-C) (see Negri et al.,
2012: Fig. 4A, C, D as C. vittatus). In C. sclopetarius, the
distal margins of the posterior lobes of the telson are broadly
rounded or nearly straight, and weakly divided, the chela
tubercles and spines are not dense, well spaced, and the
white stripes on the lateral face of the ambulatory legs are
wide, with one broad, median dark stripe on the propodus
continued on the dactyl (see Negri et al., 2012, Fig. 3A,
C, D).
Clibanarius symmetricus, C. vittatus sensu stricto, C.
sclopetarius, and C. foresti, are similar in relative length
proportion of propodi and dactyls of ambulatory legs, with
dactyls being distinctly longer than propodi, as well as in
the striped pattern of coloration on the ambulatory legs. As
discussed above, C. symmetricus, C. vittatus sensu stricto
and C. sclopetarius are morphologically nearly identical
except for subtle differences in color, whereas C. foresti
is easily distinguishable from the other three species by
its slender ocular peduncles, slender, long antennules that
exceed the corneas by more than half the length of the
ultimate antennular segments, small size of individuals, and
deeper habitat ranging from 7 to 75 m. The remaining
western Atlantic species of Clibanarius, C. antillensis and
C. tricolor, are morphologically clearly separated by having
the dactyls of the ambulatory legs distinctly shorter than the
propodi, as well as their significantly different coloration
patterns.
In conclusion, the use of molecular and morphological
data (primarily color) has made possible the resurrection and
definition of Clibanarius symmetricus, a species briefly described 174 years ago but considered a junior synonym of C.
vittatus sensu lato since Holthuis (1959). The genetic divergences found herein between C. symmetricus and C. vittatus
sensu stricto, 5.18-7.29% and 1.4%, for the COI gene and
16S rDNA, respectively, are comparable to interspecific genetic divergences known for other Paguroidea (Mantelatto
et al., 2006) and anomurans (Knowlton, 2000; Macpherson and Machordom, 2001, 2005; Mantelatto et al., 2009),
or other decapods (Tam et al., 1996; Tam and Kornfield,
1998; Macpherson and Machordom, 2004, 2005). Although
coloration is known to vary intraspecifically in some decapod crustaceans (Bauer, 1981; Wilson, 1987; Schubart et al.,
2001; Reuschel and Schubart, 2007), we have demonstrated
that at least in C. symmetricus and C. vittatus sensu stricto,
the relatively minor differences in the patterns of stripes on
the ambulatory legs do reflect species distinctness.
As result of our study, we recognize six valid western Atlantic species of Clibanarius, three of which (C. antillensis, C. tricolor and C. sclopetarius) are considered to range
broadly in the western Atlantic, albeit not always continuously, from the southeastern coast of the United States, and
Bermuda, to Brazil (e.g., Felder et al., 2009). The range
of C. symmetricus can at present only be confirmed to include the western and southern Caribbean (Panama, Colombia, Venezuela), Trinidad and Tobago, and French Guyana
to Brazil, and the range of C. vittatus sensu stricto only the
eastern coast of the United States and northern Gulf of Mexico. In contrast, C. foresti seems to have a relatively narrow
range, and is so far known only from Suriname to northern
Brazil. However, many areas of the Caribbean-Antillean region remain to be sampled for fresh specimens that could
be useful for molecular and morphological analyses in order
to fully elucidate the distributional picture of the species of
Clibanarius.
ACKNOWLEDGEMENTS
This paper is part of a multidisciplinary research project Temático BIOTAFAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo), which
aims to produce a fine-scale assessment of the marine decapod biodiversity of the State of São Paulo. The study was partly supported by
scientific fellowships from the Pró-Reitoria de Pesquisa da Universidade
de São Paulo (Proc. 2009.1.1233.59.5) and from the Conselho Nacional
de Desenvolvimento Científico e Técnológico-CNPq (Proc. 123990/20106, 160133/2011-4) to MN. Additional support for this project was provided by the ongoing PhD fellowship awarded by FAPESP to MN
(Proc. 2012/06300-3) and research grants (Temático Biota 2010/50188-8;
Coleções Científicas 2009/54931-0) CNPq (Proc. 301359/2007-5; 473050/
2007-2; 302748/2010-5) to FLM. We are extremely grateful to the Department of Biology and Postgraduate Program in Comparative Biology of the
FFCLRP/USP for partial financial support, and to many colleagues and
friends (A. Almeida, Á. Costa, B. O’Neill, C. Magalhães, D. Castiglioni,
D. L. Felder, D. Peiró, C. Schubart, E. Mossolin, E. Barba, F. Abrunhosa, F.
Alvarez, J. Marcos de Góes, J. Cuesta, J. L. Vilallobos, L. Pileggi, L. Góes,
M. Tavares, M. H. Goldman, M. Terossi, R. Robles and R. Turner), for their
help in collections, making available some essential fresh specimens, lending material from collections used in our research, critical discussion during
the preparation of this manuscript, and help in sequencing. Special thanks
to D. L. Felder for sharing with us his extensive photographic color files
and allowing use of specimen vouchers in ULLZ; A. Asakura for critical
NEGRI ET AL.: RESURRECTION OF CLIBANARIUS SYMMETRICUS
revisions and advice; P. Callomon and R. Bauer for making possible the examination by us of C. symmetricus syntypes; M. Terossi for the photographs
of the types of C. cayennensis and C. speciosus, and all members of LBSC
for their assistance during the development of this study. The collections of
species conducted in this study complied with current applicable state and
federal laws of Brazil (DIFAP/IBAMA/126/05; permanent license to FLM.
for collection of Zoological Material No. 11777-1 MMA/IBAMA/SISBIO).
R EFERENCES
Abele, L. G., and W. Kim. 1986. An Illustrated Guide to the Marine
Decapod Crustaceans of Florida. Vol. 8. Florida State University,
Department of Environmental Regulation, Technical Series, Tallahassee,
FL, 760 pp.
Ahyong, S. T., and T. V. Chan. 2010. Lithodes formosae, a new species
of king crab from Taiwan (Crustacea: Decapoda: Lithodidae). Zootaxa
2332: 61-68.
Alcock, A. 1905. Catalogue of the Indian Decapod Crustacea in the
Collections of the Indian Museum. Part II. Anomura. Fasciculus I.
Pagurides: i-xi, 1-197. Trustees of the Indian Museum, Calcutta.
Almeida, A. O., P. A. Coelho, J. T. A. Santos, and N. R. Ferraz. 2006.
Crustáceos decápodos estuarinos de Ilhéus, Bahia, Brasil. Biota Neotropica 6(2), available online at http://www.biotaneotropica.org.br/v6n2/
pt/abstract?inventory+bn03406022006.
Batista-Leite, L. M. A., P. A. Coelho, and T. C. S. Calado. 2003.
Caranguejos-ermitões (Crustacea, Decapoda, Paguroidea) do Parque
Municipal Marinho de Paripueira, Alagoas, Brasil. Boletim TécnicoCientífico CENEPE 11(1): 223-232.
Bauer, R. T. 1981. Color patterns of the shrimps Heptacarpus pictus and H.
paludicola (Caridea: Hippolytidae). Marine Biology 64: 141-152.
Bosc, L. A. G. 1802. Histoire Naturelle des Crustacés, contenant leur
description et leurs meours: avec figures dessinées d’après nature. Vol. 2.
De Guilleminet, Paris, 226 pp.
Buitendijk, A. M. 1937. Biological results of the Snellius expedition. IV.
The Paguridea of the Snellius Expedition. Temminckia 2: 251-280.
Coelho, P. A., and M. A. Ramos. 1972. A constituição e a distribuição da
fauna de decápodos do litoral leste da América do Sul, entre as latitudes
de 5°N e 39°S. Trabalhos do Instituto Oceanográfico da Universidade
Federal de Pernambuco 13: 133-236.
, and M. Ramos-Porto. 1986. Sinopse dos crustáceos decápodos
brasileiros (famílias Callianassidae, Callianideidae, Upogebiidae, Parapaguridae, Paguridae, Diogenidae). Trabalhos do Instituto Oceanográfico
da Universidade Federal de Pernambuco 14: 27-53 (dated 1985/86, published 1986).
, A. O. Almeida, L. E. A. Bezerra, and J. F. Souza-Filho. 2007.
An updated checklist of decapods crustaceans (Infraorders Astacidea,
Thalassinidea, Polychelida, Palinura, and Anomura) from the northern
and northeastern Brazilian coast. Zootaxa 1519: 1-16.
Coelho-Santos, M. A., and P. A. Coelho. 1995. Diogenidae e Paguridae
(Crustacea: Decapoda: Anomura) do litoral de Jaboatão dos Guararapes, Pernambuco, Brasil. Trabalhos do Instituto Oceanográfico da Universidade Federal de Pernambuco 23: 163-176 (dated 1994/95, published
1995).
Coffin, H. G. 1957. A new southern form of “Pagurus hirsutiusculus”
(Dana) (Crustacea, Decapoda). Walla Walla College Publications of the
Department of Biological Sciences and the Biological Station 21: 1-8.
Dana, J. D. 1851. Conspectus crustaceorum quae in orbis terrarum circumnavi gatione, Carolo Wilkes e classe reipublicae foederatae duce, lexit et
descripsit. (Preprint from) Proceedings of the Academy of Natural Sciences, Philadelphia 5: 267-272.
. 1852. Crustacea. Part I. United States Exploring Expedition.
During the Years 1838, 1839, 1840, 1841, 1842. Under the Command of
Charles Wilkes, U. S. N. Vol. 13: i-viii, 1-685. C. Sherman, Philadelphia
(reprinted Antiquariaat Junk, Lochem, 1972).
De Haan, W. 1833-1850. Crustacea. In, P. F. von Siebold (ed.), Fauna
Japonica sive Descriptio Animalium, quae in Itinere per Japoniam,
Jussu et Auspiciis Superiorum, qui Summum in India Batava Imperium
Tenent, Suscepto, Annis 1823-1830 Collegit, Notis, Observationibus et
Adumbrationibus Illustra vit. Lugduni-Batavorum, Leiden, 243 pp.
De Man, J. G. 1888. Report on the Podophthalmous Crustacea of the Mergui
Archipelago, collected for the Trustees of the Indian Museum, Calcutta,
by Dr. John Anderson, F.R.S., Superintendent of the Museum, parts IV
and V. Journal of the Linnean Society, London 22: 177-240, 241-305.
859
de Saussure, H. 1858. Mémoire sur divers Crustacés nouveaux de Mexique
et des Antilles. Mémoires, Société Physique et d’Histoire Naturelle de
Genéve 14(2): 417-496.
Fabricius, J. C. 1775. Systema Entomologiae, sistens insectorum classes,
ordines, genera, species, adiectis synonymis, locis, descriptionibus,
observationibus. Officina Libraria Kortii, Flensburgi, 832 pp.
Felder, D. L., D. K. Camp, and J. W. Tunnell Jr. 2009. An introduction to
Gulf of Mexico biodiversity assessment, pp. 1-13. In, D. L. Felder and
D. K. Camp (eds.), Gulf of Mexico Origin, Waters, and Biota. Vol. 1,
Biodiversity. Texas A&M University Press, College Station, 1393 pp.
Folmer, O., M. Black, W. Hoeh, R. Lutz, and R. Vrijenhoek. 1994.
DNA primers for amplification of mitochondrial cytochrome c oxidase
subunit I from diverse metazoan invertebrates. Molecular Marine Biology
and Biotechnology 3(5): 294-299.
Forest, J. 1953. Crustacés Décapodes Marcheurs des îles de Tahiti et
des Tuamotu.–I. Paguridea. Bulletin du Muséum National d’Histoire
Naturelle (2) 25(5): 441-450.
. 1989. Sur le genre Bathynarius gen. nov. (Decapoda, Diogenidae).
Bulletin du Muséum National d’Histoire Naturelle, Section A, Zoologie,
Biologie et Ecologie Animales, Paris [1988] (4) 10A(4): 759-784.
, and M. de Saint Laurent. 1968. Compagne de la ‘Calypso’ au large
des côtes atlantiques de l’Amérique du Sud (1961-1962). 6. Crustacés
Décapodes: Pagurides. Annales de l’Institut Océanographique 45(2): 47169 [1967].
García-Merchán, V. H., A. Robainas-Barcia, P. Abelló, E. Macpherson,
F. Palero, M. García-Rodríguez, L. Gil de Sola, and M. Pascual.
2012. Phylogeographic patterns of decapod crustaceans at the AtlanticMediterranean transition. Molecular Phylogenetics and Evolution 62:
664-672.
Gherardi, F., and M. Vannini. 1993. Hermit crabs in a mangrove swamp:
proximate and ultimate factors in Clibanarius laevimanus clustering.
Journal of Experimental Marine Biology and Ecology 168: 167-187.
Gibbes, L. R. 1850. On the carcinological collections of the United States,
and an enumeration of species contained in them, with notes on the
most remarkable, and descriptions of new species. Proceedings of the
American Association for the Advancement of Science 3: 167-201.
Gómez Hernández, O., and C. Pérez P. 1984. Lista de pagúridos cubanos
(Crustacea, Decapoda, Anomura). Revista de Investigaciones Marinas 5:
23-34.
, and J. C. Martínez-Iglesias. 1986. Nueva lista de pagúridos
cubanos (Crustacea, Decapoda, Anomura, Paguroidea). Revista de Investigaciones Marinas 7(2): 21-29.
Grant, W. S., and W. Cheng. 2012. Incorporating deep and shallow
components of genetic structure into the management of Alaskan red
king crab. Evolutionary Applications 5: 820-837.
Hall, T. A. 2005. BioEdit 7.0.5. North Carolina State University, Department of Microbiology. Available online at http://www.mbio.ncsu.edu/
BioEdit/bioedit.html (accessed 3 January 2011).
Harvey, A. W. 1996. Delayed metamorphosis in Florida hermit crabs:
multiple cues and constraints (Crustacea: Decapoda: Paguridae and
Diogenidae). Marine Ecology Progress Series 141: 27-36.
Hazlett, B. A. 1966. Social behavior of the Paguridae and Diogenidae of
Curaçao. Studies on the Fauna of Curaçao and Other Caribbean Islands
23: 1-143.
. 1981. The behavioral ecology of hermit crabs. Annual Review of
Ecology and Systematics 12: 1-22.
Heller, C. 1861. Beiträge zur Crustaceen-Fauna des rothern Meers, II. Teil.
Sitzungs-Berichte der Mathematisch-Physikisch Klasse der Kaiserlichen
Akademie der Wissenschafte, Wien 44: 241-295.
Herbst, J. F. W. 1791-1796. Versuch einer Naturgeschichte der Krabben
und Krebse nebst einer systematischen Beschreibung ihrer verschiedenen
Arten. Vol. 2: i-viii, 1-226. Stralsund, Berlin.
Hernández Aguilera, J. L., R. E. Toral Almazán, and J. A. Ruiz Nuño. 1996.
Espécies catalogadas de crustáceos estomatópodos y decápodos para el
Golfo de Mexico, Rio Bravo, Tamps. a Progreso, Yuc. Dirección General
de Oceanografía Naval, Secretaría de Marina y Comisión Nacional para
el Conocimiento y Uso de la Biodiversidad, Mexico, 132 pp.
Hess, G. S., and R. T. Bauer. 2002. Spermatophore transfer in the hermit
crab Clibanarius vittatus (Crustacea, Anomura, Diogenidae). Journal of
Morphology 253: 166-175.
Hilgendorf, F. 1879. Die von Hrn. W. Peters in Moçambique gesammelten
Crustaceen. Monatsbericht der Königlich Preussichen Akademie der Wis
senschaften zu Berlin 1878(1879): 782-851.
860
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 6, 2014
Hirose, M., M. Osawa, and E. Hirose. 2010. DNA barcoding of hermit crabs
of genus Clibanarius Dana, 1852 (Anomura: Diogenidae) in the Ryukyu
Islands, southwestern Japan. Zootaxa 2414: 59-66.
Holthuis, L. B. 1959. The crustacean Decapoda of Suriname (Dutch
Guiana). Zoologische Verhandelingen 44(1): 1-296.
Ives, J. E. 1891. Crustacea from the northern coast of Yucatan, the harbor
of Vera Cruz, the west coast of Florida and the Bermuda Islands.
Proceedings of the Academy of Natural Sciences of Philadelphia 43: 167207.
Kelly, R. P., and S. R. Palumbi. 2010. Genetic structure among 50 species
of the northeastern Pacific rocky intertidal community. PLoS ONE 5(1):
e8594.
Kelly, C. J., and R. L. Turner. 2011. Distribution of the hermit crabs Clibanarius vittatus and Pagurus maclaughlinae in the Northern Indian River
Lagoon, Florida: a reassessment after 30 years. Journal of Crustacean
Biology 31: 296-303.
Knowlton, N. 2000. Molecular genetic analyses of species boundaries in
the sea. Hydrobiologia 420: 73-90.
Krauss, F. 1843. Die Südafrikanischen Crustaceen. Eine Zusammenstellung
aller bekannten Malacostraca. Bemerkungen über deren Lebensweise
und geo graphische Verbreitung, nebst Beschreibung und Abbildung
mehrerer neuen Arten. E. Schweizerbart’sche Verlagsbuchhandlung,
Stuttgart, 68 pp.
Kröyer, H. 1838. Grönlands amphipoder beskrevne af Henrik Kröyer.
Danske Videnskabs Selskabet Naturvidenskabelige og Mathematiske
Afhandlinger 7: 229-326.
Latreille, P. A. 1818. Pagure. Nouveau Dictionnaire d’Histoire Naturelle
24: 358-367.
Lowery, W. A., and W. G. Nelson. 1988. Population ecology of the hermit
crab Clibanarius vittatus (Decapoda: Diogenidae) at Sebastian Inlet,
Florida. Journal of Crustacean Biology 8: 548-556.
Macpherson, E. 1988. Revision of the family Lithodidae Samouelle, 1819
(Crustacea, Decapoda, Anomura) in the Atlantic Ocean. Monografías de
Zoología Marina 2: 9-153.
, and A. Machordom. 2001. Phylogenetic relationships of species
of Raymunida (Decapoda: Galatheidae) based on morphology and
mitochondrial cytochrome oxidase sequences, with the recognition of
four new species. Journal of Crustacean Biology 21: 696-714.
, and
. 2004. Rapid radiation and cryptic speciation in
galatheid crabs of the genus Munida and related genera in the South West
Pacific: molecular and morphological evidence. Molecular Phylogenetics
and Evolution 33: 259-279.
, and
. 2005. Use of morphological and molecular data to
identify three new sibling species of the genus Munida Leach, 1820
(Crustacea, Decapoda, Galatheidae) from New Caledonia. Journal of
Natural History 39: 819-834.
Mantelatto, F. L., and J. M. Martinelli. 2001. Relative growth and sexual
dimorphism of the South Atlantic hermit crab Loxopagurus loxochelis
(Anomura, Diogenidae) from Ubatuba, Brazil. Journal of Natural History
35(3): 429-437.
, L. C. Fernandes-Góes, M. Z. Fantucci, R. Biagi, L. M. Pardo,
and J. M. De Góes. 2010. A comparative study of population traits
between two South American populations of the striped-legged hermit
crab Clibanarius vittatus. Acta Oecologica 36: 10-15.
, L. M. Pardo, L. G. Pileggi, and D. L. Felder. 2009. Taxonomic
re-examination of the hermit crab species Pagurus forceps and Pagurus
comptus (Decapoda: Paguridae) by molecular analysis. Zootaxa 2133:
20-32.
, R. Robles, and D. L. Felder. 2007. Molecular phylogeny of the
western Atlantic species of the genus Portunus (Crustacea: Brachyura,
Portunidae). Zoological Journal of the Linnean Society 150: 211-220.
,
, R. Biagi, and D. L. Felder. 2006. Taxonomic and
distributional status based on molecular data for hermit crab genera
Loxopagurus Forest, 1964, and Isocheles Stimpson, 1858 (Decapoda,
Anomura, Diogenidae). Zoosystema 28: 495-506.
Markham, J. C., F. E. Donath-Hernández, J. L. Villalobos-Hiriart, and A. C.
Diaz-Barriga. 1990. Notes on the shallow-water marine Crustacea of
the Caribbean coast of Quintana Roo, Mexico. Anales del Instituto de
Biología, Universidad Nacional Autónoma de México 61: 405-446.
Martínez Campos, B., N. H. Campos, and A. Bermúdez Tobón. 2012.
Distribución de cangrejos ermitaños (Anomura: Paguroidea) en el mar
Caribe colombiano. Revista de Biología Tropical 60: 233-252.
Matzen da Silva, J., S. Creer, A. dos Santos, A. C. Costa, M. R. Cunha, F. O.
Costa, and G. R. Carvalho. 2011. Systematic and evolutionary insights
derived from mtDNA COI barcode diversity in the Decapoda (Crustacea:
Malacostraca). PLoS ONE 6(5): e19449.
McLaughlin, P. A., T. Komai, R. Lemaitre, and D. L. Rahayu. 2010.
Annotated checklist of anomuran decapod crustaceans of the world
(exclusive of the Kiwaoidea and families Chirostylidae and Galatheidae
of the Galatheoidea). Part I – Lithodoidea, Lomisoidea and Paguroidea.
The Raffles Bulletin of Zoology 23(suppl.): 5-107.
, D. K. Camp, L. G. Eldredge, J. W. Goy, D. L. Felder, H. H. Hobbs,
III, B. Kensley, R. Lemaitre, and J. W. Martin. 2005. Order Decapoda. In,
P. A. McLaughlin, D. K. Camp, M. V. Angel, E. L. Bousfield, P. Brunei,
R. C. Brusca, D. Cadien, A. C. Cohen, K. Conlan, L. G. Eldredge, D. L.
Felder, J. W. Goy, T. Haney, B. Hann, R. W. Heard, E. A. Hendrycks,
H. H. Hobbs III, J. R. Holsinger, B. Kensley, D. R. Laubitz, S. E. LeCroy,
R. Lemaitre, R. F. Maddocks, J. W. Martin, P. Mikkelsen, E. Nelson,
W. A. Newman, R. M. Overstreet, W. J. Poly, W. W. Price, J. W. Reid,
A. Robertson, D. C. Rogers, A. Ross, M. Schotte, F. R. Schram, C.-T.
Shih, L. Watling, and G. D. F. Wilson (eds.), Common and Scientific
Names of Aquatic Invertebrates from the United States and Canada:
Crustaceans. American Fisheries Society Special Publication 31: i-xiii,
1-545. NOAA, National Ocean Service, Bethesda, MD.
Melo, G. A. S. 1999. Manual de Identificação dos Crustacea Decapoda
do litoral brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea.
Editora Plêiade, São Paulo, 551 pp.
Miers, E. J. 1877. On a collection of Crustacea Decapoda and Isopoda,
chiefly from South America, with descriptions of new genera and species.
Proceedings of the Zoological Society of London 1877: 653-679, pls. 6669.
Miller, M. A., W. Pfeiffer, and T. Scheartz. 2010. Creating the CIPRES
Science Gateway for inference of large phylogenetic trees, pp. 1-8. In,
Proceedings of the Gateway Computing Environments Workshop (GCE),
New Orleans, Louisiana.
Milne Edwards, H. 1848. Note sur quelques nouvelles espèces du genre
Pagure. Annales des Sciences Naturelles Zoologie, Paris (3) 10: 59-64.
Milne-Edwards, A., and E.-L. Bouvier. 1893. Reports on the results of
dredging, under the supervision of Alexander Agassiz, in the Gulf
of Mexico (1877-78), in the Caribbean Sea (1878-79), and along
the Atlantic coast of the United States (1880), by the U.S. Coast
Survey Steamer “Blake”, Lieut.-Commander C. D. Sigsbee, U.S.N., and
Commander J. R. Bartlett, U.S.N., commanding. XXXIII. Description
des Crustacés de la famille des paguriens recueillis pendant l’expédition.
Memoirs of the Museum of Comparative Zoology at Harvard College
14(3): 5-172.
Moreira, C. 1901. Contribuições para o conhecimento da fauna brasileira.
Crustáceos do Brazil. Arquivos do Museu Nacional do Rio de Janeiro 11:
1-151.
Negri, M., L. G. Pileggi, and F. L. Mantelatto. 2012. Molecular barcode
and morphological analyses reveal the taxonomic and biogeographical
status of the striped-legged hermit crab species Clibanarius sclopetarius
(Herbst, 1796) and Clibanarius vittatus (Bosc, 1802) (Decapoda: Diogenidae). Invertebrate Systematics 26: 561-571.
Nucci, P. R. 2002. Taxonomia e biogeografia da Superfamília Paguroidea
Latreille (Crustacea, Decapoda, Anomura) no litoral brasileiro. Ph.D.
Thesis, UNESP, Rio Claro (unpublished), 194 pp.
Ortmann, A. E. 1892. Die Decapoden-Krebse des Strass-burger Museum,
mit besonderer Berücksichtigung der von Herrn Dr. Döderlein bei den
Liu-Kiu-Inseln gesammelten und zur Zeit im Strassburger Museum
aufbewahrten Formen. IV. Die Abtheilungen Galatheidea und Paguridea.
Zoologische Jahrbücher 6: 241-326.
Pileggi, L. G., and F. L. Mantelatto. 2010. Molecular phylogeny of the
freshwater prawn genus Macrobrachium (Decapoda, Palaemonidae),
with emphasis on the relationships among selected American species.
Invertebrate Systematics 24: 194-208.
Provenzano, A. J. 1959. The shallow water hermit crabs of Florida. Bulletin
of Marine Science of the Gulf and Caribbean 9: 349-420.
Rahayu, D. L., and J. Forest. 1993. Le genre Clibanarius (Crustacea,
Decapoda, Diogenidae) en Indonésie, avec la description de six espèces
nouvelles. Bulletin du Muséum National d’Histoire Naturelle, Section
A, Zoologie, Biologie et Ecologie Animales, Paris [1992] (4) 14(A)(2):
745-779.
Randall, J. W. 1840. Catalogue of the Crustacea brought by Thomas Nuttall
and J. K. Townsend from the West Coast of North America and the
Sandwich Islands, with descriptions of such species as are apparently
new, among which are included several species of different localities,
NEGRI ET AL.: RESURRECTION OF CLIBANARIUS SYMMETRICUS
previously existing in the Collection of the Academy. Journal of the
Academy of Natural Sciences of Philadelphia 8: 106-147, pls. 3-7.
Rathbun, M. J. 1900. Results of the Branner-Agassiz Expedition to Brazil. I.
The decapod and stomatopod Crustacea. Proceedings of the Washington
Academy of Sciences 2(6): 133-156.
Raz-Guzman, A., A. J. Sánchez, P. Peralta, and R. Florido. 2004. Zoogeography of hermit crabs (Decapoda: Diogenidae, Paguridae) from four
coastal lagoons in the Gulf of Mexico. Journal of Crustacean Biology
24(4): 625-636.
Reuschel, S., and C. D. Schubart. 2007. Contrasting genetic diversity with
phenotypic diversity in coloration and size in Xantho poressa (Brachyura:
Xanthidae), with new results on its ecology. Marine Ecology 28: 296305.
Rieger, P. J. 1997. Os “ermitões” (Crustacea. Decapoda, Parapaguridae,
Diogenidae, e Paguridae) do litoral do Brasil. Nauplius 5: 157-159.
Rodríguez, G. 1980. Los crustáceos decápodos de Venezuela. Instituto
Venezolano de Investigaciones Científicas, Caracas, 494 pp.
Rodríguez-Almaraz, G. A., and J. C. Zavala-Flores. 2005. 9. Cangrejos ermitaños, pp. 263-350. In, J. L. Hernández Aguilera, J. A. Ruiz Nuño,
R. E. Toral Alamazán, and V. Arenas Fuentes (eds.), Camarones, langostas y cangrejos de la costa Este de México, 1. Estudio y Conservación
de la Naturaleza, A.C. y Comisión Nacional para el Conocimiento y Uso
de la Biodiversidad, Mexico.
Ruppert, E. E., and R. S. Fox. 1988. Seashore Animals of the Southeast:
A Guide to Common Shallow-Water Invertebrates of the Southeastern
Atlantic Coast. University of South Carolina Press, Columbia, SC,
429 pp.
Sakai, T. 1971. Illustrations of 15 species of crabs of the family Lithodidae,
two of which are new to science. Researches on Crustacea 4-5: 1-49.
Sánchez, H., and N. H. Campos. 1978. Los Cangrejos ermitaños (Crustacea,
Anomura, Paguridae) de la costa norte colombiana. Parte I. Anales del
Instituto de Investigaciones Marinas de Punta de Betín 10: 15-62.
Sant’Anna, B. S., A. L. D. Reigada, and M. A. A. Pinheiro. 2009.
Population biology and reproduction of the hermit crab Clibanarius
vittatus (Decapoda: Anomura) in an estuarine region of southern Brazil.
Journal of the Marine Biological Association of the United Kingdom 89:
761-767.
, C. M. Zangrande, A. L. D. Reigada, and M. A. A. Pinheiro.
2006. Shell utilization pattern of the hermit crab Clibanarius vittatus
(Crustacea, Anomura) in an estuary at São Vicente, State of São Paulo,
Brazil. Iheringia, Série Zoologia 96: 261-266.
Say, T. 1817-1818. An account of the Crustacea of the United States.
Journal of the Academy of Natural Sciences of Philadelphia 1: 57-80,
97-101, 155-169 (1817); 235-253, 313-319, 374-401, 423-441, 445-458
(1818).
Schmitt, W. L. 1935. Scientific survey of Porto Rico and the Virgin Islands.
New York Academy of Sciences 15(2): 125-227.
. 1936. Zoologische Ergebnisse einer Reise nach Bonaire, Curaçao
und Aruba im Jahre 1930. 16. Macruran and anomuran Crustacea from
Bonaire, Curaçao and Aruba. Zoologischer Jahrbücher, Abtheilung für
Systematik, Geographie und Biologie der Thiere 67: 363-378.
Schram, F. R., and S. Koenemann. 2004. Developmental genetics and
arthropod evolution: on body regions of Crustacea, pp. 75-92. In,
G. Scholtz (ed.), Evolutionary Developmental Biology of Crustacea.
Crustacean Issues 15. Balkema, Lisse.
Schubart, C. D., J. E. Conde, C. Carmona-Suárez, R. Robles, and D. L.
Felder. 2001. Lack of divergence between 16S mtDNA sequences
of the swimming crabs Callinectes bocourti and C. maracaiboensis
(Brachyura: Portunidae) from Venezuela. Fishery Bulletin 99: 475-481.
, J. E. Neigel, and D. L. Felder. 2000. Use of the mitochondrial
16S rDNA gene for phylogenetic and population studies of Crustacea.
Crustacean Issues 12: 817-830.
, and M. G. J. Hubert. 2006. Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea:
Astacidae). Bulletin Français de la Pêche et de la Pisciculture 380-381:
1019-1028.
Smith, S. I. 1869. Notice of the Crustacea collected by Prof. C. F. Hartt
on the coast of Brazil in 1867. Part I. Transactions of the Connecticut
Academy of Arts and Sciences 2: 1-41.
861
Southward, A. J., and E. C. Southward. 1977. Distribution and ecology of
the hermit crab Clibanarius erythropus in the western Channel. Journal
of the Marine Biological Association of the United Kingdom 57: 441452.
Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21): 2688-2690.
, P. Hoover, and J. Rougemont. 2008. A rapid bootstrap algorithm
for the RAxML web servers. Systematic Biology 57: 758-771.
Stimpson, W. 1857. On the Crustacea and Echinodermata of the Pacific
shores of North America. Part I. Crustacea. Boston Society of Natural
History 6(4): 444-452.
. 1859. Notes on North American Crustacea. [Preprint from] Annals
of the Lyceum of Natural History in New York 7 [1862]: 49-93 [preprint
pages 3-47].
Strasser, K. M., and W. W. Price. 1998. An annotated checklist and key
to hermit crabs of Tampa Bay, Florida, and surrounding waters. Gulf
Research Reports 11: 33-50.
Tam, Y. K., and I. Kornfield. 1998. Phylogenetic relationships of clawed
lobster genera (Decapoda: Nephropidae) based on mitochondrial 16S
rRNA gene sequences. Journal of Crustacean Biology 18(1): 138-146.
,
, and P. Ojeda. 1996. Divergence and zoogeography of
mole crabs, Emerita spp. (Decapoda: Hippidae), in the Americas. Marine
Biology 125(3): 489-497.
Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. Clustal W,
improving position the sensitivity of progressive multiple sequence
alignment through sequence weighting, position specific, gap penalties
and weight matrix choice. Nucleic Acid Research 22: 4673-4680.
Tilesius, W. C. 1815. De Cancris Camtschaticis, Oniscis, Entomostracis
et Cancellis marinis microscopicis noctilucentibus, Cum tabulis IV:
Aenaeis et appendice adnexo de Acaris et Ricinis Camtschaticis. Auctore
Tilesio. Conventui exhibuit die Februarii 1813. Mémoires de l’Académie
Impériale de Sciences de St. Petersbourg 5: 331-405.
Turra, A., and F. P. P. Leite. 2001. Fecundity of three sympatric populations
of hermit crabs (Decapoda, Anomura, Diogenidae). Crustaceana 74:
1019-1027.
, and
. 2004. Shell-size selection by intertidal sympatric
hermit crabs. Marine Biology 145: 251-257.
, and
. 2007. Embryonic development and duration of incubation period of tropical intertidal hermit crabs (Decapoda, Anomura).
Revista Brasileira de Zoologia 24: 677-686.
Vergamini, F. G., L. G. Pileggi, and F. L. Mantelatto. 2011. Genetic
variability of the Amazon River prawn Macrobrachium amazonicum
(Decapoda, Caridea, Palaemonidae). Contributions to Zoology 80: 6783.
Voss, G. L. 1976. Seashore Life of Florida and the Caribbean. E. A.
Seemann Publishing, Inc., Miami, Florida, 168 pp. (2nd (1980) and 3rd
(2002) editions, Dover, Mineola, NY).
Williams, A. B. 1965. Marine decapod crustaceans of the Carolinas. Fishery
Bulletin of the Fish and Wildlife Service 65(1): 1-298.
. 1984. Shrimps, Lobsters and Crabs of the Atlantic Coast of the
Eastern United States, Maine to Florida. Smithsonian Institution Press,
Washington, DC, 550 pp.
, L. G. Abele, D. L. Felder, H. H. Hobbs, Jr., R. B. Manning, P. A.
McLaughlin, and I. Pérez-Farfante. 1989. Common and scientific names
of aquatic invertebrates from the United States and Canada: decapod
crustaceans. American Fisheries Society Special Publication 17: i-vii, 177, pls. 1-4.
Wilson, R. P. 1987. Substrate selection and decorating behavior in Acanthonyx petiveri related to exoskeleton color (Brachyura, Majidae). Crustaceana 52: 135-140.
Young, A. M., C. Torres, J. E. Mack, and C. W. Cunningham. 2002.
Morphological and genetic evidence for vicariance and refugium in
Atlantic and Gulf of Mexico populations of the hermit crab Pagurus
longicarpus. Marine Biology 140: 1059-1066.
R ECEIVED: 9 July 2014.
ACCEPTED: 3 September 2014.
AVAILABLE ONLINE: 30 September 2014.