Evidence using morphology, molecules, and biogeography clarifies the taxonomic status of mole crabs of the genus Emerita Scopoli, 1777 (Anomura, Hippidae) and reveals a new species from the western Atlantic

Fernando L. Mantelatto; Juliana M. Paixão; Rafael Robles; Jeniffer N. Teles; Felipe C. Balbino

doi:10.3897/zookeys.1161.99432

Abstract

Uncertainties regarding the taxonomic status and biogeographical distribution of some species of the genus Emerita from the western Atlantic led to thorough examination of the subtle morphological differences between two coexistent species (E. brasiliensis Schmitt, 1935 and E. portoricensis Schmitt, 1935) along the Brazilian coast and compare them using two genetic markers. The molecular phylogenetic analysis based on sequences of the 16S rRNA and COI genes showed that individuals identified as E. portoricensis were clustered into two clades: one containing representatives from the Brazilian coast and another containing specimens distributed in Central America. Our molecular-based phylogeny, combined with a detailed morphological analysis, revealed the Brazilian population as a new species, which is described here as Emerita almeidai Mantelatto & Balbino, sp. nov. The number of species in the genus Emerita is now raised to 12, with five of them occurring in the western Atlantic, five in the Indo-Pacific, and two in the eastern Pacific.

Keywords

16S rRNA, COI, Cryptic diversity, distribution, molecular data, phylogeny

Introduction

The superfamily Hippoidea Latreille, 1825 is one of the seven superfamilies that belong to the highly diverse infraorder Anomura Macleay, 1838 (Boyko and McLaughlin 2010). It is represented by three families of sand/mole crabs: Albuneidae Stimpson, 1858 (nine genera and 53 recognized species), Blepharipodidae Boyko, 2002 (two genera and six species) and Hippidae Latreille, 1825 (three genera and 28 species) (Boyko 2002; WoRMS 2023). Representatives of all these families are well known due to their presence in intertidal sandy beaches of temperate, tropical, and subtropical areas. Their ability to bury themselves in this environment of constant hydrodynamics is one of the most outstanding characteristics of this group.

The genus Emerita Scopoli, 1777 (family Hippidae) contains eleven species that are widely distributed around the globe, living in intertidal and upper subtidal sandy marine regions. Their filter feeding habit is an ecologically essential activity in sandy beach environments (Rodgers 1987; Lercari and Defeo 1999; Hubbard and Dugan 2003). These sand crabs are also considered as bioindicators of environment quality (Pérez 2003; Petracco et al. 2003). Five species are reported in the Indo-Pacific [Emerita emeritus (Linnaeus, 1767), E. austroafricana Schmitt, 1937, E. holthuisi Sankolli, 1965, E. karachiensis Niazi & Haque, 1974, and Emerita taiwanensis Hsueh, 2015], two in the eastern Pacific [Emerita analoga (Stimpson, 1857) and Emerita rathbunae Schmitt, 1935], and four in the western Atlantic [Emerita talpoida Say, 1817, E. benedicti Schmitt, 1935, E. brasiliensis Schmitt, 1935, and E. portoricensis Schmitt, 1935].

Most of the studies that established the current taxonomic status of species in Emerita were based on morphology (see Calado 1990 and Melo 1999 for revisions). Molecular data has been used to test for genetic flow between distant populations of conspecifics of E. analoga and E. talpoida from the eastern Pacific and western Atlantic populations, respectively (Tam et al. 1996). Later, a molecular phylogeny, using two genetic markers, rejected the hypothesis that species of Emerita from the New World form a monophyletic group (Haye et al. 2002). Recently, specimens of Emerita from Indonesia were evaluated using DNA barcoding and morphology to identify, but not describe a new species (Bhagawati et al. 2020, 2022). More recently, the inaccurate identity of some specimens and the distribution of E. portoricensis was clarified (Felder et al. 2023).

The two species of Emerita reported from the Brazilian coast are E. brasiliensis and E. portoricensis. The former species can be found in Venezuela, Trinidad and Tobago, Brazil (Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina, Rio Grande do Sul), Uruguay, and Argentina (Efford 1976; Calado 1998; Melo 1999; Veloso and Cardoso 1999; Spivak et al. 2019; Mantelatto et al. 2021), with a gap of records from Venezuela to Bahia (Brazil), the species is abundant from Espírito Santo to southern Brazil (Mantelatto et al. 2021; present work). Emerita portoricensis occurs in Central American mainland shorelines of the Caribbean Sea, confirmed to include, but not limited to Puerto Rico, Dominican Republic, Virgin Islands, Jamaica, Belize, Costa Rica, Panama, Colombia, St. Lucia, St. Thomas, Venezuela, and Trinidad and Tobago (Felder et al. 2023); Brazilian records (from Maranhão to Sergipe) have been treated as E. portoricensis by several authors (Schmitt 1935; Efford 1976; Calado 1990; Melo 1999).

These patterns of geographical distribution and uncertain records in the western Atlantic raise questions about whether these gaps are due to a lack of faunal surveys and/or a misidentification of specimens that are morphologically similar. Thus, we were motivated to perform a reassessment of the specimens assigned as E. portoricensis and E. brasiliensis along the Brazilian coast, using both morphological and molecular tools to evaluate the phylogenetic relationships between species of Emerita. We also examined the possible existence of cryptic taxa, which resulted in the new species described herein.

Materials and methods

Sample collection and morphological data

Almost all specimens of Emerita analyzed herein were obtained by us and are deposited in the Crustacean Collection of the Department of Biology (CCDB) at the Faculty of Philosophy, Sciences and Letters at Ribeirão Preto (FFCLRP), University of São Paulo (USP), Brazil. Additional species of Emerita and other genera of Albuneidae (see Boyko 2002) were obtained and used in order to root the phylogenetic analyses. Individuals were collected by hand during low tide at different sandy beaches along the geographic distribution of the species (see references in Introduction). We also studied specimens obtained by means of loans or donations from University of Louisiana at Lafayette Zoological Collection, LA, United States (ULLZ – recently transferred to the National Museum of Natural History, Smithsonian Institution, Washington, D.C. USNM; old catalog numbers are used in the text).

Specimens were identified according to previous morphological characters established in the literature (Calado 1990; Melo 1999; Felder et al. 2023). All data along with new characters/variation were also considered for the comparative analysis along the species’ geographic distribution. When secondary sexual characters (presence of the gonopores on the coxae of the fifth pair of pereopods and absence of mature pleopods for males – ♂s, and the presence of the gonopores on the coxae of the third pair of pereopods and presence of mature pleopods or eggs for females – ♀s) were not conspicuously observed, specimens were classified as juveniles (Delgado and Defeo 2006). Most of the morphological characters followed the references cited above and are designated in Fig. 1. Analyses were made and photographs were taken under a LEICA M205C stereomicroscope equipped with a LEICA DFC 295 camera, and measurements (mm) of structures were taken using the software Leica Application Suite.

Figure 1.

A dorsal view of adult ♀ of Emerita almeidai sp. nov. (CCDB 3369) B ventral view of adult ♀ of Emerita brasiliensis (CCDB 2552). The main characters used for external morphology analysis are labeled. Scale bar: 5 mm.

Abbreviations

coll(s). collector(s),

cl. carapace length,

cw. carapace width,

dl. dactylus length,

dw. dactylus width,

tl. telson length,

tw. telson width.

Brazilian states

BA Bahia,

CE Ceará,

ES Espírito Santo,

PE Pernambuco,

RJ Rio de Janeiro,

RN Rio Grande do Norte,

SC Santa Catarina,

SP São Paulo.

Molecular data

The molecular markers 16S rRNA and cytochrome c oxidase subunit I (COI) were chosen because these mitochondrial genes are effective in studies that contribute to our comprehension of decapod diversity (see Schubart et al. 2000 and Timm and Bracken-Grissom 2015 for references), including anomuran members (Mantelatto et al. 2006, 2009; Miranda et al. 2020) and the target genus (Bhagawati et al. 2020, 2022). In this study, we used four different primers (see below).

We used muscle tissue from the telson or 3^rd pereopods for DNA extraction according to the protocols proposed by Mantelatto et al. (2007) and Robles et al. (2007), and some adaptations were made to suit our material using the manufacturer’s protocol of the salting-out method (Miller et al. 1988). The extracted DNA’s final concentration was measured using a spectrophotometer (NanoDrop 2000/2000c). Approximately 658 base pairs (bp) of the COI and 316 bp of the 16S rRNA genes were amplified using polymerase chain reactions (PCR) by thermal cycler (Veriti 96 Well Thermal Cycler Applied Biosystems). Fragments were amplified using the following thermal profiles: 16S rRNA – initial denaturing for 2 min at 94 °C; annealing for 40 cycles, 45 s at 94 °C, 45 sec at 46 °C and 1 min at 72 °C; final extension for 10 min at 72 °C; COI – initial denaturing for 2 min at 94 °C; annealing for 35 cycles, 30 sec at 94 °C, 30 sec at 50 °C, and 1 min at 72 °C; final extension for 7 min at 72 °C. We used the following primers: 16S-1472 (5’– AGA TAG AAA CCA ACC TGG – 3’) (Crandall and Fitzpatrick 1996) and 16SL (5’– CGC CTG TTT ATC AAA AAC AT – 3’) (Palumbi and Benzie 1991), HCO1-2198 (5’– TAA ACT TCA GGG TGA CCA AAA AAT CA – 3’) and LCO1-1490 (5’– GGT CAA CAA ATC ATA AAG ATA TTG – 3’) (Folmer et al. 1994). PCR products were observed in electrophoresis with 1.0% agarose gel and photographed with digital camera Olympus C-7070 on a UV transilluminators M20 UVP. Successful PCR products were purified using the SureClean Plus kit, following the manufacturer’s protocol. Purified samples were sent to the Department of Technology at the College of Agricultural and Veterinary Sciences (FCAV, Jaboticabal) at São Paulo State University (UNESP) for sequencing.

A consensus was reached between the forward and reverse sequences of each specimen in BioEdit v. 7.0.5 (Hall 2005), and unspecific readings were manually corrected when required. Primer regions and non-readable parts at the beginning of the sequences were omitted. All consensus sequences were deposited in GenBank (http://www.ncbi.nlm.nih.gov/genbank/).

The alignment of the consensus of all sequences used in the phylogeny was performed with MAFFT (Katoh and Standley 2006) in the software Geneious 2022.1 (Kearse et al. 2012). Three maximum likelihood (ML) phylogenetic analyses were performed using the IQ-TREE program (Miller et al. 2010), one with the COI gene, one with the16S rRNA gene, and one using a concatenated alignment. The evolutionary model that best fit the data was determined by IQ-TREE according to the Bayesian Information Criterion (BIC) (Luo et al. 2010) and used for tree inference. The branch support was evaluated by ultra-fast bootstrap with 2000 pseudoreplicates.

Results

Molecular data

We generated new sequences for 38 individuals from different localities: for 16S rRNA – 1 of Emerita analoga, 10 of Emerita almeidai sp. nov., 1 of Emerita benedicti, 11 of Emerita brasiliensis, 1 of Emerita portoricensis, 3 of Emerita rathbunae, and 3 of Emerita talpoida; for COI – 9 of E. almeidai sp. nov., 1 of E. analoga, 1 of E. benedicti, 15 of Emerita brasiliensis, 2 of E. portoricensis, 2 of E. rathbunae, and 2 of E. talpoida. Additional sequences from GenBank were used to build a robust reconstruction (Table 1).

Table 1.

Download as

CSV

XLSX

Species of Emerita and Lepidopa used in the molecular analyses. CCDB: Coleção de Crustáceos do Departamento de Biologia, FFCLRP, USP, Brazil; ULLZ: University of Louisiana at Lafayette Zoological Collection, USA (recently transferred to National Museum of Natural History, Smithsonian Institution, Washington, D.C. (USNM)); (-) = data not available.

Species	Locality	Catalogue number	GenBank accession number
Species	Locality	Catalogue number	COI	16S
E. analoga	California, USA	–	–	AF246153
	California, USA	–	–	L43107
	California, USA	–	–	L43108
	California, USA	–	–	AF425322
	Oregon, USA	–	GU443297	–
	_	–	HQ341148	–
	_	–	HQ340917	–
	Calfuco, Chile	CCDB 4870	OQ679992	KP091505
	Algaborro, Chile	–	–	AF246154
E. almeidai sp. nov.	Rio Grande Norte, Brazil	CCDB 3369	KP091512	KP091493
	Rio Grande Norte, Brazil	CCDB 3376	KP091509	KP091491
	Rio Grande Norte, Brazil	CCDB 3380	KP091507	KP091489
	Rio Grande Norte, Brazil	CCDB 3393	KP091514	KP091496
	Pernambuco, Brazil	CCDB 4937	KP091515	KP091498
	Alagoas, Brazil	CCDB 4869	KP091516	KP091497
	Bahia, Brazil	CCDB 2606	–	KP091495
	Bahia, Brazil	CCDB 3026	KP091508	KP091490
	Bahia, Brazil	CCDB 4262	KP091513	KP091494
	Espírito Santo, Brazil	CCDB 3992	KP091510	KP091488
	Rio de Janeiro, Brazil	CCDB 4376	KP091511	KP091492
E. benedicti	Los Tuxtlas, Mexico	CCDB 4674	KP091525	KP091501
	Texas, USA	–	–	AF256155
	Texas, USA	–	–	L43109
E. brasiliensis	Espírito Santo, Brazil	CCDB 3990	KP091533	KP091477
	Espírito Santo, Brazil	CCDB 3994	KP091536	KP091481
	Rio de Janeiro, Brazil	CCDB 4119	KP091537	KP091482
	Rio de Janeiro, Brazil	CCDB 4935	KP091527	–
	São Paulo, Brazil	CCDB 1442	KP091530	KP091475
	São Paulo, Brazil	CCDB 1443	KP091531	–
	São Paulo, Brazil	CCDB 2552	–	KP091478
	São Paulo, Brazil	CCDB 2751	–	KP091483
	São Paulo, Brazil	CCDB 3923	KP091529	–
	São Paulo, Brazil	CCDB 3924	KP091532	KP091476
	São Paulo, Brazil	CCDB 4617	KP091538	KP091484
	Santa Catarina, Brazil	CCDB 4407	KP091534	KP091479
	Santa Catarina, Brazil	CCDB 4409	KP091535	KP091480
	Rio Grande Sul, Brazil	CCDB 4985	KP091526	–
	Rio Grande Sul, Brazil	CCDB 4986	KP091528	–
	Rio Grande Sul, Brazil	CCDB 3921	KP091539	–
	Fortaleza de Santa Teresa, Uruguay	–	–	L43110
	–	–	–	DQ079712
E. emeritus	Pondichvory, India	–	–	AF2461556
E. holthuisi	Dubai, United Arab Emirates	–	–	AF246157
E. portoricensis	Mayaguez, Puerto Rico	–	–	L43111
	Boca del Drago, Panama	CCDB 3525	KP091517	KP091486
	Boca del Drago, Panama	USNM 1546871 (= ULLZ 13325)	KP091519	–
E. rathbunae	–	–	–	JN800539
E. rathbunae	Acapulco, Mexico	CCDB 1029	KP091523	KP091499
E. talpoida	Los Tuxtlas, Mexico	CCDB 4675	KP091521	KP091502
	South Carolina, USA	–	–	AF246150
	Massachusetts, USA	–	–	AF246151
	Massachusetts, USA	–	–	L43112
	Massachusetts, USA	–	–	L43113
	Florida, USA	ULLZ 13055	KP091522	KP091503
	Florida, USA	ULLZ 10144	–	KP091504
	Florida, USA	–	–	L43114
	Florida, USA	–	–	AF246152
Lepidopa richmondi	São Paulo, Brazil	CCDB 3920	KP091540	KP091506

16S rRNA reconstruction

The automated alignment of 16S rRNA with 316 bp included 50 sequences of Emerita species. The phylogenetic tree, generated by ML analyses, indicated a clear separation of each species of Emerita (Fig. 2). Emerita brasiliensis consisted of a single clade, with all specimens assigned to this species, which was supported by bootstrap values of 96%. In this analysis, the closest relative of E. brasiliensis was E. rathbunae, although with low support (31%).

Figure 2.

Maximum likelihood phylogram obtained for 16S rRNA sequences of Emerita specimens. Numbers represent bootstrap values (2000 pseudoreplicates). GenBank code is shown before the species name. Abbreviations: BRZ: Brazil; URG: Uruguay; MXC: Mexico; USA: United States of America; PAN: Panama; PRO: Puerto Rico; UAE: United Arab Emirates; IND: India; CHL: Chile.

All specimens of E. almeidai sp. nov. were clustered in a strongly supported clade (bootstrap values of 91%), which was the sister group of E. portoricensis s.s. from Central America (bootstrap values of 99%). Specimens of Emerita talpoida were split into two groups, one of them containing individuals from Florida (USA) and Mexico and the second one containing individuals from Massachusetts and South Carolina (USA). The positioning of a supposed “E. analoga” (AF425322) in this second group indicated a misidentification that should be fixed in the GenBank database. The phylogram positioned E. benedicti as a sister species of the clade composed by E. almeidai sp. nov., E. portoricensis, and E. talpoida, although with low support (60%). This major group, including E. almeidai sp. nov., E. portoricensis, E. talpoida, and E. benedicti, is the sister group of the clade composed of E. brasiliensis and E. rathbunae.

The clade containing E. holthuisi and E. emeritus, species from the Indo-Pacific, was positioned as a sister group of the major American clade mentioned above.

Emerita analoga, with reservations on the above-mentioned misidentified specimen, formed a single well-defined clade, with individuals from California (USA) and Chile, and was positioned as the sister species of all other species of Emerita used in the reconstruction, including members from the Americas as well as the Old World (E. emeritus and E. holthuisi).

Cytochrome Oxidase I (COI) reconstruction

The automated alignment of COI sequences with 658 bp included some sequences of Emerita species from GenBank. The phylogram also confirmed the clear separation of every species of Emerita (Fig. 3), including the strongly supported position of Emerita almeidai sp. nov. Some differences were observed in the phylogenetic position of some of the species included in this alignment compared to that of the 16S rRNA alignment. For instance, E. rathbunae was recovered as the closest relative of E. talpoida instead of E. brasiliensis. The clade composed of E. talpoida and E. rathbunae was recovered as the sister group of E. brasiliensis. Furthermore, this clade [E. brasiliensis + (E. rathbunae + E. talpoida)] was recovered as the sister group of the clade composed of E. portoricensis and E. almeidai sp. nov. In this analysis, E. benedicti was found to be the sister species of the clade comprising E. brasiliensis, E. talpoida, E. rathbunae, E. portoricensis, and E. almeidai sp. nov.

Figure 3.

Maximum likelihood phylogram obtained for COI (HCO1/LCO1) sequences of Emerita specimens. Numbers represent bootstrap values (2000 pseudoreplicates). GenBank code is shown before the species name. Abbreviations: BRZ: Brazil; MXC: Mexico; USA: United States of America; PAN: Panama; CHL: Chile.

Once again, despite the low number of specimens of E. talpoida, a clear division into two groups was recovered, with a few differences in relation to the 16S rRNA topology (the individual from Mexico was separated from the Florida one). The phylogenetic positioning of E. analoga was maintained as sister to all other species of Emerita included in this analysis.

Concatenated phylogram

The concatenated topology obtained for the 16S rRNA and COI genes (Fig. 4) recovered the main groups that were observed in the two separate analyses carried out for each gene. All specimens of Emerita almeidai sp. nov. were clustered together in a well-supported clade. The only specimen of E. portoricensis included in the analysis was well separated from other species. These two groups were recovered as sister species in a larger clade, as can be observed in the 16S rRNA and COI phylograms. Emerita rathbunae was recovered as the sister species of E. brasiliensis, and E. talpoida was recovered as the sister species of the clade composed by E. rathbunae and E. brasiliensis. The division of E. talpoida in two subclades was not observed because there were only two specimens of this species. However, subtle differences could be inferred by the long branches connecting the two specimens within this clade. Emerita benedicti was recovered as the sister species of all other species of Emerita in the analysis.

Figure 4.

Concatenated tree molecular data set (16S rRNA and HCO1/LCO1) of maximum likelihood for Emerita specimens. Numbers represent bootstrap values (2000 replicates). GenBank code is shown before the species name. Abbreviations: BRZ: Brazil; MXC: Mexico; USA: United States of America; PAN: Panama; CHL: Chile.

Taxonomy

Below we present the list of examined material and the description of the new species. A comparative image shows details about the general morphology of the seven species of Emerita from the Americas (Fig. 5) and a detailed comparison between E. brasiliensis and E. almeidai sp. nov. (Fig. 6) is furnished to complement the information. The updated distribution (Fig. 7) and a comparative analysis of the main characters of these two species and E. portoricensis was presented in Table 2.

Table 2.

Download as

CSV

XLSX

Diagnostic characters (Calado 1990; Melo 1999; Felder et al. 2023; present study) used for comparison between three studied species.

Characters	E. brasiliensis	E. portoricensis	E. almeidai sp. nov.
Antennal flagellum	103–134 articles	76–86 articles	74–104 articles
Ocular peduncle	Not exceeding the spines of the second antennal article	Usually extending beyond the spines of the second antennal article	Usually extending beyond the spines of the second antennal article
Front (rostrum + lateral projections)	Anterior margin with two triangular projections with rounded distal ends that are ca. the same size as the rostrum	Anterior margin with two triangular projections that extend beyond the level of the rostrum	Anterior margin with two triangular projections that extend beyond the level of the rostrum
Dactylus of first pereopod	Wide, oval shaped, inferior margin not serrated	Narrow, visibly longer than wide, inferior margin slightly, irregularly, or inconspicuously serrated	Narrow, visibly longer than wide, inferior margin conspicuously and regularly serrated
Carapace	Proportionally wider than that of E. portoricensis and E. almeidai sp. nov.	Proportionally longer than that of E. brasiliensis and E. almeidai sp. nov.	Proportionally longer than that of E. brasiliensis; proportionally wider than that of E. portoricensis
Carapace rugae	Broken into cusps	Dense and non-broken	Dense and non-broken
Telson	Distal end reaching the proximal region of the coxa of the first pereopod	Tends to be longer than wide in relation to the telson of E. brasiliensis	Tends to be longer than wide in relation to the telson of E. brasiliensis
Coloration	Brownish white or olive brown throughout	Olive brown carapace with wide white lines and markings, a white line marking posterior 1/4 of carapace, most rugae the same color as carapace, pleon with alternating olive brown and white bars	Olive brown carapace with slim white lines and markings, line marking posterior 1/4 of carapace usually absent, rugae white in color contrasting with carapace, pleon with alternating olive brown and white bars

Figure 5.

Dorsal view of carapace and rostrum/front, and lateral view of antenna/first pereopod of adult ♀s of Emerita species from the Americas A Emerita analoga (CCDB 4870) B Emerita benedicti (CCDB 4674) C Emerita brasiliensis (CCDB 4615) D Emerita almeidai sp. nov. (CCDB 3369) E Emerita rathbunae (CCDB 1029) F Emerita talpoida (CCDB 4675) G E. portoricensis (CCDB 3525).

Figure 6.

Comparative morphological characters observed in adult ♀s of similar sizes between Emerita brasiliensis (CCDB 2552) and E. almeidai sp. nov. (CCDB 3026). Carapace shape: Dorsal view of A E. brasiliensis and B E. almeidai sp. nov.; Dactylus of first pereopod: Lateral view of C E. brasiliensis and D E. almeidai sp. nov.; Anterior region with rostrum, lateral spines, and ocular peduncle: Dorsal view of E E. brasiliensis and F E. almeidai sp. nov.; Posterior region/telson: Ventral view of G E. brasiliensis and H E. almeidai sp. nov.; Left ventral view of antenna I E. brasiliensis and J E. almeidai sp. nov.

Figure 7.

The updated geographic distribution of Emerita brasiliensis, E. portoricensis, and E. almeidai sp. nov. according to the literature (Efford 1976; Melo 1999; Veloso and Cardoso 1999; Felder et al. 2023) and the present study.

Superfamily Hippoidea Latreille, 1825

Family Hippidae Latreille, 1825

Emerita Scopoli, 1777

Emerita almeidai Mantelatto & Balbino, sp. nov.

https://zoobank.org/6A094FCB-F019-4853-B561-E427D0963CA8

Figs 1, 5, 6, 8, 9, 10, 11, 12

Emerita portoricensis – Efford, 1976: 178, 179; Calado 1990: 266, 268, 271; Tam et al. 1996: 490; Haye et al. 2002: 904 (non Emerita portoricensis Schmitt, 1935).

Type material

Holotype : ovigerous ♀ (cl. 13.52 mm), CCDB 7233, Praia do Paiva (lower intertidal, quartzite, coarse sand off wave-washed beach), Ilha do Amor, Cabo de Santo Agostinho, PE, Brazil, 08°13'48"S, 34°55'22"W, 27 August 2022, colls. Mantelatto, F.L., Bochini, G.L., Balbino, F.C., Rios, A. Paratypes: 3 ovigerous ♀s (cl. 17.31 mm, 17.93 mm, 15.90 mm), 1 ♀ (cl. 14.67mm) (1 ovigerous ♀ cl. 17.31 mm dissected – left antennule, antennae, mouthparts, maxillipeds, pereopods, uropods and telson), CCDB 5855, Praia de Serrambi, Município de Serrambi, Ipojuca, PE, Brazil, 08°33'39.91"S, 35°00'45.15"W, 20 July 2015, colls. Mantelatto, F.L., Mantelatto, F.B., Biagi, R.; 3 ovigerous ♀s (cl. 15.01 mm, 15.93 mm, 9.94 mm), 4 ♀s (cl. 9.66 mm, 9.64 mm, 9.24 mm, 9.02 mm), 1 juvenile (cl. 4.72 mm), “1 ovigerous ♀ (cl. 15.01 mm dissected – mouthparts, maxillipeds, pereopods, uropods and telson), CCDB 4937, Praia de Boa Viagem, Recife, PE, Brazil, 08°08'12.96"S, 34°54'05.84"W, 28 January 2014, colls. Mantelatto, F.L., Mantelatto, F.B., Biagi, R.; 1 ♀ (cl. 10.49 mm), MOUFPE 20112, Praia do Paiva, Ilha do Amor, Cabo de Santo Agostinho, PE, Brazil, 08°13'48"S, 34°55'22"W, 27 August 2022, colls. Mantelatto, F.L., Bochini, G.L., Balbino, F.C., Rios, A.; 1 ♂ (cl. 7.29 mm), MZUSP 43536, Praia do Forte Orange, Vila Velha, Ilha de Itamaracá, PE, Brazil, 07°50'40"S, 34°50'33"W, 30 August 2022, colls. Mantelatto, F.L., Bochini, G.L., Balbino, F.C., Rios, A., Almeida, A.O.”

Additional material

1 ♀, CCDB 4526, Morro Branco (CE), 25 March 1989; 1 ♀, 1 ovigerous ♀, CCDB 3369, Praia de Perobas, Touros (RN), 10 June 2011, colls. Robles, R., Pileggi, L.G.; 5 ovigerous ♀s, CCDB 3376, Praia de Maracajaú, Maxaranguape (RN), 10 June 2011, colls. Robles, R., Pileggi, L.G.; 2 ♀s, 1 ovigerous ♀, CCDB 3393, Morro do Careca, Ponta Negra, Natal (RN), 06 June 2011, coll. Robles, R.; 1 ♀, 4 ovigerous ♀s, CCDB 3380, Morro do Careca, Ponta Negra, Natal (RN), 07 June 2011, coll. Robles, R.; 2 ♀s, 10 ovigerous ♀s, CCDB 4869, Praia de Maragogi, Maragogi (AL), 05 October 2013, colls. Mantelatto, F.L., Mantelatto F.B.; 2 ♀s, 2 ovigerous ♀s, CCDB 6127, Praia de Imbassaí, Mata de São João (BA), 25 January 2017, colls. Mantelatto, F.L., Mantelatto, F.B.; 1 ovigerous ♀, CCDB 2606, Praia do Pé da Serra, Uruçuca (BA), 31 March 2009, colls. Mantelatto, F.L., Almeida, A.O.; 1 ovigerous ♀, CCDB 2605, Praia do Sul, Km 01, Hotel Praia do Sol, Ilhéus (BA), 30 March 2009, colls. Mantelatto, F.L., Almeida, A.O.; 2 ovigerous ♀s, CCDB 3026, Praia do Sul, Km 01, Hotel Praia do Sol, Ilhéus (BA), 10 November 2010, colls. Mantelatto, F.L., Peiró, D.F.; 1 ♀, 1 ♂, CCDB 4262, Praia da Lagoa Pequena, Prado (BA), 12 August 2012, colls. Carvalho, F.L., Souza-Carvalho, E.A.; 1 ♂, 3 ♀s, 1 ovigerous ♀, CCDB 3992, Praia de Iriri, Iriri (ES), 19 June 2012, colls. Carvalho, F.L., Robles, R., Peiró, D.F.; 2 ovigerous ♀s, CCDB 4376, Pedra do Sal (RJ), 19 November 2009, coll. Arresda, E.

Comparative material

Emerita analoga: 4 ovigerous ♀s, CCDB 4870, Calfuco, XIV Región, Chile, 20 August 2013, coll. Fuentes, J.P.; Emerita benedicti: 5 ♀s, 4 juveniles, CCDB 4674, Playa Escondida, Los Tuxtlas, México, 07 February 2013, coll. Robles, R.; Emerita brasiliensis: 7 ♀s, 6 ♂s, CCDB 3990, Laguna Marginal, Guarapari (ES), Brazil, 18 June 2012, colls. Carvalho, F.L., Robles, R., Peiró, D.; 7 ♂s, 12 ♀s, 1 ovigerous ♀, 5 juveniles, CCDB 7226, Praia de Iriri, Anchieta (ES), Brazil, 19 June 2012, colls. Carvalho, F.L., Peiró, D., Robles, R.; 3 ♀s, CCDB 1030, Ubatuba (SP), Brazil, 20 November 2002, colls. Mantelatto, F.L., Scelzo, M.A.; 1 ♀, 1 ovigerous ♀, CCDB 2552, Praia Juquehy, São Sebastião (SP), Brazil, 26 December 2008, colls. Mantelatto, F.L., Mantelatto, F.B., Biagi, R.; 1 ♀, CCDB 7301, Praia de Guaratuba, Bertioga (SP), Brazil, 07 January 2023, colls. Mantelatto, F.L., Mantelatto, F.B., Mantelatto, H.B.; 2 ♂s, 6 ♀s, 2 ovigerous ♀s, CCDB 3924, Praia Guaiuba, Guarujá (SP), 22 October 2011, colls. Rossi, N.; Leone, I., Carvalho, F.L., Costa, A.; 5 ♀s, CCDB 1443, Praia Itararé, São Vicente (SP), Brazil, 23 October 2011, colls. Rossi, N., Leone, I., Carvalho, F.L., Costa, A.; 3 ♂s, 1 ♀, 7 ovigerous ♀s, CCDB 4409, Praia de Balneário Camboriú, Camboriú (SC), Brazil, 04 December 2012, colls. Carvalho, F.L., Souza-Carvalho, E.A.; Emerita portoricensis: ovigerous ♀ (holotype, USNM 65731, photos), Mayaguez, Puerto Rico, 19–20 January 1899; 3 ♀s, CCDB 3525, Playa Boca Del Drago, Bocas Del Toro, Panamá, 06 August 2011, colls. Mantelatto, F.L., Negri, M.P., Rossi, N., Magalhães, T.; Emerita rathbunae: 3 ♀s, CCDB 1029, Playa Del Revolcadero, Granjas Del Marquez, Acapulco, México, 06 May 2012, coll. Mantelatto, F.L.; Emerita talpoida: 9 ♀s, CCDB 4675, Playa Escondida, Los Tuxtlas, México, 07 February 2013, coll. Robles, R.

Diagnosis

Carapace dorsally convex, 1.42–1.54× longer than wide, surface densely covered by microcrenulate rugae; most rugae elongate and continuous across carapace median line not forming rows or lines; 17 or more rugae crossing median line, rugae obsolete laterally on epimeral lobes. Front with three distinct subacute lobes consisting of rostrum and two lateral projections, rostrum visibly shorter than lateral projections. Antennular flagellum dorsal ramus with 30 articles. Antennal peduncle second article large, with three distal spines, median spine the longest, antennal flagellum with 74–104 articles. First maxilla proximal endite rounded, subcircular with margins visibly convex; endopodal palp wide, short, distal end upturned. Third maxilliped without exopod, endopod with merus distal inner margin projected into strong subtriangular lobe, lateral margins of merus sinuous, outer distal margin ending on acute angle. First pereopod merus large, inflated, broad truncate lobe on inferior margin of merus, carpus distal end with large spine, propodus ca. as long as dactylus; dactylus elongate, more than twice as long as wide, superior surface almost straight, inferior surface convex with low, moderate, and regularly spaced serrations, dactylus lined by long plumose setae and short spiniform setae or spinules, terminus of dactylus with single short spine, terminus subacute. Pleon with second pleonite larger than others, tergite as wide as carapace, sides of second pleonite forming wide flanges laterally, second and third pleonite with two pairs of rugae extending from junction with next pleonite almost to ventrolateral margin. Overall coloration olive grey, white laterally, rugae distinctly white in coloration, few thin white bars or stripes near posterolateral regions of carapace.

Description

Carapace (Figs 1A, 5D, 6B, 8A, 11, 12A) elongate, 1.42–1.54× longer than wide, subcylindrical, overall dorsally convex, highly convex transversely, slightly convex longitudinally; carapace surface densely covered by low transverse microcrenulate to microdenticulate rugae, many of which are continuously elongate, not forming proper lines or rows of rugae, many continuous across middorsal region on anterior and posterior portions of carapace, usually 17 or more rugae extending across postcervical middorsal line; pterygostomial region with ventrolateral rugae; rugae separating small, anteriorly curved ridges; anterior margin of broad epimeral lobe of carapace with serrated appearance due to presence of such ridges. Pterygostomial plates densely punctate, separated from carapace by post-gastric groove; low slightly rugose ridge extending from median portion almost to distal end of plate, parallel to carapace margin for most of its extension, slightly deflected inwards near distal end. Front (Figs 5D, 6F) with three subacute dentiform projections; median projection forming broad triangular or subtriangular rostrum surrounded by relatively long plumose setae, distal end of rostrum sharply pointed, rostrum visibly shorter than lateral projections; lateral projections subtriangular with concave sides proximally and straight sides distally, visibly longer than rostrum, also surrounded by relatively long plumose setae; rostrum and lateral projections separated by wide U-shaped sulcus. Anterolateral margins of carapace just to the side of frontal projections surrounded by short plumose setae. Transverse frontal groove parallel to front, mostly straight, slightly bent at lateral extremes. Cervical groove just anterior to midlength of carapace, crescent shaped with convex face facing posteriorly, slight anteriorly facing notch on cervical groove on carapace midline. Most rugae broken, obsolete or absent on lower broad epimeral lobe.

Figure 8.

Emerita almeidai sp. nov. A ♀ paratype, cl. 14.67 mm (CCDB 5855) B, E ovigerous ♀ paratype, cl. 15.01 mm (CCDB 4937) C, D ovigerous ♀ paratype, cl. 17.31 mm (CCDB 5855) A dorsal view B lateral view of dactylus of pereopod 1 C lateral view of left antennule D lateral view of left antenna E dorsal view of telson and uropods. Scale bars: 6 mm (A); 4 mm (B, E); 3 mm (C, D).

Eyes (Fig. 5D) swollen at end of very narrow and elongated peduncles, reaching anteriorly past distal portion of fifth antennal peduncle article when extended and past spines of second antennal article when retracted; ocular peduncles composed of three articles; first article arcuate, longer than wide, convex on internal face and concave on external face; second article deflected downwards, longer than first article; third article long, first third wider, other two thirds very narrow, widening near eye.

Antennules (Fig. 8C) short; antennular peduncle composed of three articles; first article wider than others, external surface with large dentiform projection near base of article; second article densely setose, trapezoid in shape, dorsal surface shorter, ventral surface longer; third article short, also trapezoid in shape, dorsal surface longer, ventral surface shorter; flagellum dorsal ramus longer, with 30 articles, ventral ramus shorter, with 12 articles.

Antenna (Figs 6J, 8D) long; antennal peduncle composed of five articles; first article trapezoidal, longer than wide; second article large, covered by sparse rugae, distal end with three large spiniform projections, median projection longest, dorsal and ventral projections ca. the same size as each other, sulcus extending across dorsolateral surface from proximal end to base of dorsal spiniform projection, microdenticulate ridge separating ventral projection from median projection, one row of setose rugae present on mesial ventral portion; third article inserted on lateral portion of second article, completely concealed by second article in lateral view, trapezoidal in shape, proximal portion rectangular in shape, distal portion triangular, short line of setae parallel to distal margin; fourth article dorsally convex, ventrally Y-shaped; fifth article elongate, slimmer near base, inflated distally, row of setae on ventral margin; flagellum long, composed of 74–104 articles with dense long setae ventrally in adult specimens, number of articles smaller in juveniles, first article longest, ~ 3× as long as other articles.

Mandible (Fig. 9A) membranous, mostly fused with posterior margin of epistome; gnathal lobe short, kidney-shaped, inserted basally on mandible, projected inwards, external margin convex, internal margin concave, long plumose setae along mesial and distal margins; palpus composed of two articles, longer than gnathal lobe; first article subrectangular; terminal article suboval, lined by many long setae.

Figure 9.

Emerita almeidai sp. nov. A–E ovigerous ♀ paratype, cl. 17.31mm (CCDB 5855) F, G ovigerous ♀ paratype, cl. 15.01 mm (CCDB 4937) A right mandible B left first maxilla C right second maxilla D left first maxilliped E left second maxilliped F right third maxilliped external face G right third maxilliped internal face. Scale bars: 1 mm (A–D); 4 mm (E–G).

First maxilla (Fig. 9B) small; proximal endite loosely connected to rest of appendage, oval, flattened, lateral and distal margins surrounded by relatively long setae; distal endite elongate, narrow, distal end slightly wider, pin-shaped, margins lined by setae, setae on proximal internal side very long, median and distal setae shorter, setae on proximal and median external portions shorter, longer subdistally; endopodal palp nearly as wide as long, tip slightly hooked upwards.

Second maxilla (Fig. 9C) exopod developed as scaphognathite attached to base, proximal and distal lobes flattened, lined by long setae, proximal lobe semi-oval in shape, broader, distal lobe semi-oval, slimmer; endopod short, wider proximally, narrowed towards distal end, subacute tip deflected distally.

First maxilliped (Fig. 9D) membranous; exopod larger, arched, composed of two articles; proximal article subrectangular, outer margin convex, inner margin concave, distal article subovoid, surrounded distally by many long plumose setae, outer margin proximally convex until ca. midpoint, where it becomes concave, inner margin convex throughout its extension; endopod minute, elongate, membranous, with small tuft of setae subterminally; distal endite crescent shaped, exceeding length of exopod first article, extensively covered by short setae on external surface, inner margin covered by dense long plumose setae, patch of relatively long plumose setae present on distal end.

Second maxilliped (Fig. 9E) membranous, exopod and endopod subequal; exopod composed of two articles; proximal article elongate, subtriangular, widest proximally, narrowing towards distal end, sparsely setose; distal article subovoid, margins surrounded by long plumose setae; endopod composed of four articles; ischio-merus narrow, arcuate in shape, proximal end wider, narrowing towards distal end, outer margin convex lined by several long setae, inner margin concave lined by several setae; carpus short, inflated, distal and lateral margins densely covered by long plumose setae; propodus short, less robust than carpus, margins covered by setae; dactylus long, narrow, elongate, widest at base, narrowing towards distal rounded end, ~ 2/3 as long as ischio-merus, surrounded by long setae.

Third maxilliped (Fig. 9F, G) lacking exopod; endopod with coxa wider than long, small subtriangular projection on proximal inner side, base-ischium minute, much wider than long, merus broad, sparse setose rugae present on outer face, inner face mostly smooth with one large and distinct ridge crossing merus from base-ischium junction to carpus junction, margins lined by short setae, long plumose setae distally, nearly twice as long as wide, proximal third of inner margin very rounded, convex, distal two thirds straight, large subtriangular projection on distal end of inner portion of merus overlying part of carpus and propodus, outer margin slightly concave proximally, convex distally, distal end of outer portion of merus straight, carpus short, subquadrate, distal margin and inner face covered by long setae, propodus long, slightly curved inwards, outer face smooth, inner face densely covered in setae, dactylus long, shorter than propodus, slightly curved inwards, distal end rounded, outer face smooth inner face densely covered in setae.

First pereopod (Fig. 10A) coxa subtrapezoidal, sparsely covered by setose rugae on external face, setae on ventral margin and distal end, ventral dentiform projection proximally; base-ischium longer than wide, minute, lined by setae ventrally, with two lobes separated by median notch, ventral margin surrounded by setae; merus large, subcircular, sparsely covered by setose rugae, superior margin convex, inferior margin convex proximally, extended laterally forming truncate lobe with straight or almost straight lateral margin, small short sulcus on mesial portion of distal end of merus; carpus elongate, crossed by some oblique rows of setose rugae on distal ventral portion, three very distinct small perpendicular rows of setose rugae on dorsal surface separating article from large narrow distal spine, spine reaching to base of dactylus; propodus subtrapezoidal in shape, sparsely surrounded by setae, sparse setose rugae present, a transversal ridge running along most of ventrolateral portion of propodus, including distal process (Fig. 8B), dense short setae running along ridge, distal process long, subtriangular, strong oblique ridge running from dactylus junction to base of distal process, superolateral surface of distal process excavate, fits base of dactylus, long setae present on distal process; dactylus (Figs 5D, 6D, 8B) elongate, usually more than twice as long as wide, superior margin mostly straight, inferior surface convex, inferior surface moderately serrated from median portion to distal end, terminus of dactylus acute or subacute bearing one small spine, weakly arched oblique ridge across superior portion of dactylus, ridge originating near median portion of junction with propodus, running upwards towards superior margin, fusing with superior margin around median portion of dactylus, ridge lined by small setae, long plumose setae surrounding dactylus, small spiniform setae among them.

Figure 10.

Emerita almeidai sp. nov. A, D ovigerous ♀ paratype, cl. 17.31 mm (CCDB 5855) B, C, E ovigerous ♀ paratype, cl. 15.01 mm (CCDB 4937) A lateral view of right pereopod 1 B lateral view of left pereopod 2 C lateral view of left pereopod 3 D lateral view of left pereopod 4 E lateral view of right pereopod 5. Scale bars: 4 mm (A); 2 mm (B); 5 mm (C); 3 mm (D); 1 mm (E).

Second through fourth pereopods (Fig. 10B, C, D) similar in configuration. Second pereopod coxa subquadrate; base-ischium small, longer than wide, surrounded by setae; merus large, subrectangular, longer than wide, surface covered by sparse setose rugae, superior margin mostly straight, convex towards distal end, inferior margin slightly concave, large dentiform projection protruding ventrally from distal end of merus, inferior margin lined by setae; carpus subtriangular, external surface with two short ridges present, one on superior and one on inferior regions of article, internal surface setose, crossed mesially by single row of setae, inferior portion with small triangular projection distally lined by setae; propodus wider than long, subrectangular, superior margin oblique, external face with small triangular projection positioned distally on dorsal region overlying part of dactylus, transverse ridge near superior margin, internal face with large spiniform projection lined by large setae at ca. same position; dactylus large, flattened, hook-shaped, broad proximally, narrowing distally, superior margin concave, inferior margin convex, distal tip upturned, inferior margin surrounded by long setae. Third pereopod coxa and base-ischium similar to second pereopod; merus subrectangular, much longer than wide; carpus very large, subtriangular, superior and inferior ridges present, propodus wider than long, subrectangular, superior margin oblique, small ridge near superior margin present, small triangular projection positioned distally on superior margin overlying part of dactylus; dactylus large, hook-shaped, flattened, broad proximally, narrowing distally, superior margin concave, inferior margin convex, distal tip upturned, inferior margin surrounded by setae. Fourth pereopod coxa and base-ischium similar to that of second and third pereopods; merus elongate, much longer than wide, subrectangular; carpus large, longer than wide, inferior surface almost straight, superior surface convex; propodus subquadrate, nearly as wide as long, lacking triangular projection, line of short setae near superior margin; dactylus large, somewhat flattened, broad distally, narrowing towards distal end, proportionally smaller than in other pereopods, subtriangular, superior and inferior margins almost straight, tip not upturned, a line of short setae parallel to superior margin, inferior margin lined by setae.

Fifth pereopod (Fig. 10E) reduced, concealed under carapace; all articles except for dactylus elongate, much longer than wide, with small tufts of setae distally; propodus long, with distal projection that along with dactylus forms a small chela; dactylus short, deflected inwards; chela small, covered by setae.

Pleon short, partly recurved under carapace. First pleonite smallest, minute, much wider than long, fitting into posterior concavity of carapace; second pleonite larger than others, as wide as carapace, median portion of pleonite narrow, both sides of pleonite enlarged, forming two wide lateral flanges, flanges with pair of long transverse rugae extending from third pleonite junction almost to ventrolateral margins of tergite, distal portion of ventrolateral region of each pleonite with short transverse ruga extending from superior margin to inferior margin of narrowest portion of flange, wide lateral flanges forming space where third pleonite fits; third pleonite smaller than second, sides of pleonite somewhat enlarged forming flanges that are mostly covered by flanges of second pleonite, two transverse rugae extending from junction with fourth pleonite to junction with second on each flange; fourth pleonite smaller than third, sides slightly enlarged forming flanges which are mostly covered by flanges of third pleonite, one oblique ruga extending from junction with fifth pleonite to junction with third on each side of pleonite; fifth pleonite smaller than fourth, lateral flanges small; sixth pleonite subpentagonal, lateral margins forming subtriangular projections, two short longitudinal grooves near articulation with telson, each groove joined to two much smaller transverse grooves. Female pleopods on second through fourth pleonites developed as three long and narrow articles, not developed on first and fifth pleonites; males without developed pleopods on first through fifth pleonites; uropods large, protopod subrectangular, endopod suboval, rounded, distal margin densely covered in setae, exopod suboval, more elongate, distal margin densely covered in setae.

Telson (Figs 6H, 8E) lanceolate, lateral margins setose, slightly convex proximally, very slight notches at ~ 3/4 of length of telson, two short longitudinal grooves near junction with pleon, two long longitudinal ridges parallel to lateral margins of telson, distal end of telson subacute.

Coloration in life

Carapace overall olive grey dorsally, lateral regions white, rugae extending across carapace white, posterolateral regions of carapace with few slim white longitudinal lines or small white blotches; lines and blotches usually restricted to posterolateral region, but some specimens possess one white longitudinal line along posterior 1/4 of carapace median line. Pleonal somites olive-grey anteriorly, white posteriorly, forming a pattern of alternating olive-grey and white stripes (Fig. 12A).

Habitat

Shallow infaunal, lives in wave swash zone of sandy beaches or shallow subtidal sandy flats where it burrows shallowly in sand, moves with tidal rise and fall.

Distribution

Brazil: known from Maranhão, Ceará, Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, Sergipe, Bahia, Espírito Santo, and Rio de Janeiro.

Etymology

The species name honors Alexandre O. Almeida, a valued friend and respected colleague who has contributed extensively to increase knowledge of the decapod crustaceans of Brazil.

Remarks

Emerita almeidai sp. nov. is closest to E. portoricensis and thus shares a wide range of morphological similarities, which is why for many years several specimens from Brazil were wrongly assigned to E. portoricensis (see Introduction). Both species have a carapace densely covered by microcrenulate rugae (Figs 1A, 5D, G, 6B, 8A, 11, 12) distributed in similar patterns, a front with three subacute lobes with the rostrum being distinctly shorter than lateral projections (Figs 5D, G, 6B), first pereopod dactyli more than twice as long as wide and not as rounded as in other species such as Emerita brasiliensis and Emerita talpoida (Figs 5, 6C, D), two pairs of rugae extending onto lateral flanges of the first two pleonites. However, some characters such as the carapace length and width ratio (cw./cl.), the number of articles on the antennal flagellum, the first maxilla, the dactylus of the first pereopod, and the coloration in life can be used to distinguish between these two species. The carapace in E. almeidai sp. nov. (Figs 1A, 5D, 6B, 8A, 11, 12A) tends to be more oblong than that of E. portoricensis (Figs 5G, 12B), usually being 1.42–1.54× as wide as long in adult specimens (vs. 1.49–1.64× in E. portoricensis, present study), although there is some overlap. The number of articles on the antennal flagellum of E. almeidai sp. nov. (Fig. 8D) also tends to be more variable than that of E. portoricensis, varying from 74 to 104 articles in adult specimens, while E. portoricensis usually has 76–86 (Felder et al. 2023; present study). Although there is still some overlap, this character is still useful to distinguish between the two species. However, juvenile specimens (see details in Materials and methods) may have many fewer articles on the antennal flagellum in both species, and thus this character is only useful for adult specimens. The first maxilla of E. almeidai sp. nov. (Fig. 9B) also differs from that of E. portoricensis (Felder et al. 2023: 349, fig. 3): in E. almeidai sp. nov. the proximal endite is wider, rounder and with more convex margins, and the endopodal palp is proportionally wider and shorter. The first pereopod dactylus (Figs 5D, 6D, 8B) is also distinct, with E. almeidai sp. nov. having low, moderately and regularly spaced serrations on the inferior surface of the dactylus, while E. portoricensis has a slight and irregular serrations, which in many cases can be absent. The coloration of these two species can also be used to distinguish between live specimens. As shown in a recent redescription of E. portoricensis (Felder et al. 2023: 345, fig. 1) and in the present work (Fig. 12B), this species has very wide white bars on the posterolateral regions of carapace along with a wide white bar along the posterior 1/4 of the carapace median line. Although E. almeidai sp. nov. shares some of these characteristics (Fig. 12A), the white bars are usually slimmer and the white bar along the carapace median line is usually absent; however, it was observed only in one freshly collected paratype specimen (MZUSP 43536). The white colored rugae, which were observed in all of the freshly collected specimens of E. almeidai sp. nov. (Fig. 12A), however, are not present in either of the specimens shown in the recent redescription of E. portoricensis (Felder et al. 2023: 345, fig. 1) or in the specimen analyzed in this study (Fig. 12B), suggesting that this character might be unique to E. almeidai sp. nov. The southernmost record for E. portoricensis (Venezuela and Trinidad) and the northernmost record for E. almeidai sp. nov. (Maranhão, Brazil) are very far apart and there is a strong marine barrier, the Amazon–Orinoco plume (see Curtin 1986 for physical characteristics) that can promote some isolation between northern and southern decapod populations (see Peres et al. 2022), and this is possibly the reason there are no records of these species coexisting in the same environment.

Figure 11.

Emerita almeidai sp. nov. A ovigerous ♀ holotype, cl. 13.52 mm (CCDB 7233) B ♂ paratype, cl. 7.29 mm (MZUSP 43536) C ♀ paratype, cl. 10.49 mm (MOUFPE 20112) D ♀, cl. 10.20 mm (CCDB 3369). Scale bars: 4 mm (A, B); 2 mm (C); 5 mm (D).

Figure 12.

Fresh coloration of Emerita almeidai sp. nov., E. portoricensis and E. brasiliensis A E. almeidai sp. nov., ovigerous ♀ (not deposited), live specimen, Porto de Galinhas, PE, Brazil B E. portoricensis, ♀ (CCDB 3525), freshly collected specimen, Boca del Drago, Panama C Emerita brasiliensis, ♀ (CCDB 7301), freshly collected specimen, Praia de Guaratuba, Bertioga (SP), Brazil. Coloring details: 1. Thin white stripes on posterolateral portions of carapace; 2. Rugae clearly surrounded by white coloration; 3. Striped pattern on pleon; 4. Wide white bars on posterolateral portions of carapace; 5. White bar along posterior 1/4^th of median line of carapace; 6. Striped pattern on pleon; 7. Olive brown or brownish white color overall; 8. Rugae broken into cusps; 9. Absence of striped pattern on pleon.

Emerita almeidai sp. nov. has been observed to co-occur with E. brasiliensis in Praia de Iriri, in the state of Espírito Santo, Brazil (CCDB 3992 and 7226), with specimens of both species being collected at the same locality and on the same day. The distribution of these two species overlaps along the coast of the states of Espírito Santo and Rio de Janeiro, and it is possible that they co-occur in more locations in these states. Emerita almeidai sp. nov. can be distinguished from E. brasiliensis by the shape of the dactylus, which is elongated and has a serrated ventral margin in E. almeidai sp. nov. (Figs 5D, 6D, 8B) and ovate and non-serrated in E. brasiliensis (Figs 5C, 6C). The dactylus length and width ratio (dl./dw.) is also a robust parameter to distinguish the two species, especially in individuals of similar size. In E. almeidai sp. nov., the dactylus is proportionally longer and narrower than that of E. brasiliensis. The front is also different (Figs 5C, D, 6C, D): in E. brasiliensis the lateral projections and the rostrum are ca. as long as each other. The patterns of distribution of the microcrenulate rugae are also distinct between these two species (Figs 5C, D, 6A, B), with E. almeidai sp. nov. having very dense and non-broken rugae across much of the carapace, while E. brasiliensis has rugae that are more broken into cusps (Felder et al. 2023). Furthermore, the cw./cl. ratio is also useful to distinguish these two species since E. almeidai sp. nov. has an overall longer and narrower carapace when compared to E. brasiliensis. The antennae (Figs 6I, J, 8D) is another character that can be used to distinguish between the two species, because E. almeidai sp. nov. has 74–104 articles, while E. brasiliensis has 103–134 articles; however, there is a small overlap. The differences between the telson measurements obtained between the telson length and width ratio (tl./tw.) showed a tendency for telson growth in E. almeidai sp. nov. in relation to the increase in carapace length, while in E. brasiliensis this ratio tends to remain stable with increasing carapace length. Melo (1999) did not highlight significant differences for this structure, but Calado (1990) described the telson of E. brasiliensis as being lanceolate, larger than the pleon, with all margins with short bristles, and that of E. almeidai sp. nov. with a triangular shape, larger than the pleon, wider in the proximal portion, with margins also supporting short bristles, which corroborates the biometric data found in our analyses.

The other species of Emerita found in the western Atlantic Ocean, E. talpoida and E. benedicti, are not known to co-occur with E. almeidai sp. nov.; Emerita talpoida can be distinguished from the new species by the rounded and ovate dactylus of the first pereopod (Fig. 5D, F), while E. benedicti (Fig. 5B) has a very acute terminus of the dactylus compared to a more subacute and slightly rounded terminus for E. almeidai sp. nov. The morphology of the first pereopod dactylus can also be used to distinguish the new species from other congeners in the Indian Ocean, Indo-Pacific and eastern Pacific.

Previous descriptions of mouthparts of species of Emerita are scarce, only existing for two species, E. talpoida and E. portoricensis (see Snodgrass 1952 and Felder et al. 2023). Thus, comparative studies of the mouthpart morphology of Emerita are lacking and could be of great importance. At least for E. almeidai sp. nov. and E. portoricensis, it has been noted that the morphology of certain articles of the mouthparts, in this case the first maxilla, can be successfully used to distinguish between species. Thus, future descriptions and redescriptions of species of Emerita should include such characters, which might be valuable for comparative taxonomic studies.

The number of species in the genus Emerita is now raised to 12, with five occurring in the western Atlantic (E. almeidai sp. nov., E. benedicti, E. brasiliensis, E. portoricensis, E. talpoida), five in the Indian Ocean or Indo-Pacific (E. austroafricana, E. emeritus, E. holthuisi, E. karachiensis, E. taiwanensis) and two in the Eastern Pacific (E. analoga and E. rathbunae). The actual number might even be higher, given that there is a large distribution hiatus between the populations of E. analoga from North and South America and genetic differences between the northern and southern populations of E. talpoida. The record of E. brasiliensis from Venezuela is doubtful and may be a misidentification or may represent a separate species given the large geographic hiatus (Fig. 7). All of these cases require a thorough study, as made herein for some congeners, to determine whether these actually represent different, yet very similar, species.

Discussion

The combination of morphological and molecular methods confirms the validity of each species of Emerita included in the analysis and showed a clear division of E. talpoida into two subgroups that should be studied in the future. In addition, our phylogenetic trees based on two molecular markers confirmed the presence of a cryptic species previously misidentified as E. portoricensis, which we described in detail as E. almeidai sp. nov. For more than eight decades, a group of Brazilian specimens of Emerita was treated as E. portoricensis by several authors (see Introduction). The distribution of E. almeidai sp. nov. from Maranhão to Rio de Janeiro (Brazil) in combination with the redescription of E. portoricensis by Felder et al. (2023) answered questions that were raised in the past by some authors (Efford 1976; Calado 1990; Melo 1999) about the gap/discontinuity that existed in the distribution of E. portoricensis. These questions were clarified by the recognition of two different species, one in each hemisphere along the western Atlantic.

Species in the genus Emerita are known to have relatively long planktonic larval stages (i.e., E. talpoida lasting 30 days and E. rathbunae lasting 90 days, Efford 1970; E. holthuisi lasting 52 days, Siddiqi and Ghory 2006), thus favoring the chances of dispersion to suitable habitats. This extended larval development plays a critical role in governing the genetic structure, phylogeography, and dispersion of mole crabs of the genus Emerita (Dawson et al. 2011), factors which are also influenced and defined by other influences such as currents, transport effects, and sea level changes as observed in other groups (Doherty et al. 1995; Bohonak 1999; Cowen et al. 2000; Dawson 2001; Byers and Pringle 2006; Lester et al. 2007; Lessios 2008). Although the dispersal potential is high for species that present this larval profile (Palumbi and Benzie 1991), it does not always lead to strong gene flow, since physical or biological barriers can interfere with this dispersal process. Thus, disjunct populations can accumulate substantial genetic differences over time (Tam et al. 1996) that can result in the appearance of species that are not recognized as such due to the absence of studies covering all the different populations within the area of distribution as well as the lack of a representative set of specimens from these populations. The newly described species E. almeidai sp. nov. fits within this pattern, since it is a southern population that appears to be separated geographically by the Amazon–Orinoco plume, which has been shown to be an important physiological barrier for larval dispersal of many marine taxa, including decapod crustaceans (see Mandai et al. 2018 and Peres et al. 2022 for references and details).

There are some examples to support this hypothesis of separation for marine decapod crustaceans with a wide distribution along the western Atlantic, as noted in E. almeidai sp. nov. Using shrimps as an example, a recent study expanded the diversity of seabob shrimps of the genus Xiphopenaeus Smith, 1869 with descriptions of two new species (Carvalho-Batista et al. 2019), and a new species of Latreutes Stimpson, 1860 was described for a population from Brazil (Terossi et al. 2019). Considering the low number of integrative studies devoted to the huge diversity of decapods in the western Atlantic, these cases might not be exceptional, and we expect that a considerable number of cryptic and undescribed species may be revealed in the future.

Insights on the evolution of the genus

There are no known fossils that provide information about the evolutionary history of Emerita or the paleontological origins of the genus. Molecular clock-based studies have suggested that all species of the genus evolved before the mid- to late Pliocene, although no centers of origin or biogeographic scenarios have been suggested. The hypothesis that Emerita species evolved at least before the late Neogene was raised by Tam et al. (1996). Vicariance and dispersal events probably played an important role in the speciation of Emerita. Other ecological, physiological, and oceanographic processes likely contributed to the final geographic distribution of the populations that gave rise to the different species of the genus seen today. The expansion and colonization of new geographic areas with subsequent reduction of gene flow were probably the mechanisms by which most of these species originated (Haye et al. 2002).

Species of Emerita present a geographic distribution in disjunctive regions, apparently with separate conspecific populations and/or with species that may coexist (see Tam et al. 1996 and Felder et al. 2023 for reviews). In the Americas, Emerita analoga is one of two species that inhabit the Pacific coast, recorded in both hemispheres, while Emerita rathbunae is restricted to the tropical region. In the western Atlantic, Emerita talpoida is found from Massachusetts to Florida and also in the Gulf of Mexico; Emerita benedicti occurs mainly in the inner part of the Gulf of Mexico; Emerita portoricensis inhabits the tropical sandy islands and Central American mainland shorelines of the Caribbean Sea; Emerita brasiliensis is distributed along the coast of southern South America, and Emerita almeidai sp. nov. is endemic to the Brazilian coast. These examples demonstrate that the vast majority of these species have wide geographic ranges and, thus, disjunct populations can be naturally genetically isolated (Tam et al. 1996), especially when natural barriers are present.

Outside of the Americas, Emerita holthuisi has a very wide distribution, from the easternmost part of Africa to the southernmost part of India. It can also occur along the east coast of Africa, but so far there are few records for this region. Emerita emeritus overlaps with E. holthuisi along the western coast of southern India and also occurs in the Indo-Pacific on the eastern coast of India, Malaysia, Indonesia (Efford 1976), and possibly in between. In the present study, these two species grouped together in a separate clade from the one composed of specimens from the Americas. Emerita austroafricana can be found along the southern portion of the east coast of Africa, in Mozambique, Madagascar, and South Africa (Schmitt 1937; Efford 1976). The molecular phylogenetic analysis using the COI gene carried out by Haye et al. (2002) recovered E. austroafricana as the sister species of E. emeritus, although E. holthuisi, the sister species of E. emeritus recovered in their phylogenetic analysis with the 16S rRNA gene and in the present study, was not included in the analysis. This suggests a close relationship between these three species, but the precise topology of the clade formed by these taxa cannot be determined at present. Emerita karachiensis occurs on the west coast of the Indo-Pak subcontinent (Niazi and Haque 1974) and has not been included in any molecular analyses. However, Niazi and Haque (1974) mentioned morphological similarities between E. karachiensis and E. holthuisi, suggesting a close relationship between these species. Therefore, it is likely that this species is also part of the clade encompassing the Indo-Pacific species, although its exact position within this clade remains to be determined. Emerita taiwanensis is known only from two localities in Taiwan (Hsueh 2015) and has not been included in molecular phylogenetic analysis either. Hsueh (2015) suggested a close relationship between species that possess an acute and elongate pereopod 1 dactylus, such as E. portoricensis, E. benedicti, E. holthuisi, and E. karachiensis. However, as indicated by our phylogenetic analysis, this character does not seem to be phylogenetically informative, as it does not define any clades and appeared and was lost at least several times during the evolution of the species in the genus. Thus, the phylogenetic relationships of E. taiwanensis remain uncertain.

In the hypothesis proposed by Tam et al. (1996) on the evolution of the Emerita species from the Americas, it was suggested that E. analoga (Pacific species) was diverged from the other five New World species and was distant from E. rathbunae (the other Pacific species). Furthermore, E. rathbunae was clustered as sister species of the other species of Emerita found in the western Atlantic instead of with E. analoga that inhabits the Pacific coast. This hypothesis also suggests that Emerita species in the Americas evolved from an ancestral stock that was split into two branches, one leading to E. analoga and the other leading to the five remaining species. Our phylogenetic analysis corroborates this hypothesis, as E. analoga was recovered as the sister taxon to all other species of Emerita. Furthermore, it is likely that after splitting from E. analoga, the other populations of Emerita were divided into two groups, one that gave rise to the western Atlantic species and another that gave rise to the Indo-Pacific species. Consequently, with this scenario in mind, it can be assumed that the ornamentation of the second joint of the antennal peduncle present in E. analoga and some of the Indo-Pacific species (Schmitt 1937) is plesiomorphic, while the apomorphic condition is found in the clade composed of the other American species.

The biogeographic scenarios for the origin of E. analoga are not clear, and two hypotheses have been proposed (see references below): in the first, the genus Emerita originated on the western side of the Atlantic Ocean. If the center of origin is the Atlantic Ocean, it can be assumed that the species currently distributed in the eastern Pacific (E. analoga and E. rathbunae) evolved from Atlantic ancestors that dispersed into the Pacific and became isolated due to the closing of the Isthmus of Panama. The isthmus was closed to surface marine water circulation ~ 3 Mya (Late Neogene) but closed to deep-water circulation much earlier (Malfait and Dinkelman 1972; Keigwin 1982). In the second scenario, the center of origin of the genus Emerita was the Pacific Ocean. The Atlantic may have been colonized through the isthmus and taxa that differentiated in the Atlantic were likely to be ancestors of the species that later recolonized the Pacific, in this case E. rathbunae (Haye et al. 2002). At the end of the Cretaceous (~ 65 Mya), South America and Africa were completely separated (Dietz and Holden 1970). Although it is not possible to know how many species of Emerita inhabited the Tethys Sea before the complete separation of South America and Africa, it can be inferred that the separation of the continents was an important event in the speciation of these animals.

The clade composed of the northwest Atlantic species (E. benedicti, E. talpoida, E. portoricensis) and E. almeidai sp. nov. from the southwest Atlantic, as recovered in the 16S rRNA analysis, underwent extensive species diversification compared to the clade formed by E. rathbunae from the Pacific and E. brasiliensis, from the southwestern Atlantic, since the separation of the Pacific and Atlantic oceans ~ 3 Mya. This is consistent with other studies suggesting that the marine biota (mollusks, corals, and foraminiferans) of the western Atlantic were dramatically transformed ~ 2–3 Mya (Jackson and Budd 1996; Allmon 2001). Some hypotheses postulate that this change occurred as a result of the environmental disturbance associated with glaciation in the northern hemisphere and the formation of the Isthmus of Panama (Harrison 2004).

The closure of the Isthmus of Panama strongly affected ocean circulation, nutrient distribution, temperature, and salinity of the western Atlantic, and therefore had a significant influence on the evolution of marine fauna (Coates and Obando 1996; Allmon 2001). The flow of the Gulf Stream through the Yucatan Strait became more intense than it was before the closure of the Isthmus (Richards 1968) with an intense upwelling of cold deep waters (Stanley 1986). Therefore, this type of current may be a significant factor acting as a barrier to separate the group of species from the Gulf of Mexico from those located in the western side of the Atlantic, as observed in the E. talpoida clade, composed of specimens from Florida and Mexico in one group and individuals from Massachusetts and South Carolina in another group. There have been some suggestions of the occurrence of E. talpoida in Caribbean waters (see Felder et al. 2023, who say there is no confirmed evidence of this distribution). Previous usage of crabs as models of study (Felder and Staton 1994; Scheineider-Broussard et al. 1998) have identified the Florida Peninsula as a geographic barrier between the western Atlantic and Gulf of Mexico populations, raising awareness about the presence of cryptic species resulting from genetic isolation between populations distributed in these regions.

Acknowledgements

The present study is part of a long-term project to evaluate the taxonomy and genetic variability of decapods in the western Atlantic, including the Brazilian coast, and was supported by scientific grants provided to FLM by Fundação de Amparo à Pesquisa do Estado de São Paulo – FAPESP (Temáticos Biota 2010/50188-8 and INTERCRUSTA 2018/13685-5; Coleções Científicas 2009/54931-0; PROTAX 2016/50376-5 and 2021/08075-6); Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (Edital Universal 471011/2011-8; International Cooperative Project CNPq 490353/2007-0, 490314/2011-2; and PQ 302748/2015-5, 302253/2019-0); and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES (Código de financiamento 001, Ciências do Mar II Proc. 2005/2014 –23038.004308/2014-14). JMP received support by scientific fellowships from CNPq (Proc. 139656/2012-0) and FAPESP (Proc. 2013/20688-7), RR received post-doctoral scholarships from CNPq (Proc. 500460/2010-8) and FAPESP (Proc. 2013/05663-8), JNT received a PhD fellowship from CNPq (Proc. 140957/2020-0) and FCB received a scientific fellowship from FAPESP (Proc. 2022/11860-0). Among many colleagues who assisted with field sampling, loans, donations, logistics, and discussion, we thank Alexandre O. Almeida (UFPE, Brazil), Darryl Felder (ULLZ, USA), Fernando Álvarez and José Luis Villalobos (CNCR, UNAM, Mexico), Javier Luque (Yale University, USA), Luis M. Pardo (Universidad Austral, Chile), Raquel Collins (STRI, Panama), and all members of LBSC for their contributions during the development of this research. The collection and access to genetic heritage of species conducted in this study complied with current applicable state and federal laws of Brazil (permanent license to FLM for collection of Zoological Material No. 11777-2 MMA/IBAMA/SISBIO and SISGEN A4CCD88). The authors, especially FLM, are honored to recognize the many achievements of Dr. Tereza Calado (retired professor of UFAL, Brazil) to the study of mole crabs of Brazil in past and for this reason dedicate this contribution to her. We also thank Christopher Boyko, Dian Baghawati, Ingo S. Wehrtmann, and Nathalie Yonow for the useful comments during the review process.

References

Allmon WD (2001) Nutrients, temperature, disturbance, and evolution: A model for the late Cenozoic marine record of the western Atlantic. Palaeogeography, Palaeoclimatology, Palaeoecology 166(1–2): 9–26. https://doi.org/10.1016/S0031-0182(00)00199-1

Bhagawati D, Winarni ET, Nuryanto A (2020) Molecular barcoding reveal the existence of mole crabs Emerita emeritus in north coast of Central Java. Biosaintifika. Journal of Biology & Biology Education 12(1): 104–110. https://doi.org/10.15294/biosaintifika.v12i1.20497

Bhagawati D, Nuryanto A, Winarni ET, Pulungsari AE (2022) Morphological and molecular characterization of mole crab (Genus: Emerita) in the Cilacap coastlines of Indonesia, with particular focus on genetic diversity of Emerita sp. nov. Biodiversitas (Surakarta) 23(5): 2395–2404. https://doi.org/10.13057/biodiv/d230517

Bohonak AJ (1999) Dispersal, gene ﬂow, and population structure. The Quarterly Review of Biology 74(1): 21–45. https://doi.org/10.1086/392950

Boyko CB (2002) A worldwide revision of the recent and fossil sand crabs of the Albuneidae Stimpson and Blepharipodidae, new family (Crustacea: Decapoda: Anomura: Hippoidea). Bulletin of the American Museum of Natural History 272: 1–396. https://doi.org/10.1206/0003-0090(2002)272<0001:AWROTR>2.0.CO;2

Boyko CB, McLaughlin PA (2010) Annotated checklist of anomuran decapod crustaceans of the world (exclusive of the Kiwaoidea and families Chirostylidae and Galatheidae of the Galatheoidea) Part IV – Hippoidea. The Raffles Bulletin of Zoology (Supplement 23): 139–151.

Byers JE, Pringle JM (2006) Going against the ﬂow: Retention, range limits and invasions in advective environments. Marine Ecology Progress Series 313: 27–41. https://doi.org/10.3354/meps313027

Calado TS (1990) Redescrição do gênero Emerita Scopolli, 1777 e as espécies brasileiras (Decapoda, Anomura, Hippidae). Trabalhos Oceanográficos da Universidade Federal de Pernambuco 21: 263–290. https://doi.org/10.5914/tropocean.v21i1.2649

Calado TS (1998) Biogeografia dos Hippoidea no Atlântico (Crustacea: Decapoda) com ênfase ao Brasil. Boletim de Estudos de Ciência do Mar 10: 83–85.

Carvalho-Batista A, Terossi M, Zara FJ, Mantelatto FL, Costa RC (2019) A multigene and morphological analysis expands the diversity of the seabob shrimp Xiphopenaeus Smith 1869 (Decapoda: Penaeidae), with descriptions of two new species. Scientific Reports 9(1): e15281. https://doi.org/10.1038/s41598-019-51484-3

Coates AG, Obando JA (1996) The Geologic Evolution of the Central American Isthmus. In: Jackson JBC (Eds) Evolution and Environment in Tropical America. University of Chicago Press, Chicago, 21–57.

Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: Open or closed? Science 287(5454): 857–859. https://doi.org/10.1126/science.287.5454.857

Crandall KA, Fitzpatrick Jr JE (1996) Crayfish molecular systematic: Using a combination of procedures to estimate phylogeny. Systematic Biology 45(1): 1–26. https://doi.org/10.1093/sysbio/45.1.1

Curtin TB (1986) Physical observations in the plume region of the Amazon River during peak discharge–II. Water masses. Continental Shelf Research 6(1–2): 53–71. https://doi.org/10.1016/0278-4343(86)90053-1

Dawson MN (2001) Phylogeography in coastal marine animals: A solution from California? Journal of Biogeography 28(6): 723–736. https://doi.org/10.1046/j.1365-2699.2001.00572.x

Dawson MN, Barber PH, González-Gusmán LI, Toonen RJ, Dugan JE, Grosberg RK (2011) Phylogeography of Emerita analoga (Crustacea, Decapoda, Hippidae), an eastern Pacific Ocean sand crab with long-lived pelagic larvae. Journal of Biogeography 38(8): 1600–1612. https://doi.org/10.1111/j.1365-2699.2011.02499.x

Delgado E, Defeo O (2006) A complex sexual cycle in sandy beaches: the reproductive strategy of Emerita brasiliensis (Decapoda: Anomura). Journal of the Marine Biological Association of the United Kingdom 86(2): 361–368. https://doi.org/10.1017/S002531540601321X

Dietz RS, Holden JC (1970) The breakup of Pangaea. Scientific American 223(4): 30–41. https://doi.org/10.1038/scientificamerican1070-30

Doherty PJ, Planes S, Mather P (1995) Gene ﬂow and larval duration in seven species of ﬁsh from the Great Barrier Reef. Ecology 76(8): 2373–2391. https://doi.org/10.2307/2265814

Efford IE (1970) Recruitment to sedentary marine populations as exemplified by the sand crab, Emerita analoga (Decapoda, Hippidae). Crustaceana 18(3): 293–308. https://doi.org/10.1163/156854070X00248

Efford IE (1976) Distribution of the sand crabs in the genus Emerita (Decapoda, Hippidae). Crustaceana 30(2): 169–183. https://doi.org/10.1163/156854076X00558

Felder DL, Staton JL (1994) Genetic differentiation in Trans-Floridian species complexes of Sesarma and Uca (Decapoda: Brachyura). Journal of Crustacean Biology 14(2): 191–209. https://doi.org/10.2307/1548900

Felder DL, Lemaitre R, Mantelatto FL (2023) Redescription of the mole crab Emerita portoricensis Schmitt, 1935 (Crustacea: Decapoda: Hippidae), based on Caribbean populations from Puerto Rico, Belize, Costa Rica, and Panama. Zootaxa 5227(3): 341–354. https://doi.org/10.11646/zootaxa.5227.3.3

Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–297.

Hall TA (2005) BioEdit version 7.0.5. Biological sequence alignment editor for windows 95/98/NT/2000/XP. http://www.mbio.ncsu.edu/BioEdit/bioedit.html [Accessed 11 Dec 2018]

Harrison JS (2004) Evolution, biogeography, and the utility of mitochondrial 16s and COI genes in phylogenetic analysis of the crab genus Austinixia (Decapoda: Pinnotheridae). Molecular Phylogenetics and Evolution 30(3): 743–754. https://doi.org/10.1016/S1055-7903(03)00250-1

Haye PA, Tam YK, Kornfield I (2002) Molecular phylogenetics of mole crabs (Hippidae, Emerita). Journal of Crustacean Biology 22(4): 903–915. https://doi.org/10.1163/20021975-99990302

Hsueh PW (2015) A new species of Emerita (Decapoda, Anomura, Hippidae) from Taiwan, with a key to species of the genus. Crustaceana 88(3): 247–258. https://doi.org/10.1163/15685403-00003413

Hubbard DM, Dugan JE (2003) Shorebird use of an exposed sandy beach in Southern California. Estuarine, Coastal and Shelf Science 58: 41–54. https://doi.org/10.1016/S0272-7714(03)00048-9

Jackson JBC, Budd AF (1996) Evolution and environment: introduction and overview. In: Jackson JBC, Budd AF, Coates AG (Eds) Evolution and Environment in Tropical America. University of Chicago Press, Chicago, 20 pp.

Katoh K, Standley DM (2016) A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics 32: 1933–1942. https://doi.org/10.1093/bioinformatics/btw108

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12): 1647–1649. https://doi.org/10.1093/bioinformatics/bts199

Keigwin Jr LD (1982) Isotopic paleoceanography of the Caribbean and East Paciﬁc: Role of the Panama uplift in Late Neogene time. Science 217(4557): 350–353. https://doi.org/10.1126/science.217.4557.350

Lercari D, Defeo O (1999) Effects of freshwater discharge in sandy beach populations: The mole crab Emerita brasiliensis in Uruguay. Estuarine, Coastal and Shelf Science 49(4): 457–468. https://doi.org/10.1006/ecss.1999.0521

Lessios HA (2008) The great American schism: Divergence of marine organisms after the rise of the central American isthmus. Annual Review of Ecology, Evolution, and Systematics 39(1): 63–91. https://doi.org/10.1146/annurev.ecolsys.38.091206.095815

Lester SE, Ruttenberg BI, Gaines SD, Kinlan BP (2007) The relationship between dispersal ability and geographic range size. Ecology Letters 10(8): 745–758. https://doi.org/10.1111/j.1461-0248.2007.01070.x

Luo A, Qiao H, Zhang Y, Shi W, Ho SY, Xu W, Zhang A, Zhu C (2010) Performance of criteria for selecting evolutionary models in phylogenetics: A comprehensive study based on simulated datasets. BMC Evolutionary Biology 10(242): 1–13. https://doi.org/10.1186/1471-2148-10-242

Malfait BT, Dinkelman MG (1972) Circumcaribbean tectonic and igneous activity and the evolution of the Caribbean Plate. Geological Society of America Bulletin 83(2): 251–272. https://doi.org/10.1130/0016-7606(1972)83[251:CTAIAA]2.0.CO;2

Mandai SS, Buranelli RC, Schubart CD, Mantelatto FL (2018) Phylogenetic and phylogeographic inferences based on two DNA markers reveal geographic structure of the orange claw hermit crab Calcinus tibicen (Anomura: Diogenidae) in the western Atlantic. Marine Biology Research 14(6): 565–580. https://doi.org/10.1080/17451000.2018.1497184

Mantelatto FL, Robles R, Biagi R, Felder DL (2006) Molecular analysis of the taxonomic and distributional status for the hermit crab genera Loxopagurus Forest, 1964, and Isocheles Stimpson, 1858 (Decapoda, Anomura, Diogenidae). Zoosystema 28(2): 495–506.

Mantelatto FL, Robles R, Felder DL (2007) Molecular phylogeny of the western Atlantic species of the genus Portunus (Crustacea, Brachyura, Portunidae). Zoological Journal of the Linnean Society 150(1): 211–220. https://doi.org/10.1111/j.1096-3642.2007.00298.x

Mantelatto FL, Pardo LM, Pileggi LG, Felder DL (2009) Taxonomic re-examination of the hermit crab species Pagurus forceps and Pagurus comptus (Decapoda: Paguridae) by molecular analysis. Zootaxa 2133(16): 20–32. https://doi.org/10.11646/zootaxa.2133.1.2

Mantelatto FL, Miranda I, Vera-Silva AL, Negri M, Buranelli RC, Terossi M, Magalhães T, Costa RC, Zara FJ, Castilho AL (2021) Checklist of decapod crustaceans from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: IV. Infraorder Anomura: Superfamilies Chirostyloidea, Galatheoidea, Hippoidea and Paguroidea. Zootaxa 4965(3): 558–600. https://doi.org/10.11646/zootaxa.4965.3.9

Melo GAS (1999) Manual de identificação dos Crustacea Decapoda do litoral Brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. Ed. Plêiade/FAPESP, São Paulo, 551 pp.

Miller S, Dykes D, Polesky H (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research 16(3): e1215. https://doi.org/10.1093/nar/16.3.1215

Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE). https://doi.org/10.1109/GCE.2010.5676129

Miranda I, Peres P, Tavares MDS, Mantelatto FL (2020) New molecular data on squat lobster from the coast of São Paulo State (Brazil) (Anomura: Munida and Agononida) and insights on the systematics of the Family Munididae. Chapter 14. In: Hendrickx M (Ed.) Deep-Sea Pycnogonids and Crustaceans of the Americas. Springer Nature, Cham, 343–356. https://doi.org/10.1007/978-3-030-58410-8_14

Niazi MS, Haque MM (1974) On a new species of mole-crab (Emerita karachiensis sp. nov.) with a key to common Indo-Pacific species. Records of the Zoological Survey of Pakistan 5: 1–6.

Palumbi SR, Benzie J (1991) Large mitochondrial DNA differences between morphologically similar penaeid shrimp. Molecular Marine Biology and Biotechnology 1: 27–34.

Peres PA, Bracken-Grissom H, Timm LE, Mantelatto FL (2022) Genomic analyses implicate the Amazon–Orinoco Plume as the driver of cryptic speciation in a swimming crab. Genes 13(12): e2263. https://doi.org/10.3390/genes13122263

Pérez D (2003) Mercury levels in mole crabs Hippa cubensis, Emerita brasiliensis, Emerita portoricensis and Lepidopa richmondi (Crustacea: Decapoda: Hippidae) from a sandy beach at Venezuela. Bulletin of Environmental Contamination and Toxicology 63: 320–326. https://doi.org/10.1007/s001289900983

Petracco M, Veloso VG, Cardoso RS (2003) Population dynamics and secondary production of Emerita brasiliensis (Crustacea: Hippidae) at Prainha Beach, Brazil. Marine Ecology (Berlin) 24(3): 231–245. https://doi.org/10.1046/j.0173-9565.2003.00837.x

Richards HG (1968) The tertiary history of the Atlantic coast between Cape Cod and Cape Hatteras. Palaeogeography, Palaeoclimatology, Palaeoecology 5(1): 95–104. https://doi.org/10.1016/0031-0182(68)90063-1

Robles R, Schubart CD, Conde JE, Carmona-Suárez C, Álvarez F, Villalobos JL, Felder DL (2007) Molecular phylogeny of the American Callinectes Stimpson, 1860 (Brachyura: Portunidae), based on two partial mitochondrial genes. Marine Biology 150(6): 1265–1274. https://doi.org/10.1007/s00227-006-0437-7

Rodgers JA (1987) The foraging behavior of gray gulls at a sandy beach. The Wilson Bulletin 99: 271–273.

Scheineider-Broussard R, Felder DL, Chlan CA, Neigel JE (1998) Tests of phylogeographic models with nuclear and mitochondrial DNA sequences variation in stone crabs, Menippe adina and Menippe mercenaria. Evolution; International Journal of Organic Evolution 52(6): 1671–1678. https://doi.org/10.2307/2411339

Schmitt WL (1935) Crustacea Macrura and Anomura of Porto Rico and the Virgin Islands. Scientific Survey of Puerto Rico and the Virgin Islands, New York Academy of Science 15(2): 125–227. https://doi.org/10.5962/bhl.title.10217

Schmitt WL (1937) A new species of Emerita (Crustacea) from South Africa. Annals of the South African Museum 32: 25–29. [pl. 3.]

Schubart CD, Neigel JE, Felder DL (2000) Use of the mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. Crustacean Issues 12: 817–830.

Siddiqi FA, Ghory FS (2006) Complete larval development of Emerita holthuisi Sankolli, 1965 (Crustacea: Decapoda: Hippidae) reared in the laboratory. Turkish Journal of Zoology 30: 121–135.

Snodgrass RE (1952) The sand crab Emerita talpoida (Say) and some of its relatives. Smithsonian Miscellaneous Collections 117(8): 1–34.

Spivak ED, Farías NE, Ocampo EH, Lovrich GA, Luppi TA (2019) Annotated catalogue and bibliography of marine and estuarine shrimps, lobsters, crabs and their allies (Crustacea: Decapoda) of Argentina and Uruguay (Southwestern Atlantic Ocean). Frente Marítimo 26: 1–164.

Stanley SM (1986) Anatomy of a regional mass extinction: Plio-Pleistocene decimation of western Atlantic bivalve fauna. Palaios 1(1): 17–36. https://doi.org/10.2307/3514456

Tam YK, Kornfield I, Ojeda FP (1996) Divergence and zoogeography of mole crabs, Emerita spp. (Decapoda: Hippidae) in the Americas. Marine Biology 125(3): 489–497. https://doi.org/10.1007/BF00353262

Terossi M, Almeida AO, Mantelatto FL (2019) Morphology and DNA data reveal a new shrimp species of genus Latreutes Stimpson, 1860 (Decapoda: Hippolytidae) from the western Atlantic. Zoological Science 36(5): 440–447. https://doi.org/10.2108/zs190016

Timm L, Bracken-Grissom HD (2015) The forest for the trees: Evaluating molecular phylogenies with an emphasis on higher-level Decapoda. Journal of Crustacean Biology 35(5): 577–592. https://doi.org/10.1163/1937240X-00002371

Veloso VG, Cardoso RS (1999) Population biology of the mole crab Emerita brasiliensis (Decapoda: Hippidae) at Fora Beach, Brazil. Journal of Crustacean Biology 19(1): 147–153. https://doi.org/10.1163/193724099X00349

WoRMS (2023) Hippoidea Latreille, 1825. World Register of Marine Species. https://www.marinespecies.org/aphia.php?p=taxdetails&id=106686 [Accessed 23 Feb 2023]

﻿Abstract

Keywords

﻿Introduction

﻿Materials and methods

﻿Sample collection and morphological data

﻿Abbreviations

﻿Brazilian states

﻿Molecular data

﻿Results

﻿Molecular data

﻿16S rRNA reconstruction

﻿Cytochrome Oxidase I (COI) reconstruction

﻿Concatenated phylogram

﻿Taxonomy

﻿Superfamily Hippoidea Latreille, 1825

﻿ Emerita almeidai Mantelatto & Balbino, sp. nov.

Type material

Additional material

Comparative material

Diagnosis

Description

Coloration in life

Habitat

Distribution

Etymology

Remarks

﻿Discussion

﻿Insights on the evolution of the genus

﻿Acknowledgements

﻿References

Abstract

Introduction

Materials and methods

Sample collection and morphological data

Abbreviations

Brazilian states

Molecular data

Results

Molecular data

16S rRNA reconstruction

Cytochrome Oxidase I (COI) reconstruction

Concatenated phylogram

Taxonomy

Superfamily Hippoidea Latreille, 1825

Emerita almeidai Mantelatto & Balbino, sp. nov.

Discussion

Insights on the evolution of the genus

Acknowledgements

References