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ZOOTAXA

ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)Copyright © 2015 Magnolia Press

Zootaxa 3925 (4): 536–550

www.mapress.com/zootaxa/Article

http://dx.doi.org/10.11646/zootaxa.3925.4.3

http://zoobank.org/urn:lsid:zoobank.org:pub:F02FAC72-AD74-496D-9811-B8B4313A783E

A new species of Haliclona (Demospongiae: Haplosclerida: Chalinidae)

from southeastern Brazil and the first record of Haliclona vansoesti from

the Brazilian coast

GUILHERME MURICY1,4, EDUARDO L. ESTEVES2, LEANDRO C. MONTEIRO1,

BEATRIZ ROMA RODRIGUES2 & RODOLPHO M. ALBANO3

1Departamento de Invertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro. Quinta da Boa Vista, s/no, São Cris-

tóvão. 20940-040 Rio de Janeiro, RJ, Brazil2Departamento de Zoologia, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro. Rua São

Francisco Xavier, 524, PHLC, 5º andar, sala 520. 20550-013 Rio de Janeiro, RJ, Brazil3Departamento de Bioquímica, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro. Boulevard

Vinte e Oito de Setembro, 87, fundos, 4º andar, 20551-013 Rio de Janeiro, RJ, Brazil4Corresponding author. E-mail: [email protected]

Abstract

In this paper we describe two species of the cosmopolitan sponge genus Haliclona from Rio de Janeiro State, SE Brazil,

one of which is new to science and the other a new record to Brazil. Haliclona (Rhizoniera) fugidia sp. nov. is brownish-

pink, salmon or cream, thickly encrusting, without oscular tubes and tangential ectosomal reticulation. Choanosomal skel-

eton is a mostly unispicular ladder-like reticulation of oxeas, very organized near the sponge surface and denser and more

disorganized in the interior of the sponge. Haliclona (Halichoclona) vansoesti de Weerdt et al., 1999 was originally de-

scribed from the Caribbean. It has a very loose connection between ectosome and choanosome, a whitish translucent ec-

tosome combined with a purplish choanosome, a cavernous structure and a friable or crispy consistency. The

conspecificity of SE Brazilian and Caribbean populations of H. (Halich.) vansoesti was verified through phylogenetic

analysis of small subunit 18S rRNA (18S) and mitochondrial cytochrome oxidase subunit I (COI) gene sequences. A max-

imum likelihood phylogenetic tree constructed with 18S sequences indicates that specimens of H. (Halich.) vansoesti from

Rio de Janeiro were phylogenetically closer to the same species from the Caribbean than to other species of Haliclona.

Although not available for H. (Halich.) vansoesti from the Caribbean, COI sequences of our specimens were also quite

distinct from those of other Haliclona species. Molecular identification based on DNA sequences is a useful complement

to traditional morphology-based taxonomy, especially in highly plastic sponges such as Haliclona spp. and other haplo-

sclerids.

Key words: taxonomy, Haploscleromorpha, molecular systematics, COI, 18S rRNA, southwestern Atlantic

Introduction

Haplosclerida is one of the main orders of Demospongiae, rivalling with Poecilosclerida in number of species. This

diversity, however, is often hidden by the paucity of useful morphological characters for the taxonomy of the order,

which, for the taxonomist, is one of the most challenging among the Porifera (de Weerdt, 2002). The genus

Haliclona Grant, 1836 (family Chalinidae) is the most diverse of the phylum Porifera, with over 420 currently

accepted species (van Soest et al., 2014). Haliclona, together with other haplosclerids, may represent one of the

richest taxonomic groups of Porifera in Brazil, particularly in the shallow reefs, rocky shores and tropical bays in

the northeast (e.g. Hajdu et al., 2011) and southeast Brazilian coast (Muricy & Ribeiro, 1999). In spite of this high

diversity, only 13 species of Haliclona are known to occur in Brazil (Hajdu et al., 2011; Muricy et al., 2011; Bispo

et al., 2014; Sandes et al., 2014).

Taxonomic studies on Brazilian Haliclona focused mainly on the description of new species by Mothes &

Lerner (1994), Muricy & Ribeiro (1999), Campos et al. (2005), Bispo et al. (2014) and Sandes et al. (2014). Other

536 Accepted by J. Hooper: 29 Jan. 2015; published: 3 Mar. 2015

records of the genus in Brazil were made in illustrated guides (Mothes et al., 2003; Muricy & Hajdu, 2006; Hajdu

et al., 2011), taxonomic inventories or ecological studies (e.g. Lerner, 1996; Vilanova et al., 2004; Cedro et al.,

2007; Correia & Sovierzoski, 2010) and in experiments on cell biology and pharmacology (Custodio et al., 2002;

Dresch et al., 2005; Silva et al., 2006). Several records of the genus all along the Brazilian coast remain

unidentified (Muricy et al., 2011).

The diversity of Brazilian Haliclona is best known in the northeast region (Alagoas, Sergipe and Bahia States),

where seven species were identified (Hajdu et al., 2011; Bispo et al., 2014; Sandes et al., 2014), followed by the

south region (Santa Catarina State), with three species (Mothes & Lerner, 1994; Lerner, 1996). In the southeast

coast of Brazil there was a single species recorded to the present, H. (Soestella) melana Muricy & Ribeiro, 1999,

from Angra dos Reis, Parati (Rio de Janeiro State) and São Sebastião (São Paulo State) (Muricy et al., 2011).

In this study we describe two species of Haliclona from Rio de Janeiro State, Southeast Brazil, one of which is

new to science (subgenus Rhizoniera) and the other is the first record of Haliclona (Halichoclona) vansoesti de

Weerdt et al., 1999 in Brazil. In addition, we provide new small subunit 18S rRNA and the first cytochrome

oxidase subunit I (COI) gene sequences of H. (Halich.) vansoesti to verify the conspecificity of disjunct Brazilian

and Caribbean populations and to facilitate future molecular-based identification of the species through DNA

barcoding.

Material and methods

Taxonomy and morphology. Collections were made by SCUBA diving in shallow waters (max. 20 m depth) in

Cagarras Archipelago, Rasa Island, Vermelha Beach (Rio de Janeiro) and Maricás Archipelago (Maricá) in 2010

and 2012 (all in Rio de Janeiro State; Figure 1). Specimens were photographed in situ before collection and fixed in

70 or 80% ethanol. Underwater observations and photographs without collection were taken in Grande Island

(Angra dos Reis) and Franceses Island (Arraial do Cabo). The type specimens of Haliclona (Rhizoniera) fugidia

sp. nov. were deposited in the Porifera Collection of Museu Nacional, Universidade Federal do Rio de Janeiro,

Brazil (MNRJ). The specimens of H. (Halich.) vansoesti were deposited in MNRJ and in the Porifera Collection of

Universidade do Estado do Rio de Janeiro, Brazil (UERJPOR). Transverse sections were taken from specimens

embedded in paraffin for observation of the skeleton. Tangential sections were made directly in wet or dry

preserved specimens to describe the ectosomal skeleton. Spicule preparations were made with nitric acid. For each

spicule type we measured 30 spicules per specimen, except when noted otherwise. Dissociated spicules were

observed with Light Microscopy (LM) and under Scanning Electron Microscopy (SEM) in the "Centro de

Microscopia Eletrônica do Departamento de Invertebrados do Museu Nacional", Universidade Federal do Rio de

Janeiro. Classification follows the Chalinidae chapter in the Systema Porifera (de Weerdt, 2002).

DNA extraction and sequencing. Subsamples of specimens of H. (Halich.) vansoesti were placed in RNA

Later in the field for molecular analysis. Collected specimens of H. (Rhiz.) fugidia sp. nov. were fixed in ethanol

70% only. DNA was extracted with AllPrep DNA/RNA Mini kit (Qiagen) following the manufacturer’s

recommendations. Sponge DNA was used to amplify the small subunit 18S rRNA gene using primers 1F18S

(AAC CTG GTT GAT CCT GCC AGT) and 1800R18S (GTT CAC CTA CYG AAA CCT TGT T), following the

same amplification conditions described by Redmond et al. (2007). PCR products were purified, sequenced and

consensus contigs were assembled as described below. BLAST searches against GenBank database were

performed to determine sequence identity and similarity and to select reference sequences for a phylogenetic

analysis. The nucleotide sequences for the small subunit 18S rRNA gene of H. (Halich.) vansoesti samples

UERJPOR10, UERJPOR30 and UERJPOR34 were deposited in GenBank with accession numbers KM191356,

KM191357 and KM191358, respectively.

A 640 bp long fragment of the mitochondrial cytochrome oxidase subunit I (COI) gene was PCR amplified

with the primers and conditions described in Meyer et al. (2005): dgLCO1490 (GGT CAA CAA ATC ATA AAG

AYA TYG G) and dgHCO2198 (TAA ACT TCA GGG TGA CCA AAR AAY CA). PCR fragments were purified

by the Illustra GFX PCR DNA and Gel Band Purification Kit (GE Lifesciences, Brazil), sequenced with the

BigDye terminator v3.1 sequencing kit and analyzed on a AB3500 genetic analyzer system (Applied Biosystems,

Foster City, CA). Quadruplicate reactions in both directions were used to construct consensus contigs for each

sample by Geneious assembler (Geneious, Biomatters). COI sequences of H. (Halich.) vansoesti samples were

Zootaxa 3925 (4) © 2015 Magnolia Press · 537HALICLONA FROM RIO DE JANEIRO

deposited in GenBank with accession numbers KM203834, KM203835 and KM203836 for UERJPOR10,

UERJPOR30 and UERJPOR34, respectively. The DNA obtained from H. (Rhiz.) fugidia sp. nov. was too degraded

to allow amplification of the 18S and COI genes.

Phylogenetic analysis. Sequences were aligned with MAFFT (Katoh & Standley, 2013) and a maximum

likelihood (ML) phylogenetic tree was constructed with MEGA 5.0 (Tamura et al., 2011) under the general time

reversible model and 1000 bootstrap permutations. An attempt to reconstruct recently published phylogenetic

relationships for the marine Haplosclerida (= Haploscleromorpha sensu Redmond et al., 2013) was made with

sequences representative of the clades described in Redmond et al. (2011, 2013). For this, small subunit 18S

ribosomal RNA and COI sequences of different haploscleromorphs, including several Haliclona species, were

downloaded from GenBank and used to build the trees. Halisarca restingaensis Alvizu et al., 2013 (KC902130)

18S ribosomal RNA and Baikalospongia intermedia Dybowsky, 1880 (EU000567) COI gene sequences were used

as outgroups for the phylogenetic trees.

FIGURE 1. Location of sites of collection and observation of Haliclona (Halichoclona) vansoesti (asterisks) and Haliclona

(Rhizoniera) fugidia sp. nov. (black circle in D) in Rio de Janeiro State, southeastern Brazil. A, South America showing Brazil and Rio de Janeiro State (B) in the inset. B, Rio de Janeiro State showing location of Grande Island (C), Rio de Janeiro (D), and Franceses Island in Arraial do Cabo (asterisk). C, location of Dois Rios Inlet at Grande Island (asterisk). D, Rio de Janeiro and Niterói with location of Vermelha Beach (1, black circle), Tijucas Archipelago (2), Cagarras Archipelago s.l., including Redonda and Rasa Islands (3), and Maricás Archipelago (4).

Results

Systematics

Class Demospongiae Sollas, 1885

MURICY ET AL. 538 · Zootaxa 3925 (4) © 2015 Magnolia Press

Order Haplosclerida Topsent, 1928

Suborder Haplosclerina Topsent, 1928

Family Chalinidae Gray, 1867

Definition. Haplosclerina with a delicate reticulate choanosomal skeleton of uni-, pauci- or multispicular primary

lines, which are regularly connected by unispicular secondary lines. Ectosomal skeleton, if present, a regularly

hexagonal, unispicular, tangential reticulation (de Weerdt, 2002).

Genus Haliclona Grant, 1836

Definition. Chalinidae with unispicular secondary lines (de Weerdt, 2002). Type species: Spongia oculata Pallas,

1766.

Subgenus Rhizoniera Griessinger, 1971

Definition. Chalinidae with an anisotropic, ladder-like choanosomal skeleton consisting of uni- multispicular

ascending primary lines, connected by irregular unispicular secondary lines. Ectosomal skeleton usually absent; if

present, consisting only of some vaguely strewn tangentially orientated oxeas. Spongin moderate to absent.

Megascleres usually slender oxeas with acerated points. No microscleres (emmended from de Weerdt, 2002). Type

species: Reniera rhizophora Vacelet, 1969.

Haliclona (Rhizoniera) fugidia sp. nov.

(Figure 2; Table 1)

Diagnosis. Haliclona (Rhizoniera) brownish-pink to salmon in color, thickly encrusting, without oscular tubes and

without tangential ectosomal reticulation. The ectosomal skeleton is absent and the surface is thin, translucent and

pierced by abundant pores, clearly visible in LM. The choanosomal skeleton is a uni- to paucispicular, ladder-like

reticulation of oxeas with low spongin, more organized near the sponge surface and denser and more disorganized,

sub-halichondrioid in the interior of the sponge. Oxeas fusiform, acerate, 86–124 µm in length. Microscleres

absent.

Material examined. Holotype: MNRJ 16846, Vermelha Beach, Rio de Janeiro, 4 m depth, coll. Jessica Pinho

& Guilherme Muricy, July 7, 2013. Paratype: MNRJ 16860-B, collection data as for the holotype.

Description (Fig. 2A). Shape thickly encrusting to massive, irregular, 3‒8 cm wide by 1‒2 cm thick. Color

brownish pink to light salmon in vivo, becoming cream to light brown after fixation. Oscules circular, randomly

dispersed, with slightly elevated rims, 1‒3 mm in diameter. Surface irregular, uneven, with a few superficial

channels. Consistency compressible, slightly elastic.

Skeleton: Ectosome without tangential ectosomal reticulation. The ectosomal skeleton is absent and the

surface is lightly reinforced by spongin, with dispersed debris and only few oxeas at the extremities of the

choanosomal primary tracts, which slightly surpass the surface (Fig. 2B–C). Pores abundant, closely spaced,

clearly visible on the surface, 20‒60 µm in diameter (Fig. 2C). Subectosomal and choanosomal lacunae common.

Choanosomal skeleton formed by a ladder-like reticulation of uni- to paucispicular tracts of oxeas, connected by

irregular unispicular secondary lines, forming irregular or rectangular meshes 60‒150 µm wide (Fig. 2B, D‒E).

The amount of spongin is low and there is no fibre development in both primary and secondary lines. The

reticulation is more organized and ladder-like near the surface and becomes denser and more disorganized towards

the choanosome (Fig. 2D–E).

Spicules: oxeas smooth, fusiform, slightly curved, with acerate tips: 78.2–105.2 (± 11.0)–126.1 µm in length

by 1.3–3.6 (± 0.9)–5.5 µm in width (Table 1, Fig. 2F).


TABLE 1. Spicule measurements (oxeas length and width in µm) of the type specimens of Haliclona (Rhizoniera)

fugidia sp. nov. from Rio de Janeiro State, SE Brazil. Measurements are expressed as minimum–average (± standard

deviation)–maximum. N = 30.

FIGURE 2. Haliclona (Rhizoniera) fugidia sp. nov. A, holotype MNRJ 16846 in vivo. B, transverse section of the ectosome (surface at the top). C, tangential section of the ectosome. D, E, transverse sections through choanosome and ectosome (surface at the top). F, oxeas (SEM). G, embryos. A–C, E–G, MNRJ 16846; D, MNRJ 16860-B.

Ecology. Haliclona (Rhiz.) fugidia sp. nov. appears to be very rare in Rio de Janeiro, being found so far only at

Vermelha Beach, on vertical surfaces near the sandy bottom between 4‒8 m depth. It is very difficult to find,

camouflaged near the rocky/sand interface and covered with sediment and epibionts. It can be easily mistaken

underwater for Pachychalina alcaloidifera Pinheiro et al., 2005, which it resembles externally.

Reproduction. Spherical to ovoid embryos 200‒430 µm in diameter were found in the two specimens, both

collected in July 2013 (Fig. 2G).

Distribution. Provisionally endemic to Rio de Janeiro, SE Brazil, where it is known from a single location

(Vermelha Beach).

Etymology. The name fugidia comes from Latin fugitīvu, meaning "fugitive", "elusive", due to the great

difficulty in finding the species in the field.

Taxonomic remarks. Haliclona is one of the most diverse genera of Porifera, with over 420 currently

accepted species (van Soest et al., 2014). It is divided in six subgenera (Gellius, Halichoclona, Haliclona, Reniera,

Rhizoniera, and Soestella; de Weerdt, 2002), but 218 species are not allocated to any subgenus in the World

Porifera Database so far (WPD; van Soest et al., 2014, accessed in December 1, 2014). It is challenging to classify

our new species from Rio de Janeiro into these subgenera, because its skeleton does not fit precisely in any of them.

It clearly differs from subgenera H. (Reniera) and H. (Halichoclona), which have (sub)isotropic choanosomal

skeletons without well-defined primary lines (de Weerdt, 2000, 2002), and from the subgenus H. (Soestella), in

which the choanosomal skeleton is sub-anisotropic, with irregular, ill-defined choanosomal primary lines and

paucispicular secondary lines, and there is a tendency to form rounded meshes in the ectosome (de Weerdt, 2002).

The new species is closer to the subgenera H. (Haliclona), H. (Gellius) and H. (Rhizoniera) in the presence of

an anisotropic reticulation with clearly defined ascending primary lines and unispicular connecting secondary lines.

Specimen Length Width

MNRJ 16846 86.4–108.6 (± 8.7)–123.5 1.3–3.5 (± 1.1)–5.5

MNRJ 16860-B 78.2–101.8 (± 11.7)–126.1 2.5–3.6 (± 0.7)–5.1


However, in Haliclona the reticulation is very regular throughout the choanosome, regularly connected by

unispicular secondary lines and with moderate to abundant spongin. The oxeas are usually short and stout, cigar-

shaped. The secondary lines of the new species seem to be more irregular and in the deeper choanosome the

reticulation is very irregular, sub-halichondrioid, more similar to that of H. (Gellius). One of the main characters

leading to H. (Gellius) in the key to the subgenera of Haliclona proposed by de Weerdt (2002) is that the

choanosomal anisotropic reticulation becomes more disorganized and sub-halichondrioid from the surface towards

the interior of the sponge, similarly to that of the new species. This character however is not mentioned any further

in the Systema Porifera chapter, neither in the subgenus diagnosis and definition nor in the redescription of the type

species (de Weerdt, 2002). Nevertheless, a transition from a more or less regular anisotropic reticulation near the

ectosome to an irregular sub-halichondrioid reticulation deep inside the choanosome is present in at least some

species of the subgenus H. (Gellius), including H. (Gell.) angulata (Bowerbank, 1866), H. (Gell.) rava (Stephens,

1902), and the type species H. (Gell.) fibulata (Schmidt, 1862). In the subgenus H. (Gellius), however, the oxeas

are usually very large (160–1000 µm, more often 300–500 µm long) and microscleres are often present in the form

of sigmas and toxas, while H. (Rhiz.) fugidia sp. nov. has small oxeas (86–124 µm long) and no microscleres. In

the subgenus H. (Rhizoniera) the primary lines are usually pauci- to multispicular with scarce spongin, whereas in

the new species they are uni- to paucispicular with moderate to low amount of spongin. As in the new species, in

the subgenus H. (Rhizoniera) the microscleres are absent, megascleres are slender, relatively small oxeas, the

choanosomal meshes are irregular, and the ectosomal tangential skeleton is usually absent. Also, in some species

the choanosomal skeleton becomes more disorganized towards the base of the sponge (e.g., Haliclona (Rhiz.)

viscosa (Topsent, 1888); cf. de Weerdt, 1986). Therefore, it was with hesitation that we decided to allocate the new

species in the subgenus Haliclona (Rhizoniera). We made small emmendments in the subgenus definition to

accomodate the new species. It is clear, however, that the current subgeneric classification of the genus Haliclona

must be improved. Recent phylogenetic analysis based on 28S and 18S rDNA sequences (McCormack et al., 2002;

Redmond et al., 2007, 2013) indicate that the family Chalinidae, the genus Haliclona and most of its subgenera are

all probably non-monophyletic. Therefore, below we will compare the new species not only to those of the

subgenus H. (Rhizoniera), but to all 34 species of Haliclona currently known from the Tropical Western Atlantic,

most of which were tabulated by Bispo et al. (2014).

Van Soest et al. (2014) list 83 valid species in the subgenus Haliclona (Gellius), of which only three occur in

the TWA. Haliclona (Gell.) calcinea (Burton, 1954) from 720–800 m depth in Grenada is massive rounded, dark

brown in spirit; H. (Gell.) megasclera Lehnert & van Soest (1996) from 78 m depth in Jamaica is massive, grey,

and agglutinates Halimeda leaves; and H. (Gell.) tenerrima Burton, 1954 from 3.5 m depth in Belize was described

from a fragment, pale yellow in spirit. The oxea of the three species are much larger than in the new species (500 x

16 µm, 282–370 x 9–12 µm and 280 x 7 µm, respectively). Two of them also have microscleres: H. (Gell.) calcinea

has sigmas and toxas and H. (Gell.) tenerrima has toxas. H. (Gell.) megasclera has raphid-like growth stages of the

oxea (Lehnert & van Soest, 1996), which are absent in the new species.

Seven species of the subgenus H. (Halichoclona) are known from the TWA: H. (Halich.) albifragilis (Hechtel,

1965), from Florida, Barbados, Venezuela, Jamaica, Bonaire and Curaçao, is well characterized by the combination

of an opaque white color, friable consistency and slender oxea (de Weerdt, 2000). H. (Halich.) dura Sandes et al.,

2014 from Sergipe State, NE Brazil, is thick encrusting, dark brown, and has a hard, incompressible consistency. H.

(Halich.) lernerae Campos et al., 2005 from 94 m depth at the North Brazilian continental shelf is massive with

tube-like projections. H. (Halich.) magnifica de Weerdt et al., 1991 from Belize, Florida and Puerto Rico has a

massive base from which arise thick walled tubes. H. (Halich.) perforata (Pulitzer-Finali, 1986) from Puerto Rico

has a tangential ectosomal reticulation of unispicular tracts. H. (Halich.) stoneae de Weerdt, 2000 form thick

cushions with large oscules and has a subisotropic tangential ectosomal reticulation with paucispicular tracts. H.

(Halich.) vansoesti de Weerdt et al., 1999 has a whitish ectosome and a violet to pink choanosome, and the oscules

are placed on top of short tubular projections. All these species further differ from the new species by the

subisotropic choanosomal reticulation, without well-defined primary lines, and by the detachable ectosome

separated from the choanosome by large subdermal cavities, typical of the subgenus (de Weerdt, 2002).

Twenty-three species are currently accepted in the subgenus H. (Haliclona) in the World Porifera Database, of

which only one occurs in the Tropical Western Atlantic (cf. de Weerdt, 2000; van Soest et al., 2014): H. (Halicl.)

epiphytica Zea & de Weerdt, 1999 from the Colombian Caribbean forms cream-colored, thin incrustations (0.1–1.1

cm thick), exclusively epibiotic on seaweeds, has a tangential ectosomal reticulation, and has thick, short oxeas


(63–97 µm long; Zea & de Weerdt, 1999; de Weerdt, 2000). Although not allocated to any subgenera by the WPD

(van Soest et al., 2014), two other species from Southern Brazil have been included in the subgenus Haliclona due

to their ladder-like reticulate skeleton with unispicular secondary lines: H. (Halicl.) catarinensis Mothes & Lerner,

1994 and H. (Halicl.) lilaceus Mothes & Lerner, 1994 (cf. Muricy et al., 2011; Bispo et al., 2014). H. (Halicl.)

catarinensis differs from H. (Rhiz.) fugidia sp. nov. by the orange-gray color, the absence of superficial canals,

subectosomal and choanosomal lacunae, the multispicular ascending spicule tracts (vs. uni- to paucispicular tracts

in the new species), and the larger oxeas (111‒161/3‒9 vs. 86‒124/1‒6 µm). H. (Halicl.) lilaceus is distinguishable

by its violet color, thin encrusting shape (1 mm thick), microconulose surface, and multispicular ascending tracts

(Mothes & Lerner, 1994). These two species from S Brazil need revision for a more detailed description of their

skeleton and external morphology.

The subgenus H. (Reniera) is represented in TWA by eight species. H. (Ren.) chlorilla Bispo et al., 2014 from NE

Brazil forms delicate, anastomosing branches, dark green to black in color. H. (Ren.) implexiformis (Hechtel, 1965),

widely distributed in the Caribbean, is bright violet-pink. H. (Ren.) manglaris Alcolado, 1984, known from several

Caribbean localities and also from NE Brazil, is green or bright turquoise-green and form laterally spreading sheets

with low volcano-shaped elevations. H. (Ren.) mucifibrosa de Weerdt et al., 1991 from Belize, Florida, Colombia and

Jamaica is greyish purple to bluish gray, has an irregularly massive base and short thick-walled oscular chimneys. H.

(Ren.) portroyalensis Jackson et al., 2006 from Jamaica is purple and digitate. H. (Ren.) ruetzleri de Weerdt, 2000

from Belize is light brown, with extremely delicate, slender anastomosing branches. H. (Ren.) strongylophora Lehnert

& van Soest, 1996 from Jamaica is encrusting, dark brown, and its megascleres are strongyles. H. (Ren.) tubifera

(George & Wilson, 1919), known from the Caribbean to North Carolina, has abundant volcano- or chimney-shaped

oscular elevations. All these species are easily distinguishable from the new species by the (sub)isotropic

choanosomal reticulation, without well-defined primary lines, typical of the subgenus H. (Reniera).

The subgenus H. (Soestella) has 21 species, of which 11 occur in TWA: H. (Soest.) brassica Sandes et al., 2014

from NE Brazil is lamellate and its spicules are strongyles and raphides. H. (Soest.) caerulea (Hechtel, 1965) is

widely distributed from the Caribbean to Bahia State, NE Brazil (Hajdu et al., 2011); it usually forms irregular

cushions with thin digitations ranging from yellowish green to light blue in color and has sigmas. H. (Soest.)

lehnerti de Weerdt, 2000 from Jamaica is dark red and has conspicuous aquiferous canals at the surface. H. (Soest.)

luciensis de Weerdt, 2000 from Santa Lucia is dark brown and has raphides. H. (Soest.) melana Muricy & Ribeiro,

1999 from Santa Lucia and Brazil is black and has toxas. H. (Soest.) piscaderensis (van Soest, 1980) from Jamaica

and Curaçao is greyish yellow to light purplish brown and has sigmas. H. (Soest.) peixinhoae Bispo et al., 2014

from Bahia State, NE Brazil, forms dense aggregations of erect tubes with slender torn-like projections. H. (Soest.)

smithae de Weerdt, 2000 form yellow-green oscular mounds and has raphides. H. (Soest.) twincayensis de Weerdt

et al., 1991, from Belize, Florida, Guadeloupe and Venezuela, forms slender branches, whitish grey to pink in vivo.

H. (Soest.) vermeuleni de Weerdt, 2000 from E Caribbean to North Carolina is blue and forms small outgrowths

(oscular chimneys, blind digitations, and lobes). H. (Soest.) walentinae Diaz et al., 2007 from Panama is thinly

encrusting, dark brown to purple externally and tan internally. All these species further differ from the new species

by the irregular primary lines with a tendency to form rounded meshes both in the choanosomal and ectosomal

skeletons, typical of the subgenus H. (Soestella) (de Weerdt, 2002).

The subgenus H. (Rhizoniera) has 17 valid species, of which only two are currently recognized from TWA: H.

(Rhiz.) curacaoensis (van Soest, 1980) from Curaçao, Belize, South Carolina, Florida and Grenadines and H.

(Rhiz.) mammillaris Mothes & Lerner, 1994 from South Brazil. Although these are the species most similar to H.

(Rhiz.) fugidia sp. nov., both clearly differ from it in external morphology: H. (Rhiz.) curacaoensis is bluish-purple

and has an encrusting base with closely-packed oscular mounds; H. (Rhiz.) mammillaris is encrusting, white in

spirit, and its oscules are located on top of mamiliform projections. Other five species of H. (Rhizoniera) occur in

other regions in the Atlantic: H. (Rhiz.) canaliculata Hartman, 1958 from the NW Atlantic (Connecticut), is thinly

encrusting, has a ridged surface, multispicular primary lines and multispicular "horizontal" spicule tracts (cf.

Hartman, 1958). H. (Rhiz.) indistincta (Bowerbank, 1866) from NE Atlantic is greenish-brown. H. (Rhiz.)

pedunculata Boury-Esnault et al., 1994 from Alboran Sea is stipitate and has two categories of sigmas. H. (Rhiz.)

rosea (Bowerbank, 1866) from NE Atlantic has somewhat wavy primary lines and rather long oxeas (150–220 µm

long; de Weerdt, 1986). Finally, H. (Rhiz.) viscosa (Topsent, 1888) from NE Atlantic and Mediterranean is greyish-

purple verging to yellow towards the base, has chimney- or volcano-shaped osculiferous elevations and is

extremely slimy (cf. de Weerdt, 1986).


Subgenus Halichoclona Schmidt, 1862

Diagnosis. Chalinidae with a choanosomal skeleton consisting of a subisotropic, somewhat confused reticulation,

commonly intercepted by many choanosomal spaces. Ectosomal skeleton of the same structure as the choanosome,

usually very loosely overlaying the choanosome, from which it may be separated by extensive subectosomal

spaces. Spongin absent or very scarce, at the nodes of the spicules. Megascleres usually acerate or hastate oxeas.

Microscleres, if present, microxeas or sigmas. Sponges commonly relatively crisp and brittle, only slightly

compressible (de Weerdt, 2002). Type species: Halichoclona gellindra de Laubenfels, 1932.

Haliclona (Halichoclona) vansoesti de Weerdt, de Kluijver & Gomez, 1999

(Figures 3‒4; Table 2)

Synonyms: Haliclona (Halichoclona) vansoesti de Weerdt, de Kluijver & Gomez, 1999: 49; de Weerdt, 2000: 49; Valderrama & Zea, 2013:

372; Rützler et al., 2014: 80.Haliclona (Halichoclona) sp., Monteiro & Muricy, 2004: 683.

Diagnosis. Haliclona (Halichoclona) with a very loose connection between ectosome and choanosome, a whitish

or cream translucent ectosome combined with a purplish or violet to pink, lavender, or light salmon choanosome, a

cavernous structure and a friable or crisp consistency. Microscleres absent.

FIGURE 3. Haliclona (Halichoclona) vansoesti. A‒H, specimens in vivo showing variation in color and shape; I, detail of the oscular tubes. H was photographed without artificial illumination at approximately 10 m depth. Scale bars show approximate values.


FIGURE 4. Haliclona (Halichoclona) vansoesti. A‒C, preserved specimens (A, UERJPOR 06; B, MNRJ 8981; C, MNRJ 3863). D, tangential section of the ectosome (MNRJ 3863). E, transverse section of the ectosome showing subectosomal lacunae (surface at the top; UERJPOR 06). F, transverse section through choanosome and ectosome (surface at the top; MNRJ 3863). G, oxea (UERJPOR 06).

Material examined. MNRJ 3809, Palmas Island, S shore, Rio de Janeiro, between 6–12 m depth, coll. E.

Vilanova, G. Muricy, L. Monteiro, January 11, 2001. MNRJ 3863, Cagarra Islet, NE shore, Rio de Janeiro, between

6–12 m depth, coll. E. Vilanova, G. Muricy, L. Monteiro, January 11, 2001. MNRJ 3915, Cagarra Island, S shore,

Rio de Janeiro, coll. L. Monteiro, February 1, 2001. MNRJ 8981, Rasa Island, W shore ("Portinho"), Rio de

Janeiro, 10 m depth, coll. L. Monteiro, February 23, 2005. UERJPOR 6, 9, 10, 12, 15, 30 and 34, Maricás

Archipelago, 10‒12 m depth, colls. E. L. Esteves & B. Condor, February 14, 2013.

Description (Figs. 3A‒I, 4A‒C): Shape thickly encrusting, very irregular, up to 25 cm wide by 1‒3 cm thick,

with abundant, short tube-shaped projections 2‒30 mm high topped by circular oscules 2‒10 mm in diameter (Fig.

3A‒H). Oscular tubes are cylindrical or vulcaniform, with relatively thin walls (0.5‒2.0 mm thick), slightly

translucent (Fig. 3I). Some specimens also present blind fistular projections, which are more irregular, lower and

thinner than the oscular tubes (Fig. 3C‒E). Choanosome color variable from light purple or violet to pink, lavender,

light salmon or cream. The surface is translucent, usually whitish or lighter than the choanosome. Below 10 m

depth and without artificial illumination the sponge looks light blue (Fig. 3H). After fixation it becomes white to

cream (Fig. 4A‒C). Surface irregular, uneven, reticulate, very loosely connected to the choanosome, easily

detachable (Fig. 4C). Consistency friable and fragile, slightly compressible, rather inelastic.

Skeleton: Ectosomal skeleton easily detachable, formed by a slightly disorganized isotropic, predominantly

paucispicular tangential reticulation of oxeas, slightly denser than that of the choanosome (Fig. 4D). Subectosomal

and choanosomal lacunae are common (Fig. 4E–F). Choanosomal skeleton cavernous, formed by a relatively

disorganized isotropic reticulation of oxeas similar to that of the ectosome but mostly unispicular (Fig. 4F).

Amount of spongin very low in both the choanosome and ectosome.

Spicules: oxeas smooth, fusiform, slightly curved, with acerate or hastate tips: 139.1‒175.5 (± 11.1)–217.5 µm

long by 2.4–7.3 (± 1.4)–12.5 µm wide (Table 2, Fig. 4G).


TABLE 2. Spicule measurements (oxeas length and width in µm) of 11 specimens of Haliclona (Halichoclona)

vansoesti from Rio de Janeiro State, SE Brazil. Measurements are expressed as minimum–average (± standard

deviation)–maximum. N = 30.

Ecology. Haliclona (Halich.) vansoesti is one of the most common sponge species on the islands off Rio de

Janeiro State on horizontal and especially on vertical rocky surfaces, mainly between 10‒20 m depth.

Distribution. Curaçao (type locality), Jamaica, St. Vincent, Martinique (de Weerdt et al., 1999), Colombian

Caribbean (Valderrama & Zea, 2013), Belize (Rützler et al., 2014), and Brazil, where it is reported so far only from

Rio de Janeiro State (Monteiro & Muricy, 2004; present study; Fig. 1).

FIGURE 5. Maximum likelihood phylogenetic tree of the Haploscleromorpha based on sequences of the small subunit 18S rRNA gene generated in this study and downloaded from GenBank. Only bootstrap values above 50% are shown. Clades A–E refer to Redmond et al. (2013) fig. 4.

Specimen Length Width

MNRJ 3809 146.4 ‒ 162.8 (± 8.8) ‒ 180.0 4.8 ‒ 7.2 (± 1.5) ‒ 9.6

MNRJ 3863 148.8–168.5 (± 11.3) ‒ 192.0 3.6 ‒ 6.7 (± 1.2) ‒ 9.6

MNRJ 3915 170.4–187.3 (± 6.8)–201.6 7.2–9.4 (± 0.6) ‒ 9.6

MNRJ 8981 144.0–161.4 (± 8.4)–180.0 3.6–6.5 (± 1.3)–9.6

UERJPOR 06 177.2 ‒ 199.0 (± 11.2)–216.6 5.2–8.8 (± 1.9)–12.0

UERJPOR 09 147.0–170.4 (± 12.6) ‒ 195.5 3.5–5.5 (± 1.1)–7.4

UERJPOR 10 156.2–178.8 (± 13.0)–210.3 2.8–6.0 (± 1.8)–10.7

UERJPOR 12 140.4–185.1 (± 20.7)–217.5 3.7–7.6 (± 2.4)–11.2

UERJPOR 15 144.7–172.7 (± 13.8)–195.3 3.7–8.1 (±2.0)–12.5

UERJPOR 30 139.1–158.3 (± 10.8)–176.6 2.6–4.8 (± 1.0)–6.5

UERJPOR 34 181.7 ‒ 189.2 (± 5.1) ‒ 197.2 8.0 ‒ 9.2 (± 0.6)–10.6


FIGURE 6. Maximum likelihood phylogenetic tree of the Haploscleromorpha based on sequences of the COI gene generated in this study and downloaded from GenBank. Only bootstrap values above 50% are shown. Clades A–B refer to Redmond et al.

(2011) fig. 3.

Taxonomic remarks. The specimens from Rio de Janeiro studied here are very similar to Haliclona (Halich.)

vansoesti from the Caribbean identified by de Weerdt. et al. (1999), de Weerdt (2000) and Valderrama & Zea

(2013). They share the four traits considered most characteristic of the species by de Weerdt et al. (1999) and de

Weerdt (2000), and whose combination distinguishes it from all other species of the subgenus: a very loose

connection between ectosome and choanosome, a whitish translucent ectosome combined with a purplish

choanosome, a cavernous structure and a brittle or crisp consistency. They also share the thick encrusting shape,

raised oscules, the general skeletal organization and the shape and size of oxeas. The main differences between

them are the greater variation in shape and color, a more irregular surface, and especially the higher oscular tubes in

Brazilian specimens when compared to those from the Caribbean (2‒30 mm high in Brazil vs. "slightly raised

elevations" in the Caribbean; de Weerdt et al., 1999). We consider these differences as simple intraspecific

variations, because the range of variation of these characters in Brazilian specimens is wider and includes the

typical morphology of Caribbean specimens. On the other hand, H. (Halich.) vansoesti sensu Rützler et al. (2014)

from Bahamas differs from our specimens and from all other records by its black color after fixation in ethanol

instead of a whitish cream color and by its slightly longer oxeas: 160–280 µm long in Rützler et al. (2014)

specimens vs. 140–218 om in Brazilian specimens (present study), 120–221 µm in the original description (de

Weerdt et al., 1999; de Weerdt, 2000), and 166–214 µm in Colombian specimens (Valderrama & Zea, 2013). The

Bahamian specimens studied by Rützler et al. (2014) are thus atypical and may either belong to a sibling species or

represent a case of high intraspecific variation. The conspecificity of the southeastern Brazilian and the typical

Caribbean specimens of H. (Halich.) vansoesti was confirmed through phylogenetic analysis of molecular data (see

below).

Phylogenetic analysis. The maximum likelihood phylogenetic tree based on the small subunit 18S rRNA gene

included three samples of putative H. (Halich.) vansoesti from SE Brazil and representative sequences of each of

the five clades described in a recent molecular phylogenetic analysis of Demospongiae that included marine


Haplosclerida (= Haploscleromorpha; Redmond et al., 2013). It indicates that sequences of the putative H.

(Halich.) vansoesti from SE Brazil form a monophyletic cluster with the same gene sequence from Caribbean

(Panama) specimens of H. (Halich.) vansoesti, with high bootstrap support, falling within phylogenetic clade B of

Redmond et al. (2013) (Fig. 5). BLAST searches also showed that Brazilian samples share 99% nucleotide identity

with this Caribbean species. They were phylogenetically closer to H. (Halich.) vansoesti than to any other species

of Haliclona, further supporting the hypothesis that they belong to the same species. In our analysis we recovered

the same five clades (A–E) found by Redmond et al. (2013), and as in their study H. (Halich.) vansoesti fell within

clade B.

The maximum likelihood phylogenetic tree based on COI sequences included three samples of putative H.

(Halich.) vansoesti from Rio de Janeiro and representative sequences from Redmond et al. (2011) (Fig. 6). In their

analysis, Redmond et al. (2011) described two monophyletic clades for this marker: clade A, composed mainly of

Haliclona and Callyspongia species and clade B, formed by two Haliclona and Callyspongia species and

Amphimedon queenslandica Hooper & van Soest, 2006. In our analysis, the COI sequences for the putative H.

(Halich.) vansoesti from SE Brazil form a monophyletic cluster with high bootstrap support outside these two

clades that does not include any other Haliclona species.

Discussion

In the present study we described a new species of H. (Rhizoniera), a new record of H. (Halichoclona) vansoesti

from Brazil and new sequences of the small subunit 18S rRNA and cytochrome oxidase subunit I genes of H.

(Halich.) vansoesti. Unfortunately, the DNA extracted from the two specimens of H. (Rhiz.) fugidia sp. nov. was

too degraded to allow PCR amplification and could not be used in this study.

The identification and subgeneric classification of H. (Rhiz.) fugidia sp. nov. were based on morphological

characters only and were very difficult due to its atypical skeletal architecture, intermediate between three

subgenera: H. (Gellius), H. (Haliclona) and H. (Rhizoniera). We had to compare the new species with a large

number of species to be confident that it is indeed new, and our proposal of subgeneric allocation is rather tentative.

In contrast, the identification of H. (Halich.) vansoesti was based on both morphological and molecular characters

(two independent gene sequences). The skeletal arrangement of H. (Halich.) vansoesti is typical of subgneus H.

(Halichoclona), relatively homogeneous between populations, and the species is easily distinguishable from other

TWA species by external morphological characters. Small subunit 18S rRNA indicated a very high (99%) genetic

similarity between Brazilian and Caribbean samples of the species. Both 18S rRNA and COI sequences of

Brazilian samples were very different from all other species in GenBank. These results highly increased our

confidence in its identification.

Phylogenetic analysis of small subunit 18S rRNA largely recovered the same five clades (A–E) found by

Redmond et al. (2013), but the relative positions of clades B and E were interchanged. This difference may be due

to a smaller taxonomic sampling or to the use of a single outgroup in our study. As in Redmond et al. (2013)

analysis, our samples of H. (Halich.) vansoesti fell within clade B and formed a group with a sample of H. (Ren.)

tubifera. Our ML phylogenetic tree based on COI sequences recovered the two monophyletic clades described by

Redmond et al. (2011). The Brazilian samples of H. (Halich.) vansoesti clustered with Hemigellius fimbriatus

(Kirkpatrick, 1907) (Niphatidae) outside these two clades, with relatively high bootstrap support (88%). Redmond

et al. (2011) did not include H. fimbriatus in their COI analysis.

Two samples of H. (Ren.) tubifera (George & Wilson, 1919) were distantly related in our 18S rRNA

phylogenetic analysis (Fig. 5). Although the two samples of Callyspongia vaginalis (Lamarck, 1814) appeared

monophyletic in COI analysis (Fig. 6), the genetic distance between them was high, supporting in part the results of

Redmond et al. (2011). A reexamination of the vouchers of these species in GenBank is strongly recommended.

The problem of identical sequences from unrelated taxa, found by Redmond et al. (2011), did not happen in our

analyses.

With the present findings, 15 species of Haliclona can be now recognized in Brazil. Among them, nine (60%)

are provisionally endemic to the Brazilian coast: H. (Rhiz.) fugidia sp. nov.; H. (Halicl.) catarinensis Mothes &

Lerner, 1994; H. (Halicl.) lilaceus Mothes & Lerner, 1994; H. (Rhiz.) mammillaris Mothes & Lerner, 1994; H.

(Halich.) lernerae Campos et al., 2005; H. (Halich.) dura Sandes et al., 2014; H. (Ren.) chlorilla Bispo et al.,


2014; H. (Soest.) peixinhoae Bispo et al., 2014; and H. (Soest.) brassica Sandes et al., 2014. The remaining six

species are also found in the Caribbean: H. (Halich.) vansoesti; H. (Ren.) implexiformis (Hechtel, 1965); H. (Ren.)

manglaris Alcolado, 1984; H. (Ren.) tubifera (George & Wilson, 1919); H. (Soest.) caerulea (Hechtel, 1965); and

H. (Soest.) melana Muricy & Ribeiro, 1999. However, these numbers are significantly underestimated, as many

new records and new species of Haliclona have been described from Brazil in the last few years (Muricy &

Ribeiro, 1999; Hajdu et al., 2011; Bispo et al., 2014; Sandes et al., 2014) and there are still many undescribed and

unidentified records of the genus along the Brazilian coast (Muricy et al., 2011). Further investigations on the

Brazilian Haliclona species are needed to elucidate the real patterns of diversity and distribution of the genus in the

Tropical Western Atlantic.

Acknowledgements

We thank Jessica Pinho, Eduardo Vilanova and Báslavi Condor-Lújan for help with collections and Angélica

Vasques for help with spicule preparations and measurements. We thank ICMBio (Instituto Chico Mendes de

Conservação da Biodiversidade) and INEA (Instituto Estadual do Ambiente) for authorizing collections in the

Marine Protected Areas studied ("Monumento Natural das Ilhas Cagarras" and “Parque Estadual da Ilha Grande”,

respectively). We also thank the “Centro de Microscopia Eletrônica” of Museu Nacional/UFRJ for help with SEM.

The results of this study are part of "Projeto Ilhas do Rio", sponsored by Petrobras through the Program Petrobras

Ambiental. This study was supported by fellowships and grants from CNPq, FAPERJ and Petrobras. The advice of

two anonymous reviewers greatly improved the manuscript.

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