A synopsis of Salvatoria McIntosh, 1885 (Annelida: Syllidae: Exogoninae) from Brazilian coastal and oceanic waters

We compiled the records for the genus Salvatoria from Brazilian coastal and oceanic habitats, collected by several projects along the years. Here we present 12 species, eight of which already reported–S. breviarticulata comb. nov., S. clavata, S. euritmica, S. heterocirra, S. limbata, S. longiarticulata comb. nov., S. neapolitana and S. cf. nitidula–with comments regarding the confidence of some of these records. We also describe three new species, S. marielleae n. sp. and Salvatoria nitiduloides n. sp., based on material from Fernando de Noronha and Trindade islands, off the Northeastern Brazilian coast, and S. ypsiloides n. sp., from Fernando de Noronha and also, Campos Basin, off Southeastern Brazilian coast, in depths down to 970 m. Finally, we report a probably undescribed species, Salvatoria sp., represented by only one specimen lacking median antenna, preventing us to proceed with further identification properly. A dichotomous identification key and a comparative table with morphological data of specimens belonging to these species are also provided.

The subfamily Exogoninae is a monophyletic group, however, some of its genera, such as Salvatoria McIntosh, 1885 [13], are not [14]. The most recent phylogenetic hypothesis recovered Salvatoria as a paraphyletic group, based on molecular and morphological data [8]. The 4B0F-4018-9B5F-134B67686970. The electronic edition of this work was published in a journal with an ISSN and has been archived and is available from the following digital repositories: PubMed Central, LOCKSS, ResearchGate and DigitalCSIC.

Identification key for the Salvatoria species recorded in Brazilian waters
1a Palps more than twice as long as prostomium; falciger blades with faint dorsoventral gradation in length (11- 9b (7b) Antennae spindle shaped to subulated, median antenna longer; dorsal cirri spindle shaped or subulated, midbody dorsal cirri shorter than corresponding chaetiger width; falciger blades with teeth of unequal sizes at least in some region of body. Remarks. The material analysed herein matches the original description provided by [21] from São Paulo, except for details on the teeth of falciger blades and a slight variation on the number of muscle cells rows in the proventricle. Specimens from Paraíba have both teeth shorter and directed forwards, and proventricle with ca. 17 rows of muscle cells, while material from São Paulo has falciger blades with longer teeth directed slightly upwards, and 24 rows of proventricular muscle cells.
Remarks. The species Salvatoria nitidula was described from Bermuda, in the North Atlantic American coast, so the presence of animals belonging to this species along the Brazilian coast would not be totally surprising. However, the original description of the species is very brief and does not mention important characters, such as details of pharyngeal structures and compound chaetae. San Martín [19] reported S. nitidula (as Grubeosyllis nitidula), describing animals similar to those herein analysed, from Cuba, Bermuda, and the Gulf of Mexico, however, with considerable doubts due to the lack of information in the original description. One noticeable difference is related to the length of dorsal and ventral peristomial cirri: about this character, in the original description Verrill [18] describes "Tentacular cirri

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two on each side, of about the same length", while both our specimens and those analysed by [19] show ventral peristomial cirri with about half length of dorsal ones. Nonetheless, herein we follow [19] in also assigning this species with caveats, until we can examine the syntypes or a redescription based on Bermudan specimens is provided.
The Mediterranean Salvatoria vieitezi (San Martín, 1984) [16] shares with S. cf. nitidula the size of the proventricle, the spinulation pattern of falciger blades and the morphology of aciculae, dorsal and ventral simple chaetae. However, S. vieitezi differs from S. cf. nitidula by having only one acicula per parapodium throughout, subdistally curved, with acute tip; blades of dorsalmost falcigers up to 20 μm long, with long spines directed upwards, more conspicuous at mid-length of blades; intermediate and ventralmost falcigers with blades with straight spines slightly shorter than in S. cf. nitidula, 13 μm and 10 μm long, respectively. S. vieitezi can be also differentiated by its pigmentation pattern, with dark-red transverse stripes on the dorsum of each segment, more evident in live animals, but often preserved in fixed material.
Another species similar to Salvatoria cf. nitidula by sharing the overall morphology of antennae and peristomial and dorsal cirri throughout is Salvatoria heterocirra (Rioja, 1941) [28], described from the Pacific coast of Mexico. However, S. heterocirra differs from S. cf. nitidula by having only one acicula per parapodium throughout, distally rounded, hollow; falciger blades with short spinulation, distally bidentate, with subdistal tooth of even sizes throughout, without variation; and proventricle slightly smaller, through 2-2.5 segments [28]. On the other hand, S. cf. nitidula has two aciculae per parapodium on anterior body, falciger blades with subdistal tooth varying in size along the body and proventricle extending through~3-4.5 segments.
Salvatoria heterocirra was identified among Brazilian material by [24], based on body size, number of segments and of eyes, shape of palps, antennae and peristomial cirri, length of dorsal cirri of the chaetiger 1 and length and number of muscle cell rows of the proventricle; on the occasion, the author considered the pharyngeal size as the only difference between his specimens and the original description of S. heterocirra. Nonetheless, the set of characters used by [24] to justify this identification is shared by several species within the genus. Moreover, comparing the description presented by [24] with the original description of the species [28], a discrepancy in the shape of falciger blades was noticed. Although this character was not described in detail, the drawings by [28] illustrate the falciger blades of S. heterocirra as having small size variation, short spinulation and approximately equal sized teeth. In addition, [28] described the species as having only 1 acicula per parapodium, differing from [24], which follows the pattern described herein for S. cf. nitidula. [24] informs that type material of S. heterocirra was not analysed for that study, but also makes no reference to these differences in his discussion. S. heterocirra sensu [24] was also later identified in the Brazilian coast, with restrictions, by [20] (as Grubeosyllis cf. heterocirra), perhaps in both cases being the species identified herein as S. cf. nitidula. To proper address this question and solve this issue it is necessary to reanalyses the material studied by [20,24], but this has not been done for the present paper.
Remarks. Members of Salvatoria nitiduloides n. sp. are characterized by the length pattern of anterior body dorsal cirri. These animals are similar to S. clavata from the Iberian Peninsula, according to the redescription provided by [7], in overall body shape and by the falciger blades having distal tooth larger than the subdistal one throughout. San Martín [7] noticed different morphotypes of S. clavata in his material and considered those more than just intraspecific variation, suggesting the occurrence of a species complex. Salvatoria clavata is characterized by having parapodial lobes papillated, with at least three small papillae; blades of falcigers on anterior body with dorso-ventral gradation in length, 19-12 μm long, dorso-ventral gradation in length absent on posterior body, with blades 11-12 μm long; blades of falcigers with short, straight spines on anterior body and with stouter, short, straight spines on posterior body; dorsal simple chaetae bidentate, with short subdistal tooth; and single acicula per parapodium, acuminate [7]. Specimens of S. nitiduloides n. sp. described herein differ from the description of S. clavata from the Iberian Peninsula by having smooth parapodial lobes, without papillae; longer blades of falcigers, with dorso-ventral gradation in length throughout, 22-8 μm, 25-12 μm and 24-11 μm long on anterior, mid-and posterior body parapodia, respectively; longer spinulation on the cutting edges of the blades of dorsalmost falcigers throughout; dorsal simple chaetae with both teeth triangular, similar in length; and anterior parapodia with two aciculae with acute tip each, one of which straight, another subdistally inflated and twisted.
Salvatoria nitiduloides n. sp. is similar to S. nitidula [18,19] and S. cf. nitidula characterized above, in overall shape of body, antennae and cirri throughout. However, members of S. nitiduloides n. sp. have the median antenna inserted slightly posteriorly, between posterior pair of eyes; dorsal peristomial cirri similar in size to median antenna; dorsal cirri from chaetigers 4 and 5 as long as those of the chaetiger 1, and subsequent dorsal cirri shorter; falciger blades with distal tooth larger than the subdistal one throughout; falciger blades shorter, 22-8 μm, 25-12 μm and 24-11 μm long on anterior, mid-and posterior body parapodia, respectively. In contraposition, both S. nitidula and S. cf. nitidula have median antenna inserted between the anterior pair of eyes; dorsal peristomial cirri shorter median antenna; dorsal cirri from chaetiger 1 longer than remaining; falciger blades with distal tooth larger than subdistal one on anterior and midbody parapodia, teeth about same size on posterior body; and falciger blades longer, 30-10 μm on anterior and midbody parapodia, respectively. Also, S. nitiduloides n. sp. also differs from S. cf. nitidula by having ventral simple chaetae subdistally spinulated under SEM and proventricle shorter, extending for up to 3 segments.

Other material examined. Project 'ProTrindade'-Trindade and Martin
Remarks. Salvatoria marielleae n. sp. has the prostomium slightly broader than palps; antennae spindle-shaped and peristomial and dorsal cirri tapered with slightly stouter bases; dorsal peristomial cirri longer than ventral ones; dorsal cirri of chaetiger 1 longer than those of chaetigers 2-8; midbody dorsal cirri about same length or slightly shorter than those of chaetiger 1.
Salvatoria nitidula [18] is the species most similar to S. marielleae n. sp. by the overall body shape and morphology of antennae and chaetae. However, S. nitidula has palps slightly broader than prostomium; antennae and peristomial cirri about same shape; both dorsal and ventral peristomial cirri similar in length; dorsal cirri about same length as peristomial cirri or the width of corresponding segment [18]. Specimens of S. nitidula from Cuba, Bermuda, and Gulf of Mexico [19], have falciger blades bidentate with distal tooth slightly larger than subdistal one in anterior and midbody parapodia, whereas S. marielleae n. sp. has teeth of similar sizes throughout. The specimens described by [19] have stronger dorsoventral gradation in the length of the blades, 30-14 μm on anterior body and 25-15 μm on posterior body, whereas S. marielleae n. sp. presents falciger blades with 21-9 μm on anterior body, 21-10 μm on midbody, and 20-10 μm on posterior body. In addition, specimens of S. marielleae n. sp. have dorsal simple chaetae from the proventricle level and ventral simple chaetae smooth under optical microscope, whereas the specimens of S. nitidula analysed by [19] have dorsal simple chaetae from the first chaetigers onwards, and ventral simple chaetae slightly spinulated. Finally, S. nitidula presents two aciculae per parapodium on anterior body chaetigers, one of which straight, distally pointed, slightly protruding from parapodial lobes, the other subdistally inflated, twisted, with acute tip, while S. marielleae n. sp. presents only one acicula per parapodium throughout, of the latter type.
The specimens of S. cf. nitidula characterized herein differ from S. marielleae n. sp. in having median antenna longer than lateral ones; lateral antennae inserted closer to anterior

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margin of the prostomium; antennae, peristomial and dorsal cirri spindle-shaped to subulated; dorsal cirri of chaetiger 1 longer the remaining; and blades of falcigers longer, with up to 30 μm and 25 μm on anterior and posterior body, respectively. In contraposition, S. marielleae n. sp. has all antennae of similar size; lateral antennae inserted away from the anterior margin of prostomium; peristomial and dorsal cirri slightly different from the antennae, digitiform, distally tapered, with bases slightly stouter; falciger blades shorter, with up to 21 μm and 20 μm long on anterior and posterior parapodia, respectively, with teeth of similar size throughout and rounded space inbetween; ventral simple chaetae smooth; single acicula per parapodium throughout, subdistally inflated, with acute tip.
Salvatoria nitiduloides n. sp. is also similar to S. marielleae n. sp., by the overall body shape and by having falciger blades and dorsal and ventral simple chaetae bidentate and spinulated,

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and aciculae with similar morphology. However, S. nitiduloides n. sp. differs from S. marielleae n. sp. by having antennae and dorsal cirri throughout spindle-shaped to subulated; falciger blades with distal tooth larger than subdistal one and oblique space inbetween; ventral simple chaetae subdistally spinulated; and two aciculae per parapodium on anterior body chaetigers, one thin, straight, the other subdistally inflated, with acute tip. Differently, S. marielleae n. sp. has antennae typically spindle-shaped; dorsal cirri morphologically different from antennae, digitiform, distally tapered, with bases only slightly stouter; falciger blades with teeth of similar size and rounded space inbetween; ventral simple chaetae smooth; and single acicula per parapodium throughout, subdistally inflated and twisted, with acute tip.
Salvatoria brevipharyngea (Banse, 1972) [33] and S. euritmica (Sardá, 1984) [27] are also similar to S. marielleae n. sp. in the overall body shape and morphology of antennae, cirri and chaetae, especially regarding the bidentate falciger blades, with teeth of similar sizes and rounded space between teeth. However, S. brevipharyngea, described from the North Pacific coast of the United States, and so far only known from that area [33,35], is a larger species, up to 3 mm in length and with 31 chaetigers (against up to 2.3 mm long, with 22 chaetigers, as in members of S. marielleae n. sp.); it also has a slightly shorter pharynx (~2.5 segments) and slightly larger proventricle (~3.5-4.5 segments, with 20-25 muscle cell rows) than S. marielleae n. sp., which shows the pharynx extending for three segments and the proventricle, for 2-2.5, with 18-19 muscle cell rows. Finally, the aciculae in S. brevipharyngea are subdistally inflated and slightly oblique, with rounded tip, different from the aciculae with filiform, needle-like tips, as common in the genus and present in S. marielleae n. sp.
Salvatoria euritmica, described and with occurrences throughout the Mediterranean and also occurring in the North Atlantic European coast, Cuba, Brazil and Australia [7,17], is also a larger species than S. marielleae n. sp., up to 4 mm in length and with 29 chaetigers. It also differs from S. marielleae n. sp. in having all dorsal cirri of similar length throughout, except for those from chaetiger 1, which are longer; falcigers with longer blades (31-9 μm long, against 21-9 μm long in S. marielleae n. sp.); and in presenting up to two aciculae per anterior body parapodium, one of which subdistally inflated and twisted, similar to the single acicula present in each parapodium of S. marielleae n. sp., but without the acute, needle-like tip, the other acicula being nearly straight, subdistally inflated, with tapering tip. It is worth mentioning that, as specimens of S. euritmica from different localities show slight differences among them [7,17], the comparison above was made based on European specimens. Thus, this would be another good target for focused taxonomic investigations, to check whether it is a case of species complex.
Remarks. Salvatoria neapolitana has rounded, distally hollow aciculae, unusual for Salvatoria but characteristic of the genus Brania Quatrefages, 1866 [15]. Nevertheless, this species is undoubtfully placed in Salvatoria for a characteristic set of characters, such as the morphology of the dorsal simple chaetae, position of pharyngeal tooth and length of pharynx and proventricle, the latter without a conspicuous midline formed by the arrangement of the muscle cell rows, typical of Brania.
Salvatoria neapolitana resembles S. vieitezi in the morphology of falciger blades-bidentate, with subdistal tooth clearly smaller than distal one, conspicuously spinulated, with some spines directed upwards, and with dorsoventral gradation in length. Conversely, S. vieitezi differs from S. neapolitana by having clearly bidentate blades, although with subdistal tooth slightly smaller than distal one, and marked differences between blades of dorsalmost and ventralmost falcigers within same fascicle, the former with long spines directed upwards, the latter with short, straight spines; additionally, S. vieitezi presents dorsal, transverse dark-red stripes on each segment and has acuminated aciculae, with acute and filiform tips, as typical of the genus [7].
Another species with falciger blades with small, spine-like subdistal tooth is S. kerguelensis McIntosh, 1885 [14], which also shares with S. neapolitana the size of the antennae, peristomial and dorsal cirri throughout, and proventricle proportions. However, S. kerguelenesis differs from S. neapolitana in having dorsal simple chaetae slightly less sigmoid than in animals belonging to the latter species, and aciculae subdistally inflated and slightly twisted, with acute tip, as typical of Salvatoria [17] and different from the distally hollow aciculae of S. neapolitana.
Salvatoria heterocirra also has falcigers with bidentate and spinulated blades and aciculae with distally inflated, hollow tip. Conversely, S. heterocirra differs from S. neapolitana in having dorsal simple chaetae conspicuously more sigmoid than in S. neapolitana and falciger blades with teeth of similar size, with characteristic rounded space inbetween [28].
Remarks. Salvatoria ypsiloides n. sp. is characterized by having palps shorter than prostomium; median antenna inserted between posterior pair of eyes; dorsal cirri elongate, digitiform, almost of uniform width along their length and distally hollow in appearance, present on all chaetigers; tooth at about ⅔ of the pharynx; falcigers with strongly bidentate blades, with wide angle between teeth, except for dorsalmost chaetae in each fascicle, which teeth are closer to each other; dorsal simple chaetae present from anterior body, distally bifid, with "ypsiloid" shape; and ventral simple chaetae sigmoid and bidentate, with subdistal tooth slightly larger than distal one. Salvatoria euritmica, S. nitidula and S. rugulosa (Verrill, 1900) [18] are the most similar species to S. ypsiloides n. sp., in overall body shape or by sharing some of the above features. However, S. ypsiloides n. sp. differs from all congeners by the apparently distally hollow dorsal cirri and by the unique shape of the dorsal simple chaetae, looking 'ypsiloid'.

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slightly longer than the prostomium; antennae and dorsal cirri throughout larger and rather spindle-shaped (although only slightly tapered distally in S. nitidula); pharyngeal tooth inserted near anterior margin of pharynx; blades of falcigers with narrower angle between teeth than in S. ypsiloides n. sp., and with shorter spinulation in the dorsalmost blades; dorsal

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simple chaetae present from midbody (from anterior body in S. nitidula), bidentate, with short teeth and short spines; and ventral simple chaetae bidentate, with teeth similar to those of the falcigers [7,17,19].
Salvatoria rugulosa was described from Bermuda [18] and has been recorded from Florida, Gulf of Mexico and Cuba [19]; it resembles S. ypsiloides n. sp. in having the pharyngeal tooth located away from the anterior margin of pharynx and by having falcigers with bidentate, spinulated blades. In contraposition, S. rugulosa differs from S. ypsiloides n. sp. in having conical to triangular palps; short, spindle-shaped antennae and dorsal cirri throughout; all blades of falcigers with teeth closer to each other than in S. ypsiloides n. sp.; dorsal simple chaetae thin, bidentate, with teeth similar in size; and ventral simple chaetae less sigmoid, with teeth similar in size [18,16].
Etymology. The specific name refers to the characteristic "ypsiloid" appearance of the dorsal simple chaetae.
Remarks. As we found a single specimen of Salvatoria sp., we preferred not to investigate the specimen under SEM, what made it difficult to discern more detailed characters. Furthermore, the median antenna, which is an important taxonomic character, is missing in this specimen, precluding more specific identifications. The specimen was found with the sponge Plakortis insularis Moraes & Muricy, 2003 [38], without information whether the specimen was over or within the sponge.
The specimen presents some similarities with S. clavata from the Iberian peninsula, described by [7], in the overall morphology of the antennae and dorsal cirri, in the presence of characteristic distal papillae on parapodial lobes and, to some extent, in the morphology of the falciger blades. However, S. clavata differs from Salvatoria sp. for being larger and wider, 3.5 mm long, 0.35 mm wide, with 35 chaetigers; by having shorter parapodial lobes; more falcigers per parapodium, 10 chaetae on anterior body, 7-4 on posterior body; blades of falcigers with marked dorso-ventral gradation in length only in anterior parapodia, and with slightly shorter spines; both dorsal and ventral simple chaetae bidentate and spinulated; and proventricle with more muscle cell rows, 20-23.
San Martín [7] pointed out that there are at least three different forms registered as S. clavata in the Iberian peninsula, two by [39] and one by [40], each one deviating somewhat from the description presented by [7], who, nonetheless, considered them as intraspecific variations.
As mentioned above, S. cf. nitidula characterized herein is similar to S. clavata from the Iberian Peninsula reported by [7]. In comparison to Salvatoria sp., S. cf. nitidula differs by having longer and wider body, 2.37 mm long, 0.18 mm wide, with 31 chaetigers; palps as long as prostomium, with a distal notch; both dorsal and ventral simple chaetae bidentate and spinulated; and proventricle with more muscle cell rows, 16-20. Other congeneric species similar to Salvatoria sp. is S. marielleae n. sp., by the overall morphology of antennae, dorsal cirri throughout and falciger blades. Nevertheless, Salvatoria sp. has dorsal cirri larger and slightly thicker; parapodial lobes distally papillated; falciger blades with distal tooth slightly larger than the subdistal one throughout and with thicker spines; and both dorsal and ventral simple chaetae unidentate and less sigmoid.

Discussion
Five out of the 12 species reported herein are only known from Brazilian waters: Salvatoria breviarticulata comb. nov., S. longiarticulata comb. nov., S. marielleae n. sp., S. ypsiloides n. sp. and S. nitiduloides n. sp., in addition to the unidentified Salvatoria sp. Brazilian specimens of Salvatoria cf. nitidula and S. neapolitana were also described, with some subtle differences in comparison to their original descriptions. Salvatoria clavata, S. euritmica, S. heterocirra and S. limbata had previously been identified in Brazilian waters, but without voucher material, nor characterizations or illustrations provided [9,20]; the four species were not examined for this work. Additionally, no material identified as Brazilian S. limbata is available as vouchers in collections (Table 1), so we consider this record as doubtful.
Salvatoria clavata, S. euritmica, S. limbata and S. neapolitana have very wide distributions: while their type-localities are in the Atlantic Ocean, they were also recorded in the Indian and Pacific Oceans (Fig 1A and Table 1). However, such distribution is not consistent with the low dispersal capabilities and the reproduction process present in the Exogoninae, which involves parental care. Virtually all species of the Syllidae previously considered cosmopolitan, when carefully studied with morphometrics and genetic data, were found to present much more restricted distributions [41][42][43][44], which warrants for some restrictions on the records of these species, specially outside the Atlantic. On the other hand, out of all these species, only S. neapolitana was examined herein; Brazilian specimens match almost completely the type specimens from the Mediterranean Sea, thus we assume the presence of this species in the coast of Brazil is correct.
All morphological characters in Table 1 were informative for the taxonomy of Salvatoria. The shape, size and insertion of the antennae in the prostomium as well as the shape and length of the peristomial and dorsal cirri are fundamental to diagnose and describe the new species presented in this work. It is worth mentioning that most species of the genus have antennae, peristomial and dorsal cirri spindle shaped or with subtle variations, such as spindle shaped to subulated or digitiform. However, S. neapolitana has conical, thickened antennae and cirri, and S. opisthodentata (Hartmann-Schröder, 1979) [45] and S. ypsiloides n. sp. have digitiform appendages. Additionally, S. ypsiloides n. sp. also shows some dorsal and ventral cirri distally hollow in appearance, unique in the genus.
For some species, antennae, peristomial and dorsal cirri have more or less the same shape, as in S. euritmica; in contraposition, for another group of species, such as in S. mariellae n. sp., antennae and cirri have different shapes. Dorsal and ventral simple chaetae are also very informative. Here we report the Y-shaped dorsal simple chaetae and ventral simple chaetae with teeth widely open, both unique in the genus, present in S. ypsiloides n. sp.
A phylogenetic analysis, ideally combining different classes of data, such as morphological, molecular and ecological, may help to infer phylogeographic hypothesis and elucidate evolutionary routes within the genus.
to the institution. This paper is part of the Ph.D. results of Rodolfo Leandro Nascimento Silva at the Biodiversity and Evolutionary Biology Graduate Program of the Federal University of Rio de Janeiro.