Research Article |
Corresponding author: Nálita Maria Scamparle Teodoro ( nalita.scamparle@gmail.com ) Academic editor: Christopher Glasby
© 2023 Nálita Maria Scamparle Teodoro, Tatiana Menchini Steiner, Antonia Cecília Zacagnini Amaral.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Scamparle Teodoro NM, Steiner TM, Amaral ACZ (2023) A new species of Lumbrineriopsis (Annelida, Eunicida, Lumbrineridae) from southeastern Brazil. ZooKeys 1174: 175-189. https://doi.org/10.3897/zookeys.1174.101059
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Lumbrineriopsis dulcis sp. nov. is morphologically described from the continental shelf and slope of Espírito Santo and the Campos Basin of Rio de Janeiro state, southeastern Brazil, at depths between 14 and 400 m. Lumbrineriopsis mucronata is the only species of the genus recorded until now in Brazil. The new species differs from other congeneric species in its jaw-apparatus morphology with unfused mandibles and a fixed number of simple limbate chaetae and simple, bidentate, hooded hooks in each parapodium. This paper aims to fill the gap in knowledge on the family Lumbrineridae, which has not been studied in Brazil for the last 25 years and provides the first record of the genus from Espírito Santo and Rio de Janeiro states. This record is significant given the damage to the marine ecosystem of the Espírito Santo region due to the 2015 rupture of the Samarco mining company dam, the largest environmental disaster in Brazil’s history. In addition, this region has important environmental conservation units such as Costa das Algas Environmental Protection Area, Santa Cruz Wildlife Refuge, and Comboios Biological Reserve. All these preserved areas are of paramount importance for the protection of marine biological diversity.
Lumbrineriopsis dulcis sp. nov., morphology, new genus record, new species, polychaetes, South Atlantic, taxonomy
The family Lumbrineridae Schmarda, 1861 is composed of species with similar external morphology. Their identification was based, until 1990, on characters of the prostomium and parapodial lobes, as well as the type of chaetae. Consequently, the classification resulted in a generic system that arranged the existing species into three or four genera (
Lumbrineridae comprises about 279 valid species in 19 genera (
The genus Lumbrineriopsis was erected by
Herein, Lumbrineriopsis dulcis sp. nov. is described based on material from the states of Espírito Santo and Rio de Janeiro. The new species is grouped together with L. mucronata and L. paradoxa, whose distinctive feature is the presence of unfused jaws.
This is the first record of the genus from Espírito Santo state, which is significant given the damage to the marine ecosystem in this region due to the rupture of the dam belonging to the Samarco mining company. In 2015 the company dumped 50 million m3 of ore tailings into the Doce River, which flows into an estuary in the Atlantic Ocean. This was the biggest environmental disaster in the history of Brazil. In addition, this region has important environmental conservation units such as Costa das Algas Environmental Protection Area, Santa Cruz Wildlife Refuge, and Comboios Biological Reserve. All these preserved areas are of paramount importance for the protection of marine biological diversity.
The specimens were collected along southeastern Brazil during two major Brazilian oceanographic research projects carried out between 2008 and 2013 in soft bottoms from 12 to 3301 m depth and coordinated by CENPES/PETROBRAS (“Assessment of the environmental heterogeneity of the Campos Basin” (HABITATS) and “Marine environmental characterization of the Espírito Santo and northern portion of the Campos Basins” (AMBES)). The collected samples were fixed in 4% formaldehyde, and the specimens were preserved in 70% alcohol.
For detailed visualization of the jaw apparatus, some individuals were immersed in 0.2% sodium hypochlorite for 12 min and subsequently immersed in Hoyer’s solution. Chaetigers from anterior, median, and posterior regions, including parapodia, were dissected and immersed in Aquatex aqueous mounting medium. Individuals were examined using both Zeiss Stereo Discovery v. 2.0 and Zeiss Axioskop 2 Plus microscopes. Two specimens for scanning electron microscopy (SEM) imaging were dehydrated in a series of baths from 70% to 100% ethanol, then carried to the critical-point drying, metalized, and analyzed using a JEOL 6610 LV scanning electron microscope at the Laboratory of Electron Microscopy (LME), Instituto de Biologia, Universidade Estadual de Campinas (
Based on the morphology of mandibles (Figs
Class Polychaeta Grube, 1850
Order Eunicida Dales, 1962
Family Lumbrineridae Schmarda, 1862
Antennae and eyes absent. Notopodia small, without branchiae. Limbate chaetae and simple bidentate hooded hooks. Pygidium without anal cirri. Jaw apparatus with four pairs of maxillae, maxillary carriers longer than MI, joined to 1/2 of its base. MI forceps-like, without inner accessory teeth, with attachment lamella. MII with ligament, wide attachment lamella along 2/3 of posterior lateral edge; without connecting plates. MIII completely pigmented, narrow attachment lamella along 1/2 of posterior lateral edge. MIV completely pigmented, wide attachment lamella. Mandibles unfused, fused along the entire inner margin or up to 3/4 of its length (modified from
Lumbriconereis mucronata Ehlers, 1908.
Holotype complete, 0.5 mm wide, 23 mm long, 178 chaetigers. Complete adult paratypes (16 specimens): 0.3–0.75 mm wide, 4.5–43 mm long, 45–254 chaetigers. Incomplete adult paratypes (79): 0.3–0.9 mm wide, 1–71 mm long, 12–243 chaetigers. Complete juveniles paratypes (4): 0.2 mm wide, 5–11 mm long, 56–75 chaetigers. Incomplete juvenile paratypes (14): 0.1–0.25 mm wide, 5–11 mm long, 11–54 chaetigers. Body yellow or whitish in preserved specimens. Prostomium long, acuminate, 1.5–2.5 times longer than peristomium (Figs
Lumbrineriopsis dulcis sp. nov. A anterior end, dorsal view (ZUEC-POL 21515) B anterior end, ventral view (ZUEC-POL 21515) C mandibles (adult), dorsal view (ZUEC-POL 22897) D right mandible (juvenile), ventral view (ZUEC-POL 22900) E jaw apparatus, dorsal view (ZUEC-POL 21524) F MII, detailed view (ZUEC-POL 21524) G MIII, detailed view (ZUEC-POL 21524) H MIV detailed view (ZUEC-POL 21524). Arrows of C, D teeth of mandibles; arrows of G teeth of MIII. Scale bars: 125 µm (A, B); 31.25 µm (C); 25 µm (D); 31.25 µm (E–G); 12.5 µm (H).
Lumbrineriopsis dulcis sp. nov. (ZUEC-POL 21527) A simple limbate chaetae B simple bidentate hooded hook C acicula D simple limbate chaetae E simple bidentate hooded hook F acicula G simple limbate chaetae H simple bidentate hooded hook I, J aciculae K simple limbate chaetae L simple bidentate hooded hook M, N aciculae A–C parapodium 1 D–F parapodium 5 G–J parapodium 11 K–N parapodium 59. Scale bars: 31.25 µm.
Lumbrineriopsis dulcis sp. nov. (SEM micrographs). (ZUEC-POL 21522) A parapodia 1 and 2 B parapodia 30–35 C parapodium 33 D pygidium, posterior end, dorsal view (chaetae are broken, except one limbate). lc – limbate chaetae, pa – parapodium, pe – peristome, pi – pygidium, psl – post – chaetal lobe, sbhh – simple bidentate hooded hook. Scale bars: 50 µm (A, B); 10 µm (C); 50 µm (D).
Lumbrineriopsis dulcis sp. nov. (SEM micrographs). (ZUEC-POL 21522) A parapodium 1, anterior view B parapodia 9 and 10, anterior view C parapodium 12, anterior view D parapodia 29 and 32 E parapodium 30, anterior end F parapodium 65, anterior view. lc – limbate chaetae, psl – post – chaetal lobe, sbhh – simple, bidentate, hooded hook. Scale bars: 10 µm.
Lumbrineriopsis dulcis sp. nov. Mandibles (adult) A ZUEC-POL 22897 B ZUEC-POL 21526 C ZUEC-POL 22898 D ZUEC-POL 21524 jaw apparatus (adult) E ZUEC-POL 21525 F ZUEC-POL 22899 G ZUEC-POL 22905 anterior end, ventral view, partially everted pharynx. al – attachment lamella, ph – pharynx, MI – maxillae I, MII – maxillae II, MIII – maxillae III, MIV – maxillae IV, md – mandible, pr – prostomium. Scale bars: 45 µm (A); 40 µm (B, D); 50 µm (C); 48 µm (E); 52 µm (F); 200 µm (G).
Lumbrineriopsis dulcis sp. nov. A jaw apparatus (juvenile), ZUEC-POL 22900 B mandible (juvenile), ZUEC-POL 22900 C jaw apparatus (juvenile), ZUEC-POL 22901 D parapodium 7, ZUEC-POL 22527 E parapodium 8, ZUEC-POL 22527 F parapodium 96, ZUEC-POL 22528 G parapodium 97, ZUEC-POL 22528. psl – post-chaetal lobe. Scale bars: 25 µm (A–C, F, G); 15µm (D, E).
Main morphological characters of Lumbrineriopsis with unfused mandibles (from the original descriptions).
Characters | L. paradoxa Saint-Joseph, 1888 | L. mucronata Ehlers, 1908 | L. dulcis sp. nov. |
---|---|---|---|
Color of the animal | Grey | Brownish yellow | Yellow or whitish |
Prostomium shape | Elongated, rounded end | Elongated | Long, acuminate |
Prostomium length | Undocumented | As long as the first 3 segments | 1.5–2.5 times longer than peristomium |
Peristomial rings | Well-distinguishable rings | Poorly distinguishable rings, with mouth pads, narrower than the next chaetigers | Slightly demarcated rings, without mouth pads, narrower than following chaetigers |
Peristomium length | Undocumented | Slightly shorter than the following chaetigers | Slightly shorter than following chaetigers |
Color of jaw apparatus | Undocumented | Dark brown | Light brown |
Mandible (presence of denticles) | Present | Some large teeth | 14–16 denticles |
MI (shape / basal lateral projection) | Forceps / present | Forceps / absent | Forceps / present |
MII (number of teeth: left + right) | 5 + 9 | 5 + 5 | 6 + 7 |
MIII (number of teeth: left + right) | Undocumented | 1 + 1 | 1–5 + 1–5 |
MIII (aliform expansions) | Undocumented | Absent | Present |
MIV (number of teeth: left + right) | 11 + 8 | 8 | 11–16 + 11–16 |
Simple limbate chaetae (number) | 2 until the 21st segment / 1 thereafter | 4–5 anterior region / 1 thereafter | 2 throughout the body |
Simple bidentate hook (number) | 1 | 1 | 1 |
Aciculae (number/color) | 1 / yellow | Undocumented | 2, 3 from chaetiger 100 / transparent to light brown |
Type locality | Dinard, France, North Atlantic | Mouth of the Congo River, to 44 m deep, inside Foraminifera | Mouth of Doce and Paraíba do Sul rivers, to 386 m deep, soft bottoms |
The specific epithet “dulcis” is a tribute to the Doce River, which flows into an estuary in the Atlantic Ocean, where L. dulcis is recorded.
117 specimens, including 99 adults and 18 juveniles, from Espírito Santo (ES) and Rio de Janeiro (RJ) states. Holotype: ZUEC-POL 21500 (ES), 21°4'4.76"S, 40°14'14.14"W, 150 m, 23 Jan 2012. Paratypes preserved in 70% alcohol (each lot with 1 specimen): ZUEC-POL 21501 (ES), 19°42'26.81"S, 39°39'5.27"W, 14 m, 15 Jul 2011; ZUEC-POL 21502 (ES), 19°49'52.15"S, 39°52'24.51"W, 30 m, 16 Jul 2011; ZUEC-POL 21504 (ES), 20°11'25.75"S, 40°2'15.87"W, 40 m, 13 Jul 2013; ZUEC-POL 21505 (ES), 18°52'31.35"S, 39°8'41.34"W, 40 m, 15 Jul 2013; ZUEC-POL 21506 (ES), 20°1'3.73"S, 39°50'13.76"W, 53 m, 16 Dec 2010; ZUEC-POL 21507 (ES), 20°12'20.26"S, 39°57'59.7"W, 50 m, 20 Jan 2012; ZUEC-POL 21508 (ES), 19°31'51.66"S, 39°3'4.04"W, 150 m, 9 Dec 2011; ZUEC-POL 21509 (ES), 19°36'30.6"S, 39°10'19.39"W, 400 m, 26 Jun 2013; ZUEC-POL 21510 (ES), 21°12'14.60"S, 40°42'27.62"W, 15 m, 22 Jul 2009. Paratypes on stubs for SEM: ZUEC-POL 21522 (ES), 20°34'53.42"S, 40°6'27.43"W, 50 m, 21 Jan 2012; ZUEC-POL 21523 (ES), 20°6'44.162"S, 40°54'44.44"W, 30 m, 17 Jul 2009. Paratypes mounted on slides: ZUEC-POL 21524 (ES), 19°31'51.66"S, 39°3'4.04"W, 171 m, 9 Dec 2011; ZUEC-POL 21526 (ES), 22°8'9.28"S, 40°27'27.44"W, 103 m, 6 Mar 2009; ZUEC-POL 22898 (ES), 19°49'57.38"S, 39°52'14.02"W, 33 m, 15 Dec 2010; ZUEC-POL 22899 (ES), 20°11'25.75"S, 40°2'15.87"W, 40 m, 13 Jul 2013; ZUEC-POL 22902 (ES), 19°36'30.6"S, 39°10'19.39"W, 360 m, 26 Jun 2013; ZUEC-POL 22904 (ES), 19°49'57.38"S, 39°52'14.02"W, 33 m, 15 Dec 2010. Additional material preserved in alcohol 70% (each lot with 1 specimen): ZUEC-POL 21511 (RJ), 21°40'25.12"S, 40°58'26.52"W, 18 m, 19 Jul 2009; ZUEC-POL 21512 (RJ), 21°33'54.61"S, 40°42'53.90"W, 23 m, 20 Jul 2009; ZUEC-POL 21513 (RJ), 21°11'0.91"S, 40°28'27.11"W, 26 m, 5 Mar 2009; ZUEC-POL 21514 (RJ), 22°6'22.01"S, 40°43'42.32"W, 47 m, 17 Jul 2009; ZUEC-POL 21515 (RJ), 22°6'20.06"S, 40°43'41.63"W, 47 m, 17 Jul 2009; ZUEC-POL 21516 (RJ), 21°55'50.85"S, 40°25'59.21"W, 47 m, 23 Jul 2009; ZUEC-POL 21517 (RJ), 22°6'41.46"S, 40°54'44.21"W. 52 m, 17 Jul 2009; ZUEC-POL 21518 (RJ), 22°45'49.07"S, 41°45'33.35"W, 53 m, 16 Jul 2009; ZUEC-POL 21519 (RJ), 22°8'9.28"S, 40°27'27.44"W, 65 m, 23 Feb 2009; ZUEC-POL 21520 (RJ), 22°12'37.0"S, 40°13'18.76"W, 100 m, 24 Feb 2009; MZUSP 4912 and MZUSP 4913 (ES), 20°34'45.78"S, 40°11'30.74"W, 41 m, 20 Jan 2012; MZUSP 4914 (ES), 18°52'32.61"S, 39°8'42.82"W, 40 m, 18 Jan 2012; MZUSP 4915, MZUSP 4916 and MZUSP 4917 (ES), 19°36'30.6"S, 39°10'19.39"W, 360 m, 26 Jun 2013; MZUSP 4918 (RJ), 21°59'3.657"S, 40°25'11.070"W, 52 m, 6 Jul 2009; MZUSP 4919 (RJ), 22°56'2.563"S, 41°53'51.338"W, 48 m, 28 Feb 2009; MZUSP 4920 (RJ), 22°6'42.185"S, 40°54'44.182"W, 29 m, 26 Feb 2009; MZUSP 4921 (RJ), 22°12'53.401"S, 40°51'12.488"W, 52 m, 26 Feb 2009; MZUSP 4922 (RJ), 22°17'42.207"S, 40°26'59.691"W, 104 m, 23 Feb 2009; MZUSP 4923 and MZUSP 4924 (RJ), 21°44'19.481"S, 40°17'15.642"W, 50 m, 9 Mar 2009; MZUSP 4925 (RJ), 21°44'19.481"S, 40°17'15.642"W, 49 m, 9 Mar 2009; MZUSP 4926 (RJ), 21°44'19.591"S, 40°17'15.669"W, 50 m, 8 Jul 2009; MZUSP 4927 (RJ), 22°37'31.715"S, 41°21'52.696"W, 54 m, 16 Jul 2009; MZUSP 4928 (RJ), 22°11'30.609"S, 40°5'24.468"W, 44 m, 17 Jul 2009; MZUSP 4929 (RJ), 21°10'16.281"S, 40°45'58.437"W, 21 m, 22 Jul 2009; MZUSP 4930 (RJ), 21°44'39.982"S, 40°43'8.573"W, 21 m, 19 Jul 2009; MZUSP 4931 (RJ), 21°39'31.643"S, 40°31'25.347"W, 28 m, 23 Jul 2009. Additional material mounted on slides: ZUEC-POL 21525 (RJ), 22°19'3.839"S, 40°5'28.581"W, 386 m, 30 Jan 2009; ZUEC-POL 21527 (RJ), 21°44'19.481"S, 40°17'15.642"W, 50 m, 9 Mar 2009; ZUEC-POL 21528 (RJ), 21°28'2.517"S, 40°56'20.614"W, 16 m, 10 Mar 2009; ZUEC-POL 22897 (RJ), 21°50'20.765"S, 40°31'38.459"W, 28 m, 13 Mar 2009; ZUEC-POL 22900 (RJ) 22°12'37.087"S, 40°13'18.731"W, 100 m, 24 Feb 2009; ZUEC-POL 22901 (RJ), 21°50'20.765"S, 40°31'38.459"W, 33 m, 7 Mar 2009; ZUEC-POL 22903 (RJ), 21°50'20.765"S, 40°31'38.459"W, 28 m, 13 Mar 2009; ZUEC-POL 22905 (RJ), 21°10'16."S, 40°45'58."W, 21 m, Nov 2020; ZUEC-POL 22906 (RJ), 21°44'19.481"S, 40°17'15.642"W, 50 m, Nov 2020; ZUEC-POL 21503 (RJ), 22°11'30.609"S, 40°5'24.468"W, 44 m, Nov 2020.
Southeastern Brazil, Espírito Santo state.
The distribution of this new species encompasses the states of Espírito Santo and Rio de Janeiro in southeastern Brazil, from the mouth of the Doce River to the continental slope (at depths between 14 and 400 m) in mud, sand, mixed sandy-mud bottoms, in sand with biological debris, and between limestones.
The nuchal organ was observed dorsally at the base of the prostomium in specimens analyzed under SEM (Fig.
The specimens are very small, and the jaw apparatus very delicate, especially the mandibles (Figs
The notopodium, which is described as slightly developed in the description of the genus (
1 | Entire or partially fused mandibles | 2 |
– | Unfused mandibles | 4 |
2 | Mandibles fused along the entire inner margin | L. gardineri |
– | Mandibles fused up to 3/4 of the inner margin | 3 |
3 | MIV with 7–10 teeth on each side | L. gasconiensis |
– | MIV with 12–13 teeth on each side | L. tsushimaensis |
4 | Four to 5 limbate chaetae on the anterior region | L. mucronata |
– | Two limbate chaetae on the anterior region | 5 |
5 | Two pairs of light-brown aciculae along the body; 3 onwards from chaetiger 100 | L. dulcis |
– | Acicula single and yellow along the entire body | L. paradoxa |
Of the five known species so far, two groups can be clearly observed: one group with unfused mandibles (L. paradoxa and L. mucronata) and another with fused mandibles (L. tsushimaensis, L. gasconiensis, and L. gardineri). The presence of unfused mandibles in Lumbrineridae, although not common, may occur as in species of the genus Kuwaita (
Lumbrineriopsis dulcis sp. nov. differs markedly from L. tsushimaensis, L. gasconiensis, and L. gardineri, since these species have fused mandibles, with or without growth rings at the distal end. Thus, L. dulcis sp. nov. resembles L. paradoxa and L. mucronata (Table
Although
Both species have been recorded in other localities (
Regarding the stage of development of these two species,
Therefore, in view of this scenario, as well as the need for further clarify the validity of L. paradoxa and L. mucronata, we have followed
Lumbrineriopsis dulcis differs from L. mucronata in the coloration of the jaw apparatus and number of teeth of MII, MIII, and MIV, in addition to the number of limbate chaetae per parapodium (Table
Taxonomic studies of the genus carried out in South America by
Considering the peculiar characteristics of Lumbrineriopsis, with such elongated maxillary carriers, multidentate MIV, and unfused mandibles in some species, a more in-depth analysis of its phylogenetic positioning within Lumbrineridae is necessary, since questions have already been raised (
We thank the Museu de Diversidade Biológica and Museu de Zoologia for receiving the lots of L. dulcis. We thank CENPES/PETROBRAS for sampling and providing the material analyzed in this study. We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship granted to NMST (process 88882.435388/2019-01) and the Postgraduate Program in Animal Biology, UNICAMP. ACZA received a productivity grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq process 301551/2019-7). We also are thankful to the reviewers of the manuscript, Joana Zanol and Luis F. Carrera-Parra, for providing very important feedback and suggestions for its improvement.
The authors have declared that no competing interests exist.
No ethical statement was reported.
This research is funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, process 2018/10313-0).
Nálita Maria Scamparle Teodoro examined the specimens, prepared the drawings and wrote the manuscript. Tatiana Menchini Steiner examined some specimens, helped with drawings, took the photographs and wrote the manuscript. Antonia Cecilia Zacagnini Amaral contributed to the writing of the manuscript.
Nálita Maria Scamparle Teodoro https://orcid.org/0000-0003-1901-9505
Tatiana Menchini Steiner https://orcid.org/0000-0003-4710-8927
Antonia Cecília Zacagnini Amaral https://orcid.org/0000-0002-3303-1351
All of the data that support the findings of this study are available in the main text.