Biodiversity Data Journal :
Single Taxon Treatment
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Corresponding author: Daniel Martin (dani@ceab.csic.es), Chiara Romano (cromano@ceab.csic.es)
Academic editor: Wagner Magalhães
Received: 16 Mar 2021 | Accepted: 11 May 2021 | Published: 19 May 2021
© 2021 Daniel Martin, Chiara Romano
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:
Martin D, Romano C (2021) Morphology and sexual dimorphism of living mature adults of Amphiduros fuscescens (Marenzeller, 1875) (Annelida, Hesionidae, Amphidurine), first reported for the Iberian Peninsula. Biodiversity Data Journal 9: e66020. https://doi.org/10.3897/BDJ.9.e66020
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To date, the genus Amphiduros (Annelida: Hesionidae: Amphidurine) is considered as monotypic. Its single species, Amphiduros fuscescens (Marenzeller, 1875), is well characterised by lacking proboscideal papillae and emerging acicular chaetae, as well as by having three antennae, eight pairs of tentacular cirri and inflated dorsal cirri with characteristic alternating length and colour (transparent, with median orange band and white tips) in live animals.
Three specimens, one male and two females, were found below boulders at 5–7 m depth in Punta Santa Anna, Blanes and Cala Maset, Sant Feliu de Guixols (Catalan Sea, NW Mediterranean, Iberian Peninsula). Our finding allowed us to describe different, unreported morphological traits and lead us to support the existence of sexual dimorphism (in terms of colouring, cirri morphology and distribution of sexual products along the body). Despite A. fuscescens having been previously reported from the Atlantic and the Mediterranean (particularly in SE French coasts), the specimens from Blanes represent the first record of the species from the Iberian Peninsula. In addition, our molecular results strongly support that Amphiduros pacificus Hartman, 1961 from California (currently synonymised with A. fuscescens) requires to be re-described and reinstalled as a valid species. In turn, our morphological observations support suggesting all other non-Mediterranean reports of A. fuscescens, including the species still under synonymy (i.e. Amphidrornus izukai Hessle, 1925 and Amphidromus setosus Hessle, 1925) as likely being a cryptic species complex whose the taxonomic status requires further assessment.
Polychaete, Hesionid, sexual dimorphism, biogeographic distribution, Mediterranean Sea, COI
Amphiduros fuscescens (Marenzeller, 1975) (Annelida: Hesionidae: Amphidurine) appears to be well-characterised by the absence of proboscideal papillae and emerging acicular chaetae, as well as by the presence of three antennae, eight pairs of tentacular cirri and inflated dorsal cirri with characteristic alternating length pattern and in vivo colouring (transparent, with median orange band and white spots and white tips). The species was described from the Italian coasts of the Adriatic Sea by
Amphiduros fuscescens is also known to occur in the North Atlantic Ocean in Brittany (
Our finding of A. fuscescens in the shallow waters of the Catalan Sea (Iberian Peninsula, NW Mediterranean) allowed us to describe some previously unreported morphological features (particularly based on living sexually mature specimens), as well as to discuss the taxonomic status and biogeographical distribution of the species and to contribute to the pool of known molecular information on Mediterranean marine fauna.
The specimens were collected in April 2019 and January 2021 in the Catalan Sea (NW Mediterranean) by turning up submerged boulders using SCUBA diving. One male and one female were found at 6-7 m depth in Punta Santa Anna, Blanes Bay and another female at 5 m depth at Cala Maset, Sant Feliu de Guixols (25 km northeast of Blanes). The worms were detached from the lower side of the boulders with the finger and immediately introduced in a plastic jar with native seawater. In the laboratory, the specimens were placed in a Petri dish with native seawater to observe them in living conditions. After adding drops of a saturated seawater/Thymol solution until the worms were relaxed, we obtained light microscopy photos of the specimens from Blanes with a CMEX 5 digital camera connected to a ZEISS Stemi CS–2000–C stereomicroscope. The female from Sant Feliu was not relaxed before being photographed with a Nikon D7200 digital camera equipped with a 105 mm macro-objective and two Sea&Sea YS-250 flashes.
Body and gamete measurements were made on the captured digital images using the measuring tools of the Adobe Photoshop CC version 2015.5, 1990-2016 Adobe Systems Incorporated. The male and the female from Sant Feliu were directly preserved in 96% ethanol for molecular analyses. The female from Blanes was fixed in a 4% formalin/seawater solution and then preserved in 70% ethanol for further morphological observations. Additional pictures of the preserved female were obtained with an SP100 KAF1400 digital camera connected to a Zeiss Axioplan compound microscope.
All specimens are deposited in the Museo Nacional de Ciencias Naturales of Madrid, Spain (MNCN).
Total DNA was extracted from small pieces of the body wall of the specimens preserved in ethanol using DNAeasy Tissue Kit (Qiagen) and following the manufacturer’s protocol. A fragment (677 bp) of the mitochondrial cytochrome c oxidase subunit I (COI) was amplified using the primers ACOIAF 5’ CWA ATC AYA AAG ATA TTG GAAC 3’ and COIEU-R 5’TCD GGR TGD CCA AAR AAT CA 3’ (
COI pairwise uncorrected–p distances (expressed as %) between the specimens of A. fuscescens of this study and the sequences previously published in GenBank.
Accession Number |
Origin |
Amphiduros fuscescens |
Amphiduros pacificus |
Amphiduropsis cf. axialensis |
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Blanes male |
Sant Feliu female |
Banyuls |
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Amphiduros fuscescens |
MW135348 |
Blanes, male |
- |
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MW741554 |
Sant Feliu, female |
0.30 |
- |
||||
DQ442561 |
Banyuls |
0.18 |
0 |
- |
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Amphiduros pacificus |
JN631312 |
California |
20.47 |
20.48 |
20.83 |
- |
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Amphiduropsis cf. axialensis |
MG640338; MG517506 |
Oregon; Costa Rica |
17.55 |
17.66 |
17.07 |
18.95 |
- |
Gyptis mediterranea |
DQ442563 |
France |
19.93 |
20.11 |
20.11 |
20.84 |
22.63 |
Gyptini with orange/brown eyes, dispersed eye pigment, coalescing nuchal organs, inflated dorsal cirri, and reduced stout emerging acicular notochaetae.
Body anteriorly and posteriorly tapered, ventral flattened (Fig.
Amphiduros fuscescens (Marenzeller, 1857). Living specimens in dorsal view. A–C. Whole body; D. and E. Detail of the anterior end; A and D. Male from Blanes; B and E. Female from Blanes; C. Female from Sant Feliu; la: lateral antennae; pa: palps; ca: central antennae; ey: eyes; no; nuchal organs.
Amphiduros fuscescens (Marenzeller, 1857). Living specimens. A. Midbody parapodia of Blanes female, dorsal view B. Mid-body parapodia of Blanes male, dorsal view C. Mid-body parapodia of Blanes male, ventral view D. Pygidium of Blanes female. sdc: Short dorsal cirri; ldc: long dorsal cirri; vc: ventral cirri; ac: anal cirri.
Blanes female of Amphiduros fuscescens (Marenzeller, 1857), preserved in formalin. A. Anterior end; white arrow pointing on the traces of the orange band; B. Mid-body parapodia; C. Short dorsal cirri; D. Detail of the orange band of the same short dorsal cirri. dcp: dorsal cirrophore; vc: ventral cirri.
Colour in living animals transparent orange, with characteristically transparent appendages having white, iridescent bands on cirrophores and on tips of cirrostyles, a middle orange band on cirrostyles and white pigment as spots and bands on lateral antennae, dorsal cirri and cirrophores and on enlarged, anterior ventral cirri; eyes brownish; gut region orange (Fig.
Body bright orange, 36.3 mm long, 5.7 mm wide (without parapodia) at chaetiger 15, with 35 chaetigers (Fig.
Female from Blanes with violet body, 34.3 mm long, 3.8 mm wide (without parapodia) at chaetiger 15, with 40 chaetigers (Fig. 1B). Ratio body width vs. body length 0.11. Width of the long dorsal cirri 0.39 mm wide (0.08 when divided by body width). Posterior pair of eyes almost coalescent with anterior pair (Fig.
Female from Sant Feliu with orange/violet body, 37.8 mm long, showing traces of regenerating posterior segments, 5.3 mm wide (without parapodia) at chaetiger 15, with 40 chaetigers (Fig.
Southern France, eastern Sicily, northern Adriatic, north Iberian Mediterranean, Gulf of Aqaba. Other reports must be checked, as they may correspond to closely related, but distinct species (see Discussion).
Below stones, amongst coarse shell gravel, shell and muddy sand and amongst kelp holdfasts, from shallow intertidal and medio-littoral. The species has been reported up to 50 m depth; however, these deeper reports may correspond to different species (see Discussion). Our specimens were observed to quickly swim by waving their bodies when the boulders below which they were hidden were turned up. Such a quick swimming reaction was always addressed prior to hiding again below close boulders.
The Iberian male and female showed 99.8% and 100% similarity, respectively, to the COI sequences attributed in GenBank to A. fuscescens from SE French coasts (
Some relevant morphological traits appeared to be linked to the reproductive status of the Iberian specimens. The two specimens from Blanes were collected in spring, on the same day, during the same dive and less than 5 m far from each other, while that from San Feliu was collected in winter, all of them having a similar length. However, the ratio of body width vs. body length was ca. 3 times higher in the male (0.4) than in the females (i.e. 0.11 in Blanes and 0.14 in Sant Feliu). Moreover, the male had the posterior pair of eyes clearly separated from the anterior pair, while the females had both pairs almost coalescent. As for the dorsal cirri arrangement characterising the species, both the male and the females kept it even after being relaxed with Thymol. The males had the long dorsal cirri 1.35-1.5 times wider than females; however, the widths of the cirri were comparable when divided by body width (i.e. 0.1 in the male vs. 0.08 in the females).
The male had appendages much more brightly pigmented than the females, as well as a brighter orange body. According to our observations, we suggest that this difference may be influenced by the evident presence of intra-coelomic gametes (i.e. light orange sperm and dark violet oocytes). This is supported by the difference in colour between the two females, which we assumed were in a different phase of the reproductive cycle depending on the collecting season. The female from Blanes (collected in spring) had larger oocytes not restricted to the parapodia and, thus, a darker body than the female from Sant Feliu (which was collected in winter and had smaller oocytes restricted to the parapodia).
Apart from the few characters linked to the sexual dimorphism mentioned above, the morphology of the Iberian specimens, both male and females, matched well with the re-description of the species by
The Iberian specimens also showed the characteristic alternating length and thickness of dorsal cirri as described by
Our morphological observations clearly support the fact that the Iberian and French Mediterranean specimens belong to the same species, despite some slight differences in eye colouring, which could either be attributed to intraspecific variability, differences in reproductive status or preservation techniques. Thus, this will require to be confirmed by further observations. However, all other relevant morphological characters coincided. Therefore, taking into account that the French worms were used by
Based on COI sequences, the genetic distance between the male from Blanes, the female from Sant Feliu and the French specimens was lower than 0.5%. Therefore, our molecular data confirm the morphological observations and support all of them belonging to the same species. Moreover, our data also agree with those in
Such a taxonomic clarification must be extended to all currently-known non-Mediterranean populations of A. fuscescens (i.e. from Canary Islands, Papua New Guinea and Australia), as well as to the other two synonymised species, A. izukai and A. setosus from Japan (
Therefore, we strongly suggest the existence of an unresolved complex of pseudo-cryptic species (sensu
In summary, based on the specimens collected in the Catalan Sea, we report, for the first time, the existence of sexual dimorphism in a non-interstitial species of Hesionidae and the presence of A. fuscescens in the coasts of the Iberian Peninsula. Moreover, we describe some previously-undescribed morphological features in A. fuscescens, particularly the position of dorsal cirri in living specimens, while providing its westernmost Mediterranean report. Finally, we suggest the existence of a complex of pseudo-cryptic species involving the non-Mediterranean populations of A. fuscescens, highlighting that particularly A. pacificus requires to be further re-described and, more likely, reinstalled.
We would like to acknowledge Manel Bolivar for kindly helping during the sampling of the specimens in Blanes Bay, Gustavo Carreras for helping with the molecular analyses and Xavier Salvador Costa for kindly collecting the female from Sant Feliu, taking an excellent picture in vivo and then keeping the specimen in 95% ethanol, allowing molecular comparisons of the two sexes. We also acknowledge the support of the CSIC Unit of Information Resources for Research (URICI) for providing us with the publication fee through the CSIC Open Access Publication Support Initiative. This paper is a contribution of DM and CR to the Consolidated Research Group on Marine Benthic Ecology of the Generalitat de Catalunya (2017SGR378) and to the Research Project PopCOmics (CTM2017-88080), funded by the “Ministerio de Ciencia, Innovación y Universidades” of Spain (MICINU), the “Agencia Española de Investigación” (AEI) and the European Funds for Regional Development (FEDER).