How false is Nereis falsa (Annelida, Phyllodocida, Nereididae)?

¿Qué tan falsa es Nereis falsa (Annelida, Phyllodocida, Nereididae)?

As a part of the Fauna Ibérica series, Núñez (2004) made an examination of the genus Nereis Linnaeus, 1758 in the Mediterranean region. He listed N. pulsatoria (Savigny, 1822) and N. splendida Grube, 1840, but N. falsa de Quatrefages, 1866 was not recognized. Characters for N. pulsatoria include antennae about as long as the palps, a smooth anterior peristomial margin which is not projected, and homogomph falcigers with short, slightly denticulated blades. Additionally, area VI has 4-10 paragnaths in two transverse series, and areas VII-VIII have paragnaths in 3-4 series. In N. splendida antennae are shorter than palps, peristomial anterior mid-dorsal margin projects anteriorly, pharyngeal area VI has 3 paragnaths in an inverted triangle or 4(-5) paragnaths in a rhombus, areas VII-VIII have paragnaths in several series, and the homogomph falcigers have long, markedly denticulated blades. This variation has been indicated before by Amoureux (1976: 340), although he was referring to N. falsa, and Gravina, Lezzi, Bonifazi, and Giangrande (2015: 159) illustrated the morph having 3 paragnaths in area VI for N. falsa.

It is interesting that for N. splendida two patterns are recognized for area VI despite the fact there is usually a very low variation in paragnath number in this area (GonzálezEscalante & Salazar-Vallejo, 2003; Conde-Vela & Salazar-Vallejo, 2015). Further, Alós et al. (2004) listed the junior synonyms of N. pulsatoria as N. zonata Malmgren, 1867 described from Spitsbergen and N. cylindrata Ehlers, 1868 from the Adriatic Sea, whereas for N. splendida they included N. falsa de Quatrefages, 1866 originally described from the Black Sea and N. parallelogramma Claparède, 1868 from the Mediterranean Sea. How did we arrive to this point?

Rathke (1837) made a large report on the fauna of Crimea and its shores on the Black Sea, including mammals, amphibians, reptiles, fishes (8 new species), crustaceans (15 n. spp), worms (4 n. spp), and cnidarians (1 n. sp). In the section devoted to worms, Rathke (1837: 412-415, Pl. 7, Fig. 1, Fig. 4-8) made a thorough description of some of his nereidids from Balaklava Bay (44°30’ N, 33°36’ E) as N. pulsatoria? This was because he noted some differences from the description of N. pulsatoria (Savigny, 1822) such as body and eye pigmentation, and the size of the upper parapodial lobes, with dorsal cirri clearly longer than upper notopodial lobes in median and posterior chaetigers. However, the arrangement of paragnaths or fine details of the chaetal blades were not clarified or illustrated. Rathke compared his specimens with N. pulsatoria (Savigny, 1822: 33), and not after Lycoris pulsatoria Savigny in Lamarck (1818: 313) as listed in WoRMS (2016), because the latter is a nomen nudum.

For parapodial features, Savigny (1822: 33) indicated: “Cirres courts; le cirre supérieur n’atteint pas même le sommet de la branchie.” [Transl.: Cirri short; the dorsal one does not reach branchial (upper notopodial ligules) tips]. Rathke also had at hand the series by Audouin and Milne-Edwards (1832: Pl. 13, Figs. 8-13, 1833: 216-217), who provided a description and high quality illustrations for N. pulsatoria, now regarded as a junior synonym of N. zonata Malmgren, 1867 in WoRMS.

Grube (1840: 73-74) studied Rathke’s material and added some features to the earlier description, especially regarding the chaetal blades and paragnath arrangement on the pharynx, but made no further comment about its identity. For chaetal blades, Grube (1840: 73) indicated: “diesen die Anhängsel der langen Borsten gesägt erschienen, indessen treten die Zähnehen erst bei einer bedeutenderen Vergrösserung hervor.” [Transl.: the blades of the long chaetae are denticulate, but their number is only evident with a more powerful enlargement]. The paragnath pattern details are very difficult to understand, indeed. In the same contribution he described N. cultrifera (now in Perinereis), N. imbecillis (incertae sedis fide Fauvel, 1923: 362), and N. splendida. For the latter Grube (1840: 75-76) stated that the body was golden with dorsal transverse lines on each segment, the antennae were smaller than the palpophore, the longest tentacular cirri reach segment 3, and some chaetae had an additional tooth. Grube also indicated the pharyngeal paragnath patterns resembled those present in N. pulsatoria but the pharynx was not everted. This latter feature led Fauvel (1916: 81) to consider N. splendida as indeterminable.

de Quatrefages (1866: 505) proposed N. falsa for what Rathke had regarded as N. pulsatoria? However, it must be emphasized that he made no formal description or illustration for N. falsa, nor had he any specimens. Consequently, based upon Rathke’s description and illustration, and in comparison with Savigny or Audouin and Milne-Edwards, de Quatrefages indicated that: “La tête est plus courte; les antennes latérales plus grosses …; les tentacules sont plus longs; l’anneau buccal égale en longuer les deux suivants … Aux pieds, les sois sont plus nombreuses et les languettes à peu près égales” [Transl.: The head is shorter; the antennae thicker …; the tentacular cirri longer; the peristomium as long as the following two segments … In parapodia, chaetae are more abundant and lobes almost equal (to each other)]. No type material exists because Rathke’s collection was not preserved in the Kantiana University in Tartu (olim Dorpat), Estonia.

Some accounts include Nereis clava Leach in de Blainville, 1825 (p. 439), despite the fact that Hartman (1959: 256) regarded it as a nephtyid or indeterminable. It must be rejected from this discussion because de Blainville (1825: 439-440) compared it to what we now regard as Nephtys ciliata (Müller, 1778), Audouin and Milne-Edwards (1833: 257) regarded it as a junior synonym of N. hombergi Savigny in Lamarck, 1818, and de Quatrefages (1866: 434) confirmed its similarities with Nephtyidae.

Claparède (1868: 477, Pl. 9, Fig. 7, 10, Fig. 2) described N. (Nereilepas) parallelogramma by emphasizing that his species was “évidemment distincte de la N. pulsatoria Mont. (Sav.) avec laquelle M. Grube l’a confondue. La seule proportion des cirres suffirat déjà à la différencier, car ils dépassent notablement la languette supérieure chez notre espèce, tandis qu’ils sont plus courts qu’elle chez la N. pulsatoria” [Transl.: evidently distinct from N. pulsatoria Mont. (Sav.) with which it was confused by Mr. Grube. The cirri proportion will be enough to differentiate them, because they markedly surpass the dorsal lobe in our species, whereas they are shorter in N. pulsatoria]. In the following page, Claparède (1868: 478) referred to the paragnath pattern in the pharynx and explained the etymology: “L’article basilaire de la trompe est renflé sur le dos en deux éminences portant quelques paragnathes plus gros que ceux des autres groups. Ils sont en général au nombre de quatre, disposes en parallélogramme” [Transl. The basal pharynx ring is bulged dorsally into two projections larger than those present in other groups. They are generally four in number, arranged in a parallelogram].

Grube (1873: 70, p. 15 in preprint) included many known nereidid species into several genera and groups and concluded that Nereis: “parallelogramma Clap., welche mit der von mir beschriebenen N. splendida zusammenfällt” [Transl.: parallelogramma Clap., coincides with the N. splendida described by me].

Von Marenzeller (1874: 466-470, Pl. 7, Fig. 3) first recorded Hediste diversicolor Müller, 1776 for the Mediterranean Sea with specimens from Muggia Bay, Gulf of Trieste, which had been found living in fresh water. He made an extensive description and in the footnotes (p. 469) he confirmed the previous synonymy by Grube, and concluded: “N. falsa Quatrefages, eine N. pulsatoria Audouin & Milne-Edwards, ja selbst eine N. diversicolor gewesen sein.” [Transl.: N. falsa Quatrefages, a N. pulsatoria Audouin and Milne-Edwards, can be the same as N. diversicolor].

Bobretzky (1881: 192-193) indicated that by (Transl.) “recognizing that Lycoris pulsatoria Rathke is categorically different from a nereidid described under this name either by Savigny (1822: 33) or by Audouin and MilneEdwards (t. XXVII, 1832: pl. XIII, fig. 8-13 and t. XXIX, 1833: 216), Quatrefages (1866) established for Black Sea specimens a distinct species, N. falsa. Marenzeller (1874) recently supposed N. falsa to be the same as N. parallelogramma Clprd., which Claparède (1868: 477 and 1870: 84) recognized as the same species as that identified by Grube (1840: 73), in comparison with the authentic specimens of Rathke, identified as Nereis pulsatoria. On this basis Marenzeller proposed to forget the name provided by Claparède to the above mentioned species and to replace it by the older one, N. falsa.” Further, Bobretzky (1881), after a thorough study of L. pulsatoria? Rathke, synonymyzed it with Hediste diversicolor. This conclusion was followed by Hartman (1959: 259) as she regarded N. falsa as a junior synonym of H. diversicolor.

Fauvel (1923: 335-336), apparently overlooked Bobretzky (1881), and keyed-out N. falsa as closely allied to N. pelagica Linnaeus, 1758. He distinguished these two species by their chaetal blades: short, blunt, rather smooth in N. pelagica, while they are long, denticulate, with a distal tooth fused to blade’s tip in N. falsa. Fauvel (1923: 337), then listed, under N. falsa his early ideas (Fauvel 1913: 63, 1916: 81) about junior synonyms: N. splendida Grube, 1840 (indeterminable), N. parallelogramma Claparède, 1868, N. pervisceralis Claparède, 1868, N. lucipeta Ehlers, 1908, and N. splendida sensu Ehlers, 1913. These species deserve some comments.

For N. splendida, Fauvel (1916: 83) noted that Grube (1873: 70, p. 15 in preprint) had regarded his species as a synonym of N. parallelogramma, and that “Il est fort possible qu’il s’agisse de la même espèce, mais la description de Grube, sans figures, bien qu’assez détaillée, ne precise pas suffisamment certains points pour que cette identité puisse être reconnue d’une façon indubitable.” [Transl.: It is highly likely that it is the same species, but Grube’s description, without figures, and despite its many details, does not sufficiently specify several points for regarding this identity without any doubt]. Actually, Grube (1873: 70) grouped N. diversicolor, N. pelagica, N. parallelogramma and his N. splendida due to the paragnath patterns of their pharynx: area VI with 4(-5) paragnaths in a group, and he indicated that his species was coincident with N. parallelogramma. This conclusion has been indicated by Claparède (1868: 478) but he referred to what Grube indicated for N. pulsatoria, not for N. splendida. Claparède did not deposit any of his specimens because he wanted other naturalists to study living organisms rather than preserved ones.

Including N. perivisceralis in the list of synonyms was incorrect, despite the small size of the specimens (1 cm), because Claparède (1868: 471, Pl. 12, Fig. 1) stated that its pharynx has a single series of paragnaths in areas VII-VIII, whereas N. parallelogramma has 2(-3) transverse series in areas VII-VIII, although they were not illustrated. There is often a great deal of size-dependent variation but this refers to the number of paragnaths per series, not to the number of series.

Ehlers (1908: 69, Pl. 8, Figs. 7-13) described N. lucipeta based upon some atokous and epitokous specimens collected in Southern Angola. It is very similar to Mediterranean epitokous specimens illustrated by Fauvel (1916, Pl. 5, Figs. 4-7), but there are some subtle differences in parapodial features in anterior chaetigers, especially in the dorsal cirri. In Mediterranean specimens the dorsal cirri in chaetiger 7 are swollen along 2/3 of its length and it is twice longer than wide, whereas in N. lucipeta it is swollen along ¾ of its length and it is three times longer than wide. Further, in subsequent segments the dorsal cirri are barely longer than the upper notopodial ligules, whereas in N. lucipeta they are twice longer. Consequently, N. lucipeta must be regarded as a distinct species. The syntype series of N. lucipeta is in Berlin (ZMB 4440). A later record by Ehlers (1913: 496) as N. splendida from Simonstown, South Africa, must correspond to the atokous form of N. lucipeta and as such, could be the one characterized and illustrated by Day for

South Africa (1962: 639, 1967: 317, Fig. 14.7k-o). This specimen might also be in Berlin, but it was not listed by Hartwich (1993) since it was not a species newly described by Ehlers. It is interesting to note that Ramsey (1914: 212) with some South African specimens, regarded N. lucipeta as a junior synonym of N. pelagica, and that Augener (1918: 184) listed N. lucipeta as a junior synonym of N. callaoana (Grube, 1857) and recorded this Eastern Pacific species from Togo and Namibia. These specimens must be studied to clarify this supposed affinity.

In fact, Day (1962: 639) followed Hartman (1959: 271) by pointing out another important issue: N. splendida Grube, 1840 is a junior homonym of N. splendida de Blainville, 1825. Audouin and Milne-Edwards (1833: 257) indicated that de Blainville introduced the name for N. clava (see above), and that it is a junior synonym of N. hombergi. Anyway, N. splendida Grube, 1840 must be replaced (ICZN, 1999: Ch. 12, Art. 60), as has been recently indicated by Gravina et al. (2015: 162).

As indicated above, N. falsa was based upon Nereis pulsatoria? Rathke, 1837 from the Black Sea, and it is currently regarded as having a very wide distribution. This species has been frequently recorded from the Mediterranean Sea: in the harbour of Monaco (Fauvel, 1913) and included in the Fauna of France (Fauvel, 1923), in Alexandria, Egypt (Fauvel, 1937), in the Corsica Channel (Aliani & Meloni, 1999), in the Algeciras Bay (SánchezMoyano, García-Adiego, Estacio, & GarcíaGómez, 2001), in the National Park of Circeo in Italia (Andrea & Giancarlo, 2003), in the Bay of Izmir (Çinar et al., 2008), in Greece (Faulwetter, 2010), and in the region of Ceuta,

Strait of Gibraltar (Guerra-García, GonzálesVila, & García-Gómez, 2003). Several other records have been made for Western Africa: Morocco (Fauvel, 1936; Gillet, 1986, 1988), Western Sahara (Rullier & Amoureux, 1969), Mauritania (Gillet, 1990), Senegal (Fauvel, 1950; Sourie, 1954; Fauvel & Rullier, 1957, 1959) and Guinea (Amoureux, 1973).

According to WoRMS (2016), N. falsa has also been recorded for the Gulf of Mexico (Taylor, 1984; Salazar-Vallejo & Jiménez-Cueto, 1997; Felder & Camp, 2009), Caribbean Sea (de León-González, Solís-Weiss, & OchoaRivera, 1999; Miloslavich et al., 2010) and Brazil (Amaral, Nallin, Steiner, Forroni, & Filho, 2013). The same species has been recorded for the Indian Ocean in Madagascar (Fauvel, 1919), and from Durban Bay, South Africa (Day & Morgans, 1956; Day, 1962, 1967). It is remarkable that despite the fact N. falsa was proposed for a species from the Black Sea, it has not been recorded there (Surugiu, 2005; Şahin & Çinar, 2012).

The reproduction and oogenesis of N. falsa were studied by Daas, Younsi, Daas-Maamcha, and Scaps (2010) and Daas, Younsi, DaasMaamcha, Gillet, and Scaps (2011). In Algeria, sexual reproduction does not include epitoky, and spawning occurred in August/September. The lack of epitoky contradicts what was regarded as typical by Fauvel (1923), and provides additional indications that more than a single species is present in the Mediterranean.

There are a few data concerning their abundance in Algeria: mean density was 11.27 ind.m-2 with a minimum of 7.83 ind.m-2 and a maximum of 14.50 ind.m-2 (Daas et al., 2011). Regarding their living substrate, N. falsa was found on chains by Fauvel (1913), rocks (Fauvel, 1937; Gillet, 1986, 1988), and hard substrates with red algae (Daas et al., 2010, 2011) but also found on soft substrates such as mud (Fauvel, 1937) and sand (Rullier & Amoureux, 1969). This species also lives on floating debris (Aliani & Molcard, 2003), and algae (Thiel & Guttov, 2005) or as an epibiont on the carapace of loggerhead turtles (Pfaller, Bjorndal, Reich, Williams, & Frick, 2006) and in mussel beds (Çinar et al., 2008). These latter findings could explain a large distribution and if all records really belong to the same biological species, there would be a low genetic variability.

Despite the fact that N. splendida might have priority over N. falsa, because the former was not well defined, the type specimen originally deposited in Berlin is lost (Hartwich, 1993: 139), and there are no other specimens in Wroclaw (Wiktor, 1980), we must follow Fauvel and regard it as indeterminable. A recent proposal for reinstating N. splendida by Núñez (2004: 375) and Alós et al. (2004: 513), probably by strict priority, should not be followed due to the lack of type material, the incomplete original description, and because it is a junior homonym.

Nevertheless, as indicated by the above analysis, there are three distributional alternatives: 1) N. falsa is an euryhaline species that can be present in the Black Sea and other Mediterranean localities and elsewhere; 2) N. falsa is restricted to the Black Sea, its type locality, and it could be regarded as resembling H. diversicolor; or 3) Two species are involved under the same name with two combinations: 3a) None live in the Black Sea and the two are common in the Mediterranean and adjacent NE Atlantic; and 3b) Non NE-Atlantic records belong to other, perhaps undescribed, species.

The first two alternatives, involving N. falsa living in the Black Sea, must be rejected. As indicated above, recent studies on Black Sea polychaetes have failed to confirm the presence of N. falsa for the type locality, and despite ecological changes since its original description, a local extinction is unlikely. Further, at least von Marenzeller (1874) and Bobretzky (1881) regarded N. falsa as a junior synonym of H. diversicolor which would somehow support the second alternative. However, two different species currently regarded as H. diversicolor were recognized in the Baltic Sea (Audzijonyte, Ovcarenko, Bastrop, & Väinölä, 2008), and three different clades that can be regarded as different species were found in European seas, with a distinct form present in the Black Sea (Virgilio, Fauvelot Constantini, Abbiati, & Backeljau, 2009).

For the third option, and its combinations, it must be reminded that two paragnath patterns in area VI are included under N. splendida - one with 4-5 paragnaths in a diamond, and one with 3 paragnaths in an inverted triangle. The next question would be, because the species name N. splendida must be rejected, how should we call the species living outside the Black Sea, and apparently present throughout at least the Mediterranean Sea? Take N. parallelogramma, which despite the fact no type was deposited, it was described and illustrated in full detail and deserves to be reinstated.

A further issue is what should we call other species resembling N. falsa from other localities? Not an easy answer, either. Regional records should be addressed in each ocean basin and by clarifying the status of type materials and track the sequence of proposed names for each region.

Finally, we concluded that, since our study was based upon publications, not on specimens, we considered that there are four desirable future steps to fully solve the N. falsa problem, and all must be based on the study of topotype or type specimens:

1. 1. Delineate H. diversicolor in the Baltic Sea after which other similar Mediterranean species can be delineated and described.
2. 2. Find a Neapolitan specimen, or series of specimens, to clarify the variation in area VI (3 vs 4 paragnaths), and then proceed to redescribe them as N. parallelogramma Claparède, 1868 (area VI with 4 paragnaths), and propose a neotype.
3. 3. Find out other specimens from the Black Sea, Sevastopol or nearby areas, and in Trieste or Naples for what was regarded by Grube as N. splendida, because its type locality was not indicated. If they consistently have area VI with 3 paragnaths, redescribe it as N. falsa and propose a neotype, because N. splendida is unavailable.
4. 4. Other non-Mediterranean records of N. falsa deserve a similar approach; some regional species names must be reinstated, as N. lucipeta for South Africa, after making a redescription and probably including the proposal for a lectotype, or if different, then full descriptions will be needed for several specimens now included as records for N. falsa.

These steps will be relevant to avoid any future confusion and will certainly depend on collective efforts by several interested scientists. Hope this note will encourage our colleagues to move towards this direction.

Biodiversity Heritage Library, Internet Archive, and la Fédération Française des Sociétés de Sciences Naturelles made available many difficult to find documents. Julia Dunaeva, from the Library of the Zoological Institute and Museum, Russian Academy of Sciences, Saint-Petersburg, provided a fine scan of Rathke’s plates, and Tulio Villalobos one of Ehlers’ plates. The careful reading and recommendations of an anonymous referee and of Daisy Cristina Arroyo Mora helped to improve this contribution.