Apatronemertes albimaculosa Wilfert and Gibson, 1974

Kajihara, Hiroshi, Takibata, Mariko & Grygier, Mark J., 2016, Occurrence and Molecular Barcode of the Freshwater Heteronemertean Apatronemertes albimaculosa (Nemertea: Pilidiophora) from Japan, Species Diversity 21, pp. 105-110 : 106-109

publication ID	https://doi.org/ 10.12782/sd.21.2.105
persistent identifier	https://treatment.plazi.org/id/0D1587EF-FFB9-FF9A-FF2C-EF742012E634
treatment provided by	Felipe
scientific name	Apatronemertes albimaculosa Wilfert and Gibson, 1974
status

Treatment

Apatronemertes albimaculosa Wilfert and Gibson, 1974 View in CoL ( Figs 1–2 View Fig View Fig )

Apatronemertes albimaculosa Wilfert and Gibson, 1974: 89–105 View in CoL , figs 1–6 [from freshwater aquaria in Düsseldorf]; Senz 1993: 74; 1998: 11–12, 30; 2003: 35, 38 [Naturhistorisches Museum Wien, NHMW-EV 3488–3491; pet-shop aquaria in Vienna, W. Senz leg. in 1988]; Smith 2001: 111, figs 5.3, 5.4 [Museum of Comparative Zoology at Harvard University, MCZ 58906; from a private home aquarium in the Brighton section of Boston, Massachusetts, USA, D. G. Smith leg. in July 1994]; Beckers 2015: fig. 4a [type specimen].

“Undescribed freshwater heteronemertean”: Andrade et al. 2012: 159 [MCZ DNA106130 View Materials ; from a freshwater fish tank in Madrid, Y. Lucas Rodriguez leg. on 30 November 2009].

Material examined. ICHUM 5112 View Materials , serial transverse sections of anterior half of body cut at 8 µm, mounted in Entellan ® New (Merck, Germany), and stained by Mallory trichrome method, 8 slides, 31 January 2010, MT leg ., among roots of freshwater plants in a private home aquarium in Takatsuki , Osaka, Japan, 29 mm long in life; ICHUM 5113 View Materials , serial transverse sections of entire animal cut at 8–10 µm and stained as above, MT leg . on 20 July 2015, siphoned up from amidst tank-bottom gravel, 10 mm long in life; LBM1340000137 View Materials , serial transverse sections of anterior half of body cut at 8–10 µm and stained as above, 5 slides, MT leg . on 15 February 2010 from the same environment, 10–12 mm long in life. For comparison, serial digital images of the transversely sectioned type slides of A . albimaculosa provided by P. Beckers were also examined .

Brief description. Body reddish pink, posteriorly paler ( Fig. 1A, C View Fig ), 1–4 cm long, up to 0.5 mm wide; epidermis with numerous rice-grain-shaped white dots ( Fig. 1B View Fig ), about 30 µm long and 10 µm wide, varying in shape and size according to body contraction and extension, these being particularly abundant in anterior half of body, but not in far anterior end; cephalic slits rudimentary; mouth situated at a distance (about 2.0–2.5 times width) from tip of head; no caudal cirrus. Precerebral vascular system with outer vessels ( Fig. 2A View Fig ). Proboscis with muscle crosses ( Fig. 2B View Fig ), presumably two in number, but this not obvious due to small size (one cross was easily observed as shown in Fig. 2B View Fig , but the presence of another was difficult to confirm). Excretory system composed of amorphous tissue distributed between alimentary canal, blood vessels, rhynchocoel, and gonads throughout postcerebral region ( Fig. 2C View Fig ). Hermaphroditic; testes 50–80 µm in diameter ( Fig. 2C View Fig ), only found in foregut region and near posterior tip of body, largely absent in intestinal region; single oocyte, up to 250 µm in diameter, contained in each ovary ( Fig. 2D View Fig ), latter arranged in row on each side throughout intestinal region; about 50 ovaries present in each row in ICHUM 5113 (complete specimen of 10 mm body length). In life, posteriorly-moving peristaltic waves of body thickening and thinning observed in anterior region of ICHUM 5112.

Remarks. Wilfert and Gibson (1974) reported that the largest specimen from Düsseldorf reached 12 cm in body length, which is three times greater than the longest specimen we observed. They reported the red pigmentation to be darker posterior whereas in our material the posterior region was palest. The minute white spots in the epidermis ( Fig. 1B View Fig ), to which the specific name refers, are noticeable only when observed with higher magnification in the living state, and probably represent glandular cells. As Wilfert and Gibson (1974) suggested, they do not represent flecks of white pigment, but are bodies only slightly less translucent than the surrounding tissue, and their appearance depends on the illumination. They are most clearly seen on the body margins in tangential view when the worm is viewed by incident light (not visible at all by transmitted light), appearing as somewhat translucent-pale granules against the pink background. They are, however, visible over the whole body surface when illuminated by horizontally directed strobe lights for photography (e.g., Fig. 1B View Fig ). In our specimens they seem distinctly smaller than the “numerous white spots of about 50–200 µm in diameter” noted by Wilfert and Gibson (1974: 90), and also uniform in size. Similar white spots are, in any case, often found in other, marine species (e.g., Ototyphlonemertes spp. ), imparting a velvety appearance to the epidermis, and thus are not specific for A. albimaculosa .

In general, the precerebral vascular system in heteronemerteans is comprised of a single lacunar tube either hanging over or lying just beneath the rhynchodaeum, or a pair of vessels on both sides flanking the rhynchodaeum, or a mixture of these conditions. In A. albimaculosa , however, on each side an additional, narrow vessel [=‘outer vessel’ in Wilfert and Gibson’s (1974) terminology] lies lateral to the normal, main vessel [‘inner vessel’] ( Fig. 2A View Fig ); therefore, four vessels can be found in a cross section, while the outer vessels merge with the inner vessels at their anterior end and also in the brain region. Such a complex precerebral vascular system has never been reported in any other heteronemertean, and thus can be regarded as a species-specific character for A. albimaculosa . The presence of the outer vessels in our material thus strengthens our conclusion about the species identification despite the coloration differences noted above.

In marine heteronemerteans, the excretory system typically consists of collecting tubules that are often ramified and closely associated with blood vessels in the foregut region, leading to paired efferent ducts that open to the exteri- or through the epidermis ( Oudemans 1885). In contrast, the excretory system of A. albimaculosa comprises amorphous tissue spread among various internal organs and discharges into the intestine via numerous specialized cells with granular contents ( Fig. 2D View Fig ). Similar tissue has been reported in the freshwater heteronemertean Amniclineus zhujiangensis Gibson and Qi, 1991 and the brackish-water heteronemertean Yininemertes pratensis ( Sun and Lu 1998) , which suggests that this morphology is the result of adaptation to a low-salinity environment.

In freshwater forms, hermaphroditism is common among hoplonemerteans ( Gibson and Moore 1976) but has rarely been confirmed among heteronemerteans. Of the six species of fresh- and brackish-water heteronemerteans, only A. albimaculosa is known to be hermaphroditic: A. zhujiangensis and Y. pratensis are dioecious ( Gibson and Qi 1991; Sun and Lu 1998), sexually mature Planolineus exsul Beauchamp, 1928 and Siolineus turbidus Du Bois-Reymond Marcus, 1948 have been found only as females ( Beauchamp 1928, 1929; Du Bois-Reymond Marcus 1948), and Hinumanemertes kikuchii Iwata, 1970 is known only by an immature specimen ( Iwata 1970; Chernyshev 2014). That our material was hermaphroditic ( Fig. 2C, D View Fig ) lends support to our interpretation of its specific identity.

Unexpectedly, a BLAST search ( Altschul et al. 1990) of the partial COI sequence from the Japanese specimen ( LC095809 View Materials ) at the NCBI website (http://blast.ncbi.nlm.nih. gov) yielded a complete match (100% in query cover and identity) with HQ848584 from an “undescribed freshwater heteronemertean” ( Andrade et al. 2012) that was collected in a freshwater fish tank in Madrid, Spain, with voucher DNA deposited in MCZ (MCZ DNA106130). From this specimen, Andrade et al. (2012) also provided sequences of other gene markers: JF293030 (18S rRNA), HQ856860 (28S rRNA), JF277733 (histone H3), JF277666 (histone H4), and JF277587 (16S rRNA). We think it reasonable to identify this Spanish specimen as A. albimaculosa based on the complete match of its COI sequence with that of our material. So far as we are aware, this represents the first example of retrospective identification by molecular sequence of nemerteans in public databases that have been left unidentified to the species level. The presence of a myriad of such unidentified barcoding sequences of various groups of organisms in GenBank can be important in biodiversity studies, if correct taxonomy is provided post hoc. The assertion that “DNA barcoding should accompany taxonomy” ( Sundberg et al. 2010: 274) is thus true here.

It is likely that A. albimaculosa has been living in freshwater aquaria all around the world where commercially distributed tropical water plants are grown. While Wilfert and Gibson (1974) observed a particular association of A. albimaculosa with the roots of Vallisneria spiralis , this plant species was not cultured in MT’s aquaria. Instead, on one occasion, two worms were simultaneously found among roots of Potamogeton perfoliatus . The other water-plant species hitherto cultured in MT’s water tanks, which must be regarded as additional potential carrier(s) of A. albimaculosa , include Anubias barteri Schott var. nana (Engl.) Crusio , Bacopa caroliniana B. L. Rob. , Cabomba caroliniana A. Gray , Echinodorus amazonicus Rataj , Egeria densa Planch. , Helanthium bolivianum (Rusby) Lehtonen and Myllys , Hemianthus micranthemoides Nutt. , Hemianthus callitrichoides Griseb. , Hydrocotyle verticillata Thunb. , Lindernia anagallis (Burm. f.) Pennell, Ludwigia glandulosa Walter , Nymphaea sp. , Nuphar japonica DC , Ranalisma humile (Kuntze) Hutch. , Rotala rotundifolia (Roxb.) Koehne , Rotala sp. , and Vesicularia sp. However, because most of the worms in our study were found suctioned from aquarium gravel while cleaning, MT’s impression is that they dwell in the sediment as infauna, rather than having a specific association with water-plant roots.

We suggested above that A. albimaculosa shows poor resistance to cold temperatures since some specimens died in transit when sent to Sapporo. However, anecdotal evidence suggests it can survive conditions colder than 10°C for a few days. A specimen collected on 30 January 2010 from one of MT’s aquaria became whitish and stopped locomotion in the morning on 4 February 2010, having survived for five or six days after being placed in a small plastic cup filled with water from the same aquarium and left at room temperature (about 10°C, but it could have been much colder in the morning) (M. Takibata pers. obs.). Another specimen collected on 3 March 2010 and kept under the same conditions decayed and vanished on 7 March 2010, having lived for four or five days (M. Takibata pers. obs.). A specimen collected on 27 May 2016 died within 12 h after being placed in a refrigerator at 4–6°C. Therefore, even if they were released into the wild, they would be unlikely to become established in temperate or even subtropical areas where the lowest water temperature falls below 10°C for more than a week.

Except for Siolineus turbidus from the Rio Tapajós, a tributary of the Amazon, and A. albimaculosa with an un- known place of origin, the rest of the freshwater/brackishwater heteronemerteans known to date are all distributed in Asia: P. exsul in Bogol, Indonesia ( Beauchamp 1928, 1929); an unidentified form from Taiwan, reported by Takakura (1932) (for English translation see Kajihara 2004); H. kikuchii from Lake Hinuma, Japan ( Iwata 1970) and Primorsky Krai, Russia ( Chernyshev 2014); A. zhujiangensis in the lower part of the Zhujiang (Pearl) River, China ( Gibson and Qi 1991); and Y. pratensis from the Chiangjiang (Yangtze) River Estuary, China ( Sun and Lu 1998). The ‘fatherland’ of Apatronemertes may also be somewhere in tropical Asia.