Research Article |
Corresponding author: Tatiana Sitnikova ( tata-sitnikova@mail.ru ) Academic editor: Edmund Gittenberger
© 2018 Tatiana Sitnikova, Tatiana Peretolchina.
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:
Sitnikova T, Peretolchina T (2018) Description of a new species Gyraulus (Pulmonata: Planorbidae) from the land thermal spring Khakusy of Lake Baikal. ZooKeys 762: 1-12. https://doi.org/10.3897/zookeys.762.23661
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A new species of the family Planorbidae is described from the land thermal spring Khakusy, on the north-eastern shore of Lake Baikal. The description of Gyraulus takhteevi sp. n. includes morphological characters and gene sequences (COI of mtDNA) for the species separation from sister taxon Gyraulus acronicus (A. Férussac, 1807) collected from the small Krestovka River in-flowing into the south-western part of the Lake. The new species differs from G. acronicus in small shell size of adults, having smaller number of prostate folds (maximal up to 26 in G. takhteevi n. sp. vs. 40 in G. acronicus), a short preputium (approximately twice shorter than the phallotheca), and an elongated bursa copulatrix. The population of Gyraulus takhteevi sp. n. consists of two co-existent morphs: one of them has a narrow shell spire and the second is characterized by wide spire similar to the shell of G. acronicus. One of the two revealed haplotypes of the new species includes both morphs, while the second consists of snails with wide spired shells.
COI mtDNA, morphology, planorbid gastropods
The thermal spring Khakusy is located one kilometer from the shore in the north-eastern part of Lake Baikal and flows into it. The chemical composition of the water is hydrocarbonate-sulphate-sodium with a salinity of 0.3 g/l; the water temperature of the mainstream is + 47 °C (
Two hundred fourteen specimens of a new species were collected in the thermal spring Khakusy (north-eastern shore of Lake Baikal (55°21'42"N, 109°49'41"E), from pebbles covered by vegetation, mainly filamentous cyanobacterial mats. The samples were collected on 30 March 1990 (13 specimens) from spring with a water temperature of +31 °C, and 39 specimens from slightly downstream with water temperature at +22 °C by V. Takhteev; 3 July 2003 (6 spec.) by T. Sitnikova; 7 October 2004 (23 specimens) by V. Takhteev; 9 August 2009 (14 specimens, 6 dissected) by T. Sitnikova, 20 March 2003 (61 specimens) by V. Takhteev; 8 June 2015 (53 spec., 8 dissected) by T. Peretolchina, and July 2017 (5 specimens, 1 dissected) by T. Sitnikova.
The 60 adult specimens of the new species were compared with seven individuals of the Gyraulus acronicus (A. Férussac, 1807) collected in a small inflow of the Krestovka River (51°51'44"N, 104°51'11"E) on 13 October 2015 and 2 October 2017 by T. Sitnikova; 4 of these specimens were dissected. The holotype and paratypes of the newly described species were deposited in the collection of the Zoological Institute RAS (St. Petersburg), registration numbers are 522-2015 (1) for the holotype and 522-2015 (2) for three paratypes . An additional 28 paratypes were deposited in the gastropod collection of the Limnological Institute SB RAS (Irkutsk, Russia) under Nos: 901, 902, 1101, and 1102.
Anatomical study and molecular analyses were performed on snails fixed in 80% ethanol that was changed for 70% ethanol after one day. Eight snails were photographed and the shells of 12 individuals were dissected. DNA was extracted from the feet; the teeth of radula were SEM-photographed and the soft tissues were dissected under a light stereomicroscope. Morphological study and descriptive terminology are based on the review of morphological characters of planorbid gastropods (
Genomic DNA was extracted from muscle tissue using a modified method from
Taxa used for phylogenetic analyses, with their GenBank Accession Numbers and references.
Species name | COI GB# | 16S GB# | References |
---|---|---|---|
G. albus | KC495835 | KC495952 | Oheimb et al. (2013) |
G. crista | KC495836 | KC495953 | |
G. rossmaessleri | KC495714 | KC495844 | |
G. connollyi | KC495776 | ||
Gyraulus sp. | KC495834 | KC495951 | |
G. convexiusculus | KF966542 | Unpublished | |
G. acronicus, Krestovaya River | Present study | ||
a435 | MG773536 | ||
a430 | MG773535 | MG800654 | |
Gyraulus takhteevi sp. n. (haplotype 1) | Present study | ||
401_n | MG773534 | ||
a437_w | MG773537 | ||
442_w | MG773541 | ||
443_w | MG773542 | ||
439_n | MG773539 | ||
438_n | MG773538 | ||
444_w | MG773543 | ||
441_n | MG773540 | ||
445_w | MG773544 | ||
Gyraulus takhteevi sp. n. (haplotype 2) | Present study | ||
425 _w | MG773531 | ||
429_w | MG773533 | ||
427_w | MG773532 | MG800655 |
Mean pairwise, inter-specific p-distances between COI and 16S sequences were calculated using MEGA 6 (
Phylogenetic reconstructions for COI mtDNA was inferred following a Bayesian method of phylogenetic inference as implemented by MrBayes v. 3.2.2 (
Gyraulus
cf.
borealis
:
Thermal spring Khakusy (East Siberia).
Holotype (dry) registration number in ZIN collection (St. Petersburg, Russia) is 522-2015 (1), 3 paratypes (dry) registration number is 522-2015 (2) with a label: ‘East-northern shore of Lake Baikal, thermal spring Khakusy, pebbles, water temperature 23–25 °C, #0957, col. T. Sitnikova, 09.08.2009’. Collections of the Limnological Institute SB RAS (Irkutsk, Russia): 2 paratypes (dry) under numbers 901 and 902 with the label: ‘Khakusy, shallow springs at a depth down to 3 cm, water temperature 33 °C, col. V. Takhteev, #57, 07.10.2004’; 20 paratypes (in alcohol) under number 1101 with a label ‘Khakusy, #1526, 08.06.2015, col. T. Peretolchina’ and 4 paratypes (dry) and 2 paratypes (in alcohol) under number 1102 collected 3 July 2003, #0344, T. Sitnikova.
The species name ‘takhteevi’ is in honor of the Russian zoologist and hydrobiologist Prof. V.V. Takhteev (Irkutsk State University) who investigates biota of thermal springs in East Siberia.
Shell (Fig.
Shell dimensions and whorl counts of type specimens of Gyraulus takhteevi sp. n. Abbreviations: SH – height of shell; SW– width of shell; b – width of last whorl without aperture; a – height of this whorl; SpW – width of spire; AW – width of aperture; AH – height of aperture; n – number of whorls. Measurements are in mm except for number of whorls.
Specimens/Character | SW | SH | SpW | b | a | AW | AH | n |
---|---|---|---|---|---|---|---|---|
Holotype | 4.31 | 1.68 | 1.23 | 3.01 | 1.27 | 1.67 | 1.20 | 3.75 |
Paratypes (narrow spire) | 4.03 | 1.42 | 1.25 | 2.78 | 1.21 | 1.64 | 1.25 | 3.75 |
3.57 | 1.5 | 1.10 | 2.4 | 1.17 | 1.67 | 1.42 | 3.5 | |
3.45 | 1.5 | 1.0 | 2.37 | 1.12 | 1.26 | 1.19 | 3.25 | |
(wide spire) | 5.2 | 1.6 | 1.93 | 3.8 | 1.3 | 1.5 | 1.45 | 4.0 |
4.45 | 1.7 | 1.54 | 3.24 | 1.18 | 1.5 | 1.31 | 3.75 | |
4.1 | 1.65 | 1.3 | 2.9 | 1.1 | 1.5 | 1.4 | 3.5 |
Pairwise p-distances (%) between COI sequences of different species of the genus Gyraulus.
Taxa | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 |
---|---|---|---|---|---|---|---|---|---|
1. G. acronicus Krestovaya | |||||||||
2. Gyraulus takhteevi sp. n.(haplotype 1) | 0.8 | ||||||||
3. G. takhteevi sp. n. (haplotype 2) | 1.0 | 0.2 | |||||||
4. Gyraulus sp. KC495834 (Lake Baikal) | 0.7 | 1.5 | 1.3 | ||||||
5. G. albus | 6.9 | 7.0 | 6.9 | 6.9 | |||||
6. G. rossmaessleri | 11.0 | 11.0 | 10.8 | 10.6 | 11.3 | ||||
7. G. convexius | 10.5 | 10.8 | 10.8 | 10.6 | 7.4 | 12.6 | |||
8. G. crista | 12.3 | 12.6 | 12.6 | 12.4 | 12.8 | 11.6 | 12.4 | ||
9. G. connollyi | 11.5 | 11.5 | 11.3 | 11.5 | 8.8 | 12.6 | 9.0 | 14.7 |
Shells of type specimens of Gyraulus takhteevi sp. n. and G. acronicus Férussac, 1807). A Holotype G. takhteevi sp. n. B–E Paratypes G. takhteevi sp .n. A–C morph 1 with narrow spire D, E morph 2 with wide spire F–G G. acronicus from Krestovka River: F young individual F mature individual after 5 months of a cultivation. Abbreviations: a – aperture view; b – right side with umbilicus, c – left side with spire. Scale bar 1 mm.
Radular teeth. The formula of the radula is 10 (9)–1–(9) 10. The central radular teeth are bicuspid with two equal-sized cusps. Two first lateral teeth usually bicuspid, sometimes with third small cusp. Other teeth have three rounded cusps, and only young (not working or worn) tricuspid teeth have three long sharp cusps. Mesocone is flanked (Fig.
Reproductive system. Seminal vesicles have thickened bend before joining with hermaphrodite duct, which is thin up to carrefour. Prostate consists of 22–26 diverticula, bursa copulatrix is oval in shape, its length including duct more than ½ length of oviduct. Length of copulatory organ almost equal to length of prostate (Fig.
Egg mass (= cluster or syncapsula) is a round transparent sac less than 1 mm in size, consisting of 4-5 eggs (Fig.
The new species (especially morph 2 with wide spire) is similar to the Palaearctic species G. acronicus (Fig.
Snails similar to morph 1 of the new species were also found in the thermal spring Frolikha located near to Khakusy (ca. 20 km north); all of them were young and were not examined in detail. The number of gastropods in the thermal spring Khakusy in March 2016 was 1,706 individuals/m2 at water temperature +29 °C in a locality 2 m far from the main source; a minimal number of snails (59 indv./m2) was registered at water temperature +10 °C in a small pond downstream of the main source (Epova et al. 2017). The proportions of G. takhteevi sp. n. and Lymnaea were about fifty-fifty.
The confinement of morphs to different sites of the thermal spring has not been confirmed. The population of G. takhteevi consists mainly of young snails, in which the morph with a narrow spire dominated: in July 2003 28 of the 39 collected snails were juvenile, with adults presented by six snails with shells of narrow spire (morph 1) and five individuals with wide spire (morph 2). In June 2015 there were 16 individuals of morph 1 and eleven specimens of morph 2, with more than 50 young snails; in March 2016 39 young specimens were collected and 16 adult snails of morph 1 and six individuals of morph 2.
The cultivation of the new species under summer conditions of ephemeral waterbodies (sand, pebbles, water temperature +20–24 °C, food items of vegetable fodder) was not successful, and all snails died in two weeks. It is worth noting that specimens of G. acronicus under the same conditions lived more than one year and reproduced, attached their egg masses to pebbles. According to the interruption lines on shells, the snails live up to 5 years.
A total 14 COI (620 bp long) and 14 16S (500 bp long) sequences were produced. Inspection of the sequences revealed the existence of two unique haplotypes for COI among G. takhteevi sp. n. These haplotypes weakly differ from each other (in 1–2 nucleotide substitutions). Both morphs (shells with narrow or wide spire) are part of the haplotype 1, while haplotype 2 consists of the morph with wide spire shell (Fig.
The haplotype of G. acronicus from Krestovka River shares the same clade as Gyraulus sp., sequence of which is retrieved from GenBank (KC495834), which differs from that of G. takhteevi sp. n. with 5–6 nucleotide substitutions (~ 1%).
Despite the small genetic distances between G. takhteevi sp. n. and G. acronicus, morphological differences between them (shell size of mature individuals, maximal number of prostate folds, length of the phalloteka relative to length of the prepuceum, length of a stylet, shape of the bursa copulatrix) allow one to consider them as separate species. Moreover, the new species demonstrates significant adaptation to a specific habitat of the thermal spring Khakusy. The water in the spring does not freeze in winter, the temperature of the water changes very little, and the food items like microorganisms, bacterial mats, and vegetable detritus are present during all seasons of a year. However, the two co-existent morphs of G. takhteevi sp. n. are likely to correspond to two interbreeding generations, hatching from eggs, growth and reproduction of which are confined to different seasons. The co-existence of both morphs appears to be constantly maintained, since they have been found over several years of the investigation.
The low level of genetic distances between G. takhteevi sp. n. and G. acronicus from the Krestovka River indicates that a recent divergence of the species happened after the glaciers covering large areas of the northeast coast of Baikal during last glacial period started to melt about 18 kyr BP (
We are grateful to Mr. V.I. Egorov for assistance with the scanning electron microscope equipment (Electron Microscope Centre of Collective Instrumental Centre “Ultra microanalysis” at Limnological Institute SB RAS). We are grateful to the reviewer and Dr E. Soldatenko for comments and advices that have improved the content of the article. The study was partly supported by the governmentally funded projects Nos. 0345-2016-0009 (AAAA-A16-116122110067-8) (morphological investigations), 0345-2016-0004 (AAAA-A16-116122110060-9) (molecular analysis), and Russian Foundation for Basic Research, project No 15-29-02515.