Research Article |
Corresponding author: Svante Martinsson ( svante.martinsson@gu.se ) Academic editor: Samuel James
© 2015 Svante Martinsson, Emilia Rota, Christer Erséus.
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:
Martinsson S, Rota E, Erséus C (2015) On the identity of Chamaedrilus glandulosus (Michaelsen, 1888) (Clitellata, Enchytraeidae), with the description of a new species. ZooKeys 501: 1-14. https://doi.org/10.3897/zookeys.501.9279
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The taxonomy of Chamaedrilus glandulosus (Michaelsen, 1888) s. l., most commonly known previously as Cognettia glandulosa, is revised. A recent molecular systematic study has shown that this taxon harbours two cryptic, but genetically well separated lineages, each warranting species status. In this study these two lineages are scrutinized morphologically, on the basis of Michaelsen’s type material as well as newly collected specimens from Central and Northern Europe. Chamaedrilus glandulosus s. s. is redescribed and Ch. varisetosus sp. n. is recognized as new to science. The two species are morphologically very similar, differing mainly in size, but seem to prefer different habitats, with Ch. glandulosus being a larger aquatic species, and Ch. varisetosus being smaller and mainly found in moist to wet soil.
Cognettia, Chamaedrilus, cryptic species, Oligochaeta, taxonomy
In
Several cryptic forms have been found within well-known morphology-based taxa of former Cognettia (
The aim of this study is to revise the taxonomy of Chamaedrilus glandulosus s. l. by delimiting Ch. glandulosus s. s., with the designation of a lectotype, and describing Ch. varisetosus sp. n.
This study is based on two syntypes of Pachydrilus sphagnetorum var. glandulosus Michaelsen, 1888, from the original syntype series of ten, borrowed from the Zoological Museum of Hamburg University (ZMUH), Germany, of which one is here designated as lectotype, plus material analysed by
List of material included in this study, with specimen identification numbers, voucher numbers, collection data, GPS coordinates, and GenBank accession numbers for COI barcodes. Voucher numbers in bold indicate type specimens, barcode numbers in bold are newly generated sequences. Locality data are given in the form: country, province, municipality and locality; GPS coordinates are given as decimal degrees. CZ = Czech Republic, FIN = Finland, GER = Germany, NOR = Norway, SWE = Sweden.
Species | Spm. nos. | Museum voucher nos. | Sexual maturity | Collection locality | Coordinates | Leg. | Coll. date | Barcode Acc. nos. | |
---|---|---|---|---|---|---|---|---|---|
N | E | ||||||||
Ch. glandulosus | ZMUH V 429a | mature | GER. Hamburg, Hamburg, Bille River bank | 53.54 | 10.09 | W. Michaelsen | Pre 1888 | - | |
Ch. glandulosus | ZMUH V 429b | immature | GER. Hamburg, Hamburg, Bille River bank | 53.54 | 10.09 | W. Michaelsen | Pre 1888 | - | |
Ch. glandulosus | CE2011 | SMNH133613 | immature | SWE. Västergötland, Vårgårda, Lången Lake littoral | 57.9973 | 12.5868 | C. Erséus | Jun 30 2006 | KF672372 |
Ch. glandulosus | CE2841 | SMNH133614 | immature | SWE. Öland, Borgholm, Räpplinge, stream | 56.8195 | 16.9444 | A. Ansebo, L. Matamoros & C. Erséus | Jun 13 2007 | KF672374 |
Ch. glandulosus | CE2887 | SMNH133615 | submature | SWE. Södermanland, Vingåker, Låttern Lake littoral | 59.0854 | 16.0426 | C. Erséus | Jul 30 2007 | KF672375 |
Ch. glandulosus | CE2888 | SMNH133616 | submature | SWE. Södermanland, Vingåker, Låttern Lake littoral | 59.0854 | 16.0426 | C. Erséus | Jul 30 2007 | KF672376 |
Ch. glandulosus | CE2889 | SMNH133617 | immature | SWE. Södermanland, Vingåker, Låttern Lake littoral | 59.0854 | 16.0426 | C. Erséus | Jul 30 2007 | KF672377 |
Ch. glandulosus | CE2890 | SMNH133618 | immature | SWE. Södermanland, Vingåker, Låttern Lake littoral | 59.0854 | 16.0426 | C. Erséus | Jul 30 2007 | KF672378 |
Ch. glandulosus | CE2891 | SMNH133619 | immature | SWE. Södermanland, Vingåker, Låttern Lake littoral | 59.0854 | 16.0426 | C. Erséus | Jul 30 2007 | KF672379 |
Ch. glandulosus | CE8510 | SMNH133620 | immature | SWE. Lappland, Kiruna, Abisko, marsh pond | 68.3485 | 18.9719 | D. Fontaneto | Jul 6 2007 | JN260143 |
Ch. glandulosus | CE10655 | SMNH133612 | immature | FIN. Keski-Suomi, Jyväskylä, Alvajärvi Lake littoral | 62.315 | 25.730 | H. Saarikoski | Fall 2009 | JN260270 |
Ch. glandulosus | CE17761 | SMNH142041 | immature | SWE. Södermanland, Vingåker, Hjälmaren Lake littoral | 59.133 | 15.814 | C. Erséus | Jul 27 2012 | KP878475 |
Ch. glandulosus | CE17806 | SMNH142042 | immature | SWE. Södermanland, Vingåker, Hjälmaren Lake littoral | 59.133 | 15.814 | C. Erséus | Jul 27 2012 | KP878476 |
Ch. glandulosus | CE18516 | SMNH142043 | submature | SWE. Västergötland, Lerum, Aspen Lake littoral | 57.7656 | 12.2525 | C. Erséus & B. Williams | Jun 1 2013 | - |
Ch. glandulosus | CE18517 | SMNH142044 | mature | SWE. Västergötland, Lerum, Aspen Lake littoral | 57.7656 | 12.2525 | C. Erséus & B. Williams | Jun 1 2013 | KP878477 |
Ch. glandulosus | CE18518 | SMNH142045 | immature | SWE. Västergötland, Lerum, Aspen Lake littoral | 57.7656 | 12.2525 | C. Erséus & B. Williams | Jun 1 2013 | KP878478 |
Ch. glandulosus | CE20212 | SMNH142046 | immature | NOR. Östfold, Halden, Enningdalselva River | 58.9099 | 11.5210 | C. Erséus | Oct 12 2013 | KP878474 |
Ch. varisetosus | CE2634 | SMNH133600 | immature | SWE. Öland, Borgholm, S Greda, sandy soil | 56.9929 | 16.8765 | A. Ansebo, L. Matamoros & C. Erséus | Jun 12 2007 | KF672367 |
Ch. varisetosus | CE2931 | SMNH133601 | immature | SWE. Öland, Borgholm, Egby, peaty soil | 56.8621 | 16.8539 | A. Ansebo, L. Matamoros & C. Erséus | Jun 12 2007 | KF672368 |
Ch. varisetosus | CE4027 | SMNH133602 | immature | SWE. Skåne, Ystad, Nyvangsskogen, wet soil | 55.5606 | 13.8239 | C. Erséus | May 31 2008 | KF672369 |
Ch. varisetosus | CE4028 | SMNH133603 | immature | SWE. Skåne, Ystad, Nyvangsskogen, wet soil | 55.5606 | 13.8239 | C. Erséus | May 31 2008 | KF672370 |
Ch. varisetosus | CE6626 | SMNH133604 | immature | SWE. Uppland, Vallentuna, Brottby,peaty soil | 59.5477 | 18.2467 | C. Erséus | Jun 4 2009 | KF672371 |
Ch. varisetosus | CE9376 | SMNH133605 | immature | SWE. Medelpad, Timra, Söråker, forest soil | 62.5235 | 17.4782 | C. Erséus | Jun 8 2010 | KF672424 |
Ch. varisetosus | CE9517 | SMNH133606 | immature | SWE. Lappland, Kiruna, Björkliden, peat | 68.4262 | 18.3509 | C. Erséus | Jun 12 2010 | JN260194 |
Ch. varisetosus | CE9524 | SMNH133607 | immature | SWE. Lappland, Kiruna, Björkliden, river | 68.4277 | 18.4448 | C. Erséus | Jun 12 2010 | KF672425 |
Ch. varisetosus | CE9525 | SMNH133608 | immature | SWE. Lappland, Kiruna, Björkliden, river | 68.4277 | 18.4448 | C. Erséus | Jun 12 2010 | JN260195 |
Ch. varisetosus | CE9526 | SMNH133609 | immature | SWE. Lappland, Kiruna, Björkliden, river | 68.4277 | 18.4448 | C. Erséus | Jun 12 2010 | JN260282 |
Ch. varisetosus | CE9536 | SMNH133610 | immature | SWE. Lappland, Kiruna, Kiruna, forest soil | 67.8546 | 20.2173 | C. Erséus | Jun 13 2010 | JN260198 |
Ch. varisetosus | CE9581 | SMNH133611 | immature | SWE. Lappland, Vilhelmina, Klimpfjäll, grassland soil | 65.0621 | 14.8066 | C. Erséus | Jun 15 2010 | JN260206 |
Ch. varisetosus | CE11485 | SMNH142026 | immature | SWE. Västergötland, Lerum, Almekärr, wet soil | 57.7614 | 12.2706 | C. Erséus & A. Achurra | Apr 23 2011 | KP878462 |
Ch. varisetosus | CE18904 | SMNH142027 | immature | NOR. Telemark, Hjartdal, Kovstulheia, stream | 59.8182 | 8.7222 | C. Erséus & B. Williams | Jun 13 2013 | KP878463 |
Ch. varisetosus | CE19031 | SMNH142028 | immature | NOR. Telemark, Kviteseid, Kviteseid, wet forest litter | 59.3532 | 8.5196 | C. Erséus & B. Williams | Jun 13 2013 | KP878460 |
Ch. varisetosus | CE19052 | ZMBN99905 | mature | NOR. Buskerud, Hol, Örtedalsåna River, wet moss | 60.4866 | 7.8562 | C. Erséus | Aug 10 2013 | KP878464 |
Ch. varisetosus | CE19113 | SMNH142029 | immature | NOR. Buskerud, Hol, Geilo, forest soil | 60.5329 | 8.2113 | C. Erséus | Aug 11 2013 | KP878465 |
Ch. varisetosus | CE19117 | SMNH142030 | immature | NOR. Buskerud, Hol, Geilo, forest soil | 60.5329 | 8.2113 | C. Erséus | Aug 11 2013 | KP878466 |
Ch. varisetosus | CE19677 | SMNH142031 | immature | NOR. Sör-Tröndelag, Tydal, Langsvola, litter | 62.8388 | 11.805 | C. Erséus | Aug 14 2013 | KP878467 |
Ch. varisetosus | CE19716 | SMNH142032 | immature | NOR. Sör-Tröndelag, Röros, Hitterdalen, stream bank | 62.6060 | 11.6599 | C. Erséus | Aug 15 2013 | KP878461 |
Ch. varisetosus | CE19749 | SMNH142033 | immature | NOR. Sör-Tröndelag, Röros, Doktortjönna Lake shore | 62.5763 | 11.3745 | C. Erséus | Aug 15 2013 | KP878468 |
Ch. varisetosus | CE19818 | ZMBN99906 | submature | NOR. Hedmark, Engerdal, Nymoen, wet moss | 61.6569 | 11.8164 | C. Erséus | Aug 15 2013 | KP878469 |
Ch. varisetosus | CE19819 | SMNH Type-8732 | submature | NOR. Hedmark, Engerdal, Nymoen, wet moss | 61.6569 | 11.8164 | C. Erséus | Aug 15 2013 | KP878470 |
Ch. varisetosus | CE19823 | SMNH142034 | immature | NOR. Hedmark, Engerdal, Nymoen, wet moss | 61.6569 | 11.8164 | C. Erséus | Aug 15 2013 | KP878471 |
Ch. varisetosus | CE19831 | SMNH142035 | immature | NOR. Hedmark, Engerdal, Nymoen, wet moss | 61.6569 | 11.8164 | C. Erséus | Aug 15 2013 | KP878472 |
Ch. varisetosus | CE19832 | SMNH142036 | immature | NOR. Hedmark, Engerdal, Nymoen, wet moss | 61.6569 | 11.8164 | C. Erséus | Aug 15 2013 | KP878459 |
Ch. varisetosus | CE20021 | SMNH142037 | immature | NOR, Östfold, Hvaler, Asmalöy, dry soil | 59.0630 | 10.9396 | C. Erséus | Sep 22 2013 | KP878473 |
Ch. varisetosus | CE20046 | SMNH142038 | immature | NOR. Östfold, Fredikstad, Trosvik, litter on clay | 59.2364 | 10.9012 | C. Erséus | Sep 23 2013 | KP878479 |
Ch. varisetosus | SM171 | SMNH142039 | immature | CZ. NW Moravia, Okres Šumperk, Králický Sněžník, moss in stream | 50.1499 | 16.8624 | K. Elliott & S. Martinsson | Jun 15 2013 | KP878457 |
Ch. varisetosus | SM172 | SMNH142040 | immature | CZ. NW Moravia, Okres Šumperk, Králický Sněžník, moss in stream | 50.1499 | 16.8624 | K. Elliott & S. Martinsson | Jun 15 2013 | KP878458 |
Newly collected specimens were DNA-barcoded using the cytochrome c oxidase subunit I (COI) marker, as described by
Unless otherwise mentioned in the descriptions, all information refers to the studied material only, in that the two taxa treated in this paper have previously been classified as one and the same species. Michaelsen’s syntypes were first studied as temporary mounts in glycerol. The newly designated lectotype was then stained with paracarmine and permanently mounted in Canada balsam on a slide as outlined by
Boxplots showing differences in body size between Chamaedrilus glandulosus (Michaelsen, 1888) sensu stricto and Ch. varisetosus sp. n. A Length of 20 anteriormost segments B Width in segment XII. Both differences are significant (two-sided t-tests; P = 1.5E-5 and P = 5.5E-5, respectively).
The geographical distributions consider the origin of our material as well as that of COI barcode matches in BOLD (Barcoding of Life Data Systems,
All specimens studied, including new types, are deposited in the Swedish Museum of Natural History (SMNH), Stockholm, the University Museum Bergen (UMB), Norway, and the Zoological Museum Hamburg (ZMUH), Germany; all COI barcodes are deposited in GenBank (see Table
Pachydrilus sphagnetorum var. glandulosus Michaelsen, 1888: 490, plate 23, fig. 2a–c.
Marionia sphagnetorum var. glandulosa; Michaelsen 1889: 29.
Marionina glandulosa;
Chamaedrilus glandulosus;
Enchytraeoides glandulosa;
Cognettia glandulosa;
Cognettia glandulosa B;
ZMUH V 429a, mature anterior part, in alcohol, leg. W. Michaelsen, date not given (before 1888).
GERMANY: Hamburg, banks of Bille River, in detritus (“Billeufer, im Detritus”) (N 53.54°, E 10.09°).
ZMUH V 429b, immature specimen, in alcohol; same collection data as for lectotype.
(not studied). Paralectotypes ZMUH V 429b, 8 specimens in alcohol, same collection data as for lectotype.
See Table
Can be separated from all other European species of Chamaedrilus except Ch. varisetosus by its unique combination of 2–4 pairs of well-developed secondary pharyngeal glands, two chaetae per lateral bundle in preclitellar segments, and three chaetae in all other bundles, spermathecae with comparatively long ectal ducts, and genitalia shifted forward 3–4 segments (in relation to normal placement in Enchytraeidae). No characters completely separate this species from Ch. varisetosus sp. n., but specimens of Ch. glandulosus are usually larger and have only two chaetae in the lateral bundles of preclitellar segments, whereas Ch. varisetosus usually has three chaetae in lateral bundles of III-V. Furthermore, Ch. glandulosus is found in aquatic habitats only (i.e. submerged under water for most of the time), whereas Ch. varisetosus is found in both aquatic and terrestrial habitats; so far we have not found them occurring together.
EXTERNAL CHARACTERS: Size: length of 20 anteriormost segments 3.49-6.68 mm, mean 4.55±0.87 (n=11); body width in XII 0.24–0.56 mm, mean 0.42±0.10 (n = 14). Chaetae sigmoid without nodulus, 60–100 µm long, chaetal formula 2,(3)-3:3-3, with 3 lateral chaetae per bundle from VII-IX; in sexually mature specimens, ventral chaetae, or both ventral and lateral chaetae, missing in the segment bearing male pores (VIII or IX). In the sexually mature and submature specimens examined, clitellum poorly developed.
INTERNAL CHARACTERS: Brain concave posteriorly, 160–210 µm long. Pharyngeal glands 3–4 primary pairs; 2–4 pairs of well-developed secondary glands (Fig.
Chamaedrilus glandulosus (Michaelsen, 1888) sensu stricto. A Anterior part of body (immature specimen) in lateral view, indicating chaetal distribution and the size, shape and number of pharyngeal glands B Sperm funnel, ental tract of vas deferens and penial bulb, to show their relative size proportions C Nephridium at septum 8/9, lateral view D Nephridium at septum 10/11, lateral view E Spermatheca F Spermatheca redrawn from
Seminal vesicle distinct and unpaired in one specimen (CE18516), poorly developed in all other mature or submature specimens. Other genitalia paired. Sperm funnel about 200 µm long, tapering, 25 µm wide basally, 50 µm wide proximally; collar 55–60 µm wide. Spermatozoa on collar in a few mature/submature worms. Vas deferens long, simple, with several loops, about 12 µm wide. Penial bulb poorly developed, about 25 µm wide, 60–65 µm long (Fig.
Occurs in freshwater habitats, in sand and gravel bottoms in lakes and small streams, and climbing on vegetation and dead wood in water. Barcoded specimens document occurrence in Finland, Germany, Norway and Sweden, but the species is probably more widely distributed, not only in Europe. For instance, Ch. glandulosus s. l. has also been reported from North America: the records by
Seems to reproduce mainly parthenogenetically; specimens with developing genitalia are found from June to July (Sweden).
This species is represented in BOLD by BIN: AAT8923.
Chamaedrilus glandulosus;
Cognettia glandulosa;
Cognettia glandulosa A;
ZMBN99905, CE19052, mature, anterior part, COI barcode acc. no. KP878464, leg. Christer Erséus, Aug 10, 2013.
NORWAY: Buskerud, Hol, at Örtedalsåna River (S of Haugastöl), elevation 1,075 m above sea level (N60.4866°, E7.8562°).
ZMBN99906, CE19818, submature, anterior part, COI barcode acc. no. KP878469; NORWAY: Hedmark, Engerdal, Nymoen at Femundelva (Trysilelva) River, at Nordre Husfloen Farm (N61.6569°, E11.8164°), leg. Christer Erséus, Aug 15, 2013. SMNH type-8723, CE19819, submature, anterior part, COI barcode acc. no. KP878470. Same collection data as for the other paratype.
See Table
The species is named after the variation in numbers of chaetae in the lateral preclitellar bundles.
The new species can be separated from all other European species of Chamaedrilus except Ch. glandulosus s. s. by its unique combination of 3–4 pairs of well-developed secondary pharyngeal glands, two chaetae in most lateral bundles in preclitellar segments, and three chaetae in all other bundles, spermathecae with comparatively long ectal ducts, and genitalia shifted forward 3–4 segments (in relation to normal placement in Enchytraeidae). No characters completely separate this species from Ch. glandulosus, but specimens of Ch. varisetosus are generally smaller, have shorter chaetae and smaller internal organs, and usually have a few preclitellar lateral bundles with three chaetae (Ch. glandulosus constantly has two chaetae per lateral bundle in preclitellar segments). Furthermore, Ch. varisetosus is mainly found in moist to wet soils, whereas Ch. glandulosus is only found in aquatic habitats.
EXTERNAL CHARACTERS: Size: length of 20 anteriormost segments 2.33–4.38 mm, mean 2.89±0.59 (n = 13); body width in XII 0.20–0.42 mm, mean 0.28±0.07 (n = 20). Chaetae sigmoid without nodulus, 50–60 µm long, chaetal formula 2,3-(2),3:3–3; most specimens with 3 chaetae in lateral bundles of III(or IV)-V and 2 chaetae in the other lateral preclitellar bundles, but some specimens have 2 chaetae in all preclitellar lateral bundles; in sexually mature specimens, chaetae missing in the segment bearing male pores (VIII or IX). In the mature and submature specimens examined, clitellum only developed (but poorly) in the segment bearing the male pores and ½ a segment posterior and anterior to that segment.
INTERNAL CHARACTERS: Brain slightly concave posteriorly, concave anteriorly, 125–140 µm long, about twice as long as broad (Fig.
Chamaedrilus varisetosus sp. n. A Anterior part of body (immature specimen) in lateral view, indicating chaetal distribution and the size, shape and number of pharyngeal glands B Male genitalia of a mature worm with male pores in segment VIII C Spermatheca D Brain, dorsal view E Nephridium at septum 10/11, lateral view. Abbreviations: eg = ectal gland; pb = penial bulb; sa = spermathecal ampulla; sd = spermathecal duct; sf = sperm funnel; vd = vas deferens. Scale bars: 200 µm (A); 50 µm (B-E).
Seminal vesicle unpaired, distinct in all three mature/submature specimens. Other genitalia paired. Sperm funnel about 100 µm long, 40–50 µm wide; collar indistinct, 25–30 µm wide. Spermatozoa not observed on collar. Vas deferens long, with several loops, about 5–7 µm wide. Penial bulb poorly developed, about 25 µm wide, 35–40 µm long (Fig.
Found both in aquatic and terrestrial habitats. In freshwater found on stony bottoms in rivers, on land found in both deciduous and coniferous forest as well as in grassland soils. Known from Canada (BOLD record), the Czech Republic, Finland (BOLD record), Norway and Sweden, but may be more widely distributed in Europe and North America. Schlaghamerský’s (2013) description of C. glandulosa from Michigan fits our description of Ch. varisetosus. This and
Parthenogenetic reproduction more limited in time (maturing specimens found in August in Norway) than fragmentation (observed in May-September in Sweden and Norway). Worms with regenerating tails and/or heads rather frequent. This species may correspond to the population studied by
This species is represented in BOLD by BIN: AAT9501.
The two species treated in this paper, Chamaedrilus glandulosus sensu stricto and Ch. varisetosus sp. n., are easily separated morphologically from other species of Chamaedrilus by a unique combination of characters: the secondary pharyngeal glands are well developed in several segments, there are two chaetae in most preclitellar lateral bundles, but no enlarged chaetae, the genital organs are shifted forwards, and the spermathecae have comparatively long ectal ducts. The two species are morphologically similar and they have therefore been regarded as a single taxon by previous authors (e.g.,
Without the genetic data, the delimitation of Ch. glandulosus and Ch. varisetosus would have been much more challenging, all the more so because these worms, like those in the sphagnetorum complex, are mostly found sexually immature. It should also be considered that these species, even when mature, actually reproduce uniparentally, as mentioned in the introduction and discussed earlier by
Genetic studies discovering cryptic and unnoticed diversity need to be followed by formal taxonomic revision, including careful morphological scrutiny, updated descriptions and species names, if possible based on barcoded types. We believe that an integrative approach, combining genetic and morphological data with as much as possible of ecological and physiological information, will strengthen studies of enchytraeid systematics.
We are indebted to Ainara Achurra, Anna Ansebo, Kerryn Elliott, Diego Fontaneto, Lisa Matamoros, Hanna Saarikoski and Bronwyn Williams for assistance with field work or for providing specimens in other ways; and to Marcus Svensson and Per Hjelmstedt for lab assistance. Helma Roggenbuck (ZMUH) is thanked for loaning us material. Kerryn Elliott kindly checked the language of the manuscript. Financial support to the first author was given by Wilhelm och Martina Lundgrens Vetenskapsfond; and to the last author by the Swedish Research Council (VR) and the Swedish Research Council for Environment, Agricultural Science and Spatial Planning (FORMAS), the Swedish Taxonomy Initiative (ArtDatabanken), the Norwegian Taxonomy Initiative (Artsdatabanken) and the Adlerbert Research Foundation.