Milnesium alpigenum Ehrenberg, 1853,

Morek, Witold, Suzuki, Atsushi C., Schill, Ralph O., Georgiev, Dilian, Yankova, Maria, Marley, Nigel J. & Michalczyk, Łukasz, 2019, Redescription of Milnesium alpigenum Ehrenberg, 1853 (Tardigrada: Apochela) and a description of Milnesium inceptum sp. nov., a tardigrade laboratory model, Zootaxa 4586 (1), pp. 35-64: 41-46

publication ID

https://doi.org/10.11646/zootaxa.4586.1.2

publication LSID

lsid:zoobank.org:pub:2D01FAB0-53DF-4B89-A891-A51C548D4B72

persistent identifier

http://treatment.plazi.org/id/922D878E-DA52-3A67-FF14-FEBFFA64147E

treatment provided by

Plazi

scientific name

Milnesium alpigenum Ehrenberg, 1853
status

 

Milnesium alpigenum Ehrenberg, 1853 

Fig. 1View FIGURE 1, Table 3

M. tardigradum Marcus (1928) 

Material examined: The neotype series consisting of the neotype and 37 neoparatypes (see Table 1 and “Type repositories” below for details).

Integrative redescription. Females (morphometrics in Table 3): Body slightly yellowish, rather slender as for a Milnesium  ( Fig. 1AView FIGURE 1). Eyes present in live specimens, quickly dissolving after fixation in Hoyer’s medium. Cuticle smooth in SEM and with minute pseudopores visible on the caudo-dorsal part only under high quality PCM ( Fig. 1CView FIGURE 1). Weakly outlined pseudoplates on the caudo-dorsal cuticle visible in some specimens only under SEM ( Fig. 1B and DView FIGURE 1). Six peribuccal papillae present, with the ventral being the smallest. Six triangular peribuccal lamellae of unequal size; the two lateral being slightly smaller than the dorsal and ventral lamellae, i.e. with the 4+2 configuration (identifiable only in SEM; Fig. 1FView FIGURE 1). Two lateral papillae present. Buccal tube funnel-shaped ( Fig. 1EView FIGURE 1). Claws slender, primary branches with tiny accessory points, more visible on claws IV. All secondary branches with three points, i.e. with the [3-3]-[3-3] CC ( Fig. 1View FIGURE 1 G–H). Spurs on secondary branches long and slender, especially on internal and anterior claws. Cuticular bars under claws I–III present.

Males: No males were found in the sample or culture, confirming that the neotype population is parthenogenetic (at least facultatively).

Juveniles: Morphologically identical to adults, except for the lack of pseudopores.

Hatchlings: Morphologically identical to adults, except for the lack of pseudopores and the absence of cuticular bars under claws I–III in the majority of examined specimens (7/ 8 specimens = 88%).

Ontogenetic variability: No developmental variability in the CC. Pseudopores visible only in adults. Cuticular bars under claws I–III mostly absent in hatchlings but always present in juveniles and adults.

Eggs: Oval, yellow, smooth and laid in exuviae. In the culture, up to 12 eggs were recorded in a single clutch.

DNA markers: All sequences were of a very good quality and every marker was represented by a single haplotype: 18S rRNA (1054 bp, MG996146View Materials); 28S rRNA (809 bp, MH000384View Materials); ITS-2 (530 bp, MH000382View Materials); and COI (560 bp, MH000380View Materials). Sequences are provided in Appendix 1.

Neotype locality: 45°58'13''N, 07°57'07''E; 1370 m asl: Italy, Monte Rosa massif, lower chair-lift station of Macugnaga; moss on roof.GoogleMaps 

Etymology: Ehrenberg (1853) did not explain the choice of the species name; however, it seems reasonable to assume that Christian Ehrenberg named the species after the Alps, the mountain chain in which the type locality, the Monte Rosa massif, is located.

Type repositories: The neotype series consist of the neotype (slide IT.057.17) and 37 “neoparatypes” (IT.057.01–16; 18–38). The neotype and 15 neoparatypes (IT.057.01–12; 45–47) are preserved at the Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland), further 14 neoparatypes ( IT.057.13–16; 18–26) are deposited in Department of Animal Taxonomy and Ecology, Adam Mickiewicz University in Poznań , Umultowska 89, 61-614 Poznań, Poland  , 10 neoparatypes ( IT.057.27–38) are stored in the Marine Biology & Ecology Research Centre, University of Plymouth, Drake Circus , Plymouth, PL4 8AA, United Kingdom  , one paratype ( IT.057.47) is deposited in Natural History Museum, Cromwell Road, London SW 7 5BD, United Kingdom  , and the remaining 6 neoparatypes ( IT.057.39-44) are deposited in the collection of Binda & Pilato, Museum of the Department of Biological , Geological and Environmental Sciences , Section of Animal Biology “Marcello La Greca”, University of Catania, Italy  .

Phenotypic differential diagnosis: Milnesium alpigenum  has the [3-3]-[3-3] CC and “smooth” cuticle (i.e. cuticle smooth in SEM and with minute pseudopores visible only under high quality PCM, but with no sculpturing, such as reticulation, on cuticle surface). This places it in the largest group of Milnesium  species that share these characteristics (20 species; Morek et al. 2016a; Pilato & Lisi 2016; Young et al. 2016; Pilato et al. 2016; Pilato et al. 2017; Schlabach et al. 2018). Nevertheless, M. alpigenum  differs specifically from:

M. antarcticum Tumanov, 2006  , only recorded from the Antarctic ( Smykla et al. 2012), by the maximal length of the buccal tube (Ẽ 68 µm in M. alpigenum  vs> 68 µm in M. antarcticum  ), a smaller buccal tube standard width (8.6–23.6 µm in M. alpigenum  vs 25.9–31.8 µm in M. antarcticum  ), and by a statistically lower pt of the stylet support insertion point (61.1–70.3, on average 64.9 in M. alpigenum  vs 70.0–73.7, on average 71.5 in M. antarcticum  ; t 38 = 16.708, p<0.001).

M. argentinum Roszkowska, Ostrowska & Kaczmarek, 2015  , reported from Argentina, by the appearance of cuticle (faint pseudopores visible only with a high quality PCM on the caudal part of the dorsal cuticle in M. alpigenum  vs well-visible pseudopores in M. argentinum  on the entire dorsum with a standard PCM), and by the lower pt of the primary branches IV (46.9–63.2 in M. alpigenum  vs 28.4–36.4 in M. argentinum  ).

M. asiaticum Tumanov, 2006  , recorded from Kirghizstan (type locality), China ( Beasley & Miller 2007), Estonia ( Zawierucha et al. 2014) and the Svalbard archipelago ( Kaczmarek et al. 2012), by a statistically lower pt of primary branches III (39.7–51.7, on average 45.8 in M. alpigenum  vs 51.5–58.3, on average 55.3 in M. asiaticum  ; t 36 = 15.385, p<0.001) and by a lower pt of primary branches IV (46.9–63.2 in M. alpigenum  vs 63.9–76.0 in M. asiaticum  ).

M. barbadosense Meyer & Hinton, 2012  , only reported from the type locality in Barbados, by a lower pt of the stylet support insertion point (61.1–70.3 in M. alpigenum  vs 71.6–82.1 in M. barbadosense  ) and by a higher pt of the primary branches IV (46.9–63.2 in M. alpigenum  vs 28.4–42.2 in M. barbadosense  ).

M. beatae Roszkowska, Ostrowska & Kaczmarek, 2015  , only reported from the type locality in Argentina, by the appearance of cuticle (faint pseudopores visible only with a high quality PCM on the caudal part of the dorsal cuticle in M. alpigenum  vs well-visible pseudopores in M. beatae  on the entire dorsum with a standard PCM), by a more slender buccal tube (standard width/length ratio 21–38% in M. alpigenum  vs standard width/ length ratio 58–66% in M. beatae  ).

M. bohleberi Bartels, Nelson, Kaczmarek & Michalczyk, 2014  , recorded from North Carolina and Tennessee, USA, by a more slender buccal tube (standard width/length ratio 21 – 38% in M. alpigenum  vs standard width/ length ratio 54–64% in M. bohleberi  ).

M. brachyungue Binda & Pilato, 1990  , recorded from the type locality in Chile and south Argentina ( Roszkowska et al. 2016), by a higher pt of primary branches of all claws (36.0– 63.2 in M. alpigenum  vs 22.9– 33.1 in M. brachyungue  ).

M. burgessi Schlabach, Donaldson, Hobelman, Miller & Lowman, 2018  , reported from Kansas, USA, by a higher pt of the buccal tube standard width (21.0– 38.4 in M. alpigenum  vs 52.9–68.5 in M. burgessi  ) and by a lower pt of primary branches IV (46.9–63.2 in M. alpigenum  vs 66.6–96.2. in M. burgessi  ).

M. dornensis Ciobanu, Roszkowska & Kaczmarek, 2015  , recorded from Romania (type locality), Poland ( Kaczmarek et al. 2018) and Tunisia ( Gąsiorek et al. 2017b), by the appearance of cuticle (faint pseudopores visible only with a high quality PCM on the caudal part of the dorsal cuticle in M. alpigenum  vs well-visible pseudopores in M. dornensis  on the entire dorsum with a standard PCM) and by a statistically lower pt of the buccal tube standard width (21.0–38.4, on average 31.4 in M. alpigenum  vs 37.8–51.6, on average 44.1 in M. dornensis  ; t 43 = 10.473, p<0.001).

M. eurystomum Maucci, 1991  , recorded from Greenland (type locality), Chile and Argentina ( Maucci 1996), and Mongolia ( Kaczmarek & Michalczyk 2006), by a more slender buccal tube (standard width/length ratio 21 – 38% in M. alpigenum  vs standard width/length ratio 62–65% in M. eurystomum  ).

M. longiungue Tumanov, 2006  , reported from the type locality in the Himalayas ( India) and China ( Beasley & Miller 2007), by the presence of accessory points on primary branches, a lower pt of primary branches III (39.7–51.7 in M. alpigenum  vs 57.1–73.5 in M. longiungue  ), and by a lower pt of primary branches IV (46.9– 63.2 in M. alpigenum  vs 81.8–92.4 in M. longiungue  ).

M. minutum Pilato & Lisi, 2016  , only reported from the type locality in Sicily, by a lower pt of the buccal tube standard width (21.0– 38.4 in M. alpigenum  vs 38.6–42.4 in M. minutum  ).

M. sandrae Pilato & Lisi, 2016  , only reported from the type locality in Hawaii, by a higher pt of the stylet support insertion point (61.1–70.3 in M. alpigenum  vs 58.0– 60.5 in M. sandrae  ) and by a lower pt of the buccal tube standard width (21.0– 38.4 in M. alpigenum  vs 44.9–48.0 in M. sandrae  ).

M. shilohae Meyer, 2015  , only reported from the type locality in Hawaii, by a lower pt of the stylet support insertion point (61.1–70.3 in M. alpigenum  vs 75.5–77.5 in M. shilohae  ), a lower pt of the buccal tube standard width (21.0– 38.4 in M. alpigenum  vs 47.1–55.9 in M. shilohae  ), and by a higher pt of external spurs I–III (11.3–17.8 in M. alpigenum  vs 1.9–7.5 in M. shilohae  ).

M. swansoni Young, Chappell, Miller & Lowman, 2016  , only reported from the type locality in USA, by a higher number of peribuccal lamellae (six in M. alpigenum  vs four in M. swansoni  ), a lower pt of the buccal tube standard width (21.0– 38.4 in M. alpigenum  vs 39.2–42.2 in M. swansoni  ), a lower pt of the posterior buccal tube width (23.7–39.4 in M. alpigenum  vs 39.9–42.2 in M. swansoni  ), and by a lower pt of primary branches I (36.0– 47.9 in M. alpigenum  vs 48.4–53.7 in M. swansoni  ). It should be noted that the number of peribuccal lamellae in M. swansoni  was identified only with the use of PCM, thus until SEM observations are made, the number of lamellae should be treated as a working hypothesis.

M. tumanovi Pilato, Sabella & Lisi, 2016  , only reported from the type locality in Crimea, by a higher pt of the stylet support insertion point (61.1–70.3 in M. alpigenum  specimens 383–983 µm long vs ca. 52.3 in M. tumanovi  in a specimen 774 µm long) and by a lower pt of the buccal tube standard width (21.0– 38.4 in M. alpigenum  specimens 383–983 µm long vs ca. 55.1 in M. tumanovi  in a specimen 774 µm long).

M. validum Pilato, Sabella, D’Urso & Lisi, 2017  only reported from the type locality in the Antarctic, according to the measurements presented in the description of M. validum  all pt ranges overlap, but a comparison of specimens of a similar body length (414–509 µm in M. alpigenum  and 424–482 µm in M. validum  ) shows that M. alpigenum  has a shorter buccal tube (33.0–43.0 µm in M. alpigenum  vs 44.1–55.6 µm in M. validum  ), moreover the two species differ in the shape of secondary branches (slender in M. alpigenum  vs robust in M. validum  , compare Fig. 1View FIGURE 1 G–H here and Fig. 6B–D in Pilato et al. 2017), and in the shape of spurs (of typical width in M. alpigenum  vs very thin in M. validum  ).

M. inceptum  sp. nov. (described below), recorded from Germany, Japan, Switzerland and Bulgaria—please see the section “Delineation of M. alpigenum  and M. inceptum  sp. nov. ” below for a detailed differential diagnosis between these two pseudocryptic species.

M. zsalakoae Meyer & Hinton, 2010  , recorded from Arizona and New Mexico ( USA), by the presence of accessory points on primary branches and by a lower pt of primary branches of all claws (36.0– 63.2 in M. alpigenum  vs 64.4–102.9 in M. zsalakoae  ).

Genotypic differential diagnosis: All sequences obtained for M. alpigenum  were unique and distinct from the sequences deposited in GenBank. The ranges of the uncorrected p-distances between neotype M. alpigenum  and sequences of other congeners are as follows:

• 18S rRNA: 1.1%–3.6% (2.6% on average), with the most similar being M. inceptum  sp. nov. from Europe ( MH000383View Materials, present study) and the least similar being an undetermined species from Marion Island in the sub- Antarctic ( EU266922View Materials, Sands et al. 2008).

• 28S rRNA: 4.5%–8.0% (6.1% on average), with the most similar being an undetermined species from the USA ( JX888585View Materials –7, Adams et al, unpublished) and the least similar being M. tardigradum  s.s. from Poland ( KC138809View Materials, Zawierucha, unpublished).

• ITS-2: 20.4%–23.2% (20.2% on average), with the most similar being M. tardigradum  s.s. from Germany ( JF951049View Materials, Michalczyk et al. 2012a) and the least similar being M. tardigradum  s.s. from France ( MG923555View Materials, Morek et al. 2019).

• COI: 14.8%–25.8% (17.4% on average), with the most similar being M. variefidum  from the UK ( KT951663View Materials, Morek et al. 2016a) and an undetermined species from the USA ( KX306950View Materials, Fox et al., unpublished), whereas the least similar being an undetermined species from the Antarctic ( KP013598View Materials, Velasco-Castrillón et al. 2015).

Kingdom

Animalia

Phylum

Annelida

Class

Polychaeta

Order

Phyllodocida

Family

Aphroditidae

Genus

Milnesium

Loc

Milnesium alpigenum Ehrenberg, 1853

Morek, Witold, Suzuki, Atsushi C., Schill, Ralph O., Georgiev, Dilian, Yankova, Maria, Marley, Nigel J. & Michalczyk, Łukasz 2019
2019
Loc

M. inceptum

Morek & Suzuki & Schill & Georgiev & Yankova & Marley & Michalczyk 2019
2019
Loc

M. inceptum

Morek & Suzuki & Schill & Georgiev & Yankova & Marley & Michalczyk 2019
2019
Loc

M. burgessi

Schlabach, Donaldson, Hobelman, Miller & Lowman 2018
2018
Loc

M. burgessi

Schlabach, Donaldson, Hobelman, Miller & Lowman 2018
2018
Loc

M. burgessi

Schlabach, Donaldson, Hobelman, Miller & Lowman 2018
2018
Loc

M. validum Pilato, Sabella, D’Urso & Lisi, 2017

Pilato, Sabella, D'Urso & Lisi 2017
2017
Loc

M. validum

Pilato, Sabella, D'Urso & Lisi 2017
2017
Loc

M. validum

Pilato, Sabella, D'Urso & Lisi 2017
2017
Loc

M. validum

Pilato, Sabella, D'Urso & Lisi 2017
2017
Loc

M. validum

Pilato, Sabella, D'Urso & Lisi 2017
2017
Loc

M. validum

Pilato, Sabella, D'Urso & Lisi 2017
2017
Loc

M. minutum

Pilato & Lisi 2016
2016
Loc

M. minutum

Pilato & Lisi 2016
2016
Loc

M. sandrae

Pilato & Lisi 2016
2016
Loc

M. sandrae

Pilato & Lisi 2016
2016
Loc

M. sandrae

Pilato & Lisi 2016
2016
Loc

M. swansoni

Young, Chappell, Miller & Lowman 2016
2016
Loc

M. swansoni

Young, Chappell, Miller & Lowman 2016
2016
Loc

M. swansoni

Young, Chappell, Miller & Lowman 2016
2016
Loc

M. swansoni

Young, Chappell, Miller & Lowman 2016
2016
Loc

M. swansoni

Young, Chappell, Miller & Lowman 2016
2016
Loc

M. swansoni

Young, Chappell, Miller & Lowman 2016
2016
Loc

M. tumanovi

Pilato, Sabella & Lisi 2016
2016
Loc

M. tumanovi

Pilato, Sabella & Lisi 2016
2016
Loc

M. tumanovi

Pilato, Sabella & Lisi 2016
2016
Loc

M. argentinum

Roszkowska, Ostrowska & Kaczmarek 2015
2015
Loc

M. argentinum

Roszkowska, Ostrowska & Kaczmarek 2015
2015
Loc

M. argentinum

Roszkowska, Ostrowska & Kaczmarek 2015
2015
Loc

M. beatae

Roszkowska, Ostrowska & Kaczmarek 2015
2015
Loc

M. beatae

Roszkowska, Ostrowska & Kaczmarek 2015
2015
Loc

M. beatae

Roszkowska, Ostrowska & Kaczmarek 2015
2015
Loc

M. dornensis

Ciobanu, Roszkowska & Kaczmarek 2015
2015
Loc

M. dornensis

Ciobanu, Roszkowska & Kaczmarek 2015
2015
Loc

M. dornensis

Ciobanu, Roszkowska & Kaczmarek 2015
2015
Loc

M. shilohae

Meyer 2015
2015
Loc

M. shilohae

Meyer 2015
2015
Loc

M. shilohae

Meyer 2015
2015
Loc

M. shilohae

Meyer 2015
2015
Loc

M. bohleberi

Bartels, Nelson, Kaczmarek & Michalczyk 2014
2014
Loc

M. bohleberi

Bartels, Nelson, Kaczmarek & Michalczyk 2014
2014
Loc

M. barbadosense

Meyer & Hinton 2012
2012
Loc

M. barbadosense

Meyer & Hinton 2012
2012
Loc

M. barbadosense

Meyer & Hinton 2012
2012
Loc

M. zsalakoae

Meyer & Hinton 2010
2010
Loc

M. zsalakoae

Meyer & Hinton 2010
2010
Loc

M. antarcticum

Tumanov 2006
2006
Loc

M. antarcticum

Tumanov 2006
2006
Loc

M. antarcticum

Tumanov 2006
2006
Loc

M. antarcticum

Tumanov 2006
2006
Loc

M. asiaticum

Tumanov 2006
2006
Loc

M. asiaticum

Tumanov 2006
2006
Loc

M. asiaticum

Tumanov 2006
2006
Loc

M. longiungue

Tumanov 2006
2006
Loc

M. longiungue

Tumanov 2006
2006
Loc

M. longiungue

Tumanov 2006
2006
Loc

M. eurystomum

Maucci 1991
1991
Loc

M. eurystomum

Maucci 1991
1991
Loc

M. brachyungue

Binda & Pilato 1990
1990
Loc

M. brachyungue

Binda & Pilato 1990
1990
Loc

M. tardigradum

Marcus 1928
1928
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853
Loc

M. alpigenum

Ehrenberg 1853
1853