Daphnia dentifera, FORBES, 1893

Zuykova, Elena I, Simonov, Evgeniy P, Bochkarev, Nikolay A, Taylor, Derek J & Kotov, Alexey A, 2018, Resolution of the Daphnia umbra problem (Crustacea: Cladocera) using an integrated taxonomic approach, Zoological Journal of the Linnean Society 184, pp. 969-998 : 979-988

DAPHNIA DENTIFERA FORBES, 1893

( FIGS 8 , 9 , TABLE 3)

Diagnosis

Adult male: Dorsal margin straight, not elevated above head ( Fig. 8I ). Posterior head margin slightly convex, with a small prominence and a distinct step-like prominence in middle of margin ( Fig. 8J ). Postero-ventral head angle smooth. Ventral margin of head slightly convex, anterior-most extremity not fully occupied with optic vesicle. Eye is relatively small. Labrum with a very large distal labral plate ( Fig. 8J ). Valve with antero-ventral portion having numerous setae submarginally on inner face of valve ( Fig. 8K ). Postero-ventral portion of valve with small marginal denticles and few submarginal setules ( Fig. 8L ). Abdomen with small mounds on first and third segment, and larger mound on second segment ( Fig. 8M, N ). Postabdomen with long and concave pre-anal margin, its distal portion with paired teeth strongly increasing in size distally ( Fig. 8O ); gonopore opens laterally, without a genital papilla. On outer surface of postabdominal claws, pectens consist of setules only ( Fig. 8P ). Antenna I with antennular seta very small (only reaching distal end of antennular body), located at a small distance from distal end of antenna I body; male seta (flagellum) distally on antenna body without a post-aesthetasc process, this seta somewhat longer than longest aesthetasc ( Fig. 8Q ). Limb I with ODL smallest seta minute, largest seta as in other species ( Fig. 9A ); IDL with a long, bent copulatory hook; setae 2 and 2′ equally long ( Fig. 9B ), setae 3 and 4 as in other taxa ( Fig. 10A ). Limb II with anterior seta 1 armed by long, robust spinules ( Fig. 9C ). Limb V exopod with seta 2 somewhat shorter than seta 1 ( Fig. 9D ). Size 1–1.3 mm.

Type locality

‘Shoshone Lake, Yellowstone Park’, WY, USA ( Forbes, 1893).

Type material

Most probably lost, although some of Forbes’ slides existed in the 1950s ( Brooks, 1957).

Material examined here

Many parthenogenetic and ephippial females and males from Silver Lake (41.08°N; 85.9°W), IN, USA, collected by D. J. Taylor on 29 October 2006, AAK M-1129; Hammond Lake (41.3647°N; 85.6775°W), IN, USA, collected by D. J. Taylor on 29 October 2006, AAK M-1125 .

Comments

Morphological differentiation of D. dentifera and D. longispina sensu Petrusek et al. (2008) , including populations identified as D. cf. hyalina , is impossible to date. Daphnia dentifera is present in the Eastern Palaearctic ( Ishida & Taylor, 2007a; Ma et al., 2015), but the exact geographical boundary between the distributions of D. dentifera and D. longispina is unknown. Daphnia dentifera is common in western North America (although there appears to be some anthropogenic introduction in eastern North America). The examined populations were assigned to D. dentifera on the analysis of the female morphology ( Fig. 8A–H ).

DAPHNIA UMBRA TAYLOR, HEBERT ET COLBOURNE, 1996 EMEND. NOV.

( FIGS 10–16 , TABLE 3)

Neotype (selected here)

A parthenogenetic female in 90% alcohol, MGU ML 158. The selection of neotype is explained by ‘an exceptional need’ (article 75.3 of ICZN, 2000), namely: ‘75.3.1. a statement that it is designated with the express purpose of clarifying the taxonomic status or the type locality of a nominal taxon’ and ‘75.3.2. a statement of the characters that the author regards as differentiating from other taxa the nominal species-group taxon for which the neotype is designated’.

Diagnosis

Adult parthenogenetic female: Body pigmented in brown or yellow–brown, subovoid in lateral view, maximal height in middle of valves ( Figs 10 , 11 ). Dorsal margin of valves elevated above head, slightly and regularly convex, with no depression between head and rest of body. Postero-dorsal angle with a short or long caudal spine; ventral margin regularly convex.

Head with a moderate to long rostrum, its tip not bent ( Figs 11B–D , 12A, B ); posterior margin of head with a low prominence going from level of antenna I proximally; ventral margin of head slightly concave to almost straight (see Hebert, 1995). No crest or helmet on head, compound eye medium sized, ocellus small and located far from base of antenna I. Labrum with a fleshy main body and a large, setulated distal labral plate ( Fig. 11C ).

Carapace subovoid; spinules occupy the posterior half of dorsal margin and more than half of ventral margin. No setae at ventral margin; in posterior portion of valve (on its inner face), a row of delicate, setulated setae, with rows of minute setules between them ( Figs 11E , 12D ); in dorsal portion of margin, only setules present, whereas setae are absent ( Fig. 11F ).

Abdomen relatively short, consisting of four segments. The first (basal-most) abdominal segment with especially long (1.5 times longer than postabdominal claw) process, straight or bent anteriorly; the second segment with a short conical process; the third segment with a mound-like process; on all processes there are rows of minute setules ( Fig. 11G, H ). The fourth segment, lacking a process, has a convex dorsal margin.

Postabdomen elongated, somewhat tapering distally, with ventral margin straight, lacking setules ( Figs 11G , 12E ). Pre-anal margin long (remarkably longer than anal plus postanal portions of postabdomen), straight, with series of minute setules. Pre-anal angle distinct, postanal angle expressed but rounded. About ten (9–13 according to Benzie, 2005) paired spines on postanal and anal portion, their size continuously increasing distally. Postabdominal seta shorter than pre-anal margin. Postabdominal claw slightly and regularly bent, with a pointed tip ( Figs 11I , 12F ). On outer side, three successive pectens along the dorsal margin: each pecten consists of fine setules (length of longest setules less than half of claw diameter at base); the third pecten does not reach the tip of the claw. Two rows of fine setules at ventral margin of the claw.

Antenna I as a very small mound ( Fig. 11D ), with nine aesthetascs of different length terminally; their tips do not reach tip of rostrum; antennular sensory seta fine, arise immediately from head surface instead of mound of the antenna I. Antenna II with coxal part possessing two short sensory setae of different length ( Fig. 13A ). Basal segment elongated, with a welldeveloped (remarkably longer than the basal segment of exopod) distal sensory seta on its posterior face ( Fig. 13B : dss), and minute distal spine at its anterior face ( Fig. 13A ). Antennal branches somewhat longer than basal segment; all segments with series of minute setules. Spines on apical segments rudimentary; spine on the second segment of exopod small (its length less than half of the diameter of third segment) and thin ( Fig. 13A : arrow). Antennal formula: setae 0-0-1-3/1-1-3. No chitinous insertion within distal segment of a swimming seta near joint with basal segment.

Limb I without accessory seta; outer distal lobe ( Fig. 13C : ODL) with a long seta unilaterally armed distally with minute setules, and a thin, short (length ~1.5 diameters of ODL) seta bilaterally setulated distally ( Fig. 13C, D ); inner distal lobe ( Fig. 13D : IDL), or endite 4, with a single, long anterior seta ( Fig. 13D : 1), bearing short setules distally. Endite 3 with a long anterior seta 2, armed with minute setules, and two posterior setae (a, b). Endite 2 with a short anterior seta 3, and two posterior setae (c, d). Endite 1 with a small anterior seta 4 and four posterior setae (e–h). Two ejector hooks of different length.

Limb II with distal portion as a large lobe (presumably exopodite) bearing a large, soft, distal seta and a large, soft, lateral seta of similar size. Four endites bearing five setae; among them, a stiff, anterior seta ( Fig. 13E : 1) about two-thirds the length of each of two other setae on this endite, armed with fine setules distally. Gnathobase with four anterior setae ( Fig. 13E : 1–4) and ~11 posterior setae of gnathobasic ‘filter plate’.

Limb III with a setulated pre-epipodite, subglobular epipodite and a flat exopodite bearing four distal and two lateral setae (not illustrated here). Inner-distal portion of limb with four endites: endite 4 with a single anterior seta ( Fig. 13F : 1) and a single posterior seta; endite 3 with a single anterior seta (2) and a single posterior seta; endite 2 with a small anterior seta (3) and two posterior setae; endite 1 with a large anterior seta (4) and four posterior setae. Small sensilla near seta 3. The rest of limb inner-distal portion as a singular large lobe, bearing numerous posterior soft setae and a single, relatively long anterior seta ( Fig. 13F : 1) in its distal corner, plus two minute setae (2, 3) more proximally. This limb part represents a modified gnathobase III.

Limb IV with a setulated pre-epipodite, ovoid epipodite and wide, flat exopodite, with protruding and setulating inner-distal angle, and bearing four distal ( Fig. 13H : 1–4) and two lateral setae (5, 6). Inner-distal portion of this limb with completely fused endites, distally with two setae of unclear homology; the most part of limb inner margin is a gnathobase filter plate consisting of numerous posterior setae.

Limb V with a setulated pre-epipodite, subovoid epipodite, triangular exopodite supplied with two small distal setae ( Fig. 13I : 1, 2) and a large lateral seta (3). Inner limb portion as an ovoid flat lobe, with setulated inner margin and a single, large seta.

Ephippial female: Shape ( Fig. 12A, B ) in general similar to that in parthenogenetic female, but dorsal margin of valves straight ( Fig. 12A ), dorsal wall of carapace additionally chitinized, forming a dorsal plate, without spinules ( Fig. 12C ). Ephippium with two resting eggs, axes of which sub-perpendicular to its dorsal margin; egg chambers separated from each other; most part of ephippium additionally pigmented and covered with sculpturing of polygonal cells; postero-dorsal portion of valves with caudal spine incorporated into ephippium.

Adult male: Body low; dorsal margin of valves slightly convex, not elevated above head; depression between head and valves almost absent or absent; postero-dorsal angle distinct, with a long caudal spine ( Figs 14A , 15A ). Posterior head margin straight, with a very small hillock ( Fig. 15B : arrow) or without it, a step-like prominence in proximal portion of margin ( Figs 14A , 15A, B ). Postero-ventral head angle as a rudimentary rostrum. Ventral margin of head slightly concave, anterior-most extremity occupied with optic vesicle, no supra-ocular depression posteriorly to it. Eye relatively large, distal head extremity occupied by optical vesicle, ocellus small. Labrum with a very large distal labral plate ( Fig. 15B ). Valve with antero-ventral portion trapezium-form, all ventral margin with numerous setae submarginally on inner face of valve ( Figs 14B , 15C–F ). Postero-ventral portion of valve with small marginal denticles; armature of inner face of valve posterior margin as in female ( Fig. 15F, G ).

Abdomen with small mounds on first and third segment, and larger mound on second segment ( Figs 14C , 15H, I ). Postabdomen shape and armature in general as in female, but pre-anal margin longer, slightly concave ( Fig. 14C ); in some males postabdomen deformed ( Fig. 15H ). About 11 paired teeth, large (distal-most longer than claw diameter) and strongly increasing in size distally ( Fig. 15J ). Gonopore opens laterally, without a genital papilla. On outer surface of postabdominal claws, pectens consist of setules only ( Figs 14D , 15K ); a row of setules on inner face of claw proximally ( Fig. 15L ).

Antenna I elongated, almost straight ( Figs 15E , 16A ); antennular seta very small (length ~0.5 diameter of antenna I), located at a small distance from distal end of antenna I body; aesthetascs of different length; among them, largest aesthetasc ~1–1.5 times longer than antenna I maximal diameter. Male seta (flagellum) distally on antenna body without a post-aesthetasc process. This seta remarkably longer and two times thicker than an aesthetasc, bisegmented, with its distal segment finelly setulated.

Limb I: ODL large, cylindrical ( Fig. 14F : ODL), bearing a small seta and a very large seta supplied with minute setules distally; IDL with a relatively long, bent copulatory hook, and two setae of different size ( Fig. 14F : 1 and 1′); endite 3 with four setae (additional seta marked as 2′), both setae 2 and 2′ long, seta 3 remarkably larger than in female, seta 4 as in female ( Fig. 16B, C ). Limb II: distal-most endite with a modified anterior seta 1, armed by long, thin spinelike setules ( Figs 14G , 16D ). Limb V: exopod with seta 2 somewhat shorter than seta 1 ( Fig. 16E ).

Size: Neotype 2.24 mm (without caudal needle); parthenogenetic females 1.5–2.65 mm in G. O. Sars material on D. alpina , 1.64–2.34 mm in Taimyr, 0.7–1.35 mm in Borzu-Khol Lake, 1.1–2.7 mm according to Benzie (2005); adult males 1.0– 1.4 mm (~ 1.1 mm according to Benzie, 2005).

Type locality (according to neotype): Unnamed pond (‘Pond 4-7’, 69.6378°N, 83.7028°W), Melville Peninsula , Nunavut, Canada, AAK M-0527. The sample was collected in 5 August 1990 from a helicopter by D. J. Taylor .

Differential diagnosis

Daphnia umbra differs from other species of the longispina group in the unique structure of the anterior seta on the inner-distal portion of the male limb II (covered by thin setules instead of strong denticles in other taxa) and an unusual combination of other male characters, e.g. flagellum length relative to aesthetascs ( Table 3). See further discussion below.

Distribution (this study)

Canada (Nunavut): Many parthenogenetic, ephippial females and males from un-named pond (‘ Pond 4-7’), Melville Peninsula , collected on 5 August 1990 by D. J. Taylor, DJT 10–201. Twenty parthenogenetic females from Lake 3-1, Melville Peninsula , collected on 9 August 1990 by D. J. Taylor, DJT 3-468. Six females from pond 6-9, Melville Peninsula, collected on 11 August 1990 by D. J. Taylor, DJT 3-467. Ten females from Pond 8-4, Melville Peninsula, collected on 16 August 1990 by D. J. Taylor, DJT 3-466 .

Norway: Many parthenogenetic females from Otvavand, tube GOS F 1933B (syntypes of D. alpina Sars ) . Nineteen females from Stasjonsdammen (60.60°N, 7.50°E), a small shallow pond close to the Alpine Research Center at Finse, 1207 m above sea level, north-western part of Hardangervidda, collected on 3 September 1985 by A. Hobaek, DJT 3-472.

Russia (Asian): Many parthenogenetic, ephippial females and males from a lake on the right bank of the Kotuy River (71.322°N, 103.121°E), Taimyr Autonomous Area , collected in August 2011 by V. E. Fedosov, AAK M-2185-2187. Many parthenogenetic females from Borzu-Khol Lake (52.65°N, 96.73°E), Tuva Republic, collected by E. I. Zuykova, AAK M-3200 .

Reconsideration of D. umbra distribution range

The taxon was previously found in Nunavut, Canada ( Taylor et al., 1996; Schwenk et al., 2000; Strecker et al., 2008), Southern Norway ( Larsson & Wathne, 2006; Giessler & Englbrecht, 2009), Northern Norway and Bjørnøya Island ( BOLD, 2017), Finnish Lapland ( Rautio & Korhola, 2002; Schwenk et al., 2004; Eloranta et al., 2013) and the Pechora delta, Nenets Autonomous Area, Russia ( Schwenk et al., 2004). It was regarded as an Arctic species (note that Benzie, 2005 did not consider European records at the time of his monograph). Above, we add two more records based on genetic identification: an unnamed lake on the Taimyr Peninsula and Borzu-Khol Lake in the Tuva Republic, both in the Asian part of Russia. Therefore, D. umbra is present in the Asian portion of Eurasia at both temperate (albeit montane) and arctic latitudes ( Fig. 17 ). Therefore, as with D. lacustris ( Petrusek et al., 2007, 2008), D. umbra needs to be regarded as an Arctic-alpine taxon.

Taxonomic reconsideration and resolution of the ‘ umbra problem’

The name ‘ umbra ’ may be declared as unavailable and we may establish a new taxon. However, we think that such a step does not follow the logic of the ‘maximum stability compatible with taxonomic freedom’ declaration in the Preamble of ICZN (2000). Therefore, we accept the authorship of Taylor et al. (1996) for this taxon (as having a clear indication of novelty and published in paper), adding only that the taxon ‘ D. umbra ’ is based on the typification made here. Consequently, the correct name of this taxon is ‘ D. umbra Taylor, Hebert et Colbourne, 1996 emend. Zuykova et al., 2018 .

Figures

Figure 8. Daphnia dentifera, parthenogenetic (A, E–H), ephippial (B–D) female and adult male (I–Q) from Silver Lake, IN, USA, AAK M-1129. A, parthenogenetic female, general view. B, ephippial female, general view. C, its rostrum. D, dorsal plate of ephippium. E, dorsal margin of parthenogenetic female. F, abdomen and postabdomen. G, abdominal projections. H, postabdominal claw. I, adult male, general view. J, its head. K, ventral margin of valve. L, postero-ventral valve portion. M, abdomen and postabdomen. N, abdominal projections. O, postanal teeth of postabdomen. P, postabdominal claw. Q, antenna I. Scale bars denote 1 mm for A, B, F, I; 0.1 mm for C–E, G, H, J–Q.

Figure 9. Daphnia dentifera, adult male from Silver Lake, IN, USA, AAK M-1129. A, limb I. B, its distal portion. C, innerdistal portion of limb II. D, limb V. Scale bar denotes 0.1 mm.

Figure 10. Photographs of parthenogenetic females of Daphnia umbra. A, B, G. O. Sars syntypes of Daphnia alpina, GOS F 1933B. C, D, specimens from Borzu-Kol Lake, Siberia, AAK M-3200.

Figure 11. Daphnia umbra, parthenogenetic female from pond 4-7 (neotype locality), Melville Peninsula, Canada, DJT 10-201. A, general view. B, C, head. D, rostrum. E, F, armature of postero-ventral and posterior valve margin. G, postabdomen. H, abdominal projections. I, J, postabdominal claw. Scale bars denote 1 mm for A; 0.1 mm for B–J.

Figure 12. Daphnia umbra, ephippial female from a small unnamed pond close to the Alpine Research Center at Finse, Norway, DJT 3-472. A, general view. B, head. C, dorsal plate of ephippium. D, armature of postero-ventral valve margin. E, postabdomen. F, postabdominal claw. Scale bars denote 1 mm for A; 0.1 mm for B–F.

Figure 13. Daphnia umbra, head and thoracic appendages of parthenogenetic female from a small pond close to the Alpine Research Center at Finse, Norway, DJT 3-472. A, antenna II. B, distal portion of its distal segment. C, limb I. D, its distal portion. E, limb II. F, inner-distal portion of limb III. G, middle portion of gnathobase III. H, limb IV. I, limb V. Scale bars denote 1 mm for A; 0.1 mm for B–I.

Figure 14. Daphnia umbra, adult male from unnamed pond no. 4–7 (neotype locality), Melville Peninsula, Canada, DJT 10-201. A, general view. B, armature of valve margin. C, postabdomen. D, its distal portion. E, antenna I. F, distal portion of limb I. G, inner-distal portion of limb II. Scale bars denote 1 mm for A; 0.1 mm for B–G. IDL, inner-distal portion of limb I; ODL, outer distal portion of limb I.

Figure 15. Daphnia umbra, adult male from a small unnamed pond close to the Alpine Research Center at Finse, Norway, DJT 3-472.A, general view. B, head. C, armature of valve. D, E, setae in middle portion of valve. F, armature of postero-ventral valve portion. G, armature of posterior valve margin. H, abdomen and postabdomen. I, abdominal projections. J, postanal teeth on postabdomen. K, postabdominal claw in outer view. L, its inner view. Scale bars denote 1 mm for A; 0.1 mm for B–L.

Figure 16. Daphnia umbra, adult male from a small unnamed pond close to the Alpine Research Center at Finse, Norway, DJT 3-472. A, antenna I. B, limb I. C, its inner-distal portion. D, inner-distal portion of limb II. E, limb V. Scale bars denote 0.1 mm.

Figure 17. Map of Daphnia umbra known distribution (red circles). The base map is from the open domain plain map available at https://marble.kde.org/.