Bythotrephes cederströmii Schödler, 1877, Schodler, 1877

Korovchinsky, Nikolai M., 2015, Redescription of Bythotrephes longimanus Leydig, 1860 and B. cederströmii Schödler, 1877 (Crustacea: Cladocera: Onychopoda), with notes on the morphology and systematics of the genus Bythotrephes Leydig, 1860, Zootaxa 3955 (1), pp. 1-44 : 21-29

Bythotrephes cederströmii Schödler, 1877

( Figs. 10–11 )

Bythotrephes Cederströmii Schödler, 1877 , pp. 233–234; Lieder 1988, pp. 125–127, Figs. 3 , 4 .

Bythotrephes cederstroemii var. Cederströmii s. str.: Lilljeborg 1901, pp. 619–621, Tab. 82, Fig. 11 , Tab. 83, Fig. 1 , 2 .

Bythotrephes cederstroemi Schödler, 1877 : Rylov 1935a, pp. 154–155, Fig. 233 (partim); Flössner 2000, pp. 377–379, Abb. 137 (partim).

Non Bythotrephes cederströmii: Schödler 1863 , pp. 73–74; P.E. Müller 1868, pp. 203–214, Tab. 4, Fig. 29, Tab. 5, Fig. 1 –18, Tab. 6, Fig. 7 ; Lilljeborg 1901, 621–623, Tab. 83, Fig. 3–5 , Tab. 84, Fig. 1 , 2 ( B. cederströmii var. robustus ), 623–625, Tab. 84, Fig. 3–6 ( B. cederströmii var. connectens ); Linko 1901, pp. 80 ( B. longimanus var. cederströmii ); Chugunov 1922, pp. 2, 3; Ischreyt 1934b, pp. 181–202, Figs. 1–7 ; Spizharny 1929, pp. 17–23, Figs 1–8 ; Rylov 1935a, p. 154–155, Figs 231, 232 (partim); Vekhov 1987, pp. 28–29, Fig. 2 ( B. longimanus cederströmi ); Røen 1994, pp. 109–110, P. 44–47; Martin & Cash-Clark 1995, pp. 64–81, Figs. 1 –20; Litvinchuk 2002, pp. 126–127, Figs. 32, 33, 2007, pp. 190–191.

Incertae sedis: Manuilova 1964, pp. 293–294 ( B. cederströmii ); Mordukhai-Boltovskoi & Rivier 1987, pp. 149–152 ( B. longimanus ); Rivier 1998, pp. 169–173, Fig. 215e, 216 ( B. longimanus ).

Material examined. Type material. Sweden: 1) A slide (MNB (N º 1598) labelled “ Bythotrephes cedersrömii Schödl., See Saxen in Wermland” with 1 ad. (lectotype, designated by Lieder (1988)) and 1 ad. (paralectotype, the same designation) (for description of lectotype see Lieder (1988)); 2) bottle (MNB (N º 5537)) with a front label: “ Bythotrephes Cederströmi Schödler, Sjöen Saxen, Wermland , Schweden, 18.7.1863, v. Cederström S., Syntypen ”, other two labels are inside the bottle: “ Bythotrephes cederströmii Schödl., Wermland, Saxensee , leg. 18/7 63 Cedersr.”, “ Bythotrephes Cederströmii Schödl., 1877 = Bythotr. Cederstroemi Schödl, Syntypen, determ. Lieder, June 1976 ”. The bottle contains five small tubes: a) 2 ad., 1 juv (paralectotypes), b) 4 ad., 4 juv. (paralectotypes), c) 2 juv. (paralectotypes), e) 9 ad., 5 juv. (paralectotypes) (the fifth tube with a faded label “ Bythotr. Cederströmii , L 16”, possibly written by Schödler, contained specimens (4 ad.) of another species (presumably of “ B. brevimanus ”- type); these specimens, which were not mentioned in Lieder (1988), were transferred by the author of the present paper into a separate bottle); 3) bottle (MNB (N º 13752)) labelled with two labels: “ Bythotrephes cederströmi Schödler, See Nerika , Schweden, Holvuvistjärn, leg. v. Cederström, 19.7.1863 ” and “ Bythotrephes cederströmii Schödl. , Material as in See…, design. Lieder, June 86 ” and contained 6 ad. and 4 juv., 4) bottle (MNB (N º 13753) with 12 small tubes, one of them illegibly labelled “N º. 14, Nerika, 19.7.1863, Sjön Holferssnon…” (possibly Holvuvistjärn) contained remains of females of B.cederströmii – type.

Other material. There are other three samples with Bythotrephes cederströmii from the same set of type material collected by G. Cederström in Lake Saxen and kept in Museum of Evolution of Uppsala University ( MEUU). Specimens of the samples were investigated by Lilljeborg, not Schödler, the author of original description of the species under consideration, and for this reason formally they cannot be considered type specimens ( ICZN 72.4.1.1): 1) small bottle (№ 635a) labelled “ Bythotrephes cederstroemii v. Schödler (= B. borealis Lilljeborg ), Nerike, Sjön Saken, 18.7.1865 [probably 1863], G.C. Cederström, Typ-ex”, 3ad., 1 juv., 2) sample Nº 2313 labelled “ Bythotrephes cederströmii Schödler ( borealis ), ♀, Sw., Nrk., Saxen, 18.7.1865 [probably 1863], Cederström G.C., det. Lillj.”, 2 ad., 1 juv., 3) sample N º 2666 labelled ” B. cederströmii, Sw., Nrk., Saxen , 18.7.1863, G.C. Cederström”, 3 ad.

Specimens collected not in the type locality but in three other Swedish water bodies and stored in MEUU are as follows: 1) subsample N º 635c (specimens from sample № 2681) labelled “ B. c. robustus, Sw., Sm., Bolmen, 15.7.1885, F. Trybom”, 9 ad., 2 gam., 4 males; 2) sample N º 2314 labelled “ Bythotrephes cederströmii, Sw., Sm., Bolmen , 15.7.1885, Trybom F.”, 2 dissected ad.; 3) sample N º 2683 labelled “ B. c. robustus, Sw., Dsl., Stora Le, 17.8.1892, C. Aurivillius”, 3 ad., 1juv; 4) sample N º 2686 labelled “ B. cederströmii s.str., Sw., Sm., Bolmen, 27.6.1893, F. Trybom”, 1 ad.; 5) sample N º 2688 labelled “ B. ced . robustus, Sw., Vstm., Kopparberg, Ljusnaren, 23.7.1894, Trybom F.”, 4 ad.

The supposed hybrids Bythotrephes cederströmii x “ B. crassicaudus “ (the latter name is in inverted commas due to its questionable validity).

Sweden: Bottle (MNB, without a number) with a tube labelled “ B. cederströmii Schödler, Karesuando , 31/7 1875, W. Lilljeborg ”, 22 gam., 5 males, 1 juv.

Russia: 1) bottle (MNB, without а number) with another tube labeled “Onega Lake, Aug 1890 ..?, H. Linder, Bythotrephes Cederströmii Schödler ”, 5 ad, 4 males, 1 juv; 2) bottle ( ZIN, N º 73-915) labelled “Collection by A.K. Linko” with 17 tubes, one of them with a label “Lake Onega” (thus probably all samples originate from this lake and its vicinities), in total, 87 ad. and 27 juv.; 3) Lake Pozemskoje (Karelia) (65°9625’N; 34°1125’E), 0 7.08.2009, coll. A.V. Tiunov (AAK-M-1200, AAK-M-1201), 23 ad.; 4) Lake Kubenskoje (Vologodskaja region), 0 6.2011, coll. E.V. Labunicheva, 1 ad. ( NMK); 5) River Shima (Vologodskaja region), 0 5.07.2012, coll. E.V. Labunicheva, 1 ad. ( NMK); 6) Lake Kovzhozero (Vologodskaja region), 12.07.2011, coll. E.V. Labunicheva, 5 ad., 5 juv. ( NMK); 7) Uglicheskoje Reservoir (River Volga, Central European Russia), summer 2005, coll. V.I. Lazareva, 10 ad., 1 male, 8 juv. ( NMK); 8) Lake Taiylar (Viluisky district,Yakutia, Eastern Siberia), 0 8.2008, coll. I.G. Sobakina, 31 ad., 5 males, 3 juv. ( NMK).

Data on body and body parts measurements of specimens from three populations are presented in Table 3 . The main part of the description is based on population from Lake Saxen ( Sweden).

Description. Female. General body appearance and segmentation. General body shape as in B. longimanus ( Fig.10 , 11 A). Postabdomen bears ventrally a pair of massive and long claws curved anteriorly. Caudal process is very long and thin, bearing similar but shorter claws situated distantly from the former ones and one from another and a conspicuous denticulated curve posteriorly. Body length of females (without caudal process) may reach 3 mm or slightly more (in the examined specimens it ranges from 1.94 to 3.04 mm), whereas the length of caudal process surpasses body length considerably.

Head. Comparatively very large (35.6‒48.1 % of body length) and divided into two parts—rounded anterior part mostly filled by large compound eye and posterior part, bearing dorsally a large saddle-shaped neck organ, swimming antennae and mouth parts.

Antennules and swimming antennae are as to those of B. longimanus .

Mouth parts as well as thoracic limbs could not be studied in detail because only the museum’s specimens, not accessible to dissection, were at author’s disposal. But generally it seems that they are similar to those ones of B. longimanus .

Thoracic limbs. Limbs of first pair (tl I) are especially long and strong (62.9–104.6 % of body length) ( Fig. 10 , 11 A, 11J). Externally, their protopodite bears small outgrowth ( Fig. 11 E). The first segment of endopodite is long and bears 6–8 anterior lateral setae ( Fig. 2 A, 2J). Distally, this segment bears rather long anterior seta of type “j” (see Fig. 4 J) and longer posterior finely setulated seta of type “k” (see Fig. 4 K) ( Fig. 11 K, 11N). Second segment of endopodite is conspicuously shorter and bears only two apical setae: comparatively long anterior seta of type “j” and longer posterior one ( Fig. 11 L, 11M). The terminal, third segment of endopodite is also long but somewhat shorter than first proximal segment (73.0–94.6 % of the latter) and bears apically four long roughly spinulated setae, two of them terminally and two subterminally. The limbs of second and following pairs have not been studied closely but judging from the observation of the supposed hybrid specimens (author’s unpubl. data) (see further), the structure and armament of B. cederströmii limbs seem quite similar to those of B. longimanus (in particular, the protopodites of tl II–tl III bear similar external outgrowths ( Fig. 11 E)). The same may be said about the abdomen (metasome).

Postabdomen bears large stout claws with apical ends curved forward (32.1–52.8 % of body length; 13.4 –16.7 % in specimens from Lake Bolmen) that flare outwards from the midline ( Figs. 10 , 11 A, 11F–11H).

Caudal process is directly connected with postabdomen and then proceeds as a very long spine-like structure variable in its length (385.5–545.5 % of body length), thus surpassing body length in 3.9–5.5 times ( Fig. 10 , 11 A, 11B, 11F). It is thin (4.0–6.8 % and 3.8–5.9 % of distances between pairs of claws, respectively) and in its proximal half, it bears one or two pairs of claws similar to those on postabdomen but smaller (anterior pair 24.1–37.0 % and posterior pair 14.4–25.0 % of body length; in specimens from Lake Bolmen they are smaller, 6.9–13.7 % of body length) ( Fig. 10 , 11 A, 11B, 11F, 11G). All pairs of claws sit quite distantly one from another (distance between three pairs: 69.9–162.0 and 67.8–130.5 % of body length, respectively; in specimens from Lake Bolmen, 118.6– 146.1 % of body length), the posterior pair of claws is often turned upwards ( Fig. 11 F, 11G). In its middle part or usually more distally (in 50.7–64.4 % of length of caudal process), caudal process bears a prominent curve ( Fig. 10 , 11 B, 11C) covered by numerous small curved denticles directed forward, which sit on its dorsal and ventral sides ( Fig. 11 C, 11D). In specimens from Lake Saxen, this curve is moderately developed ( Fig. 11 D, 11C), while in those from Lake Bolmen it can be more strongly pronounced and is situated closer to apical end of caudal process ( Fig. 11 I, Table 3 ).

Males and gamogenethic females are not known, but again, judging from such specimens of supposed hybrids studied in detail (authors’ unpubl. data), these individuals do not differ in their specific structures from those in B. longimanus .

Juvenile females. Two studied juvenile females differed from adults in slightly thicker caudal process and position of caudal curve situated closer to postabdomen (in 35.9–37.4 % of length of caudal process).

Remarks. Specimens from Lake Holfuvistjärn have comparatively shorter tl I and their distal segment, apical setae of first and second segment of endopodite are stouter with more rough armament. Specimens from Lakes Bolmen and Store Le possess especially prominent curves on extremely long caudal processes. Those from the former locality have unusually small claws of postabdomen and caudal process.

It was found that the lectotype and paralectotype on a slide ( Fig. 10 ) were in a quite good condition, while the condition of specimens in liquid samples was not so satisfactory. Their head and eye were most readily deformed ( Fig. 11 A). For this reason, measurements of such individuals could not be provided as precisely as usual. In total, 17 adult parthenogenetic females and 12 juvenile females were recorded type specimens (lectotype and paralectotypes).

Lilljeborg (1901: p. 619) recorded rather considerable variability of “ B. cederströmii s. str. ” from some Swedish lakes. But mode of his measurements is not known and only single individuals were measured. His limited data on individuals from type locality, Saxen See, do not correspond well to data of present investigation (see Table 3 ).

Intra- and interpopulation variability. The variability of some structures of type specimens from Lake Saxen seems considerable ( Table 3 ). This mostly concerns length of tl I and their distal segment, length of caudal process and size of claws.

Differential diagnosis. B. cederströmii differs from B. longimanus in the presence of shorter tl I (62.9–104.6 % of body length) and their distal segment, the apical anterior setae of first and second segments of endopodite of tl I are long and roughly armed. Caudal process of the former species is much longer (385.5–545.5 % of body length), thinner, and possesses denticulated curve. The postabdominal and caudal claws of its adults are more numerous (two or three pairs), situated distantly one from another, usually conspicuously larger (14.4–52.8 % of body length), stouter, flared outwards and their distal ends are curved forward.

Notes on the supposed interspecific hybrids. In many samples from water bodies of different type, there appeared specimens much similar to B. cederströmii because of presence of more or less expressed curve on caudal process ( Fig. 12 F–12J) and large postabdominal and caudal claws with apical end curved forward ( Fig. 12 A–12E).

For a long time, such specimens were identified either as true B. cederströmii (or its varieties) or sometimes considered as a variety or subspecies of B. longimanus (see e.g., Lilljeborg 1901; Spizharny 1922; Ischreyt 1934b; Vekhov 1987; Yurista 1992; Martin & Cach-Clark 1995).

Litvinchuk (2002, 2007), who made morphometric and biochemical analyses of Bythotrephes , suggested consideration of different forms close at least in some respects to B. cederströmii —either true B. cederströmii or hybrids of the species with two other species ( B. cederströmii x B. brevimanus and B. cederströmii x “ B. crassicaudus ”). However, present investigation has revealed that the type specimens of B. cederströmii s.str. differ conspicuously in some morphological parameters from all other B. cederströmii –like forms, including those studied by Litvinchuk, in the presence, first of all, of an especially long and thin caudal process with the curve shifted closer to its end, and widely separated and usually very large postabdominal and caudal claws. Some B. cederströmii –like forms are reminiscent of the nominal species ( Figs. 12 C, 12D, 12E), but nevertheless differ from it in some parameters ( Figs. 13 A, 13B) (p <0.05; p <0.01).

Figures

FIGURE 1. Scheme of measurements of body parts of Bythotrephes.

FIGURE 2. Bythotrephes longimanus Leydig, parthenogenetic females, Bodensee (Germany) (type locality). A, general lateral view. B, distal part of caudal process. C, antennules. D, proximal seta on antero-dorsal side of basipodite. E, distal end of antennal basipodite, outer side. F, distal end of third segment of upper antennal branch. G, distal end of apical segment of upper antennal branch. H, the same, lower antennal branch. I, maxillule (mx I) and end of mandible. J, thoracic limb of first pair (tl I). K, proximal part of tl I, anterior view (as = anterior setae, ps = posterior seta). L, distal setae of tl I. M, N, distal setae of first segment of endopodite of tl I. O – R, distal setae of second segment of endopodite of tl I. S, abdomen, lateral view. T, terminal setae of caudal process.

FIGURE 3. Bythotrephes longimanus Leydig, parthenogenetic females, Bodensee (Germany) (type locality). A, distal end of second segment of upper antennal branch. B, distal end of mandible. C, papillae of mandibular process. D, spinules of distal part of mandible. E, upper lip (labrum). F, apical papillae of middle lobe of upper lip. Scale bars: 20 µm (A, B, E); 5 µm (C, D, F).

FIGURE 4. Bythotrephes longimanus Leydig, parthenogenetic females, Bodensee (Germany) (type locality). A, protopodite of tl II, outer view (“ exopodite ” arrowed). B, the same of tl I, inner view (co = coxa, ba = basis, e 1 = first segment of endopodite). C, basal parts of thoracic limbs, outer view. D, thoracic limb of second pair (tl II) (as = anterior setae, ps = posterior setae). E, scheme of setae arrangement of tl II (as = anterior setae, ps = posterior seta). F, apical end of tl I. G, thoracic limb of third pair (tl III). H, scheme of setae arrangement of tl III, I, apical end of tl III, outer view. J – N, setae of thoracic limbs of different type.

FIGURE 7. Bythotrephes longimanus Leydig, parthenogenetic females (Switzerland: Lake Geneva (Lac Leman): A, D, I, U – W; Vierwaldstättersee: G, K, L, P; Lake Neuchâtel: B, E, J, Q, T; Italy: Lago di Garda (Lake Garda): C, F, M, O, S; Lago di Como (Comer See): H, N, R). A – C, thoracic limbs of first pair (tl I). D, G, E, F, H, claws of postabdomen and caudal process. I – N, apical setae of first segment of endopodite of tl I. O – W, apical setae of second segment of endopodite of tl I.

FIGURE 10. Bythotrephes cederströmii Schödler, parthenogenetic female (Schweden: Lake Saxen (Prov. Värmland) (lectotype), general lateral view (bend on spine is arrowed). Scale bar 1.0 mm.

FIGURE 11. Bythotrephes cederströmii Schödler, parthenogenetic female (Schweden: Lake Saxen (Prov. Värmland) (paralectotypes): A – H, J, K, L; Lake Holvuvistjarn (Prov. Närke) (paralectotypes): M, N; Lake Bolmen (Prov. Småland): G, I. A, general lateral view. B, F, G, caudal process. C, I, caudal curve. D, denticles of caudal curve. E, proximal parts of tl I – tl III, outer view. H, claws of caudal process, dorsal view. J, tl I. K, N, apical setae of first segment of endopodite of tl I. L, M, apical setae of second segment of endopodite of tl I.

FIGURE 12. The supposed hybrids Bythotrephes cederströmii x “ B. crassicaudus ”; parthenogenetic females (Schweden, Karesuando (Prov. Norrbotten): A, F; Russia, Lake Onega: C, I; Lake Pozemskoje (Karelia): E, J; Uglecheskoje Reservoir (Central European Russia): B, G, H; Lake Taiylar (Yakutia, Eastern Siberia): D). A – E, proximal part of caudal process. F – J, curve of caudal process.

FIGURE 13. Comparative proportions of body parts of Bythotrephes cederströmii s. str. (Southern Sweden) and hybrids (Lake Pozemskoje, Karelia, Russia). A, length of postabdominal claws. B, interclaw distance.

Tables

TABLE 3. Data on body and body parts measurements of Bythotrephes cederströmii from three localities (specimens from type localities: l—lectotype, p—paralectotypes; R—range, M—mean).

N	BL, mm	HL:BL, %	T1L:BL, %	E3L:E1L, %	CPL:BL, %	PBD:CPL, %	PCL:BL, %	CPCL:BL, %	ICD:BL. %	ICTh:ICD, %
Lake Saxen (Värmland, Sweden)
1-l	2.75	47.4	75.4	76.6	410.5	62.4	35.1	28.1 – 15.8	84.2 – 77.2	5.8 – 4.5
2-p	2.30	45.2	95.1	93.2	-	-	52.8	33.3 – 20.8	119.4 – 100.0	5.3 – 4.9
3-p	2.11	-	-	-	545.5	61.1	-	-	-	-
4-p	2.38	43.0	82.5	90.0	-	-	51.0	30.9 – 21.5	115.4 – 96.9	5.2 – 4.9
5-p	2.50	37.1	88.1	85.1	-	-	47.2	32.7 – 20.8	89.3 – 90.6	6.4 – 5.5
6-p	2.93	39.9	-	-	-	-	35.0	32.2 – 19.7	69.9 – 67.8	5.4 – 5.6
7-p	2.32	44.1	92.4	90.7	496.6	60.0	41.4	33.1 – 22.8	88.3 – 91.0	6.2 – 5.7
8-p	3.04	39.5	73.7	85.4	-	-	32.1	25.8 – 17.9	82.1 – 76.3	5.7 – 5.5
9-p	2.99	41.2	73.8	85.1	-	-	37.4	24.1 – 14.4	89.8 – 79.1	4.8 – 4.7
10-p	2.75	41.9	67.4	94.6	-	-	46.5	27.9	102.3	4.0
11-p	2.56	35.6	85.6	89.1	-	-	35.0	27.5 – 19.4	91.3 – 88.8	5.8 – 5.0
12-p	2.10	38.9	84.0	74.4	412.2	50.7	34.4	22.9	91.6	5.8
13	2,16	48.1	104.6	89.2	525.0	64.4	50.9	37.0 – 25.0	117.6 – 106.5	5.5 – 5.6
14	2.62	44.3	82.4	83.3	385.5	60.8	35.9	26.0 – 18.3	74.0 – 71.0	6.8 – 5.9
Lake Holfuvistjärn (Närke, Sweden)
15-p	2.27	39.6	75.4	73.0	-	-	47.2	29.6 – 19.7	162.0 – 130.3	4.0 – 3.8
R M	2.10–3.04 2.52	35.6–48.1 41.8	67.4–104.6 83.1	73.0 –94.6 85.4	385.5– 545.5 462.5	50.7–64.4 59.9	32.1 – 52.8 41.6	24.1 – 37.0; 14.4 – 25.0 29.4 – 19.7	69.9 – 162.0; 67.8 – 130.5 98.4 – 89.6	4.0 – 6.8; 3.8 – 5.9 5.5 –5.1
Lake Bolmen (Småland,		Sweden)
1	2.04	38.2	74.5	85.1	523.5	71.2	16.7	13.7 – 6.9	146.1 – 118.6	2.7 – 3.3
2	1.94	38.1	62.9	77.3	432.0	56.8	13.4	10.3	127.8	3.2