Leptodora kindtii ( Focke, 1844 )

Korovchinsky, Nikolai M. & Boikova, Olga S., 2008, Study of the external morphology of Leptodora kindtii Focke, 1844 (Crustacea: Branchiopoda: Haplopoda), with notes on its relation to Cladocera and on conspecificity of populations of the species over the Eurasian range, Journal of Natural History 42 (45 - 46), pp. 2825-2863 : 2831-2846

Leptodora kindtii ( Focke, 1844)

( Figures 1–72 )

Polyphemus kindtii Focke 1844, pp. 108–109 .

Leptodora hyalina Lilljeborg 1861, pp. 265–268 , Figures 1–22 ; Sars 1861 [1993], pp. 157–159, Figures 110–113; Müller 1868a, pp. 226–231, Table VI, Figures 14–21 ; Weismann 1874, pp. 351–404, Tables XXXIII–XXXVIII.

Hyalosoma dux Wagner 1868, pp. 218–239 , Tables I–IV;

Leptodora kindtii Poppe 1889, p. 542 ; Lilljeborg 1901, pp. 652–658, Table 87, Figures 4–13 ; Behning 1912, pp. 7–9, Table I, Figures 1–6 ; Sebestyén 1931, pp. 10– 15, Figures 1 , 2 , Table I, Figures 1–7 , Table II, Figure 1 , Table III, Figures 1–6 ; Mordukhai-Boltovskoi and Rivier 1987, pp. 167–168, Figures 51, 52 ; Rivier, 1998, pp. 193–194, Figures 38, 39 .

Data on body parts measurements are presented in Table 1.

Female

General body appearance and segmentation. Body strongly elongated, highly transparent and divided into four parts—head, thorax, three-segmented abdomen, and postabdomen ( Figure 1 ). Head with long anterior part, frontally filled by eye and bearing ventrally small antennules in females and large and long ones in males. Posterior part of head bears long swimming antennae with massive basipodite and mouth parts consisting of mandibles, upper and lower lips. Thorax high with strongly developed muscular ventral side bearing six pairs of thoracic limbs of different size directed antero-ventrally. Dorsally posterior part of thorax bears sack-like carapace transformed into brood pouch and hung over the abdomen. The latter is long, three-segmented and flexible, connected with the elongated postabdomen, terminating in a pair of straight claws. General body length of females may reach 18.0–21.0 mm ( Gerschler 1911) but length of the examined specimens did not exceed 10.5 mm.

Head. Large (25.3–33.6% of body length), strongly elongated and slightly narrowing anteriorly. Dorsally it bears a large saddle-shaped neck organ probably responsible for osmoregulation (see Halcrow 1985; Aladin 1996). Eye comparatively small (10.0– 15.9% of head length) with numerous ommatidia (, 500 according to Wolken and Gallik (1965) and Nilsson et al. (1983)) and small central pigment spot. Ocellus (naupliar eye) is absent ( Elofsson 1966) (it occurs only in specimens hatched from resting eggs ( Sars 1873). Head pore ( Figure 14 ) lies on the ventral head side somewhat behind antennules. The pore is slightly elevated over the surrounding integument and has an oval shape reaching about 18–19 mm in length. It seems to be divided into two more or less equal parts and covered by membrane.

Antennules. Small (5.0–8.1% of head length) consisting of cylindrical basal part slightly widened distally and bearing nine long aesthetascs, and one very small sensory seta on its end which is shorter than aesthetascs ( Figures 2 , 13 ). Aesthetascs are disposed in three groups and seem two-segmented or constricted.

Swimming antennae. Long (43.4–63.8% of body length) and strong with massive basipodite ( Figure 1 ) which has dorsal thin naked seta on its folded proximal part ( Figures 3 , 16 ) and small distal outer seta between bases of branches ( Figures 4 , 15 ). Basipodite distal end bears two small denticles on its lower side ( Figure 5 ), and dorsally in front of basal segment of upper antennal branch one small seta, which varies in length ( Figure 17 , with the insertion in the left corner). Basipodite narrows distally and bears two long branches, the upper of which (exopodite) is slightly longer than lower one (endopodite) (18.3– 23.6% vs. 16.4–21.6% of body length). Upper branch is four-segmented and lower branch is five-segmented ( Figures 6, 7 ). Proximal-most segment of the lower branch is rudimentary and clearly developed only dorsally, while the following segment of the branch articulates with the basipodite ventrally under the rudimentary basal segment ( Figures 4, 8, 9 ). Integument of antennal basipodite and branches are covered by tiny spinules, which are situated solitary or in groups. Small dorsal seta on the end of second segment of upper antennal branch ( Figure 18 ), tiny denticles on end of third segment ( Figure 19 ) and small apical spine shifted somewhat proximally on the fourth segment of the same branch ( Figure 20 ). Ends of the second to fourth segments of the lower antennal branch with tiny denticles only ( Figure 21 ), and the last, fifth segment is armed by a small apical spine ( Figure 22 ).

Small proximal-most segments of both antennal branches lack setae, while other segments possess a row of two-segmented swimming setae of different size ( Figures 6, 7 , 23 ). Distal setae of second and third segments of both branches more than twice as long as proximal ones (1.0:0.6–0.8:0.4–0.5), while those on apical segments are longer proximally and shorter distally (0.7:1.0). Basal segment of each seta is comparatively short and stout and supplied with a rest near its base ( Figure 23 , and insertion in the upper right corner). Normally basal segments of most setae are of equal length but sometimes some of them may be longer than others ( Figure 10 ). General formula of antennal setae: 0 (7–12) (5–7) (8–11) / 0 (3–7) (6–13) (4–6) (6–8). Thus, their total number reaches 30 and 34 on upper and lower branches respectively, intra- and interpopulational variability may be significant. In particular, number of setae may differ in antennae of one individual ( Boikova 2005). Each seta is bilaterally armed with rows of uniform long thin setules ( Figure 24 ), length 22–25 mm and thickness about 0.5 mm ( Akeret 1995).

Mouth parts. Mouth parts are represented by upper and lower lips and mandibles. The upper lip (labrum) looks like a thick plate inflated externally, having spade-like, wide distal margin and two papillae on the inner surface ( Figure 25 ). Under the labrum there is a large trilobed lower lip with a large median lobe and two smaller lateral lobes. The anterior margin of the former one is armed by two to three rows of conical prominences of different size ( Figures 25, 26 ). Some groups of small spinules present on the internal surface of the lobe ( Figure 25 ). Each lateral lobe possesses a large anterior palpus-like outgrowth and a row of about 10 flattened, lanceolate prominences along the external margin ( Figures 25, 27 ); Sebestyén (1931) recorded two rows of such prominences on each lobe. Mandibles large with massive, widened proximal part armed with some groups of tiny spinules, and long, sabre-like distal part ( Figure 28 ). The latter one is armed distally with three large denticles, the proximal-most of which is thinner and longer than others and bent apically ( Figure 29 ). Denticles of two mandibles of one specimen may be different in shape ( Figure 49 ). Two distal denticles have a row of tiny spinules near their bases ( Figure 29 ). The mandibular apical end bears two parallel rows of small, thin spinules along its margin ( Figures 29, 30 ). Each row is composed of five combs with 6–12 spines in each situated in the slit-shaped depressions arranged under the angle to the midline of mandible.

Thoracic limbs. Six pairs of strongly chitinized, stenopodous limbs are situated along the triangular massive muscular ventral part of thorax and directed antero-ventrally ( Figure 1 ). Most of their integument is covered by groups of tiny spinules ( Figure 40 ). Limbs of each side are arranged at some angle to the midline of the thorax and to each other, and the anterior four have a much enlarged shoe-like basis adopted for the attachment of strong musculature ( Figure 36 ). All limbs are four-segmented and have complex and variously setaceous armament along their inner side ( Table 2). Setae of the limbs are also strongly chitinized, sit on an elevated basis, and most of them lack setules, having instead denticles of different type ( Figures 42, 43 , 58, 60 ). On the outer side, limbs of tl I–tl V have very small setae, set on the distal margin of their basal segment ( Figures 38 , 59 ) .

Limbs of the first pair (tl I) are especially long and strong (28.7–57.4% of the body length) ( Figures 31 , 37 ) with a very long basal segment (12.5–27.3% of the body length), having in the middle of its inner side one (rarely two) short seta (occasionally, it may be absent) ( Figures 31 , 37, 40 , 50, 51 ) and one short seta distally (rarely, it is absent too) ( Figures 31 , 37, 39 ). The second segment of the limb bears one fairly long seta (sometimes it is absent) in the middle part and two very long setae distally, which reach or slightly exceed the end of the limb. One of these setae is naked ( Figure 31 , ad) while another one bears setules distally ( Figure 31 , pd(s)). The third segment normally bears two or three pairs of lateral setae of different sizes (one of them may bear denticles) and two long setae distally; one of the latter bears denticles, another one setules ( Figure 31 , ad(d) and pd(s) respectively; Figure 41 ). The fourth distal segment of the limb with three to six pairs of lateral setae and three distal setae, most of which, excluding the proximal-most ones, bear denticles of different size ( Figures 42, 43 ). It is characteristic that all these denticles are directed anteriorly.

There is a small outgrowth, gnathobase (processus maxillaris), near the basis of basal segment tl I, bearing one long and one short seta and tiny prominence between them ( Figures 44, 45 ). Integument near the gnathobase possesses both solitary spinules and groups of spinules.

Basal segment of limbs of the second pair (tl II) bears six to eight pairs of comparatively short lateral setae and normally three median setae, two in the middle part and one distally ( Figures 32 , 56, 58 ). The structure of the lateral and median setae of basal segments of all thoracic limbs is quite similar ( Figures 56, 57, 61 ), though the median ones seem stouter and their number is more stable. Two subsequent segments of tl II bear two to four (usually three) long setae along each lateral side and one median seta distally, which differs from those on the basal segment, being slender and setulated ( Figures 34, 35 ). The fourth distal segment usually possesses one to three lateral setae on each side (sometimes only on one side) and three distal setae which seem smooth or just finely denticulated.

Limbs of the third and fourth pairs (tl III, tl IV) have a similar structure and setae armament ( Figures 33 , 46 , 60 ), however, their setae are less numerous and the basal segment of tl IV bears four median setae ( Table 2, Figure 57 ).

The structure and armament of limbs of the fifth pair (tl V) mostly resemble those of the previous ones but their basal segment is inflated, having normally four median setae, and its outer distal seta is larger and shifted more proximally ( Figures 47 , 61 ). Distal median setae of the second and third segments lack setules.

Limbs of the sixth pair (tl VI) are small, two-segmented and always bear seven stout setae distally ( Figures 48 , 62 ). A large bud-like structure lies between limbs of the sixth pair ( Figure 62 ), covering ‘‘catch basket’’ posteriorly.

Carapace. It is visible as a bag-like structure, attached to the postero-dorsal margin of thorax and reaching in adults not less than the middle part of the second abdominal segment (18.8–26.1% of the body length). It is composed of a dorsal part and two lateral valves which are separated from the former by seams. The carapace forms an open brood pouch with valve margins widely overlapped ventrally and posteriorly.

Abdomen. Long (30.3–39.7% of body length), flexible and composed of three segments, the second of which is the shortest, while the first and third are of almost equal size ( Figure 1 ). The abdominal integument is thin, subtly chitinized and lacks tiny spinules as in the case of most other body parts. Oviducts open dorsally in the anterior-most part of the third segment.

Postabdomen. Straight, comparatively long in relation to body length (17.5–26.4%), and with the chitinized integument covered by numerous spinules. Two small, twosegmented and setulated setae natatoriae in the antero-dorsal position ( Figures 11, 12 ). Postabdomen terminates in a pair of postabdominal claws with anal opening between them ( Figure 63 ). The claws are long (10.6–18.3% of body length) and almost straight with a dorsal row of 10–29 denticles and numerous groups and combs of spinules all over their surface ( Figures 64, 65, 67 ).

Male

General body shape and structure as in female but carapace is undeveloped (2.5–6.3% of body length) and looks like a postero-dorsal thoracic outgrowth ( Figure 55 ) reminiscent of juvenile females. Structure and relative size of head, thorax, abdomen and postabdomen as in females of the same population but eye, swimming antennae, tl I and postabdominal claws are relatively slightly larger ( Boikova 2005). Spermaducts open ventrally in the anterior-most part of third abdominal segment.

Antennules. Long (25.8–28.7% of body length) with thickened basal part, bearing a group of nine aesthetascs subdivided into three subgroups of three each as in the female antennules ( Figure 52 ). Solitary aesthetascs may be sited before and after this primary group. The elongated part of the antennule bears up to its apical end a long row of 30–35 aesthetascs ( Figures 53, 54 ). Probably, there is age variability in the number of aesthetascs because previous authors recorded up to 70 aesthetascs in their large individuals (see Gerschler 1911; Røen 1994).

Thoracic limbs. Mostly as in females, except for the presence of the clasping organ on tl I. This organ is composed of a large bud-like structure on the inner, proximal-most part of the distal segment, and a group of prominences on the apical end of the previous, third, segment ( Figures 66, 68, 69 , 71 ). The former is movable, being supplied with a muscle and bears tiny spinules apically. In fixed specimens it is usually retracted beneath the margin of the previous segment ( Figures 66 , 71 ) but in life it projects considerably over the antennal surface ( Figure 69 ). The number of opposite prominences varies from two to six (usually from three to four); occasionally, they may be accompanied by some tiny additional prominences. Sometimes the number of large prominences on limbs of one individual is different ( Figures 71, 72 ).

Morphological variability

The intrapopulational morphological variability has been studied in detail only in representatives of the species from Lake Glubokoe ( Boikova 2005; present study). As for age variability, three tentative juvenile stages have been selected, which differ in females in body length, length of carapace, and degree of ovary development, and in males in length of antennules, degree of testes and clasping structure development. Vijverberg and Koelewijn (2004) found seven juvenile stages in Leptodora cultivated under laboratory conditions.

In the adult females, during growth the relative sizes of eye, antennules, swimming antennae, tl I, and postabdominal claws diminish, while the number of antennal setae increases (p,0.1–0.01). In tl I, number of setae diminishes on second and third segments and increases on fourth distal segment. Postabdominal claws increase more slowly than general body length. In adult males, the size of swimming antennae, tl I, eye, and of postabdominal claws are somewhat larger than in females (p,0.1–0.01). During ontogenetic development, the number of setae on the second and third segments of tl I diminishes, especially in males, while that on the fourth distal segment increases.

In adult specimens of all studied populations, the body length, length of tl I and of its basal segment, the length of the upper antennal branch and the length of postabdominal claws were always the most variable structures ( Table 1). The prominent differences in the length of tl I were especially characteristic of the population from the Gulf of Finland, in which in individuals of similar size it might differ twice (p,0.01) ( Figure 70 , Table 1). The same was true of the number of antennal setae, and of denticles of the postabdominal claws. In thoracic limbs, the armament of two basal segments was always most variable, that of the third and fourth segments is less variable ( Table 2). Among specific male structures, the number of antennular aesthetascs and number of prominences on the end of third segment of tl I were also subject to variability (see above).

With respect to interpopulational variability, individuals from Lake Glubokoe differ significantly from those of two other populations (p,0.01) in the relatively smaller size of swimming antennae and their upper branch, postabdomen, claws, tl I and its basal segment ( Table 1). Probably, this relates to the larger body size of individuals of the former population, as was stated in the study of their age variability ( Boikova 2005).

Individuals of two other populations, from the Gulf of Finland and Lake Khanka, differ less in the studied parameters (p,0.1); however, those from the former locality display greater variability of length of tl I and its basal segment. Also, they differ in patterns of setae variability of the thoracic limbs ( Table 2).

Taxonomical implications

The interpopulational comparisons of specimens of Leptodora kindtii from different localities, including remote ones (e.g., from Europe and the Far East of Russia), mostly have not revealed any morphological differences, especially at wide regional levels, either qualitative or quantitative, which might be substantial enough for taxonomic discrimination. Intra- and interpopulational variability is high and the limits of variation in a trait usually widely overlapped. Values of populations represented by single or a few specimens readily fell within these limits.

Only one set of specimens, from Lake Bolon (the lower Amur River ), represented by just three females and one male, differed significantly from all other representatives of the taxon. They were small (body length 3.09–3.20 mm) but seemed adult, judging from the large shell of the females and developed clasping organs of male. These specimens had no specific qualitative differences save less numerous antennal setae (20–22 and 22–24 setae on upper and lower branches, respectively) but the proportions of their body parts were quite unusual. Thus, they possessed comparatively larger head (36.5–41.9% of the body length), shorter abdomen (25.7–28.1%), longer postabdominal claws (18.3–20.3%), longer upper branch of swimming antennae (22.9–26.2%), longer tl I (50.9–62.8%), and longer basal segment of tl I (25.1–32.0%) .

Figures

Figure 1. Scheme of measurements of body parts of Leptodora kindtii.

Figures 2–12. (2) Antennule; (3) proximal setae on antero-dorsal side of basipodite; (4) distal end of antennal basipodite, outer side; (5) denticles on lower side of basipodital distal end in front of upper branch; (6) upper four-segmented antennal branch (exopodite); (7) lower fivesegmented antennal branch (endopodite); (8) basal part of lower branch, inner side; (9) the same, upper side; (10) two abnormally long basal parts of setae of lower antennal branch; (11) postabdomen, lateral view; (12) seta natatoriae (10 – Lake Khanka, all others – Lake Glubokoe).

Figures 13–18. SEM micrographs. (13) End of antennule (sensory seta indicated by arrow); (14) ventral head pore; (15) distal outer seta of antennal basipodite; (16) proximal anterodorsal proximal seta of antennal basipodite; (17) distal dorsal seta of antennal basipodite (insertion in left corner – the same of another specimen); (18) end of second segment of upper antennal branch. Scale bars – 20mm.

Figures 19–24. SEM micrographs. (19) End of third segment of upper antennal branch; (20) end of upper antennal branch; (21) end of fourth segments of lower antennal branch; (22) end of lower antennal branch; (23) setae of lower antennal branch (insertion in right corner – the base of antennal seta); (24) antennal setules. Scale bars – 20 mm (20–23), 10 mm (24), 5 mm (24, insertion).

Figures 25–30. SEM micrographs. (25) Upper (labrum) and lower lips (arrows indicate papillae of labrum); (26) prominences of median lobe of lower lip; (27) prominences of lateral lobe of lower lip; (28) mandible and labrum; (29) distal mandibular denticles; (30) armament of mandibular apical end. Scale bars – 50 mm (25, 28), 20 mm (26, 29), 10mm (27, 30).

Figures 31–35. (31) Limb of first pair (tl I); 32) limb of second pair (tl II); (33) limb of third pair (tl III); (34) median seta on the end of second segment of tl II; (35) median seta on the end of third segment of tl III. (median setae in Figures 32, 33 are indicated by arrows).

Figures 36–45. SEM micrographs. (36) Basal parts of thoracic limbs from outer side; (37) limb of first pair (tl I), general view (seta on basal segment is indicated by arrow); (38) end of basal segment of tl I, outer side; (39) the same, inner side; (40) middle part of basal segment of tl I; (41) end of distal seta of third segment of tl I; (42) armament of proximal seta of fourth segment of tl I; (43) armament of distal seta of tl I; (44) gnathobase near the base of tl I; (45) gnathobase. Scale bars – 100 mm (36, 37), 50 mm (38–40), 20mm (41, 44, 45), 10 mm (42, 43).

Figures 46–55. (46) Limb of fourth pair (tl IV); (47) limb of fifth pair (tl V); (48) limb of sixth pair (tl VI); (49) ends of two mandibles of one specimen (Lake Bolon, Far East of Russia); (50) setae on the middle part of basal segments of tl I of one specimen (Lake Khanka, Far East of Russia); (51) the same (The Gulf of Finland); (52) basal part of male’s antennule; (53) the same, median part; (54) the same, apical end; (55) male’s shell, lateral view (median setae in Figures 46, 47 are indicated by arrows).

Figures 56–62. SEM micrographs. (56) Basal segment of tl II; (57) basal segment of tl IV; (58) distal median seta of first segment of tl II; (59) small outer seta on the end of basal segment of tl III; (60) ends of distal setae of tl IV; (61) basal parts of tl IV, tl V, and tl VI; (62) tl VI from outer side. Scale bars – 50 mm (56, 57, 61, 62), 10 mm (58, 59, 60).

Figures 63–69. SEM (63–67) and optical (68, 69) micrographs. (63) Basal parts of postabdominal claws and anal opening, dorsal view; (64) basal part of claw, lateral view; (65) middle part of claw, dorso-lateral view; (66) male’s clasping organ in fixed animal; (67) end of claw; (68, 69) male’s clasping organ in live animal (arrows indicate prominences on the end of third segment of tl I).

Figures 70–72. (70) Specimens with tl I of different size (The Gulf of Finland); (71) male’s clasping organs of both tl I of one specimen; (72) prominences of clasping organ (Lake Khanka, Far East of Russia).