Tonnacypris stewarti ( Daday 1908 ) Bonilla-Flores & Echeverría-Galindo & Frenzel & Pérez & Börner & Dulias & Wang & Schwalb, 2024

Bonilla-Flores, Mauricio, Echeverría-Galindo, Paula, Frenzel, Peter, Pérez, Liseth, Börner, Nicole, Dulias, Katharina, Wang, Junbo & Schwalb, Antje, 2024, Taxonomy, ontogeny, and ecology of Tonnacypris stewarti (Daday 1908) comb. nov. (Ostracoda: Cyprididae) from Nam Co, Tibetan Plateau, Zootaxa 5446 (3), pp. 331-365 : 338-352

Tonnacypris stewarti ( Daday 1908) comb. nov.

Material examined

Valves and individuals with soft parts from ten lakes on the Tibetan Plateau and Afghanistan were investigated, including measurements of right and left valves ( Table 3 ). In general, both females and males had longer and higher left valves compared to right valves. Specifically, when using the left valve as a reference, we observed that the valves of females from Mang-tsa, Tangqung Co, and Nam Co on the Tibetan Plateau were, on average, longer and higher (L= 1231 µm; H= 571 µm) than those of females recorded from Afghanistan (L= 1200 µm; H= 554 µm). Regarding males from Mang-tsa, their left valves were also longer (1276 µm) and higher (573 µm) compared to males from Afghanistan (L= 1097 µm; H= 514 µm).

In total, we examined 88 females from Nam Co , Mang-tsa , a pond near Tangqung Co , a peatland at Taro Co , rivers at Tangra Yumco , Xuru Co ( Tibetan Plateau ), Heihai lake (material provided by Steffen Mischke, University of Iceland) , Donggi Cona, Huanglong Ravine pond, and Yushu (Qinghai), and the shore of Lake Band-e Amir ( Afghanistan) , as well as 17 males from Mang-tsa (Tibetan Plateau) and Lake Band-e Amir ( Afghanistan) .

Morphological description of Tonnacypris stewarti from Nam Co, Tibetan Plateau: The morphological description includes the dissection of eight adult females, and the measurements (L= length and H= height) of 284 right valves and 277 left valves of different instars.

Carapace description: Carapace whitish (Nam Co) and sometimes yellowish ( Afghanistan) ( Fig. 3 ); smooth, elongated at the posterior end, and reniform in lateral view. Almost straight dorsal margin and slightly sinuous ventrally. Rounded anterior margin and triangular posterior end with an angle of approximately 45° on the right valve and 50° on the left. The left valve is longer and higher (L= 1171 µm, H= 591 µm) than the right valve (L= 1108, H= 545 µm) ( Fig. 3 ). In interior view, both valves present a wide calcified inner lamella in the anterior and posterior parts, along with multiple surface pores with setae. Furthermore, both valves exhibit marginal pore canals ( Fig. 3 E 1 ). In the left valve, generally, a small anteroventral peg is present, but sometimes the peg is inconspicuous ( Fig. 4 A 3 ). In this case, the left valves of females from Nam Co are very small, and in specimens from Tangra Yum Co and Afghanistan the anteroventral peg is very inconspicuous ( Fig. 4 C 1 , C 2 ).

Description of soft parts of a female from Nam Co: A1 ( Fig. 5A ). Divided into seven segments: segment I with two setae, which are twice as long as the long segment and present setules and one shorter seta on the dorsal side; segment II with a seta on the dorsal side; segment III with two setae, one ventral and one dorsal; segments IV and V each with two setae on the ventral side and two on the dorsal side; segment VI with four long seta and one α seta; terminal segment with two long setae, a short sturdy claw, and a much shorter ya aesthetasc.

A2 ( Fig. 5B ). Divided into five segments. Coxa with two setae with setules and one without setules; second segment or basis is robust with a seta on the ventral part. Exopodite with three setae, two short and the longest with setules. First endopodal segment with aesthetasc Y in the ventral part, on the apical side a large seta and a group of six short swimming setae, unequal in length (not reaching tips of terminal claws), the first on the apical side is the longest while the second to the fifth are progressively shorter. Second endopodal segment undivided, with two setae on the dorsal side, four t-setae (t1‒t4) with the longest t2 and t3. Aesthetasc y1 on the ventral side and y2 on the distal part of the second endopodal segment, aesthetasc y3 is located on the interior-distal side of the third endopodal segment with a accompanying seta. In the apical part of the penultimate segment there are three claws (G1‒G3) and three z setae, z1 slightly longer than the other two (z2 and z3). In addition, there is a GM (greater claw) and a Gm (minor claw) in the last endopodal segment.

Md coxa sclerotized ( Fig. 5C ) and 4-segmented palp of mandible ( Fig. 5D ). Md coxa has seven teeth with a plumed seta in the lateral region. First palp-segment with a respiratory plate with five setae, similar in length, except for a shorter one on the subapical part. It presents a group of four apical setae on the inner side including the α seta, two long plumed setae (S1 and S2), and one long smooth seta. Second segment with a group of three smooth setae. The β seta is next to the three distal smooth setae on the interior side. The third segment has ten smooth setae, four on dorsal side, and five situated more ventrally to a γ seta. The fourth segment has seven distal setae, three of them with setules, while four are smaller and smooth (setae incompletely illustrated).

Upper lip and rake-like organ ( Fig. 5E, F ). Rake-like organ with seven teeth on the right and eight on the left.

Mxl ( Fig. 5G ). Composed of maxillular palp, three endites, and a branchial plate. The palp is two-segmented: the first rectangular with eight setae, the second trapezoidal with five smooth setae. The first endite has four smooth setae plus two setae with setules; second endite with six setae; the third endite has four smooth setae and two with setules, in addition, there are two smooth Zahnborsten. The branchial plate consists of 23 plumed setae.

T1 (maxilliped) of female ( Fig. 6A ). The endopodite has one long smooth seta (h2) and two shorter setae (h1 and h3). The gnatobasic endite has 14 smooth setae (incompletely illustrated). Respiratory plate with six plumed setae. In the protopodite, there are two short a-setae, a single c-seta, b-seta and d-seta; b and d are smooth and longer than c.

T2 ( Fig. 6B ). Protopodite with a 33 µm long d1 seta and d2 seta approximately twice as long, 63 µm. First and second endopodal segments each with a smooth seta (e and f) in the distal part. Third endopodal segment with one g-seta and one short seta. Terminal segment with two short setae (h1 and h3) and curved serrated claw (h2).

T3 ( Fig. 6C ) with four segments. The first with a long and tiny plumed seta (d1), and with two tiny plumed d2 setae and a dp seta located at the base. In the distal part of the second segment, it presents an e-seta with setules similar to the f-seta on the third undivided segment. The fourth segment, a pincer organ, has a small h1 seta, distally serrated h2 seta and the smooth h3 seta.

CR ( Fig. 6D ) is an elongated structure of approximately 340 µm length. It has a line of chaetae on the ventral edge. The distal part has two claws, Gp smaller than Ga. In addition, there are two setae, Sa and Sp, the latter is thicker and stronger ornamented with setules. CR attachment simple, without loop. Next to the CR there are two well-differentiated genital lobes.

Female genital lobes of T. stewarti ( Fig. 6D ). Each female presents two lobes with crescent-shaped sclerotized tissue, without projections. The anterior part is triangular and in the internal part, there is an intersection where a tube joins.

Description of soft parts of a male from Lake Band-e Amir, Afghanistan: A1 ( Fig. 7A ). Regarding the morphology, the male is similar to the female, and composed of seven segments. Segment I has a short seta on the dorsal side and two long setae on the ventral region. Segment II has a trapezoidal shape, with a short seta on the dorsal zone. Segment III possesses a ventro-apical seta that extends to the end of segment four, and a dorsal-apical seta that reaches segment VII. Segment IV is slightly square-shaped, featuring two long dorsal-apical setae and one ventro-apical seta. Segment V has two long ventro-apical setae that reach the segment VII. Segment VI is elongated and bears four long apical setae and one short α seta. Finally, segment VII is somewhat slender, with three (two long and one short) apical setae and a sensory aesthetasc (ya).

A2 ( Fig. 7B ) is divided into four segments. The coxa exhibits three short setae, one smooth ventro-posterior seta, and two setae with setules on the ventro-apical region. The basis is a robust segment with a long seta on the ventro-apical region, extending to the endopodal segment. The exopodite consists of two short setae and one long seta with setules. The first endopodal segment contains a sensory aesthetasc Y located ventrally at the midpoint of the segment, a robust seta with setules on the ventro-apical region, and six natatory setae of unequal length in the apical region. Moving to the second endopodal segment, there is a tiny sensory aesthetasc y1 on the ventral side, along with four short t-setae. Additionally, there are two short setae in the mid-dorsal region, with two claws (z1 and z2), and a z3 seta. The z3 seta is long and extends to the z1 claw. G1 is short and robust with denticles, measuring 1/3 the length of G2. G3 is short and thin, located close to the sensory aesthetasc y2 and accompanied by a short seta. Claw z2 is slightly shorter than z1. Gm is half the length of GM, together with the slender aesthetasc y3.

Md ( Fig. 7C ) is composed of a sclerotized coxa and a Md-palp with four segments ( Fig. 7D ). Md coxa bears seven teeth, with one seta with setules on the ventral region and another smooth seta on the dorsal region. The first segment of Md-palp features a branchial plate consisting of five setae, with the subapical seta being shorter. On the interior side, there is a group of four apical setae, including the α seta, two long plumed setae (S1 and S2), and one long smooth seta. The second segment possesses three smooth setae. Seta β is situated alongside the three distal smooth setae on the interior side. The third segment has ten smooth setae (incompletely illustrated), with four on the dorsal side and five located more ventrally towards a γ seta. The fourth segment has seven distal setae (incompletely illustrated), three of them with setules, while the remaining four are smaller and smooth.

Upper lip and rake-like organ ( Fig. 7E ) with seven teeth on the right and eight on the left.

Mx1 ( Fig. 7F ). In the male, the Mxl structure comprises a maxillular palp, three endites (with chaetotaxy incompletely illustrated), and a branchial plate (not illustrated). The palp is divided into two segments. The first segment is rectangular in shape and bears eight setae. The second segment is trapezoidal and features five smooth setae. The first endite has four smooth setae along with two setae adorned with setules. The second endite has six setae, while the third endite has four smooth setae, two setae with setules, and two smooth setae shaped like horns. The branchial plate is equipped with ~23 plumed setae.

T1 (maxilliped) ( Fig. 8A–B , 9A ). Sexually dimorphic with prehensile palps, with a finger-shaped curvature, two small setae are located near the curvature of the endopodite on its ventral side. The gnatobasic endite is equipped with 13‒14 smooth setae (incompletely illustrated). Additionally, the respiratory plate bears six plumed setae. Within the protopodite, there are two short a-setae, along with a single c-seta, b-seta, and d-seta. Both b and d setae are smooth and longer than c-seta.

T2 ( Fig. 8B ) shows a protopodite with a long d1 seta and a d2 seta, which is approximately twice as long. The first and second endopodal segments each have a smooth seta (e and f) at their distal parts. The third endopodal segment is equipped with one g-setae and one short seta. The terminal segment possesses two short setae (h1 and h3) and a curved serrated claw (h2).

T3 ( Fig. 8C ) consists of four segments. The first segment has a long and tiny plumed seta (d1) and two tiny plumed setae (d2 and dp) located at the base. In the distal part of the second segment, an e-seta with setules is present, similar to the f-seta found on the third undivided segment. The fourth segment, known as the pincer organ, contains a small h1 seta, a distally serrated h2 seta, and a smooth h3 seta.

CR ( Fig. 8D ) is an elongated structure. Along the ventral edge, there is a line of chaetae. The distal part of each ramus features two claws, with Gp being smaller than Ga. Additionally, there are two setae, Sa and Sp, with the latter being thicker stronger set with setules. CR attachment simple.

Hemipenis ( Fig. 8E and 9C 1‒C 2 ) with small dorsal lobe (dl). The lateral shield (ls) and medial shield (ms) are sub-triangular, both are rounded and smooth. The ms is slightly longer than ls. (See also the descriptions by Daday 1908 and Peng et al. 2021.)

Zenker organ ( Figs. 8F and 9B ). The specimen from Lake Band-e Amir, Afghanistan with ~21 spines.

Comparing carapace and soft parts of specimens from Afghanistan, Nam Co, and Mang-tsa with specific observations: Specimens from Afghanistan exhibit numerous scars on the dorsal part of the right and left valves, a feature also observed in Nam Co individuals ( Fig. 3 E 2 ). Notably, females from Afghanistan display greater length (1392 µm) and height (638 µm) than those from Nam Co (1256 µm; 585 µm).

The structures and number of setae on the first antennae, second antennae, mandibles, maxilla, second thoracopod, third thoracopod, and caudal ramus remain consistent when compared with T. stewarti individuals from Nam Co ( Figs. 5‒8 ). Similarly, the T1 of males from Afghanistan present the same finger-shaped curvature as individuals from Mang-tsa ( Fig. 8A ).

In contrast, the hemipenis of the individual from Afghanistan displays more reduced medial and dorsal lobes than those of the Tibetan individuals that are slightly wider ( Fig. 10A‒C ).

We observed variations in the shape of the female genital lobes among species. Interestingly, female specimens of Tonnacypris stewarti consistently displayed lobes with a similar shape structure. Notably, the examined females of T. stewarti did not show variations, despite being collected at different sites on the Tibetan Plateau and in Afghanistan ( Fig. 10D‒G ).

Carapace ontogeny: Eight development stages were recognized from juveniles A-7 to adults, with measurements of the valves in length and height ( Fig. 11 ). In adult individuals, the average length of right valves was found to be 1108 µm, while the left valves measured 1171 µm. Additionally, adult right valves had an average height of 545 µm, while left valves had an average height of 591 µm ( Table 4 ). Among A- 7 juveniles, the average length of the right valve was recorded as 270 µm, and the left valve averaged at 276 µm. As for the height measurements, the right valve had an average of 163 µm, and the left valve measured 178 µm.

In order to identify a growth pattern of T. stewarti and to contribute to understandings of its ontogeny, we analyzed the average length and height measurements of the valves. Our findings revealed that the right valves exhibited a range from 1.188 to 1.282, with a mean of 1.224, while the left valves exhibited measurements between 1.187 and 1.283, with a mean of 1.230 (see Table 4 ). The valves’ growth ratio of length and height follows Brooks’ rule. Regularly, for the adults, the right and left valves have a distinct trapezoidal shape and are straight at the dorsal margin ( Fig. 12 ). Both have well-recognized antero-dorsal and postero-dorsal angles, and the dorsal margin is almost straight. On the other hand, in the early juvenile stages the valves display a distinct triangular morphology in the posterior segment. This characteristic is attributed to the yet-to-develop posterior appendages in this body region, as opposed to the anterior segment where the initial appendages are more developed and specialized for swimming. The anterior part presents a rounded shape at the margin ( Fig. 13 ).

Additionally, a detailed observation of the morphology of T. stewarti juveniles revealed a distinct striated pattern of lines, gradually fading in the A-1 stages and adulthood ( Figs. 12 and 13 ).

Considering the total abundances of juveniles and adults, encompassing living and sub-fossil records ( Fig. 14 ), high numbers were recorded mainly in samples from within the lake (samples 7, 10, 14, 15, and 16), with dominating juveniles. In the samples from rivers and lagoons, the individuals in samples 1, 5, and 6 were mainly adults. However, it was not possible to observe a clear pattern of abundances of juveniles or adults defined by the type of habitat, since the sampling was only undertaken during one season of the year.

Distribution and ecology of T. stewarti in Nam Co, Tibetan Plateau: The species was found at high elevations, reaching up to 4742 m a.s.l. Our results indicate that T. stewarti is widely distributed in Nam Co. The highest abundances were observed at three sites with varying water depths: sites 7 (174 individuals, 4 m depth), 10 (195 individuals, 27 m depth), 14 (186 individuals, 40 m depth). Additionally, T. stewarti can also be found in small numbers in lagoons and rivers; however, a notably higher abundance of living individuals occurs within littoral zones of Nam Co. The ecological preferences of T. stewarti are correlated with specific hydrological parameters. Notably, this species exhibits affinity to water conductivities spanning from 149 to 1894 µS/cm, water temperatures ranging from 3.6 to 18.9 °C, an average pH of 9.1, and a dissolved oxygen concentration of 6.8 mg /l. The prevailing alkalinities in the water body range from 1.3 to 18.2 mmol/l.

The cluster analysis reveals three groups of samples: Group A comprises samples from deeper lake water below 8 m depth, group B those from mostly shallow parts of the lake and open lagoons, and group C those from rivers and confined lagoons ( Fig. 15A ). Mean abundance of Tonnacypris stewarti is similar in all three groups but shows different ranges. Whereas minima range between 4 and 6 specimens /g for all three groups, samples of group A (deeper lake) show the highest maxima ( Fig. 15B ). These samples are characterized by highest conductivity, alkalinity, pH, oxygen concentration, and lowest water temperature ( Table 5 ). The shallow river and confined lagoon habitats of group C show the contrary, and the values of group B lay mostly in between except for oxygen concentration, which is similar for groups B and C.

Figures

FIGURE 1. Chronological overview of descriptions and synonyms for Tonnacypris stewarti since 1908. The green rectangle designates living specimens with preserved soft anatomical structures. The incorporation of two asterisks (*) further signifies the inclusion of male specimens exhibiting soft anatomical structures. The gray rectangle denotes scrutinized fossil and subfossil specimens.

FIGURE 2. Study area. A) Location of Nam Co on the Tibetan Plateau, and B) sampling sites according to the habitat type and abundances (living and sub-fossil organism (2 valves = 1 organism) per gram wet weight, org/g wet) of Tonnacypris stewarti (Daday 1908) in Nam Co. Abundance distribution was categorized into three distinct patterns: a complete circle (indicating low abundance), a cross-circle (indicating medium abundance), and a circle with a central line (indicating higher abundance). Sample numbers correspond to Table 2. The elevation bar corresponds to map B. Source: Esri, Maxar, GeoEye, Earthstar Geographics, CNES/Airbus DS, USDA, USGS, AeroGRID, IGN, and the GIS User Community.

FIGURE 3. Valve images of Tonnacypris stewarti (f = female, m = male): (A1) exterior view of left valve (LV) and (A2) right valve (RV); interior view (A3‒A4) of a female from Nam Co (reference-ID NC18-S-37). Exterior view of LV (B1) and RV (B2) of a female; interior view of RV (B3) and LV (B4) of male from Mang-tsa, Tibetan Plateau (TP) (Daday 1908; reference-ID HNHM-IV-369). Arrows above Figures A1‒A2 and B1‒B2 point to anterior end of the valve. Exterior view of LV (C1) and RV (C2); interior view (C3‒C4) of a female; exterior view of LV (D1) and RV (D2); interior view (D3‒D4) of a male from Lake Band-e Amir, Afghanistan (Hartmann 1964; reference-ID ZMH-K27716). (E1) shows the marginal pore canals in the anteroventral side in the right valve, and (E2) denotes the scars on the dorsal part of the left valve of T. stewarti.

FIGURE 4. Left valves of two individuals from Nam Co (A1‒A3) (reference-ID NC18-S-37). A2 and A4 indicate the inconspicuous anteroventral peg of each one. Left and right valves from Tangra Yum Co, TP (B1‒B2) (reference-ID TIP11-29); left valve of a female from Lake Band-e Amir, Afghanistan (C1) (reference-ID ZMH-K27716), with a close-up of anteroventral part (C2).

FIGURE 5. Tonnacypris stewarti, female from Nam Co (reference-ID NC18-S-37). A) left A1, exterior view; B) left A2, interior view; C) left Md coxa, exterior view; D) left Md-palp, interior view; E) upper lip; F) rake-like organ; G) right Mx1 with vibratory branchial plate, interior view. (See Broodbakker & Danielopol (1982) for chaetotaxy.)

FIGURE 6. Tonnacypris stewarti, female from Nam Co (reference-ID NC18-S-37).A) left T1, exterior view; B) left T2, exterior view; C) left T3, exterior view; D) right CR with attachment and the female genital lobes. (See Broodbakker & Danielopol (1982) for chaetotaxy.)

FIGURE 7. Tonnacypris stewarti (= E. afghanistanensis), male from Lake Band-e Amir, Afghanistan (reference-ID ZMH- K27716).A) left A1, exterior view; B) right A2, interior view; C) right Md-coxa, exterior view; D) right Md-palp, interior view; E) upper lip and rake-like organ, F) right Mx1, interior view. (See Broodbakker & Danielopol (1982) for chaetotaxy.)

FIGURE 8. Tonnacypris stewarti (= E. afghanistanensis), male from Lake Band-e Amir, Afghanistan (reference-ID ZMH- K27716). A) right T1, interior view; B) left T1, exterior view; C) left T2, exterior view; D) right T3, interior view; E) CR with attachment; F) hemipenis; and G) Zenker organ. (See Broodbakker & Danielopol (1982) for chaetotaxy.)

FIGURE 9. Tonnacypris stewarti (= E. afghanistanensis); male from Lake Band-e Amir, Afghanistan (reference-ID ZMH- K27716; Hartmann 1964), A) T1, B) Zenker organ, and C1–C2) hemipenis of male. Abbreviations: dorsal lobe (dl), lateral shield (ls), and medial shield (ms).

FIGURE 10. Hemipenis and female genital lobes of T. stewarti from:A) Mang-tsa, Tibetan Plateau (TP) (reference-ID HNHM- IV-369, Daday 1908); B) Lake Band-e Amir, Afghanistan (reference-ID ZMH-27716, Hartmann 1964); and C) near Linzhi, TP (modified from Peng et al. 2021). Dorsal lobe (dl), lateral shield (ls), and medial shield (ms). Female genital lobes from: D) Mang-tsa, TP (reference-ID HNHM-IV-369); E) Lake Band-e Amir, Afghanistan (reference-ID ZMH-27716); F) Nam Co, TP (reference-ID NC-18-S-37); G) Peat near Taro Co, TP (reference-ID TIP11-105). The arrows indicates the intersection or a hook.

FIGURE 11. Carapace ontogeny of Tonnacypris stewarti (Daday 1908) from Nam Co (reference-ID NC18-S-37), measures in length and height of (A) right valves (RV) n = 284 and (B) left valves (LV) n = 277 clearly show the different developmental stages. The histograms show the abundances of the different stages with the scatter plot (juveniles A-7 to adults).

FIGURE 12. Valves of an adult and juveniles (A-1 to A-4) of Tonnacypris stewarti from Nam Co (reference-ID NC18-S-37). Arrow points to anterior.

FIGURE 13. Valves of the first stages of development of T. stewarti from Nam Co (reference-ID NC18-S-37). They show a striated pattern on the surface of the valves. Right valve of juvenile A-5 and a close-up of center-dorsal of the valve (A). Right and left valves of juvenile A-6. Right and left valves of juvenile stage A-7, with a detail of the surface of the left valve (B). Arrow points to anterior.

FIGURE 14. Total abundance of T. stewarti from Nam Co, including both living and subfossil specimens. Bold values indicate percentages, while absolute abundance is presented within parentheses.Valve categorization includes juveniles (A-7 toA-1) and adults. Sample differentiation is based on habitat type: river, lagoon, and lake.Adult specimens are represented by the gray bar, and juvenile specimens by the black bar. (Sample codes correspond to those listed in Table 1.)

FIGURE 15. A) Classification of samples according to associated environmental factors (water depth, electrical conductivity, water temperature, and pH). Group A contains samples from the open lake, group B those from shallow waters, open lagoons and embayments, group C those from rivers and confined lagoons. B) The boxplots below the dendrogram show mean values (x) and variance of Tonnacypris stewarti abundance within the three groups of habitat types. For means and ranges of environmental factors see Table 5.