Kuqaia, Li, 1993

Peng, Jungang, Slater, Sam M., McLoughlin, Stephen & Vajda, Vivi, 2023, New species of Kuqaia from the Lower Jurassic of Sweden indicates a possible water flea (Crustacea: Branchiopoda) affinity, PLoS ONE (e 0282247) 18 (6), pp. 1-20 : 12-15

Kuqaia was first defined as belonging to an unknown palynomorph group owing to its resistance to HF during palynological processing [ 18] and later suggested to represent a megaspore or fragment thereof [ 20]. It has also been proposed that Kuqaia represents a group of gastropods [ 22].

Kuqaia ‘shells’ are typically 300–500 μm long, placing them in the typical size range of extant rotifers (100–500 μm long). The lorica (external cuticle) of rotifers is composed of scleroproteins, is resistant to acids, and some taxa bear elaborate ornamentation along with anterior and posterior spines and other appendages [ 40, 41]. Acid-resistance confers generally

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good preservational potential for those rotifers with a well-developed lorica, and this group has a fairly extensive, though under-appreciated, fossil record [ 42 – 45]. However, the lorica of rotifers is composed of several plates, is generally box- or tube-shaped, ornamentation does not generally include concentric ridges, and the posterior appendage (foot) is typically segmented [ 46].

Although most are slightly smaller, at <500 μm long, Kuqaia shells have morphological similarities to the ephippia (encasings protecting the dormant embryos) of extant cladocerans (Crustacea: Branchiopoda: Cladocera/ Diplostraca ), at 400–2500 μm long ([ 34, 47, 48]; Fig 9 ). Apart from their microscopic size, Kuqaia shares with cladoceran ephippia, a HF-resistant wall, roughly semicircular shell shape and elongate posterior appendages.

In particular, the presence of caudal spines in Kuqaia represents a striking similarity to the ephippia of extant Daphnia . An extant cladoceran specimen, possibly attributable to Leydigia ( Chydoridae ) based on the long setae at the ventral margin [ 49] ( Fig 9 ), produces ephippia [ 34] that are similar to Kuqaia scanicus as evidenced by the presence of the markedly elongate appendages, almost twice the length of the shell body. The presence of peduncles in Kuqaia scanicus is strongly similar to the architecture of extant Daphnia pulicaria ephippia ([ 34]; Fig 9 ). The presence of peduncles also links Kuqaia scanicus to the fossil ephippia of Daphnia ; e.g., it has similarities to the ephippia of Pleistocence D. similis ([ 48]; Fig 9 ), except that K. scanicus bears two longer (with respect to the shell body) peduncles on the lateral part of the postventral end, whereas the two shorter peduncles of D. similis originate from the central part of the postventral end ( Fig 9 ).

Although K. scanicus has similar morphological features to the ephippia of several types of extant and fossil cladocerans ( Fig 9 ), Kuqaia is distinguishable from the majority of extant and fossil ephippia of Daphnia in lacking any swellings or other morphological features that typically demarcate the location of the enclosed single or paired loculi ([ 34, 47, 48, 50 – 54]; Fig 9 ). Anomopod ephippia were described from Lower Cretaceous strata at the Khutel-Khara locality, Mongolia [ 50]. These bear one loculus on the lateral side of the ephippia. Similar ephippia with a single-egg/embryo loculus were recorded in the Lower Cretaceous Jehol Biota, northeastern China [ 51]. Daphnia fossils, including their associated ephippia, have also been documented from Cenozoic deposits in Germany [ 52]. These bear two-egg loculi located obliquely or at acute angles to the dorsal margin. Such features are not apparent on Kuqaia . Other late Cenozoic Daphnia ephippia also bear two-egg loculi [ 53 – 55]. Loculus orientation can be important in distinguishing ephippia of various cladoceran taxa. However, the locule position is not always evident on the exterior of ephippia and, depending on environmental conditions, some extant species of Daphnia produce between 35 and 70% of ephippia lacking an obvious locule [ 56]. The lack of strongly varied shell surface ornamentation in Kuqaia is suggestive of a morphologically simple, archaic group of cladocerans, possibly on the stem group lineage of Daphnia .

Comparisons with pre-Cenozoic forms are hindered by the sparse fossil record of Cladocerans. The oldest putative cladoceran fossils are those recorded from the Devonian Rhynie and Windyfield cherts and an ex situ Carboniferous cobble from Yorkshire, UK [ 57, 58]. However, attribution of the Paleozoic fossils to Cladocera has been questioned [ 59], and no ephippia were identified with these ‘cladocerans’. Sparse examples of this group also derive from Mesozoic strata from various parts of the world, but substantial gaps in the fossil record constrain our understanding of the evolution and diversification of cladocerans through time [ 59]. Jurassic ephippia [ 60] are sufficiently distinctive to be assigned to extant genera, so the origins of modern groups likely extend back at least to the early Mesozoic [ 61].

Shell surface ornamentation is variable (laevigate, granulate, ridged and reticulate) on the ephippia of Daphnia , such that subgenera can be recognized based on fossil ephippial morphology. The shell surfaces of Kuqaia are smooth and ridged based on studies thus far. Extant Daphinia pulicaria produces ephippia with a granulate surface ornamentation ([ 34]; Fig 9 ). Other Mesozoic anomopod ephippia differ from Kuqaia in having tuberculate shell surfaces [ 50]. Ephippia of the late Cenozoic Daphnia pulex group bear reticulate shell surfaces with setae at the ventral margin [ 53].

Intriguingly, molecular dating of the divergence of the Daphnia lineage from other cladocerans is inferred to be c. 200 or � 200 Ma ([ 62, 63]; Fig 9 ). By contrast, the earliest known fossil records of Daphnia are from the Jurassic–Cretaceous boundary (145 Ma, [ 64]; Fig 9 ). Significantly, the first appearance of Kuqaia coincides with the estimated divergence of Daphnia , supporting the hypothesis that Kuqaia may represent a stem group of the Daphnia lineage.

The geological distribution of Kuqaia indicates exclusively continental, freshwater to brackish lagoonal environments in line with extant Cladocera [ 65]. As the global climate during the Early Jurassic was warmer than present, based on fossil records and palaeo-CO 2 reconstructions estimating atmospheric concentrations [ 66], we argue that the resting eggs would have produced during dry-season intervals in middle latitudes, rather than as a result of winter cooling. The dark colour of the studied specimens suggests the presence of protective melanin [ 67], which might indicate that they inhabited clear-water lakes.

Although resistance to strong acids suggests a sporopollenin or chitinous/pseudochitinous composition like most other palynomorphs [ 68], the chemistry of Kuqaia fossils is not known. Similarly, the composition of extant cladoceran ephippia shells has been little studied but is generally assumed to be chitinous with a high proportion of melanin [ 59, 69]. An alternative is that these highly durable resting cases containing eggs or embryos are composed of a scleroprotein similar to the egg-bearing cocoons of leeches [ 70, 71], earthworms [ 72], and the lorica of rotifers [ 73]. Although the morphological similarities with cladocerans ( Diplostraca ), such as Daphnia are strong, future chemical analysis of Kuqaia mesofossils and extant cladocerans is clearly warranted, since this might help better resolve their biological affiliation.

Figures

Fig 9. Kuqaia scanicus sp. nov. and morphologically similar fossils of Daphnia ephippia. The geological ages, the estimated dates of differentiation of the Daphnia lineage, and the age of the oldest fossil record of Daphnia, are plotted. Scale bars = 100 μm. SEM image of Daphnia similis used with permission from [48]; line drawings of Daphnia pulicaria and ‘undefined Chyoridae’ compiled by the authors and interpreted from images in [34]. https://doi.org/10.1371/journal.pone.0282247.g009