4.1. Interpretation of the fossil as a tanaidacean

The described fossil has a massively sclerotized exoskeleton, an autapomorphic feature for Arthropoda sensu stricto (= Arthropoda s.l. without Onychophora, lobopodians, Tardigrada and possibly Pentastomida; Maas et al. 2004). The clear morphological distinction between the anteriormost preserved segment and the subsequent segments, is the result of a functional body tagmatisation into a tagma consisting of segments bearing distinct appendages of a very rounded cross section, and a tagma consisting of segments that bear appendages with more flattened cross sections. This is best compatible with the tagmatisation that is apomorphic for Eumalacostraca (Waloszek 1999).

Our morphometric comparison shows that tanaidaceans form a rather discrete cluster within the eumalacostracan morphospace (Fig. 7). The described fossil plots just among the other measured fossil and extant tanaidaceans. Isopodan species occupy a wide space in the overall morphospace, which is to be expected, as they show a great variety of body forms (e.g., Serolidae and Janiridae, Brandt & Poore 2003). The groups Cumacea, Mysida, Mictacea, Stomapoda and Syncarida occupy only a smaller part of the complete morphospace. With only few exceptions, representatives of each of the groups form dense clusters themselves. This may be constrained by functional aspects, for example possibly the ability of the tailfan to perform a powerful escape stroke, which seems to be absent in tanaidaceans and isopodans.

Few species of Isopoda plotted within or near to the tanaidacean cluster, in the case of Acanthastenasellus forficuloides and Corallana societensis. This may be due to the reduced number of pleon segments bearing free tergites (resulting in a shorter pleon). The other isopodans are representatives of the groups Calabozoidea, Tainisopidae and Anthuridae. Calabozoideans can be easily distinguished from the described fossil by the position of the proximal appendage element (coxa) in the last segment of the anterior trunk tagma (pereon). Anthurideans and tainisopids resemble the described fossil by having long pereon segments and distinctly shorter pleon segments (resulting in a shorter pleon). In our analysis, this aspect of similarity is represented by ratios 3 and 4. Species of both groups do not have lateral processes on the last pereon segment and lateral processes of the pleon segments only occur within species of Anthuridea (Wägele 1981, 1989), but not of Tainisopidae (Wilson & Ponder 1992; Wilson 2003).

One fossil tanaidacean, Cretitanais giganteus, does not plot within the cluster of tanaidaceans, most likely because it has an unusually short last pereon segment. This may represent a neotenous feature within the species Cretitanais giganteus. Early manca stages of tanaidaceans have a much shorter last pereon segment than the previous segment, and lack fully developed pereopods on the last pereon segment (Larsen 2003; Boyko & Wolff 2014). Even though the pereopods of pereon segment 6 are well developed, the longitudinal growth of the last pereon segment could just be ontogenetically suppressed or delayed, which would explain the exceptional morphology in Cretitanais giganteus.

Fig. 7.

Principle component analysis of different ratios measured on fossil and extant malacostracan crustaceans. The correlation between variables and the principle components 1 and 2 (x- and y-axis) is depicted by light grey arrows, the corresponding numbers refer to the variables (ratios 1 to 6). A: Analysis without logarithmized variables, B: analysis with logarithmized variables.

Some qualitative morphological features of the new fossil further support an interpretation as a tanaidacean. Typical features of tanaidaceans, or tanaidacean ingroups, are: 1) (weakly developed) hyposphaenia on the pleon segments; 2) pronounced lateral processes of pleon tergites (tergopleura); 3) posterolateral position of the coxa on the last pereon segment; 4) transverse rows of setae on the pleon tergites (preserved as punctures in the exoskeleton).

The setal rows present in the described fossil also occur within some extant tanaidomorphan tanaidaceans (e.g., Tanais dulongii; SARS 1899), but also in non-tanaidomorphan tanaidaceans, e.g., Saltipedis floccus (Guţu 1996; Błażewicz-Paszkowycz & Bamber 2007). Pore-like punctures like in the described fossil have also been recorded for the fossil tanaidacean Cretitanais giganteus, but there the punctures are on the pereon segments rather than on the pleon segments (Malzahn 1979).

4.2. Ontogenetic stage

The anteriormost preserved segment in the fossil is interpreted as the last pereon segment (post ocular segment 13). This can be inferred from the morphology of the further posterior segment (typical pleon morphology, not considerably differing from subsequent segments). That the fossil represents a manca stage can be ruled out, because manca stages in tanaidaceans do not have fully developed appendages on the last pereon segment and (at least not in early mancas) the whole segment is shorter than the anterior subsequent (pereon) segments that bear fully developed legs (Larsen 2003; Boyko & Wolff 2014). Consequently, the fossil can only be the remain of a late juvenile (last pereopod with fully developed coxa) or of an adult animal.

4.3. Sex

As in other malacostracans, tanaidacean male gonopores are located medially on the ventral side of the post-ocular segment 13 (thorax segment 8; last pereon segment in tanaidaceans), whereas female gonopores are located at post-ocular segment 11 (thorax segment 6; pereon segment 4 in tanaidaceans). The male gonopores can be closely paired (neotanaidomorphans and most of tanaidomorphans) or conjoined to a single pore (apseudomorphans) (Larsen et al. 2015). In most (or all) tanaidacean species, these male gonopores are somewhat elevated from the sternite surface. Hence, they are often referred to as genital cones (cf. “Monokonophora” & “Dikonophora”, non-monophyletic groups based on gonopore morphology). The area in which the gonopore/-s should be is perfectly preserved in the described fossil, yet there is no sign of genital openings. This leads to the conclusion that the described specimen was most likely a female.

4.4. Systematic challenges within Tanaidacea

As previously stated by Sieg (1983) and Schram (1986), “Anthracocaridomorpha” Sieg, 1980 is only based on plesiomorphic character states. As a result Anthracocaridomorpha is likely to be a non-monophyletic group. According to the most recent literature, “Anthracocaridomorpha” comprises two ingroups: Anthracocarididae Brooks, 1962 and Niveotanaidae Polz, 2005 (summarized in Schram et al. 1986; Schram 1989; Polz 2005; Anderson 2017). The latter ingroup, Niveotanaidae, is monotypic and monospecific, comprising only the species brunnensis Polz, 2005. Anthracocarididae comprises two species, scotica Peach, 1882 and rhenanus Malzahn, 1957 and might represent a natural group, although this is only supported by the presence of a uniramous uropod.

Formerly, another “group” called Cryptocarididae Sieg, 1980 was attributed to “Anthracocaridomorpha” (Schram et al. 1986; Schram 1989). However, Cryptocarididae is monospecific with Eucryptocaris asherorum Schram, 1974 (until 1989 referred to as Cryptocaris hootchi) as the only species. With flat, bipartite, biramous uropods (Schram et al. 1986; Schram 1989) the species asherorum has a plesiomorphic combination of uropod characters for tanaidaceans (as this combination is also a plesiomorphy in the ground pattern of Peracarida). All species of Anthracocarididae together with the species brunnensis Polz, 2005 already have cylindrical uropods as in extant forms. Only species of Anthracocarididae and some (but not all) extant tanaidaceans have uropods consisting of multiple elements (Larsen et al. 2015). The stem species (“last common ancestor”) of all extant tanaidaceans can be reconstructed as possessing a pleotelson (at least the sixth pleon segment, post-ocular segment 19, is conjoined with the telson), a character absent in Anthracocarididae and in the species brunnensis Polz, 2005.

In contrast to Tanaidomorpha (and Neotanaidae, which may be a tanaidomorphan ingroup) Apseudomorpha is characterized by many plesiomorphic character states (Sieg 1983; Larsen et al. 2015). One phylogenetic study based on morphological characters even pointed out that Apseudomorpha is likely not monophyletic (Siewing 1953). It is therefore not surprising that molecular phylogenetic studies (Drumm 2010; Kakui et al. 2011) do not show Apseudomorpha as a monophyletic group.

Schram (1986) proposed the groups Jurapseudidae Schram, 1986 and Jurapseudoidea Schram, 1986. Jurapseudoidea Schram, 1986 is monotypic (= unnecessary in a rankless systematic framework). Jurapseudidae sensu Schram (1986) comprises three species (friedericianus Malzahn, 1965, acutirostris Sachariewa-Kowatschewa & Bachmayer, 1965 and emersoni Schram, 1986). The diagnosis of Jurapseudidae (“Body slightly dorsoventrally flattened. Males dikonophoric, with strong chelipedes”, Schram 1986: 134) is problematic since all of the character states in it are also found in extant tanaidaceans, and the combination of the character states is not unique for the three species included in the group.

The species friedericianus and acutirostris were put in the (genus-ranked) group Jurapseudes Schram, 1986 (Schram et al. 1986). The diagnosis for Jurapseudes (Schram et al. 1986: 134) only contains characters that are not visible in the holotype of acutirostris (Malzahn in Bachmayer et al. 1965, pl. 5, fig. 3; pl. 6), which is also the only specimen known from this species. The closer relationship between friedericianus and acutirostris is solely explained by the (not further explained) similarity in the anterior region of the body (Schram et al. 1986: 137). It is thus highly questionable whether Jurapseudidae and Jurapseudes represent natural groups.

The remaining Jurassic tanaidacean species have been placed in monotypic (genus-ranked) groups and can simply be referred to by their species names (without generic name) when discussing the possible affinity to the already described species (e.g., Lanham 1965). All other non-monotypic tanaidacean groups that are only known from fossils are representatives of Tanaidomorpha (Vonk & Schram 2007; Sánchez-García et al. 2015, 2016, 2017; Heard et al. 2018).

Apart from fossil tanaidaceans that were described as species or attributed to an already described species, there are also fossil occurrences of tanaidaceans without species attribution. There are two Triassic records from the Veszprém region in Hungary. One of the occurrences is purely based on fragmentary remains (chelae). Thus, the attribution to Tanaidacea is problematic and has also been discussed as such in the original publication (Végh & Bachmayer in Bachmayer et al. 1965). The other occurrence (Hannibal 2003) is also problematic since the only reference is a conference abstract and no photograph or drawing is available to the time of this study. Further, Hannibal (2003) attributed his findings to Neotanaidae based on characters of the pleon segments. However, no further explanation is given in this regard and the pleon segments of many neotanaids resemble those of apseudomorphans or (other) tanaidomorphans. Judging from illustrations in the literature, we found no features in the pleon segments (apart from microstructures) that could be diagnostic for neotanaids.

There are also tanaidaceans from the Lower Cretaceous of Mexico that have not been formally described yet, but have been reported to occur in a very high abundance (Vega et al. 2003, 2006a, 2006b). Vega et al. (2006b) tentatively suggested an affinity to the group Ophthalmapseudes. Since Ophthalmapseudes is currently monospecific, this interpretation could be understood as an affinity to rhenanus Malzahn, 1957.

4.5. Systematic position of the fossil within Tanaidacea

The fifth pleon segment is the posteriormost preserved element of the herein described fossil. Consequently, we lack information about the uropod morphology and the formation of a pleotelson (whether the sixth pleon segment is conjoined with the telson or not). All modern tanaidaceans have a pleotelson. Consequently, their stem species (“ancestor”) can also be reconstructed as possessing a pleotelson. Due to the preservation of the here presented fossil, we can draw no conclusion whether the fossil is part of the natural group that derived from the stem species of all modern tanaidaceans. This means that a more basal position in the tanaidacean tree is possible (“Anthracocaridomorpha”).

Fig. 8.

A: Phylogenetic interpretation of GPIT/NC/07/B/34 based on morphological features (green, possible position within the tree); natural groups in fat letters. Arrows depict the occurrence of derived features. Topology based on Kakui et al. (2011) (plus independent evaluation of fossil morphology) and nomenclature from Anderson (2017); B: Reconstruction of GPIT/NC/07/B/34. Colouration: red, preserved body region; grey, not preserved in the studied specimen.

The laterally protruding tergopleura of the pleon in combination with the (although weakly developed) anterolateral processes on the last pereon segment are only seen in extant apseudomorphans, but never in neotanaids or (other) tanaidomorphans. Representatives of both latter groups have a rather smooth body surface and lack anterolateral processes on the tergites of the pereon. A possible explanation for reduction of this kind of body armature in tanaidomorphans is that they inhabit self-constructed tubes (Błażewicz-Paszkowycz et al. 2012).

As mentioned above, transverse rows of setae on the pleon tergites occur in both Apseudomorpha and Tanaidomorpha (including Neotanaidae). Dense transverse rows on the first pleon segment are characteristic for the apseudomorphan group Parapseudini Guţu, 1981 (= Parapseudinae). Pseudohalmyrapseudes Larsen & Hansknecht, 2004 and Halmyrapseudes Bacescu & Guţu, 1974 are ingroups of Parapseudini and are both characterised by additional rows of setae on the remainder pleon tergites (Guţu 2008). Some neotanaid species (e.g., Carololangia mirabunda Gardiner, 1975) have rows of setae on the pleon tergites. In Neotanais pfaffi, just like in the described fossil, rows of setae on the dorsal side of well-developed tergopleura are present.

Consequently, we find setal rows on the dorsal surface of the pleon to be a problematic character for systematic research on higher groups of tanaidaceans. There is also no clear character for identifying a “row” in this aspect. For example, other non-Parapseudini apseudomorphans have setae on the pleon tergites that are somewhat arranged in rows, with three setae in each “row” (e.g., Apseudes quasimodo Błażewicz-Paszkowycz & Bamber, 2012). Species descriptions often lack drawings or photographs of tergite structures, making it even more difficult to trace these characters in the literature (see Hyžný & Klompmaker 2015 for a discussion). Further, the disposal of setae in rows could be constrained by the position of nerves beneath the tergites.

The described fossil cannot easily be identified as a representative of a specific monophyletic ingroup of Tanaidacea. However, there are morphological features in the new fossil (anterolateral processes of posterior pereon segments) that allow to exclude some tanaidacean ingroups from the phylogenetic interpretation. This results in a “non-monophyletic” expression of the potential phylogenetic position (Fig. 8). Our phylogenetic interpretation of the here described specimen is:

Tanaidacea nec Tanaidomorpha & Neotanaidae

This expression neglects the presence of monotypic group names such as Neotanaidomorpha or Neotanaoidea. If these groups should become non-monotypic, this expression might have to be modified. Depending on the phylogenetic hypothesis this expression also contains redundant information (Neotanaidae as an ingroup of Tanaidomorpha).

4.6. Species delimitation

With respect to the assumed impermanence of biological species over time, we focus on the Jurassic species for comparison:

Species quenstedti Reiff, 1936: Palaeotanais quenstedti Reiff, 1936 is the only published fossil tanaidacean in close geographical proximity to the here described fossil (Fig. 1B). Being Early Jurassic in age there is a temporal distance of more than 25 million years between the herein described fossil and the holotype of quenstedti Reiff, 1936. The specimen described herein and the holotype of quenstedti Reiff are about equal in size (no scale-bars or well-defined measurements in the figures of Reiff 1936). The type material of quenstedti Reiff is said to be lost (Schram et al. 1986). This statement was erroneous (G. Schweigert, pers. observation 07.03.2019), however, the preservation of the specimen and the patterns of destruction due to pyrite decay as described by Reiff (1936) and Etter (2004) does not allow further analysis.

Species brunnensis Polz 2005: There is a 10 million years minimal temporal distance between the examined fossil and the type specimens of Niveotanais brunnensis Polz, 2005. Another specimen assigned to brunnesis comes from the Middle Jurassic Monte Fallano Formation in Italy, but its preservation (completely compressed) makes comparative studies very difficult. If the Middle Jurassic specimen from Monte Fallano (Jones et al. 2014) is indeed a representative of brunnensis, then there is a minimal time distance of 2.1 million years (Fig. 9). The only morphological difference between the herein described fossil and the brunnensis specimens is the size. The brunnensis type specimens are slightly smaller (2.22 mm vs. 2.63 mm), whereas the Monte Fallano specimen is much smaller (0.83 mm vs. 2.63 mm), when compared to fossil described in this study, in terms of the preserved body region. Although some of the type specimens of brunnensis are quite complete, the mode of preservation does not allow for comparison at a very detailed level. For example, punctures in the exoskeleton caused by the former presence of setae cannot be expected to be preserved and visible in the type material of brunnensis, due to the calcification of the fossils. Also, only the rough three-dimensional shape of structures can be compared as the brunnensis types are moderately compressed. There could be morphological differences between the here described fossil and brunnensis that are just not evident from the described material.

Species gracilis Heer, 1865: When compared to the type specimen of Opsipedon gracilis Heer, 1865, there is an 8.2 million years minimal temporal distance to the herein described fossil (Fig. 9). Morphological differences include: 1) lateral spines on last pereon segment projecting anterolaterally in gracilis; 2) distinct furrows on the lateral processes of the pleon tergites of gracilis that are not present on the new fossil; 3) the fifth pleon segment that is distinctly longer than the anterior ones in gracilis, while in the described fossil the fifth pleon segment is subequal in size to the anterior ones. Curiously, the tergopleura of gracilis reminded Friedrich V. Huene (famous vertebrate palaeontologist from Tübingen) of lateral processes of vertebrae. This led to the erroneous description of the “urodelan” Boomgaardia salamandriformis, later recognized as a specimen of gracilis (Schweigert & Etter 2008).

Fig. 9.

Temporal occurrences of Middle and Late Jurassic tanaidaceans based on literature information. The depicted time-spans (horizontal red and green lines) do not refer to the longevity of the species but to the temporal uncertainty of each occurrence. Different occurrences of the same species are depicted separately. The question mark accentuates an undefined geological timespan (in this case: “Lower Dogger”). Abbreviations: Bajo, Bajocian; Bath, Bathonian; Callov, Callovian.

Species acutirostris Sachariewa-Kowatschewa & Bachmayer, 1965: When compared to Jurapseudes acutirostris Sachariewa-Kowatschewa & Bachmayer, 1965, there is no minimal temporal distance to the described fossil, as the geological reference of the types of acutirostris is very unprecise (Fig. 9). The holotype of acutirostris (which is also the only fossil ascribed to this species) suggests that acutirostris was much larger than the animal that produced the herein described fossil remain. Although there is no overlap regarding the preserved body regions for the two fossils this can be roughly reconstructed. The cephalothoracic region in acutirostris is 6 mm long, whereas the herein described fossil has a total length of only 2.6 mm. As the cephalothoracic region in tanaidaceans is (usually?) no longer than the combined lengths of the pleon and last pereon segment, we can estimate that acutirostris was by far larger than the fossil described in this study. However, the reasons for the size difference could also be attributed to ontogeny or sexual dimorphism/polymorphism (e.g., Sieg 1983: 151, fig. 7C). Other morphological comparisons are not possible because only the anterior part of the acutirostris body is preserved in the holotype, meaning that there is no overlap with the described fossil.

Species friedericianus Malzahn, 1965: Between the type specimens of Jurapseudes friedericianus and the examined fossil the minimal temporal distance is of 8.2 million years, but again, if other occurrences are included the minimal temporal distance is eliminated (Fig. 9). The holotype of friedericianus Malzahn, 1965 is an arbitrary composite of three isolated remains of tanaidaceans from the same geological context. According to Malzahn (1965), the size of these pieces together is 1.2 mm (anterior rim of head to telson). Just as the specimen described in this study, some type specimens of friedericianus also show rows of indents (setae insertion points) on the tergopleura of the pleon segments. Differences in morphologies between friedericianus Malzahn, 1965 and the examined fossil include: 1) the shape of the anterolateral processes on the last pereon segment, which are distinctly spine shaped in friedericianus but rather blunt in the described fossil; 2) the hyposphaenia in friedericianus are more distinctly developed than in the herein examined fossil. The relative length of the pleon segments compared to the pereon segments in friedericianus is given as one third of the length of the pereon segment. However, there are depicted type specimens (Malzahn in Bachmayer et al. 1965) that are clearly in conflict to this description (Malzahn in Bachmayer et al. 1965, pl. 2, fig. 6). Overall, some pleon-region type specimens differ distinctly from the corresponding holotype fragments (cf. Malzahn in Bachmayer et al. 1965, pl. 1, fig. 3; pl. 2, fig. 6). Considering the amount and stratigraphical distribution of non-type specimens (7.6 million year minimal time range for the species) and the discussion above, the validity of friedericianus Malzahn, 1965 as a natural species is questionable.

All Middle Jurassic species come from Central or Southeastern Europe (Fig. 1). Thus, (palaeo-)geographical aspects cannot be used to support species delimitation. Due to the different preservation of comparable fossils and potential sexual dimorphism, a conspecificity with one (or more) described Middle Jurassic species (acutirostris, friedericianus, brunnensis, and gracilis) cannot be excluded. It is not unlikely that the fossil belongs to a new species that has not yet been described. However, we refrain from formally describing a new species based on the new specimen. This is especially with respect to the fragmentary preservation of the specimen, which would result in a holotype that is difficult to compare to future findings.

Due to the morphological similarity to some published specimens of friedericianus Malzahn, 1965 (Malzahn in Bachmayer et al. 1965, table 2, fig. 6; Malzahn 1970, table 1, fig. 4) the specimen is suggested to be referred to as:

4.7. Taphonomy

The type of preservation seen in the described fossil seems to be rather common for three-dimensionally preserved specimens that were retrieved by sieving. This type of preservation (connected pleon segments with or without some thoracic segments and pleotelson attached) is found in many fossil tanaidaceans (Bachmayer et al. 1965, pl. 1, fig. 3; pl. 2, figs. 6, 7; Glaessner & Malzahn 1962, pl. 2, figs. 6–13; pl. 3, figs. 1, 2, 5, 6, 10, 11; pl. 4, figs. 2, 3; Malzahn 1970, pl. 1, figs. 2, 4; Malzahn 1979, pl. 1, figs. 6–9; Schram et al. 1986, figs. 7B, 8C, D, 10C, D). This is most likely not only a result of the preservation potential of this specific body area, but also the result of the mechanical and chemical stress during the sieving process.

As all known tanaidaceans share a benthic lifestyle and many species live infaunal, they inhabit an environment that is prone to bioturbation or they contribute to bioturbation themselves. Bioturbation is one of the main driving forces that prevent fossilization by oxygenating deeper layers of sediments. Etter (2004) suggested a stable dysoxic (low-oxgen level), but not anoxic environment for the preservation of three-dimensionally preserved tanaidaceans, as higher oxygen levels favour bioturbation. Permanently or temporary lower (anoxic) conditions would not allow for tanaidaceans to live in a benthic environment. The upper part of the Ornatenton Formation, where the here presented fossil was found, is characterised by bioturbated mudstones with a relatively low diversity of benthic life (mainly nuculid bivalves and solitary corals; G. Schweigert, pers. comm.). With respect to lithology and paleoecology, the presence of tanaidaceans within the Ornatenton Formation fits well into model predicted by Etter (2004), that the preservation of tanaidaceans as fossils is dependent on dysoxic benthic oxygen levels.

All fossil tanaidomorphan species (according to Guţu 2004, Cretitanais giganteus is not a tanaidomorph) have been found in amber. Yet, only one apseudomorphan species has been recorded from amber deposits. This record differs from the known fossil apeudomorphans as it is less than one millimetre in total length and probably represents non-adult animal (Heard et al. 2018). There may be multiple reasons for this systematic-taphonomic distribution of tanaidaceans in the fossil record. Most geologically younger Lagerstätten yielding tanaidaceans are amber deposits. This is surely not linked to the geological age only, as for example, the youngest fossil occurrence of tanaidaceans is an apseudomorphan from a non-amber Lagerstätte (Quayle 2016). Also, taphonomical aspects could have triggered this distribution.