Research Article |
Academic editor: Robert Mesibov
© 2019 Pavel Stoev, Leif Moritz, Thomas Wesener.
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Citation:
Stoev P, Moritz L, Wesener T (2019) Dwarfs under dinosaur legs: a new millipede of the order Callipodida (Diplopoda) from Cretaceous amber of Burma. ZooKeys 841: 79-96. https://doi.org/10.3897/zookeys.841.34991
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The entire Mesozoic Era is rather poor in millipede (class Diplopoda) fossils, with less than a dozen species being taxonomically described. Here, we describe the first fossil millipede of the order Callipodida, Burmanopetalum inexpectatum gen. nov. et sp. nov., found in early Cenomanian amber of Burma, 98.79±0.62 Mya. The species possesses a number of morphological traits that exclude it from all extant suborders, and Burmanopetalidea suborder nov. and Burmanopetalidae fam. nov. are here erected to accommodate it. The new suborder can be recognized by the following unique characters: pleurotergal setae absent; telson with a specific spatulate shape twice the size of the penultimate body ring; hypoproct devoid of setae; and eyes composed of five well-separated ommatidia. While the callipodidan habitus seems to have remained generally unchanged for at least 99 million years, pleurotergal and hypoproctal setation, as well as the complexity of eyes in ground-dwelling forms may have evolved recently in the order. As B. inexpectatum gen. nov. et sp. nov. is the first true callipodidan in the fossil record, the minimum age of Callipodida is thus at least 99 Mya.
Burmanopetalidea suborder nov., Burmanopetalidae fam. nov., Burmanopetalum inexpectatum gen. nov. et sp. nov., Cenomanian, Mesozoic.
Millipedes (Diplopoda) are a highly diverse but also a largely understudied group of arthropods with >11,000 described species (
Callipodida is a small order of spinneret-carrying millipedes of the superorder Nematophora (
Callipodida show a disjunct distribution in the Northern Hemisphere, with three major centers of diversification – the North Mediterranean region, Central and South East Asia, and North America. The order is absent from South America, Africa, the Pacific Islands, Australia, and the northern parts of Eurasia (
While the known Paleozoic millipedes significantly differ from extant forms and the Cenozoic fossils can be placed in extant families and genera, the fossil record of millipedes in the entire Mesozoic Era was considered extremely poor (see
Burmese amber from the Hukawng Valley in Kachin State, northern Myanmar (formerly Burma), is precisely dated to the Cretaceous Cenomanian 98.79±0.62 Mya (
The single female specimen (ZFMK-MYR07366) came into our possession from the private collection of Mr Patrick Müller and is deposited in the Zoological Research Museum A. Koenig (ZFMK, Bonn, Germany). The authenticity of the amber was checked under UV light, producing a characteristic pale blue colour when photographed (
Morphological characters were investigated with a Discovery.V12 stereo-microscope (Zeiss) and a BX51 light microscope (Olympus). Photographs were taken with a Canon EOS 7D camera equipped with magnifier lenses.
µCT-Scans were acquired with a SKYSCAN 1272 (Bruker microCT, Kontich, Belgium) at the Zoological Research Museum Alexander Koenig. For the parameters, see the media information in MorphoBank (http://morphobank.org/permalink/?P3360). Thermal-drift correction, ring artefact reduction and digital section reconstruction was done with NRecon 1.7 (Bruker microCT, Kontich, Belgium). Volume rendering and measurements were performed in Drishti version 2.6.3 (
We use ‘body ring’ when pleurotergites and sterna are referred to collectively. Callipodida do not have fused rings as in some other millipede orders (eg. Julida) because the sterna are free.
Body less than 10 mm, composed of 35 body rings (including collum and two apodous body rings) and telson. Eyes composed of five ommatidia situated in two rows (3+2). Body rings cylindrical, with fused tergites and pleurites and free sternites. Pleurotergites composed of smooth prozonites and carinate metazonites, latter being greater in diameter than prozonites. Pleurotergal crests most pronounced from 3rd to 8th pleurotergite. Pleurotergal setae absent; telson spatulate, twice the size of the penultimate body ring; hypoproct tripartite, devoid of setae.
The suborder comprises one family: †Burmanopetalidae fam. nov.
As for the suborder.
†Burmanopetalum gen. nov.
†Burmanopetalum inexpectatum sp. nov.
From “Burma”, the country of origin, and “-petalum” a frequent generic termination in Callipodida. Gender: neuter.
Differs from all extant genera of Callipodida by its minute size (less than 1 cm in length), lack of pleurotergal setae, and its spatulate telson being twice the size of the penultimate body ring. Eyes composed of five ommatidia.
Callipodida, family undetermined:
Holotype (ZFMK-MYR07366), from the collection of Mr Patrick Müller (transferred to ZFMK), adult female, Myanmar, Kachin State, Hukawng Valley, Noije Bum amber mine, 26°15'N, 96°34'E.
As for the suborder, family and genus. Species further characterized by antennomeres III–V strongly conical (infundibular), VI and VII subrectangular; metazonites with 28 more or less well-developed narrow, subparallel crests, well-separated from one another, poriferous crests missing.
"inexpectatum" in Latin means "unexpected" referring to the stunning discovery of just a single specimen among the 529 millipede specimens so far found in Burmese amber. The species epithet is an adjective.
Burmese amber, early Cenomanian, 98.79±0.62 Mya (
Amber : Cut and polished. Piece rectangular, upper surface slightly convex, 14.1 mm × 6.3 mm × 2.5 mm. Colour: light yellow transparent.
Specimen : Close to surface, body coiled in S-shape, vulvae extended.
Syninclusions : Ensifera (Insecta: Orthoptera), Stellate hairs, large grayish spherical structure (Sporangia?).
Body length: 8.2 mm (measured from the CT scan); width of largest body ring 14: 0.4 mm. Body composed of 35 body rings and telson (Figs
Burmanopetalum inexpectatum gen. nov. et sp. nov., female holotype (ZFMK-MYR07366) A habitus B head, anterior-most body rings and vulvae, anterior view C antennae, lateral view D pleurotergal crests ornamentation, lateral view E telson, lateral view F legs, dorsolateral view G apical part of vulva, lateral view H basal part of vulva, lateral view. Abbreviations: I–VII = antennomeres I–VII; br# = body ring number #; ca = mandibular cardo; cl = claw; co = collum; cx = coxa; d = division of paraproct; ep = epiproct; fe = femur; hd = head; hp = hypoproct; il = incisura lateralis; L# = leg number #; lab = labrum; mz = metazonite; om = ommatidia; oz = ozopore; pof = postfemur; pp = paraproct; prf = prefemur; pz = prozonite; sc = sensory cones; sp = spinnerets; st = stria; sti = mandibular stipes; ta I = tarsus I, ta II = tarsus II; ti = tibia; to = Tömösváry organ; tr = trochanter; vu = vulva; * = reddish circles of the basal part of vulvae. Scale bars: 500 µm (A), 100 µm (B–G).
Burmanopetalum inexpectatum gen. nov. et sp. nov., female holotype (ZFMK-MYR07366), volume rendering A habitus B head, collum and pleurotergite 2, lateral view C head, anterior view D Gnathochilarium, ventral view E midbody body ring, dorsoposterior view F telson, and the last 3 pleurotergites, lateral view G same, ventral view. Abbreviation: I–VII = antennomere; br# = body ring number #; ca = mandibular cardo; co = collum; d = division of paraproct; em = eumentum; ep = epiproct; gs = gnathochilarium stipes; gu = gula; hp = hypoproct; lab = labrum; LL = lamella lingualis; L# = leg number #; ms = median suture; mz = metazonite; om = ommatidia; pm = promentum; pp = paraproct; pz = prozonite; sti = mandibular stipes; to = Tömösváry organ. Scale bars: 200 µm (A), 100 µm (B–F).
Head
elliptical, longer than wide, covered by long setae (Figs
Collum
not concealing head from above, nearly as wide as head, anteriorly smooth, only posterior third with poorly developed crests (Figs
Body
cylindrical, with tergites and pleurites fused, sternites free (Fig.
Telson
enlarged, spatulate, 2× the size of the last body ring, dorsal side slightly concave anteriorly (Figs
Legs
Anterior leg of body ring 14 0.35 mm long, legs composed of 8 podomeres, relative lengths coxa = trochanter < tarsus 1 = tarsus 2 < femur < tibia = postfemur = prefemur (Fig.
Male sexual characters unknown.
Female sexual characters
a pair of long, tubular, apically club-like vulvae behind leg 2 (Fig.
Several important characters used in the current systematics of Callipodida are unknown in the described specimen, such as the distribution of coxal vesicles on legs in both sexes, as well as male-specific traits such as the shape of gonopods, the presence/absence of modifications on the head and the anterior part of legs and sternites.
Burmanopetalum inexpectatum gen. nov. et sp. nov. is the first fossil callipodidan which shows the typical body plan of the order. The presence of 35 body rings, free sternites, pleurotergites with subparallel crests, well-separated from one another, a dorsal midline suture, a telson bearing spinnerets, a tripartite hypoproct and a pair of long retractable vulvae, allow the species to be unequivocally assigned to the order Callipodida. Fossil Callipodida could be confused with the nowadays much more common Cambalidea (Spirostreptida), which are known from 20 specimens in Burmese amber (
The absence of pleurotergal and hypoproctal setae and the presence of an enlarged spatulate telson are characters not observed in any of the extant suborders and families (Table
Main differential characters between Burmanopetalidae fam. nov. and the extant families of Callipodida. Hannibaliulus wilsonae Shear, Selden & Gall, 2009 from the Triassic of France is also included in the table, although clear apomorphies of the order are not known.
Burmanopetalidae fam. nov. | Hannibaliulus wilsonae | Sinocallipodidae | Callipodidae | Abacionidae | Caspiopetalidae | Dorypetalidae | Schizopetalidae | Paracortinidae | Tynnomatidae | |
---|---|---|---|---|---|---|---|---|---|---|
Length | 8.2 mm | 53–56 mm | 40–70 mm | 50–70 mm | 19–59 | 28–45 mm | 12–50 mm | 12–100 mm | 32–60 mm | 13–50 mm |
Number of PTs | 35 | 39–43 | 55–72 | 55–65 | 46–61 | 53–66 | 43–54 | 35–56 | 50–85 | 43–88 |
Antennae | Antennal articles III-V strongly conical (infundibular); 6–7th subrectangular | Unknown | antennal articles generally long; in S. thai article VI short and infudibular | Only VIth article infudibular; 7th article conical | Only VIth article infudibular; 7th article conical | V-VIth articles infudibular; 7th article conical | Generally short, article V-VI infundibular (fig. 5 |
Only Vth article infudibular; VIIth article conical | Only Vth article infudibular; VIIth article conical | V-VIth articles infudibular??; VIIth article conical |
Ommatidia | 5, well-separated, arranged in two rows | Numerous (at least 10) arranged in subtriangular patch | 5–11, arranged in 2–3 rows, in oval shape in others;reduced in some cave species | Numerous, arranged in subtriangular patch | Numerous, arranged in subtriangular patch | Numerous, arranged in subtriangular patch | Numerous, arranged in subtriangular patch | Numerous, arranged in subtriangular patch | Numerous, arranged in subtriangular patch | Numerous, arranged in subtriangular patch; reduced in some cave species |
Collum | Smooth, some crests posteriorly | Unknown | Smooth | Smooth | With crests posteriorly | With crests | Smooth or with moderate crests | With crests or smooth | With crests | With crests |
Pleurotergal crests | Moderately to poorly developed; narrow, subparallel. | Metazonites of the pleurotergites smooth, with a distinct transverse depression and ventrolateral rebordered flange | Moderately to poorly developed; narrow, subparallel | Missing, instead of crests there are grooves | Well developed; poriferous crests much larger | Well developed; poriferous crests much larger | Moderately to poorly developed | Moderately developed to lacking | Well developed; poriferous crests much larger | Well-developed, poriferous crests more pronounced |
Position of ozopores | Between crests | Not detected | Between crests | Between grooves? | On well-developed poriferous crests | On well-developed poriferous crests | At base of crests or on elevated swelling in Cyphocallipodinae | At base of crests | On well-developed poriferous crests | On well-developed poriferous crests |
Telson | Enlarged, spatulate, twice the size of the penultimate segment | Enlarged, 1.5 times the size of the penultimate segment in one specimen, posteriorly rounded in both specimens | Normal, approx. the length of penultimate segment | Normal | Normal, approx. the length of penultimate segment | Normal, approx. the length of penultimate segment | Normal, approx. the length of penultimate segment or slightly shorter/ larger | Normal, approx. the length of penultimate segment | Normal, approx. the length of penultimate segment | Normal, approx. the length of penultimate segment |
Coxal pouches present on legs | Unknown | Unknown | 3–11 | 3–21 | 3–13? | 3–15 | 3–13, 3–22 in Cyphocallipodinae | 3–16 | 3–23 | 3–19, 3–23 |
Pleurotergal setae | Absent | Unknown | In anterior position on all pleurotergites | In posterior position on all pleurotergites | In anterior and posterior position | In anterior and posterior position | In anterior and posterior position | In anterior and posterior position | In anterior and posterior position | In anterior and posterior position |
Female second leg-pair | Normal legs, maybe coxa slightly elongated | Unmodified? | Normal legs | Modified | Modified | Usually modified | Normal or modified | Normal legs, except for Euxinopetalum | Modified – two sclerites | Normal or modified |
Period | 99 million years ago | ~242–247.2 million years ago | Extant | Extant | Extant | Extant | Extant | Extant | Extant | Extant |
Extant Callipodida species vary in length from approximately 12 to 100 mm (
Burmanopetalum inexpectatum gen. nov. et sp. nov. is remarkable with a body size in an apparently mature female of just 8.2 mm, which is an extreme case of miniaturization for the order. At the same time the number of body rings is highly reduced. The presence of a pair of long vulvae demonstrates that the specimen is a mature female which most likely reached its last stadium and full body length.
Miniaturisation in fossil Chelicerata has been suggested to be due to the utilization of new ecological niches which larger chelicerates were not able to colonise (
Burmanopetalidae fam. nov. is well characterized by the lack of any pleurotergal setae. Pleurotergal setae are traditionally used as a family- and even subordinal-level character in the classification of Callipodida (
The shape of the telson in Callipodida is subtriangular and rather uniform. In most species it is almost equal in size or smaller to the last body ring. In small species up to 15 mm long, i.e. Dorypetalum, some Tynnomatidae, it is proportionally reduced. In B. inexpectatum gen. nov. et sp. nov., however, the telson is highly enlarged, twice the size of the penultimate body ring and with a spatulate shape. To the best of our knowledge, such a shape is not known in any extant callipodidan. Furthermore, although the hypoproct is subdivided into three plates as in most extant callipodidans, it lacks macrosetae, which are normally present in all extant species in the combination 1+2+1.
The majority of adult callipodidans have eyes composed of at least 30 ommatidia grouped in a subtriangular eye patch (
Callipodida is the rarest among all millipede orders preserved in Burmese amber, with only a single specimen out of 529 specimens hitherto known (
Callipodidans have not previously been recorded from Myanmar (
Burmanopetalum inexpectatum gen. nov. et sp. nov. can be readily distinguished from Hannibaliulus wilsonae
Until now, all myriapods known from Burmese amber have been assigned to Recent families and even genera. The monotypic genus Kachinophilus
With this detailed description of the first fossil Callipodida from the Mesozoic, we lay down the foundation for further research on the classification and phylogeny of the group. Furthermore, the minimum age of order Callipodida is now known to be at least 99 Mya.
We sincerely thank Mr P. Müller, the owner of a large collection of Burmese amber arthropods, who kindly arranged the transfer of the type specimen to the collections of the ZFMK. Our thanks also go to Thorsten Klug (ZFMK) who took numerous photographs of the holotype, and the journal’s referees Sergei Golovatch, Henrik Enghoff, and Robert Mesibov for their valuable comments. The Alexander Koenig Stiftung (AKS) provided the necessary funding to purchase this fossil for the collection of the ZFMK. The study was partially funded by project #KP-06-H21/1-17.12.2018 of the National Science Fund, Ministry of Education and Science of the Republic of Bulgaria to PS, as well as by the German Science Foundation (DFG) grant WE2479/4-1 to TW and Alexander Blanke (University of Cologne).