Org Divers Evol (2013) 13:425–432 DOI 10.1007/s13127-013-0129-3

ORIGINAL ARTICLE

A nymph in Baltic amber and a new approach to document amber fossils

Joachim T. Haug & Carsten H. G. Müller & Andy Sombke

Received: 17 August 2012 /Accepted: 4 February 2013 /Published online: 28 February 2013 # Gesellschaft für Biologische Systematik 2013

Abstract The fossil record and especially examples of fos- Introduction silized ontogeny have been described for many major arthro- pod taxa. However, little is yet known about ontogeny in fossil Palaeo-evo-devo is an approach that combines evolutionary representatives of . Traditionally, has morphology, developmental biology and paleontological evi- focused on adult stages, and tends to “overlook” non-adults. dence. A pre-requirement for such an ambitious approach is the Assigning an early stage to a specific species would demand preservation of “fossilized ontogenies”, which have been de- having “bridging” juvenile stages. Additionally, as shown for scribed for many major groups, e.g., vertebrates (e.g., other fossil , juvenile stages of a given species Schoch and Fröbisch 2006; Horner and Goodwin 2009; could have been recognized as separate species in the past. Sánchez-Villagra 2010), echinoderms (e.g., Sevastopulo In this context, palaeo-evo-devo links evolutionary develop- 2005;SumrallandWray2007;Sumrall2008), molluscs (e.g., mental knowledge with paleontological evidence. We report a Malchus 2000;Klug2001; Nützel et al. 2007),andalsofor nymphal lithobiomorph centipede from Baltic amber. The arthropods. Among fossil arthropods, ontogeny is especially specimen was documented under cross-polarized light com- well known for the exclusively fossil trilobites (e.g., Hughes et bined with image stacking. Stereo images were created based al. 2006) or early representatives of Crustacea sensu lato on these image stacks. Assessable characters are described (“stem-mandibulates”; Stein et al. 2008,Haugetal.2009a, and compared with data on extant lithobiomorph taxa. We 2010a, b). Also the four major extant groups have conclude that the nymph (or larva) described here can be known representatives of which the ontogeny has been at assigned to and probably represents the fourth least partly reconstructed. While there are numerous ac- post-embryonic stadium. Findings such as that described here counts for various representatives of Eucrustacea (e.g., are still rare and detailed descriptions are not usually provided. Walossek 1993; Zhang et al. 2010;Haugetal.2011)and The accessible data therefore represent an important example Hexapoda (e.g., Kukalová-Peck 1997; Wichard et al. 2009), of fossilized ontogeny for . as well as some examples of Chelicerata (Cuggy 1994; Dunlop 2002; Haug et al. 2012a), there is very little Keywords Chilopoda . Baltic amber . Nymphal stadium . developmental information for fossil Myriapoda. Palaeo-evo-devo . 3D-Imaging The fossil record of Myriapoda was summarized recently by Shear and Edgecombe (2010). Fossil diplopods are often in- complete as they are, for example, often found without the head. Furthermore, the calcified dorsal parts are often much J. T. Haug (*) : C. H. G. Müller : A. Sombke better preserved than other structures. The symphylan fossil Ernst-Moritz-Arndt-University of Greifswald, Zoological Institute record is restricted to two occurrences in Baltic and and Museum, Cytology and Evolutionary Biology, Dominican amber (Poinar and Edwards 1995; Scheller and Soldmannstrasse 23, 17487 Greifswald, Germany Wunderlich 2004). The interesting point about the piece from e-mail: [email protected] Dominican amber is that it contains two specimens that 426 J.T. Haug et al. represent different ontogenetic stages (Poinar and Edwards focus than any of the single frames. Additionally, a virtual 1995). Fossil are known from only a single piece surface based on the unsharpness of the images was calcu- of Baltic amber (Scheller and Wunderlich 2001). lated. Although this method may produce certain artifacts Chilopoda or centipedes are known from the due to the transparency of the amber, it provides additional onwards (Edgecombe 2011). They occur regularly in excep- topological information of the specimen. This 3D informa- tional preservation types such as amber and thus should also tion is provided as stereo images. Stacks containing stereo be represented therein by their earlier ontogenetic stages. images with significant artifacts are not provided as stereo Among chilopods, Scutigeromorpha, Lithobiomorpha, and images. Craterostigmomorpha hatch with fewer segments than in the Measurements were obtained from the images and adult (e.g., Manton 1965; Lewis 1981; Minelli and Sombke rounded to the next 5 μm. Descriptive terminology fol- 2011). Such larval, nymphal, or anamorphic stages should, lows, as far as possible, that of Bonato et al. (2010). To therefore, be identified easily. Also, the number of antennal make it also comparable in larger scale approaches, terms articles increases with age. For instance, earlier stages pos- derived from homology assumptions that deviate too far sess significantly shorter antennae with few articles—anoth- from standard terminology are given in squared brackets. er feature that may be used for identification without any difficulty. Representatives of Epimorpha, comprising Scolopendromorpha and Geophilomorpha, hatch with the Results full number of segments. Yet also here, subadult stages can be recognized, e.g., based on the antennal morphology. General morphology Body with two tagmata, head and Edgecombe et al. (2009), for example, reported a subadult trunk. Total body length 2.3 mm (Fig. 1a,b). geophilomorph from French amber. We report here a nymphal lithobiomorph from Baltic Head Dorso-ventrally flattened, broader (410 μm) than amber. Such findings are still rare and a detailed descrip- long (365 μm), broader than tergites 1–5 (other tergite width tion cannot usually be provided. Our data therefore repre- unclear). Head shield covered sparsely with trichomes or sent an important example of fossilized ontogeny for setae (Fig. 1a–d). Transversal suture running towards the centipedes. base of antennae (Fig. 1c,d). Clypeus and labrum not accessible.

Materials and methods Sensory organs [antennula] relatively stout, length about 500 μm, 55 μm in diameter, 14 articles A single specimen preserved in Baltic amber was investi- (Fig. 1g,h). Antennal [antennular] articles 1–13 about two gated. Baltic amber is considered to be of age, times as broad (diameter) as long. Terminal article (14) dating back to about 44 million years ago. Additional infor- four to five times as long as the preceding ones; about mation on the specimen is not available. The specimen is 2.5 times as long as broad (diameter). Antennal [anten- part of the collection of the Field Museum Chicago (FMNH) nular] articles armed with fine setae (probably trichoid and is registered under the collection number PE 61071. It sensilla), one antenna containing about 200 such struc- was documented on a Leica DM 2500P (Leica, Wetzlar, tures. Seta length about 30 μm. Five to six lateral ocelli Germany) with a ScopeTek DCM 510 ocular camera [ommatidia] on left body side (Fig. 1i,j). Tömösváry (ScopeTec, http://www.scopetek.com). To reduce optical organ not observed. deformations of the oblique surfaces of the amber piece, a drop of glycerol was placed onto the region of interest and Mouth parts Mandible and first maxilla not accessible. covered with a cover slip. This produced a flat plane surface. Telopodite of second maxilla [endopod?] visible. Three For lighting, external fiber light sources were used. Light articles plus terminal claw (Fig. 1e–h). Article 1: 40 μmin was distributed evenly from a low angle. Fiber lights were diameter, length not accessible. Article 2: 30 μm in diame- equipped with polarization filters that were cross-polarized ter, 45 μm maximal length (outer edge). Article 3: 30 μmin to a polarizer in the microscope; this set up reduces reflec- diameter, 50 μm maximal length (outer edge). Structure of tions. Objectives used were 4x and 10x, resulting approxi- terminal claw not accessible. mately in 40x and 100x magnifications. Due to the limited depth of field, stacks were recorded, i.e., Maxilliped Maxilliped [trunk appendage 1] with proximal several images (frames) of the same image detail in different and distal part. Coxosternite of both maxillipeds continuous, focal planes. Focal planes were shifted manually in 20 or 5 trapezoidal to triangular in shape, possibly with straight microns (depending on magnification). Stacks were fused in lateral margins, 155 μm in anterior-posterior dimension, Image Analyzer. Fused images have more structures in width at least 250 μm but difficult to measure due to Fossil centipede nymph and a new way of documenting amber fossils 427

Fig. 1 a–j FMNH PE 61071. A lithobiid centipede nymph. a green/light green distal part of the maxilliped. Adjacent articles are Overview of the left body side. Note the different external markers of colored differently to emphasize the subdivision. g Almost ventral trunk segments (ts); some have long tergites and can be recognized view of the head and anterior trunk. h Color-marked version of g. through these, others have short tergites (arrows) and can be recog- Blue/purple antenna, red/orange distal part of maxilla two, green/light nized mainly by the appendages, e.g., the maxilliped (mxp). Posterior green maxilliped. Adjacent articles are colored differently to em- short tergites can only be assumed (arrows with question marks). b phasize the subdivision. i Lateral view of the head shield. j Stereo-anaglyph image of a; please use red-cyan stereo glasses. c Color-marked version of i. The five possible lateral ocelli are Dorso-posterior view showing the head shield. d Stereo-anaglyph highlighted. All images recorded as stacks under cross-polarized, image of c. e Latero-ventral view of the head and the anterior trunk. f homogeneous light, processing of stacks with Image Analyzer Color-marked version of e. Red/orange distal part of maxilla two, perspective distortion. Dentition on anterior margin with twice as long (125 μm maximal length, outer edge) as broad two teeth on each side. Anterior margin with V-shaped (diameter). Femur: as a complete ring, about 20 μmin median notch between the two teeth pairs (Fig. 1g,h). length, 45 μm broad. Tibia: as a complete ring, about Telopodite [endopod?] covered with few setae. Composed 25 μm in length, 45 μm broad. Tarsungulum: tapering of four articles (Fig. 1e–h). Trochanteropraefemur: about distally, curved inwards, about 95 μm in length. 428 J.T. Haug et al.

Trunk 11 visible segments, indicating 13 trunk segments compared to a non-embedded specimen. The possibility to (see below) plus possible posterior growth zone, probably also produce anaglyph stereo images gives additional oppor- including the anal somite [telson?]. Trunk segments dorsally tunities to understand the topology of the specimen; unfortu- forming tergites (Fig. 1a–d). Trunk segment 1 is the nately, with higher magnifications there appears to be an maxillipedal segment. Traditional counting starts with the accumulation of artifacts. first walking appendage, thus trunk segment 2. Its tergite Still, the combination of polarized light with image stacking is, therefore, considered to be the first tergite (T1). Tergites provides an easy-to-apply method that can be used for a large differentiated as long and short tergites. Long tergites on sample size without the need for expensive or cumbersome trunk segments 2 (T1), 4 (T3), 6 (T5), 8 (T7), 9 (T8), 11 equipment. (T10), 13 (T12). Tergite of maxillipedal segment [first trunk segment] short (25 μm) but distinct (Fig. 1a;leftmostarrow). Identity of the specimen Shorttergitesontrunksegments3(T2),5(T4),7(T6) (Fig. 1a;markedbyarrows). Presence of short tergites of The specimen described here is identified as a lithobiomorph trunk segments 10 (T9) and 12 (T11) assumed, as they are centipede based on, e.g., the morphology of the poison claws typical for lithobiomorphs. Length of tergite 2 (T1) 255 μm. (maxillipeds). Other fossil lithobiomorphs are well known Length of tergite 3 (T2) 55 μm. Length of tergite 4 (T3) ca. from Cenozoic ambers (e.g., Weitschat and Wichard 1998); 285 μm. Length of tergite 5 (T4) not measurable. Length of they are not especially rare but can also not be considered as tergite 6 (T5) ca. 350 μm. Length of tergite 7 (T6) not common. Few lithobiomorph species have been formally measurable. Length of tergite 8 (T7) ca. 310 μm. Length of described; consequently there are several ‘nomina nuda’ tergite 9 (T8) ca. 250 μm. Length of tergite 11 (T10) ca. (Edgecombe 2011). Edgecombe (2011) pointed out, that none 170 μm. Length of tergite 13 (T12) ca. 155 μm. Length of of this material has been examined in modern times and the posterior growth zone ca. 70 μm. Six, possibly seven walking detailed affinities of these species are unknown. While adult legs visible on left side (Fig. 1a,b). All legs appear to be of lithobiomorphs have at least been depicted repeatedly, similar length. Limb buds of the posterior segments, which nymphal stages have not been formally described. A should be present, cannot be accessed. lithobiomorph nymph bearing ten leg pairs was depicted by Kobbert (2005), but with no further descriptions. The low number of trunk segments, as well as the short Discussion antennae with few articles identifies this specimen as a nymphal or larval stage. The outer morphology of nymphal Methodology and preservation stages of various extant representatives of Chilopoda has been described by numerous historic and recent taxonomists, Although the specimen lies in a suboptimal position within especially for Lithobiomorpha (e.g., Andersson 1981, the amber, close to a breakage (as seen in Fig. 1c,d lower Voigtländer 2007). The terminology of nymphal stadia of left), it is well preserved and gives access to quite some extant Lithobiomorpha has been described variously by dif- detail. Especially the ventral side of the head and anterior ferent authors. The first stage after hatching was termed either trunk region is often not accessible on fossil arthropods in fetus (Verhoeff 1905), L 0 (Andersson 1979), PL1 (Andersson amber as they tend to be hidden in white milky areas 1981) or stadium I (e.g., Scheffel 1969; Voigtländer 2007). We (in German “verlumt”). Here, the maxilliped as well as the follow the terminology by Scheffel as it appears the most maxilla can be accessed. Also the preservation of the anten- consistent for the moment. The terminological issues among na with its setae is exceptional. Yet, many other important subadult stages of arthropods need to be addressed in more details cannot be accessed, for example potentially present detail in the future, but cannot be presented at length here. coxal pores, details of the appendages, or the sternites. This In investigated extant Lithobiomorpha, a number of eight is of course due to the small size of the specimen as well as fully developed leg pairs is typical for stadium (S) I to III, at its unfortunate position within the amber piece. Already the least for Lithobiidae. In addition to these 8 legs, 2 limb buds details of the head were difficult to obtain. Image stacking is are visible (Andersson 1979). In SII, half developed legs usually difficult with stacks obtained from amber (personal sometimes occur. Deviations occur in representatives of observation). Other methods for transparent matrices (e.g., Henicopidae, for example, in SII of Lamyctes fulvicornis, Haug et al. 2009b) do not work properly with amber fossils 7 fully developed, 1 half-developed, and 2 small limb buds due to their low transparency (personal observation). are visible. In Cermatobius (=Esastigmatobius) longitarsis, The application of polarized light has a very positive effect the number of fully developed legs and limb buds stays on the reflections, and the fusion algorithms of Image constant (8+2) from SI to SIII. In SIV, the number of legs Analyzer can then produce a satisfying image, although one is consistently 10 (+2 limb buds) in all species investigated has to say that the sharpness of the image is still inferior by Andersson (1979). For forficatus, Scheffel Fossil centipede nymph and a new way of documenting amber fossils 429

(1969) showed that SIII exhibits 8 fully developed legs plus Systematics of Chilopoda in Baltic amber 2 limb buds as well as 10 tergites. SIV (with 10 legs and 2 limb buds) possesses 12 tergites. In SIV individuals of As stated above, the taxonomy of centipedes in Baltic amber Lithobius mutabilis, the number of 10 leg pairs is little is a field that needs to be revised (Edgecombe 2011). But higher than in L. forficatus, whereas the number of 2 pairs even if the taxonomy of these fossil species were to be of limb buds is identical (Voigtländer 2007). The possession resolved more satisfactorily, a proper assignment of the of 12 tergites might point to the fourth stadium (SIV) of the specimen described here would be difficult. Traditionally, lithobiomorph nymph described here. Probably not all the taxonomy is focused on adult stages. Assigning an early legs present are accessible. stage as described here would demand having “bridging” Another character that can be used to discriminate juvenile stages. As could be shown for other fossil arthro- nymphal stadia is the number of antennal articles. In inves- pods, juvenile stages could have been recognized as separate tigated extant species (Andersson 1979), mostly SIII and species in the past (e.g., Haug et al. 2012b). A thorough some SIV of Lithobiomorpha exhibit 14 antennal articles revision of the taxonomy should therefore include also a (SII: 11–12 with exception of 14 in C. longitarsis). SIV reconstruction of ontogenetic sequences of the investigated possesses 14 to 17 antennal articles, with exception of C. species. Then, it would also be possible to assign the spec- longitarsis (20–24). The number of lateral ocelli also imen described here to a species and clearly identify the changes during ontogeny. SII to SIV usually possess 2–3 nymphal stadium. lateral ocelli, SV usually 2–4. Although this would not be The ontogeny of extant centipedes has been described for consistent with an SIV status of our specimen as it possesses at least some species (e.g., Verhoeff 1905; Scheffel 1969; 5–6 lateral ocelli, it is not a strong contradiction, as this Andersson 1979, 1981; Voigtländer 2007; recent summary character varies considerably. Yet, the finding of 5–6 lateral in Minelli and Sombke 2011). Yet, literature featuring such ocelli is of importance for a clearer systematic positioning of earlier developmental stages in detail is still scarce (e.g., the specimen. Among Lithobiomorpha, two sister groups Verhoeff 1938). In other arthropod groups, for instance deca- are distinguished: Henicopidae and Lithobiidae. Besides pod , the description of post-embryonic sequences bearing walking legs with distal spinose projections on the is a standard executed for a large number of species. Also, the tibia (at least the 1st–11th pair of walking legs—a feature importance of such data for understanding the evolution and that cannot be revealed in our fossil specimen) and other phylogeny of these groups has been demonstrated repeatedly characters not accessible in the specimen described here, (for Brachyura: Yang 1971; van Dover et al. 1986;Lago1988, extant Henicopidae exhibit a single lateral ocellus on each 1993; Schubart and Cuesta 1998; Cuesta and Schubart 1999; side of the head or are blind (e.g., Edgecombe 2004; Rodriguez and Spivak 2001;Cuestaetal.2002; Santana et al. Zapparoli and Edgecombe 2011). Since our described spec- 2004a, b; for Hippolytidae: Yang and Kim 2005;for imen has at least 5–6 lateral ocelli on either side of the head, Paguridae: McLaughlin et al. 1988, 1991, 1993;for it seems reasonable to assume that it belongs to Lithobiidae. Palaemonidae: Knowlton and Vargo 2004; for Palinuridae: The lithobiomorph nymph described here bears at least 7 McWilliam 1995; for Pinnotheridae: Bolaños et al. 2004;for visible legs (most likely more), 14 antennal articles, and Thalassinida: Strasser and Felder 1999). Yet, it remains diffi- probably 13 tergites (12 in centipede terminology, not cult to find well-illustrated and complete ontogenetic se- counting that of the maxilliped), assuming two short tergites quences for centipedes (despite the mentioned catalogues of that could not be observed. In comparison to the mentioned stage-specific character states, e.g., Andersson 1981; data of extant lithobiomorphs, this set of characters points to Voigtländer 2007). A reinvestigation, including illustration, a larval stadium IV. of many extant centipede species will therefore be necessary It is often difficult to link isolated larvae to the right for a better understanding of the fossil representatives. species, even in extant species. For fossils the case is even more complicated. Yet, as Andersson (1979) pointed out, Palaeo-evo-devo of Chilopoda larval characters possess little individual variation in com- parison to adult characters. According to Voigtländer (2007), The specimen described here offers a first glimpse into the variability increases from early post-embryonic to later fossil ontogeny of centipedes. Within Chilopoda, the ontog- stages in Lithobius species. This relative constancy in char- eny evolves towards direct development. Scutigeromorpha acter appearance should in principle facilitate a discrete hatch with only 4 trunk segments, the adult has 15 trunk staging of extant species and a comparison with those of segments corresponding with 15 pairs of walking legs. fossils. This has been already carried out for a number of Lithobiomorpha hatch already with seven trunk segments; extant lithobiid species; stage-specific catalogues of charac- the status of adult lithobiomorphs (15 segments with 15 ter states have been reported (e.g., Andersson 1981; pairs of walking legs) equals that of Scutigeromorpha Voigtländer 2007). (e.g., Minelli and Koch 2011). Craterostigmomorpha hatch 430 J.T. Haug et al. with 12 segments, the adult has again 15 segments (Manton Borucki, H. (1996). Evolution und phylogentisches System der Chilopoda (Mandibulata, Tracheata). Verhandlungen des 1965). However, they are often considered as developing – “ ” naturwissenschaftlichen Vereins in Hamburg, NF, 35,95 226. almost epimeric . Epimorpha (= Scolopendromorpha + Cuesta, J. A., & Schubart, C. D. (1999). First zoeal stages of Geophilomorpha) hatch with the adult number of segments Geograpsus lividus and Goniopsis pulchra from Panama confirm (e.g., Minelli and Koch 2011). consistent larval characters for the subfamily Grapsinae – Fossil representatives of Chilopoda could preserve on- (Crustacea: Brachyura: Grapsidae). Ophelia, 51, 163 176. Cuesta, J. A., Liu, H., & Schubart, C. D. (2002). First zoeal stages of togenetic patterns that bridge existing ones. Therefore, Epigrapsus politus Heller, E. notatus (Heller) and Gecarcoidea more knowledge of the ontogenies of fossil centipedes lalandii H. Milne-Edwards, with remarks on zoeal morphology of is desirable. For example, the position of Devonobius the Gecarcinidae Macleay (Crustacea: Brachyura). Journal of – delta has been interpreted either as sister taxon to Natural History, 36, 1671 1685. Cuggy, M. B. (1994). Ontogenetic variation in Silurian eurypterids Craterostigmomorpha (Borucki 1996)orEpimorpha from Ontario and New York State. Canadian Journal of Earth (Shear and Bonamo 1988). To date, both of these alter- Sciences, 31, 728–732. natives are equally parsimonious (Edgecombe and Giribet Dunlop, J. A. (2002). Arthropods from the Lower Severnaya 2004). Ontogeny could provide additional characters for Zemlya Formation of October Revolution Island (Russia). Geodiversitas, 24(2), 349–379. solving this question. The specimen described here pro- Edgecombe, G. D. (2004). A new species of the henicopid centipede vides a hint that a palaeo-evo-devo approach could also Haasiella (Chilopoda: Lithobiomorpha): new species from be successful for centipedes. Yet, it demands more ma- Australia, with a morphology-based phylogeny of Henicopidae. – terial like that described here. At least we now know that Journal of Natural History, 38,37 76. Edgecombe, G. D. (2011). Chilopoda – Fossil history. In A. Minelli it is possible to find such specimens. (Ed.), Treatise on Zoology—Anatomy, Taxonomy, Biology. The Myriapoda I (pp. 355–361). Leiden: Brill. Edgecombe, G. D., & Giribet, G. (2004). Adding mitochondrial se- Acknowledgments Paul Mayer, Field Museum Chicago, is thanked quence data (16S rRNA and cytochrome c oxidase subunit I) to for help in the collection and loan of the specimen. Susan Butts and the phylogeny of centipedes (Myriapoda, Chilopoda): an analysis Jessica Utrup, Yale Peabody Museum, are also thanked for help with the of morphology and four molecular loci. Journal of Zoological loan of the specimen and the use of the equipment at the Peabody Systematics and Evolutionary Research, 42,89–134. Museum. Dieter Waloszek and the Work Group Biosystematic Edgecombe, G. D., Minelli, A., & Bonato, L. (2009). A Documentation, University of Ulm, are thanked for providing the geophilomorph centipede (Chilopoda) from La Buzinie amber ScopeTek DCM 510 ocular camera. We thank Gregory D. Edgecombe (Late : ), SW France. Geodiversitas, 31, for fruitful comments on our manuscript. The specimen was investigated 29–39. during a research visit at the Yale Peabody Museum, supported by the Haug, J. T., Maas, A., & Waloszek, D. (2009a). Ontogeny of two Alexander von Humboldt-Foundation with a Feodor Lynen fellowship stem crustaceans, †Goticaris longispinosa and for postdoctoral researchers for J.T.H., and by Yale University and Derek †Cambropachycope clarksoni. Palaeontographica A, 289,1–43. E. G. Briggs, Yale University and Peabody Museum, for which they are Haug, J. T., Haug, C., Maas, A., Fayers, S. R., Trewin, N. H., & Waloszek, D. heartily thanked. J.T.H. is currently kindly funded by the Alexander von (2009b). Simple 3D images from fossil and recent micromaterial using Humboldt Foundation with a Feodor Lynen return fellowship. Carolin light microscopy. Journal of Microscopy, 233,93–101. Haug, University of Greifswald, is thanked for longstanding support and Haug, J. T., Maas, A., & Waloszek, D. (2010a). †Henningsmoenicaris intense discussions. Steffen Harzsch, University of Greifswald, is thanked scutula, †Sandtorpia vestrogothiensis gen. et sp. nov. and for hosting and supporting the authors. We are grateful to people that heterochronic events in early evolution. Earth and spend their time for providing free or low cost software that was also used Environmental Science Transactions of the Royal Society of in this study, such as OpenOffice and Image Analyzer. Edinburgh, 100,311–350. Haug, J. T., Waloszek, D., Haug, C., & Maas, A. (2010b). High-level phylogenetic analysis using developmental sequences: the Cambrian †Martinssonia elongata, †Musacaris gerdgeyeri gen. et sp. nov. and their position in early crustacean evolution. References Arthropod Structure and Development, 39, 154–173. Haug, J. T., Haug, C., Waloszek, D., & Schweigert, G. (2011). The impor- tance of lithographic limestones for revealing ontogenies in fossil Andersson, G. (1979). On the use of larval characters in the classifi- crustaceans. Swiss Journal of Geosciences, 104(Suppl.), 1,85–98. cation of lithobiomorph centipedes (Chilopoda, Lithobiomorpha. Haug, C., Van Roy, P., Leipner, A., Funch, P., Rudkin, D. M., In M. Camatini (Ed.), Myriapod biology (pp. 73–81). London: Schöllmann, L., et al. (2012a). A holomorph approach to xiphosuran Academic. evolution – a case study on the ontogeny of Euproops. Development, Andersson, G. (1981). Taxonomical studies on the post-embryonic Genes and Evolution, 222,253–268. development in Swedish Lithobiomorpha (Chilopoda). Haug, J. T., Waloszek, D., Maas, A., Liu, Y., & Haug, C. (2012b). Entomologica Scandinavica (Suppl.), 16, 105–124. Functional morphology, ontogeny and evolution of mantis shrimp- Bolaños, J., Cuesta, J. A., Hernandez, G., Hernandez, J., & Felder, D. L. like predators in the Cambrian. Palaeontology, 55,369–399. (2004). Abbreviated larval development of Tunicotheres moseri Horner, J. R., Goodwin, M. B. (2009). Extreme cranial ontogeny in the (Rathbun, 1918) (: Pinnotheridae), a rare case of parental Upper Cretaceous dinosaur Pachycephalosaurus. PloS ONE, care among brachyuran . Scientia Marina, 68,373–384. 4(10), art. e7626, 11pp. Bonato, L., Edgecombe, G. D., Lewis, J. G. E., Minelli, A., Pereira, L. Hughes, N. C., Minelli, A., & Fusco, G. (2006). The ontogeny of A., Shelley, R. M., et al. (2010). A common terminology for the trilobite segmentation: a comparative approach. Paleobiology, external anatomy of centipedes (Chilopoda). ZooKeys, 69,17–51. 32, 602–627. Fossil centipede nymph and a new way of documenting amber fossils 431

Klug, C. (2001). Life-cycles of Emsian and Eifelian ammonoids Sánchez-Villagra, M. R. (2010). Developmental palaeontology in (Devonian). Lethaia, 34, 215–233. synapsids: the rock record of ontogeny in mammals and their Knowlton, R. E., & Vargo, C. K. (2004). The larval morphology of closest relatives. Proceedings of the Royal Society B, 277, Palaemon floridanus Chace, 1942 (Decapoda, Palaemonidae) 1139–1147. compared with other species of Palaemon and Palaemonetes. Santana, W., Marques, F., & Pohle, G. (2004). Larval stages of Crustaceana, 77, 683–715. Stenocionops furcatus (Olivier, 1791) (Decapoda: Brachyura: Kobbert, M. J. (2005). Bernstein—Fenster in die Urzeit. Göttingen: Majoidea) and a reappraisal of larval morphological characters Planet Poster. for Mithracidae. Journal of Plankton Research, 26, 859–874. Kukalová-Peck, J. (1997). Mazon Creek insect fossils: the origin of insect Santana, W., Pohle, G., & Marques, F. (2004b). Larval development of wings and clues about the origin of insect metamorphosis. In C. W. Apiomithrax violaceus (A. Milne Edwards, 1868) (Decapoda: Shabica & A. A. Hay (Eds.), Richardson’s guide to the fossil fauna Brachyura: Majoidea: Pisidae) reared in laboratory conditions, of Mazon Creek (pp. 194–207). Chicago: Northeastern Illinois and a review of larval characters of Pisidae. Journal of Natural University Press. History, 38, 1773–1797. Lago, R. P. (1988). Larval development of Spiroplax spiralis (Barnard, Scheffel, H. (1969). Untersuchungen über die hormonale Regulation 1950) (Brachyura: Hexapodidae) in the laboratory; the systematic der Häutung und Anamorphose von (L.) position of the family on the basis of larval morphology. Journal (Myriapoda, Chilopoda). Zoologische Jahrbücher. Abteilung für of Crustacean Biology, 8, 576–593. allgemeine Zoologie und Physiologie der Tiere, 74, 436–505. Lago, R. P. (1993). Larval development of Sesarma guttatum A. Milne Scheller, U., & Wunderlich, J. (2001). First description of a fossil Edwards (Decapoda: Brachyura: Grapsidae) reared in the labora- pauropod, Eopauropus balticus n. gen. n. sp. (Pauropoda: tory, with comments on larval generic and familial characters. Pauropodidae), in Baltic amber. Mitteilungen aus dem Geologisch- Journal of Crustacean Biology, 13, 745–762. Paläontologischen Institut der Universität Hamburg, 85,221–227. Lewis, J. G. E. (1981). The biology of centipedes. Cambridge: Scheller, U., & Wunderlich, J. (2004). Two fossil symphylan species, Cambridge University Press. Scutigerella baltica n. sp. and Hanseniella baltica n. sp. (Tracheata, Malchus, N. (2000). Early shell stages of the Middle bivalves Scutigerellidae), in Baltic amber. Stuttgarter Beiträge zur Camptochlamys (Pectinidae) and Atreta (Dimyidae) from Poland. Naturkunde Serie B (Geologie und Paläontologie), 351,1–11. Journal of Molluscan Studies, 66, 577–581. Schoch, R. R., & Fröbisch, N. B. (2006). Metamorphosis and neoteny: Manton, S. M. (1965). The evolution of arthropod locomotory mech- alternative pathways in an extinct amphibian clade. Evolution, 60, anisms. Part 8. Functional requirements and body designs in 1467–1475. Chilopoda, together with a comparative account of their Schubart, C. D., & Cuesta, J. A. (1998). First zoeal stages of four skeletomuscular systems and an appendix on the comparison Sesarma species from Panama, with identification keys and re- between burrowing forces of annelids and chilopods and its marks on the American Sesarminae (Crustacea: Brachyura: bearing upon the evolution of the arthropodan haemocoel. Grapsidae). Journal of Plankton Research, 20,61–84. Journal of the Linnean Society (Zoology), 46, 251–483. Sevastopulo, G. D. (2005). The early ontogeny of blastoids. McLaughlin, P. A., Gore, R. H., & Crain, J. A. (1988). Studies on the Geological Journal, 40, 351–362. Provenzanoi and other pagurid groups: 2. A reexamination of the Shear, W. A., & Bonamo, P. M. (1988). Devonobiomorpha, a new larval stages of Pagurus hirsutiusculus hirsutiusculus (Dana) order of centipedes (Chilopoda) from the Middle Devonian of (Decapoda: Anomura: Paguridae) reared in the laboratory. Gilboa, New York State, USA, and the phylogeny of centipede Journal of Crustacean Biology, 8, 430–450. orders. American Museum Novitates, 2917,1–30. McLaughlin, P. A., Gore, R. H., & Harvey, A. W. (1991). Studies on Shear, W. A., & Edgecombe, G. D. (2010). The geological record and the Provenzanoi and other pagurid groups: 5. The larval stages of phylogeny of the Myriapoda. Arthropod Structure and Development, Pagurus arenisaxatilis Harvey and McLaughlin, 1991 39,174–190. (Decapoda: Anomura: Paguridae), reared in the laboratory. Stein, M., Waloszek, D., Maas, A., Haug, J. T., & Müller, K. J. (2008). Journal of Crustacean Biology, 11, 416–431. Oelandocaris oelandica revisited. Acta Palaeontologica McLaughlin, P. A., Siddiqui, F. A., & Crain, J. A. (1993). Larval and Polonica, 53, 461–484. early juvenile development in Pagurus stevensae Hart, 1971 Strasser, K. M., & Felder, D. L. (1999). Larval development in two (Decapoda: Anomura: Paguridae), reared in the laboratory. populations of the ghost shrimp major (Decapoda: Journal of Crustacean Biology, 13, 322–342. Thalassinidea) under laboratory conditions. Journal of Crustacean McWilliam, P. S. (1995). Evolution in the phyllosoma and puerulus Biology, 19,844–878. phases of the spiny lobster Panulirus White. Journal of Sumrall, C. D. (2008). The origin of Lovén’s Law in glyptocystitoid Crustacean Biology, 15, 542–557. rhombiferans and its bearing on the plate homology and the Minelli, A., & Koch, M. (2011). Chilopoda—General morphology. In heterochronic evolution of the hemicosmitid peristomal border. A. Minelli (Ed.), Treatise on Zoology—Anatomy, Taxonomy, In W. I. Ausich & G. D. Webster (Eds.), Echinoderm Biology. The Myriapoda I (pp. 43–66). Leiden: Brill. Paleobiology (pp. 228–241). Bloomington, IN: University of Minelli, A., & Sombke, A. (2011). Chilopoda—Development. In A. Indiana Press. Minelli (Ed.), Treatise on Zoology—Anatomy, Taxonomy, Biology. Sumrall, C. D., & Wray, G. A. (2007). Ontogeny in the fossil record: The Myriapoda I (pp. 295–308). Leiden: Brill. Diversification of body plans and the evolution of “aberrant” Nützel, A., Fryda, J., Yancey, T. E., & Anderson, J. R. (2007). Larval symmetry in Paleozoic echinoderms. Paleobiology, 33, 149–163. shells of Late Palaeozoic naticopsid gastropods (Neritopsoidea: Tack, Y. W. (1971). The larval and postlarval development of Neritimorpha) with a discussion of the early neritimorph evolu- Parthenope serrata reared in the laboratory and the systematic tion. Paläontologische Zeitschrift, 81, 213–228. position of the Parthenopinae (Crustacea, Brachyura). Biological Poinar, G. O., & Edwards, C. A. (1995). First description of a fossil Bulletin, 140, 166–189. symphylan, Scutigerella dominica sp. n. (Scutigerellidae, vanDover,C.L.,Gore,R.H.,&Castro,P.(1986).Echinoecus ) in Dominican amber. Experientia, 51, 391–393. pentagonus (A. Milne Edwards, 1879): larval development Rodriguez, A., & Spivak, E. D. (2001). The larval development of and systematic position (Crustacea: Brachyura: Xanthoidea Panopeus margentus (Decapoda: Brachyura: Panopeidae) reared nec Parthenopoidea). Journal of Crustacean Biology, 6, in the laboratory. Journal of Crustacean Biology, 21, 806–820. 757–776. 432 J.T. Haug et al.

Verhoeff, K. W. (1905). Über die Entwicklungsstufen der Steinläufer, Wichard, W., Gröhn, C., & Seredszus, F. (2009). Wasserinsekten im Lithobiiden, und Beiträge zur Kenntnis der Chilopoden. Baltischen Bernstein: Aquatic Insects in Baltic Amber. Remagen- Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Oberwinter: Kessel. Geographie der Tiere, 8, 195–289. Yang,H.J.,&Kim,C.H.(2005).ZoealstagesofHeptacarpus Verhoeff, K. W. (1938). Zur Biologie der Scutigera coleoptrata und futilirostris (Decapoda, Caridea, Hippolytidae) reared in the lab- über die jüngeren Larvenstadien. Zeitschrift für Wissenschaftliche oratory. Crustaceana, 78, 543–564. Zoologie, 150, 262–282. Zapparoli, M., & Edgecombe, G. D. (2011). Chilopoda—Taxonomic Voigtländer, K. (2007). The life cycle of Lithobius mutabilis L. Koch, 1862 overview. Order Lithobiomorpha. In A. Minelli (Ed.), Treatise on (Myriapoda: Chilopoda). Bonner Zoologische Beiträge, 55,9–25. Zoology—Anatomy, Taxonomy, Biology. The Myriapoda I (pp. Walossek, D. (1993). The Upper Cambrian Rehbachiella and the phylog- 371–389). Leiden: Brill. eny of Branchiopoda and Crustacea. Fossils and Strata, 32,1–202. Zhang, X.-G., Maas, A., Haug, J. T., Siveter, D. J., & Waloszek, D. Weitschat, W., & Wichard, W. (1998). Atlas der Pflanzen und Tiere im (2010). A eucrustacean metanauplius from the Lower Cambrian. Baltischen Bernstein. München: Pfeil. Current Biology, 20, 1075–1079.