Enigmatic Early Cretaceous ootaxa from Western Europe with signals of extrinsic eggshell degradation

Cretaceous Research 56 (2015) 617e627

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Enigmatic Early Cretaceous ootaxa from Western Europe with signals of extrinsic eggshell degradation
Ignacio Canudo 1, Jose
Manuel Gasca 1 Miguel Moreno-Azanza*, 1, Jose Grupo Aragosaurus-IUCA, Paleontología, Facultad de Ciencias, C/ Pedro Cerbuna 12, Universidad de Zaragoza, 50009 Zaragoza, Spain

a r t i c l e i n f o

a b s t r a c t

Article history: Received 19 January 2015 Received in revised form 29 June 2015 Accepted in revised form 30 June 2015 Available online xxx

Crocodiloid eggshell is considered to be one of the most conservative among amniotes. This contrasts with the high body diversity observed within the crocodylomorph lineage, which extebds from the Triassic to the present. This incongruence raises a fundamental question in palaeology: is the crocodylomorph eggshell structure that conservative, or are there variations in this structure that have been misidentified in the fossil record or remain undiscovered to taphonomic biases? In this paper we re-examine eggshells from the Barremian of northern Spain that were previously assigned to chelonians. We erect a new oogenus and oospecies, Mycomorphoolithus kohringi, characterized by thin eggshells with mushroom-shaped or inverted cone shell units with blocky extinction with smooth or slightly undulating outer surface, covered by a highly variable number of pores of irregular size and shape. These variations in the pore opening pattern are here interpreted as evidence of degradation of the eggshell during embryo development, a process that has only been described in modern alligatorids. After discarding its chelonian and dinosaurian affinities, we identify them as related to Krokolithidae, but with enough differences to justify exclusion from this oofamily. In addition, eggshells from the Berriasian of England previously reported as dinosaurian-spherulitic eggshells, are here assigned to undetermined oospecies of Mycomorphoolithus. Thus, the record of Mycomorphoolithus extends throughout most of the Lower Cretaceous. This long-surviving oogenus may represent eggshells of the non-eusuchian crocodylomorphs that are abundant in the microfossil sites where Mycomorphoolithus eggshells are found. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Mycomorphoolithus kohringi Krokolithidae Berriasian Barremian Parataxonomy Spain

1. Introduction AMNIOTE vertebrate eggshells are biomaterials composed of organic (mostly protein) and inorganic (CaCO3 in the form of calcite or aragonite) phases (Hirsch, 1994a). The relative proportions of the organic and mineralized components determine the physical properties of the eggshell, from its rigidity to its water vapour conductance (Nys et al. 2004; Deeming, 2006). It is important to note that this proportion between mineral and organic components may vary during embryo development as a consequence of extrinsic and intrinsic degradation of the eggshell at least in some recent crocodylomorphs (Ferguson, 1981, 1982; Fernandez et al. 2013). Furthermore, the intricate relations between the protein

* Corresponding author. E-mail addresses: [email protected] (M. Moreno-Azanza), jicanudo@unizar. es (J.I. Canudo), [email protected] (J.M. Gasca). 1 http://www.aragosaurus.com. http://dx.doi.org/10.1016/j.cretres.2015.06.019 0195-6671/© 2015 Elsevier Ltd. All rights reserved.

network and the crystallographic fabric of the mineralized components result in many different textures, denominated ultrastructures, which may vary across the eggshell section, producing different eggshell morphotypes (Mikhailov, 1991). These variations in texture result in an anisotropic response of the eggshell to modifying agents, a characteristic that some crocodilians use to their advantage (e.g. making it easier to hatch the egg through partial degradation of the eggshell; Ferguson, 1981). The main consequence of the above is that the structure of fossil vertebrate eggshell is extremely diverse, and when modern analogues are not available it may be very difficult to relate egg material to taxa specific taxon. Moreover, eggshell in different states of degradation (either biological or diagenetic) may be misidentified as different ootaxa if the studied sample is not large enough. The development of egg parataxonomy in the last part of the 20th century partially overcame these problems, as eggshells can be classified on the basis of their mineralogical and morphological € hring and Hirsch, features (Mikhailov, 1991, 1997; Hirsch, 1996; Ko

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1996). Subsequent work has demonstrated that high hierarchy levels of eggshell classification (at the oofamily level) usually correspond to high hierarchy taxonomic levels e usually above the family level (Zelenitsky and Thierrien, 2008; Mikhailov, 2013). This relation also shows that eggshell morphology is partly related with the taxonomy, thus genetic or epigenetic controlled and subject of evolution and natural selection. A canonical case of such a relationship between an oofamily and a high hierarchy taxonomic €hring and Hirsch, clade is provided by the oofamily Krokolithidae Ko 1996, which contains the eggshells of all fossil crocodylomorphs, which share all diagnostic characters with modern crocodilian eggshell, suggesting that crocodylomorph eggshell (crocodiloid €hring and Hirsch, 1996) is very basic type and morphotype, Ko conservative and has not changed much from the Jurassic to the present (Hirsch 1994b, Antunes et al., 1998, Marzola et al., 2015). This contrasts sharply with the wide diversity shown by bodyfossils of crocodylomorphs, especially during the Mesozoic, when crocodylomorphs populated most of the ecosystems and occupied varied ecological niches, with subsequent adaptations and morphological changes (Stubbs et al. 2013). Nevertheless, recent work has postulated that crocodiloid basic type eggshells may be more variable than previously thought (Oliveira et al. 2011; Moreno-Azanza et al. 2014b). In this paper we restudy eggshell materials previously assigned to the dinosaur spherulithic and testudoid morphotypes. Careful examination of new specimens does not support these assignments, as they share several characters with crocodyloid eggshells. Furthermore, we observe evidences of extrinsic degradation of the eggshell which provably occurred during incubation, a process seen in modern alligatorids. 2. Geological setting The eggshells included in this study come from several Lower Cretaceous (Barremian) localities in the Maestrazgo Basin, a part of the larger Iberian Basin (Fig. 1) in the east Iberian Peninsula (Spain). Mesozoic sedimentation in the Iberian Basin took place within an intraplate extensional tectonic framework with two main rift stages (Late Permian to Early Jurassic and Late Jurassic to Early Cretaceous). During this second rifting stage, differential subsidence was caused by reactivation of late and post-Variscan or Triassic faults, and the formation of NWeSE and NEeSW normal faults (Liesa et al. 2006 and references within). This rifting cycle led to the creation of the Maestrazgo Basin, which can be subdivided into seven smaller sedimentary sub-basins. Sedimentation in these sub-basins was tectonically controlled and diachronous, and was not homogenized at the basin level until the Albian (Salas et al. 2001). This complex tecto-sedimentary framework resulted in the partitioning of depositional environments, which supported the proliferation of vertebrate-rich ecosystems that have been recorded in some geological units from the Early Cretaceous (Estes and Sanchiz, 1982; Buscalioni et al. 2008; Canudo et al. 2010; CuencaBescos et al. 2011). Of especial interest are some microfossil bonebeds (Buscalioni et al. 2008; Canudo et al. 2010; Gasca et al. 2012) from the Iberian Chain outcrops that have been regarded as time-averaged samples of their source communities (sensu Rogers and Brady, 2010) ei.e. they record the faunal and floral association of the ecosystem during periods of hundreds or thousands of years, instead of recording single punctual events. Fossil eggshell fragments are almost ubiquitous in the Lower Cretaceous microfossil bonebeds of Spain, and are usually present in high numbers, forming a significant part of the fossil assemblage (Moreno-Azanza
s et al., 2011; et al. 2009a, 2009b; Canudo et al. 2010; Cuenca-Besco

Gasca et al. 2012; Moreno-Azanza et al. 2014b, 2014c). The eggshells described in this study come from several early Barremian localities from the Maestrazgo Basin. The type material comes from the La Cantalera locality, located 2 km west of the village of Josa (Teruel, NE Spain), in an outcrop of the Barremian Blesa Formation (Canudo et al. 2010; Moreno-Azanza et al. 2014b, 2014c), within the Oliete Sub-basin. Additional material been collected from other microfossil sites from the Galve Sub-basin, more precisely from the upper part of the El Castellar Formation in the Galve Sub-basin (Canudo et al., 2012) and from the Morella Sub-basin (Mirambel Formation, Barremian in age, Castellote, Teruel). These bonebeds formed as attritional deposits through the progressive accumulation and concentration of disarticulated remains within low-energy depositional settings; more specifically, on a poorly drained floodplain in the case of the La Cantalera locality (Canudo et al. 2010; Moreno-Azanza et al. 2014b), and on shallow lacustrine de
s et al. 2011). posits in others (Cuenca-Besco The La Cantalera locality has yielded thousands of skeletal remains from at least 31 taxa (Canudo et al. 2010), and previous estimates based on preliminary studies suggest the presence of at least eight ootaxa are present (Moreno-Azanza et al. 2009a). However, the results presented here reduce this diversity to seven ootaxa, including the recently described Guegoolithus turolensis (Moreno-Azanza et al., 2014c). The La Cantalera site is the type locality of Trigonoolithus amoae (Moreno-Azanza, Canudo and Gasca 2014b). An oogenus of the oofamiliy Prismatoolithidae. 3. Materials and methods The eggshell fragments included in this study were obtained by washing and sieving the deposits from four different localities. Over three tons of rocks from the La Cantalera locality were washed and sifted, whereas only 500 kg of rocks were processed each from the Menires and Camino Canales 2 localities. The sedimentary deposits were processed using 2% hydrogen peroxide and sieves of 2.0, 1.0 and 0.5 mm mesh. The eggshell fragments were sorted under a binocular microscope, and a total of 150 fragments were selected for this study. Thirty fragments were mounted, gold-coated and viewed with a JEOL 6400 SEM at the University of Zaragoza, using both secondary and backscattered electrons. X-ray diffraction analyses were used to confirm the calcite composition of the eggshells. Twenty eggshell fragments were prepared as radial sections, and studied under an Olympus BX 41 petrographic microscope. In addition, cathodoluminescence (CL) analyses were performed with a Nikon Eclipse 50i POL optical microscope coupled with a cathodoluminescence system (model CL8200 Mk5-1) at the Institut  d'Arqueologia Cla ssica (ICAC; Tarragona, Spain). CathCatala odoluminescende images where edited using Adobe Photoshop, overexposing the whole picture þ 5, due to the low general luminescence of the samples. . The eggshell measurements were obtained from a sample of 96 eggshells, representative of each category, using a digital calliper. The pore surface areas were measured by digital analysis of scanning electron microscopy images using the software ImageJ. Due to the small mean size of the eggshell fragments (1.99 mm2, SD ¼ 0.89), and the fact that eggshell fragments tend to break at pore openings, two different approaches were used to estimate the number of pores of the eggshell (Table 1). First, only complete pore openings were counted, which is considered to underestimate the total pore opening count. Secondly, partially preserved pore openings were also counted. This number may be closer to the real porosity, but it overestimates the actual density of pores per square

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Fig. 1. Stratigraphic logs of the localities where Mycomorphoolithus kohringi oogen. et oosp. nov. has been recovered, and their geographical and geological setting in a palaeogeographic sketch of the Maestrazgo Basin and its active faults during Early Cretaceous sedimentation, modified from Salas et al. (2001).

Table 1 Measurements of Mycomorphoolithus kohringi oogen. et oosp. nov. See methods for details on the counting of pore openings and percentage of pore surface. Category

A B C D Indet All

n

8 51 27 7 3 96

Thickness/mm

Number of pores (underestimated)

Number of pores (overestimated)

% Pore area

Mean

SD

Mean

SD

Mean

SD

496 518 520 594 e 524

78 94 77 123 e 91

3.25 4.80 6.37 3.29 e 4.91

2.25 2.71 3.87 1.11 e 3.18

10.50 10.94 13.27 8.86 e 11.18

6.07 3.82 5.58 2.91 e 4.75

millimetre, so both values are provided as a minimum and maximum porosity. All the materials are housed in the Museo de Ciencias Naturales de la Universidad de Zaragoza (MPZ).

4. Systematic palaeontology Oofamily Incertae sedis. Oogenus Mycomorphoolithus oogen. nov.

5 8 17 20 e

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Type (and only included) oospecies Mycomorphoolithus kohringi. 4.1. Included material: € hring p. 332, Fig. 3, Fig. XX. 1990 Type B. Ko 1997 Type 1. Ensom pp. 80 p. pl. 1AeE.
n, 1998 p. 56, pl. 12, 13, 44. 1998 Testudoolithus sp. Amo-Sanjua 1999 Spherurigidus morphotype Amo-Sanjuan et al. p. 18. 2002 Type 1 Ensom p. 224 pl 1. 2002 cf. Type 1 Ensom, p. 224 text-Fig. 2. 2002 Type 2. Ensom pl. 1, p. 225 text-Fig. 3. 2010 Oofamily Incertae sedis 1 Canudo; Gasca; Aurell; et al. p. 218, Fig. 6.8. 2010 Oofamily Incertae sedis 2 Canudo; Gasca; Aurell; p. 218, Fig. 6.9. 4.2. Diagnosis As for the only known oospecies. 4.3. Derivation of the name Mushroom-shaped stone egg, in reference to the shape of the shell units. From mycos, ancient Greek for mushroom; morph, ancient Greek for form; and oolithus, the usual ending of fossil ootaxa, meaning stone egg. 4.4. Occurrence Berriasian of England (Purbeck facies) and lower Barremian of Spain (Blesa, El Castellar and Mirambel Formations). Oospecies: M. kohringi oosp. nov. Figs. 2e5. € hring p. 332, Fig. 3. 1990 Type B. Ko
n 1998 p. 56, pl. 12, 13, 44. 1998 Testudoolithus sp. Amo-Sanjua 1999 Spherurigidus morphotype Amo-Sanjuan et al. p. 18.

2010 218, Fig. 2010 218, Fig.

Oofamily incertae sedis 1 Canudo; Gasca; Aurell; et al. p. 6.8. Oofamily incertae sedis 2 Canudo; Gasca; Aurell; et al. p. 6.9.

4.5. Holotype MPZ2014/37 a single eggshell fragment prepared for SEM examination. 4.6. Material 149 eggshell fragments, (MPZ2014/2eMPZ2014/150) from the type locality, La Cantalera, that form the paratype, 25 of them prepared as radial standard 30 mm thin sections and 28 prepared for SEM observation. Additional material includes 58 eggshell fragments from the Camino Canales 2 locality (MPZ2014/151eMPZ2014/ 208) and 6 eggshell fragments from the Menires locality. 4.7. Diagnosis Eggshells characterized by a single autapomorphy: Mushroomshaped or inverted cone shell units comprising radiating wide crystals. They also differ from all previously known eggshell taxa in the following combination of characters: Eggshell with a mean eggshell thickness of 524 mm (n ¼ 96, SD ¼ 0.09, full range 0.31e0.81). Shell units are slender at the base of the unit, abruptly increasing in width up to fivefold at one third to one half of the eggshell. Pore openings vary in shape and dimensions, from 60 mm sub-circular pore openings to 300 mm oval to irregular pore openings that may be even larger due to the coalescence of adjacent pores. High pore density, ranging from four to 10 pores per square millimetre. Growth lines are straight to slightly wavy, over the entire eggshell thickness. 4.8. Derivation of the name In honour of the late palaeontologist Rolf Kohring (1959e2012), pioneer in studies of Iberian eggshells.

Fig. 2. Mycomorphoolithus kohringi oogen. et oosp. nov. SEM (secondary-electron) images of radial sections showing the ultrastructure of the eggshell. A. MPZ2014/37. Holotype. Freshly broken radial section. Notice the characteristic mushroom-shaped units, higher than wide,. Shell broadens half way through the thickness. These units are well spaced, and a straight and wide pore channel ends in the large interstice between shell units. Filament in the upper middle part of the photograph is a modern filament deposited during sample preparation. B. MPZ2014/28. Abraded eggshell radial section where growth lines can be observed (black arrow). C-D. MPZ2014/52 and MPZ2014/30 Freshly broken radial sections where the wedges of the shell units show typical calcite angles (white arrows). Scale bars ¼ 500 mm.

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Fig. 3. Mycomorphoolithus kohringi oogen. et oosp. nov. Standard 30 mm thin sections. A, C, E, MPZ2014/2. B, D, F, MPZ2014/5. G, H, MPZ2014/3. A-B, G. Sections in parallel nicols, where brownish wavy growth lines can be observed. Also note the highly variable spacing between shell units, where the interstices may be wider than individual shell units. C-D. Cross-nicol photographs. Wedge crystals with blocky extinction can be observed. Note that the number of crystals remains almost constant from the base of the shell units to the top. E, F, H. Overexposed cathodoluminescence photographs. A homogeneous dark blue colour indicates that there is no evidence of recrystallization, and that the original calcitic composition and crystallography of the eggshell is preserved in most of the eggshell. Note the presence of a fine coating of cement in F, in both the inner and outer surface, and filling small cracks in the eggshell in H, which luminesces in bright orange, indicating its secondary origin. The irregular spacing between shell units can be appreciated in G and H, where some shell units appear packed an others show wide interstices between them. Scale bars ¼ 250 mm (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.).

4.9. Description The eggshell fragments are small in size (less than half square millimetre). Due to their great friability, the eggshells easily break during preparation and manipulation. The mean thickness of the eggshell is 524 mm (n ¼ 96, SD ¼ 0.09). In radial section (Fig. 2), the eggshell is composed of a single layer of calcite crystals. The shell units are small at their bases and broaden at around half of the

eggshell thickness, and fuse with neighbouring units. In general, this peculiar shape leaves wide interstices between the bases of the shell units that connect different pore channels. In other areas of the eggshell, the bases of the units are more closely packed together, leaving smaller interstices. Freshly broken surfaces display a radiating ultrastructure of crystals, where distinctive calcite angles can be recognized, whereas abraded sections highlight the presence of the growth lines.

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Fig. 4. Mycomorphoolithus kohringi oogen. et oosp. nov. SEM (secondary-electron) images of the outer surfaces of four eggshell fragments used to define the pore opening distribution categories, with a progressive increase in pore opening size and number (Table 1). Category names match figure lettering. A. MPZ2014/32. Category a e fragments with few small, rounded pore openings and a smooth outer surface. B. MPZ2014/35. Category b e fragments with a greater pore density and two families of round pore openings of different size and a smooth outer surface; C. MPZ2014/48. Category c e fragments with large, oval to irregular pore openings, in addition to the small rounded ones, plus abundant depressions resembling incipient pore openings and a wavy outer surface. D. MPZ2014/38. Category d e fragments where big pore openings coalesce and give the outer eggshell surface a “wormy” aspect. White arrows point to dissolution pits, that sometimes develop through the eggshell thickness forming new pores. Note that this can be seen only in the outer surfaces of the eggshells, suggesting an extrinsic origin. Scale bars ¼ 1 mm.

Thin sections (Fig. 3A, B) reveal faint, light brown growth lines are seen. These are equidistant to one another, and straight to slightly wavy. They are continuous through adjacent shell units. Under polarizing light, the eggshells display blocky extinction. Individual extinction domains are wide, and possibly represent individual tabular crystals. They develop at acute angles with respect to the direction of eggshell growth. Cathodoluminescence images (Fig. 3) do not show evidence of recrystallization, although certain areas of the thin sections (arrow in 3C) present evidence of dogtooth spar texture, a signal of recrystallized calcite in fossil eggshells (Moreno-Azanza et al., 2014a). X-ray diffraction analyses confirm that the mineralogy is low-magnesium calcite. No traces of

cathodoluminescence quencher elements, such Fe where observed. Careful observation of the 25 thin standard thins sections analysed under petrographic microscope revealed no signs of aragonite. Thus we consider the mineral component of the eggshell preserves its original composition, and have not suffered a significant digenetic recrystallization other than small precipitation of calcite in voids within the eggshell structure. The outer surface of the eggshells (Fig. 4) is smooth to slightly wavy, although extrinsic erosion of the numerous pore openings confers a reticulate appearance upon the outer surface. This degradation resembles the extrinsic alteration of the eggshell
ndez et al., observed in modern alligatorids (Ferguson, 1981; Ferna

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Fig. 5. Mycomorphoolithus kohringi oogen. et oosp. nov. SEM (secondary-electron) images of the inner surface. A, B. MPZ2014/36. Inner surface and detail of the bases of the shell units of an unaltered inner surface showing the bases of the shell units. A massive calcite aggregate can be seen, without the radial ultrastructure of organic cores, resembling the basal knobs of other crocodylomorph eggshells. C, D. MPZ2014/49. Inner surface and detail of the bases of the shell units of an altered inner surface, where the bases of the mammillae have been eroded, and showing erosion craters. The craters do not show the radiating ultrastructure associated with mammiliary cones of dinosaur and turtle eggshell, which surrounds the organic cores. Scale bars A and C ¼ 1 mm, B and D ¼ 200 mm.

2013). However, there is no evidence available concerning when this alteration occurred eduring incubation or in early diagenesis-, and if this is related to chemical weathering or microbial degradation of the eggshell. The high number of pore openings vary in size, with pore densities ranging from 4 to 10 pores per square millimetre among eggshell fragments. The size of the pore openings is also highly variable between different eggshell fragments, and even within a single specimen, although there is not a significant difference in pore density between different fragments (Table 1). Small (60 mm) pore openings are circular in shape, whereas medium-sized and large (over 300 mm) pore openings are oval or irregularly elongated. Some eggshell fragments exhibit interconnected pore openings that give the eggshell surface a “wormy” aspect. All pore openings develop in the thinner areas of the eggshell, above the interstices between adjacent shell units. Eggshells that show large, interconnected pore openings also display small sub-circular dissolution pits in between, suggesting incipient pore openings. Taking this variation in the shape and distribution of pore openings into account, four categories of eggshell fragments are used for descriptive purposes (Fig. 4, Table 1). Small differences in shell thickness and the number of pores can be seen between these categories. The category names correspond to the labelling in Fig. 4. Category a fragments are the thinnest, together with those with the fewest pores. These values slowly increase in subsequent categories, with category d eggshells the thickest ones, measuring 600 mm. This last category has fewer pores than the previous categories, but this is due to the coalescence of adjacent pores, and the actual porosity of the fragment is in fact higher than category c eggshells (see Table 1). The eggshells present small circular to elongated openings in the eggshell surface, ranging between 50 and 100 mm in diameter (white arrows in Fig. 4). These openings not always reach the inner surface of the eggshell, and are more frequent in category b and c eggshells. Here

we interpret them as dissolution pits, similar to those seen in Alligator missisippiensis eggshells (Ferguson, 1981, 1982). Nevertheless, they do not present the concentric rings shown in Alligator eggshell (Ferguson, 1981). The stepped section of Alligator missisipiensis dissolution pits is the result of the anisotropic response of the tabular ultrastructure of the Alligator eggshell to the dissolution (Ferguson, 1081, 1982). As Mycomorpholithus eggshells do not show this tabular ultrastructure, dissolution progresses uniformly through the pit, thus resulting in circular openings with smooth walls. The inner surface presents isolated bases of the shell units arranged in groups of more packed shell units, and usually aligned around the big interstices left by the pore system (Fig. 5). Organic cores are not present in any of the examined specimens. This can be related to erosion (either extrinsic or intrinsic) in some of the fragments (Fig. 5B), but more probably they were not present, as other fragments present massive aggregates of calcite at the base of the shell units (Fig. 5A), which differ from those observed in dinosaur and avian eggshells, which present acicular calcite aggregates around a massive organic core. The basal aggregates present in Mycomorphoolithus resemble the basal knobs of crocodilian eggshell, being massive aggregates of calcite. Nonetheless, no basal plates are observed in any of the specimens, a feature observed in most crocodile and Krokolithidae eggshells. Some fragments present completely abraded inner surfaces, giving them a vermiculate appearance, similar to the outer surface. These inner surface “ridges” are the result of the complete erosion of the bases of the shell units, resulting in a sinuous rim of adjacent units.

4.10. Type locality La Cantalera site, Josa (Teruel Province).

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4.11. Occurrence Barremian of the upper part of the El Castellar Formation (Galve Sub-basin), Mirambel Formation (Morella Sub-basin) and Blesa Formation (Oliete Sub-basin), Maestrazgo Basin, Teruel, Spain. 5. Discussion 5.1. Affinities of Mycomorphoolithus The peculiar combination of characters presented by Mycomorphoolithus has previously led to very different interpretations of €hring (1990) first described the eggshell by several authors. Ko M. kohringi eggshells from the El Castellar Formation in Galve (Teruel Province) as batagurine-turtle-like eggshells (Type B). €hring (1990) described two families of pore openings on the Ko basis of their diameter. The resulting pore opening pattern resembles that of the outer surface of Cuora amboinensis eggshell €stle (Amboina box turtle), as shown in figures by Schleich and Ka €hring (1990) addresses the question of the incompat(1988). Ko ible calcitic composition of the eggshells, considering this to be a recrystallized pseudomorph of the original aragonitic eggshell, and reports some relicts of aragonite in the specimens. After careful examination of specimens from different localities specimens using RDX and petrographic microscopy, no aragonite relicts have been detected. Furthermore, cathodoluminescence analysis (Fig. 3) suggests that the original composition of the eggshell is not significantly R. A small secondary growth of calcite can be appreciated in the outer and inner surfaces of some fragments and filling small cracks in the eggshell (Fig. 3E), bit the general luminescence of the eggshell is pale blue, as in unrecrystallized eggshells. This is congruent with the lack of crystals showing an orientation different from the natural eggshell growth. The lack of organic cores, if confirmed, it is also not compatible with the eggshells being of €hring (1999) changed his chelonian origin. In subsequent work, Ko previous assignation of these eggshells and suggested a dinosaurian affinity. In the present paper, the eggshells described by €hring (1990) are assigned to M. kohringi as they are indistinKo guishable from the type material and this oospecies is present in most microfossil sites in the El Castellar Formation. Ensom (2002) described two types of eggshells (Type 1 and Type 2) from several microsites in the Purbeck Limestone Group (the Lulworth and Durlston Formations, Berriasian in age, Dorset, United Kingdom) that are assignable to Mycomorphoolithu. These eggshells are slightly thicker than the Iberian ones (no mean thickness is reported but estimates are given: “c. 0.755 mm” for Type 1 and “the maximum observed thickness is 0.8 mm” for Type 2). Type 1 and Type 2 eggshells differ in their outer surface ornamentation (flat or wavy in Type 1 as opposed to ridges and pinnacles in Type 2) and in the pattern of pore openings, which are irregular in Type 1 and somewhat connected in Type 2. Interestingly, Ensom (2002) also reports an eggshell fragment as cf. Type 1 (0.5 mm2 in surface area) which lacks pore openings. Both Type 1 and Type 2 eggshells share with Mycomorphoolithus the shape of the shell units, high number of pores, radiating tabular ultrastructure, blocky extinction of the units, straight pore system and the lack of organic cores. Nevertheless, the Purbeck eggshells are significantly thicker than the Iberian ones. Ensom (2002) discusses the possible parataxonomic affinities of these eggshells, correctly pointing out the implausibility of a chelonian origin, and identifies the material as belonging to the dinosauroid-spherulitic basic type, pointing to affinities with the oofamily Faveoloolithidae due to its irregular outer surfaces and high pore density, and its isolated shell units. It is true that Mycomorphoolithus eggshell present a similar general look to eggshells assigned to dinosaurians (Jensen, 1966,

1970; Maxwell and Horner, 1994), but the detailed examination of the eggshell structure clearly prohibits this assignation. Dinosaur-spherulitic eggshells present shell units with a radialtabular ultrastructure of acicular to fine tabular crystals that radiate out from the organic cores at the bases of the mammillae (Mikhailov, 1991, 1997), resulting in undulose extinction. Also, they present well-formed organic cores, like all dinosaur eggshells. The lack of organic cores, the wedge crystals and the blocky extinction do not support this assignation. We assign them to Mycomorphoolithus sp., as they may represent a new oospecies of Mycomorphoolithus but we have not undertaken a first-hand examination of the English material. Mycomorphoolithus shares its blocky extinction pattern, lack of organic cores and isolated shell units with eggshells assigned to €hring the oofamily Krokolithidae. The oofamily Krokolithidae (Ko and Hirsch, 1996) was erected to include eggshells of the crocodiloid basic type and crocodiloid morphotype (sensu Mikhailov, 1991), a morphotype characterized by a single calcitic layer composed of isolated shell units comprising coarse irregular wedges which nucleate from basal plate groups that develop € hring and Hirsch (1996) did not provide around the basal knobs. Ko a diagnosis of the oofamily. They instead provided the diagnosis of the only included oogenus, Krokolithes Hirsch, 1985. Krokolithes is diagnosed as being of the crocodiloid basic type and morphotype, with a smooth to undulating outer surface with erosion craters, straight pore canals ending in deep interstices between shell units, and ellipsoidal eggs with a shell thickness of 0.250e76 mm. Mycomorphoolithus fulfils this diagnosis to a certain extent, as it is single-layered and presents isolated shell units with wedge-like crystals with straight pore canals ending in wide interstices. In addition, the blocky extinction pattern is shared by all extant crocodilian eggshells and all eggshells included in Krokolithidae, and thus can be considered as a sinapomorphy of this group. Nevertheless, some recent revisions of eggshells attributed to modern crocodiles (Jin et al. 2010; Marzola et al., 2015) and fossil Krokolithidae eggshells (Moreno-Azanza et al. 2014c) have reinterpreted several features of the crocodiloid eggshells. The most notable reinterpretation concerns the type oogenus of Krokolithidae, Krokolithes (more precisely Krokolithes wilsoni Hirsch, 1985), which has been redescribed as multilayered (MorenoAzanza et al. 2014c). At least three distinct layers can be identified: an inner layer formed by the basal knobs and basal plates; a middle layer that comprises the greatest part of the wedges; and an outer layer, which is more compact and densely calcified. This multilayered condition of the crocodiloid eggshell was first described by Ferguson (1982), who differentiated up to five layers in the Alligator mississippiensis eggshell (see Moreno-Azanza et al. 2014c for a complete discussion of this topic). Compared with Bauruoolithus Oliveira, Santucci, Andrade, Fulfaro, Basílio, Benton, 2011, a Krokolithidae oogenus from the CampanianMaastrichtian of Brazil related to notosuchian crocodylomorphs, Mycomorphoolithus oogen. nov. shares the single layered eggshell, but has eggshells that are twice as thick, lacks the drop-shaped pore openings, and some fragments are significantly more porous than in the South American oogenus. Marzola et al. (2015) provide an in-depth description of the eggshell of the modern crocodilians Crocodylus mindorensis, Paleosuchus palpebrosus and Alligator mississipiensis. In addition to confirming the presence of three structural layers, these authors report new previously undescribed ornamentations, including slightly sculptured outer surfaces in some of the taxa (including anastomotuberculate, ramotubreculate and rugosocave ornamentations; Marzola et al., 2015), which further increase the disparity of Crocodilan eggshells. Nevertheless these authors stress the relative invariant crystallographic architecture of the crocodilian eggshell.

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A clear and updated diagnosis of the Krokolithidae is needed, thus, we choose not to include Mycomorphoolithus within this oofamily, as it has only one layer (though this could be two if basal plates were originally present, but not three, as there is no evidence of an outer layer). Furthermore, Mycomorphoolithus lacks the distinctive book-like tabular ultrastructure of the Krokolithidae eggshells, although this is typically not well preserved in some fossil eggshells (Hirsch, 1985; Moreno-Azanza et al. 2014c). Also, the high pore opening count seen in Mycomorphoolithus has not being reported in any crocodylomorph eggshell. Nevertheless, the blocky extinction pattern and the subtriangular shell units relate Mycomorphoolithus with crocodiloid eggshells. The lack of organic cores, if confirmed by new better preserved specimens, may also support this relation.

5.2. Eggshell porosity and extrinsic degradation Mycomorphoolithus eggshells show a significant variation in the number of pore openings (33e100% depending on how the pore openings are counted, Table 1) but display an even greater increase in pore area relative to surface area (400%). This substantial difference in the number and size of pore openings has been regarded as evidence for the existence of two different oospecies for this oogenus (Canudo et al. 2010) However analysis of a larger sample size shoes that features of the two purported oospecies overlap and that intermediate specimens exist between the two types (Table 1). Recurrent eggshell degradation has only being described in the eggshell of two species of modern alligatorids, A. mississipiensis and Caiman latirostris. Int his taxa, the porosity of the eggshell increases during the incubation period, via an increase in pore size due to the extrinsic and intrinsic degradation of the eggshell (Ferguson, 1981, 1982). The increase in porosity does not occur uniformly over the entire egg, but starts in the equatorial part and progressively reaches the poles, accompanied by a darkening of the egg area affected. This process has been related to the adherence of the embryo to the inner egg surface (Ferguson, 1982). Ferguson (1982) reported a constant eggshell thickness around the egg in newly laid A. mississippiensis eggs, but a small differential reduction in the eggshell thickness associated with the process of decay of the egg contents. This contrasts with the available evidence in Mycomorphoolithus, where more porous eggshells (category d) are in fact the thickest eggshells, similar to the evidence reported form C. latirostris (Fern
andez et al. 2013). The lack of complete eggs and the fragmentary condition of the sample, where the small size of the eggshell fragments precludes estimation of egg size and curvature, prevent us from determining whether variations in porosity are exclusively related to the incubation stage of the egg or are related to the location of the eggshell within the egg. In any case, all the localities that produce Mycomorphoolithus eggshells in significant numbers (Camino Canales 2, Menires and La Cantalera) yield eggshells at all four stages of pore opening development. This supports the notion that M. kohringi represents a single oospecies with important variations in the density and development of pore openings. The presence of incipient pore openings and dissolution pits in the eggshell surface suggest that degradation may have an important role in this process. Ensom (1997) in his initial studies in the Berriasian English materials previously reported Type 1 and Type 2 eggshells as a single eggshell type. We think that this interpretation is more plausible, and that Type 2 eggshells represent the final stage of pore development, as in the Iberian eggshells (category d), the eggshells reported as cf. Type 1by Ensom (2002) being an example of an early stage of eggshell degradation (category a) and Type 1 eggshells representing categories b and c.

625

5.3. Implications for the oological record of crocodylomorphs Crocodilian eggshells assigned to the Krokolithidae can be traced back to the Upper Jurassic (Hirsch, 1994b) and are common in Cretaceous oological assemblages (Buscalioni et al. 2008; Moreno-Azanza et al. 2014a) and during the Cenozoic (Hirsch, € hring and Hirsch 1996; Panade s, Blas and Patnaik, 2009). 1985; Ko All of this points towards a very conservative and efficient model of eggshell structure that has been mostly invariant during the last 160 million years (Marzola et al., 2015). These features predate the origin of modern crocodiles (Eusuchia; Martin et al., 2010). Nevertheless, Mesozoic crocodylomorphs were very diverse, and different lineages coexisted with the one that leads to modern crocodiles during the Cretaceous in Europe (Fig. 6). Mycomorphoolithus eggs were laid for at least most of the Early Cretaceous (Berriasian to Barremian). During this period, at least a handful of less derived taxa coexisted with lineages more closely related to eusuchians, such as atoposaurids, goniopholidids, an undetermined ziphodonts and the genus Bernissartia (Martin et al., 2010, Fig. 7). All of these taxa were present in the localities that yield Myco
rtolas-Pascual, morphoolithus eggshells (e.g. Canudo et al. 2010; Pue 2015). Without a direct association between oological and osteological remains, any relation between these taxa and Mycomorphoolithus is purely speculative, but it is important to note that possible candidates to have laid Mycomorphoolithus eggshells were present in Western Europe during the Early Cretaceous.

Fig. 6. Calibrated phylogeny of the principal clades of crocodylomorphs based on the cladogram presented by Martin et al. (2010), and distribution of the oological material referred to crocodylomorphs (based on data from Moreno-Azanza et al. and references within, and this work). Note that Krokolithidae eggshells precede the origin of Eusuchia, and persist through to present times. Abbreviations: B. Bauruoolithus fragilis. Kw. €hring and Hirsch, 1996. RC recent Krokolithes wilsoni; Kh. Krokolithes helleri Ko crocodiles.

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6. Conclusions We have erected a new oogenus and oospecies, M. kohringi, to include materials from different Lower Cretaceous (Barremian) localities in the Maestrazgo Basin, Spain. These were previously identified as chelonian or dinosaurian eggshells, but reexamination of the eggshell structure demonstrates that they do not exhibit any characters to support this assignation, other than a similar general appearance. M. kohringi presents a combination of characters that relates it to eggshells of modern and fossil crocodylomorphs, including a single layer of isolated shell units that fuse at the top of the eggshell, blocky extinction and a lack of organic cores. Nevertheless, we do not include it within the oofamily Krokolithidae, as we regard it as showing significant differences. Mycomorphoolithus eggshells have a very high density of pore openings, and the size of the pore openings varies greatly between eggshell fragments. This variation in the microstructural features of the eggshell has been regarded as an inter-oospecific variation in previous papers, but it is better explained by intra-oospecific variation, due to either differences between different areas of the eggs, to extrinsic degradation of the eggshell during embryo development or a combination of both factors. This extrinsic degradation is similar to that seem in modern alligatorids, were eggshell degrade during egg incubation. Eggshell studied by Ensom (1997, 2002) and identified as of the dinosaur-spherulitic morphotype from different localities of the Purbeck facies (Berriasian) is here assigned to Mycomorphoolithus sp. This oogenus occurs throughout for most of the Early Cretaceous, coexisting with Krokolithidae eggshells, which are more similar to the eggshells of modern crocodiles. Thus, the putative Mycomorphoolithus egg producer was probably not an eusuchian. Acknowledgements This paper is partially subsidized by the project CGL201453548-P of the Spanish Ministerio de Economía y Competitividad, the European Regional Development Fund, the Government of
n (“Grupos Consolidados” and “Direccio
n General de PatriArago monio Cultural”). M.M.A was supported by an FPI grant (BES-2008
n y Ciencia, J.M.G. 005538) from the Spanish Ministerio de Educacio was supported by an FPI grant (B064/08B) from the Government of
n. The authors would like to acknowledge the use of the Arago
n-SAI, Universidad de Servicio General de Apoyo a la Investigacio Zaragoza with special thanks to Cristina G
allego, who took the SEM images. Cathodoluminescence images were taken in the Institut  d'Arqueologia Cla ssica, Tarragona, Spain by Hernando Royo Catala Plumed. Dr. Grellet-Tinner was the first to point out the possible crocodilian affinities of Mycomorphoolithus at an MTE meeting back in 2009. Rupert Glasgow edited the text in English. We thank
vio Mateus, Museu da Lourinha ~, Portugal and an anonymous Octa reviewer for his comments, that greatly improved our original €t Heidelsubmission. We thank Eduardo Koutsoukos (Universita berg, Heidelber) for his editorial work and helpful suggestions. References
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