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Year: 2019

A new fossil-Lagerstätte from the Late Devonian of Morocco : faunal composition, taphonomy and paleoecology

Frey, Linda

Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-177848 Dissertation Published Version

Originally published at: Frey, Linda. A new fossil-Lagerstätte from the Late Devonian of Morocco : faunal composition, taphon- omy and paleoecology. 2019, University of Zurich, Faculty of Science.

A New Fossil-Lagerstätte from the Late Devonian of Morocco: Faunal Composition, Taphonomy and Palaeoecology

Dissertation

zur

Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.)

vorgelegt der

Mathematisch-naturwissenschaftlichen Fakultät

der

Universität Zürich

von

Linda Frey

von

St. Ursen FR

Promotionskommission

Prof. Dr. Christian Klug (Leitung der Dissertation)

Prof. Dr. Hugo Bucher

Prof. Dr. Marcelo Sánchez

Prof. Dr. Michael Coates

Dr. Martin Rücklin

Zürich, 2019

ABSTRACT ...... 2

INTRODUCTION...... 5

CHAPTER I Late Devonian and Early Carboniferous alpha diversity, ecospace occupation, vertebrate assemblages and bio-events of southeastern Morocco ...... 27

CHAPTER II Fossil-Lagerstätten and preservation of invertebrates and vertebrates from the Devonian in the eastern Anti-Atlas (Morocco) ...... 61

CHAPTER III Morphology, phylogenetic relationships and ecomorphology of the early elasmobranch Phoebodus ...... 89

CHAPTER IV Functional morphology of mandibular arches in symmoriids as exemplifi ed by Ferromirum oukherbouchi gen. et sp. nov. (Late Devonian) ...... 135

CONCLUSIONS ...... 167

APPENDIX

Appendix A Collaboration with other projects (abstracts) ...... 171

Appendix B Additional article published during doctoral studies ...... 175

ACKNOWLEDGEMENTS ...... 203

CURRICULUM VITAE ...... 207 Abstract

The Late Devonian (382.7 to 358.9 Ma) was a period of intense environmental perturbations and fun- damental changes in marine ecosystems impacting also the marine vertebrates. Two extinction events, namely the Kellwasser Event (Frasnian-Famennian boundary) and the Hangenberg Crisis (latest Devoni- an) caused severe losses in diversity. Especially several groups of gnathostomes were strongly affected by the Hangenberg Crisis, which represents a bottleneck in the evolutionary history of jawed vertebrates. The marine ecosystem became reshaped and the previously diverse placoderms went extinct and the taxonomic diversity of acanthodians decreased, while other chondrichthyans and osteichthyans diversifi ed. From the stratigraphic interval between the Kellwasser and the Hangenberg crises, well-preserved remains of plac- oderms and isolated teeth were well documented from Morocco before. By contrast, articulated remains of chondrichthyans were discovered only recently from the Famennian of the Maïder region (Morocco) within this PhD project. Most fossil fi sh were found in a stratigraphic interval with abundant remains of thylacocephalan arthropods preserved in ferruginous nodules (early/ middle Famennian Thylacocephalan Layer). These gnathostomes include both known and new taxa of sarcopterygians (onychodontids), plac- oderms (Dunkleosteus, Titanichthys, Alienacanthus and Driscollaspis) and chondrichthyans (phoebodon- tids, symmoriids, and several new cladodont chondrichthyans). In the framework of this thesis, the remains of chondrichthyans were in the main focus because their skeletons are rarely preserved in the fossil record due to the fragility of their cartilaginous skeletons. The Famennian chondrichthyans of the Maïder region often preserve three-dimensional skulls, the visceral as well as postcranial skeleton (pectoral and pelvic girdles with articulated fi ns, dorsal fi ns with fi n spines, neural arches and sometimes the caudal fi n) and even mineralized soft-tissues (muscles, liver, digestive tract). Therefore, the discovery of such remains of Devonian chondrichthyans is of importance to examine their phylogenetic relationships, their morpholog- ical disparity and to reconstruct their ecological diversity including changes in the respective ecological roles of these vertebrate groups in the marine ecosystems.

In chapter I, the palaeoenvironment of the gnathostome-bearing stratigraphic interval of the Maïder was quantitatively investigated by analysing the diversity and palaeocology of the accompanying inverte- brate faunas. For this purpose, 21 invertebrate associations from early Famennian to early Carboniferous age of the Maïder region (17 from Madene el Mrakib, four from Aguelmous) were sampled and deter- mined. Based on the composition of these associations, alpha diversity (changes in species richness at a single locality through time), ecospace occupation (three-dimensional modes of life including tiering, motility, and feeding mode) and trophic nucleus (dominant taxa of each association) were analysed. The species richness, ecospace occupation as well as the ratio between pelagic and benthic organisms were fl uctuating during the Famennian and Tournaisian. Those ecological changes correlate with numerous bio-events coinciding with fl uctuating global and/ or regional sea level and changes in oxygenation during the Devonian. Although the sea fl oor might have been a bit better oxygenated (extended ecospace includ- ing benthic modes of life) in some stratigraphic intervals, the Fammennian of the study area was mostly hypoxic to dysoxic because of the low taxonomic diversity of benthic invertebrates and the dominance of pelagic or benthic taxa tolerant to oxygen depletion. This is supported by the absence of benthic gnatho- stomes in the Maïder (including microremains).

The taphonomy of the gnathostomes of the Famennian Thylacocephalan Layer and some other Devo- nian Fossillagerstätten was investigated in Chapter II. The mineral composition of the remains of gnatho- stomes, thylacocephalans and some other invertebrates from various localities were analysed by Raman spectroscopy and X-ray diffraction. To understand the genesis of the Famennian Fossillagerstätten, the mineral analyses were combined with the current knowledge of the palaeogeography and palaecology of the Maïder region. The fossils mainly contain iron oxides (oxidised pyrite) and phosphates. The Maïder was a basin isolated by land and two submarine ridges (Tafi lalt and Maïder Platform) from neighbouring basins, which limited water exchange and thus also oxygen supply during the Devonian. This palaeogeo- graphic setting in combination with the mineral composition of the fossils, the soft-tissue preservation and the low abundance of benthos (even a complete lack of benthic chondrichthyans), the Thylacocephalan Layer with exceptionally well-preserved chondrichthyans represents the fi rst Konservat-Lagerstätte (con- servation deposit) of the Devonian of North Africa.

In chapter III, the morphology and palaeoecology of Phoebodus, a common and cosmopolitan chon- drichthyan from the Devonian (Givetian to Famennian), previously only known from isolated teeth, is

2 Abstract described. Phoebodus saidselachus sp. nov. of the Famennian of the Maïder region is the fi rst specimen of this genus preserving body, soft-tissue and skull remains. Its body and skull are slender and more elongate than those of other Palaeozoic chondrichthyans. Phylogenetic analyses based on a data matrix including 228 characters of 65 taxa and one outgroup taxon place Phoebodus saidselachus sp. nov. within the stem elasmobranchs. Therefore, the Devonian genus Phoebodus is the oldest stem elasmobranch with an elon- gate body shape. Other stem elasmobranchs with such body shapes are known from younger strata such as the phoebodontid Thrinacodus gracia from the Carboniferous of Bear Gulch and several taxa of xenacan- thids from the Permian. Therefore, chondrichthyans were morphologically and ecologically more diverse in the Devonian before the vertebrate bottleneck of the Hangenberg Crisis than previously thought.

Chapter IV focuses on the jaw function of symmoriiform chondrichthyans. Although the fossil re- cord of Palaeozoic chondrichthyans improved in recent years, the functional morphology of anatomical elements such as the visceral skeleton are not known in detail due to the often fragmentary or deformed preservation. For example, there was a long debate about whether hyoids had a suspensory function or not (aphetohyoidean hypothesis) in symmoriids. The newly discovered chondrichthyan Ferromirum oukher- bouchi gen. et sp. nov. from the Maïder Basin has exceptionally well-preserved and undeformed mandib- ular and branchial arches. The remains of the specimen were three-dimensionally reconstructed on the basis of CT-scans using the 3D reconstruction software Mimics. 3D-prints of the virtually reconstructed specimen allowed to mechanically examine the function of the mandibular and branchial arches. Due to the arrangement of the hyoids and jaws, it can be confi rmed that the hyoids had a suspensory function (aphetohyoidean hypothesis falsifi ed). Moreover, because of the confi guration of the jaw-articulation, the lower jaws performed a lateral and outward rotation when the chondrichthyan opened its mouth. As a result of this movement, the predatory success was probably improved since a greater portion of the dentition becomes functional than previously thought. This kind of jaw function is not known from recent chon- drichthyans and possibly vanished with the extinction of the symmoriids.

As general conclusion, the Famennian Konservat-Lagerstätten of the Maïder Basin bear abundant remains of various early gnathostomes and thylacocephalans. These gnathostomes were fossilized under oxygen depleted conditions on the sea fl oor of the Maïder Basin as corroborated by 1) the preservation in ferruginous nodules, 2) by the low diversity of accompanying benthic invertebrate, 3) by the domi- nance of taxa living in the water column (both invertebrates and vertebrates) and 4) the co-occurrence of benthic taxa tolerant to anoxic to dysoxic conditions. The two newly described taxa of chondrichthyans (Phoebodus saidselachus sp. nov and Ferromirum oukherbouchi gen. et sp. nov.) yielded new data on the morphology, phylogeny, diversity and functional morphology of Devonian chondrichthyans. Considering that much more taxa of early gnathostomes were discovered than presented here, the Famennian Konser- vat-Lagerstätten of the Maïder are of great importance to further study disparity and diversity trends of these early vertebrates as well as their ecology and evolution in the future.

3

INTRODUCTION

Introduction

Devonian Period: an overview Earth`s history (Fig. 2B). The placoderms had a characteristic bony armor consisting of thick der- The Devonian (~419 to 259 Ma years) is the third mal plates in the head and thorax region while period of the Palaeozoic. It is subdivided into four their tail was naked or covered by scales and they epochs and seven stages: the Early (Lochkovian, were roaming the waters for around ~120 Ma Pragian, Emsian), Middle (Eifelian, Givetian) and years (Silurian to Devonian; Long & Trinajstic Late (Frasnian, Famennian) Devonian (Cohen et 2010). ‘Acanthodians’ persisted longer (Silurian al. 2013, updated 2018). At this time, two main to Permian) than the placoderms and they include continents persisted: the larger continent Gond- small chondrichthyans exhibiting usually several wana south of the equator and Euamerica (also pairs of fi ns that usually carry spines, hence the known as Laurussia), which was situated north- name (Hanke et al. 2001; Karatajute-Talimaa & east of Gondwana (Scotese 2001; Fig. 1A). The Smith 2002; Burrow 2003, Denison 1979). Their two continents were separated from each other by phylogenetic relationships within the group and the Palaeotethys and the Variscan Sea (Neugebau- to other fi sh groups are still not clarifi ed due to er 1988). The climate throughout the Devonian their fossil record of often complete but heavily was generally warm to tropical (30°C) interrupted fl attened fossils (Blais 2017). Most phylogenetic by a somewhat cooler period (23 to 25°C) during studies revealed them as a paraphyletic group of the Middle Devonian (Joachimski et al. 2009; Fig. stem chondrichthyans (Brazeau 2009; Davis et al. 1B). Towards the end of the Devonian, the climate 2012; Zhu et al. 2013; Giles et al. 2015; Long et cooled down for a second time (Joachimski & al. 2015; Burrow et al. 2016; Coates et al. 2017) Buggisch 2002). but some taxa might also represent stem osteich- Among others, the Devonian period is famous thyans (Brazeau 2009, Davis et al. 2012). for the rise of land plants, in particular the evolu- A fundamental step in evolution, namely the tion of vascular plants, and the establishment of transition from fi sh to tetrapod (four-limbed ver- the fi rst forest ecosystems (Rettalack 1997; Algeo tebrates) and thus from aquatic to terrestrial life and Scheckler 1998; Stein et al. 2012). In the ma- took place during the Devonian. Fossil bodies rine realm, the fi rst ammonoids with coiled shells of tetrapods and closely related tetrapodomorph evolved from the straight-shelled to slightly coiled fi shes are known from the Middle and Late De- bactritoids during the Early Devonian (Korn & vonian (e.g., Campbell & Bell 1977; Ahlberg Klug 2002). In the context of my thesis, howev- 1998; Ahlberg & Clack 2006; Ahlberg et al. 1994, er, it is the great evolutionary success of jawed 2005, 2008; Lebedev & Clack 1993; Lebedev & fi shes in that time. Accordingly, the Devonian Coates 1995; Zhu et al. 2002; Shubin et al. 2004; is also called the “Age of Fish” because various Daeschler et al. 2006). Tetrapodomorph fi shes groups of jawed fi sh (gnathostomes) radiated and such as the elpistostegalians are sarcopterygians established in the early marine and freshwater en- already exhibiting tetrapod-like characters in their vironments (Fig. 2A). Several of the main groups fi ns (e.g., Panderichthys in Boisvert et al. 2008; of gnathostomes survived until today such as sar- Clack 2012). This fact in combination with the copterygians (lobe-fi nned fi sh), actinopterygians mostly aquatic lifestyle of Devonian tetrapods in- (ray-fi nned fi sh), and chondrichthyans (cartilagi- cluding the famous Acanthostega and Ichthyoste- nous fi sh). By contrast, two important Devonian ga evidence the initial evolution of limbs from groups of gnathostomes such as the placoderms fi ns in aquatic environments (Coates 1996; Coates and ‘acanthodians’ (a probably paraphyletic & Clack 1995; Coates & Ruta 2007; Clack 2012). group of cartilaginous fi sh) vanished throughout

7 Introduction

Figure 1. Palaeogeography and temperature curve of the Devonian. A. Palaeomap shows continents and oceans of the Late Devonian (370 Ma years), modifi ed map from Deep Time Maps (Blakey 2016, https: // deeptimemaps.com). B. Temperature curve of the surface waters, adopted from Joachimski et al. (2009).

As mentioned above, the Devonian was a pe- latest Frasnian (Kellwasser Crisis; e.g., McGhee riod of early animal and plant radiation and of 1988; Buggisch 1991; McGhee 2001; Sandberg evolutionary key events such as the fi sh-tetrapod et al. 2002; Gereke & Schindler 2012) and at the transition. However, the Devonian ecosystem end-Famennian (Hangenberg Crisis; e.g., Caplan also faced several extinction events (Walliser & Bustin 1999; Kaiser et al. 2006, 2008, 2015; 1996; House 2002; Fig. 3). The most fundamental Carmichael et al. 2015; Becker et al. 2016). The changes in this early ecosystem occurred at the Kellwasser event strongly affected the marine

8 Introduction

Figure 2. Devonian groups of gnathostomes. A. Biodiversity through time, source: Benton (2005). B. Reconstructions of some early gnathostomes: 1. Bothriolepis, 2. Remigolepis, 3. Groenlandaspis, 4. Ho- loptychius, 5. Moythomasia, 6. Culmacanthus, 7. Akmonistion. Reconstructions are taken from Sampson (1956); Jessen (1968); Lauder & Liem (1983); Young (1989a, b, 2007); Long (1983, 1991); Cloutier & Schultze (1996); Coates & Sequeira (2001); Choo (2015). biodiversity, which is evident by the loss of about versity and the placoderms got extinct, chondrich- 72-80 % of all species (McGhee 2014). The Han- thyans and actinopterygians diversifi ed rapidly af- genberg Crisis is also regarded as a bottleneck ter the crisis (Sallan & Coates 2010). Causes for in vertebrate evolution as many habitats of ear- the changes in the environment and biodiversity ly vertebrates underwent fundamental changes: during the Late Devonian are still under debate. while sarcopterygians suffered a severe loss in di- Some possible causes are marine anoxia (Caplan

9 Introduction

Figure 3. The big fi ve mass-extinctions after Sepkoski (2002) are marked by red lines. During the Devoni- an, two major crises (Kellwasser and Hangenberg) shaped the early vertebrate biodiversity. Figure adopted from Friedman & Sallan (2012).

& Bustin 1999; Riquier et al. 2006), sea level fl uc- fi lalt platform with shallower water (Wendt 1985, tuations (Kaiser et al. 2006), global cooling (Joa- 1995; Wendt et al. 2006; Fröhlich 2004; Lubeseder chimski & Buggisch 2002), eutrophication (Al- et al. 2010; Fig. 4). From this region, many fossil geo & Scheckler 1998; Algeo et al. 1995, 2001) groups of marine animals have been documented. and decreased marine selenium level (Long et al. Particularly invertebrates are extremely abundant 2015). such as trilobites (e.g., Struve 1990; Klug et al. 2009; Chatterton and Gibb 2010), crinoids (e.g., Klug et al. 2003; Webster et al. 2005; Berkows- Devonian of Morocco ki & Klug 2012), brachiopods (e.g., Franchi et al. 2012; Halamski & Baliński 2013; Tessitore et al. Morocco can be regarded as a window into 2013; Sartenaer 1998, 1999, 2000), bivalves (e.g., Earth`s deep history because its outcrops yield Kříž 2000; Hryniewicz et al. 2017), and cepha- many geological, sedimentological and palaeon- lopods including ammonoids (e.g., Korn 1999; tological information about past ecosystems from Klug 2002; Klug et al. 2008; Klug et al. 2016; the Proterozoic to today. During the Devonian Becker 2002; Kröger 2008; De Baets et al. 2010, period, Morocco was situated at the northwestern 2012; Korn & Bockwinkel 2017; Korn et al. 2014, margin of Gondwana and a lot of its surface was 2015a, b, 2016a,b). Due to the high abundance covered by an epicontinental sea (Scotese 2002; and/ or exceptional preservation of macrofos- Dopieralska 2009). Exposed Devonian sediments sils, several localities could be actually regarded cover a large area of about 20000 km2, which as Fossillagerstätte (Frey et al. submitted, Chap- often bear highly fossiliferous strata (Kaufmann ter II). As far as vertebrates are concerned, their 1998). Some of the most famous regions for De- peak abundance is in the Late Devonian strata of vonian fossils are the Tafi lalt and the Maïder in the eastern Anti-Atlas. Previously, the record of the eastern Anti-Atlas. In these regions, two ma- articulated remains of Devonian vertebrates was rine basins (Tafi lalt and Maïder Basin) formed in limited to more or less complete body and skull the Palaeozoic, which were connected via the Ta- parts of placoderms and sarcopterygians (Leh-

10 Introduction

Figure 4. Topography and bathymetry of the Maïder and Tafi lalt area in the southeastern Anti-Atlas during the Late Devonian. Figure is adopted from Dopieralska (2009). mann 1956, 1964, 1976, 1977, 1978; Lelièvre & recognizable along with some smaller bio-events Janvier 1986, 1988; Lelièvre et al. 1993; Rücklin in the Late Devonian of Morocco (House 1985; 2010, 2011; Rücklin et al. 2015; Rücklin & Clé- Becker 1993; Hartenfels & Becker 2009, 2016a, ment 2017; Fig. 5 A-D, J). By contrast, actinopte- b). These events often coincided with dysaerobic rygians and chondrichthyans are rare and only fi n or anoxic conditions and/ or transgressions on a spines, teeth, scales and few remains of isolated regional scale (Wendt and Belka 1991; Kaiser et jaws were published (Termier 1936; Lehman al. 2015; Hartenfels 2011). The new material of 1976; Derycke 1992; Hampe et al. 2004; Dery- gnathostomes from the Maïder comes from this cke et al. 2008, 2014; Ginter et al. 2002; Klug environmentally unstable interval between the et al. 2016; Derycke 2017; Fig. 5E-I). Recently, Kellwasser and Hangenberg crises. For this rea- new material of Famennian (Late Devonian) plac- son, I also investigated changes in environmental oderms, sarcopterygians, actinopterygians and conditions, which affected the early gnathostomes chondrichthyans were found in the Maïder Basin faced in this marine basin in detail (Frey et al. (Frey et al. 2018, Chapter I, Fig. 6 A-D). In par- 2018; Chapter I). ticular, the chondrichthyans are well-preserved with sometimes three-dimensional skulls as well as more or less complete and articulated bodies. Palaeozoic chondrichthyans In this PhD project, I focused on these early chon- drichthyans because they bear a plethora of new Devonian chondrichthyans are characterized by anatomical, ecological and phylogenetic informa- a skeleton consisting of calcifi ed tessellated car- tion about this group (Chapter III and IV). tilage, multiple rows of teeth that are replaced throughout life and by a body often covered by Global mass extinction events such as the Kell- placoid scales. Extant chondrichthyans include wasser Crisis (latest Frasnian; Wendt and Belka the subclasses Elasmobranchii (sharks and rays; 1991) and the Hangenberg Crisis (end-Devoni- around 1100 species) and Holocephali (chimaeras; an; e.g. Korn et al. 2004; Kaiser et al. 2011) are

11 Introduction

Figure 5. Remains of Late Devonian gnathostomes from Morocco. A-D. Skull plates of the placoderm Driscollaspis pankowskiorum Rücklin et al., 2015, dorsal (A-B) and lateral (C-D) views, scale bar = 5 cm. E-F. Teeth of Phoebodus gothicus Ginter, 1990, scale bar = 0.5 mm. G. Symphyseal tooth-whorl of an acanthodian, scale bar = 0.5 mm. H-I. Teeth of actinopterygians, scale bar = 100 μm. J. Teeth and jaw remains of onychodontid sarcopterygian. Sources of fi gures: A-D.: Rücklin et al. (2015); E-G.: Ginter et al. (2002); H-I.: Derycke et al. (2008); J: Lehmann (1976). around 50 species; Compagno et al. 2005). Some cepted as remains of chondrichthyans are the teeth of the oldest known putative remains of chon- of Leonodus from the Early Devonian (Mader drichthyans are scales from the Llandovery (Silu- 1986, Fig. 7B). First skeletons of stem chondrich- rian) of Central Asia: e.g., Mongolepis, Teslepis, thyans were documented from the Early/Middle Sodolepis, Udalepis, Xinjiangichthys, Shiqianole- Devonian; these fi nds comprise braincases with pis, Elegestolepis and Tuvalepis (Karatajūtė-Tali- parts of the visceral skeleton of Doliodus (Miller maa 1973, 1995; Karatajūtė-Talimaa et al. 1990; et al. 2003; Maisey et al. 2009, 2017; Fig. 8A, B), Karatajūtė-Talimaa & Novitskaya 1992; Novits- Pucapampella (Janvier & Suárez-Riglos, 1986, kaya & Karatajūtė-Talimaa 1986; Zhu 1998; San- Maisey & Anderson 2001), Gladbachus (Heidtke som et al. 2000; Žigaitė & Karatajūtė-Talimaa & Krätschmer 2001; Coates et al. 2018; Fig. 8C, 2008). Probably even older chondrichthyan scales D) and Anarctilamna (Young 1982). from the Ordovician were reported such as Tan- From the Famennian (Late Devonian) on- talepis and Areyongalepis (Sansom et al. 1996, wards, remains of chondrichthyans become more 2012; Young 1997, 2000; Fig. 7A). abundant although many discoveries mainly in- The oldest remains that are more widely ac- clude isolated fi n spines (e.g., ctenacanthids;

12 Introduction

Figure 6. Late Devonian localities in the Maïder region bearing remains of gnathostomes. A. Madene el Mrakib, B. Bid er Ras, C. Shivering layer contains nodules with thylacocephalan arthropods and gnatho- stomes, D. Fin remains of a chondrichthyan in the fi eld.

Maisey 1981, 1982a, 1984a) and teeth of, e.g., spines and teeth arranged in several tooth fi les Omalodontiformes Turner, 1997, Protacrodon- (e.g. Dean 1894A, 1909; Bendix-Almgreen 1975; toidea Zangerl, 1981 and Orodontiformes Zangerl, Harris 1938a, b; Maisey 1989b, 2007; Schaeffer 1981 (Ginter et al. 2010). One of the most famous 1981; Williams 2001; Woodward & White 1938). and best documented Famennian chondrichthyan These early chondrichthyans were assigned to known from complete and articulated skeletons is elasmobranchs for a long time but recent stud- Cladoselache Dean, 1894A from the Cleveland ies provided evidence that Cladoselache is more Shales of Ohio, USA. Cladoselache has a shark- closely related to holocephalans (Coates et al. like morphology including a torpedo-shaped 2017; Fig. 9A, 9E). Coates et al. (2017) assigned body with a crescent outlined caudal fi n, paired another common and divers Palaeozoic group of pectoral and pelvic fi ns, two dorsal fi ns with fi n chondrichthyans, namely the Symmoriiformes

13 Introduction

1984, 1990; Zangerl & Case 1986; Williams 1985; Fig. 9F-H). A so-called spine-brush complex is present in Stethacanthus and Akmonistion, which consists of an anterior spine and posteriorly of a brush out of globular calcifi ed cartilage covered by large spiny scales (Coates et al. 1998; Coates & Sequeira 2001). Instead of this spine-brush complex, Falcatus and Damocles dorsally have a hook-like appendage (Lund 1985, 1986). Because such structures are absent in modern chondrich- thyans, their function is not yet known. The spine- brush complex may speculatively have served to scare off predators due to the resemblance of this complex to a large, opened mouth (Zangerl, 1984). This interpretation appears doubtful be- cause the spine-brush complex and the hooks are only found in male specimens and it appears more plausible that they played a role in mating (Lund 1985; Coates et al. 1998). The affi nity of sym- moriids to holocephalans is further supported by anatomical details seen in a three-dimensionally preserved braincase of Dwykaselachus oosthui- Figure 7. Putative scales and teeth of earliest zeni Oelofsen 1986 by Coates et al. (2017): this chondrichthyans. A. Scales of Tantalepis gate- specimen shows chimaeroid-like character states housei Sansom et al., 2012 from the Ordovician, such as, for example, an elevated midbrain cham- scale bar = 50 μm. B. Teeth of Leonodus carlsi ber, large orbits and a similarly arranged otic lab- Mader, 1986 from the early Devonian, scale bar = yrinth (Coates et al. 2017). In the Famennian of 0.5 mm. Source of picture: Sansom et al. (2012) Morocco, we discovered well-preserved remains and Ginter et al. (2010). of two new taxa of symmoriids that give new in- sights into the ecology of the entire group (Frey et Zangerl, 1981, to the holocephalans. Symmoriid al. in prep., Chapter IV) . chondrichthyans persisted from the Devonian to the Permian and exhibit symplesiomorphies such Another group of holocephalans that get some as a whip-like structure connected to the metapte- attention are the Eugeneodontiformes that were rygium of both pectoral fi ns, a reduced fi rst dorsal abundant during the Permian and Triassic (Zan- fi n and reduced or specialized dorsal fi n spines gerl 1981). Their tooth whorls are planispirally ar- (e.g. Zangerl 1981; Lund 1985, 1986; Coates & ranged forming sometimes a saw-blade like denti- Sequeira 2001). In Cobelodus Cope, 1893, Sym- tion such as in Edestus and Helicoprion (Ginter et morium and Denaea Zangerl, 1981, the anterior al. 2010; Fig. 10). Both taxa might have used the of the two dorsal fi ns and the dorsal fi n spines are tooth whorls for slashing medium-sized to large absent while Falcatus, Damocles, Stethacanthus prey (Itano 2014, 2015, 2018). Generally, holo- and Akmonistion exhibit a derived structure at the cephalans were taxonomically and ecologically position of the anterodorsal fi n (Zangerl 1981, more divers during the Palaeozoic than today and many different groups have been documented

14 Introduction

Figure 8. Stem chondrichthyans of Early and Middle Devonian age. A-B. Fossil remains and illustration of Doliodus problematicus Miller et al., 2003, scale bar = 1 cm. C-D. Threedimensional reconstruction of Gladbachus adentatus Heidtke and Krätschmer, 2001 based on computer tomographs, scale bar = 5 cm. Abbreviations: bhy, basihyal; bbra; anterior basibranchial; bbrp, posterior basibranchial; cbr, cerato- branchials (I-V?); chy, ceratohyal; hb, hypobranchial; mc, Meckel’s cartilage; mmd, location of mucous membrane denticles on counterpart; na, neural arches; nc, neurocranium; or, orbital ring; pop, postorbital process; pq, palatoquadrate; pfs, pectoral fi n-spines; rad, radials; sco, scapulocoracoid; sp, partial spines; sym, symphysis; tth, area with in situ teeth; thf, in situ tooth family. Figures adopted from Miller et al. (2003) and Coates et al. (2018). from the Carboniferous of the Bear Gulch Lime- tids, xenacanthids, hybodontids and ctenacanthids stone in Montana, USA (Lund & Grogan 1997; are locally quite common and thus the best docu- Lund et al. 2012, 2015). mented. Previously, phoebodontids, a nearly cos- mopolitan group, were known by a great number Compared to holocephalans, fewer groups of of isolated teeth and by articulated skeletons of a Palaeozoic elasmobranchs were discovered so far. single species, namely Thrinacodus gracia (Gro- Among those, representatives of the phoebodon- gan and Lund, 2007) (Ginter et al. 2010; Fig. 11).

15 Introduction

Figure 9. Phylogeny and some representatives of early chondrichthyans. A. phylogenetic relationships of early and some extant chondrichthyans adopted from Coates et al. (2018), red: stem chondrichthyans, blue: elasmobranchs, yellow; holocephalans. B. Onychoselache traquairi (Dick, 1978), C. Squalus sp., D. Triodus sessilis, E. Cladoselache Dean, 1894A, F. Akmonistion zangerli Coates and Sequeira, 2001, G. Cobeldodus Cope, 1893 H. Falcatus falcatus Lund, 1985. Reconstructions: B. Coates & Gess (2007); C-D. Schaeffer & Williams (1977); E. Schaeffer (1967); F. Coates & Sequeira (2001); G. Zangerl and Case (1976); H. Lund (1985).

However, the very common genus Phoebodus was the Famennian of the Maïder region in Morocco solely known by their widespread characteristic (Frey et al. in prep., Chapter III). tricuspid teeth and isolated putative fi n spines in Xenacanthids are rather closely related to spite of its rather cosmopolitan distribution during phoebodontids and their remains have been doc- the Middle and Late Devonian (Ginter et al. 2002; umented from Late Devonian to Triassic occur- 2010). Recently, we found the fi rst remains of ar- rences (Ginter et al. 2010, Frey et al. in prep., ticulated skulls and postcrania of Phoebodus in

16 Introduction

Figure 10. Helicoprion bessonowi Karpinsky, 1899A, tooth spiral, scale bar = 5 cm. Source of picture: Ginter et al. (2010).

Figure 11. The phoebodontid Thrinacodus gracia (Grogan & Lund, 2008) from the Carboniferous of Bear Gulch, Montana. Scale bar = 5 cm. Picture taken from Grogan & Lund (2008).

Chapter III). They had an elongated body with a (Maisey 1984b; Maisey et al. 2004; Coates & dorsal fi n extending along the entire body length, Gess 2007; Fig. 9A). The hybodonts are a group a dorsal cranial spine and diplodont teeth (crown that persisted from the Devonian to the Creta- with two long lateral cusps and a reduced medi- ceous (Mesozoic). They show derived conditions an cusp; Dick 1981; Heidtke 1982, 1999; Hot- in many parts of their skeleton compared to oth- ton 1952; Schaeffer 1981; Solér-Gijon & Hampe er early elasmobranchs. In addition to many dif- 1998; Hampe 2003; Heidtke et al. 2004; Fig. 9D). ferences in the braincase, their shoulder girdle is similar to that of extant elasmobranchs (Fig. 9B); A group of early chondrichthyans that is phy- the pectoral fi ns have a tribasal arrangement (bas- logenetically most closely related to the Neosela- al elements are separated into propterygium, me- chii (modern sharks and rays) are the hybodonts sopterygium and metapterygium); a puboischiad-

17 Introduction ic bar (left and right halves of the pelvic girdle land plants and weathering regimes. In Gensel, P. are fused) is present; the palatoquadrate is not the G., Edwards, D. (Eds.), Plants invade the land. Co- lumbia University Press, New York, pp. 213-237. cleaver-shaped (instead they have a lateral quad- Becker, R. T., 1993. Anoxia, eustatic changes, and Up- rate fl ange); and labial cartilages are present (e.g. per Devonian to lowermost Carboniferous global Dick 1978; Dick & Maisey 1980; Maisey 1982b, ammonoid diversity, in: House, M. R. (Ed.), The 1983, 1987, 1989; Maisey and de Carvalho 1997; Ammonoidea: environment, ecology, and evolu- tionary change. Systematic Association Special Coates & Gess 2007; Lane 2010; Lane & Maisey Volume 47, 115-164. 2009, 2012; Coates & Tietjen 2018). Becker, R. T., House, M. R., Bockwinkel, J., Ebbighau- sen, V., and Aboussalam, Z. S., 2002. Famennian In this thesis, I focus on two groups of chon- ammonoid zones of the eastern Anti-Atlas (south- drichthyans, namely the phoebodontids and sym- ern Morocco). Münstersche Forschungen zur Geo- logie und Paläontologie, 93, 159-205. moriids. The recently discovered material of these Becker, R. T., Kaiser, S. I., Aretz, M., 2016. Review of two groups of the Devonian of Morocco yields chrono-, litho- and biostratigraphy across the glob- important information about the phylogenetic al Hangenberg Crisis and Devonian-Carboniferous relationships and ecomorphological disparity of Boundary. Geological Society, London, Special Publications 423(1), 355386. some of the earliest chondrichthyans. Bendix-Almgreen, S. E., 1975. The paired fi ns and shoulder girdle in Cladoselache, their morphology and phyletic signifi cance. Colloques internatio- naux Centre national de la recherche scientifi que References (France), 111-123. Ahlberg, P. 1998. Postcranial stem tetrapod remains Benton, M. J., 2005. Vertebrate Palaeontology, Black- from the Devonian of Scat Craig, Morayshire, well, 3rd edition. Scotland. Zoological Journal of the Linnean Soci- ety, 122, 99-141. Berkowski, B., and Klug, C., 2012. Lucky rugose cor- als on crinoid stems: unusual examples of subep- Ahlberg, P. E., and Clack, J. A. 2006. Palaeontology: idermal epizoans from the Devonian of Morocco. a fi rm step from water to land. Nature, 440(7085), Lethaia, 45(1), 24-33. 747. Blais, S. A., 2017. Precise occlusion and trophic niche Ahlberg, P. E., Clack, J. A., and Blom, H. 2005. The differentiation indicate specialized feeding in Early axial skeleton of the Devonian tetrapod Ichthyoste- Devonian jawed vertebrates. Facets, 2(1), 513530. ga. Nature, 437, 137-140. Boisvert, C. A., Mark-Kurik, E., and Ahlberg, P. E., Ahlberg, P. E., Clack, J. A., Luksevics, E., Blom, H., 2008. The pectoral fi n of Panderichthys and the or- and Zupins, I. 2008. Ventastega curonica and the igin of digits. Nature, 456, 636-638. origin of tetrapod morphology. Nature, 453, 1199- 1204. Brazeau, M.D., 2009. The braincase and jaws of a De- vonian ‘acanthodian’ and modern gnathostome ori- Ahlberg, P. E., Luksevics, E., and Lebedev, O. 1994. gins. Nature, 457, 305308. The fi rst tetrapod fi nds from the Devonian (Upper Fammenian) of Latvia. Philosophical Transactions Buggisch, W., 1991. The global Frasnian-Famenni- of the Royal Society of London, B343, 303-328. an “Kellwasser Event”. Geologische Rundschau, 80(1), 4972. Algeo, T. J., Berner, R. A., Maynard, J. B., Scheckler, S. E., 1995. Late Devonian oceanic anoxic events Burrow, C.J., 2003. Redescription of the gnathostome and biotic crises: ‘rooted’ in the evolution of vascu- fi sh fauna from the mid-Palaeozoic Silverband For- lar plants. GSA Today, 5, 63-66. mation, the Grampians, Victoria. Alcheringa: An Australasian Journal of Palaeontology, 27, 37-49. Algeo, T. J., Scheckler, S. E., 1998. Terrestrial-marine doi:10.1080/03115510308619543. teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and Burrow, C.J., den Blaauwen, J., Newman, M., and marine anoxic events. Philosophical Transactions Davidson, R., 2016. The diplacanthid fi shes (Ac- of the Royal Society of London B, 353, 113-130. anthodii, Diplacanthiformes, Diplacanthidae) from the Middle Devonian of Scotland. Palaeontologia Algeo, T. J., Scheckler, S. E., Maynard, J. B., 2001. Ef- Electronica 19.1.10A, 1-83, palaeo-electronica.org/ fects of Middle to Late Devonian spread of vascular content/2016/1398-scottish-diplacanthid-fi shes.

18 Introduction

Campbell, K. S. W., and Bell, M. W., 1977. A primitive drichthyan braincase and the origin of chimaeroid amphibian from the Late Devonian of New South fi shes. Nature, 541(7636), 208. Wales. Alcheringa, 1, 369-381. Coates, M. I., and Ruta, M., 2007. Skeletal changes Caplan, M. L., Bustin, R. M., 1999. Devonian-Carbon- in the transition from fi ns to limbs. In Hall, B. K. iferous Hangenberg Mass extinction event, wide- (ed.). Fins into Limbs: Evolution, Development, spread organic-rich mudrock and anoxia: causes and Transformation. University of Chicago Press, and consequences. Palaeogeography, Palaeocli- Chicago, pp. 15-37. matology, Palaeoecology, 148, 187207. Coates, M. I., Sansom, I. J., and Smith, M. M., 1998. Carmichael, S. K., Waters, J. A., Batchelor, C. J., Cole- Spines and tissues of ancient sharks. Nature, 396, man, D. M., Suttner, T. J., Kido, E., McCain Moore, 729-730. L., Chadimová, L., 2015. Climate instability and Coates, M. I., and Sequeira, S. E. K., 2001. A new tipping points in the Late Devonian: Detection of stethacanthid chondrichthyan from the Lower Car- the Hangenberg Event in an open oceanic island arc boniferous of Bearsden, Scotland. Journal of Verte- in the Central Asian Orogenic Belt. Gondwana Re- brate Paleontology, 21, 754-766. search, 32, 213231. Coates, M. I., and Tietjen, K., 2018. The neurocranium Chatterton, B. D., and Gibb, S. 2010. Latest Early to of the Lower Carboniferous shark Tristychius ar- early Middle Devonian trilobites from the Erben- cuatus (Agassiz, 1837). Earth and Environmental ochile bed, Jbel Issoumour, southeastern Morocco. Science Transactions of the Royal Society of Edin- Journal of Paleontology, 84(6), 1188-1205. burgh, 108(1), 19-35. Choo, B., 2015. A New Species of the Devonian Ac- Cohen, K.M., Finney, S.C., Gibbard, P.L. and Fan, tinopterygian Moythomasia from Bergisch Glad- J.X., 2013 (updated 2018). The ICS International bach, Germany, and Fresh Observations on M. Chronostratigraphic Chart. Episodes, 36, 199-204. durgaringa from the Gogo Formation of Western Australia. Journal of Vertebrate Paleontology, Compagno, L., Dando, M., and Fowler, S., 2005. 35(4). http://www.bioone.org/doi/full/10.1080/027 Sharks of the World. 368 pp. Princeton University 24634.2015.952817 Press (Princeton and Oxford). Clack, J. A., 2012. Gaining Ground: The Origin and Cope, E. D., 1893. On Symmorium and the position Evolution of Tetrapods. 2nd edition, Indiana Uni- of the cladodont sharks. American Naturalist, 27, versity Press, Bloomfi eld, IN, 523 p. 999-1001. Cloutier, R., and Schultze, H.P., 1996. Porolepiform Daeschler, E. B., Shubin, N. H., and Jenkins, F. A., Jr., fi shes (Sarcopterygii). In: Schultze H-P. and Clout- 2006. A Devonian tetrapod-like fi sh and the evolu- ier R. (eds.) Devonian Fishes and Plants of Migua- tion of the tetrapod body plan. Nature, 440, 757- sha, Quebec, Canada, pp. 248 – 270, Verlag Dr. 763. Friedrich Pfeil, München. Davis, S.P., Finarelli, J.A., and Coates, M.I., 2012. Ac- Coates, M. I., 1996. The Devonian tetrapod Acantho- anthodes and shark-like conditions in the last com- stega gunnari Jarvik: Postcranial anatomy, basal mon ancestor of modern gnathostomes. Nature, tetrapod relationships and patterns of skeletal evo- 486, 247- 250. lution. Transactions of the Royal Society of Edin- Dean, B. 1894A. A new cladodont from the Ohio Wa- burgh: Earth Sciences, 87, 363-421. verly, Cladoselache newberryi n. sp. Transactions Coates, M. I., and Clack, J. A., 1995. Romer’s gap: Tet- of the New York Academy of Sciences, 13, 115-119. rapod origins and terrestriality. Bulletin du Museum Dean, B., 1894. Contributions to the morphology of National d’Histoire Naturelle, 4(17), 373-388. Cladoselache (Cladodus). Journal of Morphology, Coates, M. I., Finarelli, J. A., Sansom, I. J., Andreev, P. 9(1), 87-114. S., Criswell, K. E., Tietjen, K., and La Riviere, P. J., Dean, B., 1909. Studies on fossil fi shes (sharks, chi- 2018. An early chondrichthyan and the evolution- maeroids and arthrodires. Memoirs of the American ary assembly of a shark body plan. Proceedings of Museum of Natural History, 9(5), 1-287. the Royal Society B, 285(1870), 20172418. De Baets, K., Klug, C., and Monnet, C. 2013. Intra- Coates, M. I., and Gess, R. W., 2007. A new recon- specifi c variability through ontogeny in early am- struction of Onychoselache traquairi, comments monoids. Paleobiology, 39(1), 75-94. on early chondrichthyan pectoral girdles and hy- bodontiform phylogeny. Palaeontology, 50(6), De Baets, K., Klug, C., and Plusquellec, Y. 2010. 1421-1446. Zlíchovian faunas with early ammonoids from Mo- rocco and their use for the correlation of the eastern Coates, M. I., Gess, R. W., Finarelli, J. A., Criswell, Anti-Atlas and the western Dra Valley. Bulletin of K. E., & Tietjen, K., 2017. A symmoriiform chon-

19 Introduction

Geosciences, 85(2), 317-352. million years of extinction and recovery: a Pha- nerozoic survey of large scale diversity patterns in Denison, R.H., 1979. Handbook of paleoichthyol- fi shes. Palaeontology, 55(4), 707-742. ogy, Part 5: Acanthodii. Gustav Fischer Verlag, - Stuttgart, Germany. 222 p. Fröhlich, S. 2004. Evolution of a Devonian carbonate shelf at the northern margin of Gondwana (Jebel Derycke, C., 1992. Microrestes de Sélaciens et autres Rheris,eastern Anti-Atlas, Morocco). Unpublished Vertébrés du Dévonien supérieur du Maroc. Bulle- PhD Thesis, University of Tübingen, Germany. tin du Muséum national d’Histoire Naturelle, Sec- tion C, Sciences de la terre, paléontologie, géolo- Gereke, M., Schindler, E., 2012. “Time-specifi c facies” gie, minéralogie 14 (1), 15-61. and biological crisis - the Kellwasser event inter- val near the Frasnian/Famennian boundary (Late Derycke, C., 2017. Paléobiodiversité des gnathos- Devonian). Palaeogeography, Palaeoclimatology, tomes (chondrichthyens, acanthodiens et actinopté- Palaeoecology, 367, 19-29. rygiens) du Dévonien du Maroc (NW Gondwana), in: Zouhri, S. (ed), Paléontologie des vertébrés du Giles, S., Friedman, M., and Brazeau, M. D., 2015. Os- Maroc: état des connaissance, Mémoires de la So- teichthyan-like cranial conditions in an Early De- ciété Géologique de France 180, p. 624. vonian stem gnathostome. Nature, 520(7545), 82. Derycke, C., Olive, S., Groessens, E., Goujet, D., Ginter, M., 1990. Late Famennian shark teeth from the 2014. Paleogeographical and paleoecological con- Holy Cross Mts, Central Poland. Acta Geologica straints on Paleozoic vertebrates (chondrichthyans Polonica, 40, 69-81. and placoderms) in the Ardenne Massif Shark ra- Ginter, M., Hairapetian, V., and Klug, C., 2002. diations in the Famennian on both sides of the Pa- Famennian chondrichthyans from the shelves of laeotethys. Palaeogeography, Palaeoclimatology, North Gondwana. Acta Geologica Polonica, 52(2), Palaeoecology 414, 61-67. 169215. Derycke, C., Spalletta, C., Perri, M. C., Corradini, C., Ginter, M., Hampe, O., and Duffi n, C. J., 2010. Chon- 2008. Famennian chondrichthyan microremains drichthyes: Paleozoic Elasmobranchii: teeth, in: from Morocco and Sardinia. Journal of Paleontol- Schultze, H. (Ed.), Handbook of Paleoichthyology, ogy 82(5), 984995. 3D, 168 p. Dick, J. R. R., 1978. On the Carboniferous shark Tristy- Grogan, E. D., and Lund, R., 2008. A basal elas- chius arcuatus Agassiz from Scotland. Transaction mobranch, Thrinacoselache gracia n. gen and of the Royal Society of Edinburgh, 70, 63-109. sp.,(Thrinacodontidae, new family) from the Bear Dick, J. R. R., 1981. Diplodoselache woodi gen. et sp. Gulch Limestone, Serpukhovian of Montana, USA. nov., an early Carboniferous shark from the Mid- Journal of Vertebrate Paleontology, 28(4), 970- land Valley of Scotland. Transaction of the Royal 988. Society of Edinburgh, 72, 99-113. Halamski, A. T., and Baliński, A., 2013. Middle De- Dick, J. R. F., and Maisey, J. G., 1980. The Scottish vonian brachiopods from the southern Maїder Lower Carboniferous shark Onychoselache traqu- (eastern Anti-Atlas, Morocco). Annales Societatis airi. Palaeontology 23, 363-374. Geologorum Poloniae, 83(4), 243-307. Dopieralska, J. 2009. Reconstructing seawater circula- Hampe, O., 2003. Revision of the Xenacanthida tion on the Moroccan shelf of Gondwana during the (Chondrichthyes: Elasmobranchii) from the Car- Late Devonian: Evidence from Nd isotope composi- boniferous of the British Isles. Transaction of the tion of conodonts. Geochemistry, Geophysics, Geo- Royal Society of Edingburgh, Earth Sciences, 93, systems, 10, Q03015,doi:10.1029/2008GC002247. 191-237. Franchi, F., Schemm-Gregory, M., and Klug, C., 2012. Hanke, G.F., Wilson, M.V.H., and Lindoe, L.A., 2001. A new species of Ivdelinia Andronov, 1961 and its New species of Silurian acanthodians from the palaeoecological and palaeobiogeographical impli- Mackenzie Mountains, Canada. Canadian Journal cations (Morocco, Givetian). Bulletin of Geosci- of Earth Sciences, 38, 1517-1529. doi:10.1139/e01- ences, 87(1), 1-11. 039. Frey, L., Rücklin, M., Korn, D., and Klug, C. 2018. Harris, J. E., 1938a. The dorsal fi n spine of Cladose- Late Devonian and Early Carboniferous alpha di- lache. Scientifi c Publications of the Cleveland Mu- versity, ecospace occupation, vertebrate assem- seum of Natural History, 8, 1-6. blages and bio-events of southeastern Morocco. Harris, J. E., 1938b. The neurocranium and jaws of Palaeogeography, Palaeoclimatology, Palaeoecol- Cladoselache. Scientifi c Publications of the Cleve- ogy, 496, 1-17. land Museum of Natural History, 8, 7-12. Friedman, M., and Sallan, L. C., 2012. Five hundred Hartenfels, S. 2011. Die globalen Annulata-Events

20 Introduction

und die Dasberg-Krise (Famennium, Oberdevon) tematic Palaeontology, 15(1), 19-41. in Europa und Nord-Afrika - hochaufl ösende Co- Itano, W. M., 2015. An abraded tooth of Edestus nodonten-Stratigraphie, Karbonat-Mikrofazies, (Chondrichthyes, Eugeneodontiformes): Evidence Paläoökologie und Paläodiversität. Münstersche for a unique mode of predation. Transactions of the Forschungen zur Geologie und Paläontologie, 105, Kansas Academy of Science, 118(1-2), 1-9. 1-527. Itano, W. M. 2018. A tooth whorl of Edestus heinrichi Hartenfels, S. and Becker, R. T. 2009. Timing of the (Chondrichthyes, Eugeneodontiformes) displaying global Dasberg Crisis-implications for Famennian progressive macrowear. Transactions of the Kansas eustasy and chronostratigraphy. Palaeontographi- Academy of Science, 121(1-2), 125-133. ca Americana, 63, 71-97. Itano, W. M., 2014. Edestus, the strangest shark? First Hartenfels, S. and Becker, R.T. 2016a. The global An- report from New Mexico, North American paleo- nulata Events: review and new data from the Rheris biogeography, and a new hypothesis on its method Basin (northern Tafi lalt) of SE Morocco, in: Beck- of predation. The Mountain Geologist, 51(3), 201- er, R. T., Königshof, P., Brett, C. E. (Eds.), Devo- 221. nian Climate, Sea Level and Evolutionary Events. Geological Society, London, Special Publications, Janvier, P., and Suarez-Riglos, M., 1986. The Silurian 423, http://doi.org/10.1144/SP423.14 and Devonian vertebrates of Bolivia. Bulletin de l’Institut français d’Études andines, 15(3-4), 73- Hartenfels, S. and Becker, R. T., 2016b. Age and cor- 114. relation of the transgressive Gonioclymenia Lime- stone (Famennian, Tafi lalt, eastern Anti-Atlas, Mo- Jessen, H., 1968. Moythomasia nitida Gross und M. cf. rocco). Geological Magazine, 1-44. striata Gross, Devonische palaeonisciden aus dem oberen Plattenkalk der Bergisch-Gladbach-Paf- Heidtke, U. H. J., 1982. Der Xenacanthide Orthacant- frather Mulde (Rheinisches Schiefergebirge). Pa- hus senckenbergianus aus dem pfälzischen Rotlie- laeontographica Abteilung A, 128, 87–114. genden (Unter-Perm). Pollichia, 70, 65-86. Joachimski, M.M., Breisig, S., Buggisch, W., Talent, Heidtke, U. H. J., 1999. Orthacanthus (Lebachacant- J.A., Mawson, R., Gereke, M., Morrow, hus) senckenbergianus Fritsch 1889 (Xenacanthi- da: Chondrichthyes): revision, organisation und J.R., Day, J., Weddige, K., 2009. Devonian climate and phylogenie. Freiberger Forschungsheft, 481, 63- reef evolution: insights from 106. oxygen isotopes in apatite. Earth Planet Science Let- Heidtke, U. H. J., and Krätschmer K., 2001. Gladba- ters, 284, 599-609. chus adentatus nov. gen. et sp., ein primitiver Hai Joachimski, M. M., Buggisch, W., 2002. Conodont ap- aus dem Oberen Givetium (Oberes Mitteldevon) atite δ18O signatures indicate climatic cooling as a der Bergisch Gladbach - Paffrath-Mulde (Rheini- trigger of the Late Devonian mass extinction. Geol- sches Schiefergebirge). Mainzer geowissenschaftli- ogy, 30(8), 711714. che Mitteilungen, 30, 105-122. Kaiser, S. I., Aretz, M., Becker, R. T., 2015. The global Heidtke, U. H. J., Schwind, C., and Krätschmer K., Hangenberg Crisis (Devonian-Carboniferous tran- 2004. Über die Organisation des Skelettes und die sition): review of a fi rst-order mass extinction. In verwandschaftlichen Beziehungen der Gattung Tri- Becker, R. T., Königshof, P., Brett, C. E. (Eds.), De- odus Jordan 1849 (Elasmobranchii: Xenacanthida). vonian climate, sea level and evolutionary events. Mainzer geowissenschaftliche Mitteilungen, 32, Geological Society of London, Special Publica- 9-54. tions, pp. 387437. Hotton, N., 1952. Jaws and teeth of American xena- Kaiser, S. I., Becker, R. T., Steuber, T., and Aboussalam canth sharks. Journal of Paleontology, 26, 489-500. S. Z. 2011. Climate-controlled mass extinctions, House, M.R. 1985. Correlation of mid-Palaeozoic am- facies, and sea-level changes around the Devoni- monoid evolutionary events with global sedimenta- an-Carboniferous boundary in the eastern Anti-At- ry perturbations. Nature, 313, 1722. las (SE Morocco). Palaeogeography, Palaeoclima- tology, Palaeoecology, 310, 340364. House, M.R., 2002. Strength, timing, setting and cause of mid-Palaeozoic extinctions. Palaeogeography, Kaiser, S. I., Steuber, T., Becker, T., 2008. Environ- Palaeoclimatology, Palaeoecology, 181, 525. mental change during the Late Famennian and Early Tournaisian (Late Devonian-Early Carbon- Hryniewicz, K., Jakubowicz, M., Belka, Z., Dopier- iferous): implications from stable isotopes and alska, J., and Kaim, A., 2017. New bivalves from conodont biofacies in southern Europe. Geological a Middle Devonian methane seep in Morocco: Journal, 42, 241260. the oldest record of repetitive shell morphologies among some seep bivalve molluscs. Journal of Sys- Kaiser, S. I., Steuber, T., Becker, R. T., Joachimski, M.

21 Introduction

M., 2006. Geochemical evidence for major envi- Klug, C., Schulz, H., and De Baets, K., 2009. Red De- ronmental change at the Devonian-Carboniferous vonian trilobites with green eyes from Morocco boundary in the Carnic Alps and the Rhenish Mas- and the silicifi cation of the trilobite exoskeleton. sif. Palaeogeography, Palaeoclimatology, Palaeo- Acta Palaeontologica Polonica, 54(1), 117-123. ecology, 240(1), 146-160. Korn, D. 1999. Famennian Ammonoid Stratigraphy of Karatajūtė-Talimaa, V., 1973. Elegestolepis grossi gen. the Ma’der and Tafi lalt (Eastern Anti-Atlas, Moroc- et sp. nov., ein neues Typ der Placoidschuppe aus co). In: R. Feist, J.A. Talent and A. Daurer (Eds), dem oberen Silur der Tuwa. Palaeontographica North Gondwana: Mid-Paleozoic Terranes, Stratig- Abteilung A, 143, 35-50. raphy and Biota. Abhandlungen der Geologischen Bundesanstalt, 54, 147-179. Karatajūtė-Talimaa, V., 1995. The Mongolepidida: scale structure and systematic position. Geobios, Korn, D., Belka, Z., Fröhlich, S., Rücklin, M., and MS, 19, 35-37. Wendt, J. 2004. The youngest African clymeniids (Ammonoidea, Late Devonian)-failed survivors of Karatajūtė-Talimaa, V., and Novitskaya, I., 1992. the Hangenberg Event. Lethaia, 37(3), 307-315. Teslepis, a new mongolepid elasmobranchian fi sh from the Lower Silurian of Mongolia. Paleontolo- Korn, D. and Bockwinkel, J., 2017. The genus Gonio- gischeskii Zhurnal, 4, 36-47. clymenia (Ammonoidea; Late Devonian) in the An- ti-Atlas of Morocco. Neues Jahrbuch für Geologie Karatajūtė-Talimaa, V., and Smith, M.M. 2002. Ear- und Paläontologie-Abhandlungen, 285(1), 97-115. ly acanthodians from the Lower Silurian of Asia. Earth and Environmental Science Transactions Korn, D., Bockwinkel, J. and Ebbighausen, V., 2014. of the Royal Society of Edinburgh, 93, 277 299. Middle Famennian (Late Devonian) ammonoids doi:10.1017/S0263593300000444 from the Anti-Atlas of Morocco, 1. Prionoceras. Neues Jahrbuch für Geologie und Paläontologie, Karatajūtė-Talimaa, V., Rozman, K. H. S., and Sodov, Abhandlungen 272(2), 167204. Z.H., 1990. Mongolepis, a new elasmobranch ge- nus from the Lower Silurian of Mongolia. Paleon- Korn, D., Bockwinkel, J. and Ebbighausen, V., 2015a. tologicheskii Zhurnal, 1, 76-86. The Late Devonian ammonoid Mimimitoceras in the Anti-Atlas of Morocco. Neues Jahrbuch für Ge- Kaufmann, B. 1998. Facies analysis, stratigraphy and ologie und Paläontologie, Abhandlungen, 275(2), diagenesis of Middle Devonian reef- and mud- 125-150. mounds in the Mader (eastern Anti-Atlas, Moroc- co). Acta Geologica Polonica , 48(1), 43-106. Korn, D., Bockwinkel, J. and Ebbighausen, V., 2015b. Middle Famennian (Late Devonian) ammonoids Karpinski, A. P., 1899A. Ueber die Reste von Edestiden from the Anti-Atlas of Morocco, 2. Sporadocera- und die neue Gattung Helicoprion. Verhdl. Kaiser. tidae. Neues Jahrbuch für Geologie und Paläonto- Russ. Miner. Ges. St. Petersburg, 36(2), 1-111. logie, Abhandlungen, 278(1), 4777. Klug, C. 2002. Quantitative stratigraphy and taxonomy Korn, D., Bockwinkel, J. and Ebbighausen, V., 2016a. of late Emsian and-Eifelian ammonoids of the east- The late Famennian tornoceratid ammonoids ern Anti-Atlas (Morocco). Courier Forschungsins- in the Anti-Atlas of Morocco. Neues Jahrbuch titut Senckenberg, 238, 1-109. für Geologie und Paläontologie Abhandlungen, Klug, C., Frey, L., Korn, D., Jattiot, R., and Rücklin, 281(2), 201220. M. 2016. The oldest Gondwanan cephalopod man- Korn, D., Bockwinkel, J. and Ebbighausen, V., 2016b. dibles (Hangenberg Black Shale, Late Devonian) Middle Famennian (Late Devonian) ammonoids and the mid Palaeozoic rise of jaws. Palaeontolo- from the Anti-Atlas of Morocco. 3. Tornoceratids. gy, 59(5), 611-629. - Neues Jahrbuch für Geologie und Paläontologie Klug, C., Kröger, B., Korn, D., Rücklin, M., Abhandlungen, 281(3), 267281. Schemm-Gregory, M., De Baets, K., and Mapes, Korn, D., and Klug, C., 2002. Ammoneae Devonicae. R. H. 2008. Ecological change during the early Fossilium Catalogus. I. Animalia 138. 375 pp. Emsian (Devonian) in the Tafi lalt (Morocco), the Backhuys Publishers (Leiden, Netherlands). origin of the Ammonoidea, and the fi rst African pyrgocystid edrioasteroids, machaerids and phyllo- Kříž, J., 2000. Lochkovian bivalves of Bohemian type carids. Palaeontographica Abteilung A, 283(4-6), from the eastern Anti-Atlas (Lower Devonian, Mo- 83-176. rocco). Senckenbergiana lethaea, 80(2), 485-523. Klug, C., Rücklin, M., Meyer-Berthaud, B., and Soria, Kröger, B., 2008. Nautiloids before and during the or- A., 2003. Late Devonian pseudoplanktoniccrinoids igin of ammonoids in a Siluro-Devonian section in from Morocco. Neues Jahrbuch für Geologie und the Tafi lalt, Anti-Atlas, Morocco., Special Papers Mineralogie, 3, 153-163. in Palaeontology, 79, 1-110.

22 Introduction

Lane, J. A., 2010. Morphology of the braincase in the 139173. Cretaceous hybodont shark Tribodus linnae (Chon- Long, J. A., 1983. A new diplacanthoid acanthodian drichthyes: Elasmobranchii), based on CT scan- from the Late Devonian of Victoria. Association of ning. American Museum Novitates, 2758, 1-70. Australasian Palaeontologists Memoir, 1, 51 – 65. Lane, J. A., and Maisey, J. G., 2009. Pectoral anato- Long, J. A., 1991. The long history of Australian fossil my of Tribodus limae (Elasmobranchii: Hybodon- fi shes. In: Vickers-Rich P., Monaghan J. M., Baird tiformes) from the Lower Cretaceous of Northeast- R. F. and Rich T. H. (eds). Vertebrate Palaeontol- ern Brazil. Journal of Vertebrate Paleontology, 29, ogy of Australasia, pp. 337 – 428. Pioneer Design 25-38. Studio, Lilydale. Lane, J. A., and Maisey, J. G., 2012. The visceral Long, J. A., Large, R. R., Lee, M. S., Benton, M. J., skeleton and jaw suspension in the durophagous Danyushevsky, L. V., Chiappe, L. M., Halpin, J. A., hybodontid shark Tribodus limae from the Lower Cantrill, D., Lottermoser, B., 2015. Severe seleni- Cretaceous of Brazil. Journal of Paleontology, 86, um depletion in the Phanerozoic oceans as a factor 886-905. in three global mass extinction events. Gondwana Lebedev, O. A., and Clack, J. A., 1993. Upper Devoni- Research, 36, 209218. an tetrapods from Andreyevka, Tula Region, Rus- Long, J.A., Mark-Kurik, E., Johanson, Z., Lee, sia. Palaeontology, 36, 721-734. M.S.Y.,Young, G.C., Min, Z., Ahlberg, P.E., New- Lebedev, O. A., and Coates, M. I., 1995. The postcra- man, M., Jones, R., Blaauwen, J.d., Choo, B., and nial skeleton of the Devonian tetrapod Tulerpeton Trinajstic, K. 2015. Copulation in antiarch placo- curtum Lebedev. Zoological Journal of the Linnean derms and the origin of gnathostome internal fertil- Society, 114, 307-348. ization. Nature, 517, 196-199. Lehman, J. P., 1956. Les Arthrodires du Dévonien supé- Long, J. A., Trinajstic, K., 2010. The Late Devonian rieur du Tafi lalt (Sud Marocain). Notes et Mémoires Gogo Formation Lägerstatte of Western Australia: du Service Géologique du Maroc, 129, 170. exceptional early vertebrate preservation and diver- sity. Annual Review of Earth and Planetary Scienc- Lehman, J. P., 1964. A propos de quelques Arthrodires es, 38, 255279. et Ichthyodorulites sahariens. Mémoire IFAN, 68, 193-200. Lubeseder, S., Rath, J., Rücklin, M., Messbacher, R., 2010. Controls on Devonian hemi-pelagic lime- Lehman, J. P., 1976. Nouveaux poissons fossiles du stone deposition analyzed on cephalopod ridge to Dévonien du Maroc. Annales de Paléontologie Ver- slope sections, Eastern Anti-Atlas, Morocco. Fa- tébrés, 62, 134. cies, 56, 295-315. Lehman, J. P., 1977. Sur la présence d’un Ostéolé- Lund, R., 1985. The morphology of Falcatus falcatus piforme dans le Dévonien supérieur du Tafi lalt. (St. John and Worthen), a Mississippian stethacan- Compte-Rendus de l’Académie des Sciences, 285D, thid chndrichthyan from the Bear Gulch Limestone 151153. of Montana. Journal of Vertebrate Paleontology, 5, Lehman, J. P., 1978. A propos de deux poissons du Fa- 1-19. mennien du Tafi lalt. Annales de Paléontologie Ver- Lund, R., 1986. On Damocles serratus nov. gen. et sp., tébrés, 64, 143152. (Elasmobranchii: Cladodontida) from the Upper Lelièvre, H., Janvier, P., 1986. L’Eusthénopteridé Mississippian Bear Gulch Limestone of Montana. (Osteichthyes, Sarcopterygii) du Famennian (Dé- Journal of Vertebrate Paleontology, 6, 12-19. vonien supérieur) du Tafi lalt (Maroc): nouvelle Lund, R., and Grogan, E. D., 1997. Relationships of description. Bulletin du Muséum National d’His- the Chimaeriformes and the basal radiation of the toire naturelle, 4e Série, Section C, Sciences de la Chondrichthyes. Reviews in Fish Biology and Fish- Terre, Paléontologie, Géologie, Minéralogie, 3, eries, 7(1), 65-123. 351365. Lund, R., Greenfest-Allen, E., and Grogan, E. D., Lelièvre, H., Janvier, P., 1988. Un Actinistien (Sar- 2012. Habitat and diversity of the Bear Gulch fi sh: copterygii, Vertebrata) dans le Dévonien supérieur Life in a 318 million year old marine Mississippian du Maroc. Compte-Rendus de l’Académie des bay. Palaeogeography, Palaeoclimatology, Palae- Sciences, Paris 307, 14251430. oecology, 342, 1-16. Lelièvre, H., Janvier, P., Blieck, A., 1993. Silurian-De- Lund, R., Greenfest-Allen, E., and Grogan, E. D., vonian vertebrate biostratigraphy of western Gond- 2015. Ecomorphology of the Mississippian fi shes wana and related terranes (South America, Africa, of the Bear Gulch Limestone (Heath formation, Armorica-Bohemia, Middle East). Palaeozoic Montana, USA). Environmental biology of fi shes, vertebrate biostratigraphy and biogeography, pp. 98(2), 739-754.

23 Introduction

Mader, H., 1986. Schuppen und Zähne von Acantho- 3875, 1-15. diern und Elasmobranchiern aus dem Unter-Devon Maisey, J. G., Naylor, G. J., and Ward, D. J., 2004. Me- Spaniens (Pisces). Göttinger Arbeiten zur Geologie sozoic elasmobranchs, neoselachian phylogeny and und Paläontologie, 28, 1-59. the rise of modern elasmobranch diversity. Mesozo- Maisey, J.G., 1981. Studies on Paleozoic Selachian ic fi shes, 3, 17-56. Genus Ctenacanthus Agassiz No. 1. Historical Re- McGhee, G. R., 1988. The Late Devonian extinction view and Revised Diagnosis of Ctenacanthus, With event: evidence for abrupt ecosystem collapse. Pa- a List of Referred Taxa. American Museum Novi- leobiology, 14(3), 250257. tates, 2718, 1-22. McGhee Jr., G. R., 2001. The `multiple impacts hy- Maisey, J.G., 1982a. Studies on the Paleozoic Sela- pothesis` for mass extinction: a comparison of the chian genus Ctenacanthus Agassiz. No. 2, Byth- Late Devonian and the late Eocene. Palaeogeog- iacanthus St. John and Worthen, Amelacanthus, raphy, Palaeoclimatology, Palaeoecology, 176, new genus, Eunemacanthus St. John and Worthen, 4758. Sphenacanthus Agassiz, and Wodnika Münster. American Museum novitates, 2722. McGhee Jr., G.R., 2014. When the Invasion of Land Failed. The Legacy of the Devonian Extinctions. Maisey, J. G., 1982b. The anatomy and interrelation- Columbia University Press, New York (317 pp.). ships of Mesozoic hybodont sharks. Am. Mus. No- vit. 2724, 1-48. Miller, R. F., Cloutier, R. and Turner, S., 2003. The oldest articulated chondrichthyan from the Early Maisey, J. G., 1983. Cranial anatomy of Hybodus Devonian period. Nature 425, 501-504. basanus Egerton from the Lower Cretaceous of England. American Museum Novitates. 2758, 1-64. Neugebauer, J. (1988), The Variscan plate tectonic evo- lution: An improved Iapetus model. Schweizerische Maisey, J.G., 1984a. Studies on the Paleozoic sela- Mineralogische und Petrographische Mitteilungen, chian genus Ctenacanthus Agassiz. No. 3, Nominal 68, 313-333. species referred to Ctenacanthus. American Muse- um novitates, 2774. Novitskaya, L. I. and Karatajūtė-Talimaa, V. N., 1986. Remarks about the cladistic analysis in connection Maisey, J. G., 1984b. Higher elasmobranch phylogeny with myopterygian hypothesis and the problem of and biostratigraphy. Zoological Journal of the Lin- the origin of gnathostomes. pp. 102-125. In Vorob- nean Society, 82(1-2), 33-54. yeva, E. and Lebedkina, N. (eds): Morfologiya i Maisey, J. G., 1989a. Hamiltonichthys mapesi g. & sp. evolyutsiya zhivotnykh [Morphology and evolu- nov. (Chondrichthyes; Elasmobranchii), from the tion of animals]. Nauka, Moscow, 246 pp. Upper Pennsylvanian of Kansas. American Muse- Oelofsen, B. W., 1986. in Indo-Pacifi c Fish Biology: um Novitates, 2931, 1-42. Proceedings of the Second International Confer- Maisey, J. G., 1989b. Visceral skeleton and muscula- ence on Indo-Pacifi c Fishes. (eds Uyeno, T., Arai, ture of a Late Devonian shark. Journal of Verte- R., Taniuchi, T., Matsuura, K.) 107-124 (Ichthyo- brate Paleontology, 9, 174-190. logical Society of Japan, Tokyo). Maisey, J. G., 2009. The spine-brush complex in sym- Retallack, G. J., 1997. Early forest soils and their role moriiform sharks (Chondrichthyes; Symmorii- in Devonian global change. Science, 276(5312), formes), with commenst on dorsal fi n modularity. 583-585. Journal of Vertebrate Paleontology, 29, 14-24. Riquier, L., Tribovillard, N., Averbuch, O., Devlee- Maisey, J. G., and Anderson, M. E., 2001. A primitive schouwer, X., Riboulleau, A., 2006. The Late Fras- chondrichthyan braincase from the Early Devonian nian Kellwasser horizons of the Harz Mountains of South Africa. Journal of Vertebrate Paleontolo- (Germany): two oxygendefi cient periods resulting gy, 21, 702-713. from different mechanisms. Chemical Geology, 233 (1-2), 137-155. Maisey, J. G., and de Carvalho, M. R., 1997. A new look at old sharks. Nature 385, 779-780. Rücklin M., 2010. A new Frasnian placoderm assem- blage from the eastern Anti-Atlas, Morocco, and its Maisey, J. G., Miller, R. and Turner, S., 2009. The palaeobiogeographical implications. Palaeoworld braincase of the chondrichthyan Doliodus from the 19, 8793. Lower Devonian Campbellton Formation of New Brunswick, Canada. Acta Zoologica, 90, 109-122. Rücklin M., 2011. First selenosteid placoderms from the eastern Anti-Atlas of Morocco; osteology, phy- Maisey, J. G., Miller, R., Pradel, A., Denton, J. S. S., logeny and palaeogeographical implications. Pa- Bronson, A. and Janvier, P., 2017 Pectoral morphol- laeontology 54, 2562. ogy in Doliodus: bridging the ‘acanthodian’-chon- drichthyan divide. American Museum Novitates, Rücklin, M., Clément, G., 2017. Une revue des Placo-

24 Introduction

dermes et Sarcoptérygiens du Dévonien du Maroc, Bulletin of the American Museum of Natural His- in: Zouhri, S. (ed), Paléontologie des vertébrés du tory, 169, 1-66. Maroc: état des connaissance, Mémoires de la So- Scotese, C. R., 2001. Atlas of Earth History, Volume 1, ciété Géologique de France 180, p. 624. Paleogeography, PALEOMAP Project, Arlington, Rücklin, M., Long, J. A., Trinajstic, K., 2015. A new Texas, 52 pp. selenosteid arthrodire (‘Placodermi’) from the Late Sepkoski, J. J. Jr, 2002. A compendium of fossil ma- Devonian of Morocco. Journal of Vertebrate Pale- rine animal genera. Bulletin of American Paleon- ontology 35(2), e908896, 113. tology, 363, 1–560. Sallan, L. C., Coates, M. I., 2010. End Devonian ex- Shubin, N. H., Daeschler, E. B., and Coates, M. I., tinction and a bottleneck in the early evolution of 2004. The early evolution of the tetrapod humerus. modern jawed vertebrates. Proceedings of the Na- Science, 304, 90-93. tional Academy of Science 107(22), 1013110135. Solér-Gijon, R., and Hampe, O., 1998. Evidence of Sandberg, C.A., Morrow, J.R., Ziegler, W., 2002. Late Triodus Jordan 1849 (Elasmobranchii: Xenacan- Devonian sea-level changes, catastrophic events, thidae) in the Lower Permian of the Autun basin and mass extinctions. In Koeberl, C., MacLeod, (Muse, France). Neues Jahrbuch für Geologie und K.G. (Eds.), Catastrophic Events and Mass Extinc- Paläontologie, Monatshefte, 1998, 335-348. tions: Impacts and Beyond, Geological Society of America, Special Papers, 356, 473-487. Stein, W. E., Berry, C. M., Hernick, L. V., and Man- nolini, F., 2012. Surprisingly complex community Sansom, I.J., Aldridge, R.J., and Smith, M.M., 2000. discovered in the mid-Devonian fossil forest at Gil- A microvertebrate fauna from the Llandovery of boa. Nature, 483(7387), 78. South China. Transactions Royal Society of Edin- burgh, 90, 255-272. Struve, W., 1990. Beiträge zur Kenntnis der Phacopi- na (Trilobita), 18: Die Riesen-Phacopiden aus dem Sansom, I. J., Davies, N. S., Coates, M. I., Nicoll, R. S., Ma‘der, SEmarokkanische Prä-Sahara. Sencken- and Ritchie, A., 2012. Chondrichthyan like scales bergiana Lethaea, 75 (1/2), 77-129. from the Middle Ordovician of Australia. Palaeon- tology, 55(2), 243-247. - Termier, H., 1936. Etudes géologiques sur le Maroc central et le Moyen atlas septentrional. Notes et Sansom, I. J., Smith, M. M. and Smith, M. P., 1996. Mémoires Service des Mines et de la carte géolo- Scales of thelodont and shark-like fi shes from the gique du Maroc 33, 1566p. Ordovician of Colorado. Nature, 379, 628-670. Tessitore, L., Schemm-Gregory, M., Korn, D., Wild, F. Sartenaer, P., 1998. The presence in Morocco of the R., Naglik, C., & Klug, C. (2013). Taphonomy and late Famennian genus Hadyrhyncha Havlíĉek, 1979 palaeoecology of the green Devonian gypidulid (rhynchonellid, brachiopod). Bulletin de l`Institute brachiopods from the Aferdou El Mrakib, eastern Royal des sciences naturelles de belgique, sciences Anti-Atlas, Morocco. Swiss Journal of Palaeontol- de la terre, 68, 115120. ogy, 132(1), 23-44. Sartenaer, P., 1999. Tetragonorhynchus, new late Turner, S., 1997. “Dittodus” species of Eastman 1899 Famennian rhynchonellid genus from Maïder, and Hussakopf and Bryant 1918 (Mid to Late De- southern Morocco, and Tetragonorhynchidae n. vonian). Modern Geology, 21, 87-119. fam. Bulletin de l’institute royal des sciences natu- relles de belgique, sciences de la terre, 69, 6775. Walliser, O. H., 1996. Global events in the Devoni- an and Carboniferous. In Walliser, O. H., Global Sartenaer, P., 2000. Phacoiderhynchus, a new middle events and event stratigraphy in the Phanerozoic, Famennian rhynchonellid genus from the Anti-At- 225250. las, Morocco, and Phacoiderhynchidae n. fam. Bul- letin de l’institute royal des sciences naturelles de Webster, G. D., Becker, R. T., and Maples, C. G., 2005. belgique, sciences de la terre, 70, 7588. Biostratigraphy, paleoecology, and taxonomy of Devonian (Emsian and Famennian) crinoids from Schaeffer, B., 1967. Comments on elasmobranch evo- southeastern Morocco. Journal of Paleontology, lution. In P. W. Gilbert, R. F. Mathewson, and D. P. 79(6), 1052-1071. Rall (eds.), Sharks, skates and rays, pp. 3-35. Johns Hopkins Press, Baltimore, Maryland. Wendt, J., 1985. Disintegration of the continental mar- gin of northwestern Gondwana: late Devonian of Schaeffer, B., and Williams, M., 1977. Relationships the eastern Anti-Atlas (Morocco). Geology, 13, of fossil and living elasmobranchs. American Zool- 815-818. ogist, 17(2), 293-302. Wendt, J., 1995. Shell directions as a tool in palaeocur- Schaeffer, B., 1981. The xenacanth shark neurocrani- rent analysis. Sedimentary Geology, 95, 161-186. um, with comments on elasmobranch monophyly.

25 Introduction

Wendt, J. and Belka, Z. 1991. Age and depositional Young G.C., 2000. Replacement name for Areyonga environment of Upper Devonian (early Frasnian Young 1997 (preoccupied name). Journal of Verte- to early Famennian) black shales and limestones brate Paleontology, 20, 611. (Kellwasser facies) in the eastern Anti-Atlas, Mo- Young, G.C., 2007. Devonian formations, vertebrate rocco. Facies, 25, 51-90. faunas and age control on the far south coast of Wendt, J., Kaufmann, B., Belka, Z., Klug, C., and Lu- New South Wales and adjacent Victoria. Australian beseder, S., 2006. Sedimentary evolution of a Pa- Journal of Earth Sciences, 54(7), 991-1008. DOI: laeozoic basin and ridge system: the Middle and 10.1080/08120090701488313 Upper Devonian of the Ahnet and Mouydir (Alge- Zangerl, R., 1981. Chondrichthyes I: Paleozoic Elas- rian Sahara). Geological Magazine, 143 (3), 269- mobranchii. In: Schultze, H. P. (ed.), Handbook 299. of Paleoichthyology 3A, 115 pp. Gustave Fischer, Williams, M. E., 2001. Tooth retention in cladodont Stuttgart, New York. sharks: with a comparison between primitive Zangerl, R., 1984. On the microscopic anatomy and grasping and swallowing, and modern cutting and possible function of the spine “brush”complex gouging feeding mechanisms. Journal of Verte- of Stethacanthus (Elasmobranchii: Symmoriida). brate Paleontology, 21, 214-226. Journal of Vertebrate Paleontology, 4(3), 372-378. Williams, M. E. 1985. The “cladodont level” sharks of DOI: 10.1080/02724634.1984.10012016 the Pennsylvanian Black Shales of central North Zangerl, R., 1990. Two new stethacanthid sharks America. Palaeontographica A, 190, 83-158. (Stethacanthidae, Symmoriida) from the Pennsyl- Woodward, A. S., and White, E. I., 1938. The dermal vanian of Indiana, USA. Palaeontographica A, tubercles of the Upper Devonian shark, Cladose- 213, 115-141. lache. Annals and Magazine of Natural History, 11, Zangerl, R. and Case, G. R., 1976. Cobelodus aculeatus 367-368. (Cope), ananacanthous shark from Pennsylvanian Young, G. C., 1982. Devonian sharks from South-East- black shales of North America. Palaeontographica ern Australia and Antarctica. Palaeontology, 25, A, 154, 107-157. 817-843. Zhu, M. 1998. Early Silurian sinacanths (Chondrich- Young, G. C., 1989a. The Aztec fi sh fauna of southern thyes) from China. Palaeontology, 41, 157-171. Victoria Land-evolutionary and biogeographic sig- Zhu, M., Yu, X., Ahlberg, P.E., Choo, B., Lu, J., Qiao, nifi cance. In: Crame J. A. (ed.) Origins and Evolu- T., Qu, Q., Zhao, W., Jia, L., Blom, H., and Zhu, tion of the Antarctic Biota, pp. 43 – 62. Geological Y.A., 2013. A Silurian placoderm with osteich- Society of London Special Publication , 47. thyan-like marginal jaw bones. Nature, 502, 188- Young, G.C., 1989b. New occurrences of culmacan- 193. thid acanthodians (Pisces, Devonian) from Antarc- Zhu, M., Ahlberg, P. E., Zhao, W., and Jia, L., 2002. tica and southeastern Australia. Proceedings of the First Devonian tetrapod from Asia. Nature, 420, Linnean Society of New South Wales, 111, 12– 25. 760-761. Young, G. C., 1997. Ordovician microvertebrate re- Žigaitė, E.Z., and Karatajūtė-Talimaa, V., 2008. New mains from the Amadeus Basin, central Australia. genus of chondrichthyans from the Silurian-Devo- Journal of Vertebrate Paleontology, 17, 1-25. nian boundary deposits of Tuva. Acta Geologica Polonica, 58, 127-131.

26 CHAPTER I

Late Devonian and Early Carboniferous alpha diversity, ecospace occupation, vertebrate assemblages and bio-events of southeastern Morocco

Linda Frey, Martin Rücklin, Dieter Korn and Christian Klug

Published in: Palaeogeography, Palaeoclimatology, Palaeoecology, 496 (2018), 1-17 https://doi.org/10.1016/j.palaeo.2017.12.028

Chapter I: Alpha Diversity and Palaeoecology

3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ²

Contents lists available at ScienceDirect

Palaeogeography, Palaeoclimatology, Palaeoecology

journal homepage: www.elsevier.com/locate/palaeo

Late Devonian and Early Carboniferous alpha diversity, ecospace occupation, vertebrate assemblages and bio-events of southeastern Morocco

Linda Freya,⁎, Martin Rücklinb, Dieter Kornc, Christian Kluga a Palaeontological Institute and Museum, University of Zurich, Karl Schmid-Strasse 4, CH-8006 Zurich, Switzerland b Naturalis Biodiversity Center, Postbus 9517, 2300, RA, Leiden, The Netherlands c Museum für Naturkunde Berlin, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstraße 43, D-10115 Berlin, Germany

ARTICLE INFO ABSTRACT

Keywords: The Late Devonian was a time of dramatic environmental perturbations affecting marine ecosystems. Both the Fossillagerstätte Kellwasser (latest Frasnian) and the Hangenberg crises (latest Famennian) are primarily reported as phases of Famennian drastic decreases in marine diversity while the Hangenberg Crisis is also described as a bottleneck in vertebrate Gnathostomes evolution. Fossil-bearing localities with Upper Devonian strata are of great interest to assess variations in the Invertebrates effects of environmental perturbations on biodiversity. For this purpose, we examined changes in alpha diversity Palaeoecology and ecospace utilization of 21 Famennian (Late Devonian) and early Tournaisian (Early Carboniferous) in- Sea level vertebrate associations containing 9828 specimens from Madène el Mrakib and Aguelmous (southern Maïder Basin, northeastern Anti-Atlas, Morocco), where some layers yield exceptionally preserved gnathostome re- mains. Both the invertebrate and vertebrate associations contain predominantly opportunistic and pelagic taxa indicating oxygen depletion near the seafloor in this region. Nevertheless, the ecospace extension was fluctuating and correlated with regional and/or global sea-level changes and oxygenation of bottom waters. In the Maïder Basin, the ecospace was depleted after and during several bio-events such as the Kellwasser and Hangenberg crises, the Annulata event (middle Famennian) as well as during the early Tournaisian. Abiotic as well as biotic changes (instability of the invertebrate ecosystem) are considered to have influenced Famennian vertebrate diversity because they were more or less directly dependent on invertebrates as a food source.

1. Introduction caused severe losses of global diversity of many marine and terrestrial biotic groups (Newell, 1952, 1956, 1963; Raup and Sepkoski, 1982; Fundamental environmental perturbations and evolutionary McGhee, 1996; McGhee Jr, 2001, 2014; Alroy, 2010; McGhee Jr et al., changes in vertebrates and invertebrates were widely reported to have 2013; Sallan and Coates, 2010; Friedman and Sallan, 2012; Sallan and occurred during the Late Devonian (e.g. House, 1985; McGhee, 1988; Galimberti, 2015). However, causes for ecosystem changes and di- Walliser, 1996; Algeo et al., 1995, 2001; Algeo and Scheckler, 1998; versity loss during the Late Devonian are still highly debated (e.g. Caplan and Bustin, 1999; Murphy et al., 2000; Joachimski and Buggisch, 1991; Algeo et al., 1995, 2001; Algeo and Scheckler, 1998; Buggisch, 2002; Goddéris and Joachimski, 2004; Racki, 2005; Bond and Sandberg et al., 2002; Riquier et al., 2006; Long et al., 2015) and Wignall, 2008; Sallan and Coates, 2010; Sallan and Galimberti, 2015; concerning vertebrates, this time interval was mainly studied via global Long et al., 2015). Two biotic crises that strongly affected global biota diversity curves (e.g. Sallan and Coates, 2010; Friedman and Sallan, were the Kellwasser and Hangenberg crises (Buggisch, 1991; Kaiser 2012; Sallan and Galimberti, 2015). Therefore, a regional study on the et al., 2006, 2008, 2015; Carmichael et al., 2015; Becker et al., 2016); vertebrate ecosystem including other organisms such as invertebrates in addition small-scale events such as the Condroz (Becker, 1993), from a locality with detailed stratigraphical and sedimentological in- Annulata (Becker and House, 1997, 2000; Sandberg et al., 2002; Korn, formation is needed. The Maïder Basin of the eastern Anti-Atlas is 2002, 2004; Racka et al., 2010; Hartenfels and Becker, 2016a) and suitable for this purpose. Dasberg events (Hartenfels and Becker, 2009; Hartenfels, 2011; Kaiser The eastern Anti-Atlas of Morocco is well-known for its highly fos- et al., 2011) have been recognized in Frasnian and Famennian succes- siliferous outcrops of Devonian marine sedimentary rocks. In recent sions (House, 1985, 2002; Walliser, 1996; Table 1). Both the Kellwasser years (e.g., Klug et al., 2008, 2016), some stratigraphic intervals of Crisis (latest Frasnian) and the Hangenberg Crisis (end-Devonian) several localities became known for their Fossillagerstätten qualities

⁎ Corresponding author. E-mail addresses: [email protected] (L. Frey), [email protected] (M. Rücklin), [email protected] (D. Korn), [email protected] (C. Klug). https://doi.org/10.1016/j.palaeo.2017.12.028 Received 30 June 2017; Received in revised form 21 December 2017; Accepted 22 December 2017

$YDLODEOHRQOLQH-DQXDU\ ‹(OVHYLHU%9$OOULJKWVUHVHUYHG 29 Chapter I: Alpha Diversity and Palaeoecology

L. Frey et al. 3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ² ) ) ; ected by the Platyclymenia ff Friedman and sh) a ) ; fi ed only after the fi ) Kaiser et al., 2015 ; ) Sallan and Galimberti, 2015 Decombeix et al., 2011 ; ) ; McGhee Jr, 2014 Sallan and Coates, 2010 Becker, 1993 Hartenfels and Becker, 2009 Korn, 2004 Poty, 1999 Global - Loss in marine biodiversity (e.g. - Extinction of few ammonoid( genera Sallan, 2012 - Mass occurence of the ammonoid Hangenberg Crisis, diversi - Coincides with environmental( changes - Small-scale extinction ( - Loss in marine biodiversity - Bottleneck in vertebrates (e.g. - Some groups (corals, trees, Alum Shale Event. ( Denayer et al., 2011 ) Becker et al., , 2007; Kaiser et al., 2015 , ) ) Platyclymenia ) Korn et al., 2002 ) ; see also Hartenfels and Becker, 2009 ) ; Kaiser et al., 2011 ; ; Ebbighausen and Bockwinkel, 2007 ; ects ff Wendt and Belka, 1991 Becker, 1993 Becker, 1993 Korn, 2004 Korn, 2004 Kaiser et al., 2015 Regional: Maïder E - Kellwasser facies rich( in fossils - Species level extinction ( - Extinction of few( ammonoid genera - Extinction in invertebraterhynchonellid groups brachiopods, (mostly ammonoids, bivalves, rugose trilobites, gnathostomes corals) (arthodires, and chondrichthyans) in early ( - Mass occurrence of- the Small-scale ammonoid extinction in( ammonoids Hartenfels and Becker, 2016a, 2016b - Ammonoids: species level( extinction 2006 ; ) Bond ; ) Long et al., ; Hartenfels, ; Siegmund et al., ; ) Algeo and Scheckler, Sandberg et al., 2002 ; ; Carmichael et al., 2015 ; Becker, 1993 ) ; Sandberg et al., 2002 ; House, 1985 Becker et al., 2012 ; Johnson et al., 1985 Hartenfels and Becker, 2009 ; ; ; Gereke and Schindler, 2012 ; Kaiser et al., 2006 Racka et al., 2010 Buggisch, 1991 Caplan and Bustin, 1999 ) ; ; ) Becker, 1993 House, 1985 Walliser, 1996 Becker, 1993 - Anoxia - Sea-level changes - Drop in selenium level (e.g. et al., 2004 2015 - Regional blackshales - Transgression ( - Regression ( Joachimski et al., 2009 1998 - Anoxia - Global cooling - Regression - Transgression followed by- a Eutrophication regression - Drop in selenium level (e.g. - Anoxia - Transgression ( 2002 2011 - Anoxia - Transgression ( ; ) ) ) ; ) Hartenfels ; ) ) ects of Famennian (Late Devonian) and Tournaisian (early Carboniferous) bio-events and environmental perturbations. ff Wendt and Belka, 1991 Wendt and Belka, 1991 Hartenfels and Becker, 2009 Kaiser et al., 2011, 2015 Hartenfels, 2011 Kaiser et al., 2011 Causes Regional: Maïder Global - Dysaerobic condition - High sea level stands ( Becker, 1993 Hartenfels, 2011 - Hypoxic conditions - Two transgressive events ( - Regression ( - Hypoxia to anoxia,- dysoxic Transgression ( - Anoxia - Transgression followed byregression a ( and Becker, 2016a, 2016b - Anoxia - Transgression ( (End-Frasnian) (early Famennian) (Middle Famennian) (End-Famennian) (Late Famennian) (Lower-middle Tournaisian) Bio-event/environmental changes Condroz Kellwasser Annulata Hangenberg Dasberg Alum shale Table 1 Summary of possible causes and e 30  Chapter I: Alpha Diversity and Palaeoecology

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Fig. 1. Geological map of the Maïder and Tafilalt region in the eastern Anti-Altas of Morocco. Localities with phyllocarid layer containing well-preserved remains of gnathostomes are marked here; faunal changes have been studied from lower to upper Famennian at Madène el Mrakib and from lower to middle Tournaisian at Aguelmous. New data about vertebrate diversity has been compared to the locality Filon 12 of the Tafilalt region. because of the abundance (“Kondensat-Lagerstätte”) and exceptional Basin, we recently discovered new, often articulated skeletons of gna- preservation of fossils (“Konservat-Lagerstätte” sensu Seilacher, 1970). thostomes such as placoderms, actinopterygians, sarcopterygians and Among those, Madène El Mrakib (Maïder Basin; cf. Wendt, 1985; chondrichthyans, which will strongly improve the knowledge of this Wendt and Belka, 1991; see Fig. 1, Fig. 3) became famous for its wealth Devonian Konservat-Lagerstätte and thus the palaeoenvironment of this and diversity of remains of well-preserved invertebrates such as ce- small marine basin. phalopods (Petter, 1959, 1960; Korn, 1999; Becker, 1995, 2002; Becker In order to better understand Late Devonian ecosystems of the et al., 2000, 2002; Korn and Klug, 2002; Klein and Korn, 2014; Korn Maïder through time, we studied alpha diversity and palaeoecology of et al., 2014, 2015a, b, 2016a, b; Hartenfels and Becker, 2016a, b; Klug the gnathostomes and invertebrates of a series of sufficiently fossili- et al., 2016; Korn and Bockwinkel, 2017), crinoids (Klug et al., 2003; ferous strata. Our aim is to answer the following questions: (1) How did Webster et al., 2005), brachiopods (Sartenaer, 1998, 1999, 2000) and the ecosystem change during the Famennian in the Maïder? (2) Which trilobites (Struve, 1990). Vertebrate macroremains are rather rare in groups of gnathostomes were present in the assemblages and were their most Devonian strata of Morocco, but they become more abundant in occurrences related to invertebrate diversity? (3) What were the effects sediments of Late Devonian age. Particularly, three-dimensionally of global ecological changes and events on the composition and fluc- preserved remains of various Late Devonian (Frasnian and Famennian) tuations in these assemblages? species, mostly of placoderms, from the eastern Anti-Atlas have been described during the last decades (Lehman, 1956, 1964, 1976, 1977, 2. Material and methods 1978; Lelièvre and Janvier, 1986, 1988; Lelièvre et al., 1993; Rücklin, 2010, 2011; Rücklin et al., 2015; Rücklin and Clément, 2017). Remains 2.1. Geological setting of other gnathostome groups such as actinopterygians, acanthodians and chondrichthyans are restricted to microremains, fin spines or iso- Konservat-Lagerstätten conditions prevailed in wide areas of the lated jaws (Termier, 1936; Lehman, 1976; Derycke, 1992; Hampe et al. Maïder Basin (northeastern Anti-Atlas, Morocco) during the Famennian 2004; Derycke et al., 2008; Ginter et al., 2002; Klug et al., 2016; (Fig. 1); only south of Tafraoute, exceptionally preserved fossils have Derycke, 2017). In several middle Famennian layers of the Maïder not been found yet. We discovered two layers containing exceptionally 31  Chapter I: Alpha Diversity and Palaeoecology

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Fig. 2. Positions of the Famennian samples collected from Madène el Mrakib within the global and regional condodont zonations (Ziegler and Sandberg, 1984 and Hartenfels, 2011) and ammonoid horizons (Becker et al. 2002; Korn et al., 2014). Asterisks and bars mark the approximate position of the samples. preserved vertebrate fossils, particularly chondrichthyans, in the (latest Famennian, Hangenberg Black Shale equivalent) bearing mostly Maïder: The middle Famennian (Maeneceras horizon) phyllocarid layer, macroinvertebrates and rarely acanthodian teeth has recently been named after its high abundance of phyllocarids, contains most of the documented by Klug et al. (2016). gnathostome remains preserved in ferruginous nodules while in the The phyllocarid layer crops out at various localities such as Bid er second layer (early-middle Famennian) fewer remains were found so far Ras, Jebel Oufatene, Mousgar, Tizi Mousgar, Aguelmous Azizaou, Oued (Fig. 2). A third layer with prevailing Konservat-Lagerstätten conditions Chouairef, Tizi n'Aarrat Chouiref and Madène El Mrakib (Fig. 1). 32  Chapter I: Alpha Diversity and Palaeoecology

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Fig. 3. Famennian invertebrate and gnathostome remains from the Maïder. A – B – Bactrites sp., lateral and septal view, ×2, PIMUZ 34012. C – D – Falcitornoceras falciculum, lateral and ventral views, ×3, PIMUZ 34014. E – F – Ch. (Staffites) afrispina, lateral and ventral views, ×1, PIMUZ 34015. G – H – Planitornoceras pugnax, lateral and ventral views, ×2, PIMUZ 34013. I – J – Platyclymenia annulata, lateral and ventral views, ×1, PIMUZ 34010. K – L – Pseudoclymenia sp., lateral and ventral view, ×1.5, PIMUZ 34011. M – N – Aulatornoceras sp., lateral and ventral view, ×1.5, PIMUZ 34016. O – Glyptohallicardia sp., lateral view, ×2, PIMUZ 34017. P – Prosochasma sp., lateral view, ×0.75, PIMUZ 34018. Q – Guerichia sp., lateral view, ×3, PIMUZ 34019. R – S – Loxopteria sp., lateral views, ×1, PIMUZ 34020. T – U – Paleoneilo sp., lateral and dorsal view, ×2, PIMUZ 34021. V – X – undetermined gastropod, apical, apertural and basal view, ×2, PIMUZ 34022. Y – Z – undetermined gastropod, apical and apertural view, ×2, PIMUZ 34023. AA – AC – undetermined bellerophontid, lateral, dorsal and apertural view, ×2, PIMUZ 34024. AD – AH – Phacoiderhynchus antiatlasicus, lateral, dorsal, posterior, ventral and anterior views, ×0.75, PIMUZ 34025. AI – AM – undetermined brachiopod, lateral, dorsal, posterior, ventral and anterior views, ×1, PIMUZ 34026. AN – Rugose coral, lateral view, ×1.5, PIMUZ 34027. AO – Moroccocrinus ebbigh- auseni, lateral view, ×1, PIMUZ 34028. AP – Phoebodus sp., labial and aboral view, scale bar = 5 mm, PIMUZ A/I 4656. AQ – cladodont shark tooth, lingual view, scale bar = 10 mm, PIMUZ A/I 4657. AR – cladodont shark tooth, labial and oral view, scale bar = 5 mm, PIMUZ A/I 4658.

However, in many of these localities, the sedimentary succession of the and erosion towards the Maïder Valley and Tafraoute. Therefore, we Famennian strata is partially covered by scree, often delivered from the measured a section at this locality from strata of latest Frasnian age overlying massive sandstone of the Fezzou Formation which is an (“Upper Kellwasser Event”) up to the Hangenberg Black Shale equiva- equivalent to the Hangenberg Sandstone of the Tafilalt (Kaiser et al., lent (Rücklin, 2010, 2011; Klug et al., 2016). 2011; Klug et al., 2016). The Famennian succession is best exposed at Madène el Mrakib in the southern Maïder because of large scale folding

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Fig. 4. Changes in diversity and ecospace use during the Famennian at Madène el Mrakib. A – Histograms represent the number of species per association and the changes in diversity (Table S1). Intervals without histograms often contained rare and/or weathered and compressed fossils which were mostly impossible to determine to the species level. These intervals were not included in the analysis as they would have resulted in biased species numbers. B – Ecospace expansion (ecological classification after Bush et al., 2007) shows change in the number of three-dimensional modes of life along the section. C – Changes in gnathostome diversity and composition. Abbreviations of ecological categories: Tiering – p: pelagic, er: erect, su: surficial, smi: semi-infaunal, si: shallow infaunal; Motility – ff: freely fast, fs: freely slow, fu: facultative unattached, fa: facultative attached, nu: non-motile and unattached, na: non- motile and attached; Feeding mechanism – sf: suspension feeder, df: deposit feeder, g: grazer, pr: predators.

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2.2. Collection of alpha diversity data considered that recent benthic phyllocarids are able to survive short- term anaerobic conditions and that this tolerance might have existed in Twelve successive fossil assemblages containing 3591 specimens of extinct taxa as well (Vannier et al., 1997). Besides the crinoid Mor- macroinvertebrates (Figs. 3, 4A: associations A-I, K, P-Q; Table S1) co- occocrinus ebbighauseni that was probably pseudoplanktonic in early to occurring with gnathostome remains were collected from the Fa- middle ontogenetic stages and perhaps benthic in adult stages (Klug mennian of Madène el Mrakib to examine changes in alpha diversity et al., 2003; Webster et al., 2005), we found one specimen of a crinoid and palaeoecology. To achieve an adequate resolution in species holdfast in one of the associations, which might be benthic and erect abundance and composition and to reduce biases from differences in (unless it was attached to a living ammonoid). All gastropods (Macro- sample size, only horizons yielding at least 100 specimens were sam- chilina), amphigastropods (Bellerophon), brachiopods (rhynchonellids, pled. Most associations contain numerous formerly pyritized specimens Aulacella), rugose corals and trilobites in the samples inhabited the (now limonitic and haematitic caused by deep weathering of the sedi- sediment surface (Bush et al., 2007). Cladochonid-type tabulate corals ments) whereas other associations are preserved in limestone nodules, (Webster et al., 2005) are lacking in our samples of Madène el Mrakib. sideritic nodules and marly beds. In the latter case, specimens were The lifestyle of bivalves is highly diverse and it is still not completely counted in situ on a bedding plane, depending on the outcrop condi- clarified for all fossil taxa. Species of the genera Guerichia, Prosochasma, tions. To complement our data, we examined 3458 specimens of three Opisthocoelus, Ptychopteria and Streblopteria were probably living on the middle Famennian (Platyclymenia and Procymaclymenia horizons) and sediment surface (Amler, 1996, 2004, 2006). Amler (2004) assumed two late Famennian (Gonioclymenia to Wocklumeria horizons) samples that small bellerophontids, gastropods and the bivalve genus Guerichia from Madène el Mrakib that are housed in the Museum für Naturkunde could have lived on erect benthic or floating algal thalli and therefore, in Berlin (Fig. 2: associations J, L-O; Table S1; biozonation is figured in their occurrence was not limited to the sea floor (oxygen-poor condi- Korn et al., 2014). This material contains mostly ammonoids and was tions cannot be ruled out). We determined these organisms as surficial published by Korn et al. (2014, 2015a). In addition to the Famennian because we found only little organic matter in our section and the ha- samples A to Q from Madène, we examined four samples R to U (Table bitat might have been too deep for large benthic algae (estimated depth S1) containing another 2779 specimens of Early to Middle Tournaisian at Madène el Mrakib is around 200 m and therefore below the euphotic (Early Carboniferous) age from Aguelmous. The ammonoids of these zone; Tessitore et al., 2016). Epibenthic to semi-infaunal lifestyles were samples were published by Ebbighausen and Bockwinkel (2007). proposed for the bivalve Buchiola (Buchiola) and Glyptohallicardia The ages of the associations were determined by ammonoids (cf. (Grimm, 1998) whereas Loxopteria might have been semi-infaunal Korn, 1999; Becker et al., 2002; Korn et al., 2014). For some associa- (Nagel, 2006). Paleoneilo and Metrocardia as well as lingulid brachio- tions (A–C, E, G–U in Table S1), a correlation between ammonoid pods have been suggested to be shallow infaunal based on actualistic horizons and conodont zones was possible (Fig. 2; Hartenfels 2011). comparisons (Thayer and Steele-Petrovic, 1975; Amler, 1996; Kříž, The conodont biozonation of the Famennian was recently revised 2004). Bivalve species that we could neither determine nor assign to (Kaiser et al., 2009; Spalletta et al., 2017). However, for the correlation modes of life, we summarized as ‘benthic organism’ in a separate ca- of our data to global and regional sea level curves (Wendt and Belka, tegory. 1991; Haq and Schutter, 2008; Kaiser et al., 2011), we used the pre- ‘Motility’ refers to locomotory capabilities of organisms such as vious conodont zonation of Sandberg et al. (1978) and Ziegler and freely, fast or slow motile, attached or non-attached facultatively motile Sandberg (1984). or completely non-motile. We assigned phyllocarids and trilobites to The fossils were determined at species level wherever possible and freely, fast motile organisms (Vannier et al., 1997; Fortey, 2004), subsequently, the relative abundance of every taxon was calculated and whereas cephalopods and gastropods were rather slow motile organ- plotted as histograms per association. Moreover, the trophic nucleus isms (Westermann, 1999; Westermann and Tsujita, 1999). Rugose concept of Neyman (1967) was applied to our abundance data to detect corals, crinoids, brachiopods and the bivalve genera Guerichia, Pty- taxa that were dominating each fauna. The trophic nucleus includes chopteryia and Streblopteria were non-motile organisms attached to their taxa whose relative abundances contribute to 80% of the total abun- substrate whereas Prosochasma and Opisthocoelus were attached as well dance of all taxa of a fauna. Additionally to the analysis of the alpha but facultatively motile (Bush et al., 2007; Amler, 1996, 2004; Nagel, diversity of complete samples, we counted ammonoid genera of every 2006; Kříž, 2004). Buchiolid bivalves were sessile and unattached association because some middle and upper Famennian samples ex- (Grimm, 1998). clusively contained cephalopods when considering macrofossils only. In ‘Feeding mechanism’ describes whether animals acquire food by order to compare samples of different sample sizes and to avoid biases predation, mining, grazing suspension filtering or deposit feeding. For caused by different methods or by varying sampling efforts to each cephalopods, we assume this group to be microphagous predators (Klug other, we rarefied the abundance data of each fauna with the software and Lehmann, 2015). Brachiopods, rugose corals, crinoids and most package PAST (Hammer et al., 2001). bivalves were suspension feeders (Paleoneilo represents a deposit feeder; Amler, 2004) while gastropods were assigned to grazers. The phyllo- 2.3. Ecospace occupation carids of the Maïder were suspension feeders as they were probably pelagic due to the dysoxic sediments and poor benthic bottom life. Analyses in palaeoecology are based on the theoretical ecospace Trilobites had a high variety in acquiring food including feeding on concept sensu Bush et al. (2007). We grouped all taxa according to plankton and organic particles, scavenging or preying on small organ- ecological categories of “tiering”, “motility” and “feeding mechanism”. isms on or near the bottom (Fortey and Owens, 1999; Fortey, 2004). On The combination of these three ecological parameters leads to a unique the one hand, the trilobites in our sample were rather small benthic three-dimensional mode of life per taxon. ‘Tiering’ categorises the po- forms that possibly were deposit feeding. On the other hand, they look sition of organisms in the water column such as pelagic, erect, surficial, morphologically similar to forms (e.g. big eyes for good vision, Fortey, semi-infaunal and shallow or deep infaunal. We assigned all cephalo- 2004) that were scavengers or also microphagous predators. pods such as ammonoids, bacritids and orthocerids to a pelagic lifestyle. The habitat of fossil phyllocarid crustaceans is still a matter of debate. 3. Results Due to the ferruginous sediments (probably due to pyrite weathering; the pyrite points at low oxygen conditions) in the Maïder Basin, we 3.1. Fluctuations in invertebrate diversity assigned the phyllocarids to a nektobenthic or pelagic mode of life as it was proposed before by several authors (e.g. Siveter et al., 1991; In total, the 21 associations contain 9828 specimens that were as- Vannier and Abe, 1993; Zatoń et al., 2013). Nevertheless, it has to be signed to around 227 species (Tables S1, S3). Since we separately 35  Chapter I: Alpha Diversity and Palaeoecology

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Fig. 5. Species abundances of 11 successive faunal samples of early to late Famennian age from Madène el Mrakib in the Maïder region (Morocco); red bars represent the dominant species of each association. A – association A, early Famennian, all three sampled taxa are shown. B – association B, early Famennian, all four sampled taxa are shown here. C – association C, early Famennian, nine of thirteen taxa are shown. D – association D, middle Famennian, all five sampled taxa are shown here. E – association E, middle Famennian, five of eight taxa are shown here. F – association F, middle Famennian, eight of eleven taxa are shown here. G – association G, middle Famennian, four of nine taxa are shown here. H – association H, middle Famennian, seven out of fourteen taxa are shown here. I – association I, middle Famennian, Annulata event layer, all two sampled taxa are shown here. J – association K, middle Famennian, 11 out of 22 sampled taxa are shown here. K – association Q, late Famennian, Hangenberg Black Shale, five out of eleven sampled taxa are shown here. Not depicted species are listed in Table S3. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 36  Chapter I: Alpha Diversity and Palaeoecology

L. Frey et al. 3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ² analyzed ammonoids and the complete assemblages of selected layers, three modes of life were present and pelagic lifestyles had higher re- the entire assemblage is concerned when we write of species; ammo- lative abundance than benthic lifestyles (67 versus 33%; Fig. 4B; as- noid diversity is separately depicted and indicated. During the early sociation A–C). The middle Famennian phyllocarid layer (Maeneceras Famennian (Cheiloceras horizon), the general species richness increases horizon) contains taxa dominated by pelagic lifestyles and taxa with an from three up to twelve species and one to five ammonoid genera were additional mode of life (freely pelagic, fast motile deposit feeders that counted within this interval (Fig. 4A: association A–C; Fig. 5A–C). The are represented by phyllocarids) were found. By contrast, the next middle Famennian phyllocarid layer (Maeneceras horizon) contains younger association yielded a high relative abundance of benthic modes numerous gnathostome remains (Fig. 4: association E; Fig. 5E) and of life (82%), which stays high (46–68%) in the following middle Fa- eight species of invertebrates including two ammonoid genera. In the mennian associations (F–H). The association of the Annulata Black following middle Famennian associations (Maeneceras to Planitorno- Shales represents only pelagic modes of life, while the association above ceras horizon), 11 to 14 species and one to four ammonoid genera were the Annulata Black Shales (Platyclymenia/Procymaclymenia horizon) present (Fig. 4A, associations F–H; Fig. 5F–H). We found two cepha- contains seven modes of life represented by benthic and pelagic or- lopod species and one ammonoid genus in the Annulata Black Shales ganisms (freely pelagic, slow-motile predators having the highest (middle Famennian, Platyclymenia horizon) whereas in the subsequent abundance, 57%). In the latest Famennian (Gonioclymenia to Wocklu- sample, 24 ammonoid species and five ammonoid genera were counted meria horizon), pelagic, freely motile predators were highly abundant (Figs. 4I, 7, Table S1: association I-J). In the following sample above the (92%). However, samples were biased towards cephalopods and Annulata Black Shales, species richness reaches 22 species comprising therefore, they were excluded from this analysis. The Wocklumeria six ammonoid genera (Fig. 4A: association K; Fig. 5J). In the two other horizon (latest Famennian age, association P) contained organisms of samples of the middle Famennian (Platyclymenia/Procymaclymenia four modes of life and benthic organisms had a high relative abundance horizon), thirteen and nine species were counted and in both samples, (75%) in comparison to pelagic forms (25%). In the following Hang- seven ammonoid genera were present (Fig. 7: associations L–M). In the enberg Black Shale equivalent (association Q), only two modes of life latest Famennian (Gonioclymenia to Wocklumeria horizons), 13 species were present of which the pelagic organisms had the highest abundance including seven ammonoid genera and three species including one (60%). During the Early Tournaisian, the ecospace of associations R and ammonoid genus were counted (Fig. 7: association N–O). Nine taxa S (Aguelmous, Fig. 9C) consists of five modes of life but in the following were found so far in the Wocklumeria horizon (latest Famennian; two associations (Fig. 9C: associations T and U), the ecospace is reduced however, these layers are not yet sufficiently sampled to provide ac- to one single mode of life. In all the Tournaisian associations, pelagic curate abundance data (Figs. S1, 4A: association P). In the Hangenberg organisms are more abundant than benthos. Black Shale equivalent (latest Famennian), eleven species containing In total, we report here 12 or possibly 13 modes of life (some bi- four ammonoid genera were found (Fig. 4A, association Q; Fig. 5K). The valves could not be assigned to certain three-dimensional lifestyles) earliest Tournaisian association (Fig. 6A) is diverse containing 32 spe- from 216 theoretically possible combinations. This value lies below the cies (thereof eight ammonoid genera) while the other three Tournaisian middle Palaeozoic (Late Ordovician to Devonian) value of about 21 associations contained eight to fifteen species including two to seven modes of life known from North America and Europe (Bush et al., ammonoid genera (Fig. 6B–D; Table S1, association R–U). 2007). Nineteen modes of life were recorded in the Early Devonian We estimated the sampling bias caused by differences in the method strata of the Tafilalt region (Jebel Ouaoufilal, Filon 12, see Fig. 1) that and duration of sampling by rarefaction analysis. The rarefaction curves is palaeogeographically and temporally closer situated to the Late De- describe the number of taxa that could have been collected with ex- vonian of the Maïder (Frey et al., 2014). The slightly impoverished Late tending the sampling duration (increasing number of specimens). Some Devonian ecological diversity of the southern half of the Maïder Basin graphs show steep curves that mean more taxa would have been found points at unfavorable living conditions that coincide with the occur- with further collecting within some of the samples (Figs. S2, S3). rence of reddish ferruginous deposits indicating dysoxic environmental However, the biased samples still show low species numbers compared conditions (Korn, 1999; Korn et al., 2015b; Kaiser, 2005; Webster et al., with the most diverse samples regarding the species numbers that could 2005). have been found within a certain number of collected specimens (we checked for 90 specimens in each graph). Therefore, trends in diversity 3.4. Diversity and ecospace use in vertebrates are not strongly biased and here considered reliable; nevertheless, it cannot be ruled out that these results are influenced by faunal mixing to Skeletal remains of chondrichthyans, sarcopterygians and acti- a small extend (e.g., Kidwell and Bosence, 1991); indicators for strong nopterygians are restricted to specific layers, while placoderms were condensation, such as eroded and reworked fossils, very reduced found in many more horizons of the section and in other parts of the thickness, extensive hiatuses and iron crusts, are absent. eastern Anti-Atlas (Fig. 4C). The highest abundance and species rich- ness in gnathostomes was found in the phyllocarid layer (middle Fa- 3.2. Changes in the trophic nucleus mennian corresponding to the Maeneceras horizon) containing seven species, whereas only one to two species occurred in the other layers Cephalopods such as ammonoids and orthocerids are the most im- (Fig. 8). In this layer, we found three species of placoderms (Dunk- portant components of the trophic nucleus in some early, middle and leosteus, Driscollaspis sp. nov., and a second undescribed placoderm n. late Famennian samples (Fig. 5B, F, H, J) or were even the only gen. et sp.), chondrichthyans (Phoebodus sp., two undescribed clado- dominant group (Fig. 5C–D, G, J). Phyllocarids occur only in one donts) and one actinopterygian (work in progress). Approximately 20 m sample but in great abundance and thus are dominant at Madène el above the phyllocarid layer, remains of cladodont chondrichthyans Mrakib (Fig. 5E). Brachiopods and bivalves contributed rarely to the were found, while the sarcopterygians were found six meter below the trophic nucleus except for in a middle Famennian sample and in the Annulata Black Shales (Fig. 4C). Further skeletal remains of Dunkleos- Hangenberg Black Shale equivalent (Fig. 5A, F, H). In the Tournaisian teus occurred in the late middle Famennian strata and a co-occurrence associations, ammonoids mainly constitute the trophic nucleus except of Titanichthys and Dunkleosteus was found in layers of late Famennian for one single gastropod species that is present in the oldest Tournaisian age. The Hangenberg Black Shale equivalent yielded small teeth of association (association R in Fig. 6A). ischnacanthid acanthodians (Klug et al., 2016). The ecospace use of the gnathostomes of the Maïder Basin is 3.3. Ecospace occupation during the Famennian homogenous. Placoderms such as Dunkleosteus and Titanichthys as well as cladodont chondrichthyans are assumed to have been pelagic ani- In the early Famennian (Cheiloceras horizon) associations, two to mals (Ginter et al., 2010; Carr, 2008, Carr and Jackson, 2008; Long & 37  Chapter I: Alpha Diversity and Palaeoecology

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Fig. 6. Abundances of species and faunal composition of early and middle Tournaisian associations from Aguelmous (Maïder region); data and bed numbers were taken from the collection of Ebbighausen & Bockwinkel (2007); red bars represent dominant taxa. A – association R, early Tournaisian association, 17 out of 32 sampled taxa are shown here. B – association S, early Tournaisian association, all eight sampled taxa are shown here. C – association T, early Tournaisian association, all 15 sampled taxa are shown here. D – association U, middle Tournaisian association, all the nine sampled taxa are shown here. Not depicted species are listed in Table S3. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Trinajstic, 2010). The two additional placoderm species are assumed to 4. Discussion have lived in the water column as well because they do not show mouth parts specialized for crushing hard shelled prey. Phoebodont chon- 4.1. Invertebrate diversity, ecospace occupation and trophic nuclei during drichthyans inhabited a narrower range of environments (“moderately the Famennian deep to moderately shallow waters”; Ginter et al., 2010). Onychodus was reported from the inter-reefal basin of the Gogo Formation Examination of alpha diversity, taxonomic composition and eco- (Playford, 1980; Andrews et al., 2006; Long and Trinajstic, 2010) and space occupation shows that environmental conditions at Madène el therefore, the onychodont sarcopterygians of Madène might have been Mrakib were mostly oxygen-depleted during much of the Famennian. living in the water column as well. Most of these gnathostomes have The faunal composition often includes opportunistic species that were been assumed to have been preying on other vertebrates or in- tolerant to oxygen depletion (Guerichia, buchiolid bivalves, small veti- vertebrates such as phyllocarids, cephalopods as well as conodonts gastropods and bellerophontids, Chondrites; Wignall and Simms, 1990; (e.g., Jaekel, 1919; Miles, 1969; Williams, 1990; Mapes et al., 1995, Amler, 1996, 2004) and deep-water species (e.g. the brachiopods Au- Zatoń et al., 2017). An exception is the placoderm Titanichthys that was lacella and Phacoiderhynchus as well as the bivalve Loxopteria; supposedly a filter feeder because of its long jaw plates with rounded Sartenaer, 2000; Nagel-Myers et al., 2009). Occurrences of pelagic and cross section (Denison, 1978). opportunistic taxa as well as fluctuant environments (several trans- gressions within a larger regressive cycle) in the Famennian were re- ported from the Maïder Basin (Becker 1993; Hartenfels and Becker, 2009; Hartenfels, 2011; Hartenfels and Becker, 2016a, b) as well as from localities outside Morocco (Dreesen et al., 1988; Becker and House, 1997; Sandberg et al., 2002; Kaiser et al., 2006; Marynowski et al., 2007; Joachimski et al., 2009; Racka et al., 2010). 38  Chapter I: Alpha Diversity and Palaeoecology

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4.1.1. Early Famennian In this time interval at Madène el Mrakib, the predominant presence of brachiopods and the increase in ammonoid diversity can be ex- plained by a regionally high sea level (Wendt and Belka, 1991)(Fig. 4A: associations A–C; Fig. 9A–C). Abundant early Famennian rhynchonellid brachiopods were also reported from the East European Platform and they were often flourishing during major transgressions (Sokiran, 2002). Similar associations containing abundant cephalopods and bra- chiopods were reported from the early Fammenian Pa. crepida and rhomboidea zones of the Holy Cross Mountains (Racki, 1990). During this time interval, the ecosystem recovered from the Kellwasser Crisis that caused great structural changes within the marine ecosystem (Becker, 1986; Droser et al., 2000). However, oxygen-poor conditions likely persisted from the Frasnian well into the Famennian, as reflected by the widespread Kellwasser Facies characterized by fossiliferous, black bituminous early Famennian limestones and claystones in the Anti-Atlas (Figs. 4, 9; Wendt and Belka, 1991). We did not detect the Condroz event,which coincides with a regression (sea level curves in Fig. 9), perhaps due to insufficient sampling. Probably this interval was covered by scree at Madène el Mrakib (see stratigraphy in Fig. 4).

4.1.2. Middle Famennian During the middle Famennian, species richness varies between six and fourteen species (Fig. 4A, associations A–H) in our samples. The ecospace occupation fluctuates between three and seven modes of life and the proportion between benthic and pelagic lifestyles is varying (between 33% and 82%) in these associations. Changes in the compo- sition of the associations reflect fluctuations in the level of oxygenation at the seafloor, which, in turn, coincide with global rather than regional sea level changes (Fig. 9). For instance, the widest extension of eco- space use (including several benthic lifestyles represented by relatively large and epibenthic bivalves and the contemporary decrease in am- monoid diversity; Figs. 4B, 9C, association F) indicates an increased ventilation of the seafloor that correlates with a global regression (global sea level curve in Fig. 9; Haq and Schutter, 2008; Becker et al., 2012). The faunal signals appear to coincide with eustatic rather than with regional sea-level changes; therefore, we assume that the Fa- mennian sea level of southern Morocco (Wendt and Belka, 1991)is more fluctuant than previously reported by these authors (regional sea level curve in Fig. 9). This is not so surprising when the configuration of the Maïder Basin is taken into account. Towards the northwest and southeast, it was surrounded by land and in the West and East by to- pographic highs, namely the marine Maïder Platform and the Tafilalt – Platform (Wendt, 1985; Kaufmann, 1998). This area of shallower water Fig. 7. Number of ammonoid genera per association. Associations A Q were collected from the Famennian of Madène el Mrakib, associations R–U were sampled from the limited the water exchange between the two basins; this implies a Tournaisian of Aguelmous. further reduction of water exchange during eustatic sea-level low- stands. By contrast, during lowstands, some areas might have been more oxygenated because wave action reached closer to the sediment Hartenfels and Becker, 2016a). Anoxic conditions during the deposition surface. Another factor we have not assessed yet is the influence of fresh of the Annulata Black Shales were reported from geochemical analyses water from the surrounding land. The existence of rivers is documented of southern Poland as well, although they were interrupted by a better by local occurrences of fine clastic sediments and trunks of Archae- oxygenated phase (Racka et al., 2010). Annulata Black Shales with oc- opteris in the Maïder and Tafilalt Basins (Wendt and Belka, 1991). currences of pelagic species and the opportunistic bivalve Guerichia were reported worldwide (Becker, 1993; Becker and House, 1997; Sanz- 4.1.3. Middle Famennian Annulata black shales López et al., 1999; Becker and House, 2000; Sandberg et al., 2002; During the deposition of the Annulata Black Shales, the ecosystem Korn, 1999, 2002, 2004; Becker et al., 2004; Hartenfels et al., 2009; was depleted with only two species represented by nektonic cephalo- Hartenfels and Becker, 2016a). ff pods only at Madène el Mrakib. However, 25 species of cephalopods Bio-events do not always strongly a ect the ecospace: e.g., the ff (including seven ammonoid genera) were previously reported from the global species richness in bivalves was a ected while the ecological entire Platyclymenia horizon of the Maïder (Korn, 1999; Korn et al., diversity stayed stable throughout Earth's history (Mondal and Harries, 2014, 2015a, b; Fig. 7: association J; Fig. 9A; Table S1). Hartenfels and 2016). However, on the regional scale and including higher time-stra- ff Becker (2016a) reported some benthic taxa from the Lower Annulata tigraphic resolution and di erent invertebrate groups, ecospace might Event interval of Mrakib such as small gastropods and guerichid bi- be more variable. The ecospace use can quickly change as well; for valves. The dominance of pelagic taxa in our section of Madène el example, the association that follows the Annulata Black Shales is quite fl Mrakib and the possible occurrence of benthos tolerant to oxygen de- diverse, thus re ecting a rapid recovery of the biota corresponding to a pletion indicates anoxic to dysoxic conditions at the bottom caused by a global and rapid drop of the sea level (22 species including several global transgression (Haq and Schutter, 2008; Hartenfels, 2011; benthic lifestyles and abundant ammonoids are present; Figs. 4A, 9A, C: 39  Chapter I: Alpha Diversity and Palaeoecology

L. Frey et al. 3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ² association K). The biota recovered faster than after the Kellwasser Crisis, probably because the Annulata Event caused less profound eco- logical changes. Diversity data of the complete invertebrate associa- tions are missing from the overlying middle Famennian interval. However, three ammonoid-based samples show that at least in this group, no major changes were occurring (five to seven genera are present) and therefore, environmental conditions might have stayed similar. In the late Fammenian parts of our section at Madène el Mrakib, we did not find any black shales corresponding to the Dasberg Crisis at the transition of the Lower/Middle expansa conodont Zone, although it has been documented from the Maïder Basin (Becker, 1993; Kaiser et al., 2008; Hartenfels and Becker, 2009). Fig. 8. Species abundance of Famennian gnathostomes in the phyllocarid layer of the southern Maïder region (northeastern Anti-Atlas, Morocco). 4.1.4. Latest Famennian and Hangenberg black shale equivalent The uppermost Famennian sedimentary succession at Madène el the ammonoid diversity at Aguelmous. But the regional sea level (Bou Mrakib is largely covered by the scree of massive sandstone blocks of Tlidat, Kaiser et al., 2011) remained high during this interval and from the Fezzou Formation (Hangenberg Sandstone equivalent). In the scree, several localities of the Tafilalt, a second eustatic transgression was we found material of several ammonoid species and only few benthic reported (Lower Alum Shale Event, early/middle Tournaisian organisms. Ammonoid samples (benthos is underrepresented with very boundary; crenulata biozone), that favored pelagic life (Kaiser et al., few specimens of nuculid bivalves, rhynchonellid and chonetid bra- 2008, 2011, 2015). The Lower Alum Shale Event caused extinction in chiopods as well as crinoids) from Madène el Mrakib do not show any several groups, however in ammonoids probably only at species level major changes in the Gonioclymenia horizon (seven genera are present (Kaiser et al., 2011, 2015; see ammonoid record in Ebbighausen and like in the preceding, i.e., slightly older, late Famennian strata; Korn Bockwinkel, 2007). et al., 2015a; Korn et al., 2016a, b; Table S3). However, only one am- monoid genus is present in the Kalloclymenia to Wocklumeria horizons of Madène el Mrakib. When comparing collections from other localities in 4.2. Diversity and palaeoecology of gnathostomes the Maïder (Lambidia, Tourirt and Bou Tlidat), these comprise seven ammonoid genera and therefore, some species might have been missed Similar to the invertebrates, the Famennian vertebrate diversity of at Madène el Mrakib due to insufficient sampling effort and the spatial the Maïder Basin was depleted (placoderms: Dunkleosteus, Titanichthys, variation of the fossil record. Driscollaspis sp. nov., an undescribed placoderm; chondrichthyans: The associations of Hangenberg Black Shale equivalent contain a Phoebodus sp., two undescribed cladodonts; sarcopterygian: higher overall diversity including more benthos represented by bivalves Onychodontidae; actinopterygian: aff. Moythomasia)(Figs. 4C, 8, 9B). (especially Guerichia elliptica) and bryozoans (but possibly as epizoans Previously reported microremains of chondrichthyans from the middle on ammonoids) as well as bioturbation (small and ubiquitous Famennian (Palmatolepis trachytera and Pa. postera zones) of the Maïder Chondrites) compared with the Annulata Black Shales (Fig. 4: associa- include similar faunal components (Thrinacodus tranquillus, Stetha- tions P–Q; Fig. 9C). The abundance of bioturbation indicates that the canthus, possibly Cobelodus, Denaea, undetermined cladodonts) and Hangenberg Black Shale equivalent was deposited under hypoxic rather pointed at a low diversity as well (Derycke et al., 2008; Derycke et al., than entirely anoxic conditions, or at least with varying levels of oxygen 2014, 2017). The pelagic and highly to moderately mobile predators (Klug et al., 2016) at Madène el Mrakib. This finding does not contra- (except for the supposedly filter feeding placoderm Titanichthys) pre- dict results of geochemical analyses of sections in localities of Morocco ferably preyed on other pelagic organisms such as cephalopods, fishes and southern Europe that revealed evidence for anoxia during the de- and phyllocarids (Williams, 1990; Mapes et al., 1995) this might ex- position of the Hangenberg Black Shale (Kaiser, 2005, Kaiser et al., plain the high abundance of gnathostomes (especially chondrichthyans: 2006, 2008), because all these benthic organisms (reflected also in the 23 individuals) in the phyllocarid layer. A co-occurrence of crustaceans trace fossils) were likely tolerant towards low oxygen levels at the sea- and gnathostomes is known from Frasnian rocks of the Gogo-Formation floor. Sea-level curves for the Devonian of Morocco show a transgres- of Australia (Briggs et al., 2011) as well as the Cleveland Shale in the sion during the deposition of the Hangenberg Black Shales followed by USA (Williams, 1990) and indicates that crustaceans could have been a a regression in the overlying Hangenberg Sandstone equivalent (Kaiser, nutritive food source for early vertebrates. However, it has to be con- 2005; Kaiser et al., 2011, 2015). Similarly, the global sea level curve sidered that the preservational probability was higher in these layers at shows a transgression followed by a regression during the Hangenberg these localities as even small phyllocarids have been preserved. The Crisis (Haq and Schutter, 2008). deposition of the Moroccan phyllocarid layer coincides with a global regressive cycle showing that the gnathostome preferred an environ- 4.1.5. Early and middle Tournaisian ment that was shallower and better ventilated. However, when com- During the early to middle Tournaisian of Aguelmous, nektonic pared to the regional sea-level curve (Fig. 9B), these correlations are not cephalopods were flourishing while benthic organisms were rare (bi- evident. valves, tabulate and rugose corals, gastropods, bellerophontids, bra- Gnathostome abundance and diversity is much lower (one to two chiopods, spiriferids; Fig. 6, Table S3, association R–U) with some ex- species of placoderms) in the upper parts of the middle and upper ceptions in the Maïder and Tafilalt. This is reflected in the scarcity of Famennian sedimentary rocks where cephalopods and brachiopods are strata with abundant bioturbation, but this might be a wrong im- most common. Last occurrences of vertebrates, namely two teeth of pression rooting in the fact that the fine-grained siliciclastic sediments ischnacanthid acanthodians, were found in the Hangenberg Black Shale (claystones, siltstones and fine-grained sandstones) are deeply weath- equivalent of Madène el Mrakib, although the potential for the pre- ered and often covered by scree (personal observation by CK). How- servation of vertebrate macroremains is high in these shales (Klug et al., ever, the samples are biased (sampling) towards ammonoids what is 2016). Nevertheless, the upper Famennian rocks (Pa. expansa Zone) of reflected by the almost parallel curves of the ammonoid genera and the adjacent Tafilalt region (northeastern Anti-Atlas, Morocco) are rich total species richness. Haq and Schutter (2008) reported a sea-level rise in gnathostome microremains (Ginter et al., 2002). Generally, the followed by a drop in the sandbergi Zone which could have decreased middle and upper Famennian carbonates of the Tafilalt region are more 40  Chapter I: Alpha Diversity and Palaeoecology

L. Frey et al. 3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ²

Fig. 9. Conodont zones (after Ziegler and Sandberg, 1984), ammonoid horizons (after Becker et al., 2002, Korn et al., 2014) and eustatic sea levels of the Famennian and Early Tournaisian according to Haq and Schutter (2008). Regional sea level is adopted from Wendt and Belka (1991) for the Famennian and from Kaiser et al. (2011) for the Tournaisian. Arrows mark regional fluctuations proposed by this work here. A – Changes in diversity: invertebrates of Madène el Mrakib and Aguelmous (brown); number of ammonoid genera (blue) B – Gnathostome diversity of the Maïder (light purple); microremains of the Maïder from Derycke et al. (2008) (dark purple); gnathostomes of the Tafilalt according to Ginter et al. (2002) and Rücklin and Clément (2017) (orange). Exact positions of vertebrate assemblages within the conodont zones are unknown. C – Changes in pelagic-to-benthic lifestyle ratio within ecospace at Madène el Mrakib and Aguelmous. Dashed lines: sufficient samples are missing.

41  Chapter I: Alpha Diversity and Palaeoecology

L. Frey et al. 3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ² diverse compared to the Maïder Basin in yielding about 17 pelagic and occurrence of benthic lifestyles, we propose that changes in regional benthic species of the chondrichthyan genera Jalodus, Thrinacodus, sea-level and their effects were stronger than previously thought; this Phoebodus, Ctenacanthus, Stethacanthus, Symmorium, Cobelodus, Denaea, applies in particular to the beginning of the middle Famennian and Protacrodus, Siamodus, Clairina (Derycke, 1992, 2017; Ginter et al., around the Annulata Black Shales. A fluctuating sea level is also sup- 2002). There is a clear difference in preservation of cartilaginous fishes: ported by changes in sedimentological composition (alternating clay, more or less complete skeletons in the Maïder versus exclusively mi- marls and nodular limestone) in the Maïder. croremains in the Tafilalt. These differences in gnathostome ecology, Reduction of ecospace occupation (especially in benthic lifestyles) diversity and preservation likely resulted from different environmental occurred after and during bio-events: The slightly recovered biota after conditions between the two regions. The Maïder Basin was deeper than the Kellwasser crises was strongly affected during the late Famennian, the Tafilalt pelagic ridge and the western part of the Tafilalt Basin and which is reflected in a low ecological diversity (two modes of life) was isolated from the open ocean by land and shallow marine areas during the deposition of the Annulata Black Shales. Although the biota (Wendt, 1985, 1995; Wendt et al., 2006; Fröhlich, 2004; Lubeseder recovered rapidly from this bio-event (seven modes of life), the ecolo- et al., 2010) and therefore, the Maïder Basin and especially its bottom gical diversity declined again during the Wocklumeria horizon and the waters were not well ventilated at all times. These conditions could Hangenberg Crisis (five and two modes of life). The biota did not re- explain the poor diversity in invertebrates (especially benthos) and cover very quickly from these crises and ecological depletion persisted vertebrates. Additionally, this partially explains the preservation of during the early Tournaisian. articulated vertebrate skeletons as strong currents and scavengers were Attention should not solely be paid to big events (Kellwasser and rare or absent close to the sediment surface. Hangenberg crises) but also to small-scale environmental changes (e.g. In the Tournaisian (Early Carboniferous), neither the Maïder nor the Condroz, Annulata and Dasberg events) as well as other environmental Tafilalt was rich in vertebrates. This is in accordance with the global and ecological changes during the Famennian. Unstable biota fluctu- fossil record of vertebrates. With a few exceptions (Alekseev et al., ating in numbers of species and modes of life might have been affected 1994), early Tournaisian vertebrates are globally rare and even the even more strongly by mass-extinctions than biota in stable ecosystems. extremely diverse late Famennian gnathostome fauna of the Cleveland It is hardly assessable how the changes in environmental conditions and Shales vanished entirely (Hansen, 1996; Friedman and Sallan, 2012). invertebrate ecology affected the accompanying vertebrates due to the Environmental perturbations during the late Famennian might have comparably low diversity and abundance of gnathostomes in the strongly affected the ecosystem but the environment in the Tournaisian Maïder Basin (except for the phyllocarid layer where phyllocarids were itself was probably not suitable for a diverse gnathostome ecosystem. abundant and likely a suitable prey). Nevertheless, biotic interactions Living conditions were probably suitable for some pelagic but not for are probable and strong fluctuations in the abundance and diversity of benthic gnathostomes due to high sea levels, and an environment primary consumers (invertebrates) disturbed the local food web and dominated by pelagic cephalopods. represent the likely explanation for the limited abundance and diversity It has to be considered that the biota reacted not only to abiotic but of secondary and third level consumers (gnathostomes). In order to indirectly also to biotic changes. Biotic factors as causes for changes in obtain more information about the impact of small-scale events and ancient ecosystem are often dismissed because direct evidence of botic environmental changes on regional and global biota of the end- interactions (e.g. stomach contents) are rarely preserved (Williams, Devonian, it is necessary to examine ecospace occupation of in- 1990; Martill et al., 1994; Cavin, 1996; Richter and Baszio, 2001; vertebrates as well as vertebrates in other localities during this time McAllister, 2003; Kriwet et al., 2008; Sallan et al., 2011; Zatoń et al., interval. 2017; Chevrinais et al., 2017). In the case of the Famennian and Tournaisian of the Maïder, pre- Acknowledgments vailing anoxic to dysoxic conditions at the seafloor likely limited ben- thonic life (primary consumers), important food source for small fishes We thank the Swiss National Fond for supporting this project (S- (secondary consumers), which, in turn, represent prey for bigger fishes 74602-11-01) and the NWO, VIDI 864.14.009 to support the colla- such as predatory placoderms and chondrichthyans (third level con- boration of Martin Rücklin. The Ministère de l'Energie, des Mines, de sumers). Moreover, the missing predation pressure by gnathostomes on l'Eau et de l'Environnement (Rabat, Morocco) kindly provided permis- the ammonoids during the early Tournaisian might have fostered the sions for fieldwork and sampling. We thank the excellent preparators rapid re-diversification of ammonoid taxa. Patterns like this were de- Christina Brühwiler (University of Zurich), Ben Pabst (Zürich) and scribed from early Carboniferous crinoids that diversified after the ex- Claudine Misérez (Neuchâtel) for their careful work. Many thanks to tinction of their predators (Sallan et al., 2011). However, work on René Kindlimann (Aathal), Michael Coates (University of Chicago) and higher stratigraphic resolution and comparisons among different lo- Michał Ginter for the instructive discussions about Paleozoic and calities have to be carried out in order to test the assumed relationship modern chondrichthyans. We also would like to thank Michael Amler between extinction of predators and a subsequent radiation of ammo- (Köln) for the kind help with the determination of bivalves. We also noids. thank the reviewers (Sandra Kaiser, State Museum of Natural History of Moreover it is hardly assessable to what extend regional migration Stuttgart; Thomas Becker, University of Münster) who helped to im- patterns influenced the biota of the Maïder and therefore, if the regional prove this manuscript. diversity and ecological trends can be fully assigned to the global ecosystem. Appendix A. Supplementary data

5. Conclusions Supplementary data to this article can be found online at https:// doi.org/10.1016/j.palaeo.2017.12.028. Quantitative analyses of 21 invertebrate associations from the Famennian to middle Tournaisian sedimentary rocks of the Maïder References Basin document an ecosystem mostly dominated by pelagic in- vertebrates (particularly cephalopods) and gnathostomes (phoebodont Alekseev, A.A., Lebedev, O.A., Barskov, I.S., Barskova, M.I., Kononova, L.I., Chizova, V.A., and cladodont chondrichthyans, placoderm such as Dunkleosteus and 1994. On the stratigraphic position of the Famennian and Tournaisian fossil verte- brate beds in Andreyevka, Tula Region, Central Russia. Proc. Geol. Assoc. 105, Titanichthys). The ecospace extension of invertebrates reacted to eu- 41–52. static and/or regional sea-level changes that caused fluctuations in Algeo, T.J., Scheckler, S.E., 1998. Terrestrial-marine teleconnections in the Devonian: ventilation and thus, oxygenation of the seafloor. Based on the variable links between the evolution of land plants, weathering processes, and marine anoxic 42  Chapter I: Alpha Diversity and Palaeoecology

L. Frey et al. 3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ²

events. Philos. Trans. R. Soc. Lond. B 353, 113–130. interactions: food web structure in middle to late Devonian fish assemblages with Algeo, T.J., Berner, R.A., Maynard, J.B., Scheckler, S.E., 1995. Late Devonian oceanic exceptional fossilization. Bull. Geosci. 92 (4), 491–510. anoxic events and biotic crises: ‘rooted’ in the evolution of vascular plants. GSA Decombeix, A.L., Meyer-Berthaud, B., Galtier, J., 2011. Transitional changes in arbor- Today 5, 63–66. escent lignophytes at the Devonian-carboniferous boundary. J. Geol. Soc. Lond. 168, Algeo, T.J., Scheckler, S.E., Maynard, J.B., 2001. Effects of Middle to Late Devonian 547–557. spread of vascular land plants and weathering regimes. In: Gensel, P.G., Edwards, D. Denayer, J., Poty, E., Aretz, M., 2011. Uppermost Devonian and Dinantian rugose corals (Eds.), Plants Invade the Land. Columbia University Press, New York, pp. 213–237. from Southern Belgium and surrounding areas. Kölner Forum für Geologie und Alroy, J., 2010. Geographical, environmental and intrinsic biotic controls on Phanerozoic Paläontologie 20, 151–201. marine diversification. Palaeontology 53, 1211–1235. Denison, R., 1978. Handbook of Paleoichthyology. Placodermi, vol. 2 Gustav Fischer, Amler, M.R.W., 1996. Die Bivalvenfauna des Oberen Famenniums West-Europas. 2. Stuttgart. Evolution, Paläogeographie, Paläoökologie, Systematik. 2. Palaeotaxodonta und Derycke, C., 1992. Microrestes de Sélaciens et autres Vertébrés du Dévonien supérieur du Anomalodesmata. Geol. Palaeontol. 30, 49–117. Maroc. Bulletin du Muséum national d'Histoire Naturelle, Section C, Sciences de la Amler, M.R.W., 2004. Late Famennian bivalve, gastropod and bellerophontid molluscs terre, paléontologie, géologie, minéralogie 14 (1), 15–61. from the Refrath 1 Borehole (Bergisch Gladbach-Paffrath Syncline; Ardennes-Rhenish Derycke, C., 2017. Paléobiodiversité des gnathostomes (chondrichthyens, acanthodiens et Massif, Germany). In: Courier Forschungs-Institut Senckenberg. 251. pp. 151–173. actinoptérygiens) du Dévonien du Maroc (NW Gondwana). In: Zouhri, S. (Ed.), Amler, M.R.W., 2006. Bivalven und Rostroconchien. In: Deutsche Stratigraphische Paléontologie des vertébrés du Maroc: état des connaissance, Mémoires de la Société Kommission (Ed.), Stratigraphie von Deutschland VI. Unterkarbon (Mississippium). Géologique de France 180, pp. 624. 41. Schriftenreihe der Deutschen Gesellschaft für Geowissenschaften, pp. 121–146. Derycke, C., Spalletta, C., Perri, M.C., Corradini, C., 2008. Famennian chondrichthyan Andrews, S.M., Long, J., Ahlberg, P., Barwick, R., Campbell, K., 2006. The structure of the microremains from Morocco and Sardinia. J. Paleontol. 82 (5), 984–995. sarcopterygian Onychodus jandemarrai n. sp. from Gogo, Western Australia: with a Derycke, C., Olive, S., Groessens, E., Goujet, D., 2014. Paleogeographical and paleoeco- functional interpretation of the skeleton. Earth Environ. Sci. Trans. R. Soc. Edinb. 96, logical constraints on Paleozoic vertebrates (chondrichthyans and placoderms) in the 197–307. Ardenne Massif Shark radiations in the Famennian on both sides of the Palaeotethys. Becker, R.T., 1986. Ammonoid evolution before, during and after the “Kellwasser-even- Palaeogeogr. Palaeoclimatol. Palaeoecol. 414, 61–67. t”—revien and preliminary new results. Global Bio-Events 181–188. Dreesen, R., Paproth, E., Thorez, J., 1988. Events documented in Famennian sediments Becker, R.T., 1993. Anoxia, eustatic changes, and Upper Devonian to lowermost (Ardenne-Rhenish Massif, Late Devonian, NW Europe). In: Devonian of the World: Carboniferous global ammonoid diversity. In: House, M.R. (Ed.), The Ammonoidea: Proceedings of the 2nd International Symposium on the Devonian System — Memoir Environment, Ecology, and Evolutionary Change. Systematic Association Special 14. Sedimentation, vol. II. pp. 295–308. Volume 47. pp. 115–164. Droser, M.L., Bottjer, D.J., Sheehan, P.M., McGhee Jr., G.R., 2000. Decoupling of taxo- Becker, R.T., 1995. Taxonomy and Evolution of Late Famennian Tornocerataceae nomic and ecologic severity of Phanerozoic marine mass extinctions. Geology 28 (8), (Ammonoidea). Berl. Geowiss. Abh. 16, 607–643. 675–678. Becker, R.T., 2002. Alpinites and other Posttornoceratidae (Goniatitida, Famennian). In: Ebbighausen, V., Bockwinkel, J., 2007. Tournaisian (Early Carboniferous/Mississippian) Mitteilungen der Museum für Naturkunde, Geowisse-schaftliche Reihe. 5. pp. 51–73. ammonoids from the Ma'der Basin (Anti-Atlas, Morocco). Fossil Record 10 (2), Becker, R.T., House, M.R., 1997. Sea-level changes in the Upper Devonian of the Canning 125–163. Basin, Western Australia. Cour. Forschungsinst. Senck. 199, 129–146. Fortey, R.A., 2004. The lifestyles of the trilobites. Am. Sci. 92, 446–453. Becker, R.T., House, M.R., 2000. Devonian ammonoid zones and their correlation with Fortey, R.A., Owens, R.M., 1999. Feeding habits in trilobites. Palaeontology 42 (3), established series and stage boundaries. Cour. Forschungsinst. Senck. 220, 113–151. 429–465. Becker, R.T., Bockwinkel, J., Ebbighausen, V., House, M.R., 2000. Jebel Mrakib, Anti- Frey, L., Naglik, C., Hofmann, R., Schemm-Gregory, M., Frýda, J., Kröger, B., Taylor, P.D., Atlas (Morocco), a potential Upper Famennian substage boundary stratotype section. Wilson, M.A., Klug, C., 2014. Diversity and palaeoecology of early Devonian in- In: Notes et Mémoires du Service géologique Maroc. 399. pp. 75–86. vertebrate associations in the Tafilalt (Anti-Atlas, Morocco). Bull. Geosci. 89 (1), Becker, R.T., House, M.R., Bockwinkel, J., Ebbighausen, V., Aboussalam, Z.S., 2002. 75–112. Famennian ammonoid zones of the eastern anti-atlas (southern Morocco). In: Friedman, M., Sallan, L.C., 2012. Five hundred million years of extinction and recovery: a Münstersche Forschungen zur Geologie und Paläontologie. 93. pp. 159–205. Phanerozoic survey of large-scale diversity patterns in fishes. Palaeontology 55 (4), Becker, R.T., Ashouri, A.R., Yazdi, M., 2004. The upper Devonian Annulata event in the 707–742. Shotori range (eastern Iran). Neues Jahrb. Geol. Palaontol. Abh. 119–143. Fröhlich, S., 2004. Evolution of a Devonian carbonate shelf at the northern margin of Becker, R.T., Kaiser, S.I., Aboussalam, Z.S., 2006. The Lower Alum Shale Event (Middle Gondwana (Jebel Rheris,eastern Anti-Atlas, Morocco) (Unpublished PhD Thesis). Tournaisian) in Morocco – facies and faunal changes. In: Aretz, M., Herbig, H.-G University of Tübingen, Germany. (Eds.), Carboniferous Conference Cologne, From Platform to Basin. Kölner Forum für Gereke, M., Schindler, E., 2012. “Time-specific facies” and biological crisis — the Geologie und Paläontologie, Program and Abstracts. 15. pp. 7–8. Kellwasser event interval near the Frasnian/Famennian boundary (Late Devonian). Becker, R.T., Gradstein, F.M., Hammer, O., 2012. The Devonian period. In: Gradstein, Palaeogeogr. Palaeoclimatol. Palaeoecol. 367–368, 19–29. F.M., Ogg, J.G., Schmitz, M.D., Ogg, G.M. (Eds.), The Geologic Time Scale. Elsevier, Ginter, M., Hairapetian, V., Klug, C., 2002. Famennian chondrichthyans from the shelves pp. 559–603. of North Gondwana. Acta Geol. Pol. 52 (2), 169–215. Becker, R.T., Kaiser, S.I., Aretz, M., 2016. Review of chrono-, litho- and biostratigraphy Ginter, M., Hampe, O., Duffin, C.J., 2010. Chondrichthyes: Paleozoic Elasmobranchii: across the global Hangenberg crisis and Devonian–carboniferous boundary. Geol. teeth. In: Schultze, H. (Ed.), Handbook of Paleoichthyology. vol. 3D 168 p. Soc. Lond., Spec. Publ. 423 (1), 355–386. Goddéris, Y., Joachimski, M.M., 2004. Global change in the Late Devonian: modelling the Bond, D.P.G., Wignall, P.B., 2008. The role of sea-level change and marine anoxia in the Frasnian-Famennian short-term carbon isotope excursions. Palaeogeogr. Frasnian-Famennian (Late Devonian) mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoclimatol. Palaeoecol. 202, 309–329. Palaeoecol. 263, 107–118. Grimm, M.G., 1998. Systematik und Paläoökologie der Buchiolinae nov. subfam. Bond, D., Wignall, P.B., Racki, G., 2004. Extent and duration of marine anoxia during the Schweizerische Paläontologische Abhandlungen 118, 1–176. Frasnian–Famennian (Late Devonian) mass extinction in Poland, Germany, Austria Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Palaeontological statistics software and France. Geol. Mag. 141 (2), 173–193. package for education and data analysis. Palaeontol. Electron. 4 (1), 1–9. Briggs, D.E.G., Rolfe, W.D.I., Butler, P.D., Liston, J., Ingham, J.K., 2011. Phyllocarid Hampe, O., Aboussalam, Z.S., Becker, R.T., 2004. Omalodus teeth (Elasmobranchii: crustaceans from the upper Devonian Gogo formation, Western Australia. J. Syst. Omalodontida) from the northern Gondwana margin (middle Givetian: ansatus con- Palaeontol. 9 (3), 399–424. odont Zone, Morocco). In: Arratia, G., Wilson, M.V.H., Cloutier, R. (Eds.), Recent Buggisch, W., 1991. The global Frasnian-Famennian “Kellwasser event”. Geol. Rundsch. Advances in the Origin and Early Radiation of Vertebrates, pp. 487–504. 80 (1), 49–72. Hansen, M.C., 1996. Phylum Chordata–vertebrate fossils. In: Feldman, R.M. (Ed.), Fossils Bush, A.M., Bambach, R.K., Daley, G.M., 2007. Changes in theoretical ecospace utilization of Ohio. Bulletin 70. Division of Geological Survey, Columbus 288–369 pp. in marine fossil assemblages between the mid-Paleozoic and late Cenozoic. Haq, B.U., Schutter, S.R., 2008. A chronology of Paleozoic sealevel changes. Science 322, Paleobiology 33 (1), 76–97. 64–68. Caplan, M.L., Bustin, R.M., 1999. Devonian-carboniferous Hangenberg mass extinction Hartenfels, S., 2011. Die globalen Annulata-Events und die Dasberg-Krise (Famennium, event, widespread organic-rich mudrock and anoxia: causes and consequences. Oberdevon) in Europa und Nord-Afrika – hochauflösende Conodonten-Stratigraphie, Palaeogeogr. Palaeoclimatol. Palaeoecol. 148, 187–207. Karbonat-Mikrofazies, Paläoökologie und Paläodiversität. Münstersche Forschungen Carmichael, S.K., Waters, J.A., Batchelor, C.J., Coleman, D.M., Suttner, T.J., Kido, E., zur Geologie und Paläontologie 105, 1–527. McCain Moore, L., Chadimová, L., 2015. Climate instability and tipping points in the Hartenfels, S., Becker, R.T., 2009. Timing of the global Dasberg crisis–implications for Late Devonian: detection of the Hangenberg event in an open oceanic island arc in Famennian eustasy and chronostratigraphy. Palaeontogr. Am. 63, 71–97. the Central Asian Orogenic Belt. Gondwana Res. 32, 213–231. Hartenfels, S., Becker, R.T., 2016a. The global annulata events: review and new data from Carr, R.K., 2008. Paleoecology of Dunkleosteus terrelli (Placodermi: Arthrodira). In: the Rheris Basin (northern Tafilalt) of SE Morocco. In: Becker, R.T., Königshof, P., Kirtlandia. 57. pp. 36–45. Brett, C.E. (Eds.), Devonian Climate, Sea Level and Evolutionary Events. 423 Carr, R.K., Jackson, G.L., 2008. The vertebrate fauna of the Cleveland member Geological Society, London, Special Publications. http://dx.doi.org/10.1144/ (Famennian) of the Ohio Shale. In: Guide to the Geology and Paleontology of the SP423.14. Cleveland Member of the Ohio Shale. 68th Annual Meeting of the Society of Hartenfels, S., Becker, R.T., 2016b. Age and correlation of the transgressive Vertebrate Paleontology, Cleveland, Ohio. Gonioclymenia limestone (Famennian, Tafilalt, eastern Anti-Atlas, Morocco). Geol. Cavin, L., 1996. Supposed and direct evidence of trophic relationships within the marine Mag. 1–44. fish community from the Lower Turonian of Goulmima, Morocco. In: First European Hartenfels, S., Becker, R.T., Tragelehn, H., 2009. Marker conodonts around the global Workshop on Vertebrate Palaeontology. Online Series 1 Geological Society of Annulata Events and the definition of an Upper Famennian substage. In: Denmark. Subcommission on Devonian Stratigraphy Newsletter. 24. pp. 40–45. Chevrinais, M., Jacquet, C., Cloutier, R., 2017. Early establishment of vertebrate trophic House, M.R., 1985. Correlation of mid-Palaeozoic ammonoid evolutionary events with 43  Chapter I: Alpha Diversity and Palaeoecology

L. Frey et al. 3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ²

global sedimentary perturbations. Nature 313, 17–22. Kriwet, J., Witzmann, F., Klug, S., Heidtke, U.H., 2008. First direct evidence of a verte- House, M.R., 2002. Strength, timing, setting and cause of mid-Palaeozoic extinctions. brate three-level trophic chain in the fossil record. Proc. R. Soc. Lond. B Biol. Sci. 275 Palaeogeogr. Palaeoclimatol. Palaeoecol. 181, 5–25. (1631), 181–186. Jaekel, O., 1919. Die Mundbildung der Placodermen. In: Sitzungsberichte der Gesellschaft Kříž, J., 2004. Latest Frasnian and earliest Famennian (Late Devonian) bivalves from the Naturforschender Freunde, Berlin. 1919. pp. 73–110. Montagne Noire (France). In: Senckenbergiana lethaea. 84. pp. 85–123. Joachimski, M.M., Buggisch, W., 2002. Conodont apatite δ18O signatures indicate cli- Lehman, J.P., 1956. Les Arthrodires du Dévonien supérieur du Tafilalt (Sud Marocain). In: matic cooling as a trigger of the late Devonian mass extinction. Geology 30 (8), Notes et Mémoires du Service Géologique du Maroc. 129. pp. 1–70. 711–714. Lehman, J.P., 1964. A propos de quelques Arthrodires et Ichthyodorulites sahariens. Joachimski, M.M., Breisig, S., Buggisch, W., Talent, J.A., Mawson, R., Gereke, M., Mémoire IFAN 68, 193–200. Morrow, J.R., Day, J., Weddige, K., 2009. Devonian climate and reef evolution: in- Lehman, J.P., 1976. Nouveaux poissons fossiles du Dévonien du Maroc. In: Annales de sights from oxygen isotopes in apatite. Earth Planet. Sci. Lett. 284, 599–609. Paléontologie Vertébrés. 62. pp. 1–34. Johnson, J.G., Klapper, G., Sandberg, C.A., 1985. Devonian eustatic fluctuations in Lehman, J.P., 1977. Sur la présence d'un Ostéolépiforme dans le Dévonien supérieur du Euramerica. Geol. Soc. Am. Bull. 96, 567–587. Tafilalt. In: Compte-Rendus de l'Académie des Sciences. 285D. pp. 151–153. Kaiser, S.I., 2005. Mass Extinctions, Climatic and Oceanographic Changes at the Lehman, J.P., 1978. A propos de deux poissons du Famennien du Tafilalt. In: Annales de Devonian/Carboniferous boundary (Unpublished Dissertation). University of Paléontologie Vertébrés. 64. pp. 143–152. Bochum, pp. 1–156. Lelièvre, H., Janvier, P., 1986. L'Eusthénopteridé (Osteichthyes, Sarcopterygii)du Kaiser, S.I., Steuber, T., Becker, R.T., Joachimski, M.M., 2006. Geochemical evidence for Famennian (Dévonien supérieur) du Tafilalt (Maroc): nouvelle description. In: major environmental change at the Devonian–carboniferous boundary in the carnic Bulletin du Muséum National d'Histoire naturelle, 4e Série, Section C, Sciences de la alps and the Rhenish massif. Palaeogeogr. Palaeoclimatol. Palaeoecol. 240 (1), Terre, Paléontologie, Géologie, Minéralogie. 3. pp. 351–365. 146–160. Lelièvre, H., Janvier, P., 1988. Un Actinistien (Sarcopterygii, Vertebrata) dans le Dévonien Kaiser, S.I., Steuber, T., Becker, T., 2008. Environmental change during the late supérieur du Maroc. In: Compte-Rendus de l'Académie des Sciences, Paris. 307. pp. Famennian and early Tournaisian (late Devonian-early carboniferous): implications 1425–1430. from stable isotopes and conodont biofacies in southern Europe. Geol. J. 42, Lelièvre, H., Janvier, P., Blieck, A., 1993. Silurian-Devonian vertebrate biostratigraphy of 241–260. western Gondwana and related terranes (South America, Africa, Armorica-Bohemia, Kaiser, S.I., Becker, R.T., Spalletta, C., Steuber, T., 2009. High-resolution conodont stra- Middle East). In: Palaeozoic Vertebrate Biostratigraphy and Biogeography, pp. tigraphy, biofacies, and extinctions around the Hangenberg event in pelagic succes- 139–173. sions from Austria, Italy, and France. Palaeontogr. Am. 63, 97–139. Long, J.A., Trinajstic, K., 2010. The late Devonian Gogo formation Lägerstatte of Western Kaiser, S.I., Becker, R.T., Steuber, T., Aboussalam, S.Z., 2011. Climate-controlled mass Australia: exceptional early vertebrate preservation and diversity. Annu. Rev. Earth extinctions, facies, and sea-level changes around the Devonian-Carboniferous Planet. Sci. 38, 255–279. boundary in the eastern Anti-Atlas (SE Morocco). Palaeogeogr. Palaeoclimatol. Long, J.A., Large, R.R., Lee, M.S., Benton, M.J., Danyushevsky, L.V., Chiappe, L.M., Palaeoecol. 310, 340–364. Halpin, J.A., Cantrill, D., Lottermoser, B., 2015. Severe selenium depletion in the Kaiser, S.I., Aretz, M., Becker, R.T., 2015. The global Hangenberg crisis Phanerozoic oceans as a factor in three global mass extinction events. Gondwana Res. (Devonian–Carboniferous transition): review of a first-order mass extinction. In: 36, 209–218. Becker, R.T., Königshof, P., Brett, C.E. (Eds.), Devonian Climate, Sea Level and Lubeseder, S., Rath, J., Rücklin, M., Messbacher, R., 2010. Controls on Devonian hemi- Evolutionary Events. Geological Society of London, Special Publications, pp. pelagic limestone deposition analyzed on cephalopod ridge to slope sections, Eastern 387–437. Anti-Atlas, Morocco. Facies 56, 295–315. Kaufmann, B., 1998. Facies, stratigraphy and diagenesis of middle Devonian reef- and Mapes, R.H., Sims, M.S., Boardman, D.R., 1995. Predation on the Pennsylvanian am- mud-mounds in the Mader (eastern Anti-Atlas, Morocco). Acta Geol. Pol. 48, 43–106. monoid Gonioloboceras and its implications for allochthonous vs. autochthonous ac- Kidwell, S.M., Bosence, D.W.J., 1991. Taphonomy and time-averaging of marine shelly cumulations of Goniatites and other ammonoids. J. Paleontol. 69 (3), 441–446. faunas. In: Allison, P.A., Briggs, D.E.G. (Eds.), Releasing the Data Locked in the Fossil Martill, D.M., Taylor, M.A., Duff, K.L., Riding, J.B., Bown, P.R., 1994. The trophic Record. Topics in Geobiology 9. Plenum Press, New York, pp. 113–211. structure of the biota of the Peterborough member, Oxford clay formation (Jurassic), Klein, C., Korn, D., 2014. A morphometric approach to conch ontogeny of Cymaclymenia UK. J. Geol. Soc. Lond. 151, 173–194. and related genera (Ammonoidea, late Devonian). Fossil Record 17 (1), 1–32. Marynowski, L., Rakociński, M., Zatoń, M., 2007. Middle Famennian (late Devonian) Klug, C., Lehmann, J., 2015. Soft part anatomy of ammonoids: reconstructing the animal interval with pyritized fauna from the Holy Cross Mountains (Poland): organic geo- based on exceptionally preserved specimens and actualistic comparisons. In: Klug, C., chemistry and pyrite framboid diameter study. Geochem. J. 41, 187–200. Korn, D., de Baets, K., Kruta, I., Mapes, R.H. (Eds.), Ammonoid Paleobiology, Volume McAllister, J., 2003. Predation of Fishes in the Fossil Record. In: Kelley, P.H., Kowalewski, I: from Anatomy to Ecology. Topics in Geobiology 43. Springer, Dordrecht, pp. M., Hansen, T.H. (Eds.), Predator–Prey Interactions in the Fossil Record. Academic/ 539–552. Plenum Publishers, New York, NY, pp. 303–324. Klug, C., Rücklin, M., Meyer-Berthaud, B., Soria, A., 2003. Late Devonian pseudoplank- McGhee, G.R., 1988. The late Devonian extinction event: evidence for abrupt ecosystem tonic crinoids from Morocco. Neues Jahrbuch für Geologie und Mineralogie 3, collapse. Paleobiology 14 (3), 250–257. 153–163. McGhee, G.R., 1996. The Late Devonian Mass Extinction: The Frasian/Famennian Crises. Klug, C., Kröger, B., Rücklin, M., Korn, D., Schemm-Gregory, M., De Baets, K., Mapes, Columbia University Press, New York (303 p). R.H., 2008. Ecological change during the early Emsian (Devonian) in the Tafilalt McGhee Jr., G.R., 2001. The `multiple impacts hypothesis` for mass extinction: a com- (Morocco), the origin of the Ammonoidea, and the first African pyrgocystid parison of the late Devonian and the late Eocene. Palaeogeogr. Palaeoclimatol. edrioasteroids, machaerids and phyllocarids. Palaeontographica A 283, 1–94. Palaeoecol. 176, 47–58. Klug, C., Frey, L., Korn, D., Jattiot, R., Rücklin, M., 2016. The oldest Gondwanan ce- McGhee Jr., G.R., 2014. When the Invasion of Land Failed: The Legacy of the Devonian phalopod mandibles (Hangenberg black shale, late Devonian) and the mid-palaeozoic Extinctions. Columbia University Press, New York 317 pp. rise of jaws. Palaeontology 19, 611–629. McGhee Jr., G.R., Clapham, M.E., Sheehan, P.M., Bottjer, D.J., Droser, M.L., 2013. A new Korn, D., 1999. Famennian Ammonoid Stratigraphy of the Ma'der and Tafilalt (Eastern ecological severity ranking of major Phanerozoic biodiversity crises. Palaeogeogr. Anti-Atlas, Morocco). Abhandlungen der geologischen Bundesanstalt 54, 147–179. Palaeoclimatol. Palaeoecol. 370, 260–270. Korn, D., 2002. Die Ammonoideen-Fauna der Platyclymenia annulata-Zone vom Miles, R.S., 1969. Features of placoderm diversification and the evolution of the ar- Kattensiepen (Oberdevon, Rheinisches Schiefergebirge). Senckenb. Lethaea 82 (2), throdire feeding mechanism. In: Transactions of the Royal Society of Edinburgh. 68. 557–608. pp. 123–170. Korn, D., 2004. The mid-Famennian ammonoid succession in the Rhenish Mountains: the Mondal, S., Harries, P.J., 2016. Phanerozoic trends in ecospace utilization: the bivalve “annulata Event” reconsidered. Geological Quarterly 48, 245–252. perspective. Earth Sci. Rev. 152, 106–118. Korn, D., Bockwinkel, J., 2017. The genus Gonioclymenia (Ammonoidea; late Devonian) in Murphy, A.E., Sageman, B.B., Hollander, D.J., 2000. Eutrophication by decoupling of the the anti-atlas of Morocco. Neues Jahrb. Geol. Palaontol. Abh. 285 (1), 97–115. marine biogeochemical cycles of C, N, and P: a mechanism for the late Devonian mass Korn, D., Klug, C., 2002. Fossilium Catalogus I: Animalia Pars 138, Ammoneae Devonicae. extinction. Geology 28 (5), 427–430. Backhuys Publishers, Leiden, Netherlands. Nagel, J., 2006. Middle and Upper Devonian Cryptodonta (Bivalvia) from the Pelagic Korn, D., Klug, C., Ebbighausen, V., Bockwinkel, J., 2002. Palaeogeographical meaning of Hercynian Facies - Taxonomy, Stratigraphy, and Paleoecology (Unpublished PhD- a Middle Tournaisian ammonoid fauna from Morocco. Geol. Palaeontol. 36, 79–86. thesis). Westfälischen Wilhelms-Universität, Münster. Korn, D., Bockwinkel, J., Ebbighausen, V., 2014. Middle Famennian (Late Devonian) Nagel-Myers, J., Amler, M.R.W., Becker, R.T., 2009. The Loxopteriinae n. subfam. ammonoids from the Anti-Atlas of Morocco, 1. Prionoceras. Neues Jahrb. Geol. (Dualinidae, Bivalvia): review of a common bivalve taxon from the Late Devonian Palaontol. Abh. 272 (2), 167–204. pelagic facies. Palaeontogr. Am. 63, 167–185. Korn, D., Bockwinkel, J., Ebbighausen, V., 2015a. The late Devonian ammonoid Newell, N.D., 1952. Periodicity in invertebrate evolution. J. Paleontol. 371–385. Mimimitoceras in the Anti-Atlas of Morocco. Neues Jahrb. Geol. Palaontol. Abh. 275 Newell, N.D., 1956. Catastrophism and the fossil record. Evolution 10 (1), 97–101. (2), 125–150. Newell, N.D., 1963. Crises in the history of life. Sci. Am. 208, 77–93. Korn, D., Bockwinkel, J., Ebbighausen, V., 2015b. Middle Famennian (late Devonian) Neyman, A.A., 1967. Limits to the application of the ‘trophic group’ concept in benthic ammonoids from the Anti-Atlas of Morocco, 2. Sporadoceratidae. Neues Jahrb. Geol. studies. In: Oceanology, Academy of Sciences of the USSR. 7. pp. 49–155. Palaontol. Abh. 278 (1), 47–77. Petter, G., 1959. Goniatites devoniénnes du Sahara. In: Publications du Sérvice de la Carte Korn, D., Bockwinkel, J., Ebbighausen, V., 2016a. The late Famennian tornoceratid am- Géologique de l'Algérie, nouvelle série, Paléontologie 2. pp. 1–313. monoids in the Anti-Atlas of Morocco. Neues Jahrb. Geol. Palaontol. Abh. 281 (2), Petter, G., 1960. Clymènies du Sahara. In: Publications du Sérvice de la Carte Géologique 201–220. de l'Algérie, nouvelle série, Paléontologie 6. pp. 1–58. Korn, D., Bockwinkel, J., Ebbighausen, V., 2016b. Middle Famennian (late Devonian) Playford, P.E., 1980. The Devonian “great barrier reef” of the Canning Basin, Western ammonoids from the Anti-Atlas of Morocco. 3. Tornoceratids. Neues Jahrb. Geol. Australia. Am. Assoc. Pet. Geol. 64, 814–840. Palaontol. Abh. 281 (3), 267–281. Poty, E., 1999. Famennian and Tournaisian recoveries of shallow water Rugosa following 44  Chapter I: Alpha Diversity and Palaeoecology

L. Frey et al. 3DODHRJHRJUDSK\3DODHRFOLPDWRORJ\3DODHRHFRORJ\  ²

late Frasnian andblate Strunian major crisis, southern Belgium and surrounding area, 1970 (1), 34–39. Hunan (South China) and the Omolon region (NE Siberia). Palaeogeogr. Siegmund, H., Trappe, J., Oschmann, W., 2002. Sequence stratigraphic and genetic as- Palaeoclimatol. Palaeoecol. 154, 11–26. pects of the Tournaisian ‘Liegender Alaunschiefer’ and adjacent beds. Int. J. Earth Sci. Racka, M., Marynowski, L., Filipiak, P., Sobstel, M., Pisarzowska, A., Bond, D.P.G., 2010. 91, 934–949. Anoxic Annulata events in the late Famennian of the Holy Cross Mountains (southern Siveter, D.J., Vannier, J., Palmer, D., 1991. Silurian myodocopes: pioneer pelagic os- Poland): geochemical and palaeontological record. Palaeogeogr. Palaeoclimatol. tracodes and the chronology of an ecological shift. J. Micropalaeontol. 10, 151–173. Palaeoecol. 297, 549–575. Sokiran, E.V., 2002. Frasnian–Famennian extinction and recovery of rhynchonellid bra- Racki, G., 1990. Frasnian/Famennian event in the Holy Cross Mts, Central Poland: stra- chiopods from the east European platform. Acta Palaeontol. Pol. 47 (2), 339–354. tigraphic and ecologic aspects. In: Kauffman, E.G., Walliser, A. (Eds.), Extinction Spalletta, C., Perri, M.C., Over, D.J., Corradini, C., 2017. Famennian (Upper Devonian) Events in Earth History. Lecture Notes in Earth Sciences. 30. pp. 169–181. conodont zonation: revised global standard. Bull. Geosci. 92 (1), 31–57. Racki, G., 2005. Toward understanding Late Devonian global events: few answers, many Struve, W., 1990. Beiträge zur Kenntnis der Phacopina (Trilobita), 18: Die Riesen- questions. In: Over, D.J., Morrow, J.R., Wignall, P.B. (Eds.), Understanding Late Phacopiden aus dem Ma'der, SEmarokkanische Prä-Sahara. Senckenb. Lethaea 75 (1/ Devonian and Permian-Triassic Biotic and Climatic Events: Towards an Integrated 2), 77–129. Approach. Elsevier, Amsterdam, pp. 337. Termier, H., 1936. Etudes géologiques sur le Maroc central et le Moyen atlas septen- Raup, D.M., Sepkoski, J.J., 1982. Mass extinctions in the marine fossil record. Science trional. Notes et Mémoires Service des Mines et de la carte géologique du Maroc 33 215, 1501–1503. 1566p. Richter, G., Baszio, S., 2001. Traces of a limnic foodweb in the Eocene Lake Messel—a Tessitore, L., Naglik, C., De Baets, K., Galfetti, T., Klug, C., 2016. Neptunian dykes in the preliminary report based on fish coprolite analyses. Palaeogeogr. Palaeoclimatol. Devonian carbonate buildup Aferdou El Mrakib (eastern Anti-Atlas, Morocco) and Palaeoecol. 166, 345–368. implications for its growth. Neues Jahrb. Geol. Palaontol. Abh. 281 (3), 247–266. Riquier, L., Tribovillard, N., Averbuch, O., Devleeschouwer, X., Riboulleau, A., 2006. The Thayer, C.W., Steele-Petrovic, H.M., 1975. Burrowing of the lingulid brachiopod Glottidia late Frasnian Kellwasser horizons of the Harz Mountains (Germany): two oxygen- pyramidata: its ecological and paleoecologic significance. Lethaia 8, 209–221. deficient periods resulting from different mechanisms. Chem. Geol. 233 (1), 137–155. Vannier, J., Abe, K., 1993. Functional morphology and behaviour of Vargula hilgendorfii Rücklin, M., 2010. A new Frasnian placoderm assemblage from the eastern anti-atlas, (Ostracoda, Myodocopida). J. Crustac. Biol. 13, 51–76. Morocco, and its palaeobiogeographical implications. Palaeoworld 19, 87–93. Vannier, J., Boissy, P., Racheboeuf, P.R., 1997. Locomotion in Nebalia bipes: a possible Rücklin, M., 2011. First selenosteid placoderms from the eastern Anti-Atlas of Morocco; model for Palaeozoic phyllocarid crustaceans. Lethaia 30, 89–104. osteology, phylogeny and palaeogeographical implications. Palaeontology 54, 25–62. Walliser, O.H., 1996. Global events in the Devonian and Carboniferous. In: Walliser, O.H. Rücklin, M., Clément, G., 2017. Une revue des Placodermes et Sarcoptérygiens du (Ed.), Global Events and Event Stratigraphy in the Phanerozoic, pp. 225–250. Dévonien du Maroc. In: Zouhri, S. (Ed.), Paléontologie des vertébrés du Maroc: état Webster, G.D., Becker, R.T., Maples, C.G., 2005. Biostratigraphy, paleoecology, and des connaissance, Mémoires de la Société Géologique de France. 180. pp. 624. taxonomy of Devonian (Emsian and Famennian) crinoids from southeastern Morocco. Rücklin, M., Long, J.A., Trinajstic, K., 2015. A new selenosteid arthrodire (‘Placodermi’) J. Paleontol. 79 (6), 1052–1071. from the Late Devonian of Morocco. J. Vertebr. Paleontol. 35 (2), 1–13 e908896. Wendt, J., 1985. Disintegration of the continental margin of northwestern Gondwana: Sallan, L.C., Coates, M.I., 2010. End Devonian extinction and a bottleneck in the early late Devonian of the eastern Anti-Atlas (Morocco). Geology 13, 815–818. evolution of modern jawed vertebrates. Proc. Natl. Acad. Sci. 107 (22), Wendt, J., 1995. Shell directions as a tool in palaeocurrent analysis. Sediment. Geol. 95, 10131–10135. 161–186. Sallan, L.C., Galimberti, A.K., 2015. Body-size reduction in vertebrates following the end- Wendt, J., Belka, Z., 1991. Age and depositional environment of Upper Devonian (early Devonian mass extinction. Science 350 (6262), 812–815. Frasnian to early Famennian) black shales and limestones (Kellwasser facies) in the Sallan, L.C., Kammer, T.W., Ausich, W.I., Cook, L.A., 2011. Persistent predator–prey eastern Anti-Atlas, Morocco. Facies 25, 51–90. dynamics revealed by mass extinction. Proc. Natl. Acad. Sci. 108 (20), 8335–8338. Wendt, J., Kaufmann, B., Belka, Z., Klug, C., Lubeseder, S., 2006. Sedimentary evolution Sandberg, C.A., Ziegler, W., Leuteritz, K., Brill, S.M., 1978. Phylogeny, speciation, and of a Palaeozoic basin and ridge system: the Middle and Upper Devonian of the Ahnet zonation of Siphonodella (Conodonta, upper Devonian and lower carboniferous). and Mouydir (Algerian Sahara). Geol. Mag. 143 (3), 269–299. Newsl. Stratigr. 7 (2), 102–120. Westermann, G.E.G., 1999. Life of habits of nautiloids. In: Savazzi, E. (Ed.), Functional Sandberg, C.A., Morrow, J.R., Ziegler, W., 2002. Late Devonian sea-level changes, cata- Morphology of the Invertebrate Skeleton. John Wiley and Sons, New York, pp. strophic events, and mass extinctions. In: Koeberl, C., MacLeod, K.G. (Eds.), 263–298. Catastrophic Events and Mass Extinctions: Impacts and Beyond, Geological Society of Westermann, G.E.G., Tsujita, C.J., 1999. Life habits of ammonoids. In: Savazzi, E. (Ed.), America, Special Papers 356, pp. 473–487. Functional Morphology of the Invertebrate Skeleton. John Wiley and Sons, New York, Sanz-López, J., García-López, S., Montesinos, J.R., Arbizu, M., 1999. Biostratigraphy and pp. 299–325. sedimentation of the vidrieros formation (middle Famennian–lower Tournaisian) in Wignall, P.B., Simms, M.J., 1990. Pseudoplankton. Palaeontology 33, 359–378. the Gildar–Montó unit (northwest Spain). Boll. Soc. Paleontol. Ital. 37, 393–406. Williams, M.E., 1990. Feeding behavior in Cleveland shale fishes. In: Boucot, A.J. (Ed.), Sartenaer, P., 1998. The presence in Morocco of the late Famennian genus Hadyrhyncha Evolutionary Paleobiology of Behavior and Coevolution. Elsevier, Amsterdam, pp. Havlíĉek, 1979 (rhynchonellid, brachiopod). In: Bulletin de l'Institute Royal des 237–287. sciences naturelles de belgique, sciences de la terre. 68. pp. 115–120. Zatoń, M., Filipiak, P., Rakociński, M., Krawczyński, W., 2013. Kowala Lagerstätte: Late Sartenaer, P., 1999. Tetragonorhynchus, new late Famennian rhynchonellid genus from Devonian arthropods and non-biomineralized algae from Poland. Lethaia 47 (3), Maïder, southern Morocco, and Tetragonorhynchidae n. fam. In: Bulletin de l'institute 352–364. royal des sciences naturelles de belgique, sciences de la terre. 69. pp. 67–75. Zatoń, M., Broda, K., Qvarnström, M., Niedźwiedzki, G., Ahlberg, P.E., 2017. The first Sartenaer, P., 2000. Phacoiderhynchus, a new middle Famennian rhynchonellid genus direct evidence of a Late Devonian coelacanth fish feeding on conodont animals. Sci. from the Anti-Atlas, Morocco, and Phacoiderhynchidae n. fam. In: Bulletin de l'in- Nat. 104 (26), 1–5. http://dx.doi.org/10.1007/s00114-017-1455-7. stitute royal des sciences naturelles de belgique, sciences de la terre. 70. pp. 75–88. Ziegler, W., Sandberg, C.A., 1984. Palmatolepis-based revision of upper part of standard Seilacher, A., 1970. Begriff und Bedeutung der Fossil-Lagerstätten. N. Jb. Geol. Paläont. late Devonian conodont zonation. Geol. Soc. Am. Spec. Pap. 196, 179–194.

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Supplementary material

Table S1. Primary data of invertebrate associations found in the Famennian at Madène el

Mrakib.

Association Source of data Stratigraphic age Number Groups in Modes of life of all species; trophic only ammonoids nucleus genera A (Fig. 4A- Newly collected at -lower Famennian 3; 1 -Brachiopods - Pelagic, slow-motile, predator B, 5A) Madène el Mrakib, (1 taxa) - Surficial, non-motile attached, housed at PIM -Ammonoids: suspension feeder Ammonoidea indet. 1 → Cheiloceras horizon B (Fig. 4A- Newly collected at -lower Famennian 4; 1 -Ammonoids -Pelagic, slow-motile, predator B, 5B) Madène el Mrakib, (1 taxa) -Surficial, non-motile attached, housed at PIM -Ammonoids: -Brachiopods suspension feeder Ch. (Staffites) afrispina (1 taxa) -Semi-infaunal or surficial, non- → Cheiloceras horizone motile, unattached, suspension feeder C (Fig. 4A- Newly collected at -lower Famennian 12; 5 -Ammonoids -Pelagic, slow-motile, predator B, 5C) Madène el Mrakib, (3 taxa) -Surficial, non-motile attached, housed at PIM -Ammonoids: -Orthocerids suspension feeder Ch. (Staffites) afrispina (1 taxa) -Benthic, no further details known Armatites beatus Aulatornoceras sp. Torleyoceras sp. Falcitornoceras bilobatum falciculum → Cheiloceras horizon D (Fig. 4A- Newly collected at -middle Famennian 5; 2 -Orthocerids -Pelagic, slow-motile, predator B, 5D) Madène el Mrakib, (1 taxa) -Surficial, non-motile attached, housed at PIM -Ammonoids : suspension feeder Tornoceratidae -Semi-infaunal or surficial, non- → horizon ? motile, unattached, suspension feeder E (Fig. 4A- Newly collected at -middle Famennian 8; 2 -Phyllocarids -Pelagic, fast-motile, deposit B, 5E) Madène el Mrakib, (1 taxa) feeder housed at PIM -Ammonoids: -Pelagic, slow-motile, predator Maeneceras acutolaterale -Surficial, facultatively motile, → Maeneceras horizon unattached, suspension feeder -Semi-infaunal or surficial, non- motile, unattached, suspension feeder -Benthic, no further details known F (Fig. 4A-B, Newly collected at -middle Famennian 11; 1 -Brachiopods -Pelagic, slow-motile, predator 5F) Madène el Mrakib, (1 taxa) -Erected, non-motile attached, housed at PIM -Ammonoids : -Bivalves suspension feeder Sporadoceras sp. (1 taxa) -Surficial, facultatively motile, → horizon? -Orthocerids attached, suspension feeder (1 taxa) -Surficial, non-motile attached, suspension feeder -Semi-infaunal or surficial, non- motile, unattached, suspension feeder -Shallow infaunal, facultatively motile, unattached, suspension feeder -Benthic, no further details known G (Fig. 4A- Newly collected at -middle Famennian 9; 2 -Ammonoids -Pelagic, slow-motile, predator B, 5G) Madène el Mrakib, (1 taxa) -Surficial, slow-motile, grazer housed at PIM -Ammonoids : -Orthocerids -Surficial, facultatively motile, Planitornoceras pugnax (1 taxa) unattached, suspension feeder Erfoudites sp. -Surficial, non-motile attached, → Planitornoceras horizon suspension feeder -Semi-infaunal or surficial, non- motle, unattached, suspension feeder -Benthic, no further details known

46 Chapter I: Alpha Diversity and Palaeoecology

Association Source of data Stratigraphic age Number Groups in Modes of life of all trophic nucleus species; only ammonoids genera H (Fig. 4A- Newly collected at -middle Famennian 14; 4 -Ammonoids -Pelagic, slow-motile, predator B, 5H) Madène el Mrakib, (1 taxa) -Surficial, non-motile attached, housed at PIM -Ammonoids: -Orthocerids predator Planitornoceras pugnax (1 taxa) -Surficial, non-motile attached, Erfoudites spiriferus -Brachiopods suspension feeder Pseudoclymenia sp. (2 taxa) -Semi-infaunal or surficial, → Planitornoceras horizon facultatively motile, unattached, suspension feeder -Semi-infaunal, non-motile, unattached, suspension feeder -Shallow infaunal, facultatively motile, unattached, suspension feeder I (Fig. 4A-B, Newly collected at -Upper Famennian 2; 1 -Ammonoids -Pelagic, slow-motile, predator 5I) Madène el Mrakib, (Annulata Black Shales) (1 taxa) housed at PIM -Ammonoids : Platyclymenia annulata → Platyclymenia horizon J (Fig. 7, Madène el Mrakib, -Upper Famennian NA; 5 -Ammonoids -Pelagic, slow-motile, predator Table S3) partially published in (2 taxa) Korn et al. (2014, -Ammonoids: 2015a) → Platyclymenia horizon housed at MNB K (Fig. 4A- Newly collected at -Upper Famennian 22; 6 -Ammonoids -Pelagic, slow-motile, predator B, 5J) Madène el Mrakib, (7 taxa) -Surficial, slow-motile, grazer housed at PIM -Ammonoids : -Orthocerids -Surficial, facultatively motile, Playtclymenia sp. (1 taxa) unattached, suspension feeder Prionoceras lamellosum -Surficial, non-motile attached, and lentis suspension feeder Cyrtoclymenia sp. -Semi-infaunal or surficial, non- Procymaclymenia motile, unattached, suspension ebbighauseni feeder Erfoudites rherisensis -Shallow infaunal, facultatively Sporadocers cf. muensteri motile, unattached, suspension → Platyclymenia/ feeder Procymaclymenia horizon L (Fig. 7, Madène el Mrakib, -Upper Famennian NA; 7 -Ammonoids -Pelagic, slow-motile, predator Table S3) partially published in (5 taxa) Korn et al. (2014, - Ammonoids: 2015a), → Platyclymenia/ housed at MNB Procymaclymenia horizon M (Fig. 7, Madène el Mrakib, -Upper Famennian NA; 7 -Ammonoids -Pelagic, slow-motile, predator Table S3) partially published in (4 taxa) Korn et al. (2014, -Ammonoids: 2015a), →Platyclymenia/ housed at MNB Procymaclymenia horizon N (Fig. 7, Madène el Mrakib, -Uppermost Famennian NA; 7 -Ammonoids -Pelagic, slow-motile, predator Table S3) partially published in (7 taxa) Korn et al. 2014, -Ammonoids : 2015a), → Gonioclymenia horizon housed at MNB O (Fig. 7. Madène el Mrakib, -Uppermost Famennian NA; 1 -Ammonoids -Pelagic, slow-motile, predator Table S3) partially published in (6 taxa) Korn et al. (2014, -Ammonoids: 2015a), → Kalloclymenia to housed at MNB Wocklumeria horizon P (Fig. 4A- Newly collected at -Uppermost Famennian 7; 1? -Ammonoids -Pelagic, slow-motile, predator B, 5K) Madène el Mrakib, (1 taxa) -Surficial, fast-motile, suspension housed at PIM -Ammonoids: -Orthocerids feeder/predators → Wocklumeria horizon (1 taxa) -Surficial, slow-motile -Trilobites -Surficial, non-motile attached, (1 taxa) suspension feeder Q (Fig. 4A- Newly collected at -Uppermost Famennian 11; 4 -Bivalves -Pelagic, slow-motile, predator B, 5L) Madène el Mrakib, (Hangenberg Black (1 taxa) -Surficial, non-motile attached, housed at PIM Shales); - Cephalopods suspension feeder (2 taxa) -Ammonoids: Postclymenia calceola Mimimitoceras sp. Acutimitoceras sp. Tornoceratoidea → Postclymenia horizon

47 Chapter I: Alpha Diversity and Palaeoecology

Table S2. Primary data of invertebrate associations found in the Tournaisian at Aguelmous

(according to Ebbighausen and Bockwinkel, 2007).

Association Source of data Stratigraphic age Number Groups in the Modes of life of all trophic species; nucleus only ammonoids genera R (Fig. 6A) Aguelmous, -Lower Tournaisian 32; 8 -Ammonoids -Pelagic, slow-motile, predator Bed 2 in Ebbighausen -Ammonoids: (4 taxa) -Surficial, slow-motile, grazer and Bockwinkel (2007), Acutimitoceras intermedium -Gastropods -Surficial, non-motile attached, housed at MNB Acutimitoceras sarahae (1 taxa) predator Acutimitoceras endoserpens -Surficial, non-motile attached, Acutimitoceras algeriense suspension feeder Acutimitoceras posterum -Benthic, no further details Acutimitoceras known pentaconstrictum Acutimitoceras hollardi Acutimitoceras depressum Acutimitoceras occidentale Acutimitoceras mfisense Costimitoceras aitouamar Imitoceras oxydentale Weyerella sp. Eocanites simplex Kazakhstania nitida Kazakhstania evoluta Kornia citrus Gattendorfia jacquelinae → Gattendorfia/ Kahlacanites horizon S (Fig. 6B) Aguelmous, -Lower Tournaisian 8; 2 -Ammonoids -Pelagic, slow-motile, predator Bed 12 in Ebbighausen -Ammonoids: (3 taxa) -Surficial, slow-motile, grazer and Bockwinkel (2007), Acutimitoceras algeriense -Benthic, no further details housed at MNB Gattendorfia ihceni known Gattendorfia jacquelina → Gattendorfia/ Kahlacanites horizon T (Fig. 6C) Aguelmous, -Lower Tournaisian 15; 6 -Ammonoids -Pelagic, slow-motile, predator Bed 16 in Ebbighausen -Ammonoids: (6 taxa) and Bockwinkel (2007), Kahlacanites mariae housed at MNB Kahlacanites meyendorffi Gattendorfia debouaaensis Gattendorfia gisae Gattendorfia jacquelinae Hasselbachia arca Hassdelbachia gourara Acutimitoceras algeriense Eocanites sp. Becanites sp. → Gattendorfia/ Kahlacanites horizon U (Fig. 6D) Aguelmous, -middle Tournaisian 9; 7 -Ammonoids -Pelagic, slow-motile, predator Bed 18 in Ebbighausen -Ammonoids: (4 taxa) and Bockwinkel (2007), Acutimitoceras sp. housed at MNB Protocanites hollardi Globimitoceras rharrizense Imitoceras sp. Gattendorfia sp. Goniocyclus elatrous Eocanites → Goniocyclus horizon

48 Chapter I: Alpha Diversity and Palaeoecology

Figure S1. Relative abundances of species occurring in the Maïder region (Morocco); red bars represent the dominant species of the association. Diversity corresponding with the

Wocklumeria Stage of Madène el Mrakib, 7 taxa (excluding crinoids and bioturbation) are depicted.

Figure S2. Rarefaction tests of Famennian and Tournaisian associations including all invertebrate groups; blue lines represent confidential intervals; red lines show how many taxa would have been theoretically sampled with further collection of specimens; green line: how many taxa would have been theoretically sampled within 90 specimens.

49 Chapter I: Alpha Diversity and Palaeoecology

50 Chapter I: Alpha Diversity and Palaeoecology

Figure S3. Rarefaction tests of Famennian and Tournaisian ammonoid associations containing at least three taxa; blue lines represent confidential intervals; red lines show how many taxa would have been theoretically sampled with further collection of specimens.

51 Chapter I: Alpha Diversity and Palaeoecology

52 Chapter I: Alpha Diversity and Palaeoecology Table S3

Cephalopoda Class . Raw data of Famennian invertebrate at samples collected Armatites beatus Planitornoceras pugnax Aulatornoceras Falcitornoceras bilobatum Falcitornoceras falciculum Tornoceratoidea Ammonoidea indet. 6 Ammonoidea indet. 5 Ammonoidea indet. 4 Ammonoidea indet. 3 Ammonoidea indet. 2 Ammonoidea indet. 1 Bactritidae indet. Spyroceras Orthocerida indet. 6 Orthocerida indet. 5 Orthoccerida indet. 4 Orthocerida indet. 3 ( Orthocerida indet. 2 Orthocerida indet. 1 sp. sp.

Species

Murchisoniceras)

p, fs, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, Mode of life

2 3 Association A

47 Association B

21 16 38

6 2 Association C

86

1 3 Association D

14

2 Association E

Madène el Mrakib (northeastern Anti-Atlas, Morocco). 15 Association F

231 67 Association G

36 31

1 1 1 Association H

2 Association I

Association J

19

2 3 2 Association K

Association L

Association M

4 Association N

Association O

7 3 Association P

5 1 3 Association Q

49 Association R

14 Association S

9 Association T

Association U

53 Chapter I: Alpha Diversity and Palaeoecology Platyclymenia Platyclymenia ibnsinai Platyclymenia Platyclymenia Platyclymenia Cyrtoclymenia Protactoclymenia Protactoclymenia Protactoclymenia Prionoceras subtum Prionoceras ouarouroutense Prionoceras mrakibense Prionoceras takhbtitense Prionoceras vetus Prionoceras lamellosum Prionoceras lentis Erfoudites Erfoudites spiriferus Erfoudites rherisensis Sporadoceras conforme Sporadoceras globulosum Sporadoceras muensteri Sporadoceras Maeneceras acutolaterale Ch. Torleyoceras Procymaclymenia ebbighauseni Pseudoclymenia ( Staffites sp. ) sp afrispina xxPls 2 sp. sp. 1

sp. annulata sp. . sp du di 2 sp.

.

p, fs, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p,

160

56 1

1

1

1

2 1

100

1752 356 30 74 16 34 3 1 17 37 5 6 6 2 1 6 138 210 38 11 10 61

10 11 58 3 3 1

54 Chapter I: Alpha Diversity and Palaeoecology Acutimitoceras pentaconstrictum Acutimitoceras posterum Acutimitoceras algeriense Acutimitoceras endoserpens Acutimitoceras mfisense Acutimitoceras sarahae Acutimitoceras depressum Acutimitoceras occidentale Acutimitoceras intermedium Acutimitoceras hollardi Acutimitoceras Acutimitoceras Acutimitoceras comtum Mimimitoceras carnatumMimimitoceras Mimimitoceras Cymaclyenia carnata Cymaclyenia lambidia Cymaclyenia formosa Cymaclyenia subvexa Postclymenia calceola Platyclymenia Platyclymenia Platyclymenia Platyclymenia Platyclymenia Platyclymenia Platyclymenia umb evo inv a-i xxPlg xxPlv xxPli sp. A sp. 4 sp. 3 sp.

p, fs, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p,

24 28 23 3 6 6 4

31 49 4 8

59 78 79

15 16 1

22 33 2

1084 119 171 292 16 43 18 19 1 1 1 9 17 73

17 5

83

55 Chapter I: Alpha Diversity and Palaeoecology Nanoclymenia Protoxyclymenia wendti Trigonoclymenia Weyerella Protocanites hollardi Kahlacanites Kahlacanites meyendorffi Kahlacanites mariae Becanites Goniocyclus elatrous Kazakhstania nitida Kazakhstania evoluta Kornia citrus Hasselbachia Hasselbachia arca Hasselbachia gourara Costimitoceras aitouamar Globimitoceras rharrhizense Eocanites Eocanites Eocanites simplex Gattendorfia Gattendorfia Gattendorfia gisae Gattendorfia lhceni Gattendorfia debouaaensis Gattendorfia jacquelinae lmitoceras lmitoceras oxydentale sp. sp.2 sp.1 sp. sp. sp. 2 sp. 1 sp.

sp.

sp.

sp.

p, fs, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, 5 10 9

24 13 49 14 32 5 7 1 5 28 2 55 52 25 18 21 35 1 1 3 2 3 9 64 32 21 10 21 9 1 2

56 Chapter I: Alpha Diversity and Palaeoecology Bivalvia Guerichia Glyptohallicardia Buchiola (Buchiola) Bivalvia indet. 13 Bivalvia indet. 10 Bivalvia indet. 12 Bivalvia indet. 11 (nuculid) Bivalvia indet. 9 Bivalvia indet.8 Bivalvia indet. 7 Bivalvia indet. 6 Bivalvia indet. 5 Bivalvia indet. 4 Bivalvia indet. 3 Bivalvia indet. 2 Bivalvia indet. 1 Kosmoclymenia Kosmoclymeniidae indet. Gonioclymenia spiniger Gonioclymenia ali Gonioclymenia wendti Alpinites zigzag Discoclymenia atlantea Ebbighausenites weyeri Alpinites schultzei Posttornoceras eegantum Gundolficeras vescum Ungusporadoceras unguiforme Procymaclymenia ebbighauseni cf. cf. venusta

sp. sp.

sp.

smi/su, nu, sf smi/su,nu, sf su, na, sf p, fs, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, pr fs, p, benthic benthic benthic benthic benthic benthic benthic benthic benthic benthic benthic benthic benthic 2 1 2 1 3 8 5 3 1 1 4 2 3 1 3 2 1 1 3 8 1 2 98 3 3 1 26 10 17 1 1 1 2 1 1 3

3 1 6

57 Chapter I: Alpha Diversity and Palaeoecology Brachiopoda Lingulata Spiriferida Rhynchonellata Gastropoda Amphigastropoda Brachiopoda indet. 1 Lingulata indet. Spiriferida indet. Aulacella Phacoiderhynchus antiatlasicus Rhynchonellata indet. 5 Rhynchonellata indet. 4 Rhynchonellata indet. 3 Rhynchonellata indet. 2 Rhynchonellata indet. 1 Macrochilina Gastropoda indet. 7 Gastropoda indet. 6 Gastropoda indet. 5 Gastropoda indet. 4 Gastropoda indet. 3 Gastropoda indet. 2 Gastropoda indet. 1 Bellerophontidae indet. Bellerophon Palaeoneilo ?Streblopteria ?Ptychopteria Loxopteria ?Metrocardia Opisthocoelus Prosochasma Guerichia elliptica sp. sp. ( sp. sp. Aglaoglypta sp. sp. sp. sp.

sp.

)

su, na, sf su, na, sf su, na, sf su, na, sf su, na, sf su, na, sf su, na, sf su, na, sf su, fa, sf sf fa, su, sf fa, su, sf fu, su, sf fa, su, sf fa, su, si, na, sf su, fs, g su, fs, g su, fs, g su, fs, g su, fs, g su, fs, g su, fs, g su, fs, g su, fs, g su, fs, g si,df fu, si,sf fu, 1700 122 5 1 39 34 3 3 12 1 1 3 3 2 1 1 4 3 4 3 2 3 1 4 1 2

280 3 3

13 58 60 1 9 2 7

6

58 Chapter I: Alpha Diversity and Palaeoecology

Bryozoa Rugosa Tabulata Crinoidea Trilobita Phyllocarida Bryozoa indet Rugosa indet. 3 Rugosa indet. 2 Rugosa indet. 1 Tabulata indet. Crinoidea indet. Trilobita indet. Phyllocarida indet su,pr/df ff, su, na, pr su, na, pr su, na, pr su, na, sf su, na, sf er, na, sf p, ff, df ff, p, 151 1 2 1 7 5

6 1

59

CHAPTER II

Fossil-Lagerstätten and preservation of invertebrates and vertebrates from the Devonian in the eastern Anti-Atlas (Morocco)

Linda Frey, Alexander Pohle, Martin Rücklin and Christian Klug

Submitted to : Lethaia

Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fossil-Lagerstätten and preservation of invertebrates and vertebrates from the Devonian in the eastern Anti-Atlas (Morocco)

LINDA FREY, ALEXANDER POHLE, MARTIN RÜCKLIN and CHRISTIAN KLUG

Frey, L., Pohle, A., Rücklin, M. & Klug, C. 20XX. Fossil-Lagerstätten and preservation of vertebrates and invertebrates from the Moroccan Devonian (eastern Anti-Atlas). Lethaia.

Throughout the Devonian, fossil invertebrates are abundant in the eastern Anti-Atlas and depending on the strata, they display a high taxonomic diversity. Fossils of jawed vertebrates have been recorded after the early Lochkovian so far and are relatively common with their abundance and diversity increasing towards the Late Devonian. Fossil preservation varies strongly, partially refl ecting the disintegration of the continental shelf of Gondwana in this region in three epicontinental basins and pelagic ridges during the Devonian and fl uctuations of the regional sea-level. We analyzed the mineral composition of several invertebrate and vertebrate samples of Devonian and Early Carboniferous age by Raman spectroscopy and X-ray diffraction. We use the results of these analyses combined with palaeogeographic and palaeoecological data to interpret the genesis of Devonian Fossil-Lagerstätten of this region. Accordingly, we list eight examples of the numerous Devonian Konzentrat-Lagerstätten and two examples of Konservat-Lagerstätten with soft-tissue preservation (the Famennian Thylacocephalan Layer and the Hangenberg Black Shale of the southern Maïder). The latter are the fi rst two of this kind of Fossil-Lagerstätte from the Devonian of North Africa. The taphonomic and oceanic settings suggest that these Konservat-Lagerstätten formed due to stagnation (perhaps related to vertical restriction of water exchange and water depth rather than limited spatial water exchange and a lateral restriction) in the relatively small Maïder Basin with limited water exchange with the neighboring Tafi lalt Basin. The poor lateral or vertical water exchange could also explain the reduced chondrichthyan diversity compared to the Tafi lalt Platform, where the water was shallower and probably better oxygenated at depth. □ Exceptional preservation, Raman-spectroscopy, X-ray Diffraction, mineralogy, weathering, Chondrichthyes, Placodermi, Ammonoidea.

Linda Frey [[email protected]], Alexander Pohle [[email protected]], Christian Klug [[email protected]], Paläontologisches Institut und Museum, University of Zurich, Karl Schmid-Strasse 4, CH-8006 Zürich, Switzerland; Martin Rücklin [[email protected]], Naturalis Biodiversity Center, Postbus 9517, NL-2300 RA Leiden, the Netherlands.

Two fi elds of research concerning the of the fossils under consideration. Based on the palaeontology of the Devonian in Morocco have colour, host sediments and surface patterns, been explored only rarely yet: Fossil-Lagerstätten preservation in a series of different minerals and taphonomy. The term Fossil-Lagerstätten is inferred for vertebrate and invertebrate (Seilacher 1970) applies to deposits where fossils from the arid eastern Anti-Atlas (Fig. 1). fossils occur either in a very high abundance or Although their actual mineralogical composition in exceptional preservation including soft tissues was rarely tested (e.g., Klug et al. 2009, 2016), and articulated skeletons; both cases occur in the mineralogy of the respective fossil is inferred the eastern Anti-Atlas as we demonstrate here, commonly based rather on speculation than actual although the former kind is much more common mineralogical examinations (e.g., Pohle & Klug than the latter. Therefore, we put a special 2018). Consequently, the analysis of the mineral emphasis on two poorly documented Famennian composition of fossils of various ages and localities cases of the latter kind (Konservat-Lagerstätten). from the Devonian of the Anti-Atlas is crucial. In order to understand the formation of Fossil- Here, we discuss possible implications of fossil Lagerstätten, we follow three approaches: it preservation for palaeoenvironment reconstruction is essential to examine and understand the and interpretations of the taphonomy and consider taphonomic processes that are involved (approach possible secondary alteration due to weathering. 1), the palaeogeographic setting (approach 2) and Based on taphonomic, palaeogeographic and facies the palaeo-environmental conditions (approach data, palaeoenvironment and palaeoecology are 3). reconstructed and the infl uence on the vertebrate Taphonomic processes (approach 1) can diversity is analysed. partially be reconstructed using information from The study of taphonomy is of interest because the mode of preservation and also the mineralogy only in the Maïder Basin, chondrichthyans

63 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 1. Geologic map of the eastern Anti-Atlas of the Maïder and Tafi lalt Basins as well as the Tafi lalt Platform. Only some examples of vertebrate occurrences of the Famennian are given: arthodire remains can be found in almost every larger outcrop of the Famennian in this region. preserving cartilaginous body parts as well as the literature, we do not add new details to this soft tissues have been discovered. Hence, the aspect, but provide a brief review necessary for new data on preservation will shed light on how the interpretation of the Lagerstätten type. the Konservat-Lagerstätten of the Maïder region In our third approach, we qualitatively assess formed (Klug et al. 2016; Frey et al. 2018). the palaeo-environment and palaeoecology The second approach to understand the through the Devonian of the eastern Anti-Atlas. formation of Fossil-Lagerstätten is the study of the Devonian sedimentary sequences of this region palaeogeographic setting and facies. Fortunately, contain numerous different facies types and thus the arid climate keeps vegetation to a minimum also various kinds of sediments with a broad range in the Moroccan pre-Sahara, thus creating of vertebrate, invertebrate and plant fossils (e.g., formidable outcrops. Therefore, facies changes Clariond 1936; Termier and Termier 1950; Lehman can be examined in space and through geologic 1956, 1964, 1976, 1977; Lelièvre and Janvier time in order to reconstruct the arrangement of 1986, 1988; Belka et al. 1999; Derycke 1992; basins and carbonate ramps with ridge and swell Becker et al. 2000; Rücklin 2010, 2011; Frey et topography, and the approximate situation of al. 2014; Rücklin et al. 2015; Korn et al. 2016a, b; coastlines throughout the Devonian (e.g., Hollard Rücklin and Clément 2017). In the Famennian of 1974; Wendt 1985, 1988; Wendt and Belka the eastern Anti-Atlas, fossil invertebrates but also 1991; Kaufmann 1998; Döring and Kazmierczak vertebrates can be found in sometimes impressive 2001; Lubeseder et al. 2010). Since the required numbers. As far as vertebrates are concerned, palaeogeographic data are readily available from microremains of gnathostomes are quite common

64 Chapter II: Fossil-Lagerstätten and Preservation of Fossils in some strata (Derycke 1992; Ginter et al. stored at the Institut für Geowissenschften at the 2002; Derycke et al. 2008) due to condensed University of Tübingen with the abbreviation sedimentation, particularly in the Tafi lalt. In the GPIT. latter region, chondrichthyan diversity can be reasonably high (up to nine species in one layer). Mineral analyses By contrast, in the Famennian of the southern Maïder Basin, chondrichthyan diversity appears We analysed 30 samples (Tab. 1, 2) taken from to be lower (four to fi ve species) and some genera invertebrates and vertebrates of mostly Devonian have not been found there yet although they are age (two from the Early Carboniferous) from the documented from the neighbouring Tafi lalt Basin Maïder and the Tafi lalt (eastern Anti-Atlas). Table (Ginter et al. 2002; Derycke et al. 2008). 1 and 2 show details and the mineral composition. Invertebrates, however, can usually deliver Fossil preservation was examined by analysing more detailed information on palaeoecology, their mineral composition using Raman partially because they often occur in statistically spectroscopy and XRD (X-ray Diffraction) at the relevant numbers to carry out quantitative Swiss Federal Institute of Technology in Zurich analyses. Several groups of invertebrates are (ETHZ). very common in Devonian strata of the eastern Raman spectroscopy was performed with a Anti-Atlas. It is thus not surprising that some DILOR LabRam (with built-in Olympus BX 40 of the carbonate build-ups contain abundant microscope); grating was 600 or 1800 grooves/ corals (e.g., Kaufmann 1998; Berkowski 2006) mm, CCD sensor resolution 1152*298 pixels and brachiopods (Halamski and Baliński 2013; spectral resolution 1.3 – 1.5 cm-1 (for 1800 Tessitore et al. 2013). Similarly, ammonoids are grating). Laser wavelength was 532.14 nm common from the Emsian to the Visean (e.g., (with max. 500 mW laser power at the source) Klug 2001; De Baets et al. 2013; Korn et al. 2007, generated by a DPSS laser (Diode-pumped solid- 2016a, b) and occur in an impressive diversity, but state lasers). Measurements of laser Power were their modes of preservation are almost as diverse. performed with a COHERENT LaserCheck Other groups such as trilobites, crinoids, bivalves hand-held device at 40% (Laser power: 195 mW etc. occur as well, sometimes in vast numbers, but at source, 19.7 mW with 100x, 26 mW with 50x these were examined only in the palaeoecological on the sample). For the analyses of the spectra, context and not for their preservation. In this we used the software CrystalSleuth (Laetsch & approach, we also rely on published data, which Downs 2006) and the American Mineralogist are briefl y summarized. Crystal Structure Database (Downs & Hall- In this article, we address the following Wallace 2003). Some of the minerals rich in iron questions: (1) What is the mineral composition of could not be measured properly, because the laser invertebrate and vertebrate fossils in the Devonian in use is red and too close in wavelength to that of the eastern Anti-Atlas? (2) Is this composition refl ected by these minerals. primary or altered by taphonomic or weathering For the XRD, we used a D8-advance (Bruker processes? (3) What can we deduce from the AXS) diffractometer in the Geochemistry and palaeogeographic setting for the formation of Petrology Laboratories of the ETHZ. All samples Fossil-Lagerstätten? (4) What are the implications were crushed in an Agate bowl prior to analysis derived from the preservational mode for the and the resulting fi ne powder was then prepared palaeoenvironment and the according differences on sample holders. The diffractometer operated at in faunal composition? (5) What kinds of Fossil- 40 mA and 40 kV with Cu Kα radiation at room Lagerstätten occur in the Anti-Atlas? temperature (25°C). A scintillation counter with secondary monochromator was used to identify the minerals. The scans were performed as θ-2θ Material and methods locked with a step size of 0.02° and step time of 1.0 s between 5°-90°2θ. In several cases of the Material minerals rich in iron, crystal-size was possibly too small to be well-analyzed by XRD, hence the All specimens (except one) were collected by often noisy signal seen in the analyses. the authors in the eastern Anti-Atlas. We chose the samples with the intention to include a broad Comparison of Konservat-Lagerstätten range of different preservations in order to cover the main minerals occurring in fossils of the In order to better classify the Konservat- eastern Anti-Atlas. Most of these specimens are Lagerstätten of the Maïder (Thylacocephalan kept at the Paläontologisches Institut und Museum Layer, erroneously dubbed Phyllocarid Layer of the University of Zurich with numbers with before, Hangenberg Black Shale), we used the abbreviation PIMUZ. Some specimens are the questionnaire proposed by Seilacher et al.

65 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Tab. 1. Results of Raman-analyses of various Devonian and Carboniferous fossils from the eastern Anti-Atlas.

Tab. 2. Results of XRD-analyses of various Devonian fossils from the eastern Anti-Atlas. Samples kept under the number PIMUZ 36879.

(1985). This questionnaire represents a list ecology, taphonomy, and diagenesis. We did not of characteristics grouped into aspects of the code (1) the setting, because all are marine, (2) sedimentary basin, stratigraphy, sedimentology, the origin, because all are sedimentary, (3) the geochemistry (here, we excluded some isotopy, because of missing data from many of characteristics because of missing data from most the localities, (4) terrestrial organisms, because of Konservat-Lagerstätten), taxonomic composition, the marine setting, and (5) articulation, because

66 Chapter II: Fossil-Lagerstätten and Preservation of Fossils all localities yielded articulated specimens. We of the mineral content by Raman-spectroscopy slightly reduced their list to 31 characters. The impossible, but the XRD-analyses (Tab. 2) completed questionnaire for both Konservat- proved that particularly the black internal moulds Lagerstätten of the eastern Anti-Atlas (Appendix of cephalopods are composed predominantly 1) and for 19 well-known marine Konservat- of goethite. More reddish specimens contain Lagerstätten (Tab. 3) are added. Characters were additionally haematite. These goethitic internal coded as follows: moulds sometimes contain remains of a pyritic Marine basin size: 0 ‒ ≤ 1 km2; 0.5 ‒ 1 to 10 km2; core. This indicated already, that all these goethitic 1 ‒ ≥ 10 km2 internal moulds derive from pyritic specimens Facies: 0 ‒ limestone; 1 ‒ clastics (this is corroborated by pseudomorphoses of Palaeolatitude: 0 ‒ tropical; 1 ‒ moderate goethite after pyrite), where the iron of the Thickness: 0 ‒ ≥ 1 m; 0.5 ‒ 1 to 10 m; 1 ‒ ≤ 10 m pyrite was slowly oxidized in the course of the Duration: 0 ‒ ≥ 1 Ma; 0.5 ‒ 1 to 10 Ma; 1 ‒ ≤ 10 deep weathering of the clay sediments. Further Ma corroboration of this scenario is provided by a Sea-level: 0 ‒ ≥ 10 m; 0.5 ‒ 10 to 100 m; 1 ‒ ≤ specimen of Cymaclymenia (Fig. 2A), which was 100 m found in a depth of about ten meters in a well. Sediment structures: 0 ‒ lamination; 1 ‒ ripple Its pyritic composition was determined by Raman marks spectroscopy (Tab. 1). Fauna: 0 ‒ invertebrates dominant; 1 ‒ vertebrates The late Famennian of the Jebel El Mrakib, common; Jebel Krabis and Lambidia region (Aguelmous Pelagics (macrofossils): 0 ‒ mostly nekton; 1‒ syncline; Becker et al. 2018) has stratigraphic mostly plankton. intervals rich in Cymaclymenia (Klein & Korn The following characters were coded as 0 when 2014). Claystones, marls and thin nodular absent and as 1 when present: limestones characterized these intervals. These Pyrite in sediment; trace fossils; infauna; nodules and their fossil content usually carry epibenthos; death marches; landing marks; soft a dessert varnish giving them a shiny surface. tissue preservation; cuticles; roll marks; current We analysed one specimen each from the Rich alignment of fossils; aragonite preservation; Chouiref and Jebel El Krabis, both of calcitic pyrite internal moulds; concretions; deformation composition. (compaction); carbonization; phosphatisation; In the Visean concretion containing the pyritisation of tissues; tissues replaced by clay ammonoid Entogonites (C10), quartz and calcite minerals; silicifi cation; obrution (tempestites occur. Other Tournaisian and Visean goniatites or turbidites etc.); stagnation (phases of low collected in proximity of Erg Chebbi are oxygen); bacterial/ algal mats preserving fossils. comparable in their quartz and calcite composition The matrix was analysed in PAST (Hammer et al. (Tab. 1, 2). The inner whorls of the phragmocone 2001) by a Principal Component Analysis on the of goniatites from the Visean of the southeastern correlation matrix. Tafi lalt (Fig. 2I) and other faunas are preserved in baryte. This preservation is also known from roughly coeval strata of the Rhenish Massif Mineralogy of fossil groups (Germany: Korn 1988) and some Jurassic sites (Blum 1843; Wenk 1967). All analyses are shown in Tab. 1 and 2. The highly abundant thylacocephalans from the Correspondingly the method used for each Famennian Thylacocephalan Layer of Madene El analysis is indicated there. Therefore, no Mrakib (Fig. 3) have a hydroxypatite composition individual indication whether the mineral content in the greyish to bluish remains of the carapace, was determined by XRD or Raman is given. while the sparitic fi lling of the carapace is calcitic. The surrounding concretions are occasionally Invertebrates greenish, where they consist of calcite. The reddish concretions are rich in haematite. In the Devonian limestones of the eastern Anti- Atlas, cephalopod remains usually occur as Vertebrates limestone internal moulds and occasionally shells are replaced with calcite. Near faults and the Since actinopterygians and sarcopterygians play angular disconformity contact of the Cenomanian a subordinate role in the Famennian faunas of transgression, the fossils are often slightly the eastern Anti-Atlas, we analysed the mineral dolomitized (Fig. 2L). Many clayey intervals content of remains of chondrichthyans and yield internal moulds of cephalopods that are placoderms (Table 1, 2, Fig. 3, 4), both of which preserved in iron oxides and hydroxides (Fig. 2B, occur abundantly in some Late Devonian strata C, J). Their reddish colour made the determination (Lehman 1956, 1964, 1976, 1977; Frey et al. 2018).

67 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Tab. 3. Characterization of marine Konservatlagerstätten based on the “questionnaire” of Seilacher et al. (1985). Character coding is explained in the material and methods chapter (where only 0 and 1 is coded, 0 means absence and 1 means presence).

The vertebrate remains are usually contained subordinate haematite. Anterior to the pelvic in nodules of varying colours suggesting a girdle a pyrite nodule is preserved with the carbonatic or iron-rich composition, respectively. characteristic cubic crystals, surrounded by a Mineral analyses of greyish to greenish nodules crust of iron minerals (haematite, goethite). contain calcite and perhaps siderite matching with presumed carbonatic composition (Tab. 1, 2). Several nodules with chondrichthyan or Palaeogeography and facies thylacocephalan remains share an orange, red to yellowish colour. Composed of calcite, haematite Palaeogeography (causing the colour), and goethite (and possibly other hydroxides). The palaeogeographical setting of the eastern Hydroxyapatite is measured as expected in Anti-Atlas was published in a series of articles placoderm bones, chondrichthyan cartilage, teeth (for more details, see Wendt 1985, 1988; Wendt and in the thylacocephalan carapaces (Tab. 1, and Belka 1991; Kaufmann 1998; Klug and Korn 2). The cartilaginous branchial arches of a small 2002). The interpretation of a homocline carbonate chondrichthyan are preserved in hydroxyapatite ramp in the Early Devonian that disintegrated and and calcite, while in the body, there is mainly developed into three small epicontinental marine calcite, perhaps combined with siderite and basins during the Middle Devonian in the eastern

68 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Anti-Atlas is widely accepted (Fig. 5). For the Late the presence of the Maïder Platform. Eastern Devonian a nearly rectangular western basin, the areas are covered and therefore lack outcrops of so-called Maïder Basin is described. It has a width Devonian sediments. Further east series of E-W (E-W) of about 70 km in longitude and a length (N- trending synclines with exposures of more or less S) of about 80 km in latitude. Hiatuses spanning strongly condensed carbonatic sediments in the the Devonian or more refl ect the approximate Eifelian and Famennian. Wendt (1985, 1988) and limits of the basin to the south and north. In the Kaufmann (1998) suggested that these sediments west, outcrops of Devonian sediments represent were laid down in a continuously submerged area a strongly reduced thickness, thus documenting of reduced water depth, the Tafi lalt Platform.

69 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

↑ Fig. 2. Ammonoids from the eastern Anti-Atlas in different modes of preservation. Scale bar (1 cm) applies to all materials except H (ruler with millimetre scale at the bottom right). A to G, Cymaclymenia spp., Famennian, Maïder. A, PIMUZ 36863, pyritic internal mould, found in a depth of ca. 10 m in a well near Tafraoute (analysis in Tab. 1, Fig. 4). B, C, PIMUZ 36864 and PIMUZ 36865, surface collected specimens, pyrite entirely replaced by goethite with some iron hydroxides. D, PIMUZ 36866, calcium carbonatic internal mould with collapsed body chamber; Lambidia. E, PIMUZ 36867, calcium carbonatic specimen with replacement shell (also calcite) showing growth lines, Lambidia. F, PIMUZ 36868, calcium carbonatic internal mould with dessert varnish, Chouiref (analysis in Tab. 1, Fig. 4). G, PIMUZ 36869, calcium carbonatic internal mould with growth lines on replacement shell and collapsed phragmocone. H, Postclymenia evoluta, PIMUZ 31561, Hangenberg Black Shale, Madene El Mrakib; fl attened internal mould preserving fi ne shell structures (wrinkle layer, sutures, growth lines) and carbonatic remains of the formerly chitinous lower jaw (also fi gured in Klug et al. 2016, fi g. 3I). I, Neogoniatites delicatus, GPIT 1851-101, Viséan-Namurian boundary, E of Taouz; baritic internal mould of the phragmocone. J, typical surface- collected Famennian ammonoids, mostly goethitic internal moulds, Filon Douze. K, Gonioclymenia cf. inornata, PIMUZ 36870, Famennian, Madene El Mrakib; external mould of the umbilicus with collapsed replacement shell and internal mould of the thick dorsal siphuncle. L, Sobolewia nuciformis, GPIT 1871-245, Eifelian, Richt Tamirant; dolomitized internal mould (also fi gured in Klug 2002, pl. 13, fi g. 5). M, Ponticeras kayseri, GPIT 1849-388, late Givetian, Ouidane Chebbi (also fi gured in Belka et al. 1999, pl. 4, fi g. 12); chambers fi lled by white sparitic calcite, septa replaced by black calcite.

Probably, this palaeogeographic setting et al. 2018). At the onset of the Emsian, nodular reduced the water exchange with the surrounding marls occur in the Tafi lalt, followed by fi ne basins and the open ocean towards the north. claystones (weathering to a greenish scree) that Additionally, there are indications for a water yielded the largely haematitic Faunule 1 (Klug depth exceeding 200 metres in the Maïder Basin: et al. 2008). During a short regression, the In the Givetian, a large reef mound formed on the Deiroceras Limestone (Kröger 2008) was laid southern slope of the basin (Kaufmann 1998). This down; these carbonates commonly form a 50 to mound was about 200 to 300 m high (Kaufmann 100 cm thick limestone bed that can be easily 1998, Tessitore et al. 2016). It is unknown, how recognized in the Tafi lalt. This dacryoconarid much sediment accumulated around the mound wackestone to packstone contains abundant large during the time of its growth, but it is well nautiloids of the genus Deiroceras, hence the conceivable that the water depth was around 200 name (see also Pohle and Klug 2018). Above, m, because indications for subaerial exposure are claystones follow that contain the predominantly missing and the mound slopes appear rather steep haematitic Faunule 2 (Klug et al. 2008; De Baets today. With the cessation of mound growth, sea- et al. 2010); this sedimentary unit was dubbed level was rising, as suggested by the very thick Metabactrites-Erbenoceras Shale by Becker and overlying sequence of clayey sediments of late Aboussalam (2011; see also Aboussalam et al. Givetian to middle Famennian age. Consequently, 2015). The Erbenoceras Limestone (Klug 2001; the water was possibly over 200, maybe 300 or = Anetoceras Limestone of Bultynck and Walliser even 400 metres deep in the depocentre (Tessitore 2000; see also De Baets et al. 2010) varies in et al. 2016). It is thus well conceivable that, during thickness and facies. In the northern Maïder, the Middle and Late Devonian, water exchange the Erbenoceras Limestone consists of an over was low between the Tafi lalt Basin in the East and 40 m thick sequence of moderately thin-bedded the very distant Tindouf Basin in the Southwest mudstones and wackestones (Döring 2002). At and the Maïder Basin, especially with the deeper Jebel Mdouar (= Gara Mdouara, Klug 2017), the parts of the Maïder Basin. Erbenoceras Limestone (Units D and E of Klug 2001) is only 5 m thick and three fossiliferous Facies massive limestone beds (mostly dacryoconarid packstones, sometimes with great amounts of In the eastern Anti-Atlas, the Devonian succession crinoids; Klug 2001), each about one meter thick, starts with a thick sequence of clayey sediments, dominate the sequence. The Daleje Shales were usually poor in fossils of benthic organisms and laid down during a global transgression (Haq and dark in colour. This suggests anoxic to hypoxic Schutter 2008); their carbonate content is usually conditions during most of the Lochkovian low and thickness varies between over 160 m (Belka et al. 1999; Dopieralska et al. 2006; Frey southeast of Tazoulait in the Maïder Basin and et al. 2014). Pragian sediments contain more less than 40 m at the northern and southern limits carbonate and marls as well as marly limestones. of the basin (Döring 2002). Some of these layers contain rich benthonic Both thickness and facies variation increase as well as planktonic assemblages, indicating throughout the Devonian (Hollard 1974; Wendt increased oxygen levels (Frey et al. 2014; Klug 1985; Kaufmann 1998; Döring and Kazmierczak

70 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 3. XRD-spectra of various fossils from the eastern Anti-Atlas. For additional results see Tab. 1. Samples kept with the number PIMUZ 36879.

2001; Döring 2002; Lubeseder et al. 2010). The towards the Maïder Basin (Kaufmann 1998; maximum thickness of the Middle Devonian Lubeseder et al. 2010). Throughout most of the sedimentary succession in this small basin can eastern Anti-Atlas, the Middle Devonian sequence be found east of Tazoulait and reaches over 700 is dominated by limestone, marl and claystone m (Fig. 1; Döring and Kazmierczak 2001). The alternations. The closer to the depocentre in the corresponding sequence in the Tafi lalt is much Maïder Basin, the greater gets the proportion thinner and varies mostly between 30 m on the of mudstones and the thicker the argillaceous Tafi lalt Platform (e.g., at Bou Tchrafi ne, Hamar proportion of the sequences (Kaufmann 1998; Laghdad or Filon Douze) and over 220 m at Lubeseder et al. 2010). On the Tafi lalt Platform, Ottara, which was probably situated on the slope condensed sedimentation prevailed; cephalopod

71 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 4. Raman-spectra of Devonian invertebrates and vertebrates from the eastern Anti-Atlas. For additional results see Tab. 1. A, Cymaclymenia sp., PIMUZ 36863, Tafraoute. B, Cymaclymenia sp., PIMUZ 36868, Chouiref. C, Maxigoniatites sp., PIMUZ 36871, 12 km S of Dar Kaoua. D, Thylacocephala gen. et sp. indet., PIMUZ 36873, Madene El Mrakib. E, F, large chondrichthyan, PIMUZ 36881, Madene El Mrakib. G, arthrodire, PIMUZ 36877, Ouidane Chebbi. H, small chondrichthyan, PIMUZ XX, Madene El Mrakib. limestones (dacryoconarid wackestones and which is refl ected in extreme differences in facies packstones) are common and macrofossils occur and thickness (Hollard 1974; Wendt 1985, 1988; in great numbers (Wendt 1988; Kaufmann 1998; Wendt and Belka 1991; Belka et al. 1999). In Döring and Kazmierczak 2001). In the late the Maïder and Tafi lalt Basins, sedimentation Givetian, the clay content increases and thick was dominated by claystones with sideritic and claystone sequences were laid down particularly a few carbonatic levels (often nodular such as in the southern Maïder Basin while on the Tafi lalt the Thylacocephalan Layer). Simultaneously, Platform, sometimes carbonate sedimentation cephalopod limestones, sandy limestones and continued into the Frasnian (e.g., Ouidane Chebbi: thick-bedded crinoid or cephalopod limestones Belka et al. 1999). (wackestones and packstones) were laid down During the Late Devonian, synsedimentary on the Tafi lalt Platform (Wendt 1985). The tectonics intensifi ed in the eastern Anti-Atlas, terminal Devonian sedimentary sequence of the

72 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 5. Geologic map of the eastern Anti-Atlas showing the supposed outlines of the Maïder and Tafi lalt Basins as well as the Tafi lalt Platform in the Late Devonian (modifi ed after Wendt & Belka 1991). We indicated the occurrences of cephalopod-bearing Konzentrat-Lagerstätten as well as of gnathostome-bearing Konservat-Lagerstätten. Note that the indicated Konzentrat-Lagerstätten represent only some examples of a much greater number of such Lagerstätten. The various shades of blue suggest differences in water depth in the Late Devonian with darker blue indicating greater depth.

Hangenberg Black Shale is composed of fi ne- shelled fauna (benthic, nektonic and planktonic). grained clastics in most sections (Kaiser et al. Occasional wave ripples document rather shallow 2011; Klug et al. 2016). In the southern Tafi lalt, water. the correlate of the Hangenberg Sandstone is rather fi ne-grained and between 3 m and 28 m thick, while in the Maïder, the 5 m to 15 m thick Palaeoecology massive sandstone beds form a high cliff in most of the region (Kaiser et al. 2011). The Hangenberg In spite of the proximity of the Maïder and the Sandstone is overlain by a several hundred meter Tafi lalt Basins, ecological differences are evident thick clastic sequence of fi ne-grained sandstones, not only from sediment thickness and facies siltstones and claystones (latest Famennian to (Massa 1965; Hollard 1974; Kaufmann 1998) but Viséan) with abundant trace fossils, occasional also from the faunal composition of coeval strata, plant remains and very few thin shell beds (Kaiser especially in the Middle and Late Devonian. et al. 2011), some containing ammonoids (e.g., Regional palaeoecology was examined by Frey Korn et al. 1999, 2002; Klug et al. 2006) and other et al. (2014, 2018) for the Early Devonian of the

73 Chapter II: Fossil-Lagerstätten and Preservation of Fossils southern Tafi lalt and the Famennian to Tournaisian Frey et al. 2013, 2018). and locally for the Pragian to Eifelian by Klug et With the Daleje-transgression (basal Late al. (2018). The differences in palaeoecological Emsian), overall diversity was reduced (but this dynamic shifts through the Devonian in the two might also be an effect of increased sediment basins refl ects the special position and palaeo- accumulation rates) and benthics are much less environment of the Maïder Basin and is required abundant (Frey et al. 2014; Klug et al. 2018). for the explanation of the Famennian Konservat- Occasionally, trilobites, tabulate and rugose Lagerstätten in the southern Maïder. corals occur as well as small orthocerids and ammonoids, mostly preserved in goethite. It is well Lochkovian and Pragian conceivable that the oxygen content of the lower part of the water column was low again linked In the Lochkovian of Tafi lalt and Maïder, to the transgression (Haq and Schutter 2008). fossiliferous layers are rare and usually During the latest Emsian, carbonate deposition dominated by remains of nektonic to planktonic resumed and diversity increased markedly organisms like cephalopods with orthoconic including benthos (trilobites, gastropods, bivalves conchs and graptolites (Frey et al. 2014). In the etc.), plankton (mostly dacryoconarids and Maïder, the Lochkovian is not so well exposed orthocerids) and nekton (several ammonoid taxa, because its sediments are mostly argillaceous rare gnathostomes), refl ecting both a lower sea- with little carbonate. The high clay-content level and improved sea-fl oor oxygenation (Frey indicates moderately deep water with low oxygen et al. 2014; Klug et al. 2018). Particularly in the conditions near the sediment surface. Maïder, late Emsian strata yielded several highly Towards the top of the Lochkovian sequence, spinose trilobite taxa (e.g., Morzadec 2001; the carbonate content rises, fossils become more Chatterton and Gibb 2010). abundant and some bivalves as well as gastropods The demersal acanthodian Machaeracanthus are present. This suggests an increasing can locally be very abundant in the early Emsian oxygenation of the water column during the (Klug et al. 2008; De Baets et al. 2010) and Pragian and early Emsian (as refl ected by high various placoderm taxa occur: remains of large invertebrate diversities in the Tafi lalt and highly arthrodires can be found in the late Zlíchovian diverse trilobite faunas in the Maïder; Morzadec (early Emsian) and the Dalejan (late Emsian) 2001; Frey et al. 2014; Klug et al. 2018). The yielded remains of Atlantidosteus hollardi and increasing oxygenation eventually reached Antineosteus lehmani in various localities of the the top centimetres of the sediment (refl ected Tafi lalt (Klug et al. 2008; Lelièvre 1984, 1995; in occurrences of trace fossils: e.g., Klug & Lelièvre et al. 1993, Rücklin and Clément 2017 ; Hoffmann 2018), possibly in correlation with a Rücklin et al. 2018). The wealth of –sometimes reduced water depth. Vertebrate remains are rare large- invertebrate prey organisms represented the in the Lochkovian and Pragian; some pectoral fi n trophic base to sustain such large predators, which spines of Machaeracanthus are found (Frey et al. reached body lengths exceeding one meter. 2014). Eifelian and Givetian Emsian At the beginning of the Eifelian, the carbonate Oxygen content continued to fl uctuate in the production increased further and some massive Emsian of the eastern Anti-Atlas, probably limestone beds were deposited, interrupted only controlled by sea-level to some extent (Klug et by the Choteč-transgression. On the Tafi lalt al. 2008; De Baets et al. 2010; Frey et al. 2014; Platform, the carbonates overlying the dark Aboussalam et al. 2015; Klug et al. 2018). sediments of this transgression show many Facies changes in the Tafi lalt and Maïder are indications for condensed sedimentation such rather uniform in the sense that changes from as eroded fossils, iron oxide-stained layers, high argillaceous to carbonate sedimentation occurred abundance of more or less fragmented mollusc roughly synchronously in the Emsian (Massa conchs etc. The fauna is dominated by cephalopods 1965; Hollard 1974; Kaufmann 1998). In the (ammonoids, orthocerids, oncocerids, bactritids) Emsian sediments, geographical differences in and dacryoconarids, but bivalves (abundant), facies, sediment thickness and fossil content are crinoids, trilobites, brachiopods and gastropods still low and correspondingly, the marine basins of also occur. Overall, benthos plays a subordinate the eastern Anti-Atlas did not change ecologically role, while nektonic and planktonic organisms are very much geographically. Although the oxygen both diverse and abundant. content was likely varying, both benthic and non- In the Maïder, carbonates prevail as well, but the benthic diversity stayed reasonably high until the sequences are much thicker and less fossiliferous end of the Zlíchovian (early Emsian; Massa 1965; (e.g., Jebel El Otfal, eastern Jebel El Mrakib,

74 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Jebel Issoumour), thus suggesting a greater water placoderms Maideria falipoui Eastmanosteus sp. depth. Until the end of the Eifelian, the carbonate and Hollardosteus marocanus. Remains of large and fossil content fl uctuated gently (Massa 1965), arthrodires possibly belonging to Eastmanosteus likely refl ecting a mix of eustatic and regional were found both in the strata following the sea-level changes (cf. Kaufmann 1998; Haq and Choteč- and Kačák-Events of Filon Douze Schutter 2008). Following the early Eifelian and Ouidane Chebbi. Chondrichthyan teeth of Choteč-Event and the late Eifelian Kačák-Event, Omalodus schultzei and Phoebodus fastigatus the clay and organic content increased and locally, from the Givetian of the southern Tafi lalt Platform fossils are preserved in iron oxides. were also reported (Hampe et al. 2004; Kaufmann On the Tafi lalt Platform, carbonate deposition 1998). Additionally, the dipnoan Dipnotuberculus lasted through the entire or at least parts of the gnathodus was described from the Maïder Givetian. In the basal Givetian, ammonoids and (Campbell et al. 2002). In any case, this moderate other cephalopods occur in a moderate abundance diversity of vertebrate predators of varying size and diversity. Especially in the northern Tafi lalt, suggests that the invertebrate fauna provided the sometimes massive limestone beds are full enough prey organisms for these predators to of trace fossils, indicating a good oxygenation thrive. of the sea-fl oor. In the southern Tafi lalt, the early Givetian contains allochthonous sediments full of Frasnian corals and brachiopods; these organisms possibly lived in somewhat shallower water. As mentioned above, lateral and vertical facies From the Tafi lalt Platform towards the Tafi lalt changes are more pronounced than during the and Maïder Basin, the Givetian sections become Early and Middle Devonian. This suggests an marly or clayey close to the base of the Frasnian. increasing ecological differentiation of the region. As far as invertebrate fossil preservation is At the latest with the beginning of the Frasnian, concerned, it changes accordingly from carbonatic argillaceous sedimentation began in most parts internal moulds (sometimes with calcitic shell; of the Tafi lalt Basin, the Maïder Basin and e.g., Bockwinkel et al. 2009) to goethite where the even on parts of the Tafi lalt Platform, refl ecting clay content reaches higher levels (e.g., at Hassi rising sea-levels (e.g., Wendt 1988; Kaufmann Nebech; Bensaïd 1974; Bockwinkel et al. 2013). 1998; Lubeseder et al. 2010). At the same time, Cephalopod diversity became rather high towards strongly condensed sedimentation happened in the end of the Givetian with tens of ammonoid the Frasnian in the southwestern Maïder and on species (Bockwinkel et al. 2015, 2017) as well as the northern Tafi lalt Platform (e.g., Wendt 1988; other cephalopods and only rare benthics. On the Wendt and Belka 1991; Hüneke 2006). Therefore, slope from the Tafi lalt to the Maïder Basin (Jebel there was likely a stronger differentiation in both Amessoui, Ottara), allochthonous layers rich in water depth and oxygen availability. corals, stromatoporoids, crinoids and brachiopods Frasnian to early Famennian sediments often alternate with argillaceous layers, yielding a more display dark colours and have a high organic pelagic fauna. This documents an increase in content with abundant iron-bearing minerals water depth (Lubeseder et al. 2010). (‘Kellwasser Facies’ sensu Wendt and Belka The light grey Eifelian to early Givetian 1991), refl ecting the high organic productivity carbonates and claystones of the Maïder do yield on land (abundant wood fragments) and in the occasional invertebrate remains such as corals, sea as well as the low oxygen of the lower water crinoids, brachiopods, trilobites, etc. Particularly layers. This is corroborated by the facts that these at Jebel Rheris, Jebel Issoumour, Jebel Oufatene, sediments are rather poor in benthic fauna. In Madene El Mrakib and around the reef-mound spite of the widespread low oxygen content, there Aferdou El Mrakib, reef fauna occurs in more or still was enough oxygen for some organisms as less rock-forming amounts, sometimes in the form documented in local trace fossil assemblages of biostromes or carbonate build-ups (Kaufmann (e.g., Filon Douze; own fi eld data). 1998; Fröhlich 2006; Tessitore et al. 2013, 2016). In the central Tafi lalt Platform, carbonate Towards the end of the Givetian, carbonate sedimentation persisted throughout much of the production decreased and locally (particularly in Late Devonian (Wendt 1985) and brachiopods, the depocentre), ammonoid associations occur crinoids, bivalves, gastropods, as well as small that show the same goethite-preservation as in the rugose corals occur in a mostly low diversity and Tafi lalt Basin (Bockwinkel et al. 2015). moderate to low abundance (own observations; Machaeracanthus cf. peracutus continues compare, e.g., Massa 1965). The Kellwasser into the Eifelian of Tafi lalt and Maïder, but it Limestone as well as some early and middle is less abundant than in the Emsian. From the Famennian limestones can be very rich in Tafi lalt and Maïder, Lelièvre et al. (1993) and fossils, but mostly cephalopods (occasionally, Rücklin and Clément (2017) further report the brachiopods, gastropods, bivalves, trilobites and

75 Chapter II: Fossil-Lagerstätten and Preservation of Fossils solitary corals also occur in low to moderate In spite of the great end-Frasnian mass numbers). extinction, which left its impressive traces also Although the early Frasnian deposits are in Morocco (Buggisch 1991; Wendt and Belka rather poor in vertebrates, the late Frasnian 1991; Rücklin 2010, 2011), the Famennian sediments yielded a rich vertebrate assemblage. vertebrate diversity is even higher than that of For example, Rücklin and Clément (2017) listed the Frasnian. Apparently, vertebrate assemblages the genera Enseosteus, Walterosteus, Rhinosteus, recovered during the early Famennian. Draconichthys, Erromenosteus, Brachyosteus, Accordingly, a great number of placoderm taxa Brachydeirus, Oxyosteus, Dinomylostoma, were found in the Tafi lalt: Selenosteidae gen. et Holonema, and Aspidichthys. As far as sp. indet., Dunkleosteus marsaisi, D. terrelli, chondrichthyans are concerned, Derycke (2017) Tafi lalichthys lavocati, Mylostomidae gen. et sp. reported fi n spines of Ctenacanthus sp. indet., Titanichthys termieri and Alienacanthus In the southeastern of the Maïder Basin sp. (Lehman 1956, 1964, 1967; Frey et al. (Madene El Mrakib, Rich Bel Ras), the 2018). Rücklin and Clément (2017) also report Kellwasser levels are represented by dark and sarcopterygians of the families Actinistia and massive cephalopod limestones (Wendt and Belka Tristichopteridae (Lehman 1977, 1978; Lelièvre 1991). These sediments are rich in Archaeopteris- and Janvier 1986). The number of chondrichthyan wood (Meyer-Berthaud et al. 1999), sometimes taxa is even more impressive. Derycke (1992, overgrown by holdfasts of some of the oldest 2017) as well as Ginter et al. (2002) listed pseudoplanktonic crinoids (Klug et al. 2003). numerous taxa from the Tafi lalt. In the Maïder, oxygen-depleted conditions Famennian recurred repeatedly in the lower part of the water column, which were not suited for such Much of the Famennian succession is argillaceous more demersal durophagous chondrichthyans in the Maïder and condensed carbonatic on the to survive over a prolonged time. By contrast, Tafi lalt Platform. In both regions, the Famennian chondrichthyans with grasping dentition such as is rich in diverse cephalopod associations (e.g., the phoebodontids and cladodonts were probably Korn and Bockwinkel 2017 and references living in the water column (Ginter et al. 2010) therein); these fossils are preserved either in and thus, oxygen-poor conditions in the bottom goethite or in carbonates (based on comparisons water represented only a minor problem for with our analysed samples; see Tab. 1). In them. Following Ginter (2000, 2001), we thus combination with the mostly scarce benthic fauna, interpret the Maïder chondrichthyan assemblage this suggests low oxygen levels of the bottom as belonging to the “intermediate Phoebodus- waters. In the middle and late Famennian of the Thrinacodus biofacies […] of moderately deep Tafi lalt, limestones of locally strongly fl uctuating shelves”. In addition to the vertebrates listed thickness occur, which also vary strongly in above, we found skulls of onychodontids in the their fossil content (cephalopods, crinoids, middle Famennian, which await their description. brachiopods), documenting phases of moderate According to these published occurrences, the to good aeration in more or less shallow water palaeobiodiversity of chondrichthyans surpassed conditions (e.g., Wendt et al. 1984; Wendt 1988). that of placoderms following the Kellwasser Remarkably, the sediments of the Hangenberg Facies in the Tafi lalt. Black Shale contain abundant ammonoids, occasionally orthocerids, small trace fossils, abundant bivalves and other fossils (Klug et al. 2016). The massive sandstones above indicate a Exceptional preservation and Fossil- regressive regime and likely were deposited during Lagerstätten the end-Famennian regression (Kaiser et al. 2011; Becker et al. 2018). Palaeoecological changes Already in 1970, Seilacher coined the term throughout the Famennian and Tournaisian of “Fossil-Lagerstätte”, which is widely used today the southern Maïder were studied by Frey et al. (Seilacher et al. 1985; Bottjer et al. 2002). He (2018). sub-classifi ed Fossil-Lagerstätten into Konservat- Around the Devonian/ Carboniferous Lagerstätten and Konzentrat-Lagerstätten. boundary, palaeobiodiversity is usually low. Some silt- and sandstone beds contain abundant Konzentrat-Lagerstätten of the eastern Anti-Atlas brachiopods and there are also some layers rich This kind of Fossil-Lagerstätte is characterized by in cephalopods. Starting from the latest Devonian a vast amount of specimens that do not necessarily into the Viséan, trace fossils can be diverse and have to be particularly well-preserved (e.g., abundant (Cruziana-like and Rusophycos-like Seilacher et al. 1985; Seilacher 1990; Bottjer et traces, Diplichnites, Asteriacites etc.). al. 2002). In the eastern Anti-Atlas, this kind of

76 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fossil-Lagerstätte is quite common. Thus, it is 6. Low diversity cephalopod accumulations impossible to provide a comprehensive list. We (several species of Platyclymenia, are focusing here on cephalopods, although there Prionoceras, Orthocerida) in the middle are also Konservat-Lagerstätten of, e.g., crinoids Famennian (Platyclymenia annulata (e.g., Scyphocrinites/ Camarocrinus, Silurian/ Zone) of the Tafi lalt Platform and the Devonian boundary), brachiopods (e.g., Ivdelinia southeastern Maïder region (Korn 1999). and Devonogypa, Middle Devonian), corals (e.g., This stratigraphic interval often also yields Phillippsastrea, Middle Devonian), mixed benthic placoderm remains of Dunkleosteus, in the communities (e.g., Red Fauna; Klug et al. 2018) Maïder even complete skeletons in huge and other invertebrates in the eastern Anti-Atlas. nodules up to 4 m long (Lehman 1956, Some conspicuous examples of cephalopod mass 1964, 1976). occurrences (Fig. 5, 6) are listed below: 7. Moderate diversity cephalopod 1. Low diversity mass occurrences of the accumulations (several species of orthocerid Temperoceras ludense and Alpinites, Cymaclymenia, Cyrtoclymenia, other cephalopods in the late Silurian Discoclymenia, Endosiphonites, (Polygnathoides siluricus conodont Zone) Erfoudites, Falciclymenia, Gundolfi ceras, and late Lochkovian (Kröger 2008); Mimimitoceras, Platyclymenia, 2. High diversity cephalopod accumulations Posttornoceras, Praeglyphioceras, (Fidelites spp., Subanarcestes Prionoceras, Orthocerida) of the marhoumensis, Pinacites jugleri, late Famennian Clymenia Stufe Crispoceras spp., Lobobactrites sp., (Gonioclymenia ammonoid genozone; Oncocerida, Orthocerida) in the early e.g., Korn 1999). This interval contains Eifelian (Pinacites jugleri ammonoid also abundant microremains of Zone) of the southern Tafi lalt Platform chondrichthyans in the southern Tafi lalt (e.g., Filon Douze/ Jebel Ouaoufi lal; Klug (Ginter et al. 2002). 2002; Kröger 2008); In the Middle Devonian, there are numerous 3. High diversity cephalopod accumulations localities with Konzentrat-Lagerstätten of more or (many species of Allopharciceras, less allochthonous reefal faunal assemblages; true Extropharciceras, Petteroceras, reefs and biostromes are rare in the eastern Anti- Pharciceras, Pseudoprobeloceras, Atlas (Fröhlich 2003). These moderate diversity Oxypharciceras, Sympharciceras, accumulations of reef fauna may contain the Tornoceras, Orthocerida, Oncocerida) in following taxa: Phillipsastrea sp., Xystriphyllum the late Givetian (e.g., Synpharciceras sp., Heliophyllum halli moghrabiense, clavilobum ammonoid Zone) of the Cystiphylloides sp., Acanthophyllum sp., northern Tafi lalt Platform (Bockwinkel et Thamnopora spp., auloporids, favositids, al. 2009, 2017); heliolitids, brachiopods, crinoids, stromatoporoids 4. Moderate diversity cephalopod (e.g., Kaufmann 1998). accumulations (several species of Archoceras Beloceras, Carinoceras, Konservat-Lagerstätten of the eastern Anti-Atlas Crickites, Manticoceras, Tornoceratidae, Orthocerida, Oncocerida) occur in Also called conservation lagerstätten, these several layers, some of which associated deposits received their name from their unusual with remains of arthrodires (upper preservation of animals or body parts that Palmatolepis rhenana – Pa. linguiformis are normally not preserved (Seilacher 1970, conodont Zones; Rücklin 2010, 2011) 1990). The most famous Palaeozoic Konservat- and Archaeopteris wood fragments in Lagerstätte of Morocco occurs undoubtedly in the Kellwasser Limestone of the Tafi lalt the Fezouata Formation, which was compared to Platform and the southeastern Maïder the classical Konservat-Lagerstätte of the Burgess (Wendt and Belka 1991); Shale (van Roy et al. 2010). The term Konservat- 5. Moderate diversity cephalopod Lagerstätte implies exceptional preservation of accumulations (several species of soft tissues, be they part of an organism with or Armatites, Cheiloceras, Falcitornoceras, without hard parts. The Devonian of Morocco is Maeneceras, Paratorleyoceras, known for localities yielding articulated skeletons Polonoceras, Orthocerida, Oncocerida, of various organisms such as trilobites, crinoids Brachiopoda) in the early Famennian and also fi shes, but soft parts were not documented (Cheiloceras subpartitum to previously and thus, Konservat-Lagerstätten in a Paratorleyoceras globosum ammonoid stricter sense were also unknown. Zones) of the Tafi lalt Platform and the Recently, we described a fauna from the southeastern Maïder (Becker 2002). latest Famennian Hangenberg Black Shale of

77 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 6. Examples of Konzentrat-Lagerstätten (concentration lagerstätten) in the eastern Anti-Atlas. A, Mass occurrences of Temperoceras ludense and other cephalopods in the late Silurian, Ouidane Chebbi. Width about 1.5 m. B, High diversity cephalopod accumulation in the Eifelian of Filon Douze. C, Moderate diversity cephalopod accumulations (mainly Gephuroceratidae) in the Frasnian Kellwasser Limestone of Jebel Amelane. Width ca. 0.5 m. D, Moderate diversity reef fauna assemblage dominated by thamnoporids, Eifelian, Madene El Mrakib. E, F, Moderate diversity cephalopod accumulations (mainly cheiloceratids, orthocerids and brachiopods) in the early Famennian of Taouz (E) and Madene El Mrakib (F). G, H, Low diversity cephalopod accumulations (mainly Platyclymenia) in the middle Famennian (Platyclymenia annulata Zone) of Tachbit/ Mkarig (G) and Madene El Mrakib (H); width (in H) ca. 0.7 m.

78 Chapter II: Fossil-Lagerstätten and Preservation of Fossils the southern Maïder (Klug et al. 2016). These covered by sediment), ‘stagnation’ (hydrographic deposits yielded abundant non-mineralized régime; organic remains preserved due to low cephalopod jaws, a few carbonized plant remains oxygen levels) and ‘bacterial sealing’ (early (algae), articulated arthropod remains lacking diagenetic régime; bacterial fi lms replace or mineralized cuticles and also organic parts inside surround soft tissues, sometimes also fostering ammonoid body chambers that likely represent rapid phosphatisation; e.g., Kear et al. 1995). soft part remains. Accordingly, this deposit could The fossils of the Thylacocephalan Layer are be considered a Konservat-Lagerstätte because preserved in a set of minerals including mainly of articulated remains of skeletons and the hydroxyapatite, haematite, iron hydroxides, pyrite, preservation of abundant non-mineralized tissues. siderite and quartz (Tab. 1). As discussed above, Near the early to middle Famennian boundary the iron oxides and hydroxides likely are products (probably Palmatolepis rhomboidea or Pa. of slow weathering of primary pyrite in both the marginifera conodont Zone), we discovered a vertebrates and invertebrates (rarely, remains reddish argillaceous layer a few tens of centimeters of which are preserved). This reduces the list of thick and rich in iron oxides in the southern Maïder primary (now altered) minerals to phosphates and (Frey et al. 2018). This layer is characterized by pyrite. Other Konservat-Lagerstätten with fossils abundant fl at nodules, mostly 50 to 100 mm in preserved in pyrite and phosphates are the famous diameter and usually containing the carapaces Early Devonian Hunsrück Slate and the Early and sometimes (primarily chitinous) appendages, Jurassic Posidonia Slate (Seilacher et al. 1985). eyes, gills, and possibly other organs (ongoing Seilacher et al. (1985) somewhat arbitrarily research) of thylacocephalans (Fig. 7, 8). This placed these two Konservat-Lagerstätten in two Thylacocephalan Layer (Frey et al. 2018) also different parts of the proposed ternary diagram yields articulated gnathostome remains, mostly of of Konservat-Lagerstätten. While the Posidonia chondrichthyans, especially cladoselachian-like Slate is placed in the stagnation corner, the forms, symmoriids and phoebodontids as well as Hunsrück Slate (and also Solnhofen) are half way sarcopterygians and various arthrodires (Fig. 9, between the stagnation corner and the obrution 10). Placoderms are commonly preserved in huge corner, because post mortem transport and mass nodules, which likely refl ect the outline of the fl ows rapidly covering organic remains played entire body (Fig. 9). As far as the chondrichthyans an important role. In the case of Solnhofen, are concerned, we found remains of musculature, bacterial mats were also important, shifting its liver, digestive tract with prey remains, lateral position towards the ‘bacterial sealing’ corner. lines, body outline, integument and cartilage Evidence for transport, obrution and bacterial (the latter being calcifi ed primarily, but still mats have not been detected in the Devonian having a low preservation potential; Fig. 10). Thylacocephalan Layer. In combination with The preservation of such structures in articulated the facts that the Maïder Basin was a restricted skeletons are classical characters of a Konservat- basin with water exchange being limited by Lagerstätte (e.g., Seilacher et al. 1985). the Tafi lalt Platform and the scarcity of benthic Seilacher et al. (1985: fi g. 11) further refi ned organisms in the Thylacocephalan Layer, the the classifi cation of Konservat-Lagerstätten in a Konservat-Lagerstätte of the Thylacocephalan triangle (Fig. 12). Its corners are labelled ‘obrution’ Layer and other fossiliferous layers of the (sedimentational régime; organic remains quickly Famennian in that region are here assigned to

Fig. 7. The Thylacocephalan Layer (early middle Famennian) in the southern Maïder (Madene El Mrakib). A, thylacocephalan-bearing concretions in situ. B, surface accumulation of thylacocephalan-bearing nodules.

79 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 8. Phosphatic preservation of thylacocephalans from the Thylacocephalan Layer (early middle Famennian) in the southern Maïder (the orange-coloured sparitic fi lling is calcitic), PIMUZ 36872. A, lateral view of a carapace. B, broken specimen showing parts of the appendages preserved in apatite (Tab. 1).

Fig. 9. Preservation of gnathostomes from the Thylacocephalan Layer (early middle Famennian) in the southern Maïder. A, undescribed placoderm (? Driscollaspis sp.), PIMUZ 36882, Rich Bel Ras; note the preserved dorsal fi n and the caudal fi n (the concretion traced the body outline). B, cladoselachid chondrichthyan, PIMUZ 36883, Madene El Mrakib; preserved with several haematitic soft parts; note the ridge around the body that likely formed when the carcass sank into the mud ‒ the body itself collapsed later due to decay and sediment compaction, leaving a shallow depression.

80 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 10. Soft-tissue preservation of a cladoselachid chondrichthyan, PIMUZ 36884, Thylacocephalan Layer (early middle Famennian), Madene El Mrakib (same specimen as in Fig. 12B. A, thoracal region directly anterior to the pelvic fi n with mineralized soft parts (muscles, neural arch cartilage, liver). B, detail of A showing muscle fi bres. the stagnation corner. Another shared character characters predominantly based on Seilacher underlining the taphonomic similarity to the (1985). 19 well-known Konservat-Lagerstätten Posidonia Slate is the stratigraphically (much of and the two herein described ones of the Devonian the early and middle Famennian; Webster et al. of Morocco were coded accordingly and analyzed 2005) and geographically widespread occurrence in a Principal Component Analysis (Fig. 13). of pseudoplanktonic crinoids in the middle Remarkably, the Burgess-type Lagerstätten Famennian of both the Maïder and the southern plotted in a fi eld well separated from the black Tafi lalt Platform (Klug et al. 2003; Webster et al. shales and the Plattenkalke plotted again in a 2005; own unpublished fi eld data; Fig. 11). distinct fi eld. A black shale fi eld contains both In the attempt to classify marine Konservat- Moroccan Konservat-Lagerstätten at opposite Lagerstätten in a more coherent way we use 31 ends with the Thylacocephalan Layer being

Fig. 11. Detail of a huge colony (1.10 m long with over 70 calyces) of the pseudoplanktonic crinoid Moroccocrinus ebbinghauseni from the late early Famennian of Jebel Ouaoufi lal. The Archaeopteris log is not preserved but was likely at the top of the image (note the difference in stem alignment on top and in the lower three quarters), running parallel to the hammer, and burying some of the crinoids below it. The colony was already excavated and is seen from below; on the other side, the degree of articulation is much lower.

81 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 12. Ternary diagram of the three main types of conservation deposits of Seilacher et al. (1985). Some of the most famous examples are indicated by circles; note that the positions of the circles are somewhat arbitrary, partially because the respective roles of the main factors like, e.g., obrution and stagnation, change within these deposits and across the sedimentary basins. Also, there is no quantitative measure yet to place Lagerstätten within this diagram. In any case, obrution plays a much larger role in the famous Cambrian deposits compared to the Mesozoic black shales as well as the here portrayed Late Devonian Konservatlagerstätten from the eastern Anti-Atlas. close to La Voulte (which share the abundance weathering in the desert environment. This is of echinoderms, arthropods and ammonoids) corroborated by rare fi nds of completely pyritized and the Hangenberg Black Shale being close to fossils from the same strata in depths of over 10 Mazon Creek. This underlines the important role m below today’s surface and by pyrite remains in of low oxygen levels in the Maïder Basin during the centre of some only partially oxidized fossils. the Famennian, as proposed already by Frey et al. In turn, this primary abundance of pyrite (now (2018). goethite and iron hydroxides) in combination with the clayey facies and the scarcity of benthos in some strata suggest that the Thylacocephalan Conclusions Layer containing exceptionally preserved gnathostomes was deposited under oxygen-poor We chemically analysed various Devonian conditions (Klug et al. 2016, Frey et al. 2018). and Early Carboniferous fossils from the This is supported by the palaeogeographical eastern Anti-Atlas. Ammonoids and other situation of the Maïder Basin (Fig. 4) that was cephalopods from this region and time interval closed to the south and north by land, while to the are preserved in calcite, goethite (sometimes east and west, the shallower regions of the Tafi lalt with haematite), quartz, baryte (only in the Early Platform and the Maïder Platform limited water Carboniferous; Korn 1988), and clay minerals. exchange (Wendt 1988; Kaufmann 1998). As far as vertebrates and the thylacocephalansare Hypoxic to anoxic conditions in the bottom concerned, we found the same minerals except waters explain the absence of protacrodontids, baryte but with hydroxyapatite. In particular, which mainly occur in shallower, better oxygenated the results show that the chondrichthyan waters (Ginter 2000). Clairina and Jalodus likely musculature is now predominantly preserved in preferred deeper environments than the one in the goethite and haematite. Both placoderm bones Maïder Basin. Following Ginter (2000), the taxa and chondrichthyan cartilage are preserved in present in the Maïder (Phoebodus and cladodonts) apatite (mainly hydroxyapatite and probably point at an intermediate water depth. also francolite). Especially the abundance of Taking the exceptional fossil preservation iron oxides and hydroxides suggest that some of (soft-tissue preservation), composition of the these fossils were originally preserved in pyrite fossil assemblages (scarcity of benthos and (at least partially), which was altered due to deep demersal forms), the mineralogic composition of the fossils (primary pyrite, phosphates) and

82 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Fig. 13. Principal Component Analysis of some marine Konservat-Lagerstätten. Classifi cation based on Tab. 3, which is based on the questionnaire by Seilacher et al. (1985). Note the perfect grouping of early Palaeozoic Burgess type Lagerstätten, Black Shale Lagerstätten and the Plattenkalke. Also note that the two Famennian Lagerstätten from Morocco plot at the limits of the Black Shale Lagerstätten. the palaeogeographic setting into account, Oukherbouch (Tafraoute) and René Kindlimann the Famennian Thylacocephalan Layer is a (Aathal, Switzerland) helped in the fi eld. Lydia Konservat-Lagerstätte. Since indications for Zehnder and Sebastian Cionoiu (both Earth mass movements, current alignment and traces of Sciences Department, ETH Zürich) are thanked microbial activity sealing organismic remains have for their generous help with the XRD- and Raman- not been found, the Thylacocephalan Layer and analyses. We acknowledge the constructive the Hangenberg Black Shale are here considered reviews of XX and XX. as two examples of stagnation Lagerstätten sensu Seilacher et al. (1985) and thus the fi rst two of this kind from the Devonian of northern Africa (Fig. References 12, 13). In our Principal Component Analysis of marine Konservat-Lagerstätten, these two Aboussalam, Z.S., Becker, R.T. & Bultynck, P. 2015: Moroccan Lagerstätten plotted in the fi eld with of Emsian (Lower Devonian) conodont stratigraphy the black shales such as, e.g. the Triassic ones of and correlation of the Anti-Atlas (Southern Austria, Switzerland and China, the Jurassic ones Morocco). Bulletin of Geosciences, 90(4), 893–980. of Europe etc. This new approach, based on the Arratia, G., Schultze, H.-P., Tischlinger, H. & Viohl, G. questionnaire by Seilacher et al. (1985), allows 2015: Solnhofen. Ein Fenster in die Jurazeit. Pfeil, München. a more objective classifi cation of Konservat- Becker, R.T. 2002: Stratigraphische Gliederung und Lagerstätten. Ammonoideen-Faunen im Nehdenium (Oberdevon II) von Europa und Nord-Afrika. Courier Acknowledgements. ‒ We greatly appreciate Forschungsinstitut Senckenberg, 155, 1–405. the support of the Swiss National Science Becker, R.T. & Aboussalam, Z.S. 2011: Emsian Foundation for fi nancial support of our research chronostratigraphy – preliminary new data and projects (Project Numbers 200020_132870, a review of the Tafi lalt (SE Morocco). SDS 200020_149120, 200021_156105). We thank Newsletter, 26, 33–43. the colleagues of the Ministère de l’Energie, Becker, R.T., Bockwinkel, J., Ebbighausen, V. & des Mines, de l’Eau et de l’Environnement House, M.R., 2000. Jebel Mrakib, Anti-Atlas (Morocco), a potential Upper Famennian substage (Direction du Développement Minier, Division boundary stratotype section. Notes et Mémoires du du Patrimoine, Rabat, Morocco) who provided Service géologique Maroc, 399, 75–86. working and sample export permits. Saïd Becker, R. T., Hartenfels, S., Klug, C., Aboussalam,

83 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Z. S. & Afhüppe, L. 2018: The cephalopod-rich eastern Anti-Atlas and the western Dra Valley. Famennian and Tournaisian of the Aguelmous Bulletin of Geosciences, 85, 317–352. DOI Syncline (southern Maïder). Münstersche 10.3140/bull.geosci.1172 Forschungsberichte zur Geologie und Paläontologie, Derycke, C., 1992. Microrestes de Sélaciens et autres 110 (1): 273-306 Vertébrés du Dévonien supérieur du Maroc. Bulletin Belka, Z., Klug, C., Kaufmann, B., Korn, D., Döring, du Muséum national d’Histoire Naturelle, Section S., Feist, R. & Wendt, J. 1999: Devonian conodont C, Sciences de la terre, paléontologie, géologie, and ammonoid succession of the eastern Tafi lalt minéralogie, 14 (1), 15–61. (Ouidane Chebbi section), Anti-Atlas, Morocco. Derycke, C., 2017. Paléobiodiversité des gnathostomes Acta Geologica Polonica, 49 (1), 1–23. (chondrichthyens, acanthodiens et actinoptérygiens) Bensaïd, M. 1974 : Etude sur des Goniatites a la limite du Dévonien du Maroc (NW Gondwana). In : du Dévonien Moyen et Supérieur, du Sud Marocain. Zouhri, S. (ed.), Paléontologie des vertébrés du Notes de Service Carte géologique du Maroc, 36 Maroc : état des connaissances. Mémoires de la (264), 81–140. Société Géologique de France, 180, 47–78. Berkowski, B. 2006 : Vent and mound rugose coral Derycke, C., Spalletta, C., Perri, M.C. & Corradini, associations from the Middle Devonian of Hamar C. 2008. Famennian chondrichthyan microremains Laghdad (Anti-Atlas, Morocco). Geobios, 39, 155– from Morocco and Sardinia. Journal of Paleontology, 170. 82, 984–995. Blum, J.R. 1843: Die Pseudomorphosen des Dietl, G. & Schweigert, G. (2001). Im Reich der Mineralreichs. 378 pp., Schweizerbart, Stuttgart. Meerengel. Pfeil Verlag, München. Bockwinkel, J., Becker, R.T. & Aboussalam, Z.S. 2017: Döring, S. 2002. Sedimentological evolution of the Ammonoids from the late Givetian Taouzites Bed late Emsian to early Givetian carbonate ramp in the of Ouidane Chebbi (eastern Tafi lalt, SE Morocco). Mader (eastern Anti-Atlas, SE-Morocco). 121 pp. Neues Jahrbuch für Geologie und Paläontologie PhD-thesis, unpublishes, Tübingen. http://tobias- Abhandlungen, 284, 307–354. lib.ub.uni-tuebingen.de/volltexte/2002/560/ Bockwinkel, J., Becker, R.T. & Ebbighausen, V. Döring, S. & Kazmierczak, M. 2001. Stratigraphy, 2009: Upper Givetian ammonoids from Dar geometry, and facies of a Middle Devonian ramp- Kaoua (Tafi lalt, SE Anti-Atlas, Morocco). Berliner to-basin transect (Eastern Anti-Atlas, SE Morocco). paläobiologische Abhandlungen, 10, 61–128. Facies, 44, 137–150. Bockwinkel, J., Becker, R.T. & Ebbighausen, V. 2013: Downs, R.T. & Hall-Wallace, M. (2003) The American Late Givetian ammonoids from Hassi Nebech Mineralogist Crystal Structure Database. American (Tafi lalt Basin, Anti-Atlas, southern Morocco). Mineralogist 88, 247-250. Fossil Record, 16, 5–65. Etter, W. 2002. Monte San Giorgio: Remarkable Bockwinkel, J., Becker, R.T. & Ebbighausen, V. Triassic Marine Vertebrates. pp. 221–242.In: 2015: Late Givetian ammonoids from Ait Ou Bottjer, D. J., Etter, W., Hagadorn, J. W. & Tang Amar (northern Maider, Anti-Atlas, southeastern C.M. (Eds.), Exceptional Fossil Preservation. 403 Morocco). Neues Jahrbuch für Geologie und pp.Columbia University Press, New York. Paläontologie, Abh., 278, 123–158. Forey, P.L., Yi, L., Patterson, C. & Davies, C.E. Bottjer, D.J., Etter, W., Hagadorn, J.W. & Tang, C.M. (2003) Fossil fi shes from the Cenomanian (Upper (eds.) 2002: Exceptional Fossil Preservation. Cretaceous) of Namoura, Lebanon. Journal of Columbia University Press, New York. Systematic Palaeontology, 1: 227-330. Buggisch, W. 1991: The global Frasnian-Famennian Frey, L., Naglik, C., Hofmann, R., Schemm-Gregory, “Kellwasser Event”. Geologische Rundschau, 80, M., Frýda, J., Kröger, B., Taylor, P.D., Wilson, M.A. 49–72. & Klug, C. 2014. Diversity and palaeoecology Campbell, K.S.W., Barwick, R.E., Chatterton, B.D.E. of Early Devonian invertebrate associations in & Smithson, T.R.2002. A new Middle Devonian the Tafi lalt (Anti-Atlas, Morocco). Bulletin of dipnoan from Morocco: structure and histology of Geoscience, 89(1), 75–112. the dental plates. Records of the Western Australian Frey, L., Rücklin, M., Korn, D. & Klug, C. 2018. Effects Museum, 21, 39–61. of Late Devonian mass extinctions on alpha diversity, Chatterton, B.D.E. & Gibb, S. 2010. Latest Early ecospace occupation and vertebrate assemblages to Early Middle Devonian Trilobites from the in south-eastern Morocco. Palaeogeography, Erbenochile Bed, Jbel Issoumour, Southeastern Palaeoclimatology, Palaeoecology, 496, 1-17. Morocco. Journal of Paleontology, 84, 1188–1205. Fröhlich, S. 2003. Facies pattern and genesis of the Clariond, L. 1935. Etude stratigraphique sur les terrains Jebel Rheris biostromes (Givetian, Eastern Anti- du Sud-Marocain. La série primaire du Sarhro, Atlas, Morocco). Facies, 49, 209-220. du Maider et du Tafi lalt. Publication Association Ginter, M. 2000. Late Famennian pelagic shark Etudes géologiques du Méditerrané occidental, assemblages. Acta Geologica Polonica, 50, 369– Géologie des Chaines nordafricaines, 5,1 (12), 386. 3–10. Ginter, M. 2001. Chondrichthyan biofacies in the De Baets, K., Klug, C. & Monnet, C. 2013. Intraspecifi c Late Famennian of Utah and Nevada, Journal of variability through ontogeny in early ammonoids. Vertebrate Paleontology, 21, 714-729. Paleobiology, 39 (1), 75-94. Ginter, M., Hairapetian, V. & Klug, C. 2002. De Baets, K., Klug, C. & Plusquellec, Y. 2010. Famennian chondrichthyans from the shelves of Zlíchovian faunas with early ammonoids from North Gondwana. Acta Geologica Polonica, 52, Morocco and their use for the correlation of the 169–215.

84 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Grogan, E. D. & R. Lund. 2002. The geological and of Morocco. Acta Palaeontologica Polonica, 59, biological environment of the Bear Gulch Limestone 135–145. (Mississippian of Montana, USA) and a model for Klug, C., Frey, L., Korn, D., Jattiot, R. & Rücklin, M. its deposition. Geodiversitas, 24: 295-315. 2016. The oldest Gondwanan cephalopod mandibles Halamski, A. T. & Baliński, A., 2013. Middle (Hangenberg Black Shale, Late Devonian) and the Devonian brachiopods from the southern Maïder Mid-Palaeozoic rise of jaws. Palaeontology, 59, (eastern Anti-Atlas, Morocco). Annales Societatis 611–629. Geologorum Poloniae, 83, 243–307. Klug, C., Döring, S., Korn, D. & Ebbighausen, V. 2006. Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001): The Viséan sedimentary succession at the Gara PAST: Palaeontological statistics software package el Itima (Anti-Atlas, Morocco) and its ammonoid for education and data analysis. Palaeontologia faunas. Fossil Record, 9 (1), 3–60. Electronica, 4(1): 1-9. Klug, C. & Hoffmann, R. (2018): Trace fossils of Hampe, O.Z., Aboussalam, Z.S. & Becker, R.T. 2004. Actiniaria (Conichnus) from the Early Devonian Omalodus teeth (Elasmobranchii: Omalodontida) of Morocco. In: Klug, C. & Korn, D. (eds.): from the northern Gondwana margin (middle Palaeontology of the Devonian of Hamar Laghdad Givetian: ansatus conodont Zone, Morocco). In (Tafi lalt, Morocco). Special volume honouring Arratia, G., Wilson, M.V.H. & Cloutier, R. (eds.): JOBST WENDT. Neues Jahrbuch für Geologie und Recent Advances in the Origin and Early Radiation Paläontologie, Abhandlungen, 290 (1): 65-74. of Vertebrates, pp. 487-504, Verlag Dr. Friedrich Klug, C., Kröger, B., Rücklin, M., Korn, D., Schemm- Pfeil, München, Germany. Gregory, M., De Baets, K. & Mapes, R.H. 2008. Haq, B.U. & Schutter, S.R. 2008: A chronology of Ecological change during the early Emsian Paleozoic sealevel changes. Science, 322, 64–68. (Devonian) in the Tafi lalt (Morocco), the origin of Hemleben, C. & Freels, D. 1977. Algen-laminierte und the Ammonoidea, and the fi rst African pyrgocystid gradierte Plattenkalke in der Oberkreide Dalmatiens edrioasteroids, machaerids, and phyllocarids. (Jugoslawien). Neues Jahrbuch für Geologie und Palaeontographica A, 283, 83–176. Paläontologie, Abhandlungen, 154, 61-93. Klug, C. Samankassou, E., Pohle, A., De Baets, K., Hollard, H. 1974: Recherches sur la stratigraphie Franchi, F. & Korn, D. (2018): Oases of biodiversity: des formations du Dévonien moyen, de l’Emsien Early Devonian palaeoecology at Hamar Laghdad, supérieur au Frasnien, dans le Sud du Tafi lalt et Morocco. In: Klug, C. & Korn, D. (eds.): dans le Ma’der (Anti-Atlas oriental, Maroc). Notes Palaeontology of the Devonian of Hamar Laghdad du Service Géologique du Maroc, 36, 7–68. (Tafi lalt, Morocco). Special volume honouring Hüneke, H. 2006 : Erosion and deposition from Jobst Wendt. Neues Jahrbuch für Geologie und bottom currents during the Givetian and Frasnian: Paläontologie, Abhandlungen, 290 (1): 9-48 Response to intensifi ed oceanic circulation between Klug, C., Schulz, H. & De Baets, K. 2009. Red Gondwana and Laurussia. Palaeogeography, trilobites with green eyes from the Early Devonian Palaeoclimatology, Palaeoecology 234, 146–167 of the Tafi lalt (Morocco). Acta Palaeontologica Kaiser, S.L., Becker, R.T., Steuber, T. & Aboussalam, Polonica, 54, 117–123. Z.S. 2011. Climate-controlled mass extinctions, Klug, C., Rücklin, M., Meyer-Berthaud, B. & Soria, facies, and sea-level changes around the A. 2003. Late Devonian pseudoplanktonic crinoids Devonian–Carboniferous boundary in the eastern from Morocco. Neues Jahrbuch für Geologie und Anti-Atlas (SE Morocco). Palaeogeography, Mineralogie, 3, 153163. Palaeoclimatology, Palaeoecology, 310, 340–364. Korn, D. 1988. Die Goniatiten des Kulmplattenkalkes Kaufmann, B. 1998. Facies, stratigraphy and diagenesis (Cephalopoda, Ammonoidea; Unterkarbon; of Middle Devonian reef- and mud-mounds in Rheinisches Schiefergebirge). Geologie und the Mader (eastern Anti-Atlas, Morocco). Acta Paläontologie in Westfalen, 11, 1-293. Geologica Polonica, 48, 43–106. Korn, D. 1999. Famennian Ammonoid Stratigraphy Kear, A.J., Briggs, D.E.G. & Donovan, D.T. 1995. of the Ma`der and Tafi lalt (Eastern Anti-Atlas, Decay and fossilization of non-mineralized tissue in Morocco). Abhandlungen der geologischen coleoid cephalopods. Palaeontology, 38, 105–131. Bundesanstalt, 54, 147179. Klein, C. & Korn, D. 2014. A morphometric approach Korn, D. & Bockwinkel, J. 2017. The genus to conch ontogeny of Cymaclymenia and related Gonioclymenia (Ammonoidea; Late Devonian) genera (Ammonoidea, Late Devonian). Fossil in the Anti-Atlas of Morocco. Neues Jahrbuch für Record, 17, 1–32. Geologie und Paläontologie, Abhandlungen, 285, Klug, C. 2001. Early Emsian ammonoids from the 97–115. eastern Anti-Atlas (Morocco) and their succession. Korn, D., Bockwinkel, J. & Ebbighausen, V. 2007. Paläontologische Zeitschrift, 74 (4), 479–515. Tournaisian and Viséan ammonoid stratigraphy in Klug, C. 2002. Quantitative stratigraphy and taxonomy North Africa. Neues Jahrbuch für Geologie und of late Emsian and Eifelian ammonoids of the eastern Paläontologie Abhandlungen, 243, 127–148. Anti-Atlas (Morocco). Courier Forschungsinstitut Korn, D., Bockwinkel, J. & Ebbighausen, V. 2016a. Senckenberg, 238, 1–109. The late Famennian tornoceratid ammonoids in Klug, C. & Korn, D. 2002. Occulded umbilicus in the the Anti-Atlas of Morocco. Neues Jahrbuch für Pinacitinae (Devonian) and its palaeoecological Geologie und Paläontologie Abhandlungen, 281(2), implications. Palaeontology, 45, 917–931. 201220. Klug, C. De Baets, K., Naglik, C. & Waters, J. 2014. Korn, D., Bockwinkel, J. & Ebbighausen, V. 2016b. New species of Tiaracrinus from the latest Emsian Middle Famennian (Late Devonian) ammonoids

85 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

from the Anti-Atlas of Morocco. 3. Tornoceratids. Devonian vertebrate biostratigraphy of western Neues Jahrbuch für Geologie und Paläontologie Gondwana and related terranes (South America, Abhandlungen, 281(3), 267281. Africa, Armorica-Bohemia, Middle East). In: Long, Korn, D., Klug, C. & Mapes, R.H. 1999. Viséan and J.A. (ed.), Palaeozoic vertebrate biostratigraphy and Early Namurian Ammonoids from the Tafi lalt biogeography. Belhaven Press , London, 139-173. (Eastern Anti-Atlas, Morocco). Abhandlungen der Lubeseder, S., Rath, J., Rücklin, M. & Messbacher, R. Geologischen Bundesanstalt, Wien, 54, 345-375. 2010. Controls on Devonian hemi-pelagic limestone Korn, D., Klug, C., Ebbighausen, V. & Bockwinkel, deposition analyzed on cephalopod ridge to slope J. 2002. Palaeogeographic meaning of a Middle sections, Eastern Anti-Atlas, Morocco. Facies, 56, Tournaisian ammonoid fauna from Morocco. 295–315. Geologica et Palaeontologica, 36, 79-86. Massa, D. 1965. Observations sur les séries siluro- Kröger, B. 2008. Nautiloids before and during the dévoniennes des confi ns algéro-marocains du Sud origin of ammonoids in a Siluro-Devonian section (1954-1955). Compagnie Française des Pétroles, in the Tafi lalt, Anti-Atlas, Morocco. Special Papers Notes et Mémoires, 8, 1187. in Palaeontology, 79, 1–112. Meyer-Berthaud, B., Scheckler, S.E. & Wendt, J. 1999. Kulczycki, J. 1957. Upper Devonian fi shes from Archaeopteris is the earliest known modern tree. the Holy Cross Mountains (Poland). Acta Nature, 398, 700701. Palaeontologica Polonica, 2, 285395. Morzadec, P. 2001. Les trilobites Asteropyginae Laetsch, T. & Downs, R. (2006) Software for du Dévonian de lAnti-Atlas (Maroc). identifi cation and refi nement of cell parameters Palaeontographica A, 262, 53-85. from powder diffraction data of minerals using the Pohle, A. & Klug, C. 2018: Body size of orthoconic RRUFF Project and American Mineralogist Crystal cephalopods from the late Silurian and Devonian of Structure Databases. Abstracts from the 19th the Anti-Atlas (Morocco). Lethaia, 51, 126-148. General Meeting of the International Mineralogical Röhl, H. J., Schmid-Röhl, A., Oschmann, W., Association, Kobe, Japan. Frimmel, A. & Schwark, L. (2001).The Posidonia Lehman, J.-P. 1956. Les Arthrodires du Dévonien Shale (Lower Toarcian) of SW-Germany: An supérieur du Tafi lalt (Sud Marocain). Notes et oxygen-depleted ecosystem controlled by sea Mémoires du Service Géologique du Maroc, 129, level and palaeoclimate. Palaeogeography, 170. Palaeoclimatology, Palaeoecology 165, 27–52 Lehman, J.-P. 1964. A propos de quelques Arthrodires Röhl, A., Schmid-Röhl, H. J., Oschmann, W., Frimmel, et Ichthyodorulites sahariens. Mémoire IFAN, 68, A. & Schwark, L. (2002). Palaeoenvironmental 193200. reconstruction of Lower Toarcian epicontinental Lehman, J.-P. 1976. Nouveaux poissons fossiles du black shales (Posidonia Shale, SW Germany): Dévonien du Maroc. Annales de Paléontologie, Global versus regional control. Geobios 35, 13–20. Vertébrés 62, 134. Rücklin, M. 2010. A new Frasnian placoderm Lehman, J.-P. 1977. Sur la présence dun assemblage from the eastern Anti-Atlas, Morocco, Ostéolépiforme dans le Dévonien supérieur du and its palaeobiogeographical implications. Tafi lalt. Compte-Rendus de lAcadémie des Palaeoworld, 19, 8793. Sciences, 285D, 151153. Rücklin, M. 2011. First selenosteid placoderms from Lehman, J.-P. 1978. A propos de deux poissons du the eastern Anti-Atlas of Morocco; osteology, Famennien du Tafi lalet. Annales de Paléontologie, phylogeny and palaeogeographical implications. Vertébrés, 64, 143-152. Palaeontology, 54, 2562. Lelièvre, H. 1984. Antineosteus lehmani n.g., n. sp., Rücklin, M. & Clément, G. 2017. Une révue des noveau brachythoraci du Dévonien inférieur du placodermes et sarcoptérygiens du Devonien Maroc présaharien. Annales de Paléontologie, 70, du Maroc. In : Zouhri, S. (ed.), Paléontologie 116-158. des vertébrés du Maroc: état des connaissances. Lelièvre, H. 1995. Description of Maideria falipoui n. Mémoires de la Société Géologique de France, 180, g., n. sp., a long snouted brachythoracid (Vertebrata, 79102. Placodermi, Arthrodira) from the Givetian of Rücklin, M., Lelièvre, H. & Klug, C. (2018): Placodermi Maider (South Morocco), with a phylogenetic from the Early Devonian Kess-Kess Mounds of analysis of primitive brachythoracids. Bulletin du Hamar Laghdad, Southern Morocco. In: Klug, C. Muséum National dHistoire Naturelle, Paris, 4e & Korn, D. (eds.): Palaeontology of the Devonian série, C, 17, 163207. of Hamar Laghdad (Tafi lalt, Morocco). Special Lelièvre, H. & Janvier, P. 1986. LEusthénopteridé volume honouring Jobst Wendt. Neues Jahrbuch für (Osteichthyes, Sarcopterygii) du Famennian Geologie und Paläontologie, Abhandlungen, 290 (Dévonien supérieur) du Tafi lalt (Maroc): nouvelle (3): 301-306. description. Bulletin du Muséum National Rücklin, M., Long, J. A. & Trinajstic, K. 2015. A new dHistoire naturelle, 4e Série, Section C, Sciences selenosteid arthrodire (‘Placodermi’) from the de la Terre, Paléontologie, Géologie, Minéralogie, Late Devonian of Morocco. Journal of Vertebrate 3, 351365. Paleontology, 35(2), e908896, 113. Lelièvre, H. & Janvier, P. 1988. Un Actinistien Seilacher, A. 1970. Begriff und Bedeutung der Fossil- (Sarcopterygii, Vertebrata) dans le Dévonien Lagerstätten. Neues Jahrbuch für Geologie und supérieur du Maroc. Compte-Rendus de Paläontologie, Monatshefte, 1970, 3439. lAcadémie des Sciences, Paris, 307, 14251430. Seilacher, A. 1990. Taphonomy of Fossil-Lagerstätten. Lelièvre, H., Janvier, P. & Blieck, A. 1993. Silurian- In Briggs, D.E.G. & Crowther, P.R. (eds),

86 Chapter II: Fossil-Lagerstätten and Preservation of Fossils

Palaeobiology: A synthesis. 266-270. Blackwell, Devonian (Emsian and Famennian) crinoids from Oxford. southeastern Morocco. Journal of Paleontology, 79, Seilacher, A., Reif, W.-E. & Westphal, F. 1985. 1052–1071. Sedimentological, ecological and temporal patterns Wendt, J. 1985. Disintegration of the continental of fossil Lagerstätten. Philosophical Transactions of margin of northwestern Gondwana: Late Devonian the Royal Society of London B, 311, 5–23. of the eastern Anti-Atlas (Morocco). Geology, 13, Termier, G. & Termier, H. 1950. Paléontologie 815–818. Marocaine. II. Invertébrés de I’ère Primaire. Wendt, J. 1988. Facies pattern and palaeogeography Fascicule III. Mollusques. Service géologique, of the Middle and Late Devonian in the eastern Protectorat de la République française au Maroc, Anti-Atlas (Morocco). In: Mc Millan, N.J., Embry, Notes et Mémoires, 78, 1246. A.F. & Glass, D.J. (Eds), Devonian of the World, Tessitore, L., Schemm-Gregory, M., Korn, D., Wild, I. Canadian Society of Petroleum Geologists, 467– F.R.W.P., Naglik, C. & Klug, C. 2013. Taphonomy 480. and palaeoecology of the green pentamerid Wendt, J. Aigner, T. & Neugebauer, J. 1984. Cephalopod brachiopods from the Devonian of Aferdou el limestone deposition on a shallow pelagic ridge: the Mrakib, eastern Anti-Atlas, Morocco. Swiss Journal Tafi lalt-platform (Upper Devonian, eastern Anti- of Palaeontology, 132 (1), 23–44. Atlas, Morocco). Sedimentology, 31, 601-625. Tessitore, L., Naglik, C., De Baets, K., Galfetti, T. & Wendt, J. & Belka, Z. 1991. Age and depositional Klug, C. 2016. Neptunian dykes in the Devonian environment of Upper Devonian (early Frasnian carbonate buildup Aferdou El Mrakib (eastern Anti- to early Famennian) black shales and limestones Atlas, Morocco) and implications for its origin. (Kellwasser facies) in the eastern Anti-Atlas, Neues Jahrbuch für Geologie und Paläontologie, Morocco. Facies, 25, 51–90. Abhandlungen, 281, 247-266. Wenk, R. 1967. Baryt und Ankerit aus Ammoniten Van Roy, P., Orr, P.J., Botting, J.P., Muir, L.A., Vinther, des Berner Juras (Schweiz). Contributions to J., Lefebvre, B., el Hariri, K. & Briggs, D.E.G. Mineralogy and Petrology, 14(2), 81–85. 2010. Ordovician faunas of Burgess Shale type. Wilby, P. R., Duff, K., Page, K. & Martin, S. (2008). Nature, 465, 215–218. Preserving the unpreservable: a lost world Webster, G.D., Becker, R.T. & Maples, C.G. 2005. rediscovered at Christian Malford, UK”, Geology Biostratigraphy, paleoecology, and taxonomy of Today 24.3: 95-98.

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Appendix I

Tab. 4. Tübingen questionnaires Fossil-Lagerstätten (after Seilacher et al. 1985).

88 CHAPTER III

Morphology, phylogenetic relationships and ecomorphology of the early elasmobranch Phoebodus

Linda Frey, Michael Coates, Michal Ginter, Vachik Hairapetian, Martin Rücklin und Christian Klug

In preparation, formatted for Proceedings B

Chapter III: Phoebodontid Chondrichthyans of the Maider

Morphology, phylogenetic relationships and ecomorphology of the early elasmobranch Phoebodus

Linda Frey1, Michael Coates2, Michał Ginter3, Vachik Hairapetian4, Martin Rücklin5, Iwan Jerjen6 and Christian Klug1

1Paläontologisches Institut und Museum, University of Zurich, Karl-Schmid-Strasse 4, CH-8006 Zürich ([email protected]; [email protected]) 2Department of Organismal Biology and Anatomy, University of Chicago, 1027 E. 57th St., USA-60637 Chicago 3Faculty of Geology, University of Warsaw, al. Żwirki i Wigury 93, PL-02-089 Warszawa 4Department of Geology, Khorasgan Branch, Islamic Azad University, PO Box 81595-158, Esfahan, Iran 5Naturalis Biodiversity Center, Postbus 9517, 2300 RA, Leiden, The Netherlands 6Institute for Biomedical Engineering, ETH Zürich, Gloriastrasse 35, CH- 8092 Zürich

Although the anatomical knowledge of early chondrichthyans and thus their phylogeny is constantly im- proving, some taxa are still known only by microremains. Assumptions about the ecomorphology of the nearly cosmopolitan and regionally abundant Devonian chondrichthyan genus Phoebodus and the phy- logenetic relations to other phoebodontids were solely based on teeth and fi n spines. Here, we report the fi rst body remains and braincases of Phoebodus from the Famennian (Late Devonian) of the Maïder re- gion of Morocco. Phoebodus differs from other phoebodontids such as Thrinacodus in following features: an anguilliform but less slender body, a short otic process on the palatoquadrate, a derived shape of the ceratohyals and the presence of two dorsal fi n spines. Our phylogenetic analyses confi rm phoebodontids (Phoebodus and Thrinacodus) as stem elasmobranchs (crown Chondrichthyes). Phoebodontids form a polytomy together with Cladodoides, Tamiobatis, xenacanthids and hybodontids. They represent the earli- est anguilliform chondrichthyans in the fossil record and therefore underline the Devonian morphological disparity and ecological diversity of early gnathostomes.

Keywords: Gnathostomes, Chondrichthyes, neurocranium, homoplasy, Devonian, Morocco

1. Introduction teeth (and tentatively, isolated fi n spines [Maisey in 18]) were recovered from numerous localities During the last decades, new records of ear- of Middle Devonian to Early Carboniferous age ly chondrichthyans ameliorated our anatomical worldwide [18, 21-29]. knowledge of these jawed fi sh[1-15]. Although occasionally, articulated and complete skeletons Based on their abundant teeth, evolution- of Palaeozoic chondrichthyans were discovered, ary scenarios of members of the Phoebodontidae some groups of early chondrichthyans are still were postulated from symmetric teeth with broad exclusively known from microremains or mac- bases (Ph. fastigatus [23], Ph. latus [24], Ph. bi- roscopic isolated hard parts such as teeth and fi n furcatus [23]) of Frasnian and earliest Famennian spines [16-18]. Accordingly, the skeletal anatomy age to asymmetric tricuspid teeth with narrow of phoebodontids was entirely unknown until the bases of late Famennian age (Thrinacodus tran- discovery and description of Thrinacodus gra- quillus [30], Th. ferox [31]) [18]. The early/ mid- cia [19] from the Serpukhovian locality of Bear dle Famennian Phoebodus gothicus transitans Gulch, Montana. Thrinacodus gracia shows a already displays some asymmetry in base and highly derived body plan compared to other early crown and therefore, this species was inferred to chondrichthyans in having an extremely slender represent a phylogenetic link between Phoebodus and elongate body as well as asymmetric tricus- and Thrinacodus [26]. pid teeth with a recurved crown [19-20]. Howev- er, complete crania or other skeletal remains of Here, we describe one nearly complete skel- the common phoebodontid Phoebodus were un- eton and several three-dimensionally preserved known, even though their characteristic tricuspid skulls of Phoebodus that were discovered in the

91 Chapter III: Phoebodontid Chondrichthyans of the Maider middle Famennian of the Maïder Basin of Moroc- (c) Phylogenetic analyses co. We discuss the morphological similarities to the phoebodontid Thrinacodus gracia and its phy- Our phylogenetic data matrix is based on those logeny as well as ecology. We also discuss which of Coates et al. [5] and Brazeau [36]. Data on ac- impact the new morphological data of Phoebodus anthodian stem chondrichthyans are from Davis has on the ecomorphological diversity of Devoni- et al. [37] and Burrow et al. [38] while Zhu et al. an chondrichthyans. [39] and Qiao et al. [40] provide data from the out- group. We updated the character matrix by adding character 58 (ceratohyal anteriorly blade-shaped) and by excluding 35 uninformative characters, 2. Material and methods which is the result of the adapted taxa list (22 taxa of stem gnathostomes were excluded; see supple- a) Specimens mentary material: chapter 3). The updated data matrix contains now 228 characters, 65 in-group The material includes visceral and postcranial re- taxa (including Phoebodus and Thrinacodus) and mains of a skeleton of Phoebodus saidselachus sp. one out-group taxon (Entelognathus). Phyloge- nov. (PIMUZ A/I 4712) as well as four three-di- netic analyses were performed in TNT 1.5 (Tree mensionally preserved cranial remains (PIMUZ Analysis Using New Technology [41]) via heuris- A/I 4656, 4710, 4711, 4713) that are housed at tic parsimony analysis (traditional search in TNT) the Palaeontological Institute and Museum of the using 10000 multiple random addition sequences. University of Zurich, Switzerland. Over the last Swapping algorithm is tree bisection reconnection decades, the material was collected from Madene (TBR) with 10 trees saved per replication. For the El Mrakib, which is situated in the southern nodal support, we resampled the data using 1000 Maïder region of the eastern Anti-Atlas of Moroc- bootstrap replicants (standard bootstrap and tra- co (Fig. S1). The skeletal remains are preserved ditional search options in TNT 1.5) and we per- in ferruginous nodules of reddish colour found in formed Bremer support retaining trees suboptimal the Thylacocephalan Layer (formerly described by 5 steps (Fig. S9). as Phyllocarid Layer; [32]) in which thylacoceph- alan arthropods are highly abundant. Dating of the host rocks by index ammonoids (Maeneceras horizon) suggest an early to middle Famennian 3. Results age [33, 34]. a) Genus and species diagnosis and description

For some of the material (PIMUZA/I 4656, 4710, (b) Anatomy inferred from CT-data 4712), we introduce the species Phoebodus said- selachus sp. nov. because it combines characters Computed tomograms of the three-dimensionally of previously known microremains such as mul- preserved skulls were acquired using a Nikon XT ticuspid body scales (Fig. S8), ctenacanthid fi n H 225 ST industrial CT-scanner at the University spines (resembling Amelacanthus sp., Fig. S6; of Zurich, Switzerland. The braincase of PIMUZ [16]) and teeth intermediate between Phoebodus A/I 4711 preserving parts of the otic and occiput typicus [24] and Phoebodus politus [42]. Two yielded an image stack with good contrast be- specimens (PIMUZ A/I 4711, 4713) were deter- tween matrix and fossil. Data acquisition and im- mined as Phoebodus sp. because they preserve age reconstruction parameters: 221 kV, 349 mA; neither diagnostic teeth nor fi n spines. The new fi lter: 2 mm of copper; voxel sizes in mm: 0.0776 fossils yield important novel anatomical informa- in each direction; the data was exported as a raw tion about Phoebodus concerning body parts such volume. as the mandibular and branchial arches, shoulder The volume was manually segmented and girdle and neural arches (Fig. 1). Additionally, anatomical reconstructions were performed using computer tomographs revealed details of the otic the software Mimics v.17 (http://www.biomedi- and occipital regions of the braincase, endocast cal.materialise.com/mimics; Materialise, Leuven, and brachial arches (Fig. 2-3, S5). Using this ad- Belgium). Smoothing, colours and lighting were ditional anatomical data, we emend the genus di- edited in MeshLab v. 2016 (http://www.meshlab. agnosis of Phoebodus (previously based on teeth net; [35]) and blender v2.79b (https://www.blend- only). er.org; Amsterdam, Netherlands). The current genus defi nition of Phoebodus

92 Chapter III: Phoebodontid Chondrichthyans of the Maider

Figure 1. Phoebodus saidselachus sp. nov., (a – d) PIMUZ A/I 4712, (e) PIMUZA/I 4656. (a) ferruginous nodule containing cranial and postcranial remains; (b) drawing, scale bar = 200 mm; (c) detail of visceral skeleton, scale bar 100 mm; (d) tooth, scale bar = 5 mm (e) tooth in labial, aboral, baso-lateral and linguo-basal views, scale bar = 10 mm. adbc: anterior dorsal basal cartilage; bh, basihyal; cb, ceratobranchial; ch, ceratohyal; col, cololite; fs, fi n spine; mc, Meckel`s cartilage; mpt, metapterygium; n, neurocranium; na, neural arches; pdbc: posterior dorsal basal carti- lage; pq, palatoquadrate; rad, radials; sc, scapulacoracoid. based on teeth [18] is as follows: crown with three cartilage, jaws amphystylic with tooth fi les sep- long main cusps equally sized or median cusps arated by gaps, multicuspid trunk scales; pharyn- slightly shorter; sigmoid outline of main cusps; geal teeth present; otico-occipital fi ssure present, intermediate cusplets absent or present, if present two dorsal fi n spines with ctenacanthid ornamen- then short and thin; base is symmetric, extending tation; dorsal fi ns with calcifi ed base plate; high lingually, a single orolingual button on lingual to- supraoccipital crest; dorsal otic ridge forming rus for articulation with the overlying tooth, arcu- crests posteriorly; elongate endolymphatic fossa; ate basolabial projection; two openings for basal occipital arch deeply wedged between otic cap- canal: one aborally and one lingually. sule; massive hypotic lamina; external opening for endolymphatic ducts anterior to a crus com- With the new material of Phoebodus (notes mune; elongate and narrow body (eel-like shape) in electronic supplementary material), the follow- and mandibular arches; long occipital region, ap- ing characters are now added to the genus defi - proximately 75 % of the otic length; ceratohyal nition: Skeleton consisting of tesselate calcifi ed anteriorly blade-shaped; otic process of the pala-

93 Chapter III: Phoebodontid Chondrichthyans of the Maider

Figure 2. Otic and occipital region of Phoebodus saidselachus sp. nov., PIMUZ A/I 4711, reconstructed on the basis of CT-scans: (a) anterior; (b) ventral; (c) dorsal; (d) lateral; (e) posterior view. Braincase and articulated branchial arches: (f) ventral view of braincase and ceratohyals, (g) anterior aspect of ceratohyal, (h) lateral view of ceratohyal, (i) dorsolateral view on hyomandibula-braincase articulation. Scale bars = 30 mm. Abbreviations: chy, ceratohyal; dor, dorsal otic ridge; endf, endolymphatic foramen; esc, external semicircular canal; fm, foramen magnum; glc, glossopharyngeal canal; hl, hypotic lamina; hym, hyomandibula; lda, lateral dorsal aorta; lof, lateral otic fossa; nc, notochordal canal; oc cot, occipital condyle; occr, occipital crest; psc, posterior semicircular canal; sac, sacculum. toquadrate is dorsoventrally short. verify if only one or several tooth forms [e.g. 18, 26, 28-29] are present in the jaws. The homodonty The dentition of Phoebodus appears to be ho- has to be confi rmed with further fi ndings or higher modont. However, most teeth are broken and the resolved tomographies in the future. diagnostic tooth bases are usually poorly visible, hard to prepare or lack resolution in the CT-imag- ery (Fig. S2c, S3c, S7). Therefore, we could not

94 Chapter III: Phoebodontid Chondrichthyans of the Maider

Figure 3. Otic and occipital region of the endocast of Phoebodus saidselachus sp. nov., (PIMUZ A/I 4711): (a) dorsal, (b) ventral, (c) lateral, (d) anterior and (e) posterior views. Scale bar = 30 mm. Abbreviations: esc, external semicircu- lar canal; med, medulla; pa, posterior ampulla; psc, posterior semicircular canal; sac, sacculum; socc, spino-occipital. b) Phylogenetic analyses almost one order of magnitude higher in propor- tions. The dorsal fi ns as well as their fi n spines are Our phylogenetic analyses are based on a matrix completely reduced in Thrinacodus [19; Fig. 5]. with 228 characters, 65 ingroup taxa and one out- They also differ in the shape of their palatoquad- group taxon (Entelognathus), which resulted in rates; the quadrate region is higher in Thrinaco- 720 most parsimonious trees of 543 steps. The dus and offers a larger attachment surface for the strict consensus tree places Phoebodus and Thri- adductor muscles. In contrast to Thrinacodus, the nacodus on the elasmobranch branch of the chon- palatoquadrate as well as Meckel`s cartilage are drichthyan group (Fig. 4). Both taxa form part of elongated in Phoebodus. More differences be- a polytomy together with Cladodoides and the Ta- tween Thrinacodus and Phoebodus are present in miobatis-xenacanth (Diplodoselache, Triodus and their visceral skeletons. From Thrinacodus, hy- Orthacanthus) branch. pohyals and a simple rod-shaped ceratohyal was described by Grogan and Lund [19: Fig. 10C]. Remarkably, the branchial skeleton of Phoebodus 4. Discussion challenges previous interpretations of phoebodon- tid branchial anatomy: In Phoebodus, the derived (a) Phylogenetic relationships blade-shaped ceratohyal articulates anteriorly directly to the basihyal and hypohals are absent Based on dental characters, it is widely accepted (Fig. 1a, b, 2f-h). Due to the imperfect preserva- that thrinacodontids derived from phoebodontids tion in Phoebodus, pectoral, pelvic and caudal fi ns during the Famennian [e.g., 18, 26]. The skeletal cannot be compared adequately between the two material of Phoebodus described here corrobo- phoebodontids and thus hamper the discussion of rates the close phylogenetic relationship to Thr- differences in locomotion and manoeuvrability. inacodus. Both taxa are characterised by elon- gate body morphologies with long and slender Our phylogenetic analyses revealed that heads including elongated mandibles with teeth Phoebodus is a stem elasmobranch. In the clado- with three main cusps of similar size. However, gram (strict consenus tree in Fig. 4), this genus as already suggested by tooth morphology, Thr- is situated in a polytomy together with Clado- inacodus is indeed more derived in some cranial doides, Tamiobatis-xenacanthids branch and hy- and postcranial characters than Phoebodus. Thr- bodontids. Phoebodus, Tamiobatis, Orthacanthus inacodus has a lower body height; in Thrinaco- and Tristychius share characters in the braincase dus, the body is only 20 mm high (body height to such as the elongated endolymphatic fossa later- length ratio c. 0.02) while in Phoebodus it is 140 ally fl anked by prominent dorsal otic ridges [Fig. mm high (body height to length ratio c. 0.13), i.e. 2a-e; 6, 43, 44]. Moreover, a prominent supraoc- cipital crest is a common feature in Phoebodus,

95 Chapter III: Phoebodontid Chondrichthyans of the Maider values > 3. Holocephali (crown Chondrichthyes). White circles: bootstrap support of knot > 50% and/ or Bremer decay values 1; black circl group); green, Osteichthyes; red, Acanthodii (stem Chondrichthyes); orange, stem Chondrichthyes excluding Acanthodii; blue, Elasmobranchii (crown Chondrichthyes); purple, Figure 4. Entelognathus Youngolepis Guiyu Cladogram (strict consensus tree) showing the placement of Psarolepis Cheirolepis Mimipiscis Raynerius Moythomasia Culmacanthus Ischnacanthus Nerepisacanthus Poracanthodes Tetanopsyrus Uraniacanthus Diplacanthus Rhadinacanthus Cassidiceps Mesacanthus Promesacanthus Cheiracanthus Acanthodes Homalacanthus Halimacanthodes Gladbachus Brachyacanthus Brochoadmones Phoebodus Climatius Parexus Ptomacanthus V waynensis and Gyracanthides

Thrinacodus Latviacanthus Pucapampella Kathemacanthus Lupopsyrus Obtusacanthus

within the elasmobranchs. Colour coding: black, stem group gnathostome (out- Doliodus Acronemus Egertonodus Hamiltonichthys Onychoselache Tribodus Squalus Synechodus Tristychius Homalodontus Cladodoides

es: bootstrap support > 75% and/or Bremer decay Phoebodus Thrinacodus Diplodoselache Orthacanthus Triodus Tamiobatis Dwykaselachus Ozarcus Cladoselache Cobelodus Akmonistion Damocles Falcatus Debeerius Chimaeroidei Chondrenchelys Helodus Iniopera Kawichthys

96 Chapter III: Phoebodontid Chondrichthyans of the Maider

Tristychius, and xenacanthids [Fig. 2a, e; 6, 44]. ?occipital elements in fi g. 10C, 12C). The low otic In both Tristychius and Phoebodus, the dorsal and process on the palatoquadrate (Fig. 1c) separates occipital crests are arranged similarly relative to Phoebodus from all other early elasmobranchs. each other and the ceratohyal that anterolaterally expands forming a medially directed blade (Fig. The phylogenetic results corroborate the pro- 2g,h). However, the semicircular canals form a posed close relationship between phoebodontid crus commune unlike in Tristychius, which indi- and xenacanthid taxa based on tooth morphology cates that Phoebodus did not have any phonore- [18,45]. However, more morphological data of ception. Moreover, the arrangement of the semi- phoebodontids is necessary to get a better reso- circular canals and the massive hypotic lamina lution of the phylogenetic relationship between with two openings for the lateral aortae in com- these two groups. bination with the large diameter of the occipital condyle are characters shared with Cladodoides and Orthacanthus [9,44]. Compared to other ear- (b) Palaeoecology ly groups of elasmobranchs, phoebodontid elas- mobranchs have a very elongate occipital region The skeletal material of Phoebodus was found in (Phoebodus: Fig. 1B, S4; Thrinacodus: see [19]: the Maïder basin, which is a small epicontinental

Figure 5. Possible body reconstruction of (a) Phoebodus saidselachus sp. nov., Late Devonian, (b) Thrinacodus gracia (Grogan & Lund, 2008), Early Carboniferous, and (c) picture of Chlamydoselachus anguineus Garman, 1884, Recent.

97 Chapter III: Phoebodontid Chondrichthyans of the Maider marine basin at the southern margin of the Palae- behaviours [56, 57]. Because of the grasping den- otethys [46-50]. Rough estimation of the palae- tition of Phoebodus, they were unable to cut prey odepth of the Maïder basin suggested depths of and only prey much smaller than their own body maximally 400 meters in the depocentre and about (which they could swallow whole) is feasible. Ad- 100 to 300 m at Madene el Mrakib [51]. Teeth of ditionally, the morphology of the ceratohyal may Phoebodus were mainly found in localities where inform about feeding mechanisms. Similarly to moderately deep to moderately shallow water the ceratohyals of hybodontid Tristychius, those conditions prevailed during the Late Devonian; of Phoebodus are large and broad with a medial- this taxon was proposed to live in the middle parts ly directed anterior blade. Therefore, Phoebodus of the water column [18]. This coincides with the might have been a suction-feeder like hybodonts. environmental conditions of the Maïder basin, where hypoxic to dysoxic conditions occurred Stomach contents of phoebodontids were repeatedly at the sea fl oor during the Famennian only found in Thrinacodus so far and they include [32]; therefore, benthic life was rare and its diver- remains of small chondrichthyans (Falcatus falca- sity was correspondingly low in this region during tus [58], Harpagofututor volsellorhinus [59]) and much of the Famennian. crustaceans [19]. In recent frilled sharks, epipe- lagic squids, scyliorhinid and squaloid sharks [57, Among early chondrichthyans, phoebodon- 60] were reported as stomach content. Possible tids are the fi rst taxa with an anguilliform body. prey for Phoebodus could have been thylacoceph- Permian xenacanthid elasmobranchs also have a alan arthropods, which occur in great numbers in rather eel-like body but with several differences the host rocks of the Moroccan phoebodontids in anatomy [52-55]. Therefore, the discovery of [32]. skeletons of phoebodontids shows that the mor- phological disparity and ecological diversity of Devonian chondrichthyans was higher than pre- viously assumed. (c) Macroevolutionary implications

The anguilliform body of phoebodontids is Based on the identifi cation of phoebodontids as remarkably similar to that of the very distantly stem elasmobranchs, an important macroevolu- related modern neoselachian Chlamydoselachus. tionary trend is emphasized. Generally, the Han- The length-to-height proportion of the body rather genberg Crisis is interpreted as a phase of a major resembles Phoebodus, while dorsal fi n spines and turnover among vertebrates forming a bottleneck dorsal fi ns are absent as in Thrinacodus except for in their evolutionary history [61,62]. The pattern a small second dorsal fi n in Chlamydoselachus. for Actinopterygii indicates a low diversity and Because of these similarities in morphology and disparity in the Devonian followed by an increase the absence of calcifi ed vertebrae centrae, we sug- of morphological and taxonomic diversity after gest that undulation was the mode of locomotion the Hangenberg Event [63]. Our new data about in phoebodontids (likely representing the plesio- phoebodontids and thus the earliest anguiliform morphic state of stem elasmobranchs). chondrichthyans emphasizes the morphological and taxonomic diversity of stem elasmobranchs The quadrate region of the palatoquadrate of during the Devonian. Remains of phoebodontids both Phoebodus and Chlamydoselachus is dor- were reported from the Givetian (Middle Devo- soventrally only slightly higher than the palatine nian; [18, 23]), which shows that stem elasmo- ramus (Fig. 1a-c). Related to the function of the branchs were probably ecologically diverse long jaws, this implies that the surface for the attach- before the Hangenberg Event. This suggested ment of the adductor muscle is reduced and that disparate pattern for stem elasmobranchs and the bite was probably weaker than in other Palae- stem actinopterygians needs further analyses of ozoic (e.g., xenacanthids, symmoriids) and mod- the comparative anatomy of organ systems, their ern chondrichthyans. functional morphology and ecological interpreta- tion. Due to the similarities in body outline and tooth shape, Phoebodus probably pursued a feed- ing strategy comparable to chlamydoselachids al- though it is still unknown how the slow moving 4. Conclusions chlamydoselachids are capable of catching prey. The fi rst anatomical information of the very com- Ram-feeding or lurking in combination with sud- mon genus Phoebodus based on the new species denly snatching the prey are proposed feeding Ph. saidselachus sp. nov. in combination with the

98 Chapter III: Phoebodontid Chondrichthyans of the Maider knowledge of Thrinacodus gracia revealed that FischerVerlag. phoebodontids are anguiliform chondrichthyans. 2. Stahl BJ. 1999 Chondrichthyes III. In Holocephali. Our phylogenetic analyses show that phoebodon- Handbook of paleoichthyology 4 (ed. H-P Schult- tids are good candidates as the earliest stem elas- ze), 164 p. München, Verlag Dr. Friedrich Pfeil. mobranchs exhibiting elongate bodies. Including 3. Coates, M. I. and Sequeira, S. E. K. 2001. A new the fact that the oldest phoebodontid remains stethacanthid chondrichthyan from the Lower Car- are of Givetian age, this indicates that the root boniferous of Bearsden, Scotland. J. Vert. Paleon- of stem elasmobranch diversifi cation temporally tol. 21(3), 438-459. 4. Coates MI, Finarelli JA, Sansom IJ, Andreev PS, took place far back in the evolutionary history of Criswell KE, Tietjen K, Rivers ML, La Riviere PJ. chondrichthyans. 2018 An early chondrichthyan and the evolution- ary assembly of a shark body plan. Proc. R. Soc. Lond. Ser. B. Biol. Sci. 285: 20172418. (dx.doi. Author contributions: C.K, M. R., M.C and org/10.1098/rspb.2017.2418) L.F.: developing the project; C.K, M. R. and L.F: 5. Coates MI, Gess RW, Finarelli JA, Criswell KE, Tiet- fi eld work; I. J.: acquisition of computer tomogra- jen K. 2017 A symmoriiform chondrichthyan brain- case and the origin of chimaeroid fi shes. Nature, phy scans; M.G and V. H. determination of tooth 541(7636), 208. (doi.org/10.1038/nature20806) material; M.C. and L.F: interpretation of fossils 6. Coates MI, Tietjen K. 2018 The neurocranium of and 3D-models; phylogenetic analysis. L.F. illus- the Lower Carboniferous shark Tristychius arcua- trations, anatomical reconstruction, drafting man- tus (Agassiz, 1837). Earth Environ. Sci. Trans. uscript. R. Soc. Edinb. 108(1), 19-35. (doi.org/10.1017/ S1755691018000130) Competing interests: The authors declare no 7. Maisey JG. 2001 A primitive chondrichthyan brain- competing interests. case from the middle Devonian of Bolivia. In Ma- jor events in early vertebrate evolution (ed. PE Ahl- Funding: The project (project number S-74602- berg), pp. 263-288. London, UK: Taylor & Francis. 11-01) was fi nancially supported by the Swiss Na- 8. Maisey JG, Anderson ME. 2001 A primitive chon- tional Fond. . M.R. was supported by NWO (VIDI drichthyan braincase from the Early Devonian of 864.14.009). South Africa. J. Vert. Paleontol. 21, 702-713. (doi. org/10.1671/0272-4634(2001)021[0702:APCB- Data accessibility: In preparation. FT]2.0.CO;2) 9. Maisey JG. 2005 Braincase of the Upper Devonian shark Cladodoides wildungensis (Chondrichthyes, Acknowledgments: We greatly appreciate the Elasmobranchii), with observations on the brain- help of Saïd Oukherbouch (Tafraoute, Morocco) case in early chondrichthyans. Bull. Am. Mus. Nat. who supported us during fi eld work and discov- Hist. 288, 1-103. (doi:10.1206/0003-0090(2005)28 8<0001:BOTUDS>2.0.CO;2) ered some of the main specimens. We acknowl- 10. Maisey JG. 2007 The braincase in Paleo- edge Ben Pabst (Aathal) and Christina Brühwiler zoic symmoriiform and cladoselachian (University of Zurich) for their excellent prepara- sharks. Bull. Am. Mus. Nat. Hist. 307, 1-122. tion work. Moreover, we thank Anita Schweizer (doi:10.1206/0003-0090(2007)307[1:TBIPSA]2.0. (Zurich), Alexandra Wegmann (University of Zu- CO;2) rich) for the acquisition of CT-scans. Many thanks 11. Maisey JG, Miller R, Turner S. 2009 The braincase to Thodoris Argyriou (University of Zurich), To- of the chondrichthyan Doliodus from the Lower bias Reich (University of Zurich) and Amane Ta- Devonian Campbellton Formation of New Bruns- jika (NHM of New York) for CT-scanning and wick, Canada. Acta Zool.-Stockholm Suppl. 90, help with segmentation. Gabriel Aguirre kindly 109-122. (doi:10.111/j.1463-6395.2008.00330.x) helped with the phylogenetic analyses. We thank 12. Janvier P, Maisey JG. 2010 The Devonian verte- René Kindlimann (Aathal) for the very fruitful brates of South America and their biogeographical discussions and inputs. relationships. In Morphology, phylogeny and pale- obiogeography of fossil fi shes (eds DK Elliot, JG Maisey, X Yu, D Miao), pp. 431-459. München, Verlag, Dr. Freidrich Pfeil. 5. References 13. Pradel A. 2010 Skull and brain anatomy of Late Carboniferous Sibyrhynchidae (Chondrichthy- 1. Zangerl R. 1981 Chondrichthyes I. In Paleozoic es, Iniopterygia) from Kansas and Oklahoma Elasmobranchii. Handbook of paleoichthyology (USA). Geodiversitas 32, 595–566. (doi:10.5252/ 3A (ed. H-P Schultze), 115 p. New York, Gustave g2010n4a2)

99 Chapter III: Phoebodontid Chondrichthyans of the Maider

14. Pradel A, Tafforeau P, Maisey JG, Janvier P. 2011 Polon. 60(3), 357-371. A new Paleozoic Symmoriiformes (Chondrichthy- 30. Ginter M. 2000 Late Famennian pelagic shark as- es) from the Late Carboniferous of Kansas (USA) semblages. Acta Geol. Polon. 50(2), 369-386. and Cladistic Analysis of Early Chondrichthyans. 31. Turner S. 1982 Middle Palaeozoic elasmobranch PLoS ONE 6, e24938. (doi:10.1371/journal. remains from Australia. J. Vert. Paleontol. 2, 117- pone.0024938) 131. 15. Pradel A, Maisey JG, Tafforeau P, Mapes RH, 32. Frey L, Rücklin M, Korn D, Klug C. 2018 Late Mallatt JA. 2014 A Palaeozoic shark with osteich- Devonian and Early Carboniferous alpha diversity, thyan-like branchial arches. Nature 509, 608-611. ecospace occupation, vertebrate assemblages and (doi:10.1038/nature13195) bio-events of southeastern Morocco. Palaeogeogr. 16. Maisey JG. 1982 Studies on the Paleozoic selachian Palaeoclimatol. Palaeoecol. 496, 1-17. genus Ctenacanthus Agassiz. No. 2, Bythiacanthus 33. Becker RT, House M R, Bockwinkel J, Ebbighau- St. John and Worthen, Amelacanthus, new genus, sen V, Aboussalam ZS. 2002 Famennian ammonoid Eunemacanthus St. John and Worthen, Sphenacan- zones of the eastern Anti-Atlas (southern Moroc- thus Agassiz, and Wodnika Münster. Am. Mus. No- co). Münster. Forsch. Geol. Paläont. 93, 159-205. vit. 2722. 34. Korn D, Klug C. 2002 Fossilium Catalogus I: An- 17. Maisey JG. 1984 Studies on the Paleozoic sela- imalia Pars 138, Ammoneae Devonicae. Leiden, chian genus Ctenacanthus Agassiz. No. 3, Nominal Netherlands, Backhuys Publishers. species referred to Ctenacanthus. Am. Mus. Novit. 35. Cignoni P, Callieri M, Corsini M, Dellepiane 2774. M, Ganovelli F, Ranzuglia G. 2008 MeshLab: an 18. Ginter M, Hampe O, Duffi n, C J. 2010 Chondrich- Open-Source Mesh Processing Tool. Sixth Euro- thyes: Paleozoic Elasmobranchii: teeth. In Hand- graphics Italian Chapter Conference, 129-136. book of paleoichthyology, 3D (ed. H-P Schultze), 36. Brazeau MD. 2009 The braincase and jaws of a 168 p. Devonian acanthodian and modern gnathostome 19. Grogan ED, Lund R. 2008 A basal elasmobranch, origins. Nature 457, 305-308. (doi: 10.1038/na- Thrinacoselache gracia n. gen & sp., (Thrinaco- ture07436) dontidae, new family) from the Bear Gulch Lime- 37. Davis SP, Finarelli JA, Coates MI. 2012. Acanth- stone, Serpukhovian of Montana, USA. J. Vert. Pa- odes and shark-like conditions in the last common leontol. 28(4), 970-988. ancestor of modern gnathostomes. Nature 486, 20. Ginter M, Turner S. 2010 The middle Paleozoic Se- 247-250. (doi:10.1038/nature11080) lachian genus Thrinacodus. Journal of Vertebrate 38. Burrow CJ, den Blaauwen J, Newman M, David- Paleontology 30(6), 1666–1672, DOI:10.1080/027 son R. 2016 The diplacanthid fi shes (Acanthodii, 24634.2010.520785. Diplacanthiformes, Diplacanthidae) from the Mid- 21. Long J A. 1990 Late Devonian chondrichthyans dle Devonian of Scotland. Palaeontol. Electron. and other microvertebrate remains from northern 19, 1-83. Thailand. J. Vert. Paleontol. 10, 59-71. 39. Zhu M, Yu X, Ahlberg PE, Choo B, Lu J, Qiao QL, 22. Ginter M. 1990 Late Famennian shark teeth from Zhao J, Blom H, Zhu Y. 2013 A Silurian placoderm the Holy Cross Mts, Central Poland. Acta Geol. Po- with osteichthyan-like marginal jaw bones. Nature lon. 40, 69-81. 502, 188-193. (doi:10.1038/nature12617) 23. Ginter M, Ivanov A. 1992 Devonian phoebodont 40. Qiao T, King B, Long JA, Ahlberg PE, Zhu M. shark teeth. Acta Geol. Polon. 37(1), 55-75. 2016 Early gnathostome phylogeny revisited: mul- 24. Ginter M, Ivanov A. 1995 Middle/Late Devonian tiple method consensus. PLoS ONE 11, e0163157. Phoebodont-based ichthyolith zonation. [Zonation (doi:10.1371/journal.pone.0163157) ichthyologique du Dévonien moyen/supérieur fon- 41. Goloboff PA, Catalano SA. 2016 TNT version 1.5, dée sur les Phoebodontes]. Geobios 19, 351-355. including a full implementation of phylogenetic 25. Ivanov A. 1995 Late Devonian vertebrate fauna of morphometrics. Cladistics 32, 221-238. the South Urals. Geobios, 28, 357-359. 42. Newberry JS. 1889 The Paleozoic fi shes of North 26. Ginter M, Hairapetian V, Klug C. 2002 Famennian America, Monograph of the U.S. Geological Sur- chondrichthyans from the shelves of North Gond- vey 16, 1-340. wana. Acta Geol. Polon. 52 (2), 169-215. 43. Williams ME. 1998 A new specimen of Tamiobatis 27. Ginter M, Turner S. 1999 The early Famennian re- vetustus (Chondrichthyes, Ctenacanthoidea) from covery of phoebodont sharks. Acta Geol. Polon., the Late Devonian Cleveland Shale of Ohio. J. Vert. 49(2), 105-117. Paleontol. 18(2), 251-260. 28. Hairapetian V, Ginter M. 2009 Famennian chon- 44. Schaeffer B. 1981 The xenacanths shark neurocra- drichthyan remains from the Chahriseh section, nium, with comments on elasmobranch monophy- central Iran. Acta Geol. Polon. 59(2), 173-200. ly. Bull. Am. Mus. Nat. Hist.169, 1-66. 29. Hairapetian V, Ginter M. 2010 Pelagic chondrich- 45. Ginter M. 2004 Devonian sharks and the origin of thyan microremains from the Upper Devonian of Xenacanthiformes. In Recent advances in the ori- the Kale Sardar section, eastern Iran. Acta Geol. gin and early radiation of vertebrates (eds. G Ar-

100 Chapter III: Phoebodontid Chondrichthyans of the Maider

ratia, MVH Wilson, R Cloutier). p. 473-486. Mün- 55. Heidtke UHJ, Schwind C, Krätschmer K. 2004 chen, Friedrich Pfeil. Über die Organisation des Skelettes und die ver- 46. Wendt J. 1985 Disintegration of the continental wandschaftlichen Beziehungen der Gattung Trio- margin of northwestern Gondwana: Late Devonian dus Jordan 1849 (Elasmobranchii: Xenacanthida). of the eastern Anti-Atlas (Morocco). Geology 13, Mainzer geowiss. Mitt. 32, 9-54. 815-818. 56. Smith BG. 1937 The Anatomy of the Frilled Shark, 47. Wendt J.1995 Shell directions as a tool in palae- Chlamydoselachus anguineus Garman. Bashford ocurrent analysis. Sediment. Geol. 95, 161-186. Dean Memorial Volume: Archaic Fishes Article 6, 48. Wendt J, Kaufmann B, Belka Z, Klug C, Lubeseder 333-506. American Museum of Natural History, S. 2006 Sedimentary evolution of a Palaeozoic ba- N.Y. sin and ridge system: the Middle and Upper Devo- 57. Ebert DA, Compagno LJV. 2009 Chlamydosela- nian of the Ahnet and Mouydir (Algerian Sahara). chus africana, a new species of frilled shark from Geol. Mag. 143(3), 269-299. southern Africa (Chondrichthyes, Hexanchiformes, 49. Fröhlich S. 2004 Evolution of a Devonian carbon- Chlamydoselachidae). Zootaxa 2173, 1-18. ate shelf at the northern margin of Gondwana (Jebel 58. Lund R. 1985 The morphology of Falcatus falcatus Rheris,eastern Anti-Atlas, Morocco). Unpublished St. John & Worthen, a Mississippian stethacanthid PhD Thesis, University of Tübingen, Germany. chondrichthyan from the Bear Gulch Limestone of 50. Lubeseder S, Rath J, Rücklin M, Messbacher R. Montana. J. Vert. Paleontol. 5, 1-19. 2010 Controls on Devonian hemi-pelagic lime- 59. Lund R. 1982 Harpagofututor volsellorhinus new stone deposition analyzed on cephalopod ridge to genus and species (Chondrichthyes, Chondrenche- slope sections, Eastern Anti-Atlas, Morocco. Fa- lyiformes) from the Namurian Bear Gulch Lime- cies 56, 295-315. stone, Chondrenchelys problematica Traquair 51. Tessitore L, Naglik C, De Baets K, Galfetti T, and (Visean), and their sexual dimorphism. J. Vert. Pa- Klug C. 2016 Neptunian dykes in the Devonian leontol. 56, 938-958. carbonate buildup Aferdou El Mrakib (eastern An- 60. Kubota T, Shiobara Y, Kubodera, T. 1991 Food ti-Atlas, Morocco) and implications for its growth. habits of the Frilled Shark Chlamydoselachus an- Neues Jahrb. Geol. Paläontol. Abhl. 281(3), 247- guineus Collected from Suruga Bay, Central Japan. 266. Nippon Suisan Gakk. 57(1), 15-20. 52. Heidtke UHJ. 1982 Der Xenacanthide Orthacant- 61. Sallan LC, Coates MI. 2010 End Devonian ex- hus senckenbergianus aus dem pfälzischen Rotlie- tinction and a bottleneck in the early evolution of genden (Unter-Perm). Pollichia 70, 65-86. modern jawed vertebrates. Proc. Natl. Acad. Sci. 53. Heidtke UHJ. 1999 Orthacanthus (Lebachacant- 107(22), 1013110135. hus) senckenbergianus Fritsch 1889 (Xenacanthi- 62. Friedman M, Sallan LC. 2012 Five hundred mil- da: Chondrichthyes): revision, organisation und lion years of extinction and recovery: a Phanerozo- phylogenie. Freiberger Forschungsheft 481, 63- ic survey of large scale diversity patterns in fi shes. 106. Palaeontology, 55(4), 707-742. 54. Heidtke UHJ, Schwind C. 2004 Über die Organisa- 63. Giles S, Xu GH, Near- TJ, Friedman M. 2017 Early tion des Skelettes der Gattung Xenacanthus (Elas- members of ‘living fossil’lineage imply later origin mobranchii: Xenacanthida) aus dem Unterperm of modern ray-fi nned fi shes. Nature, 549(7671), des südwestdeutschen Saar-Nahe-Beckens. Neues 265. Jahrb. Geol. Paläontol. Abhl. 231(1), 85-117.

101 Chapter III: Phoebodontid Chondrichthyans of the Maider

SUPPLEMENTARY FIGURES

Fig. S1. Geological map of the southeastern Anti-Atlas of Morocco. The Thylacocephalan Layer with gnathostomes crops out in the Maïder region. Remains of Phoebodus were collected from the Famennian (Late Devonian) of Madene (30°44`407`` N, 4°42`899``W; 30°47`188`` N, 004°40`965`` W).

102 Chapter III: Phoebodontid Chondrichthyans of the Maider

Fig. S2. Phoebodus saidselachus sp. nov. (PIMUZ A/I 4659), neurocranium and jaw fragments with mandibular teeth. (a) dorsal and (b) lateral aspects, scale bar = 100 mm. (c) ventral aspect of the anterior part of the snout and jaws with exposed tooth families, scale bar = 50 mm. j. frag, jaw fragments; n, neurocranium; pq, palatoquadrate; ros, rostrum; t, teeth.

103 Chapter III: Phoebodontid Chondrichthyans of the Maider

Fig. S3. Phoebodus saidselachus sp. nov. (PIMUZ A/I 4710), Meckel`s cartilages (mc) with intact anterior tooth whorls in situ (t). (a) ventral view, scale bar =100 mm. (b) detail and (c) drawing of the at least six most anterior tooth families of the right ramus of the lower jaw, scale bar = 10 mm. mc, Meckel`s cartilage; t, teeth.

Fig. S4. Braincase of Phoebodus sp. (PIMUZ A/I 4713). (a) Weathered specimen and (b) illustration in dorsal view; scale bar = 100 mm. asc, anterior semicircular canal; end.d, endolymphatic ducts; end.f, endolymphatic fossa; into, interorbital space; occ, occipital cotylus; psc, posterior semicircular canal; pop, postorbital process; soc, spino-oc- cipital canal.

104 Chapter III: Phoebodontid Chondrichthyans of the Maider

Fig. S5. Reconstructed braincase, mandibular and visceral arches of Phoebodus sp. (PIMUZ A/I 4711): (a) anterior, (b) posterior, (c) lateral, (e) dorsal and (f) ventral view. Colour coding: grey, braincase; orange, ceratohyal; blue, hy- omandibulare; turquoise, palatoquadrate; yellow, Meckel`s cartilage; light blue, fragments of ?epibranchials; purple, branchial elements; red, ?ceratobranchial; green, part of ?palatoquadrate.

105 Chapter III: Phoebodontid Chondrichthyans of the Maider

Fig. S6. Phoebodus saidselachus sp. nov. (PIMUZ A/I 4712), dorsal fi n spines. Lateral view of (a) anterior and (b) posterior dorsal fi n spines, scale bar = 50 mm. (c) detail showing ctenacanthid ornamentation, scale bar = 10 mm.

106 Chapter III: Phoebodontid Chondrichthyans of the Maider

Fig. S7. Phoebodus saidselachus sp. nov. (PIMUZ A/I 4712), mandibular teeth. Photo of the dentition with explana- tory drawing (a); scale bar = 10 mm. (b - e) detail of the dentition, photo with explanatory drawing, (b,c) oral views of teeth, (d) teeth in aborolateral view, (e) lateral cross-section of teeth in a row. Scale bars in (b-e) = 5 mm.

107 Chapter III: Phoebodontid Chondrichthyans of the Maider

Fig. S8. Scales in the cranial region of Phoebodus sp. (PIMUZ A/I 4713). Scale bar = 5 mm.

108 Chapter III: Phoebodontid Chondrichthyans of the Maider

Entelognathus Youngolepis 2 Guiyu 4/83 Psarolepis 4/75 Cheirolepis 60 Mimipiscis 3/73 Raynerius 5/98 Moythomasia Culmacanthus 5/100 Ischnacanthus Nerepisacanthus Poracanthodes Tetanopsyrus Uraniacanthus 5/79 Diplacanthus 4/57 Rhadinacanthus Cassidiceps Mesacanthus 4 Promesacanthus Cheiracanthus Acanthodes 2 50 Homalacanthus Halimacanthodes Gladbachus Brachyacanthus Brochoadmones Climatius Parexus Ptomacanthus

V waynensis c knots. Bremer scores: 3, good support; 5, highly supported. Boostrap values: fi Gyracanthides Latviacanthus Pucapampella Kathemacanthus Lupopsyrus Obtusacanthus Doliodus Acronemus Egertonodus Hamiltonichthys 4 Onychoselache Tribodus Squalus 3 3 Synechodus Tristychius Homalodontus 5 Cladodoides Phoebodus Thrinacodus Diplodoselache 2 Orthacanthus 5/76 Triodus Tamiobatis 5 Dwykaselachus Ozarcus Cladoselache 3 Cobelodus Akmonistion Damocles Falcatus 5?/51 Debeerius 4 Chimaeroidei Chondrenchelys Strict consensus tree including values of Bremer`s decay and bootstrap support at speci 3/53 Helodus Iniopera 2 Kawichthys Fig. S9. more than 50: weak support, more than 75; good support; 100: highest support. Colour coding: black, stem group gnathtostome (outgroup); green, Osteichthyes; red, Acanthodii green, Osteichthyes; red, more than 50: weak support, 75; good support; 100: highest support. Colour coding: black, stem group gnathtostome (outgroup); (crown Chondrichthyes). Acanthodii; blue, Elasmobranchii (crown Chondrichthyes); purple, Holocephali (stem Chondrichthyes); orange, stem Chondrichthyes excluding

109 Chapter III: Phoebodontid chondrichthyans of the Maider

SUPPLEMENTARY NOTES 1) Devonian gnathostomes of Morocco

Morocco is famous for its often highly fossiliferous Devonian outcrops, which bear sometimes abundant invertebrates but also, somewhat rarer, inarticulated as well as articulated remains of vertebrates. Concern- ing vertebrates, macro- and microremains of placoderms and sarcopterygians are locally abundant in some strata and they were repeatedly reported from the Tafi lalt and Maïder regions of the southeastern Anti-Atlas (Lehmann 1956, 1964, 1976, 1977, 1978; Lelièvre & Janvier 1986, 1988; Lelièvre et al. 1993; Rücklin 2010, 2011; Rücklin et al. 2015, Rücklin & Clément 2017). Many taxa of Devonian chondrichthyans (e.g. Jalodus, Thrinacodus, Phoebodus, Ctenacanthus, Stethacanthus, Symmorium, Cobelodus, Denaea, Oro- dus, Protacrodus, Siamodus, Clairina) are documented by abundant isolated teeth and fi n spines, while cartilaginous structures such as a jaw were documented only once thus far (Lehman 1976; Derycke, 1992; Hampe et al. 2004; Derycke et al. 2008; Ginter et al. 2002; Derycke 2017). Only recently, more or less complete skeletons and braincases of chondrichthyans were found in the southern Maïder Basin (Fig. S1). The skeletal remains are preserved in ferruginous clayey nodules of reddish color found in the early/ mid- dle Famennian Thylacocephalan Layer in which thylacocephalans are highly abundant (Frey et al. 2018). Phoebodus is accompanied by numerous haematitic internal molds of cephalopods and phosphatised thyla- cocephalan as well as a few benthic invertebrates (Buchiola, Guerichia, ostracods and brachiopods). Con- cerning other gnathostomes, several species of well-preserved placoderms, sarcopterygians and cladodont chondrichthyans were found in and above the Thylacocephalan Layer. The palaeoenvironment at Madene el Mrakib was, during much of the Famennian stage, characterized by well-oxagenated waters in much of the water column while deeper water levels near the sea fl oor were oxygen-depleted, as inferred from the scarcity and low diversity of benthic invertebrates and the absence of bottom dwelling vertebrates (Frey et al. 2018). Taxa of invertebrates and vertebrates inhabiting higher water levels were more common and diverse, thus suggesting a better oxygenated water column.

2) Systematic Paleontology and specimen description

Class Chondrichthyes Huxley, 1880B

Subclass Elasmobranchii Bonaparte, 1838B

Family Phoebodontidae Williams in Zangerl, 1981

Included genera – Phoebodus St. John & Worthen, 1875A; Thrinacodus St. John & Worthen, 1875A; tentatively Diademodus Harris, 1951.

Family defi nition – Multicuspid teeth; three long main cusps intercalated by two small intermediate cus- plets; main cusps are sigmoidal; modestly ornamented cusps showing subparallel cristae; basis with lingual torus containing a single button for articulation; arcuate basolabial projection.

Remarks – The family Phoebodontidae includes the genera Diademodus, Phoebodus and Thrinacodus. While Phoebodus was only known from teeth for a long time, skeletal remains of Diademodus hydei Harris, 1951were found in the Devonian Cleveland Shales of Ohio, USA and complete skeletons of Thri- nacodus gracia (Grogan & Lund, 2008) were described from the Carboniferous of Bear Gulch, Montana. However, the inclusion of Diademodus in the Phoebodontidae is arguable as its teeth show multiple small cusps in contrast to the three large main cusps in Phoebodus (Ginter et al. 2010). Thrinacodus was as- signed to the family Thrinacodontidae by Grogan & Lund (2008) due to differences in tooth and base shape compared to Phoebodus. However, the differences are too weak to keep Thrinacodus in a separate family and therefore, it was suggested to place Thrinacodus together with Phoebodus within the Phoebodontidae (Long 1990; Ginter & Turner 2010).

110 Chapter III: Phoebodontid chondrichthyans of the Maider

Genus Phoebodus St. John & Worthen, 1875A

Type species – Bathycheilodus macisaacsi St. John & Worthen, 1875A, later named Phoebodus macisaa- csi Wells, 1944C and fi nally Phoebodus sophiae Ginter et al., 2010.

Stratigraphical and geographical distribution– Givetian to Famennian; nearly cosmopolitan.

Diagnosis – emended genus diagnosis, see main article.

Phoebodus saidselachus sp. nov.

Holotype – PIMUZ A/I 4712

Stratigraphic and geographic occurrences – early to middle Famennian of the Madene (30°44`407`` N, 4°42`899``W) and Aguelmous, Maïder region, Anti-Atlas, Morocco.

Material – One nodule with cranial and postcranial material (PIMUZ A/I 4712) and two braincases (PIMUZA/I 4656, PIMUZ A/I 4710).

Derivation of name – After Said Oukherbouch (Tafraoute), the fi rst name of our Moroccan collaborator in .(means ‘happy’), and the Latin word selachus (shark ﺩﻱﻉﺱ the fi eld (the Arabic word

1. Specimen PIMUZA/I 4656 and PIMUZ A/I 4710

Mandibular dentition and tooth morphology – Several mandibular tooth fi les are exposed in specimen PIMUZ A/I 4656 and PIMUZ A/I 4710 (Fig. S2c; S3b-c). The teeth are weathered, very soft and encrusted by a hard ferruginous layer. Removing these crusts by preparation results in destruction of the fossil ma- terial with its structure. Therefore, very little of the fi ner morphological details is visible. PIMUZ A/I 4656 bears six, probably seven tooth fi les separated by gaps in the anterior parts of the upper jaws and in PIMUZ A/I 4710, six tooth fi les are countable in the anterior region of the lower jaws.

Tooth fi les 1 to 3 of the upper left and fi les 1 to 2 of the upper right jaw in PIMUZ A/I 4656 contain three teeth, which are exposed from mostly labial and orolabial aspects (Fig. S2c). In PIMUZ A/I 4710, between two and six teeth are countable within the tooth fi les and several views are exposed (1A-D: labial; 2B: aborolabial; 3A-B: lingual; 4A-F: aboral and orolateral; 5A-C:?; 6A-B: oral and labial; Fig. S3b,c). PIMUZ A/I 4656 shows a single tooth that is well-preserved and which is exposed from labial, lateral and oral sides (Fig. S2c: tooth 4A; Fig. 1e). Labially, there is a large median cusp and two large lateral cusps of nearly identical length, but the lateral cusps appear to be more massive and broader in diameter than the median cusp (Fig. 1e). All main cusps are lingually recurved and show a sigmoid outline in lateral view. Between the large central and lateral cusps, there are two minute intermediate cusplets reaching maximally half of the length and thickness of the central cusp. Each main cusp shows an ornamentation consisting of two distinct striae forming rather sharp edges. The tooth base is squarish with rounded angles in ab- oral view and is 5.2 mm wide and 4.5 mm long. From labial, aboral and lateral aspects, the base shows a concave outline. The basolabial projection is wider than the median cusp and consists of a labiolingually narrow and slightly arcuate prominence. A large aboral foramen of the main basal canal lays lingually to the basolabial projection. In PIMUZ A/I 4710, a single tooth (Fig. S3b-c, 2b) with a well-preserved base of the same morphology is present, which shows that the two specimens are conspecifi c.

The dentition of Phoebodus saidselachus sp. nov. is homodont when size and shape of all preserved teeth are compared among each other. Size appears to differ hardly among teeth of the same tooth fi le, but this might be a view biased by the insuffi cient preservation or exposure of only parts of each tooth whorl. Grogan & Lund (2008) reported a homodont dentition from Thrinacodus gracia, while Ginter & Turner (2010) described a minor heterodonty (teeth between lower and upper jaw and between anterior and poste- rior positions differ in size and symmetry) based on unarticulated teeth of Thrinacodus ferox.

111 Chapter III: Phoebodontid chondrichthyans of the Maider

Neurocranium and mandibular arches - Neurocranial and mandibular remains of Phoebodus saidse- lachus sp. nov. are three-dimensionally preserved but embedded in ferruginous rocks or covered by fer- ruginous crusts and therefore, anatomical details are hardly exposed. Internal structures of the braincase are recognizable in some cross-sections. Computer tomography scanning and neutron scanning resulted in image stacks of insuffi cient contrast because of hydroxyl-rich compounds in the host rocks. Thus, the morphology of the cranial region of the specimens is here described only superfi cially.

In PIMUZ A/I 4656, a ferruginous crust revealed the outline of the braincase, palatoquadrates and Meckel`s cartilages (the rock containing all these elements measures 0.33 m in length). In dorsal and ventral view, the skull becomes increasingly slender from posterior to anterior and anteriorly ends in a rounded and somewhat blunt snout that is much less pointed than in Thrinacodus gracia (Fig. S2a, c). The overall shape of the skull is elongated and slender compared to most Palaeozoic chondrichthyans but less slender than in the more derived phoebodont Thrinacodus gracia. Laterally, fragments of the long jaws are present that fl ank the entire specimen (Fig. S2b, c). In PIMUZ A/I 4710, parts of both Meckel`s cartilages are exposed and show no symphysial fusion anteriorly, which is the common condition in Palaeozoic chon- drichthyans (Fig. S2c, S3a). Anterior to the lower jaws, teeth are present whose sizes are small compared to jaw dimensions. These proportions appear to correspond well with the reconstructions of Thrinacodus (Grogan & Lund, 2008).

Remarks - Quite a few species of Phoebodus based on teeth with almost identical crowns and only minor differences in the bases were described from the Famennian. These are: Ph. rayi (Ginter & Turner, 1999), Ph. typicus (Ginter & Ivanov, 1995), Ph. turnerae (Ginter & Ivanov, 1992), Ph. gothicus (Ginter, 1990), and Ph. politus (Newberry, 1889). Ph. rayi (Ginter & Turner, 1999) and Ph. turnerae (Ginter & Ivanov, 1992) can easily be removed from the comparison with Ph. saidselachus sp. nov., because their orolingual button is not situated in the centre of the base, but at the lingual rim. Most specimens of Ph. gothicus have much longer bases, which are lingually rounded or end with an angle. However, the teeth of Ph. typicus and Ph. politus are very similar to those of Ph. saidselachus sp. nov. and in fact, they can easily be confused among each other. Tooth bases of Ph. typicus are more rectangular and wider than in Ph. saidselachus sp. nov., while the tooth bases are more circular in Ph. politus. The published teeth of the latter species (New- berry 1889, pl. 27, fi gs 27, 28; Eastman 1907, pl. 7, fi g. 5; 1908, pl. 1, fi g. 9) are relatively large and about the same size as Ph. saidselachus sp. nov. (base width about 7-8 mm), whereas all the known teeth of Ph. typicus do not exceed 2 mm. As far as the tooth morphology is concerned, Ph. saidselachus sp. nov. is situated between the older species (Ph. typicus, early-middle Famennian) and the younger one (Ph. politus, late Famennian).

2. Specimen PIMUZ A/I 4712

Mandibular dentition and tooth morphology - Remains of small partially articulated teeth lie in the space between the right upper and lower jaw (Fig. 1a,c). All teeth are extremely fragile and it is not possi- ble to extract one without damaging it signifi cantly. The diagnostic morphological details of the tooth base is often not exposed or not preserved. However, some bases show a rounded outline lingually similar to specimen PIMUZA/I 4656 and PIMUZ A/I 4710. Therefore, we assign all three specimens to Phoebodus saidselachus sp. nov.

In labial aspects, the teeth show the characteristic crown shape of phoebodontids with three long main cusps (one median and two laterals) of similar length. In oral view, the cusps appear to recurve subtly lin- gually (Fig. S7c). Very faint traces of cross-sections of minute intermediate cusplets between the central and lateral cusps are present in two teeth (Fig. S7b,c). Cusp ornamentation is either not preserved or not present. In oral and aborolateral aspects, the preserved remains of the tooth bases show a rather subcircular or probably slightly rectangular outline. Lingually and close to the crown, a single orolingual button of oval shape is visible. This protrusion is wider than the central cusp and covers around half of the labiolin- gual length of the base (Fig. S7b). Posterior to the orolingual button, the lingual opening of the main basal canal is situated. In aborolateral view, the base shows remains of an elliptical concavity in the center, which serves as an articulation surface for the orolingual button of a former tooth (Fig. S7d). Cross-sections of lateral aspects of tightly packed teeth are visible in some jaw regions (Fig. S7a, e). The articulated teeth do

112 Chapter III: Phoebodontid chondrichthyans of the Maider not differ measurably in size among each other. In lateral view, the base shows sometimes an aborolingual concavity, which fi ts to the orolingual convexity of the former tooth.

The preserved teeth let assume that the dentition of the described specimen of Phoebodus was homo- dont: its teeth do not signifi cantly differ in size or shape within or between jaw types. There are few teeth that look slightly different: the most posterior tooth (marked with an asterisk in Fig. S7a) appears to have a stouter crown with median and lateral cusps showing a wider diameter compared to the other teeth. A second tooth shows a much bigger base from the oral aspect (marked with asterisk in around the middle of Fig. S7a). However, mostly the crowns are exposed or preserved, which are less diagnostic on the species level than the tooth bases.

Body form and proportions - In PIMUZ A/I 4712, the right and left Meckel`s cartilage, the right pala- toquadrate, some parts of the branchial and postcranial skeleton (shoulder girdles, pelvic fi n remains, dorsal fi n spines, neural arches) and traces of the body outline are present (Fig. 1a,b). The caudal region is largely eroded. According to this specimen, Phoebodus had an elongated, anguilliform body shape similar to Thrinacodus, but less slender. The entire specimen measures 0.98 m from the preserved anterior edge of the jaws to the most posterior fragment of cartilage. However, this specimen was longer; based on the length of the nodule, which usually corresponds roughly to the shape of the incorporated carcass, we esti- mate that the complete animal was at least 1.2 m long. The jaws are long and delicate measuring 0.18 m, although the anterior ends of the jaws are missing. The distance between the anterior end of jaws to the fi rst dorsal fi n spine measure 0.38 m and the distance between the fi rst and second dorsal fi n spines is 0.4 m. The body height of Phoebodus is low but both relatively and absolutely higher than in Thrinacodus (only 20 mm high): In PIMUZ A/I 4712, the anterior part of the lower and upper jaws together is around 0.05 m high, the branchial arch region around 0.11 m and the thoracic region around 0.14 m high. Estimated body proportions are as follows: jaw length to body length maximal 15% (Thrinacodus: head length to body length 8.5%) and body height to body length maximal 11% (Thrinacodus: 3%).

Mandibular arches - The right and left Meckel`s cartilage (mc) as well as the right palatoquadrate (pq) are exposed from the lateral and slightly ventral view (Fig. 1c). Anteriorly, the tips of the lower jaws and palatine rami are missing. Estimation of the missing nodule part is approximately 50 mm in anteroposterior length. Like in Thrinacodus gracia, there are no traces of labial cartilages that are a common feature in hybodonts and recent chondrichthyans.

All jaw elements are elongated, which contrasts the mandibular conditions in many other Palaeozoic chondrichthyans (xenacanthids, cladoselachians, symmoriids and hybodontids). This morphological trait segregates Phoebodus from Heslerodus that was previously described as Ph. heslerorum (Zangerl 1981; Stahl 1988) and therefore supports the teeth-based revision of Ginter (2002). In contrast to Thrinacodus gracia, where the palatoquadrate is much shorter than Meckel`s cartilage, both upper and lower jaws are elongated to roughly the same extend in Phoebodus. In Ph. saidelachus sp. nov. (PIMUZ A/I 4656) de- scribed in this work, the upper jaw appears to reach some millimeters anterior of the lower jaw (Fig. S2c).

Both Meckel`s cartilages are exposed from lateral and slightly ventral aspects and show an anteriopos- teriorly elongation. The overall slender shape resembles the lower jaws of chlamydoselachids, xenacan- thids and Thrinacodus gracia. The posterior half is dorsoventrally about the same height as the quadrate re- gion of the palatoquadrate. Towards the anterior end of the nodule, Meckel`s cartilage is slightly narrowing dorsoventrally. Posteriorly, the dorsoventral outline thins out and forms an amphistylic articulation with the palatoquadrate. The dorsal edge of the right lower jaw is slightly concave anterior to the articulation; it is also rather straight along the rest of the jaw. Posteroventrally, the edge of the right jaw fl ips laterally forming a rim.

The ventral edge of the right palatoquadrate is covered anteriorly by teeth and posteriorly by Meckel`s cartilage. A little dorsal to the ventral edge and anterior to the articulation of the jaws, a prominent lateral ridge (80 mm long and 10 mm high) extends from the quadrate region and runs in parallels across two thirds of its anteroposterior length (Fig. 5, 7a-c; mcr). However, this ridge might have formed due to ta- phonomic alteration such as compcation. The quadrate region is dorsoventrally only slightly broader than the suborbital palatine, which differs from the condition in Thrinacodus gracia, the xenacanthids and the symmoriiforms. Similar conditions with a dorsoventrally relatively short quadrate region are known from

113 Chapter III: Phoebodontid chondrichthyans of the Maider recent Chlamydoselachus and hybodontids, although in latter one the quadrate region is laterally expanded forming a quadrate fl ange (Smith 1937; Maisey 1982, 1986). In Phoebodus, the posterodorsal edge of the quadrate region is fl ipped laterally, thus forming a strong posterolateral rim where the adductor muscles are inserted. The remains of the suborbital palatine ramus are slightly narrower dorsoventrally than the quadrate region.

Hyoid and gill arches - The basihyal (bh), a ceratohyal (ch) and two ceratobranchials (cb) are preserved (Fig. 1c). Additional branchial arches might be preserved, but they are hardly distinguishable from each other due to its mode of preservation. Branchial rays are either not present or not preserved and were also not described from Thrinacodus gracia (Grogan & Lund 2008).

A long triangular cartilage lies posterior to the point where the lower jaws meet. This cartilage proba- bly represents the basihyal in ventral aspect. A comparable structure was not described from Thrinacodus (Grogan & Lund 2008) but the position of the cartilage corresponds to the subtriangular anteriormost ba- sibranchial documented for Akmonistion and Stethacanthus (Coates & Sequeira 2001; Lund 1985a). Other basibranchial elements such as those described from Cobelodus (Zangerl & Case 1976) and Heslerodus (Williams 1985) were not found in Phoebodus.

The left ceratohyal articulates posteriorly to the basihyal and it parallels the left Meckel`s cartilage. It is exposed from its lateral aspect posteriorly and from the ventrolateral aspect anteriorly. The ceratohyal mea- sures between around 1/2 and 1/3 of the mandibular length and posteriorly, it curves to the same degree as the posteroventral edge of the left Meckel`s cartilage. It is rather straight in profi le compared its semicres- cent shape in symmoriids, cladoselachids (Coates & Sequeira 2001) and xenacanthids (Heidtke & Schwind 2004). Moreover, unlike in Akmonistion zangerli (Coates & Sequeira 2001), the ceratohyal of Phoebodus is not uniformly thick throughout its length: its posterior edge is dorsoventrally broad but towards the ante- rior end, the cartilage is narrowing. In ventral view, the ceratohyal is narrow over around 3/4 of its length, but in its anteriormost quarter, the ventral surface is laterally expanding and forms a fl ange (anteriorly blade-like shaped) articulating anteriorly with the basihyal. A similar medial fl ange is present in Tristychius arcuatus (unpublished information M. Coates). There is no hypohyal anterior to the ceratohyal such as it is present in Thrinacodus gracia and xenacanthids (Triodus and Xenacanthus; Heidtke et al. 2004).

Remains of ceratobranchials are preserved dorsal to the left ceratohyal. There is a rod-shaped rest of a ceratobranchial of slightly shorter length than the ceratohyal. Weak traces of two additional ceratobranchi- als are exposed above the relatively well-preserved ceratobranchial. Other elements such as epibranchials, hypobranchials and pharyngobranchials cannot be determined with certainty, although the body outline adumbrates the presence of more branchial elements.

Pectoral girdle and fi ns - The scapulacoracoid (sc) is partially preserved in PIMUZ A/I 4712. From the pectoral fi n, fragments of the metapterygium and remains of fi ve tightly packed radials (rad) or basals alike Thrinacodus are preserved (Fig. 1a, b). Dorsally, the scapula is broken and there is no information about anterodorsal and posterodorsal processes preserved. The scapula and coracoid are fused and their shape re- sembles the scapulacoracoids of symmoriids. The coracoid region is anteriorly convex and there is a broad ventral concavity probably serving as an articular surface for fi n radials. On the posterior edge of the cora- coid, there is a rather deep and small concavity; however, this concavity could be the result of taphonomic alteration. Coracoid plates separated from the scapula such as in Thrinacodus gracia (Grogan & Lund 2008) are absent in Phoebodus. Posterior to the coracoid, there are possible fragments of a metapterygium (mpt) that is articulated to fi ve poorly preserved radials.

Pelvic girdle and fi ns - On the ventral side of the specimen at the position of the second dorsal fi n spine, the nodule extends into a fi n-like protrusion, probably documenting the former presence of pelvic fi ns and their position (Fig. 1a, b). Below the second dorsal fi n spine, several remains of cartilage are visible. The different cartilages are hardly distinguishable from each other. Two of these cartilages may represent remains of radials (rad).

Dorsal fi n and fi n spines - Radials of dorsal fi ns are absent but faint traces of cartilage (adbc, pdbc, Fig. 1a,b) are located posterioventrally to both fi n spines. Probably, this cartilage was serving as a support for the fi n spine like the triangular basal elements in hybodonts (Maisey 1982). Two fi n spines are well exposed in association with the anterior and posterior dorsal fi ns (fs, Fig. 1a, b, Fig. S6a, b). Both spines

114 Chapter III: Phoebodontid chondrichthyans of the Maider are closely aligned to the body outline, but their orientation could have been altered taphonomically while their relative positions appear to correspond to their primary relative positions, at least with respect to their distance from each other. The anterior fi n spine is proximodistally longer and anteroposterioly thicker than the posterior one. The fi n spines are slender, slightly recurved, deeply inserted and in that respect resemble Sphenacanthus aquistriatus and Amelacanthus (Maisey 1982). Their edges are smooth and the dorsal edg- es of both fi n spines are slightly convex while the ventral spine wall is slightly sigmoidal in profi le (pos- teriorly, the last third of the spine length shows a subtle concavity). The ornamentation of the fi n spine is poorly visible because most of the spine surface is weathered. There still are some remains of ctenacanthid ornaments (Fig. S6c) consisting of regular costae intercalated by narrow intercostal grooves and transverse ridges interrupting the costae regularly, giving the ornament a zipper-like appearance.

Axial Skeleton - Ventral to the anterior dorsal fi n spine, remains of neural arches are discernible (Fig. 1a, b). Anteriorly, it is not possible to visually separate the neural arches from each other. Towards the posteri- or, the outlines of twelve neural arches of vertebrae become clearer. The dorsal edge of the closely packed, slender and rod-shaped neural arches are directed posteriorly. Among the preserved arches, the posterior arches are dorsoventrally longer than the more anterior ones forming a crest-like structure; it is not clear whether this might be due to a taphonomic alteration (e.g., compaction, collapse, etc.). Vertebral elements such as interventrals, basidorsals, basiventrals and hemal spines were described in Thrinacodus but these are not preserved in the Phoebodus specimen described here.

Remarks - In spite of its unique completeness, especially when compared to the previously known fossil record of Phoebodus consisting of countless teeth mainly, the preservation of the here described specimen is far from perfect. For example, the caudal fi n and much of both pelvic and pectoral fi ns are missing. This is quite characteristic for the taphonomy of the gnathostomes of the Thylacocephalan Layer in the southern Maïder (Frey et al. submitted). Usually, the fi sh remains are incorporated in large fl at nodules rich in hae- matite and limonite. The head and gill regions usually is encased in the thickest part of the nodule, while most of the postcranium lies on top of the nodule that thins out posteriorly. In some rare cases, the caudal fi n still rests on the nodule while in most other cases, the posterior of the skeletons is eroded, because it was embedded in the deeply weathered crumbling claystone. Nevertheless, the shape of the nodules very roughly traces the outline of the former carcass, thus documenting the overall body shape, position of fi ns and their rough dimensions. Based on this indirect evidence, we suggest that the caudal fi n resembled that of Thrinacodus in lacking strongly developed dorsal and ventral lobes as in, e.g., modern elasmobranchs like Carcharodon. Instead, the caudalis probably had a shape like that known from Thrinacodus (but less elongate) or Cladoselache.

Phoebodus sp.

Specimen PIMUZ A/I 4711 and PIMUZ A/I 4713

Neurocranium - In PIMUZ A/I 4713, the dorsal portion of the otic and occipital region and a small part of the interorbital space is preserved. In PIMUZ A/I 4711, computer tomographies provide anatomical insights into the otic region including semicircular canals and the entire occipit.

The preserved remains of the postorbital process indicate a short, anteroposteriorly narrow process (Fig. S4). In the otic region, the anterior and posterior semicircular canals dorsally unify to a crus commune such as in symmoriiforms, Cladodoides and xenacanthids. Therefore, Phoebodus likely had no for phono- reception. The endolymphatic chamber is narrow anteriorly and broadens dorsally; paired endolymphatic ducts are located anterior to the crus commune (Fig. S4). The endolymphatic fossa is narrow and laterally fl anked by prominent dorsal otic ridges (Fig. 2a-d, S5a-e), which closely resembles the condition seen in Tamiobatis, Orthacanthus, and Tristychius (Williams 1998; Schaeffer 1981; Coates & Tietjen 2018). This shape of the endolymphatic fossa is in contrast to the ovoid shape in Stethacanthus Newberry, 1889, Ak- monistion Coates & Sequeira, 2001 and Dwykaselachus Oelofsen, 1986. Similar to the condition in Clado- doides, the glossopharyngeal canals are fl oored by a massive hypotic lamina, which hosts two openings for the lateral dorsal aortae posteriorly (Fig. 2b). Therefore, the dorsal aorta splits posterior to the occipital

115 Chapter III: Phoebodontid chondrichthyans of the Maider level like in Cladodoides, Tamiobatis, Tristychius and xenacanthids (Maisey 2005; Schaeffer 1981; Coates & Tietjen 2018).

The occipital region is elongated compared to other early and modern elasmobranchs but might be similarly elongated in the phoebodont Thrinacodus gracia (Fig. S4a-b; fi g. 10C in Grogan & Lund 2008). On the right lateral side of the occiput, traces of three canals for the spino-occipital nerves are preserved. Moreover, the prominent supraoccipital crest is a common feature of Phoebodus, Tristychius, and xenacan- thids (Schaeffer 1981; Coates & Tietjen 2018).

Branchial arches – Remains of hyoids articulate at the periotic region of the braincase (Fig. S5a, e). They are fl at, dorsoventrally broad and slightly curved. Anteriorly, the ceratohyals anteriorly have a fl ange like in PIMUZ A/I 4712 (Fig. 1c, 2i, S5a, e). Remains of mandibular and gill arches with little anatomical details are preserved (Fig. S5a-f): the palatoquadrate has fl ipped to the ventral side of the braincase and it has been recognized by the presence of the dorsal crest of the otic process (Fig. S5f).

Endocast – The reconstructed endocast (Fig. 3a-e) shows parts of the sacculum, the external and posterior semicircular canals, and the medulla. Like in symmoriids, xenacanthids and Cladodoides, the posterior semicircular canals form a wide arch each and unify with the posterior ampullae. The medulla of Phoebo- dus is anteroposteriorly long which resembles the condition in other elasmobranchs such as Cladodoides and xenacanthids (Maisey 2007; Schaeffer 1981).

Body squamation - Multicuspid scales are preserved in the head region of PIMUZ A/I 4713. Due to their poor preservation and because they are embedded in the host rock, a morphological description is impos- sible at this point (Fig. S8).

3) Taxa and sources

The taxa list was adopted from Coates et al. (2018). 22 taxa of stem gnathostomes (including Agnatha, Placodermi and some Osteichthyes) were excluded from the phylogenetic analyses as they were not rele- vant for the position of the phoebodontid chondrichthyans within the chondrichthyan phylogeny.

Acanthodes: Benznosov 2009; Brazeau & de Winter 2015; Coates 1994; Davis et al. 2012; Heidtke 1993, 2011a,b; Jarvik 1977, 1980; Miles 1968, 1973a, b; Nelson 1968; specimens AMNH 1037b, 10370, 10376, 19628; CMNH 30725b, 30726, 4591; FMNH PF2875; GM C145, 146, 180; HM V8251, 252; HU MB.F.4209, 4277, 4284, 4285, 7286, MB3b, 4a & b, 5a & b, 7a & b, 8a & b, 11a & b, 12a, 13a &b, 14a &b, 16a &b, 17a & b, 18a & b, 23 (resin copy), 24, MM L1693, 1698, 9432B, W1994; NHM P.11287, P.13139, 13140, 14558, 1728, 34912, 34914, 4057, 49941, 49944, 49959, 49967, 49979, 49980, 49990, 49995, 49996, 60928, 60939, 62138, 7335; NMS 2001.7.1, 3; UCL GM C1126; UMZC GN9, 11, 13, 14, 15a &b, 16, 39, 756. Acronemus: Maisey 2011; Rieppel 1982. Akmonistion: Coates & Sequiera 1998, 2001a, b; Coates et al. 1998; Coates et al. 2017. Brachyacanthus: Denison 1979; Miles 1973a; Watson 1937; specimens NMS Kinnaird 88, NMS (Powrie) 1891.92.212, 213, 214, 220, 222, 224, 225, 226, 227. Brochoadmones: Bernacsek & Dineley 1977; Gagnier & Wilson 1996b; Hanke & Wilson 2006; specimens UALVP 32672, 41487, 41493, 41494, 41495. Callorhinchus/Hydrolagus: Cole 1896; De Beer 1937; De Beer & Moy-Thomas 1935; Didier 1995; Didier et al. 1994, 1998, 2012; Howard et al. 2013; Kesteven 1937; Patterson 1965, 1992; Pradel et al. 2013; Stahl 1999. Cassidiceps: Gagnier & Wilson 1996a; specimen UALVP 32454. Cheiracanthus: Denison 1979; Miles 1973a; Watson 1937; specimens AMNH 317, 6929, 7082; GM C295, 296, 325, 490; HM V7614; IC 214, 215, 216, 217; UMZC GN14a &b, 19, 20, 21, 31, 50; 1131a & b, 1132a & b, 1133a & b, 1134a & b, 1135a & b, 1136a & b, 1137a & b, 1138, 1139, 1140. Cheirolepis: Arratia & Cloutier 1996; Pearson & Westoll 1979; Giles et al. 2015a. Chondrenchelys: Finarelli & Coates 2012, 2014; Lund 1982; Moy-Thomas 1935; specimens NMS 1885.54.5/5A, 1891.53.33, 1998.35.1, 2002.68.1; BGS-GSE 13328; HM V.7173.

116 Chapter III: Phoebodontid chondrichthyans of the Maider

Cladodoides: Gross 1937, 1938; Maisey 2005. Cladoselache: Bendix-Almgreen 1975; Harris 1938a, b; Maisey 1989a, 2007; Schaeffer 1981; Williams 2001; Woodward & White 1938; specimens CMNH 8110, 8111, 8207, NHM P9273, P9285. Climatius: Miles 1973a, b; Watson 1937: specimens AMNH 7762; GSM 49785; MM L12096a & b; NMS Kinnaird 80; NMS 1881.5.62; NMS 1887 (Peach) 35.3a, 35.5b, 35.5e; NMS 1891 (Powrie) 92.195, 204, 206, 214; NMS 1967.12.4; NMS 1973.9.4; NMS 2001.7.2. Cobelodus: Zangerl & Case 1976; Zidek 1992. Culmacanthus: Long 1983. Damocles: Lund 1986: specimens CM 35472, 48760. Debeerius: Grogan & Lund 2000: specimens CM 35479, 35480, 48831, 62811. Diplacanthus: Gagnier 1996; Miles 1973a; Watson 1937; specimens FMNH PF11633; GM C12, 13, 148; GM P482; MM L5503, 1609; NMS (Powrie) 1891.92.334; NMS 2001.7.4; UMZC GN17, 18, 22. Diplodoselache: Dick 1981. Doliodus: Miller et al. 2003; Maisey et al. 2009, 2013, 2017; Long et al. 2015. Dwykaselachus: Coates et al. 2017; Oelofsen 1986; specimen SAM K5840. Egertonodus: Maisey 1982, 1983; Lane, 2010. Entelognathus: Zhu et al. 2013. Falcatus: Lund 1985; Maisey 2007; specimens CM 35465, 37532 Gladbachus: Heidtke & Krätschmer 2001; Heidtke 2009; Burrow & Turner 2013; specimen UMZC 2000.32. Guiyu: Zhu et al. 2009. Gyracanthides: Miles 1973a; Warren et al. 2000; Turner et al. 2005. Halimacanthodes: Burrow et al. 2012. Hamiltonichthys: Maisey 1989b. Helodus: Patterson 1965; Stahl 1999; specimens NHM P.6706, 8207, 8209, 8212, 8213. Homalacanthus: Gagnier 1996; Watson 1937; specimens FMNH PF4875; MM LL12452. Homalodontus: Mutter et al. 2007, 2008. Iniopera: Zangerl & Case 1973; Pradel et al. 2009, Pradel 2010; Pradel et al. 2010. Ischnacanthus; Miles 1973a; Watson 1937; specimens GM C3, 6, 149, 324; GM P298; MM L9522, 9431, 9432; MM STR0585; NMS (Powrie) 92.254, 258; UALVP 32401, 32405, 32414, 39060, 39075, 40478, 41491, 41861, 42201, 42215, 42660, 43245, 44048, 44049, 44091, 45014. Kathemacanthus: Gagnier & Wilson 1996a; Hanke & Wilson 2010; specimens UALVP 32402, 42269, 43113. Kawichthys: Pradel et al. 2011. Latviacanthus: Schultze & Zidek 1982. Lupopsyrus: Hanke & Davis 2012; Bernacsek & Dineley 1977; specimens NMC 22700B, 22700C, 22715, 22718, 22719, 22700D, 22700E, 22700F, 22701C, 22701D, 22716, 22717, 22720, 22745; UALVP 19260, 32420, 32442, 32456, 32458, 32474, 32476, 32480, 32482, 39065, 39067, 39079, 39080, 39081, 39082, 39121, 41493, 41629, 41632, 41665, 41931, 41939, 41945, 42000, 42002, 42008, 42012, 42013, 42027, 42046, 42061, 42113, 42142, 42150, 42173, 42208, 42274, 42518, 42524, 42529, 42530, 42533, 42538, 42453, 42454, 42455, 42544, 42597, 42605, 43064, 43091, 43092, 43094, 43095, 43256, 43409, 43456, 45154, 45155. Mesacanthus: Miles 1973a; Watson 1937; specimens FMNH PF1439; GM C18, 288a &b; NMS (Powrie) 1891.92.275; UMZC GN1143. Mimipiscis: Gardiner & Bartram 1977; Gardiner 1984; Choo 2011; Giles & Friedman 2014. Moythomasia: Gardiner & Bartram 1977; Gardiner 1984; Coates et al. 2017; specimen MV P222915. Nerepisacanthus: Burrow 2011; Burrow et al. 2014. Obtusacanthus: Hanke & Wilson 2004; specimen UALVP 41488. Onychoselache: Dick & Maisey 1980; Coates & Gess 2007. Orthacanthus: Heidtke 1982, 1999; Hotton 1952; Schaeffer 1981; Maisey 1983; Lane & Maisey 2009. Ozarcus and FMNH PF 13242: Maisey 2007; Pradel et al. 2014; Coates et al. 2017. Parexus: Watson 1937; Miles 1973a. specimens AMNH 1163, 7766; NMS Kinnaird 94; NMS (Peach) 1887.35.3a, 5e; NMS 1891 (Powrie) 92.183, 184, 186, 188, 194, 197, 207; NMS 1956.14.4.15; NMS 1977.46.3a & b.

117 Chapter III: Phoebodontid chondrichthyans of the Maider

Phoebodus: Newberry 1889; Ginter 1990; Ginter & Ivanov 1992, 1995; Ginter et al. 2002; Ginter et al. 2010; specimen PIMUZA/I 4656, PIMUZ A/I 4710, PIMUZ A/I 4712, PIMUZ A/I 4711, PIMUZ A/I 4713. Poracanthodes: Denison 1979; Valiukevicius 1992. Promesacanthus: Hanke 2008; specimens UALVP 41672, 41859, 41860, 42652, 43027. Psarolepis: Yu 1998; Zhu & Schultze 1997; Zhu et al. 1999; Qu et al. 2013a. Ptomacanthus: Brazeau 2009, 2012; Denison 1979; Miles 1973a; specimens BM P.19999, 24919b. Pucapampella: Maisey 2001a; Maisey & Anderson 2001; Maisey & Lane 2010; Janvier & Maisey 2010. Raynerius: Giles et al. 2015b. Rhadinacanthus: Burrow et al. 2016. Squalus: Schaeffer 1981; Gans & Parsons 1964; Marinelli & Strenger 1959. Synechodus: Maisey 1985; NHM P.6135, 41675. Tamiobatis: Schaeffer 1981; Williams 1998; specimen FMNH PF5414. Tetanopsyrus: Gagnier & Wilson 1995; Gagnier et al. 1999; Hanke et al. 2001; specimens UALVP 32571, 38682, 39062, 39078, 42512, 43026, 43246, 44030, 43089. Thrinacodus: Turner 1982; Ginter 2000; Ginter & Sun 2007; Ginter & Turner 2010; Ginter et al. 2010; Grogan & Lund 2008. Tribodus: Maisey & de Carvalho 1997; Lane 2010; Lane & Maisey 2009, 2012. Triodus: Solér-Gijon, R. & Hampe 1998; Hampe 2003; Heidtke et al. 2004. Tristychius: Dick1978; Coates & Gess 2007; Coates & Tietjen in press: specimens NMS 1972.27.455A, 1974.51.5A; HM V8299. Uraniacanthus: Bernacsek & Dineley 1977; Hanke & Davis 2008; Newman et al. 2012; Burrow et al. 2016; specimens UALVP 19259, 32448, 32469, 38679, 41669, 41857, 41858, 41862, 42095, 42095, 44046, 45366 to 45396. Vernicomacanthus waynensis: Miles 1973a. Youngolepis: Chang & Yu 1981; Chang 1982, 1991, 2004.

4) Character list Skeletal tissues 1 Tessellate calcifi ed cartilage: absent (0); present (1). Brazeau (2009); Coates & Sequeira (2001a, b); Davis et al. (2012); Dean & Summers (2006); Dean et al. (2009); Grogan et al. (2012); Maisey (1984, 2001, 2013); Lund & Grogan (1997, 2004a, b); Seidel et al. (2016). 2 Perichondral bone: present (0); absent (1). Janvier (1996); Donoghue & Aldridge (2001); Brazeau (2009); Davis et al. (2012); Lund (1985); Coates et al. (1999). 3 Extensive endochondral ossifi cation: absent (0); present (1). Forey (1980); Gardiner (1984); Brazeau (2009); Davis et al. (2012). 4 Extensive calcifi ed cartilage: absent (0); present (1). This character refers to taxa where perichon- dral bone is absent but where cranial or postcranial skeletal parts consist of mineralized and therefore, more robust cartilage (Coates et al. 2018). 5 Dentine kind: mesodentine or semidentine (0); orthodentine (1). Donoghue et al. (2000); Brazeau (2009); Davis et al. (2012); Burrow et al. (2016). Orthodentine was coded as `non-applicable` in the data matrix of Grogan and Lund (2008). However, according to Ivanov (2000), the teeth of Thrinaco- dus contain orthodentine in the cusps and osteodentine in the base. 6 Pore canal network: absent (0); present (1). Lu et al. (2016). 7 Acrodin tooth caps (enameloid cap restricted to crown apex): absent (0); present (1). Friedman & Brazeau (2010); Zhu et al. (2013, 2009); Lu et al. (2016).

Squamation & related structures 8 Trunk scales monocuspid (0); multicuspid (1). Revised after Davis et al. (2012); Burrow et al. (2016). Scale growth differs among different groups of gnathostomes: scales of teleostomes (osteich- thyans and acanthodians) have a sustained growth whereas in non-teleostomes (chondrichthyans), the scales stop growing when reaching a determinate size (Nelson 1969; Reif 1985). However, in several Palaeozoic chondrichthyans, scales grow throughout their life (Nelson 1970; Zangerl 1981) and there- fore, limited scale growth is assumed to be a derived condition. In Phoebodus, we fi nd multicuspid scales, but their growth pattern is unkown thus far.

118 Chapter III: Phoebodontid chondrichthyans of the Maider

9 Scale growth concentric: absent (0); present (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Burrow et al. (2016). 10 Peg-and-socket articulation: absent (0); present (1). Gardiner (1984); Coates (1999); Brazeau (2009); Davis et al. (2012). 11 Anterodorsal process on scale: absent (0); present (1). Zhu et al. (2009, 2013); Gardiner (1984); Coates (1999); Brazeau (2009); Davis et al. (2012). 12 Body scales with bulging base: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Burrow et al. (2016). 13 Body scales with fl attened base: absent (0); present (1). Brazeau (2009, 2012); Davis et al. (2012); Burrow et al. (2016). 14 Body scales with basal canal or open basal vascular cavity: absent (0); present (1). Placoid scales of both modern as well as early chondrichthyans (e.g. Akmonistion, Antarctilamna) are characterized by the presence of a basal canal (Reif 1978; Coates & Sequeira 2001a; Young 1982). Basal canals were identifi ed in disarticulated chondrichthyan scales such as Elegestolepis (Karatajūte-Talimaa 1992), Polymerolepis and Seretolepis (Hanke & Wilson 2010) as well as in a few acanthodian taxa such as Kathemacanthus, Tetanopsyrus (Hanke et al. 2001, fi g.2c), Lupopsyrus (Hanke and Davis 2012), and Ptomacanthus (Brazeau 2012, tentative identifi cation in fi g. 7D). Basal canals could not yet be identifi ed in the scales of Phoebodus. 15 Neck canal: absent (0) present (1). The presence of neck canals is a common feature in placoid scales, but neck canals were either found in scales of placoderms (Burrow & Turner 1998, 1999) and osteichthyans (Qu et al. 2013a, b). 16 Sensory line canal passes between or beneath scales (0); passes over scales and/or is partially enclosed or surrounded by scales (1); perforates and passes through scales (2). Davis (2002); Friedman & Brazeau (2010); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014); Burrow et al. (2016). In Thrinacodus, the lateral line system of the mandibular region is enclosed by tesserate mineralized tissue. 17 Lepidotrichia or lepidotrichia-like scale alignment: present (0); absent (1). Davis et al. (2012). 18 Epichordal lepidotrichia: absent (0); present (1). Zhu et al. (2009, 2013). 19 Fringing fulcra: absent (0); present (1). Zhu et al. (2009, 2013); Coates (1999). 20 Scute-like ridge scales (fulcra): absent (0); present (1). Giles et al. (2015c).

Cranial dermal skeleton 21 Sclerotic ring: absent (0); present (1). Giles et al. (2015c); Qiao et al. (2016); Zhu et al. (2016); Burrow et al. (2016). Sclerotic rings are present in early chondrichthyans such as Cladoselache (Lund 1986; Williams 2001; CMNH 8207 exhibits especially well preserved plates: pers. obs. MIC), Cobe- lodus (Zangerl & Case, 1976), Falcatus (Lund, 1985), Damocles (Lund, 1986), Ctenacanthus (Wil- liams, 2001), Gladbachus (Coates et al., 2018) and Iniopteryx (Zangerl & Case, 1973). No sclerotic ring is preserved in the available material of Phoebodus and Thrinacodus. 22 Number of sclerotic plates: four or less (0); more than four (1). Zhu et al. (2013, c170); Qiao et al. (2016, c.241); Zhu et al. (2016, c.239); Burrow et al. (2016). 23 Dermal ornamentation: smooth (0); parallel, vermiform ridges (1); concentric ridges (2); tuber- culate (3). Giles et al. (2015c). 24 Dermal skull roof includes large dermal plates (0); consists of undifferentiated plates, tesserae or scales (1); naked or largely scale free (2). Forey (1980); Gardiner (1984); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 25 Cranial tessera morphology: large interlocking plates (0); microsquamose, no larger than body squamation (1). Brazeau (2009) through to Giles et al. (2015c). 26 Anterior or mesial edge of nasal notched for anterior nostril: absent (0); present (1). Contra Zhu et al. (2013), the anterior rim of the nasal in Cheirolepis is notched. 27 Supraorbital: absent (0); present (1). Zhu et al. (2009, 2013). 28 Large median bone contributes to posterior margin of skull roof: absent (0); present (1). Zhu et al. (2016). 29 Medial process of paranuchal wraps around posterolateral corners of nuchal plate: absent (0); present (1); paranuchals precluded from nuchal by centrals (2); no median bone in posterior of skull roof (3). Giles et al. (2015c). 30 Pineal opening perforates dermal skull roof: present (0); absent (1). Davis et al. (2012); Giles et

119 Chapter III: Phoebodontid chondrichthyans of the Maider

al. (2015c). 31 Consolidated cheek plates: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 32 Enlarged postorbital tessera separate from orbital series: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 33 Dermal intracranial joint: absent (0); present (1). Zhu et al. (2009, 2013) 34 Foramina (similar to infradentary foramina) on cheek bones: absent (0); present (1). Zhu et al. (2009, 2013). 35 Preopercular bone: absent (0); present (1). Zhu et al. (2013). 36 Maxilla expanded posteriorly: absent - splint shaped (0); present - cleaver shaped (1). Zhu et al. (2009, 2013); Lu et al. (2016). 37 Sensory line network preserved as open grooves (sulci) in dermal bones (0); sensory lines pass through canals enclosed within dermal bones (1). (Davis 2002); Davis et al. (2012); Zhu et al. (2013). 38 Sensory canal or pit-line associated with maxilla: absent (0); present (1). Friedman (2007) 39 Jugal portion of infraorbital canal joins supramaxillary canal: present (0); absent (1). Brazeau (2009), but see redefi nition in Davis et al. (2012); Zhu et al. (2013). 40 Anterior pit line of skull roof: absent (0); present (1). Giles et al. (2015c). 41 Spiracular opening in dermal skull roof bounded by bones carrying otic canal: absent (0); pres- ent (1). Giles et al. (2015); Lu et al. (2016). 42 Endolymphatic ducts open in dermal skull roof: present (0); absent (1). Janvier (1996); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Giles et al. (2015c). 43 Dermohyal (submarginal) ossifi cation: absent (0); present (1). 44 Dermohyal (submarginal) shape: broad plate that tapers towards its proximal end (0); narrow plate (1). Brazeau’s (2009) 45 Branchiostegal series: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 46 Opercular and subopercular bones: absent (0); present (1). 47 Branchiostegal plate series along ventral margin of lower jaw: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 48 Branchiostegal ossifi cations plate-like (0); narrow and ribbon-like (1); fi lamentous (2). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Lu et al. (2016). 49 Branchiostegal ossifi cations ornamented (0); unornamented (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 50 Branchiostegals imbricated: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 51 Opercular cover of branchial chamber complete or partial (0); separate gill covers and gill slits (1). Lund & Grogan (1997); Hanke & Wilson (2004); Davis et al. (2012); Zhu et al. (2013). Condition ´1` is likely a synapomorphy of recent elasmobranchs although opercular covers are not present in most Paleozoic chondrichtyans (Coates et al. 2017, see data matrix discussion in Coates et al. 2018). Opercular cover in holocephalans secondarily evolved (cf. Coates et al. 2017). 52 Gular plates: absent (0); present (1). Gardiner (1984); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 53 Size of lateral gular plates: extending most of length of the lower jaw (0); restricted to the anteri- or third of the jaw (no longer than the width of three or four branchiostegals) (1). Coates (1999); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013).

Hyoid and gill arches 54 Gill skeleton mostly beneath otico-occipital region (0); mostly posterior to occipital region (1). Zangerl (1981); Lund & Grogan (1997); Stahl (1999). Except for holocephalans, the gill skeleton is mostly located posteriorly to the neurocranium in chondrichthyans. In acanthodians, gill skeletons are located either beneath or posterior to the occipital region of the braincase. 55 Perforate hyomandibula: absent (0); present (1). Zhu et al. (2009, 2013); Lu et al. (2016). 56 Interhyal: absent (0); present (1). Davis et al. (2012); Zhu et al. (2013). 57 Ceratohyal smooth with posterior, lateral fossa: absent (0); present (1). Coates et al. (2018). Characteristic feature in Recent and early elasmobranchs such as Egertonodus (Maisey 1983), Ortha-

120 Chapter III: Phoebodontid chondrichthyans of the Maider

canthus (Hotton 1952), Tristychius (Coates et al. 2018, supplementary Fig. 10e, f) and also Phoebo- dus (Fig. 1a-c). 58 Ceratohyal anteriorly blade-shaped: absent (0), present (1). The ceratohyal is a simple slightly curved, uniformely thick, rod-shaped cartilage in Recent and fossil chondrichthyans. Fossil examples are e.g. Akmonistion (Coates & Sequeira, 2001a), Denaea (Williams, 1985), Cobelodus (Zangerl & Case, 1976), Triodus (Heidtke et al., 2004) and Gladbachus (Coates et al., 2018). However, in Tristy- chius (pers. obs. MC) and Phoebodus, the ceratohyal exhibits a derived shape with the anteriormost portion laterally expanding. This is apparently not the condition in the phoebodont Thrinacodus, in which the ceratohyal shows a non-derived shape (Grogan & Lund, 2008, fi g. 10C). But because of the fl attened preservation of the Thrinacodus specimens, the character was coded as non-applicable. 59 Hypohyals: absent (0); present (1). Friedman & Brazeau (2010); Pradel et al. (2014). Present in osteichthyans and some Paleozoic chondrichthyans including Cobelodus, Akmonistion (Coates & Se- queira 2001a), Triodus (Heidtke et al. 2004; Hampe 2002, fi g. 18), Orthacanthus (Heidtke 1999, fi g. 7c) and possibly Falcatus (Lund 1985, fi g. 8b). Hypohyals were reconstructed for Thrinacodus gracia (Grogan & Lund 2008, fi g. 10C) while they are absent in Phoebodus (Fig. 1c), which corresponds to the condition in other chondrichthyans such as Gladbachus (Coates et al. 2018) and Tristychius (Coates & Tietjen 2018). In Acanthodes and stem group gnathostomes, hypohyals seem to be absent. 60 Basihyal absent, hyoid arch articulates directly with basibranchial (0); basihyal present (1). Pradel et al. (2014); see also discussion in Carr et al. (2009); Brazeau et al. (2017). In osteichthyans, basihyals are rarely present and therefore, the hyoid arch articulates directly with basibranchials like in Acanthodes (Nelson 1968; Miles 1973b; Gardiner 1984). Basihyals are known from a variety of placoderms (Long 1997; Carr et al. 2009; Brazeau et al. 2017), and early and modern chondrichthyans (Zangerl &Case 1973, 1976; Maisey 1983; Didier 1995; see discussion in data matrix of Coates et al. 2018). In phoebodont chondrichthyans the basihyal is preserved in Phoebodus while it seems to be absent in Thrinacodus (Grogan & Lund 2008). 61 Separate supra- and infra-pharyngobranchials absent (0); present (1). Gardiner (1984); Pradel et al. (2014). Absent in many early gnathostome taxa such as Halimacanthodes, Acanthodes, Glad- bachus, Debeerius, Tristychius, hybodontids, and Triodus. Present in osteichthyans, but also in the chondrichthyan Ozarcus (Pradel et al. 2014). 62 Pharyngobranchials directed anteriorly (0); posteriorly (1). Pradel et al. (2014). Pharyngobran- chials are anteriorly directed in osteichthyans whereas in most chondrichthyans they are directed pos- teriorly. Among Paleozoic chondrichthyans posteriorly directed pharyngobranchials are known from e.g., Orthacanthus, Triodus, Debeerius, Tristychius and Falcatus (Coates et al. 2018, Lund 1985, fi g. 6). As exceptions, Gladbachus (Coates et al. 2018) and Ozarcus (Pradel et al. 2014) exhibit anteriorly directed pharyngobranchial elements. Pharyngobranchials are not known from Phoebodus yet. 63 Posteriormost branchial arch bears epibranchial unit: absent (0); present (1). Coates et al. (2018). Absent in osteichthyans; present in chondrichthyans, Gladbachus and Acanthodes (Davis et al. 2012; Pradel et al. 2014). 64 Epibranchials bear posterior fl ange: absent (0); present (1). Coates et al. (2018). Present in Acan- thodes (Coates et al. 2018, supplementary Fig. 9di), Gladbachus (Coates et al. 2018, supplementary Fig. 9dii), Halimacanthus (Burrow et al. 2012) and Ozarcus (Pradel et al. 2014). 65 Hypobranchials directed anteriorly (0); hypobranchials of second and more posterior gill arches directed posteriorly (1). Coates et al. (2018). Hypobranchials are common in early osteichthyans and chondrichthyans but also in Acanthodes . Posteriorly directed: crown-chondrichthyans, xenacan- thids (Hampe 2002; Heidtke et al. 2004) and hybodontids. Anteriorly directed: Ozarcus and Falcatus (Coates et al. 2018).

Dentition & tooth-bearing bones and cartilages 66 Oral dermal tubercles borne on jaw cartilages: absent (0); present (1). Hanke & Wilson (2004); Brazeau (229); Davis et al. (2012); Zhu et al. (2013). 67 Pharyngeal teeth or denticles: absent (0); present (1). Commen feature in most early gnathostomes except for placoderms. In early chondrichthyans: often small whorls on a fused base (Zangerl & Case 1976; Coates & Sequeira 2001a). Other shapes/arrangements of pharyngeal teeth are present in the hybodontid Hamiltonichthys (Maisey 1989) and Tribodus (Lane & Maisey 2012, Figs 4.1, 5). Disar- ticulated specimens are preserved in Phoebodus. 68 Tooth families/whorls: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau

121 Chapter III: Phoebodontid chondrichthyans of the Maider

(2009); Davis et al. (2012); Zhu et al. (2013). 69 Bases of tooth families/whorls: single, continuous plate (0); some or all whorls consist of sepa- rate tooth units (1). Adjusted by Coates et al. (2018) from Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Giles et al. (2015). 70 Lingual torus: absent (0); present (1). After Ginter et al. 2010; Coates et al. (2018). Present in most Palaeozoic chondrichthyans, exception: holocephalans with tooth plates. 71 Basolabial shelf: absent (0); present (1). After Ginter et al. (2010): The basolabial shelf at the tooth base articulates with the tooth crown of the overlying tooth of the same tooth family. Common feature in Palaeozoic chondrichthyans. 72 Tooth families/whorls restricted to symphysial region (0); distributed along jaw margin (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). Character score ´1` is likely a synapomorphic condition of chondrichthyans (Tucker and Fraser 2014, Coates et al. 2018). 73 Number of tooth families/whorls per jaw ramus: 15 or fewer (0); 20 or more (1). Coates et al. (2018). Character not applicable in Phoebodus because dentition is mostly disarticulated and/or not complete. 74 Toothplates absent (0); present (1). Follows defi nition of Coates et al. (2018): tooth plates are de- fi ned by fused adjacent tooth families. 75 Toothplate complement restricted to two pairs in the upper jaw and a single pair in the lower jaw: absent (0); present (1). After Patterson (1965); Coates et al. (2018). 76 Mandibular teeth fused to dermal plates on biting surfaces of jaw cartilages: absent (0); present (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 77 Dermal plates on biting surface of jaw cartilages: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Giles et al. (2015c). 78 Gnathal plates mesial to and/or above (or below) jaw cartilage: absent (0); present (1). Zhu et al. (2016). 79 Maxilla and premaxilla sensu stricto (upper gnathal plates lateral to jaw cartilage without pala- tal lamina): absent (0); present (1). Zhu et al. (2016). 80 Dentary bone encloses mandibular sensory canal: absent (0); present (1). Gardiner (1984) and references therein; Zhu et al. (2009, 2013). 81 Infradentary foramen and groove, series: absent (0); present (1). Zhu et al. (2010). 82 Tooth-bearing median rostral: absent (0); present (1). Zhu et al. (2009, 2013). 83 Median dermal bone of palate (parasphenoid): absent (0); present (1). Gardiner (1984); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 84 Denticulated fi eld of parasphenoid: without spiracular groove (0); with spiracular groove (1). Friedman (2007); Zhu et al. (2009, 2013). 85 Denticle fi eld of parasphenoid with multifi d anterior margin: absent (0); present (1). Friedman (2007); Zhu et al. (2009, 2013); Lu et al. (2016).

Mandibular arch 86 Large otic process of the palatoquadrate: absent (0); present (1). Coates & Sequeira (2001a); Davis (2002); Brazeau (2009); Zhu et al. (2009, 2013). In Paleozoic chondrichthyans, the palatoquad- rate is usually cleaver-shaped with a dorsoventrally large otic process. Examples are xenacanthids (Schaeffer 1981), symmoriiforms (Coates and Sequeira, 2001a, Zangerl 1981) and cladoselachians (Zangerl 1981). The otic process of Phoebodus shows a derived short shape (Fig. 1a-c). This contrasts the condition in Thrinacodus, in which the palatoquadrate appears to be higher (Grogan & Lund 2008, fi g. 10B). In hybodontids, the otic process is short but the quadrate expands laterally to form a deep adductor fossa (Maisey 1982). 87 Oblique ridge or groove along medial face of palatoquadrate: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Lu et al. (2016). Present in Acanthodes and chondrich- thyans such as Gladbachus and Orthacanthus. 88 Fenestration of palatoquadrate at basipterygoid articulation: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Lu et al. (2016). 89 Perforate or fenestrate anterodorsal (metapterygoid) portion of palatoquadrate: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 90 Articulation surface of the palatoquadrate with the postorbital process directed anteriorly (0); laterally (1); dorsally (2). Coates et al. (2017). Character varies among early gnathostomes and even

122 Chapter III: Phoebodontid chondrichthyans of the Maider

within the chondrichthyans: e.g. anteriorly in Acanthodes, Orthacanthus, Tamiobatis and Phoebodus; laterally (or anterolaterally) in Cobelodus and Akmonistion; dorsally in Tristychius. 91 Palatoquadrate fused to the neurocranium: absent (0); present (1). Coates et al. (2017). 92 Pronounced dorsal process on Meckelian bone or cartilage: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 93 Mandibular mesial process: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). Synonyms of the mandibular mesial process are mandibular knob, preglenoid articular process, or mandibular condyle. It describes the auxiliary articular facet of the double jaw articulation in chondrichthyans (Hotton 1952; Maisey 1989a; Lane & Maisey 2012). 94 Jaw articulation located on rearmost extremity of mandible: absent (0); present (1). Davis et al. (2012); Zhu et al. (2013). 95 Dental sulcus (trough) adjacent to oral rim on Meckel’s cartilage and palatoquadrate: absent (0); present (1). Coates et al. (2017). Characteristic feature of chondrichthyans, but absent in Glad- bachus as well as in holocephalans having toothplates. This character is not present in Phoebodus. 96 Scalloped oral margin on Meckel’s cartilage and palatoquadrate: absent (0); present (1). Coates et al. (2017). Characteristic of some symmoriiform chondrichthyans such as Akmonistion, Ozarcus, and Cladoselache, but also present in Helodus (pers. obs. MIC). 97 Mandibular symphysis fused: absent (0); present (1). Coates et al. (2017).

Neurocranium 98 Internasal vacuities: absent (0); present (1). Lu et al. (2016). 99 Precerebral fontanelle: absent (0); present (1). Schaeffer (1981); Lund & Grogan (1997); Coates & Sequeira (1998, 2001a, b); Maisey (2001a); Brazeau (2009); Pradel et al. (2011) Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 100 Space for forebrain and (at least) proximal portion of olfactory tracts narrow and elongate, extending between orbits: absent (0); present (1). Coates et al. (2017). 101 Prominent, pre-orbital, rostral expansion of the neurocranium: present (0); absent (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). Present in chimaeroids (Giles et al. 2015c). 102 Rostral bar: absent (0); present (1). Adapted from Maisey (1985); Coates et al. (2017). 103 Internasal groove absent (0); present (1). Coates et al. (2017); present in Iniopera and Dwykasela- chus (Pradel 2010). 104 Orbitonasal lamina dorsoventrally deep: absent (0); present (1). Patterson (1965); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2017). Present in chimaeroids and some Palaeozoic holoceph- alans including Debeerius, Chondrenchelys, and Helodus (Coates et al. 2018). 105 Palatobasal (or orbital) articulation posterior to the optic foramen (0); anterior to the optic foramen, grooved, and overlapped by process or fl ange of palatoquadrate (1); anterior to optic foramen, smooth, and overlaps or fl anks articular surface on palatoquadrate (2). Adapted by Coates et al. (2018) from Pradel et al. (2011, character 26), Coates et al. (2017, character 71) and Maisey (2005, p.61) 106 Trochlear nerve foramen anterior to optic nerve foramen: absent (0); present (1). Coates & Se- queira (2001). Characteristic in hybodontids, absent in Tristychius (Coates & Tietjen 2018). 107 Supraorbital shelf broad with convex lateral margin: absent (0); present (1). Coates & Sequeira (1998); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 108 Orbit directed mostly laterally and free of fl anking endocranial cartilage or bone: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Coates et al. 2018). 109 Interorbital space broad (0); narrow (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2017). 110 Optic pedicel: absent (0); present (1). Dupret et al. (2014); Zhu et al. (2009, 2013); Coates et al. (2017). 111 Ophthalmic foramen in anterodorsal extremity of orbit communicates with cranial interior: absent (0); present (1). Coates et al. (2017). 112 Extended prehypophysial portion of sphenoid: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 113 Canal for efferent pseudobranchial artery within basicranial cartilage: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 114 Entrance of internal carotids: through separate openings fl anking the hypophyseal opening or

123 Chapter III: Phoebodontid chondrichthyans of the Maider

recess (0); through a common opening at the central midline of the basicranium (1). Schaeffer (1981); Coates & Sequeira (1998); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 115 Internal carotids: entering single or paired openings in the basicranium from a posterolateral angle (0); entering basicranial opening(s) head-on from an extreme, lateral angle (1); absent (2). Coates et al. (2017). 116 Ascending basisphenoid pillar pierced by common internal carotid: absent (0); present (1). Miles (1973b); Brazeau (2009); Friedman & Brazeau (2010); Davis et al. (2012); Zhu et al. (2013). 117 Spiracular groove on basicranial surface: absent (0); present (1). Davis et al. (2012); Zhu et al. (2013). 118 Spiracular groove on lateral or transverse wall of jugular canal: absent (0); present (1). Davis et al. (2012); Zhu et al. (2013). 119 Spiracular groove open (0); enclosed by spiracular bar or canal (1). Lu et al. (2016), Coates et al. (2018). 120 Orbit larger than otic capsule: absent (0); present (1). Lund & Grogan (1997); Coates et al. (2017). 121 Postorbital process and arcade: absent (0); present (1). Pradel et al. (2011); see also Maisey (2007) and Coates et al. (2017). Character absent in crown group elasmobranchs (Coates et al. 2018). 122 Postorbital process and arcade short and deep - width not more than maximum braincase width (excluding arcade) (0); process and arcade wide - width exceeds maximum width of braincase, and anteroposteriorly narrow (1); process and arcade massive (2); arcade forms postorbital pillar (3). Coates et al. (2017). 123 Postorbital process downturned, with anhedral angle relative to basicranium: absent (0); pres- ent (1). Present in hybodontids, Acronemus (Maisey 2011) and Tristychius (Dick 1978; Coates & Tietjen 2018). 124 Jugular canal diameter small (0); large (1); canal absent (2). Pradel et al. (2011); see Coates et al. (2018) for defi nition of small and large canals. 125 Canal, likely for trigeminal nerve (V) mandibular ramus, passes through the postorbital process from proximal dorsal entry to distal and ventral exit: absent (0); present (1). Present in early chondrichthyans such as Cladodoides (Maisey, 2005), Dwykaselachus (Coates et al., 2017), Ortha- canthus, Tamiobatis and Pucapampella. In the latter two taxa, the canal was initially interpreted as the branch of the palatine nerve (Schaeffer 1981; Maisey 2001) but later reinterpreted by Coates et al. (2018). Also in Acanthodes the canal was reinterpreted (Coates et al. 2018) which was formerly described as the canal for the middle cerebral vein and a branch of the lateral line nerve (Davis et al. 2012). No such canal is evident in early actinopterygians (Gardiner 1984), Janusiscus, or placoderms. 126 Postorbital process expanded anteroposteriorly: absent (0); present (1). Generally a characteristic feature of hybodontids, but absent in Tristychius (Coates et al. 2018). 127 Postorbital process articulates with palatoquadrate: absent (0); present (1). Schaeffer (1981); Coates & Sequeira (1998); Maisey (2001a); Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). Archaeostyly (Maisey 2008; here corresponding to character state ´1`) is a characteristic feature of early chondrichthyans and some acanthodians such as Acanthodes and Promesacanthus (Coates et al. 2018). In the neoselachian Synechodus, the archaeostylic condition secondarily evolved (Maisey 1985). 128 Trigemino-facial recess: absent (0); present (1). Goodrich (1930); Gardiner (1984 and references therein); Pradel (2010); Pradel et al. (2011); Davis et al. (2012). 129 Jugular canal long, extends throughout most of otic capsule wall posterior to the postorbital process (0); short and/or groove present on exterior of otic wall (1); absent, path of jugular re- moved from otic wall (2). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Giles et al. (2015c); Coates et al. (2017). 130 C-bout notch separates postorbital process from supraotic shelf: absent (0); present (1). Charac- teristic feature of Tristychius, present in Acronemus (Maisey 2011). 131 Postorbital fossa: absent (0); present (1). Zhu et al. (2013). 132 Hyoid ramus of facial nerve (N. VII) exits through posterior jugular opening: absent (0); pres- ent (1). Friedman (2007); Brazeau (2009); Friedman & Brazeau (2010); Davis et al. (2012); Zhu et al. (2013). 133 Periotic process: absent (0); present (1). Maisey (2007); Coates et al. (2017). 134 Articulation facet for hyomandibula: single-headed (0), double-headed (1). Zhu et al. (2009, 2013).

124 Chapter III: Phoebodontid chondrichthyans of the Maider

135 Relative position of jugular groove and hyomandibular articulation: hyomandibula dorsal or same level (i.e. on bridge) (0); jugular vein passing dorsal or lateral to hyomandibula (1). Brazeau & de Winter (2015). 136 Transverse otic process: absent (0); present (1). Lu et al. (2016); Giles et al. (2016) 137 Craniospinal process: absent (0); present (1). Giles et al. (2015); Lu et al. (2016). 138 Lateral otic process: absent (0); present (1). Schaeffer (1981); Coates & Sequeira (1998); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). The lateral otic process projects far posteriorly from the otic region and it connects the hyomandibula to the braincase (Schaeffer 1981; Coates & Sequeira 1998). Such a process is well-known from Orthacanthus and Tamiobatis. The character is currently coded as ´0` in Akmonistion, because the “short, posterolateral angle” of the otic differs reasonably in shape from the lateral otic process in Orthacanthus and Tamiobatis (Coates et al., 2018). In Clado- doides (Maisey 2005) as well as in Phoebodus, lateral projections from the otic capsular wall are completely absent. 139 Hyomandibula articulates with neurocranium beneath otic shelf: absent (0); present (1). 140 Sub-otic occipital fossa: absent (0); present (1). Coates et al. (2017, 2018). See Schaeffer (1981; p. 15, fi g. 6, occipital view): concavity underneath the lateral otic process. The feature is present in Orthacanthus and Tamiobatis (Schaeffer 1981), but not in Cladodoides which has a similar braincase (Maisey 2005). For Phoebodus, the character was coded as inapplicable but it is most probably absent. 141 Postotic process: absent (0); present (1). Pradel et al. (2011); Coates et al. (2017). 142 Otic capsule extends posterolaterally relative to occipital arch: absent (0); present (1). Maisey (1985). 143 Otic capsules: widely separated (0); approaching dorsal midline (1). Coates et al. (2017). 144 Otic capsules project anteriorly between postorbital processes: absent (0); present (1). Present in neoselachians (Maisey 1983) and probably in some early elasmobranchs, e.g., Acronemus (Maisey 2011). 145 Endocranial roof anterior to otic capsules dome-like, smoothly convex dorsally and anteriorly: absent (0); present (1). Coates et al. (2017). 146 Roof of skeletal cavity for cerebellum and mesencephalon signifi cantly higher than dorsal-most level of semicircular canals: absent (0); present (1). Coates et al. (2017). 147 Roof of the endocranial space for telencephalon and olfactory tracts offset ventrally relative to level of mesencephalon: absent (0); present (1). Coates et al. (2017). 148 Labyrinth cavity separated from the main neurocranial cavity by a cartilaginous or ossifi ed capsular wall (0); skeletal medial capsular wall absent (1). Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). 149 Double octaval nerve foramena in chondrifi ed mesial wall of otic capsule: absent (0); present (1). Present in Tribodus and Egertonodus (Lane 2010); absent in chondrichthyans exhibiting a medial capsular wall (e.g Tristychius; Coates & Tietjen 2018). 150 External (horizontal) semicircular canal joins the vestibular region dorsal to posterior ampulla (0); joins level with posterior ampulla (1). Davis et al. (2012); Zhu et al. (2013). 151 Angle of external semicircular canal: in lateral view, straight line projected through canal in- tersects anterior ampulla, external ampullae, and base of foramen magnum: absent (0); present (1). Coates et al. (2017). 152 Left and right external semicircular canals approach or meet the posterodorsal midine of the hindbrain roof: absent (0); present (1). Coates et al. (2017). 153 Preampullary portion of posterior semicircular canal absent (0); present (1). Coates et al. (2017). Known from crown chondrichthyans (Daniel 1922; Maisey 2001b; Maisey & Lane 2010). 154 Crus commune connecting anterior and posterior semicircular canals present (0); absent (1). Coates et al. (2017). A crus commune is present in most early chondrichthyan groups (e.g. Coates et al. 2017, Maisey 2005, 2007, Schaeffer 1981). However, some hybodontids show a derived condition (posterior and anterior semicircular canals are separated from each other) such as in modern elasmo- branchs (Daniel 1922, Maisey 2001b, Maisey and Lane 2010, Pradel et al. 2011). 155 Sinus superior: absent or indistinguishable from union of anterior and posterior canals with saccular chamber (0); present, elongate and nearly vertical (1). Davis et al. (2012); Zhu et al. (2013). 156 Lateral cranial canal: absent (0); present (1). Zhu et al. (2009, 2013); Lu et al. (2016). Character is present in early actinopterygians (Gardiner 1984; Coates 1998) and a putative stem osteichthyan

125 Chapter III: Phoebodontid chondrichthyans of the Maider

(Basden et al. 2000). 157 Endolymphatic ducts: posteriodorsally angled tubes (0); tubes oriented vertically through endo- lymphatic fossa/posterior dorsal fontanelle (1). Schaeffer (1981); Coates & Sequeira (1998, 2001); Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 158 Posterior dorsal fontanelle connected to persistent otico-occipital fi ssure (0); posterior tectum separates fontanelle from fi ssure (1). Schaeffer (1981); Coates & Sequeira (1998); Pradel et al. (2011). 159 Subcircular endolymphatic foramen: absent (0); present (1). Pradel et al. (2015), Coates et al. 2017. Character was renamed from subcircular endolymphatic fossa to subcircular endolymphatic foramen by Coates et al. (2017). It was suggested as a holocephalan synapomorphy (Maisey & Lane 2010). 160 External opening for endolymphatic ducts anterior to crus commune: absent (0); present (1). Coates et al. (2017). 161 Supraotic shelf broad: absent (0); present (1). Present in Tristychius and Acronemus (Maisey 2011). 162 Dorsal otic ridge: absent (0); present (1). Coates & Sequeira (1998, 2001); Maisey (2001); Davis (2002); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 163 Dorsal otic ridge forms a crest posteriorly: absent (0); present (1). Coates & Sequeira (1998, 2001); Pradel et al. (2011). 164 Endolymphatic fossa: absent (0); present (1). Pradel et al. (2011). 165 Endolymphatic fossa elongate (slot-shaped), dividing dorsal otic ridge along midline: absent (0); present (1). Coates et al. (2017). 166 Perilymphatic fenestra within the endolymphatic fossa: absent (0); present (1). Pradel et al. (2011); Coates et al. (2017). 167 Ventral cranial fi ssure: absent (0); present (1). Janvier (1996); Coates & Sequeira (2001); Maisey (2001); Davis (2002); Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). 168 Endoskeletal intracranial joint: absent (0); present (1). Janvier (1996); Davis et al. (2012); Zhu et al. (2013). 169 Metotic (otic-occipital) fi ssure: absent (0); present (1). Schaeffer (1981); Janvier (1996); Coates & Sequeira (1998); Maisey (2001); Davis (2002); Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). 170 Vestibular fontanelle: absent (0); present (1). Brazeau (2009); Friedman & Brazeau (2010). Davis et al. (2012); Zhu et al. (2013). 171 Hypotic lamina: absent (0); present (1). Schaeffer (1981); Maisey (1984, 2001); Brazeau (2009); Pradel et al. (2011, 2013); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2017). 172 Glossopharyngeal nerve path: directed laterally, across fl oor of the saccular chamber and exits via foramen in side wall of the otic capsule (0); directed posteriorly, and exits through metotic fi ssure or foramen in posteroventral wall of otic capsule (1); exits laterally through a canal con- tained ventrally (fl oored) by the hypotic lamina (2); exits through a foramen anterior to the pos- terior ampulla (3). Coates et al. (2017), adapted from Schaeffer (1981); Coates & Sequeira (1998, 2001); Brazeau (2009): Davis et al. (2012); Zhu et al. (2013); Pradel et al. (2011, 2013). 173 Glossopharyngeal and vagus nerves share common exit from neurocranium: absent (0); present (1). Uniquely present in hybodontids such as Egertonodus and Tribodus. 174 Basicranial morphology: platybasic (0); tropibasic (1). Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). Defi nition of tropibasic versus platybasic: see Maisey (2007) and Pradel et al (2011). 175 Channel for dorsal aorta and/or lateral dorsal aortae passes through basicranium (0): exter- nal to basicranium (1). Schaeffer (1981); Coates & Sequeira (1998); Brazeau (2009); Pradel et al. (2011); Brazeau & Friedman (2014); Coates et al. (2017). 176 Dorsal aorta divides into lateral dorsal aortae posterior to occipital level (0); anterior to level of the occiput (1). Pradel et al. (2011); Giles et al. (2015); Coates et al. (2017). 177 Ventral portion of occipital arch wedged between rear of otic capsules: absent (0); present (1). Schaeffer (1981); Coates & Sequeira (1998); Maisey (2001a); Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Coates et al. (2017). 178 Dorsal portion of occipital arch wedged between otic capsules: absent (0); present (1). Schaeffer (1981); Coates & Sequeira (1998); Maisey (2001a); Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Coates et al. (2017).

126 Chapter III: Phoebodontid chondrichthyans of the Maider

179 Occipital crest anteroposteriorly elongate, and extends from the roof of the posterior tectum: absent (0); present (1). The elongate condition (posterior tectum to the level of foramen magnum) is present in Callorhinchus and in the Palaeozoic chondrichthyans Kawichthys (Pradel et al. 2011, fi g. 5) and Iniopera (Pradel 2010, fi g. 5) (see Finarelli & Coates 2014). In contrast, Dwykaselachus, Akmonistion and FMNH PF 13242 (Maisey 2007, fi g. 7), show an anteroposteriorly short occipital crest (not exceeding the level of the anterior margin of the occipital fi ssure). The character is coded as ´absent` in Phoebodus, Orthacanthus, Triodus and hybodontids because their occipital crests extend from the occipital arch wedged between the otic capsules (Schaeffer 1981; Maisey 1982).

Axial and appendicular skeleton 180 Calcifi ed vertebral centra: absent (0); present (1). Maisey (1985): biconcave calcifi ed vertebral centra are absent in Palaeozoic chondrichthyans and therefore this character is suggested as a synapo- morphy of crown elasmobranchs (Coates et al. 2017). 181 Chordacentra: absent (0); present (1). Stahl (1999); Coates and Sequeira (2001); Coates et al. (2017). Known in Chondrenchelys (Finarelli & Coates 2014), Damocles (Lund 1986; CM 48760), Falcatus (Lund 1985) and in the caudalis of Akmonistion (Coates & Sequeira 2001). 182 Chordacentra polyspondylous and consist of narrow closely packed rings: absent (0); present (1). Derived from Patterson (1965); Coates et al. (2017). 183 Synarcual: absent (0); present (1). Stahl (1999); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2017). 184 Macromeric dermal pectoral girdle (0); micromeric or lacking dermal skeleton entirely (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 185 Macromeric dermal pectoral girdle composition: ventral and dorsal components (0); ventral components only (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 186 Macromeric pectoral dermal skeleton forms complete ring around the trunk: present (0); ab- sent (1). Goujet & Young (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 187 Median dorsal plate: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 188 Scapular process (dorsal) of shoulder endoskeleton: absent (0); present (1). Coates & Sequeira (2001a); Zhu & Schultze (2001); Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 189 Ventral margin of separate scapular ossifi cation: horizontal (0); deeply angled (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 190 Cross sectional shape of scapular process: fl attened or strongly ovate (0); subcircular (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 191 Flange on trailing edge of scapulocoracoid: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 192 Scapular process with posterodorsal process: absent (0); present (1). Coates & Sequeira (2001a); Davis et al. (2012); Zhu et al. (2013). 193 Mineralisation of internal surface of scapular process: mineralised all around (0); un-min- eralised on internal face forming a hemicylindrical cross-section. Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 194 Coracoid process: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 195 Procoracoid mineralisation: absent (0); present (1). Davis (2002); Hanke & Wilson (2004): Brazeau (2009). 196 Fin base articulation on scapulocoracoid: stenobasal, deeper than wide (0); eurybasal, wider than deep (1). Lu et al. (2016). 197 Pectoral fi n articulation monobasal (0); dibasal (1); three or more basals (2). 198 Metapterygium pectinate subtriangular plate or bar supporting numerous (six or more) radials along distal edge: absent (0); present (1). Present in symmoriiforms and Diplodoselache. 199 Metapterygial whip: absent (0); present (1). Coates et al. (2017). 200 Biserial pectoral fi n endoskeleton: absent (0); present (1). Lu et al. (2016). 201 Propterygium perforated: absent (0); present (1). Rosen et al. (1981); Patterson (1982); Davis et al. (2012); Zhu et al. (2013). 202 Pelvic girdle with fused puboischiadic bar: absent (0); present (1). Maisey (1984); Coates & Se- queira (2001a); Coates et al. (2017). 203 Mixipterygial/mixopterygial claspers: absent (0), present (1). Coates & Sequeira (2001a,b);

127 Chapter III: Phoebodontid chondrichthyans of the Maider

Brazeau & Friedman (2014). 204 Pre-pelvic clasper or tenaculum: absent (0); present (1). After Patterson (1965); Coates et al. (2017). 205 Number of dorsal fi ns, if present: one (0); two (1); one, extending from pectoral to anal fi n level (2). Coates & Sequeira (2001a); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 206 Brush complex of bilaterally distributed calcifi ed tubes fl anking or embedded in calcifi ed carti- lage core: absent (0); present (1). Coates et al. (2017, 2018); description of Brush complex in Lund (1985) and Coates et al. (1998). The rod-like structure in Falcatus and the brush complex in Akmonis- tion are homologous (Maisey 2009; Coates et al. 2018) 207 Posterior or pelvic-level dorsal fi n with calcifi ed base plate: absent (0); present (1). Coates & Sequeira (2001a, b). Present in Tristychius, hybodontids, and “Ctenacanthus”. Character was coded with state ´1` for Phoebodus because the specimen shows remains of cartilage ventrally to the dorsal fi n spine. 208 Posterior dorsal fi n with delta-shaped cartilage: absent (0); present (1). Coates & Sequeira (2001a, b). Present in many symmoriid taxa; absent in Cladoselache. 209 Posterior or pelvic-level dorsal fi n shape, base approximately as broad as tall and not broader than other median fi ns (0); base much longer than fi n height, substantially longer than other median fi ns (1). Brazeau & deWinter (2015); Lu et al. (2017). 210 Anal fi n: absent (0); present (1). Coates & Sequeira (2001); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 211 Anal fi n base narrow, posteriormost proximal segments radials broad: absent (0); present (1). Heidtke (1999). Present in xenacanthids, exception: Diplodoselache. 212 Caudal radials restricted to axial lobe (0); extend beyond level of body wall and deep into hypo- chordal lobe (1). Davis et al. (2012); Zhu et al. (2013). 213 Caudal neural and/or supraneural spines or radials short (0); long, expanded, and supporting high aspect-ratio (lunate) tail with notochord extending to posterodorsal extremity (1); noto- chord terminates pre-caudal extremity, neural and heamal radial lengths near symmetrical and support epichordal and hypochordal lobes respectively (2). Coates & Sequeira (2001a, b).

Spines: fi ns, cranial and elsewhere 214 Dorsal fi n spine or spines: absent (0); present (1). Zhu et al. (2001); Zhu & Yu (2002); Friedman (2007); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Lu et al. (2016). 215 Dorsal fi n spine at anterior (pectoral level) location only: absent (0); present (1). Coates & Sequei- ra (2001a); Ginter et al. (2010). This character has been coded inapplicable in taxa having a continu- ous dorsal fi n extending throughout trunk length (Coates et al. 2017, 2018). 216 Dorsal fi n spine cross section: horseshoe shaped (0); fl at sided, with rectangular profi le (1); sub- circular (2). Hampe (2002); Brazeau & de Winter (2015). 217 Anterior dorsal fi n spine leading edge concave in lateral view: absent (0); present (1). This char- acter is present in chondrichthyan genera in which fi n spines form derived shapes such as brush com- plexes or hook-like extensions. Examples are mostly symmoriids such as Akmonistion, Falcatus and Damocles but also Physonemus, which is a taxon based on fi n spines (Lund 1985, 1986). However, such fi n spines are known from males only and they are probably absent in females (Lund 1985; Maisey 2009). Therefore, the usefulness of this character is still challenged (Coates et al. 2018). 218 Anal fi n spine: absent (0); present (1). Maisey (1986); Davis (2002); Brazeau (2009). 219 Pectoral fi n spines: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 220 Pectoral fi n spine with denticles along posterior surface: absent (0); present (1). Burrow et al. (2016). 221 Prepectoral fi n spines: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). Present in Doliodus (Maisey et al. 2017). 222 Admedian pectoral spines absent (0); present (1). Burrow et al. (2016); see also description of Doliodus pectoral girdle (Maisey et al. 2017). 223 Median fi n spine insertion: shallow, not greatly deeper than dermal bones/ scales (0); deep (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009). Davis et al. (2012); Zhu et al. (2013). 224 Intermediate (pre-pelvic) fi n spines: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). Pre-pelvic spines are generally absent in early

128 Chapter III: Phoebodontid chondrichthyans of the Maider

and recent chondrichthyans. Doliodus is an exception (Maisey et al. 2017). 225 Fin spines with ridges: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 226 Fin spines with nodes: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009). Davis et al. (2012); Zhu et al. (2013). 227 Fin spines (dorsal) with rows of large denticles: absent (0); on posterior surface (1); on lateral surface (2). Maisey (1989b); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 228 Cephalic spines: absent (0); present (1). Maisey (1989); Coates et al. (2017)

crossopterygian from Yunnan, south-western China. Doctor- 5) References al dissertation, Department of Geology, Stockholm University Arratia, G. & Cloutier, R. in Devonian Fishes and Plants of Migua- (1982). sha, Quebec, Canada (eds. Schultze, H.-P. & Cloutier, R.) 165- Chang, M. M. Head exoskeleton and shoulder girdle of Youngole- 197 (Verlag Dr. Friedrich Pfeil, Munich, 1996). pis. In Early vertebrates and related problems of evolutionary Agassiz, L. J. R. Recherches sur les poissons fossiles. 3, viii+390+32 biology, M. M. Chang, Y. H. Liu & G. R. Zhang, eds. (Beijing: pp. Petitpierre, Neuchâtel et Soleure (1843B, 1937-1843). Science Press), pp. 355-378 (1991). Basden, A. M., Young, G. C., Coates, M. I. & Ritchie, A. The most Chang, M. M. Synapomorphies and scenarios - more characters of primitive osteichthyan braincase? Nature 403, 185-188 (2000). Youngolepis betraying its affi nity to the Dipnoi. In Recent Ad- Bendix-Almgreen, S. E. The paired fi ns and shoulder girdle in vances in the Origin and Early Radiation of Vertebrates, G. Ar- Cladoselache, their morphology and phyletic signifi cance. ratia, M. V. H. Wilson & R. Cloutier, eds. (München: Verlag Dr. Colloques Internationaux du Centre National de la Recherche Friedrich Pfeil), pp. 665-686 (2004). Scientifi que 218, 111-123 (1975). Chang, M.-M. & Yu, X.-B. A new crossopterygian, Youngolepis Bernacsek, G.M., & Dineley, D.L. New acanthodians from the De- praecursor, gen. et sp. nov., from Lower Devonian of E. Yun- lorme Formation (Lower Devonian) of N.W.T., Canada. Paleon- nan, China. Sci. Sin. 24, 89-97 (1981). tographica Abt.A 158, 1-25 (1977). Choo, B. Revision of the actinopterygian genus Mimipiscis (= Bonaparte, C. L. J. L. Iconografi a della fauna italica per le quatro Mimia) from the Upper Devonian Gogo Formation of West- classi degli animali vertebrati. Tomo III : Pesci. 266 pp. (Salvi- ern Australia and the interrelationships of early Actinopterygii. ucci), Roma (1838B). Earth and Environmental Science Transactions of the Royal So- Brazeau, M. D. The braincase and jaws of a Devonian ‘acanthodian’ ciety of Edinburgh, 102: 77-104 (2011) and modern gnathostome origins. Nature 457, 305-308 (2009). Coates, M. I. Actinopterygians from the Namurian of Bearsden, Brazeau, M. D. A revision of the anatomy of the early Devonian Scotland, with comments on the early evolution of actinoptery- jawed vertebrate Ptomacanthus anglicus Miles. Palaeontology gian neurocrania. Zool. J. Linn. Soc. 122, 27-59. (1998). 55, 355-367 (2012). Coates, M.I., Finarelli, J.A., Sansom, I.J., Andreev, P.S., Criswell, Brazeau, M. D. & Friedman, M. The characters of Palaeozoic jawed K.E., Tietjen, K., Rivers, M.L., La Riviere, P.J. An early chon- vertebrates. Zoological Journal of the Linnean Society, 170, drichthyan and the evolutionary assembly of a shark body plan. 779-821 (2014). Proceedings of the Royal Society B 285: 20172418. (2018) Brazeau, M. D. & de Winter, V. The hyoid arch and braincase anato- http://dx.doi.org/10.1098/rspb.2017.2418 my of Acanthodes support chondrichthyan affi nity of ‘acantho- Coates, M. I., Gess, R. W., Finarelli, J. A., Criswell, K. E. & Tietjen, dians’. Proc. R. Soc. B 282: 20152210 (2015). K. A symmoriiform chondrichthyan braincase and the origin of Brazeau, M. D., Friedman, M., Jerve, A., & Atwood, R. C. A chimaeroid fi shes. Nature 541, 209-211 (2017). three-dimensional placoderm (stem-group gnathostome) pha- Coates, M. I., Sansom, I. J. & Smith, M. M. Spines and tissues of ryngeal skeleton and its implications for primitive gnathostome ancient sharks. Nature 396, 729-730 (1998). pharyngeal architecture. Journal of Morphology. DOI: 10.1002/ Coates, M. I. & Sequeira, S. E. K. The braincase of a primitive shark. jmor.20706 (2017). Trans. R. Soc. Edinb. (Earth Sci.) 89, 63-85 (1998). Burrow, C. J. A new lophosteiform (Osteichthyes) from the Lower Coates, M. I. & Sequeira, S. E. K. A new stethacanthid chondrich- Devonian of Australia. Geobios M. S. 19, 327-333 (1995). thyan from the Lower Carboniferous of Bearsden, Scotland. J. Burrow, C. J. A partial articulated acanthodian from the Silurian Vertebr. Paleontol. 21, 754-766 (2001a). of New Brunswick, Canada. Can. J. Earth Sci 48, 1329-1341 Coates, M. I. & Sequeira, S. E. K. in Major Events in Early Verte- (2011). brate Evolution (ed. Ahlberg, P. E.) 241-262 (Taylor and Fran- Burrow, C. J., den Blaauwen, J., Newman, M. & Davidson, R. The cis, 2001b). diplacanthid fi shes (Acanthodii, Diplacanthiformes, Diplacan- Coates, M. I. & Tietjen, K. The neurocranium of the Lower Car- thidae) from the Middle Devonian of Scotland. Palaeontologica boniferous shark Tristychius arcuatus (Agassiz, 1837). Earth Electronica 19, 1-83 (2016). and Environmental Science Transactions of the Royal Society Burrow, C. J. & Rudkin, D. Oldest near-complete acanthodian: of Edinburgh (2018). the fi rst vertebrate from the Silurian Bertie formation konser- Cole, F. J. On the cranial nerves of Chimaera monstrosa (Linn.); with vat-Lagerstätte, Ontario. PLoS ONE 9(8), DOI:10.1371/journal. a discussion of the lateral line system and of the morphology of pone.0104171 (2014). the chorda tympani. Trans. R. Soc. Edinb. 38, 631-680 (1896). Burrow, C. J., Trinajstic, K. & Long, J. First acanthodian from the Daniel, J. F. The Elasmobranch Fishes (Univ. California Press, Upper Devonian (Frasnian) Gogo Formation, Western Austra- Berkeley, 1922). lia. Historical Biology 24, DOI:10.1080/08912963.2012.66015 Davis, S. P. Comparative anatomy and relationships of the acanthodi- 0 (2012). an fi shes. Unpublished PhD thesis, Unv. London, 1-318. (2002). Burrow, C. J. & Turner, S. Devonian placoderm scales from Aus- Davis, S. P., Finarelli, J. A., & Coates, M. I. Acanthodes and shark- tralia. Journal of Vertebrate Paleontology 18, 677-695 (1998). like conditions in the last common ancestor of modern gnatho- Burrow, C. J. & Turner, S. A review of placoderm scales, and their stomes. Nature 486, 247-250 (2012). signifi cance in placoderm phylogeny. Journal of Vertebrate Pa- Dean, M. N. & Summers, A. P. Cartilage in the skeleton of cartilagi- leontology 19, 204-219 (1999). nous fi shes. Zoology 109,164-168 (2006). Burrow, C. J. & Turner, S. Scale structure of the putative chondrich- Dean, M. N., Mull, C. G., Gorb, S. N. & Summers, A. P. Ontogeny of thyan Gladbachus adentatus Heidtke & Krätschmer, 2001 from the tessellated skeleton: insight form the skeletal growth of the the Middle Devonian Rheinisches Schiefergebirge, Germany. round stingray Urobatis halleri. J. Anat. DOI:10.1111/j.1469- Historical Biology 25, 385-390 (2013). 7580.2009.01116x (2009). Carr, R. K., Johanson, Z. & Ritchie, A. The phyllolepid placoderm DeBeer, G. R. The Development of the Vertebrate Skull (Univ. Chi- Cowralepis mclachlani: insights into the evolution of feed- cago, 1937). ing mechanisms in jawed vertebrates. J. Morph 270, 775-804 De Beer, G. R. & Moy-Thomas, J. A. On the skull of Holocephali. (2009). Philos. Trans. R. Soc. London B. Biol. Sci. 224: 287-312 (1935). Chang, M. M. The braincase of Youngolepis, a Lower Devonian

129 Chapter III: Phoebodontid chondrichthyans of the Maider

Denison, R. in Handbook of Paleoichthyology Vol. 5 (ed. Schultze, Friedman, M. & Brazeau, M. A reappraisal of the origin and basal H.-P.) (Gustav Fischer Verlag, Stuttgart, 1979). radiation of the Osteichthyes. J. Vertebr. Paleontol. 30, 36-56 Derycke, C. Microrestes de Sélaciens et autres Vertébrés du Dévo- (2010). nien supérieur du Maroc. Bulletin du Muséum national d’His- Gans, C. & Parsons, T. S. A Photographic Atlas of Shark Anatomy toire Naturelle, Section C, Sciences de la terre, paléontologie, (Academic Press, New York, 1964). géologie, minéralogie 14(1), 15-61 (1992). Gagnier, P. Y. in Devonian Fishes and Plants of Miguasha, Quebec, Derycke, C. Paléobiodiversité des gnathostomes (chondrichthyens, Canada. (eds Schultze, H. P. & Cloutier, R.) 149-163 (Freidrich acanthodiens et actinoptérygiens) du Dévonien du Maroc (NW Pfeil, 1996). Gondwana), in: Zouhri, S. (ed), Paléontologie des vertébrés du Gagnier, P. Y., Hanke, G. F. & Wilson, M. V. H. Tetanopsyrus lin- Maroc: état des connaissance, Mémoires de la Société Géolo- doei gen. et sp. nov., an Early Devonian acanthodian from the gique de France 180, p. 624 (2017). Northwest Territories, Canada. Acta Geologica Polonica 49, 81- Derycke, C., Olive, S., Groessens, E., & Goujet, D. Paleogeograph- 96 (1999). ical and paleoecological constraints on Paleozoic vertebrates Gagnier, P. Y. & Wilson, M. V. H. New evidences on jaw bones and (chondrichthyans and placoderms) in the Ardenne Massif Shark jaw articulations in acanthodians. Geobios 19 (1995). radiations in the Famennian on both sides of the Palaeotethys. Gagnier, P. Y. & Wilson, M. V. H. Early Devonian acanthodians from Palaeogeography, Palaeoclimatology, Palaeoecology 414, 61- northern Canada. Palaeontology 39, 241-258 (1996a). 67 (2014). Gagnier P. Y. & Wilson M. V. H. An unusual acanthodian from Derycke, C., Spalletta, C., Perri, M. C., & Corradini, C. Famennian Northern Canada: revision of Brochoadmones milesi. Modern chondrichthyan microremains from Morocco and Sardinia. Geology 20, 235-251 (1996b). Journal of Paleontology 82(5), 984-995 (2008). Gardiner, B. G. The relationships of the palaeoniscoid fi shes, a re- Dennis, K. D. & Miles, R. S. A pachyosteomorph arthrodire from view based on new specimens of Mimia and Moythomasia from Gogo, Western Australia. Zoological Journal of the Linnean So- the Upper Devonian of Western Australia. Bull. Br. Mus. Nat. ciety 73, 213-258 (1981). Hist. (Geol.) 37, 173-428 (1984). Dick, J. R. F. On the Carboniferous shark Tristychius arcuatus Agas- Giles, S., Coates, M., Garwood, R. J., Brazeau, M. D., Atwood, R., siz from Scotland. Trans. R. Soc. Edinb. 70, 63-109 (1978). Johanson, Z. & Friedman, M. Enodskeletal structure in Cher- Dick, J. R. F. Diplodoselache woodi gen. et sp. nov., an early Car- olepis (Osteichthyes, Actinopterygii), an early ray-fi nned fi sh. boniferous shark from the Midland Valley of Scotland. Trans. R. Palaeontology 2015, DOI:10.1111/pala. 12182 (2015a). Soc. Edinb. 72, 99-113 (1981). Giles, S., Darras, L., Clément, G., Blieck, A. & Friedman, M. An ex- Dick, J. R. F. & Maisey, J. G. The Scottish Lower Carboniferous ceptionally preserved Late Devonian actinopterygian provides shark Onychoselache traquairi. Palaeontology 23, 363-374 a new model for primitive cranial anatomy in ray-fi nned fi shes. (1980). Proc. R. Soc. B 282: 20151485 (2015b). Didier, D. A. Phylogenetic systematics of extant chimaeroid fi sh- Giles, S., Friedman, M. Virtual reconstruction of endocast anatomy es (Holocephali, Chimaeroidei). Am. Mus. Novit. 3119, 1-86 in early ray-fi nned fi shes (Osteichthyes, Actinopterygii). Jour- (1995). nal of Paleontology, 88(4), 636-651 (2014). Didier, D. A., Kemper, J. M. & Ebert, D. A. in Biology of Sharks and Giles, S., Friedman, M. & Brazeau, M. D. Osteichthyan-like cranial Their Relatives (eds Carrier, J. C., Musick, J. & Heithaus, M. R.) conditions in an Early Devonian stem gnathostome. Nature 520, 97-122 (CRC Press, 2012). 82-85 (2015c). Didier, D. A., Stahl, B. J. & Zangerl R. Development and growth of Ginter, M. Late Famennian shark teeth from the Holy Cross Mts, compound tooth plates in Callorhinchus milii (Chondrichthyes, Central Poland. Acta Geologica Polonica 40, 69-81 (1990). Holocephali). Journal of Morphology 222, 73-89 (1994). Ginter, M. Late Famennian pelagic shark assemblages. Acta Geolog- Donoghue, P.C.J., & Aldridge, R. J. in Major events in early verte- ica Polonica 50(2), 369-386 (2000). brate evolution: palaeontology, phylogeny, genetics and devel- Ginter, M. Devonian sharks and the origin of Xenacanthiformes. opment. (ed Ahlberg, P. E.) 85–105 (Taylor & Francis, 2001). In: Arratia, G., Wilson, M. V. H. and Cloutier, R. (eds.), Recent Donoghue, P. C. J., Forey, P. L., & Aldridge, R. J. Conodont affi nity advances in the origin and early radiation of vertebrates. p. 473- and chordate phylogeny. Biol. Rev.75, 191-251 (2000). 486. Friedrich Pfeil, München (2004). Dupret, V., Sanchez, S., Goujet, D., Tafforeau, P. & Ahlberg, P. E. Ginter, M., Hairapetian, V. & Klug, C. Famennian chondrichthyans A primitive placoderm sheds light on the origin of the jawed from the shelves of North Gondwana. Acta Geologica Polonica vertebrate face. Nature 507, 500-503 (2014). 52(2), 169-215 (2002). Eastman, C. R. Tamiobatis vetustus: a new form of fossil skate. Ginter, M., Hampe, O. & Duffi n, C. J. Chondrichthyes: Paleozoic American Journal of Science Elasmobranchii: teeth, in: Schultze, H. (Ed.), Handbook of Pa- 4(4), 85-90 (1897A). leoichthyology, 3D, 168 p. (2010). Ebert, D. A. & Compagno, L. J. V.. Chlamydoselachus africana, a Ginter, M. & Ivanov, A. Devonian phoebodont shark teeth. Acta Pa- new species of frilled shark from southern Africa (Chondrich- laeontologica Polonica 37(1), 55-75 (1992). thyes, Hexanchiformes, Chlamydoselachidae). Zootaxa 2173, Ginter, M. & Ivanov, A. Middle/Late Devonian Phoebodont-based 1-18 (2009). ichthyolith zonation. [Zonation ichthyologique du Dévonien Finarelli, J. A. & Coates, M. I. First tooth-set outside the jaws in a moyen/supérieur fondée sur les Phoebodontes]. Geobios 19, vertebrate. Proceedings of the Royal Society of London Series 351-355 (1995). B-Biological Sciences 279, 775-779 (2012). Ginter, M. & Sun, Y. Chondrichthyan remains from the Lower Car- Finarelli, J. A. & Coates, M. I. Chondrenchelys problematica (Tra- boniferous of Muhua, southern China. Acta Palaeontologica quair, 1888) redescribed: a Lower Carboniferous, eel-like ho- Polonica 52(4), 705-727 (2007). locephalan from Scotland. Earth and Environmental Science Ginter, M. & Turner, S. The early Famennian recovery of pheobo- Transactions of the Royal Society of Edinburgh 105, 1-25 sont sharks. Acta Palaeontologica Polonica 49(2), p. 105-117 (2014). (1999). Forey, P. L. Latimeria: a paradoxical fi sh. Proc. R. Soc. London, Ser. Ginter, M. & Turner, S. The middle Paleozoic Selachian genus Thri- B 208, 369-384 (1980). nacodus. Journal of Vertebrate Paleontology 30(6), 1666-1672, Frey, L., Pohle, A., Rücklin, M. & Klug, C. Fossil-Lagerstätten and (2010), doi:10.1080/02724634.2010.520785. preservation of vertebrates and invertebrates from the Moroccan Goodrich E. S. Studies on the structure and development of verte- Devonian (eastern Anti-Atlas). Lethaia, XX (XX), XXX–XXX. brates (Univ. Chicago Press, 1930). (20XX) Goujet, D. & Young, G. C. Interrelationships of placoderms revisit- Frey, L., Rücklin, M., Korn, D., & Klug, C. Late Devonian and ed. Geobios Mem. Spec. 19, 89-95 (1995). Early Carboniferous alpha diversity, ecospace occupation, ver- Goujet D, & Young G. C. in Recent Advances in the Origin and Early tebrate assemblages and bio-events of southeastern Morocco. Radiation of Vertebrates, (eds Arratia, G., Wilson, M. V. H. & Palaeogeography, Palaeoclimatology, Palaeoecology 496, 1-17 Cloutier, R.) 109-26 (Friedrich Pfeil, 2004). (2018). Grogan, E. D. and Lund, R. Debeerius ellefseni (Fam. Nov., Gen. Friedman, M. Styloichthys as the oldest coelacanth: implications for Nov., Sped. Nov.) an Autodiastylic Chondrichthyan From the early osteichthyan interrelationships. J. Syst. Palaeontol. 5, 289- Mississippian Bear Gulch Limestone of Montana (USA), the 343 (2007). Relationships of the Chondrichthyes, and Comments on Gna-

130 Chapter III: Phoebodontid chondrichthyans of the Maider

thostome Evolution. J. Morphol. 243, 219-245 (2000). Heidtke, U. H. J. Revision der unterpermischen Acanthodier (Acan- Grogan, E.D. & Lund, R. A basal elasmobranch, Thrinacoselache thodii: Pisces) des südwestdeutschen Saar-Nahe-Beckens. Mitt. gracia n. gen & sp., (Thrinacodontidae, new family) from the Pollichia 95, 15-41 (2011b). Bear Gulch Limestone, Serpukhovian of Montana, USA. Jour- Heidtke, U. H. J. & Krätschmer K. Gladbachus adentatus nov. gen. nal of Vertebrate Paleontology 28(4), 970-988 (2008). et sp., ein primitiver Hai aus dem Oberen Givetium (Oberes Mit- Grogan, E. D., Lund, R. & Greenfest-Allen, E. in Biology of Sharks teldevon) der Bergisch Gladbach – Paffrath-Mulde (Rheinisches and Their Relatives (eds Carrier, J. C., Musick, J. A. & Heithaus, Schiefergebirge). Mainzer geowiss. Mitt. 30, 105-122 (2001). M. R.) 3-29 (CRC Press, 2012). Heidtke, U. H. J., Schwind, C. Über die Organisation des Skelet- Gross, W. Das Kopfskelett on Cladodus wildungensis Jaekel; 1. Teil. tes der Gattung Xenacanthus (Elasmobranchii: Xenacanthida) Endocranium und Palatoquadratum. Senckenbergiana 19, 80- aus dem Unterperm des südwestdeutschen Saar-Nahe-Beckens. 107 (1937). Neues Jahrbuch der Geologie und Paläontologie, Abhandlun- Gross, W. Das Kopfskelett on Cladodus wildungensis Jaekel; 2. Teil. gen 231(1), 85–117 (2004). Der Kieferbogen. Anhang: Protractodus vetusus Jaekel. Sen- Heidtke, U. H. J., Schwind, C. & Krätschmer K. Über die Organisa- ckenbergiana 20, 123-145 (1938). tion des Skelettes und die verwandschaftlichen Beziehungen der Hairapetian, V. & Ginter, M. Famennian chondrichthyan remains Gattung Triodus Jordan 1849 (Elasmobranchii: Xenacanthida). from the Chahriseh section, central Iran. Acta Geologica Polon- Mainzer geowiss. Mitt. 32, 9-54 (2004). ica 59(2), 173-200 (2009). Hotton, N. Jaws and teeth of American xenacanth sharks. Journal of Hairapetian, V. & Ginter, M. Pelagic chondrichthyan microremains Paleontology 26, 489-500 (1952). from the Upper Devonian of the Kale Sardar section, eastern Howard, L. E., Holmes, W. M., Ferrando, S., Maclaine, J. S., Kelsh, Iran. Acta Geologica Polonica 60(3), 357-371 (2010). R. N., Ramsey, A., Abel R. L. & Cox P. L. J. Functional nasal Hampe, O. Revision of the Xenacanthida (Chondrichthyes: Elasmo- morphology of chimaeroid fi shes. Journal of Morphology 274: branchii) from the Carboniferous of the British Isles. Trans. R. 987-1009 (2013). Soc. Edinb. (Earth Sci.) 93, 191-237 (2003). Huxley, T. A manual of the anatomy of vertebrated animals, 431pp. Hampe, O., Aboussalam, Z. S. & Becker, R. T. Omalodus teeth (D-Appleton and Co.), New York (1880B). (Elasmobranchii: Omalodontida) from the northern Gondwana Janvier, P. Early Vertebrates (Oxford Univ. Press, 1996). margin (middle Givetian: ansatus conodont Zone, Morocco), in: Janvier, P. & Maisey, J. G. (2010) in Morphology, Phylogeny and Arratia, G., Wilson, M. V. H., Cloutier, R. (Eds.), Recent ad- Paleobiogeography of Fossil Fishes. (eds Elliot, D.K., Maisey, vances in the origin and early radiation of vertebrates, 487-504 J.G., Yu, X. & Miao, D.) 431-459 (Freidrich Pfeil, 2010). (2004). Jarvik, E. Middle and Upper Devonian Porolepiformes form East Hanke G. F. Promesacanthus eppleri n. gen., n. sp., a mesacanthid Greenland with special reference to Glyptolepis groenlandica n. (Acanthodii, Acanthodiformes) from the Lower Devonian of sp. Meddelelser om Grønland 187, 1-307 (1972). northern Canada. Geodiversitas 30, 287-302 (2008). Jarvik, E. in Problems in Vertebrate Evolution. (eds Andrews, S. M., Hanke, G. F. & Davis, S. P. Redescription of the acanthodian Gladio- Miles, R. S., Walker & A. D.) 199-225 (Linnean Symposium branchus probaton Bernacsek & Dineley, 1977, and comments Series, London, 1977). on diplacanthid relationships. Geodiversitas 30, 303-330 (2008). Jarvik, E. Basic Structure and Evolution of Vertebrates (Academic, Hanke, G. F. & Davis, S. P. A re-examination of Lupopsyrus pygmae- 1980). us Bernacsek & Dineley, 1977 (Pisces, Acanthodii). Geodiversi- Karatajūte-Talimaa, V. in Fossil Fishes as Living Animals (ed. tas 34, 469-487 (2012). Mark-Kurik, E.) 223-232 (Academy of Sciences of Estonia, Hanke, G. F., Davis, S. P. & Wilson, M. V. H. A new species of Tallinn, 1992). the acanthodian genus Tetanopsyrus from Northern Canada, Kesteven, H. L. The anatomy of the head of Callorhynchus antarcti- with comments on related taxa. J. Vert. Paleontol. 21, 740-753 cus. Journal of Anatomy 67, 443-474 (1937). (2001). Lane, J. A. Morphology of the braincase in the Cretaceous hybodont Hanke, G. F., & Wilson, M. V. H. in Recent Advances in the Origin shark Tribodus linnae (Chondrichthyes: Elasmobranchii), based and Early Radiation of Vertebrates. (eds Arratia, G., Wilson, M. on CT scanning. Amer. Mus. Novitates 2758, 1-70 (2010). V. H., & Cloutier, R.) 189–216 (Freidrich Pfeil, 2004). Lane, J. A. & Maisey, J. G. Pectoral anatomy of Tribodus limae Hanke, G. F. & Wilson, M. V. H. Anatomy of the Early Devonian (Elasmobranchii: Hybodontiformes) from the Lower Cretaceous Acanthodian Brochoadmones milesi based on nearly complete of Northeastern Brazil. Journal of Vertebrate Paleontology 29, body fossils, with comments on the evolution and development 25-38 (2009). of paired fi ns. J. Vert. Paleontol. 26, 526-537 (2006). Lane, J. A. & Maisey, J. G. The visceral skeleton and jaw suspension Hanke, G. F., & Wilson, M. V. H. in Morphology, Phylogeny and in the durophagous hybodontid shark Tribodus limae from the Paleobiogeography of Fossil Fishes. (eds Elliot, D.K., Maisey, Lower Cretaceous of Brazil. Journal of Paleontology 86, 886- J.G., Yu, X. & Miao, D.) 159-182 (Freidrich Pfeil, 2010). 905 (2012). Harris, J. E. The dorsal fi n spine of Cladoselache. Scientifi c Pub- Lehman, J. P. Les Arthrodires du Dévonien supérieur du Tafi lalt (Sud lications of the Cleveland Museum of Natural History 8, 1-6 Marocain). Notes et Mémoires du Service Géologique du Maroc (1938a). 129, 1-70 (1956). Harris, J. E. The neurocranium and jaws of Cladoselache. Scientif- Lehman, J. P. A propos de quelques Arthrodires et Ichthyodorulites ic Publications of the Cleveland Museum of Natural History 8, sahariens. Mémoire IFAN 68, 193-200 (1964). 7-12 (1938b). Lehman, J. P. Nouveaux poissons fossiles du Dévonien du Maroc. Harris, J. E.. Diademodus hydei, a new fossil shark from the Cleve- Annales de Paléontologie Vertébrés 62, 1-34 (1976). land Shale. Proceedings of the Zoological Societey of London Lehman, J. P. Sur la présence d’un Ostéolépiforme dans le Dévo- 120, 683-697 (1951). nien supérieur du Tafi lalt. Compte-Rendus de l’Académie des Heidtke, U. H. J. Der Xenacanthide Orthacanthus senckenbergianus Sciences 285D, 151-153 (1977). aus dem pfälzischen Rotliegenden (Unter-Perm). Pollichia 70, Lehman, J. P. A propos de deux poissons du Famennien du Tafi lalt. 65-86 (1982). Annales de Paléontologie Vertébrés 64, 143-152 (1978). Heidtke, U. Studien über Acanthodes. 4. Acanthodes boyi n. sp., die Lelièvre, H., Janvier, P. L’Eusthénopteridé (Osteichthyes, Sarcopte- dritte Art der Acanthodier (Acanthodii: Pisces) aus dem Rotlie- rygii) du Famennian (Dévonien supérieur) du Tafi lalt (Maroc): gend (Unterperm) des Saar-Nahe-Beckens (S-W-Deutschland. nouvelle description. Bulletin du Muséum National d’Histoire Paläont. Z. 67, 331-341 (1993). naturelle, 4e Série, Section C, Sciences de la Terre, Paléontolo- Heidtke, U. H. J. Orthacanthus (Lebachacanthus) senckenbergianus gie, Géologie, Minéralogie 3, 351-365 (1986). Fritsch 1889 (Xenacanthida: Chondrichthyes): revision, organi- Lelièvre, H., Janvier, P. Un Actinistien (Sarcopterygii, Vertebra- sation und phylogenie. Freiberger Forschungsheft 481, 63-106 ta) dans le Dévonien supérieur du Maroc. Compte-Rendus de (1999). l’Académie des Sciences, Paris 307, 1425-1430 (1988). Heidtke, U. H. J. Gladbachus adentatus, die Geschichte des weltweit Lelièvre, H., Janvier, P., Blieck, A. Silurian-Devonian vertebrate bio- ältesten Hais – untersucht und beschriebenaus dem AK Geowis- stratigraphy of western Gondwana and related terranes (South senschaften. Pollichia Kurrier 25, 24-26 (2009). America, Africa, Armorica-Bohemia, Middle East). Palaeozo- Heidtke, U. H. J. Neue Erkenntnisse über Acanthodes bronni Agassiz ic vertebrate biostratigraphy and biogeography, pp. 139-173 1833. Mitt. Pollichia 95, 1-14 (2011a). (1993).

131 Chapter III: Phoebodontid chondrichthyans of the Maider

Long, J. A. A new diplacanthoid acanthodian from the Late Devoni- Maisey, J. G. The diversity of tessellated calcifi cation in modern and an of Victoria. Memoirs of the Association of Australasian Pa- extinct chondrichthyans. Revue de Paléobiologie, Geneve 32, laeontologists 1, 51-65 (1983). 355-371 (2013). Long, J. A. Late Devonian chondrichthyans and other microverte- Maisey, J. G. & Anderson, M. E. A primitive chondrichthyan brain- brate remains from northern Thailand. Journal of Vertebrate case from the Early Devonian of South Africa. Journal of Verte- Paleontology 10, 59-71 (1990). brate Paleontology 21, 702-713 (2001). Long, J. A., Barwick, R. E., & Campbell. Osteology and function- Maisey, J. G. & de Carvalho, M. R. A new look at old sharks. Nature al morphology of the osteolepiform fi sh Gogonasus andrewsae 385, 779-780 (1997). Long 1995, from the Upper Devonian Gogo Formation, Western Maisey, J. G. & Lane, J. A. Labyrinth morphology and the evolution Australia. Records of the Western Australian Museum Supple- of low-frequency phonoreception in elasmobranchs. C. R. Pa- ment 53, 1-89 (1997). levol 9, 289-309. (2010) Long, J. A., Burrow, C. J., Ginter, M., Maisey, J., Trinajstic, K. M., Maisey, J. G., Miller, R. & Turner, S. The braincase of the chon- Coates, M. I., Young, G. C. & Senden, T. J. First shark from drichthyan Doliodus from the Lower Devonian Campbellton the Late Devonian (Frasnian) Gogo Formation, Western Aus- Formation of New Brunswick, Canada. Acta Zoologica 90 (sup- tralia sheds new light on the development of tessellated calci- plement 1), 109-122 (2009). fi ed cartilage. PLoS ONE 10: e0126066 DOI:10.1371/journal. Maisey, J. G., Miller, R., Pradel, A., Denton, J. S. S., Bronson, A. & pone.0126066 (2015). Janvier, P. Pectoral morphology in Doliodus: bridging the ‘ac- Lund, R. Harpagofututor volsellorhinus new genus and species anthodian’-chondrichthyan divide. American Museum Novitates (Chondrichthyes, Chondrenchelyiformes) from the Namurian 3875, 1-15. (2017). Bear Gulch Limestone, Chondrenchelys problematica Traquair Maisey, J. G., Turner, S., Naylor, G. J. P. & Miller, R. F. Dental pat- (Visean), and their sexual dimorphism. Journal of Paleontology terning in the earliest sharks: implications for tooth evolution. 56, 938-958 (1982). Journal of Morphology. DOI:10.1002/jmor.20242 (2013) Lund, R.. Stethacanthid elasmobranch remains from the Bear Gulch Marinelli, W. & Strenger, A. Vergleichende Anatomie und Morpholo- Limestone (Namurian E2b) of Montana. American Museum No- gie der Wirbeltiere. III. 174-308 (Franz Deuticke, Wien, 1959). vitates 2828, 1-24 (1985a). Miles, R. S. Articulated acanthodian fi shes from the Old Red Sand- Lund, R. The morphology of Falcatus falcatus (St. John and Worth- stone of England, with a review of the structure and evolution en), a Mississippian stethacanthid chndrichthyan from the Bear of the acanthodian shoulder- girdle. Bull. Br. Mus. Nat. Hist. Gulch Limestone of Montana. Journal of Vertebrate Paleontol- (Geol.) 24, 111-213 (1973a). ogy 5, 1-19 (1985b). Miles, R. S. in Interrelationships of Fishes (eds Greenwood, P. H., Lund, R. On Damocles serratus nov. gen. et sp., (Elasmobranchii: Miles, R. S. & Patterson, C.) 63-103 (Academic, 1973b). Cladodontida) from the Upper Mississippian Bear Gulch Lime- Miller, R. F., Cloutier, R. & Turner, S. The oldest articulated chon- stone of Montana. Journal of Vertebrate Paleontology 6, 12-19 drichthyan from the Early Devonian period. Nature 425, 501- (1986). 504 (2003). Lund, R. & Grogan, E. D. Relationships of the Chimaeriformes and Moy-Thomas, J. A. The structure and affi nities of Chondrenchelys the basal radiation of the Chondrichthyes. Reviews in Fish Biol- problematica Tr. Proceedings of the Zoological Society, Lon- ogy and Fisheries 7, 65-123 (1997). don1935, 391-403 (1935). Lund, R. & Grogan, E. D. in Recent Advances in the Origin and Ear- Mutter, R. J., de Blanger, K., & Neuman, A. G. Elasmobranchs from ly Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & the Lower Triassic Sulphur Mountain Formation near Wapiti Cloutier, R.) 171-187 (Friedrich Pfi el, 2004a). Lake (BC, Canada). Zoological Journal of the Linnean Society Lund, R. & Grogan, E. D. in Recent Advances in the Origin and Ear- 149, 309-37 (2007). ly Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Mutter, R. J., Neuman, A. G. & de Blanger, K. Homalodontus nom. Cloutier, R.) 505-531 (Friedrich Pfi el, 2004b). nov. a replacement for Wapitiodus Mutter, de Blanger and Neu- Mader, H. Schuppen und Zähne von Acanthodiern und Elasmobran- man 2007 (Homalodontidae nom. nov., ?Hybodontoidea), pre- chiern aus dem Unter-Devon Spaniens (Pisces). Göttinger Ar- occupied by Wapitiodus Orchard, 2005. Zoological Journal of beiten zur Geologie und Paläontologie 28, 1-59 (1986). the Linnean Society 154, 419-420 (2008). Maisey, J. G. The anatomy and interrelationships of Mesozoic hy- Nelson, G. J. in Current problems of lower vertebrate phylogeny. bodont sharks. Am. Mus. Novit. 2724, 1-48 (1982). (ed. T. Ørvig) 129-143 (Almqvist & Wiksell, Stockholm, 1968). Maisey, J. G. Cranial anatomy of Hybodus basanus Egerton from Nelson, G. J. Gill arches and the phylogeny of fi shes, with notes on the Lower Cretaceous of England. Am. Mus. Novit. 2758, 1-64 the classifi cation of vertebrates. Bull. Am. Mus. Nat. Hist. 141, (1983). 475-552 (1969). Maisey, J. G. Cranial Morphology of the Fossil Elasmobranch Syn- Nelson, G. J. Pharyngeal denticles (placoid scales) of sharks with echodus dubrisiensis. Am. Mus. Novit. 2804, 1-28 (1985). notes on the dermal skeleton of vertebrates. Amer. Mus. Novi- Maisey, J. G. Visceral skeleton and musculature of a Late Devonian tates 2416, 1-26 (1970). shark. J. Vertebr. Paleontol. 9, 174-190 (1989a). Newberry, J. S. The Paleozoic fi shes of North America, Monograph Maisey, J. G. Hamiltonichthys mapesi g. & sp. nov. (Chondrichthy- of the U.S. Geological Survey 16, 1–340 (1889). es; Elasmobranchii), from the Upper Pennsylvanian of Kansas. Newman, M. J., Davidson, R. G., den Blaauwen, J. L. & Burrow, American Museum Novitates 2931, 1-42 (1989b). C. J. The Early Devonian acanthodian Uraniacanthus curtus Maisey, J. G. in Major Events in Early Vertebrate Evolution (ed. Ahl- (Powrie, 1870) n. comb., from the Midland Valley of Scotland. berg, P. E.) 263-288 (Taylor and Francis, 2001a). Geodiversitas 34, 739-759 (2012). Maisey, J. G. Remarks on the inner ear of elasmobranchs and its in- Oelofsen, B. W. A fossil shark neurocranium from the Permo-Car- terpretation from skeletal labyrinth morphology. J. Morph. 250, boniferous (lowermost Ecca Formation) of South Africa. In In- 236-264. (2001b). do-Pacifi c fi sh biology. Proceedings of the Second International Maisey, J. G. Braincase of the Upper Devonian shark Cladodoides Conference on Indo-Pacifi c Fishes. Ichthyological Society of wildungensis (Chondrichthyes, Elasmobranchii), with observa- Japan, Tokyo, pp. 107-124 (1986). tions on the braincase in early chondrichthyans. Bull. Am. Mus. Patterson, C. The phylogeny of the chimaeroids. Philosophical Nat. Hist. 288, 1-103 (2005). Transactions of the Royal Society of London, Series B 249, 101- Maisey, J. G. The braincase in Paleozoic symmoriiform and cladose- 219 (1965). lachian sharks. Bull. Am. Mus. Nat. Hist. 307, 1-122 (2007). Patterson, C. Morphology and interrelationships of primitive acti- Maisey, J. G. The postorbital palatoquadrate articulation in elasmo- nopterygian fi shes. American Zoologist 22, 241-259 (1982). branchs. Journal of Morphology 269, 1022-1040 (2008). Patterson, C. Interpretation of the toothplates of chimaeroid fi shes. Maisey, J. G. The spine-brush complex in symmoriiform sharks Zool. J. Linn. Soc. 106, 33-61 (1992). (Chondrichthys; Symmoriiformes), with commenst on dorsal Pearson, D. M. & Westoll, T. S. The Devonian actinopterygian Chei- fn modularity. Journal of Vertebrate Paleontology 29, 14-24 rolepis Agassiz. Trans. R. Soc. Edinb. 70, 337-399 (1979). (2009). Pradel, A. Skull and brain anatomy of Late Carboniferous Siby- Maisey, J. G. The braincase of the Middle Triassic shark Acronemus rhynchidae (Chondrichthyes, Iniopterygia) from Kansas and tuberculatus (Bassani, 1886). Palaeontology 54, 417-428 Oklahoma (USA). Geodiversitas 32, 595-661 (2010). (2011). Pradel A., Didier, D., Casane, D., Tafforeau, P. & Maisey J. G. Ho-

132 Chapter III: Phoebodontid chondrichthyans of the Maider

locephalan embryo provides new information on the evolution St. John, O. and Worthen, A. H.. Description of fossil fi shes. Geolog- of the glossopharyngeal nerve, metotic fi ssure and parachordal ical Survey of Illinois 6(2), 245-488 (1875A). plate in gnathostomes. PLoS ONE 8: e66988 DOI:10.1371/jour- Thomson, K. S. The endocranium and associated structures in the nal.pone.0066988 (2013). Middle Devonian rhipidistian fi sh Osteolepis. Proceedings of Pradel A., Langer M., Maisey J. G., Geffard-Kuriyama D., Cloetens the Linnean Society of London 176, 181-195 (1965). P., Janvier P., & Tafforeau P. Skull and brain of a 300 million- Tucker A. S. & Fraser, G. J. Evolution and developmental diversity year-old chimaeroid fi sh revealed by synchrotron holotomog- of tooth regeneration. Semin Cell Dev Biol DOI:10.1016/j.sem- raphy. Proceedings of the National Academy of Sciences 106, cdb.2013.12.013 (2014). 5224-5228 (2009). Turner, S. Middle Palaeozoic elasmobranch remains from Australia. Pradel, A., Maisey, J. G., Tafforeau, P., Mapes, R. H. & Mallatt, J. Journal of Vertebrate Paleontology 2, 117-131 (1982). A Palaeozoic shark with osteichthyan-like branchial arches. Na- Turner, S., Burrow, C. J. & Warren, A. Gyracanthides hawkinsi sp. ture 509, 608-611 (2014). nov. (Acanthodii, Gyracanthidae) from the Lower Carbonifer- Pradel, A., Tafforeau, P. & Janvier P. Study of the pectoral girdle and ous of Queensland, Australia, with a review of gyracanthid taxa. fi ns of the Late Carboniferous sibyrhynchid iniopterygians (Ver- Palaeontology 48, 963-1006 (2005). tebrata, Chondrichthyes, Iniopterygia) from Kansas and Okla- Valiukevicius, J. in Fossil Fishes as Living Animals (ed. Mark-Kurik, homa (USA) by means of microtomography, with comments on E.) 193-213 (Academy of Sciences of Estonia, Tallinn, 1992). iniopterygian relationships. Comptes Rendus Palevol 9, 377-387 Warren, A., Currie, B. P., Burrow, C. & Turner, S. A redescription (2010). and reinterpretation of Gyracanthides murrayi Woodward 1906 Pradel A., Tafforeau P., Maisey J. G. & Janvier P. A new Paleo- (Acanthodii, Gyracanthidae) from the Lower Carboniferous of zoic Symmoriiformes (Chondrichthyes) from the Late Car- the Mansfi eld Basin, Victoria, Australia. Journal of Vertebrate boniferous of Kansas (USA) and Cladistic Analysis of Early Paleontology 20, 225-242 (2000). Chondrichthyans. PLoS ONE 6: e24938 DOI:10.1371/journal. Watson, D. M. S. The acanthodian fi shes. Philosophical Transac- pone.0024938 (2011). tions of the Royal Society of London B 228, 49-146 (1937). Qu, Q., M., Zhu, M. & Wang, W. Scales and dermal skeletal histolo- Wells, J. W. Fish remains from the Middle Devonian bone beds of gy of an early bony fi sh Psarolepis romeri and their bearing on the Cincinnati Arch region. Palaeontographica Americana 3, the evolution of rhombic scales and hard tissues. PLoS One 8, 5-62 (1944C). e61485 (2013a). Williams, M. E. The ‘‘cladodont level’’ sharks of the Pennsylvanian Qu, Q., Sanchez, S., Blom, H., Tafforeau, P. & Ahlberg P. E. Scales Black Shales of central North America. Palaeontographica 190, and tooth whorls of ancient fi shes challenge distinction between 83-158 (1985). external and oral ‘teeth’. PLoS ONE 8, DOI:10.1371/journal. Williams, M. E. A new specimen of Tamiobatis vetustus (Chondrich- pone.0071890 (2013b). thyes, Ctenacanthoidea) from the Late Devonian Cleveland Qiao, T., King B., Long J. A., Ahlberg P. E., & Zhu M. Early gnatho- Shale of Ohio. Journal of Vertebrate Paleontology 18(2), 251- stome phylogeny revisited: multiple method consensus. PLoS 260 (1998). ONE 11, DOI:10.1371/journal.pone.0163157 (2016). Williams, M. E. Tooth retention in cladodont sharks: with a compar- Reif, W. E. Types of morphogenesis of the dermal skeleton in fossil ison between primitive grasping and swallowing, and modern sharks. Paläont. Z. 52, 110-128 (1978). cutting and gouging feeding mechanisms. Journal of Vertebrate Reif, W. E. Squamation and ecology of sharks. Cour. Forsch.-Inst. Paleontology 21, 214-226 (2001). Senckenberg 78, 1-255 (1985). Woodward, A. S. & White, E. I. The dermal tubercles of the Upper Rieppel, O. A new genus of shark from the Middle Triassic of Monte Devonian shark, Cladoselache. Annals and Magazine of Natural San Giorgio, Switzerland. Palaeontology 25, 399-412 (1982). History 11, 367-368 (1938). Rücklin M. A new Frasnian placoderm assemblage from the eastern Yu, X. A new porolepiform-like fi sh, Psarolepis romeri, gen. et sp. Anti-Atlas, Morocco, and its palaeobiogeographical implica- nov. (Sarcopterygii, Osteichthyes) from the Lower Devonian of tions. Palaeoworld 19, 87-93 (2010). Yunnan, China. J. Vertebr. Paleontol. 18, 261-264 (1998). Rücklin M. First selenosteid placoderms from the eastern Anti-Atlas Zangerl, R. Chondrichthyes I: Paleozoic Elasmobranchii. In: Schul- of Morocco; osteology, phylogeny and palaeogeographical im- tze, H. P. (ed.), Handbook of Paleoichthyology 3A, 115 pp. Gus- plications. Palaeontology 54, 25-62 (2011). tave Fischer, Stuttgart, New York (1981). Rücklin, M., Clément, G. Une revue des Placodermes et Sarcoptéry- Zangerl, R. & Case, G. R. Iniopterygia, a new order of chondrich- giens du Dévonien du Maroc, in: Zouhri, S. (ed), Paléontologie thyan fi shes from the Pennsylvanian of North America. Fieldi- des vertébrés du Maroc: état des connaissance, Mémoires de la ana: Geology 6, 1-67 (1973). Société Géologique de France 180, p. 624 (2017). Zangerl, R. and Case, G. R. Cobelodus aculeatus (Cope), an anacan- Rücklin, M., Long, J. A., Trinajstic, K. A new selenosteid arthrodire thous shark from Pennsylvanian Black Shales of North America. (‘Placodermi’) from the Late Devonian of Morocco. Journal of Palaeontographica A 154, 107-57 (1976). Vertebrate Paleontology 35(2), e908896, 1-13 (2015). Zhu, M. & Schultze, H. P. The oldest sarcopterygian fi sh. Lethaia Schaeffer, B. The xenacanth shark neurocranium, with comments on 30, 293-304 (1997). elasmobranch monophyly. Bull. Am. Mus. Nat. Hist. 169, 1-66 Zhu, M. & Schultze, H. P. in Major Events in Early Vertebrate Evo- (1981). lution (Palaeontology, phylogeny, genetics, and development). Schultze, H.NP. & Zidek, J. Ein primitiver acanthodier (Pisces) aus (ed. Ahlberg, P. E.) 289-314 (Taylor and Francis, 2001). dem Unterdevon Lettlands. Paläontologische Zeitschrift 56, 95- Zhu, M & Yu, X. A primitive fi sh close to the common ancestor of 105 (1982). tetrapods and lungfi sh. Nature 418, 767-770 (2002). Seidel, R., Lyons, K., Blumer, M., Zalansky, P., Fratzl, P., Weaver, J. Zhu, M., Yu, X, & Ahlberg, P. E. A primitive sarcopterygian fi sh with C. & Dean, M. N. Ultrastructural and developmental features of an eyestalk. Nature 410, 81-84 (2001). the tessellated endoskeleton of elasmobranchs (sharks and rays). Zhu, M., Yu, X., Ahlberg, P. E., Choo, B., Lu, J., Qiao, Q., Zhao, J. Anat. DOI:10.1111/joa.12508 (2016). L. J., Blom, H., & Zhu, Y. A Silurian placoderm with osteich- Smith, B. G. The Anatomy of the Frilled Shark, Chlamydoselachus thyan-like marginal jaw bones. Nature 52, 188-193 (2013). anguineus Garman. Bashford Dean Memorial Volume: Archaic Zhu, M., Yu, X. & Janvier, P. A primitive fossil fi sh sheds light on the Fishes Article 6, 333-506. American Museum of Natural Histo- origin of bony fi shes. Nature 397, 607-610 (1999). ry, N.Y (1937). Zhu, M., Zhao, W., Jia, L., Lu, J., Qiao, T. & Qu, Q. The oldest artic- Solér-Gijon, R. & Hampe, O. Evidence of Triodus Jordan 1849 ulated osteichthyan reveals a mosaic of gnathostome characters. (Elasmobranchii: Xenacanthidae) in the Lower Permian of the Nature 458, 469-474 (2009). Autun basin (Muse, France). N. Jb. Geol. Paläont. Mh. 1998, Zidek, J. Late Pennsylvanian Chondrichthyes, Acanthodii, and 335-348 (1998). deep-bodied Actinopterygii from the Kinney Quarry, Manzani- Stahl, B. J. Reconstruction of the head skeleton of the fossil elas- ta Moutains, New Mexico. In Geology and paleontology of the mobranch, Phoebodus heslerorum (Pisces, Chondrichthyes). Kinney Brick Quarry, Late Pennsylvanian, central New Mexi- Copeia 4, 858-866 (1988). co. J. Zidek ed. Bulletin 138, New Mexico Bureau of Mines & Stahl, B. J. in Handbook of Paleoichthyology Vol. 4 (ed. Schultze, Mineral Resources (Socorro: New Mexico Bureau of Mines & H.-P.) (Friedrich Pfeil, München. 1999). Mineral Resources), pp. 199-214. (1992).

133

CHAPTER IV

Functional morphology of mandibular arches in symmoriids as exemplifi ed by Ferromirum oukherbouchi gen. et sp. nov. (Late Devonian)

Linda Frey, Michael Coates, Martin Rücklin and Christian Klug

In preparation, formatted for Science Advances

Chapter IV: Functional Morphology of Symmoriid Jaws

Functional morphology of mandibular arches in symmoriids as ex- emplifi ed by Ferromirum oukherbouchi gen. et sp. nov. (Late Devoni- an, Morocco) L. Frey1*, M. I. Coates2, M. Rücklin3 and C. Klug1

1Paläontologisches Institut und Museum, University of Zurich, Karl-Schmid-Strasse 4, CH-8006 Zürich ([email protected]; [email protected]). 2Department of Organismal Biology and Anatomy, University of Chicago, 1027 E. 57th St., USA-60637 Chicago. 3 Naturalis Biodiversity Center, Postbus 9517, 2300 RA, Leiden, The Netherlands.

The functional morphology of mandibular and branchial arches in early chondrichthyans is poorly known because of the lack of articulated and undistorted fossil material. A recently discovered exceptionally well-preserved specimen of the symmoriiform Ferromirum oukherbouchi gen. et sp. nov. of Famennian age from the southern Maïder (Morocco) yields new information about the anatomy and function of the cranial and visceral skeleton. A three-dimensional model based on CT-scans of the holotype shows the undeformed mandibular and branchial arches such as the hyoids and ceratohyals allowing the reconstruc- tion of mandible movement during feeding. The way the Meckel’s cartilages rotate around their sagittal axes was previously unknown from chondrichthyans and probably became extinct with the end of the symmoriid clade. At the same time, the new species corroborates that cranial morphology of Palaeozoic symmoriiforms is quite conservative and allowed to falsify the aphetohyoidean hypothesis for these early chondrichthyans, because in the new taxon, the hyoid is tightly attached to the lower jaw.

Key words: chondrichthyans, gnathostomes, jaws, Famennian, Maïder, Palaeozoic

1. Introduction swallowed in one piece while forms with prot- acrodont or orodont teeth were likely duropha- The evolution of the structured visceral skeleton gous [14]. Filter feeding chondrichthyans such as including jaws was a fundamental step in ver- Diademodus were rarely reported from the Palae- tebrate evolution as it opened up the access to a ozoic so far; they usually have minute teeth com- much greater variety of food sources. The visceral pared to jaw size [13]. Other feeding modes such skeleton of chondrichthyans, osteichthyans, and as suction feeding were inferred for hybodontid extinct stem gnathostomes including placoderms chondrichthyans from the Carboniferous based on and acanthodians consists of paired, serially ar- their mandibular and branchial skeletons [16]. ranged lower and upper jaws, jaw supporting el- ements (hyoids and ceratohyals) and gill arches The function of jaws and branchial arches of [1-6]. Knowledge of morphological details and the Symmoriiformes is hardly known although the function of jaws in Devonian chondrichthyans it is a very common and geographically widely is still poor, mostly due to incompleteness or de- distributed group of early chondrichthyans with formation of specimens. With a few exceptions cladodont teeth. It is known from the Devonian [7-9], the visceral skeleton and the jaws are of- and Carboniferous and was recently assigned to ten disarticulated and/ or distorted by compaction the holocephalans branch within the chondrich- or tectonics. Therefore, reconstructions of feed- thyans [17]. Although complete skeletons [18-23] ing mechanisms of Palaeozoic chondrichthyans and braincases [17, 24-26] of several species were are largely based on tooth morphology and ar- described in the last decades, branchial arches and rangement in combination with comparisons to jaws in three-dimensional preservation remained analogous or homologous conditions in Recent unknown. In a recently discovered symmoriiform chondrichthyans [10-15]. As in modern chon- chondrichthyan from the Devonian of Morocco, drichthyans, the dentitions of Devonian chon- superbly preserved and articulated branchial and drichthyans display a great morphologic disparity mandibular arches are preserved. These remains corresponding to a similarly wide range of feed- reveal the fi rst insights into the feeding mecha- ing strategies. Chondrichthyans with cladodont or nism of these early holocephalans. phoebodont teeth were grasping prey, which they

137 Chapter IV: Functional Morphology of Symmoriid Jaws

into account, we suggest that Ferromirum might be the only Devonian and thus oldest member of 2. Results the Falcatidae. 2.1 Systematic palaeontology and anatomical description Ferromirum oukherbouchi gen. et sp. nov. Class Chondrichthyes Huxley, 1880 Order Symmoriiformes Zangerl, 1981 Holotype. PIMUZ A/I XXXX Family ?Falcatidae Zangerl, 1990 Genus Ferromirum gen. nov. Material. Only the holotype.

Type species. Ferromirum oukherbouchi gen. et Locality and horizon. Famennian, Planitornoc- sp. nov. eras euryomphalum to Afrolobites mrakibensis Zone; Ibaouane Formation, Lahfi ra Member, Thy- Etymology. Derived from ferrum (lat. - iron) lacocephalan Layer (formerly described as Phyl- and mirus (lat. - miraculous). Ferrum is includ- locarid Layer; [27]), Madene el Mrakib, Maïder ed because of the preservation of the holotype of Basin, southeastern Anti-Atlas, Morocco. the type species in a reddish ferruginous nodule, which is characteristic for fossils from the Thyla- Etymology. The species name oukherbouchi hon- cocephalan Layer of the Maïder. Mirus refers to ours the fi nder of the specimen Said Oukherbouch the fact that we erroneously interpreted the gill re- (Tafraoute). mains of the holotype as appendages of a crusta- Species defi nition. As for genus. cean, and it was like a miracle when a chondrich- thyan emerged.

Genus defi nition. Small symmoriid with slen- Description der body; head with rounded triangular outline, rostrum protruding anterior of the mouth; large The complete body of Ferromirum oukherbouchi orbits; tessellated cartilage; jaws amphystylic; gen. et sp. nov. is approximately 33 cm long. It cladodont teeth; cleaver-shaped palatoquadrate; was prepared from its ventral side. Thus, ventral fi ve gill arches; otico-occipital fi ssure; narrow parts of the pectoral and pelvic girdles, branchi- suborbital shelf; palatoquadrate ventrally sig- al and mandibular arches and of the left orbit are moid; coronoid process on Meckel`s cartilage; tri- exposed (Fig. 1A, B). In the anterior part of the angular pelvic girdle; anterior fi n spine broad and head region, a rostrum like in Falcatus and Dam- dorsally recurved. ocles [20-21] is present and some soft tissues such as both elongate wings of the liver, parts of the Included species. Only the type species. digestive tract and parts of the body outline are preserved. The computed tomograms and the re- Systematic remarks. Although the cladistics constructed 3D-model show much more anatom- analysis did not resolve the family-position of ical details of the braincase, pectoral and pelvic the new taxon, we tentatively assign it to the Fal- girdles, as well as a fi n spine (Fig. 2A-D). The catidae for the following reason: There are cur- visceral skeleton shows a basic arrangement with rently seven other genera included in this clade: serially arranged paired mandibular and hyoid Dwykaselachus has a short rostrum; Ozarcus has arches and fi ve gill arches as known from Ozarcus a different geometry of the palatoquadrate and mapesae [8]. a rostrum like in Ferromirum seems missing; Cladoselache has short fi n spines; Cobelodus Mandibular arches lacks the anterior dorsal fi n and fi n spine as well as a shorter rostrum; the jaws are quite similar in The mandibular arches underwent very little dis- Ferromirum and Akmonistion, but the latter has tortion and compression (Fig. 3A-I) and there- a large spine-brush complex; Damocles and Fal- fore, they represent the best-preserved jaws cur- catus share the small body size, the slender body, rently known from symmoriid chondrichthyans. similar jaws, a neurocranium protruding anterior- The palatoquadrate of Ferromirum gen. nov. is ly in front of the palatoquadrate, and the strongly cleaver-shaped with a high otic process, which is developed dorsal fi n spine above the pectoral gir- a common feature in symmoriids and other Pa- dle with Ferromirum but differ in the shape of the laeozoic chondrichthyans [10, 28]. Anteriorly, the fi n spine. Taking these differences and similarities otic process articulates with the postorbital pro-

138 Chapter IV: Functional Morphology of Symmoriid Jaws

Fig. 1. Ferromirum oukherbouchi gen. et sp. nov., PIMUZ XXXX, early/ middle Famennian, Madene el Mrakib. (A) Photo and (B) line drawing of the specimen. (C) Head region including parts of the braincase, sclerotic ring, mandib- ular arches and branchial skeleton and shoulder girdles from ventral view. (D) Soft tissue remains including liver and spiral valves. (E) Pelvic and caudal region. Abbreviations - chy: ceratohyal; cop: copula; cbr: ceratobranchials; fs: fi n spine; liv: liver; mc: Meckel`s cartilage; p.pl: pelvic plate; pq: palatoquadrate; ros: rostrum; scl.r: sclerotic ring; scor; scapulacoracoid; stc?: stomach content; spv: spiral valves. Scales: A-B = 100 mm; C-E = 30 mm.

139 Chapter IV: Functional Morphology of Symmoriid Jaws

Fig. 2. Ferromirum oukherbouchi gen. et sp. nov. PIMUZ XX, virtually reconstructed specimen based on CT-data showing the neurocranium, mandibular arches the pectoral girdle and the dorsal fi n spine. Ventral (A) and dorsal view with (B) and without (C) braincase. (D) lateral view. Colour coding: grey, braincase; turquoise, palatoquadrate; yellow, Meckel’s cartilage; dark green, hypohyal; light blue, hyoid; orange, ceratohyal; blue, epihyals; red, cerato- branchials; green, copula; brown, fi n spine; purple, shoulder girdle; light turquoise, ? neural arches. cess of the neurocranium. A distinctive otic crest concave forming a large attachment area for ad- at the dorsoposterior margin of the palatoquadrate ductor muscles. The ventral margin of the entire is present. A second smaller crest is situated on palatoquadrate is sigmoid like in Stethacanthidae the most anterior part of the dorsal margin of the [19, 23] and Falcatidae [20-21]. Dorsally, the pal- otic process (anterodorsal crest) that serves as a atine region is mediolaterally expanded similar to support for nerve VII (Fig. 3C, D). Laterally, the Ozarcus [8]. Anteromedially, a serrated margin quadrate region of the palatoquadrate is strongly articulates with the ethmoid region of the neuro-

140 Chapter IV: Functional Morphology of Symmoriid Jaws cranium. Like the palatoquadrate, the Meckel`s glenoid mandibular process are present posterior- cartilages have a prominent lateral concavity in ly of the Meckel`s cartilage. the posterior portion (Fig. 3E-I). The ventroposte- rior jaw margin forms a distinctive crest. Dorsal- Branchial arches ly, the mediolateral expanded margin bears eight small circular concavities for tooth families. At Like in Ozarcus, the preserved hyoid arches in- two thirds of its length, the dorsal margin of the clude paired epihyals, ceratohyals and hypohyals Meckel`s cartilage shows a coronoid process pos- [8], while pharyngohyals, interhyals and basihy- teriorly followed by a concavity similar to Falca- als are not preserved (maybe poorly calcifi ed) in tus [20]. For the articulation with the palatoquad- Ferromirum gen. nov. Both the ceratohyals and rate, two processes including the mesial process epihyals are closely aligned to the mandibular (also known as mandibular knob; [29]) and the arches throughout their complete length. This

Fig. 3. Mandibular arches of Ferromirum oukherbouchi gen. et sp. nov., PIMUZ XX. Right and left palatoquadrates in dorsal (A) and ventral (B) view. Right palatoquadrate, lateral (C) and medial (D) view. (E) Right and left Meck- el’s cartilage in ventral aspect. Right Meckel’s cartilages in lateral (F), medial (G), dorsal (H) and ventral (I) views. Abbreviations: adc, anterodorsal crest; gl, glenoid; ma, mandibular articulation; mp, mandibular process; oa: orbital articulation; oaf, otic articular fossa; opr, otic process; ppr, palatine process; sym, symphysis.

141 Chapter IV: Functional Morphology of Symmoriid Jaws contrasts the condition in Ozarcus and Cobelodus two openings for the lateral dorsal aortae far pos- where some space seems to be left between the teriorly. In the occipital region, the occipital plate hyoid and mandibular arches (fi n 3 a in [8]; [30]). is perforated by the foramen magnum. With the new anatomical data of Ferromirum gen. nov. provided here, the supposed space between Remains of a deformed sclerotic ring are ex- the hyoid and mandibular arches in Ozarcus and posed (Fig. 1A-C), but its fi ne morphological de- Cobelodus is likely taphonomically biased. Both tails are not preserved. Sclerotic rings are formed the upper and lower hyoid arches are slightly by numerous sclerotics in Cladoselache [33], Fal- curved and posteriorly, the hyoid is inserted in the catus [20] and Damocles [21]. articular notch of the ceratohyal. Anteriorly, the dorsoventrally broad end of the hyoid articulates Pectoral girdle with the lateral otic region of the braincase. Right and left parts of the pectoral girdle are pres- From the gill arches, fi ve pairs of epibranchi- ent, where the left part is better preserved. The als and of seven ceratobranchials are present. All scapulacoracoid of Ferromirum gen. nov. has a are rod-shaped, and have a smooth surface (unlike shape characteristic for symmoriiform chondrich- Tristychius [31]). The basibranchial copula [32] thyans [e.g. 10, 24]. The fl at, sheet-like scapula in Ferromirum gen. nov. is long and of rectangu- is dorsoventrally long and bears an anteriorly lar shape but its articulation with basibranchials directing process (anterior process) at the dorsal is unknown. Smaller elements such as hypobran- apex (Fig. 5A-E). The region bearing the posteri- chials, infrapharyngobranchials and suprapharyn- ordorsal process is broken (compare fi g. 10A-C in gobranchials reported from Ozarcus [8] are not [24]). Anteriorly and posteriorly, the scapula has recognizable. a concave outline. Towards the ventral end, the scapulacoracoid is mediolaterally broadening. In Neurocranium and sclerotic ring ventral view, the base of the scapulacoracoid ap- pears triangularly and its posterior portion shows The neurocranium of Ferromirum gen. nov.is a concavity for the articulation with the proximal somewhat deformed. It shows a somewhat com- radials of the pectoral fi n. The coracoid region is pressed ethmoidal and orbital region, while the convex anteriorly and concave posteriorly. A pro- otic and occipital regions are three-dimensionally coracoid has not been detected but was probably preserved (Fig. 4A-D). The overall shape of the present as in, e.g., Akmonistion and other symmo- braincase shows the affi nity of this specimen to riids. other symmoriids. At the anterolateral edges of the narrow subotic shelf of the ethmoid, a serrated Pelvic girdle margin for the articulation with the palatine ramus of the palatoquadrate is present. The orbital region The pelvic girdle is poorly preserved in Fer- shows the common condition as in holocephalans: romirum gen. nov.; only a small, simple triangular its size is very large and about the same length plate is visible posterior of a pyrite concretion, as the otic and occipital regions together [17]. A which possibly is located in the middle of the body large opening for the optic nerve II is perforating (Fig. 1B, E). In other symmoriiform chondrich- the interorbital wall. The postorbital process is thyans such as Akmonistion, Cobelodus, Denaea laterally broken but it is rather thin anteroposte- and Symmorium, the pelvic plate is subtrianglar to riorly compared to the rest of the braincase. From oval in shape [10, 24]. In Falcatus, it is triangular the dorsal view, only little anatomical detail of but the anterolateral edge is concave [20]. Trian- the otic region is recognizable. Characteristical- gular plates are present in Cladoselache (fi g. 18 ly for early chondrichthyans, the occipital unit is in [33]) and xenacanthids [fi g. 12a-b in [34]; fi g. wedged between the otic capsule and traces of an 14 in [35]). otic-occipital fi ssure are preserved. The hyoman- Fin spine dibula articulates with the otic unit posterior to the postorbital process. However, a periotic pro- A dorsal fi n spine on the pectoral level is pre- cess is not recognizable where the hyomandibula served between the pectoral girdle and the pos- is supposed to articulate (see e.g., Cobelodus in terior end of the neurocranium in Ferromirum [25]; Dwykaselachus in [17]). Ventrally and pos- gen. nov.. It resembles the fi ns spines of cladose- teriorly to the postorbital process, the otic region lachians [10, 36] in having an anteroposteriorly shows a waist typical for symmoriids [e.g., 17]. broad shape and a strongly recurved dorsal apex. The otic region and the glossopharyngeal canals Its position is comparable to genera such as Fal- are fl oored by a hypotic lamina, which exhibits catus or Stethacanthus. By contrast, the fi n spine

142 Chapter IV: Functional Morphology of Symmoriid Jaws

Fig. 4. Ferromirum oukherbouchi gen. et sp. nov., PIMUZ XX. Neurocranium in dorsal (A), ventral (B), lateral (C) and posterior (D) views. (E) Articulation between braincase and visceral arches. (F-G) Arrangement of mandibular and branchial arches. Colour coding: grey, braincase; turquoise, palatoquadrate; yellow, Meckel’s cartilage; dark green, hypohyal; light blue, hyoid; orange, ceratohyal. Abbreviations: fm, foramen magnum; hl, hypotic lamina; hya, hyomandibular articulation; glc, glossopharyngeal canal; oa, orbital articulation; ocpl, occipital plate; oof, otico-oc- cipital fi ssure; popr, postorbital process; sup.s, supraorbital shelf; II, optic nerve.

Fig. 5. Virtually reconstructed pectoral elements and the fi n spine (possibly slightly distorted) of Ferromirum oukher- bouchi gen. et sp. nov., PIMUZ XX. Left part of the pectoral girdle in anterior (A), lateral (B, D), posterior (C) and ventral (E) views. (F) dorsal fi n spine of the pectoral fi n-level. Abbreviations: apr, anterior process; cor, coracoid; ppr, posterior process; sc, scapula.

143 Chapter IV: Functional Morphology of Symmoriid Jaws of Ferromirum gen. nov. is longer and more slen- Although our phylogenetic analyses does not ful- der than in Cladoselache (Fig. 5F). The dorsal fi n ly resolve the relation within the symmoriiform on the pelvic level is not visible in the CT-scan clade, the small size, body proportions, shape of and possibly absent. the head (including shape of the palatoquadrate, pointed rostrum) and the presence of one fi n spine 2.2 Phylogenetic relationships in the pectoral region of Ferromirum gen. nov. are reminiscent of the Falcatidae (Fig. 7). In the Phylogenetic analyses resulted in 730 parsimoni- light of this systematic proximity, the absence of a ous trees of 545 steps. The strict consensus tree well-developed dorsal fi n and a posterior fi n spine based on the data matrix including 228 characters, can be considered primary. An assignment to this 66 ingroup taxa and one outgroup taxon plac- family would extend the stratigraphic range of es Ferromirum gen. nov. within the Symmorii- the Falcatidae from the Early Carboniferous into formes (Fig. 6, S1). Ferromirum gen. nov. shares the Late Devonian, which is not surprising tak- the narrow interorbital space, the absence of anal ing the bizarre morphological specialisations of fi ns, the presence of a fi n spine at pectoral level the Carboniferous falcatids into account. More and a longer orbit compared to the otic unit (in discoveries of postcranial material of Dwykasela- Ferromirum gen. nov. only subtly longer) with chus, Ozarcus and Ferromirum, in particular, will other stem Holocephali. The presence of a scle- help reconstructing the phylogenetic relationships rotic ring is shared with other Symmoriiformes among symmoriids and testing the hypothesis of (Cladoselache, Falcatus and Damocles). Ferromirum being a falcatid.

Doliodus Acronemus Egertonodus Hamiltonichthys Onychoselache Tribodus Squalus Synechodus Tristychius Homalodontus Cladodoides Phoebodus Thrinacodus Diplodoselache Orthacanthus Triodus Tamiobatis Ferromirum gen. nov Dwykaselachus Ozarcus Cladoselache Cobelodus Akmonistion Damocles Falcatus Debeerius Chimaeroidei Chondrenchelys Helodus Iniopera Kawichthys

Fig. 6. Crown part of the strict consensus tree showing phylogenetic affi liation of Ferromirum gen. nov. to sym- moriform chondrichthyans. Colour coding: orange, stem Chondrichthyes without Acanthodii; blue, Elasmobranchii (crown Chondrichthyes); purple, Holocephali (crown Chondrichthyes). White circles: bootstrap support of knot > 50% and/ or Bremer decay values > 1; black circles: bootstrap support > 75% and/or Bremer decay values > 3. For the complete cladogram, see Fig. S1.

144 Chapter IV: Functional Morphology of Symmoriid Jaws

Fig. 7. Possible reconstruction of Ferromirum oukherbouchi gen. et sp. nov. and the thylacocephalans found in the Famennian of the Maïder region of Morocco. 2.3 Functional morphology of the mandibular the animal closed its mouth, the Meckel’s carti- arches lage rotates back into its initial position, i.e. both lower jaws rotated inward, possibly thereby im- Symmoriiformes show morphological conserva- proving the grip on prey items. tism in the jaw to braincase articulation among all its genera. This was tested by rescaling the braincase of Dwykaselachus oosthuizeni recon- structed by Coates [17] to the dimensions of the 3. Discussion well-preserved jaws of Ferromirum oukherbouchi gen. et sp. nov. and by virtually combining them. The neurocranial-mandibular articulation is quite All these elements fi t perfectly together, corrob- conservative in symmoriiform chondrichthyans orating their close relationships and functional as demonstrated by the perfect fi t between the similarities. The quadrate process articulates an- palatoquadrate of the Late Devonian Ferromirum teriorly with the postorbital process and serrated oukherbouchi gen. et sp. nov. and the braincase of edges of the palatine ramus joints with the orbital the much younger Early Permian Dwykaselachus. articulation of the braincase (Fig. 8A-B). The jaws fi t similarly well to the braincase of oth- er symmoriiforms such as Akmonistion or Cobe- Using a 3D-print of the computationally vi- lodus. Therefore, this type of articulation and its sualized 3D-model, the movement of the jaws function changed hardly through the evolution of was reconstructed. The shape of the jaw articula- this group. tion makes the Meckel`s cartilage rotate laterally while it is dropping. Therefore, a larger surface of The three-dimensionally preserved mandibu- the dentition is presented to the water column and lar arches enabled us to reconstruct the jaw func- prey (Fig. XX and video in preparation). When tion of these early chondrichthyans. Although the

145 Chapter IV: Functional Morphology of Symmoriid Jaws

Fig. 8. Neurocranium of Dwykaselachus oosthuizeni Oelofsen, 1986 virtually articulated with the mandibular arches (pink and blue) of Ferromirum oukherbouchi gen. et sp. nov. A, mouth closed. B, mouth opened; note the inward rotation along the sagittal axes when the mouth closes and the outward rotation during opening, which created a larger surface exposing functional teeth. feeding mechanisms in extant chondrichthyans are The discovery of Ferromirum gen. nov. also also poorly known, they display a high diversity challenges hypotheses on the arrangement and in prey capture including ram feeding, biting, suc- function of branchial arches in early gnatho- tion feeding, and fi lter feeding [37]. By contrast, stomes. During the last fi fty years, there was a the jaws are amphystylic in Palaeozoic chondrich- debate about if whether an aphetohyoidean con- thyans, thus implying a rather stiff articulation be- dition in early symmoriiform chondrichthyans tween the braincase and the jaws. Therefore, they existed or not [7, 8, 10, 18, 25, 30]. The apheto- did not perform jaw propulsion while snatching hyoidean hypothesis suggests that the hyoid was the prey as observable in extant elasmobranchs not closely attached to the upper jaw and there- with hyostylic jaws. The amphystylic jaw articu- fore, the hyoid lacked a suspensory function be- lation combined with grasping teeth suggests ram tween the mandibular arch and the braincase [39, feeding for symmoriiforms, phoebodontids, and 40]. This hypothesis seemed to be supported by xenacanthids [2, 12, 14, 15, 24, 38]. Additionally, a space between the hyoid and the upper jaws in the shape of the jaw articulation in Ferromirum the falcatid Ozarcus mapesae [8]. Accordingly, gen. nov. revealed a lateral rotation of the Meck- interpretations of cladoselachians and Cobelodus el`s cartilage while the animal was opening and as a non-aphetohoidean [7, 25] were doubted. The closing its mouth. Therefore, a larger surface of well-preserved branchial and mandibular arches the dentition becomes exposed to the prey, there- of Ferromirum gen. nov. show that indeed the by optimizing its predatory success. This partic- hyoid was very closely aligned to the mandibular ular feeding ecomorphology is unknown from arch without a gap and therefore, the hyoid had Recent chondrichthyans and might have vanished a supporting function. This new result falsifi es with the extinction of symmoriiforms. The mor- the aphetohyoidean hypothesis for symmoriiform phology of the visceral skeleton of Ferromirum chondrichthyans. gen. nov. differs from Palaeozoic chondrichthyans that performed suction prey capture. Early suction To conclude, Ferromirum oukherbouchi gen. feeders such as some hybodontids exhibit reduced et sp. nov. is a new symmoriid which refl ects the teeth, labial cartilages enclosing the mouth and a morphological conservatism of the Symmorii- massive ceratohyal that fl exibly articulates with formes and its well-preserved visceral skeleton the mandibular arches as it is involved in the suc- shows that the hyoid had a suspensory function, tion movement [16]. In the new symmoriiform thereby falsifying the aphetohyoidean hypothesis. portrayed here, labial cartilages are absent and the The reconstruction of the exceptionally preserved ceratohyals are slender and closely attached to the upper and lower jaws provide fi rst evidence for jaws (Fig. 4G), which were not suitable for suc- the jaw function in symmoriiform chondrich- tion feeding. thyans. As jaw function (subtle rotation of the lower jaws) is unknown from any other Palaeo-

146 Chapter IV: Functional Morphology of Symmoriid Jaws zoic (and probably Recent) chondrichthyan so far, bootstrap replicants (standard bootstrap and tra- these fi ndings signifi cantly improve the knowl- ditional search options in TNT 1.5) and Bremer edge about the ecomorphological diversity of support retaining trees suboptimal by 5 steps was their early relatives. performed for calculating the nodal supports.

4. Material and methods Acknowledgments

4.1 Specimen and anatomical reconstruction General: We are deeply indebted to Saïd Oukhar- based on computered tomograms bouch (Tafraoute, Morocco) who discovered the holotype and who supported us during fi eld work. The here described specimen (PIMUZ A/I The holotype was prepared by the team of the XXXX) of Ferromirum oukherbouchi gen. et sp. Tahiri Museum of Fossils and Minerals (Erfoud, nov. is housed at the Palaeontological Institute Morocco). Anita Schweizer (Zurich) and Alexan- and Museum of the University of Zurich, Swit- dra Wegemann (University of Zurich) kindly ac- zerland. The specimen was prepared out of a fer- quired CT-scans for us. Many thanks to Thodoris ruginous reddish nodule (rich in haematite) from Argyriou (University of Zurich) who helped seg- the Famennian (Late Devonian) of Madene El menting the image stack. Mrakib in the Maïder region of the southeastern Anti-Atlas (Morocco). Funding: The project (number S-74602-11-01) was fi nancially supported by the Swiss National The specimen was CT-scanned using an indus- Science Foundation. trial computer tomography scanner (Nikon XT H 225 ST) at the University of Zurich, Switzerland. Author contributions: L.F.: segmentation of Data acquisition and image reconstruction param- computer tomographs, preparing fi gures, drafting eters are: 224 kV, 474μA; fi lter: 4mm of copper; manuscript. C.K., M.C., L.F., creating the project. voxel sizes in mm: x = 0.091, y= 0.091, z = 0.091; C.K.: photography. M.C.: 3D-printing, interpreta- 16-bit TIFF images were acquired; 8-bit TIFF im- tion of 3D-models. All authors contributed to the ages were used for reconstruction. text.

Reconstruction of the 3D model was performed Competing interests: The authors declare no using Mimics v.17 (http://www.biomedical.ma- competing interests. terialise.com/mimics; Materialise, Leuven, Bel- gium) and the reconstructed 3D-object was edited Data and materials availability: In preparation. (smoothing, colours and lightning) in MeshLab v. 2016 (http://www.meshlab.net; [41]) and blend- er v2.79b (https://www.blender.org; Amsterdam, Netherlands). 3D prints of the palatoquadrates References and Meckel`s cartilages were made to reconstruct jaw biomechanics of this early chondrichthyan. 1. G. R. DeBeer, The Development of the Vertebrate Skull (Univ. Chicago, 1937). For the phylogenetic analysis, the data ma- 2. R. L. Carroll, Vertebrate paleontology and evolution trix of Frey et al. [27] was used. This matrix is (W. H. Freeman and Company, New York, 1988). based on gnathostome data matrices of Coates et 3. P. Janvier, Early Vertebrates (Oxford Univ. Press, al. [9, 17] and Brazeau [42], which contains data 1996) on Acanthodii published by Davis et al. [43] and 4. J. Mallat, Ventilation and the origin of jawed verte- Burrow et al. [44] and data on the outgroup from brates: a new mouth. Zool. J. Linn. Soc. 117, Zhu et al. [45] and Qiao et al. [46]. 228 characters, 329-404 (1996). 5. S. Kuratani, Evolution of the vertebrate jaw from 66 ingroup taxa and one outgroup taxon (Entelo- developmental perspective. Evol. Dev. 14, gnathus) were included in this data matrix. TNT 76-92 (2012). 1.5 (Tree Analysis Using New Technology [41]) 6. S. Kuratani, N. Adachi, N. Wada, Y. Oisi, F. Sugaha- was used to perform phylogenetic analyses via ra, Developmental and evoultionary signifi cance heuristic parsimony analysis (traditional search of the mandibular arch and prechordal/preman- in TNT) using 10000 multiple random addition dibular cranium in vertebrates: revising the sequences and swapping algorithm: tree bisection heterotopy scenario of gnathostome jaw evolution. reconnection (TBR) with 10 trees saved per rep- J. Anat. 222, 41-55 (2013). lication. The data was resampled by using 1000

147 Chapter IV: Functional Morphology of Symmoriid Jaws

7. J. G. Maisey, Visceral skeleton and musculature of a (1985). Late Devonian shark. J. Vertebr. Paleon- 23. M. I. Coates, S. E. K. Sequeira, The braincase of a tol. 9, 174–190 (1989). primitive shark. Trans. R. Soc. Edinb. (Earth Sci.) 8. A. Pradel, J. G. Maisey, P. Tafforeau, R. H. Mapes, J. 89, 63–85 (1998). Mallatt, A Palaeozoic shark with osteichthyan-like 24. M. I. Coates, S. E. K. Sequeira, A new stethacan- branchial arches. Nature 509, 608-611 (2014). thid chondrichthyan from the Lower Carboniferous 9. M.I. Coates, J.A. Finarelli, I.J. Sansom, P.S. An- of Bearsden, Scotland. J. Vertebr. Paleontol. 21, dreev, K.E. Criswell, K. Tietjen, M.L. Rivers, P.J. 754–766 (2001). La Riviere, An early chondrichthyan and the evo- 25. J. G. Maisey, The braincase in Paleozoic symmo- lutionary assembly of a shark body plan. Proc. R. riiform and cladoselachian sharks. Bull. Am. Mus. Soc. Lond., B, Biol. Sci. 285: 20172418. (2018) Nat. Hist. 307, 1–122 (2007). http://dx.doi.org/10.1098/rspb.2017.2418 26. A. Pradel, P. Tafforeau, J. G. Maisey, P. A. Janvier, 10. R. Zangerl, Handbook of Paleoichthyology: Chon- New Paleozoic Symmoriiformes (Chondrichthy- drichthyes I, Paleozoic Elasmobranchii, H.P. Schul- es) from the Late Carboniferous of Kansas (USA) tze, Ed. (Gustave Fischer, Stuttgart, New York, and Cladistic Analysis of Early Chondrichthyans. 1981), vol. 3A. PLoS ONE 6: e24938 DOI:10.1371/journal. 11. R. E. Plotnick, T. K. Baumiller, Invention by evolu- pone.0024938 (2011). tion: functional analysis in paleobiology. Pa- 27. L. Frey, M. Rücklin, D. Korn, C. Klug, Late Devo- leobiology 26(4), 305-323. nian and Early Carboniferous alpha diversity, 12. E.D. Grogan, R. A Lund, basal elasmobranch, Thr- ecospace occupation, vertebrate assemblages and inacoselache gracia n. gen & sp., (Thrinacodonti- bio-events of southeastern Morocco. Palae- dae, new family) from the Bear Gulch Limestone, ogeogr. Palaeoclimatol. Palaeoecol. 496, 1-17 Serpukhovian of Montana, USA. J Vertebr. Paleon- (2018). tol. 28(4), 970–988 (2008). 28. B. Schaeffer, The xenacanth shark neurocranium, 13. M. Ginter, Devonian fi lter-feeding sharks. Acta with comments on elasmobranch monophyly. Bull. Geol. Pol. 58(2), 147-153 (2008). Am. Mus. Nat. Hist. 169, 1–66 (1981). 14. M. Ginter, O. Hampe, C. J. Duffi n, Handbook of 29. Hotton, N. Jaws and teeth of American xenacanth Paleoichthyology: Chondrichthyes, Paleozoic Elas- sharks. J. Paleontol. 26, 489-500 (1952). mobranchii, teeth, H.P. Schultze, Ed. (Verlag Dr. 30. R. Zangerl, M.E. Williams. New evidence of the Friedrich Pfeil, München, 2010) vol. 3D. nature of the jaw suspension in Palaeozoic anacan- 15. L. Frey, M.I. Coates, M. Ginter, V. Hairapetian, M. thus sharks. Palaeontology 18, 333.341 (1975). Rücklin, I. Jerjen, C. Klug, Morphology, phyloge- 31. J. R., Dick. On the Carboniferous shark Tristychius netic relationships and ecomorphology of the early arcuatus Agassiz from Scotland. Earth Environ Sci elasmobranch Phoebodus (in preparation). Trans R Soc Edinb. 70(4), 63-108 (1978). 16. J. G. Maisey, Cranial anatomy of Hybodus basanus 32. G. J. Nelson, Gill arches and the phylogeny of fi sh- Egerton from the Lower Cretaceous of England. es, with notes on the classifi cation of vertebrates. Am. Mus. Novit. 2758, 1–64 (1983). Bull. Am. Mus. Nat. Hist. 141, 475–552 (1969). 17. M. I. Coates, R. W. Gess, J. A Finarelli, K. E 33. B. Dean, Studies on fossil fi shes (sharks, chimae- Criswell, K. A. Tietjen, symmoriiform chondrich- roids and arthrodires. Memoirs of the AMNH 9(5), thyan braincase and the origin of chimaeroid fi shes. 209-287 (1909C). Nature 541, 209-211 (2017). 34. U. H. J. Heidtke , C. Schwind, Über die Organisa- 18. R. Zangerl, G. R. Case, Cobelodus aculeatus tion des Skelettes der Gattung Xenacanthus (Elas- (Cope), an anacanthous shark from Pennsylvanian mobranchii: Xenacanthida) aus dem Unterperm Black Shales of North America. Palaeontographi- des südwestdeutschen Saar-Nahe-Beckens. Neu- ca A 154, 107–57 (1976). es Jahrb. Geol. Paläontol. Abhl. 231(1), 85–117 19. R. Lund, Stethacanthid elasmobranch remains (2004). from the Bear Gulch Limestone (Namurian E2b) of 35. U. H. J. Heidtke, C. Schwind, K. Krätschmer, Montana. Am. Mus. Novit. 2828, 1–24 (1985a). Über die Organisation des Skelettes und die ver- 20. R. Lund, The morphology of Falcatus falcatus (St. wandschaftlichen Beziehungen der Gattung Trio- John and Worthen), a Mississippian stethacanthid dus Jordan 1849 (Elasmobranchii: Xenacanthida). chndrichthyan from the Bear Gulch Limestone of Mainzer geowiss. Mitt. 32, 9-54 (2004). Montana. J. Vert. Paleontol. 5, 1-19 (1985b). 36. J. E. Harris, The dorsal fi n spine of Cladoselache. 21. R. Lund, On Damocles serratus nov. gen. et sp., Sci. publ. Clevel. Mus. Nat. Hist. 8, 1-6 (1938a). (Elasmobranchii: Cladodontida) from the Upper 37. P. J. Motta, Prey capture behavior and feeding me- Mississippian Bear Gulch Limestone of Montana. chanics of elasmobranchs. In Biology of sharks and J. Vert. Paleontol. 6, 12-19 (1986). their relative, P.L. Lutz, Ed. (CRC Press. 2004), pp. 22. Williams, M. E. The ‘‘cladodont level’’ sharks of 245-301. the Pennsylvanian Black Shales of central North 38. R. Lund, E. D. Grogan, Relationships of the Chi- America. Palaeontographica A 190, 83–158 maeriformes and the basal radiation of the Chon-

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drichthyes. Rev. Fish Biol. Fish 7, 65-123 (1997). and shark-like conditions in the last common an- 39. C. Gegenbaur, Untersuchungen zur vergleichenden cestor of modern gnathostomes. Nature 486, 247- Anatomie der Wirbelthiere. III. Das Kopfskelet der 250 (2012). (doi:10.1038/nature11080) Selachier, ein Beitrag zur Erkenntniss der Gene- 44. C.J. Burrow, J. den Blaauwen, M. Newman, R. se des Kopfskeletes der Wirbelthiere (Engelmann, Davidson, The diplacanthid fi shes (Acanthodii, Di- Leipzig, 1872). placanthiformes, Diplacanthidae) from the Middle 40. D. M. S. Watson, The acanthodian fi shes. Philos. Devonian of Scotland. Palaeontol. Electron. 19, Trans. Royal Soc. B 228, 49-146 (1937). 1-83 (2016). 41. P. Cignoni, M. Callieri, M. Corsini, M. Dellepiane, 45. M. Zhu, X. Yu, P.E. Ahlberg, B. Choo, J. Lu, Q.L. F. Ganovelli, G. Ranzuglia, MeshLab: an Open- Qiao, J. Zhao, H. Blom, Y. Zhu. A, Silurian plac- Source Mesh Processing Tool. Sixth Eurographics oderm with osteichthyan-like marginal jaw bones. Italian Chapter Conference, 129-136 (2008). Nature 502, 188-193 (2013). (doi:10.1038/na- 42. M. D. Brazeau, The braincase and jaws of a De- ture12617) vonian acanthodian and modern gnathostome ori- 46. T. Qiao, B. King, J.A. Long, P.E. Ahlberg, M. Zhu, gins. Nature 457, 305-308 (2009). (doi: 10.1038/ Early gnathostome phylogeny revisited: multi- nature07436) ple method consensus. PLoS ONE 11, e0163157 43. S.P. Davis, J.A. Finarelli, M.I. Coates, Acanthodes (2016). (doi:10.1371/journal.pone.0163157)

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SUPPLEMENTARY FIGURE

Entelognathus Youngolepis Guiyu 5/95 Psarolepis 5/93 Cheirolepis Mimipiscis 3/79 65 Raynerius 5/99 Moythomasia Culmacanthus 5/100 Ischnacanthus Nerepisacanthus Poracanthodes Tetanopsyrus Uraniacanthus 5/87 Diplacanthus 2/62 Rhadinacanthus Cassidiceps Mesacanthus 4 Promesacanthus Cheiracanthus Acanthodes 2 58 Homalacanthus Halimacanthodes Gladbachus Brachyacanthus Brochoadmones Climatius Parexus Ptomacanthus c knots. Colour coding: black, stem group gnathostome (outgroup); green, V waynensis fi Gyracanthides Latviacanthus Pucapampella Kathemacanthus Lupopsyrus Obtusacanthus Doliodus Acronemus Egertonodus Hamiltonichthys 2/54 Onychoselache Tribodus Squalus 4/52 3/94 Synechodus Tristychius Homalodontus 3 Cladodoides Phoebodus Thrinacodus Diplodoselache 2/54 Orthacanthus 2 4/83 Triodus Tamiobatis 5/85 Ferromirum gen. nov Dwykaselachus Ozarcus Cladoselache Cobelodus Akmonistion Damocles 2 5/71 Falcatus Debeerius Chimaeroidei Chondrenchelys 5/66 Helodus . Strict consensus tree including values of Bremer`s decay and bootstrap support at speci Iniopera 4 Kawichthys Fig. S1 Osteichthyes; red, Acanthodii (stem Chondrichthyes); orange, stem Chondrichthyes excluding Acanthodii; blue, Elasmobranchii (crown Chondrichthyes); purple, Holo- Acanthodii; blue, Elasmobranchii (crown Acanthodii (stem Chondrichthyes); orange, stem Chondrichthyes excluding Osteichthyes; red, more than 75; good support; 100: cephali (crown Chondrichthyes). Bremer scores: 3, good support; 5, highly supported. Boostrap values: more than 50: weak support, highest support.

150 Chapter IV: Functional Morphology of Symmoriid Jaws

Supplementary material 2. Taxa and sources

Acanthodes: Beznosov 2009; Brazeau & de Winter 2015; Coates 1994; Davis et al. 2012; Heidtke 1993, 2011a,b; Jarvik 1977, 1980; Miles 1968, 1973a, b; Nelson 1968; specimens AMNH 1037b, 10370, 10376, 19628; CMNH 30725b, 30726, 4591; FMNH PF2875; GM C145, 146, 180; HM V8251, 252; HU MB.F.4209, 4277, 4284, 4285, 7286, MB3b, 4a & b, 5a & b, 7a & b, 8a & b, 11a & b, 12a, 13a &b, 14a &b, 16a &b, 17a & b, 18a & b, 23 (resin copy), 24, MM L1693, 1698, 9432B, W1994; NHM P.11287, P.13139, 13140, 14558, 1728, 34912, 34914, 4057, 49941, 49944, 49959, 49967, 49979, 49980, 49990, 49995, 49996, 60928, 60939, 62138, 7335; NMS 2001.7.1, 3; UCL GM C1126; UMZC GN9, 11, 13, 14, 15a &b, 16, 39, 756. Acronemus: Maisey 2011; Rieppel 1982. Akmonistion: Coates & Sequiera 1998, 2001a, b; Coates et al. 1998; Coates et al. 2017. Brachyacanthus: Denison 1979; Miles 1973a; Watson 1937; specimens NMS Kinnaird 88, NMS (Powrie) 1891.92.212, 213, 214, 220, 222, 224, 225, 226, 227. Brochoadmones: Bernacsek & Dineley 1977; Gagnier & Wilson 1996b; Hanke & Wilson 2006; specimens UALVP 32672, 41487, 41493, 41494, 41495. Callorhinchus/Hydrolagus: Cole 1896; De Beer 1937; De Beer & Moy-Thomas 1935; Didier 1995; Didier et al. 1994, 2012; Howard et al. 2013; Kesteven 1937; Patterson 1965, 1992; Pradel et al. 2013; Stahl 1999. Cassidiceps: Gagnier & Wilson 1996a; specimen UALVP 32454. Cheiracanthus: Denison 1979; Miles 1973a; Watson 1937; specimens AMNH 317, 6929, 7082; GM C295, 296, 325, 490; HM V7614; IC 214, 215, 216, 217; UMZC GN14a &b, 19, 20, 21, 31, 50; 1131a & b, 1132a & b, 1133a & b, 1134a & b, 1135a & b, 1136a & b, 1137a & b, 1138, 1139, 1140. Cheirolepis: Arratia & Cloutier 1996; Pearson & Westoll 1979; Giles et al. 2015a. Chondrenchelys: Finarelli & Coates 2012, 2014; Lund 1982; Moy-Thomas 1935; specimens NMS 1885.54.5/5A, 1891.53.33, 1998.35.1, 2002.68.1; BGS-GSE 13328; HM V.7173. Cladodoides: Gross 1937, 1938; Maisey 2005. Cladoselache: Bendix-Almgreen 1975; Harris 1938a, b; Maisey 1989a, 2007; Schaeffer 1981; Williams 2001; Woodward & White 1938; specimens CMNH 8110, 8111, 8207, NHM P9273, P9285. Climatius: Miles 1973a, b; Watson 1937: specimens AMNH 7762; GSM 49785; MM L12096a & b; NMS Kinnaird 80; NMS 1881.5.62; NMS 1887 (Peach) 35.3a, 35.5b, 35.5e; NMS 1891 (Powrie) 92.195, 204, 206, 214; NMS 1967.12.4; NMS 1973.9.4; NMS 2001.7.2. Cobelodus: Zangerl & Case 1976; Zidek 1992. Culmacanthus: Long 1983. Damocles: Lund 1986: specimens CM 35472, 48760. Debeerius: Grogan & Lund 2000: specimens CM 35479, 35480, 48831, 62811. Ferromirum oukherbouchi gen. et sp. nov.: holotype specimen PIMUZ XX. Diplacanthus: Gagnier 1996; Miles 1973a; Watson 1937; specimens FMNH PF11633; GM C12, 13, 148; GM P482; MM L5503, 1609; NMS (Powrie) 1891.92.334; NMS 2001.7.4; UMZC GN17, 18, 22. Diplodoselache: Dick 1981. Doliodus: Miller et al. 2003; Maisey et al. 2009, 2013, 2017; Long et al. 2015. Dwykaselachus: Coates et al. 2017; Oelofsen 1986; specimen SAM K5840. Egertonodus: Maisey 1982, 1983; Lane, 2010. Entelognathus: Zhu et al. 2013. Falcatus: Lund 1985; Maisey 2007; specimens CM 35465, 37532. Gladbachus: Heidtke & Krätschmer 2001; Heidtke 2009; Burrow & Turner 2013; specimen UMZC 2000.32. Guiyu: Zhu et al. 2009. Gyracanthides: Miles 1973a; Warren et al. 2000; Turner et al. 2005. Halimacanthodes: Burrow et al. 2012. Hamiltonichthys: Maisey 1989b. Helodus: Patterson 1965; Stahl 1999; specimens NHM P.6706, 8207, 8209, 8212, 8213. Homalacanthus: Gagnier 1996; Watson 1937; specimens FMNH PF4875; MM LL12452. Homalodontus: Mutter et al. 2007, 2008.

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Iniopera: Zangerl & Case 1973; Pradel et al. 2009, Pradel 2010; Pradel et al. 2010. Ischnacanthus; Miles 1973a; Watson 1937; specimens GM C3, 6, 149, 324; GM P298; MM L9522, 9431, 9432; MM STR0585; NMS (Powrie) 92.254, 258; UALVP 32401, 32405, 32414, 39060, 39075, 40478, 41491, 41861, 42201, 42215, 42660, 43245, 44048, 44049, 44091, 45014. Kathemacanthus: Gagnier & Wilson 1996a; Hanke & Wilson 2010; specimens UALVP 32402, 42269, 43113. Kawichthys: Pradel et al. 2011. Latviacanthus: Schultze & Zidek 1982. Lupopsyrus: Hanke & Davis 2012; Bernacsek & Dineley 1977; specimens NMC 22700B, 22700C, 22715, 22718, 22719, 22700D, 22700E, 22700F, 22701C, 22701D, 22716, 22717, 22720, 22745; UALVP 19260, 32420, 32442, 32456, 32458, 32474, 32476, 32480, 32482, 39065, 39067, 39079, 39080, 39081, 39082, 39121, 41493, 41629, 41632, 41665, 41931, 41939, 41945, 42000, 42002, 42008, 42012, 42013, 42027, 42046, 42061, 42113, 42142, 42150, 42173, 42208, 42274, 42518, 42524, 42529, 42530, 42533, 42538, 42453, 42454, 42455, 42544, 42597, 42605, 43064, 43091, 43092, 43094, 43095, 43256, 43409, 43456, 45154, 45155. Mesacanthus: Miles 1973a; Watson 1937; specimens FMNH PF1439; GM C18, 288a &b; NMS (Powrie) 1891.92.275; UMZC GN1143. Mimipiscis: Gardiner & Bartram 1977; Gardiner 1984; Choo 2011; Giles & Friedman 2014. Moythomasia: Gardiner & Bartram 1977; Gardiner 1984; Coates et al. 2017; specimen MV P222915. Nerepisacanthus: Burrow 2011; Burrow & Rudkin 2014. Obtusacanthus: Hanke & Wilson 2004; specimen UALVP 41488. Onychoselache: Dick & Maisey 1980; Coates & Gess 2007. Orthacanthus: Heidtke 1982, 1999; Hotton 1952; Schaeffer 1981; Maisey 1983; Lane & Maisey 2009. Ozarcus and FMNH PF 13242: Maisey 2007; Pradel et al. 2014; Coates et al. 2017. Parexus: Watson 1937; Miles 1973a. specimens AMNH 1163, 7766; NMS Kinnaird 94; NMS (Peach) 1887.35.3a, 5e; NMS 1891 (Powrie) 92.183, 184, 186, 188, 194, 197, 207; NMS 1956.14.4.15; NMS 1977.46.3a & b. Phoebodus: Newberry 1889; Ginter 1990; Ginter & Ivanov 1992, 1995; Ginter et al. 2002; Ginter et al. 2010; specimen PIMUZA/I 4656, PIMUZ A/I 4710, PIMUZ A/I 4712, PIMUZ A/I 4711, PIMUZ A/I 4713. Poracanthodes: Denison 1979; Valiukevicius 1992. Promesacanthus: Hanke 2008; specimens UALVP 41672, 41859, 41860, 42652, 43027. Psarolepis: Yu 1998; Zhu & Schultze 1997; Zhu et al. 1999; Qu et al. (2013). Ptomacanthus: Brazeau 2009, 2012; Denison 1979; Miles 1973a; specimens BM P.19999, 24919b. Pucapampella: Maisey 2001a; Maisey & Anderson 2001; Maisey & Lane 2010; Janvier & Maisey 2010. Raynerius: Giles et al. 2015b. Rhadinacanthus: Burrow et al. 2016. Squalus: Schaeffer 1981; Gans & Parsons 1964; Marinelli & Strenger 1959. Synechodus: Maisey 1985; NHM P.6135, 41675. Tamiobatis: Eastman 1897A; Schaeffer 1981; Williams 1998; specimen FMNH PF5414. Tetanopsyrus: Gagnier & Wilson 1995; Gagnier et al. 1999; Hanke et al. 2001; specimens UALVP 32571, 38682, 39062, 39078, 42512, 43026, 43246, 44030, 43089. Thrinacodus: Turner 1982; Ginter 2000; Ginter & Sun 2007; Ginter & Turner 2010; Ginter et al. 2010; Grogan & Lund 2008. Tribodus: Maisey & de Carvalho 1997; Lane 2010; Lane & Maisey 2009, 2012. Triodus: Solér-Gijon & Hampe 1998; Hampe 2003; Heidtke et al. 2004. Tristychius: Dick1978; Coates & Gess 2007; Coates & Tietjen 2018. Uraniacanthus: Bernacsek & Dineley 1977; Hanke & Davis 2008; Newman et al. 2012; Burrow et al. 2016; specimens UALVP 19259, 32448, 32469, 38679, 41669, 41857, 41858, 41862, 42095, 42095, 44046, 45366 to 45396. Vernicomacanthus waynensis: Miles 1973a. Youngolepis: Chang & Yu 1981; Chang 1982, 1991, 2004.

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3. Character list

Skeletal tissues 1 Tessellate calcifi ed cartilage: absent (0); present (1). Brazeau (2009); Coates & Sequeira (2001a, b); Davis et al. (2012); Dean & Summers (2006); Dean et al. (2009); Grogan et al. (2012); Maisey (1984, 2001, 2013); Lund & Grogan (1997, 2004a, b); Seidel et al. (2016). 2 Perichondral bone: present (0); absent (1). Janvier (1996); Donoghue & Aldridge (2001); Brazeau (2009); Davis et al. (2012); Lund (1985); Coates et al. (1999). 3 Extensive endochondral ossifi cation: absent (0); present (1). Forey (1980); Gardiner (1984); Brazeau (2009); Davis et al. (2012). 4 Extensive calcifi ed cartilage: absent (0); present (1). Coates et al. (2018). 5 Dentine kind: mesodentine or semidentine (0); orthodentine (1). Donoghue et al. (2000); Brazeau (2009); Davis et al. (2012); Burrow et al. (2016) 6 Pore canal network: absent (0); present (1). Lu et al. (2016). 7 Acrodin tooth caps (enameloid cap restricted to crown apex): absent (0); present (1). Friedman & Brazeau (2010); Zhu et al. (2009, 2013); Lu et al. (2016).

Squamation & related structures 8 Trunk scales monocuspid (0); multicuspid (1). Revised after Davis et al. (2012); Burrow et al. (2016). 9 Scale growth concentric: absent (0); present (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Burrow et al. (2016). 10 Peg-and-socket articulation: absent (0); present (1). Gardiner (1984); Coates (1999); Brazeau (2009); Davis et al. (2012). 11 Anterodorsal process on scale: absent (0); present (1). Zhu et al. (2009, 2013); Gardiner (1984); Coates (1999); Brazeau (2009); Davis et al. (2012). 12 Body scales with bulging base: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Burrow et al. (2016). 13 Body scales with fl attened base: absent (0); present (1). Brazeau (2009, 2012); Davis et al. (2012); Burrow et al. (2016). 14 Body scales with basal canal or open basal vascular cavity: absent (0); present (1). Reif (1978); Coates & Sequeira (2001a); Young (1982). 15 Neck canal: absent (0) present (1). Coates et al. (2017). 16 Sensory line canal passes between or beneath scales (0); passes over scales and/ or is partially enclosed or surrounded by scales (1); perforates and passes through scales (2). Davis (2002); Friedman & Brazeau (2010); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014); Burrow et al. (2016). 17 Lepidotrichia or lepidotrichia-like scale alignment: present (0); absent (1). Davis et al. (2012). 18 Epichordal lepidotrichia: absent (0); present (1). Zhu et al. (2009, 2013). 19 Fringing fulcra: absent (0); present (1). Zhu et al. (2009, 2013); Coates (1999). 20 Scute-like ridge scales (fulcra): absent (0); present (1). Giles et al. (2015c).

Cranial dermal skeleton 21. Sclerotic ring: absent (0); present (1). Giles et al. (2015c); Qiao et al. (2016); Zhu et al. (2016); Burrow et al. (2016). 22 Number of sclerotic plates: four or less (0); more than four (1). Zhu et al. (2013, c170); Qiao et al. (2016, c.241); Zhu et al. (2016, c.239); Burrow et al. (2016). 23 Dermal ornamentation: smooth (0); parallel, vermiform ridges (1); concentric ridges (2); tuber- culate (3). Giles et al. (2015c). 24 Dermal skull roof includes large dermal plates (0); consists of undifferentiated plates, tesserae or scales (1); naked or largely scale free (2). Forey (1980); Gardiner (1984); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 25 Cranial tessera morphology: large interlocking plates (0); microsquamose, no larger than body squamation (1). Brazeau (2009) through to Giles et al. (2015c). 26 Anterior or mesial edge of nasal notched for anterior nostril: absent (0); present (1). Contra Zhu et al. (2013), the anterior rim of the nasal in Cheirolepis is notched.

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27 Supraorbital: absent (0); present (1). Zhu et al. (2009, 2013). 28 Large median bone contributes to posterior margin of skull roof: absent (0); present (1). Zhu et al. (2016). 29 Medial process of paranuchal wraps around posterolateral corners of nuchal plate: absent (0); present (1); paranuchals precluded from nuchal by centrals (2); no median bone in posterior of skull roof (3). Giles et al. (2015c). 30 Pineal opening perforates dermal skull roof: present (0); absent (1). Davis et al. (2012); Giles et al. (2015c). 31 Consolidated cheek plates: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 32 Enlarged postorbital tessera separate from orbital series: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 33 Dermal intracranial joint: absent (0); present (1). Zhu et al. (2009, 2013) 34 Foramina (similar to infradentary foramina) on cheek bones: absent (0); present (1). Zhu et al. (2009, 2013). 35 Preopercular bone: absent (0); present (1). Zhu et al. (2013). 36 Maxilla expanded posteriorly: absent - splint shaped (0); present - cleaver shaped (1). Zhu et al. (2009, 2013); Lu et al. (2016). 37 Sensory line network preserved as open grooves (sulci) in dermal bones (0); sensory lines pass through canals enclosed within dermal bones (1). (Davis 2002); Davis et al. (2012); Zhu et al. (2013). 38 Sensory canal or pit-line associated with maxilla: absent (0); present (1). Friedman (2007) 39 Jugal portion of infraorbital canal joins supramaxillary canal: present (0); absent (1). Brazeau (2009), but see redefi nition in Davis et al. (2012); Zhu et al. (2013). 40 Anterior pit line of skull roof: absent (0); present (1). Giles et al. (2015c). 41 Spiracular opening in dermal skull roof bounded by bones carrying otic canal: absent (0); pres- ent (1). Giles et al. (2015); Lu et al. (2016). 42 Endolymphatic ducts open in dermal skull roof: present (0); absent (1). Janvier (1996); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Giles et al. (2015c). 43 Dermohyal (submarginal) ossifi cation: absent (0); present (1). 44 Dermohyal (submarginal) shape: broad plate that tapers towards its proximal end (0); narrow plate (1). Brazeau’s (2009) 45 Branchiostegal series: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 46 Opercular and subopercular bones: absent (0); present (1). 47 Branchiostegal plate series along ventral margin of lower jaw: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 48 Branchiostegal ossifi cations plate-like (0); narrow and ribbon-like (1); fi lamentous (2). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Lu et al. (2016). 49 Branchiostegal ossifi cations ornamented (0); unornamented (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 50 Branchiostegals imbricated: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 51 Opercular cover of branchial chamber complete or partial (0); separate gill covers and gill slits (1). Lund & Grogan (1997); Hanke & Wilson (2004); Davis et al. (2012); Zhu et al. (2013). 52 Gular plates: absent (0); present (1). Gardiner (1984); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 53 Size of lateral gular plates: extending most of length of the lower jaw (0); restricted to the anteri- or third of the jaw (no longer than the width of three or four branchiostegals) (1). Coates (1999); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013).

Hyoid and gill arches1 54 Gill skeleton mostly beneath otico-occipital region (0); mostly posterior to occipital region (1). Zangerl (1981); Lund & Grogan (1997); Stahl (1999). 55 Perforate hyomandibula: absent (0); present (1). Zhu et al. (2009, 2013); Lu et al. (2016). 56 Interhyal: absent (0); present (1). Davis et al. (2012); Zhu et al. (2013).

154 Chapter IV: Functional Morphology of Symmoriid Jaws

57 Ceratohyal smooth with posterior, lateral fossa: absent (0); present (1). Coates et al. (2018). 58 Ceratohyal anteriorly blade-shaped: absent (0), present (1). Frey et al. (in prep.). Tristychius and Phoebodus exhibit ceratohyals with an anteriorly derived shape. 59 Hypohyals: absent (0); present (1). Friedman & Brazeau (2010); Pradel et al. (2014). 60 Basihyal absent, hyoid arch articulates directly with basibranchial (0); basihyal present (1). Pradel et al. (2014); see also discussion in Carr et al. (2009); Brazeau et al. (2017). 61 Separate supra- and infra-pharyngobranchials absent (0); present (1). Gardiner (1984); Pradel et al. (2014). 62 Pharyngobranchials directed anteriorly (0); posteriorly (1). Pradel et al. (2014). 63 Posteriormost branchial arch bears epibranchial unit: absent (0); present (1). Coates et al. (2018). Absent in osteichthyans; present in chondrichthyans, Gladbachus and Acanthodes (Davis et al. 2012; Pradel et al. 2014). 64 Epibranchials bear posterior fl ange: absent (0); present (1). Coates et al. (2018). 65 Hypobranchials directed anteriorly (0); hypobranchials of second and more posterior gill arches directed posteriorly (1). Coates et al. (2018).

Dentition & tooth-bearing bones and cartilages 66 Oral dermal tubercles borne on jaw cartilages: absent (0); present (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 67 Pharyngeal teeth or denticles: absent (0); present (1). Coates et al. (2017, 2018). 68 Tooth families/ whorls: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 69 Bases of tooth families/ whorls: single, continuous plate (0); some or all whorls consist of sepa- rate tooth units (1). Adjusted by Coates et al. (2018) from Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Giles et al. (2015). 70 Lingual torus: absent (0); present (1). After Ginter et al. 2010; Coates et al. (2018). 71 Basolabial shelf: absent (0); present (1). Coates et al. (2017), after Ginter et al. (2010) 72 Tooth families/whorls restricted to symphysial region (0); distributed along jaw margin (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 73 Number of tooth families/whorls per jaw ramus: 15 or fewer (0); 20 or more (1). Coates et al. (2018). 74 Toothplates absent (0); present (1). Follows defi nition of Coates et al. (2018). 75 Toothplate complement restricted to two pairs in the upper jaw and a single pair in the lower jaw: absent (0); present (1). After Patterson (1965); Coates et al. (2018). 76 Mandibular teeth fused to dermal plates on biting surfaces of jaw cartilages: absent (0); present (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 77 Dermal plates on biting surface of jaw cartilages: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Giles et al. (2015c). 78 Gnathal plates mesial to and/ or above (or below) jaw cartilage: absent (0); present (1). Zhu et al. (2016). 79 Maxilla and premaxilla sensu stricto (upper gnathal plates lateral to jaw cartilage without pala- tal lamina): absent (0); present (1). Zhu et al. (2016). 80 Dentary bone encloses mandibular sensory canal: absent (0); present (1). Gardiner (1984) and references therein; Zhu et al. (2009, 2013). 81 Infradentary foramen and groove, series: absent (0); present (1). Zhu et al. (2010). 82 Tooth-bearing median rostral: absent (0); present (1). Zhu et al. (2009, 2013). 83 Median dermal bone of palate (parasphenoid): absent (0); present (1). Gardiner (1984); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 84 Denticulated fi eld of parasphenoid: without spiracular groove (0); with spiracular groove (1). Friedman (2007); Zhu et al. (2009, 2013). 85 Denticle fi eld of parasphenoid with multifi d anterior margin: absent (0); present (1). Friedman (2007); Zhu et al. (2009, 2013); Lu et al. (2016).

Mandibular arch 86 Large otic process of the palatoquadrate: absent (0); present (1). Coates & Sequeira (2001a); Davis (2002); Brazeau (2009); Zhu et al. (2009, 2013).

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87 Oblique ridge or groove along medial face of palatoquadrate: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Lu et al. (2016). 88 Fenestration of palatoquadrate at basipterygoid articulation: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Lu et al. (2016). 89 Perforate or fenestrate anterodorsal (metapterygoid) portion of palatoquadrate: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 90 Articulation surface of the palatoquadrate with the postorbital process directed anteriorly (0); laterally (1); dorsally (2). Coates et al. (2017). 91 Palatoquadrate fused to the neurocranium: absent (0); present (1). Coates et al. (2017). 92 Pronounced dorsal process on Meckelian bone or cartilage: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 93 Mandibular mesial process: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 94 Jaw articulation located on rearmost extremity of mandible: absent (0); present (1). Davis et al. (2012); Zhu et al. (2013).1 95 Dental sulcus (trough) adjacent to oral rim on Meckel’s cartilage and palatoquadrate: absent (0); present (1). Coates et al. (2017). 96 Scalloped oral margin on Meckel’s cartilage and palatoquadrate: absent (0); present (1). Coates et al. (2017). Characteristic of some symmoriiform chondrichthyans such as Akmonistion, Ozarcus, and Cladoselache, but also present in Helodus (pers. obs. MIC). 97 Mandibular symphysis fused: absent (0); present (1). Coates et al. (2017).

Neurocranium 98 Internasal vacuities: absent (0); present (1). Lu et al. (2016). 99 Precerebral fontanelle: absent (0); present (1). Schaeffer (1981); Lund & Grogan (1997); Coates & Sequeira (1998, 2001a, b); Maisey (2001a); Brazeau (2009); Pradel et al. (2011) Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 100 Space for forebrain and (at least) proximal portion of olfactory tracts narrow and elongate, ex- tending between orbits: absent (0); present (1). Coates et al. (2017). 101 Prominent, pre-orbital, rostral expansion of the neurocranium: present (0); absent (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 102 Rostral bar: absent (0); present (1). Adapted from Maisey (1985); Coates et al. (2017). 103 Internasal groove absent (0); present (1). Coates et al. (2017); present in Iniopera and Dwykasela- chus (Pradel 2010). 104 Orbitonasal lamina dorsoventrally deep: absent (0); present (1). Patterson (1965); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2017). 105 Palatobasal (or orbital) articulation posterior to the optic foramen (0); anterior to the optic foramen, grooved, and overlapped by process or fl ange of palatoquadrate (1); anterior to optic foramen, smooth, and overlaps or fl anks articular surface on palatoquadrate (2). Adapted by Coates et al. (2018) from Pradel et al. (2011, character 26), Coates et al. (2017, character 71) and Maisey (2005, p.61) 106 Trochlear nerve foramen anterior to optic nerve foramen: absent (0); present (1). Coates & Se- queira (2001). 107 Supraorbital shelf broad with convex lateral margin: absent (0); present (1). Coates & Sequeira (1998); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 108 Orbit directed mostly laterally and free of fl anking endocranial cartilage or bone: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2018). 109 Interorbital space broad (0); narrow (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2017). 110 Optic pedicel: absent (0); present (1). Dupret et al. (2014); Zhu et al. (2009, 2013); Coates et al. (2017). 111 Ophthalmic foramen in anterodorsal extremity of orbit communicates with cranial interior: absent (0); present (1). Coates et al. (2017). 112 Extended prehypophysial portion of sphenoid: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 113 Canal for efferent pseudobranchial artery within basicranial cartilage: absent (0); present (1).

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Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 114 Entrance of internal carotids: through separate openings fl anking the hypophyseal opening or recess (0); through a common opening at the central midline of the basicranium (1). Schaeffer (1981); Coates & Sequeira (1998); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 115 Internal carotids: entering single or paired openings in the basicranium from a posterolateral angle (0); entering basicranial opening(s) head-on from an extreme, lateral angle (1); absent (2). Coates et al. (2017). 116 Ascending basisphenoid pillar pierced by common internal carotid: absent (0); present (1). Miles (1973b); Brazeau (2009); Friedman & Brazeau (2010); Davis et al. (2012); Zhu et al. (2013). 117 Spiracular groove on basicranial surface: absent (0); present (1). Davis et al. (2012); Zhu et al. (2013). 118 Spiracular groove on lateral or transverse wall of jugular canal: absent (0); present (1). Davis et al. (2012); Zhu et al. (2013). 119 Spiracular groove open (0); enclosed by spiracular bar or canal (1). Lu et al. (2016), Coates et al. (2018). 120 Orbit larger than otic capsule: absent (0); present (1). Lund & Grogan (1997); Coates et al. (2017). 121 Postorbital process and arcade: absent (0); present (1). Pradel et al. (2011); see also Maisey (2007) and Coates et al. (2017). 122 Postorbital process and arcade short and deep - width not more than maximum braincase width (excluding arcade) (0); process and arcade wide - width exceeds maximum width of braincase, and anteroposteriorly narrow (1); process and arcade massive (2); arcade forms postorbital pillar (3). Coates et al. (2017). 123 Postorbital process downturned, with anhedral angle relative to basicranium: absent (0); pres- ent (1). Present in hybodontids, Acronemus (Maisey 2011) and Tristychius (Dick 1978; Coates & Tietjen 2018). 124 Jugular canal diameter small (0); large (1); canal absent (2). Pradel et al. (2011); Coates et al. (2018). 125 Canal, likely for trigeminal nerve (V) mandibular ramus, passes through the postorbital process from proximal dorsal entry to distal and ventral exit: absent (0); present (1). (Coates et al., 2017) 126 Postorbital process expanded anteroposteriorly: absent (0); present (1). (Coates et al. 2018). 127 Postorbital process articulates with palatoquadrate: absent (0); present (1). Schaeffer (1981); Coates & Sequeira (1998); Maisey (2001a); Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). 128 Trigemino-facial recess: absent (0); present (1). Goodrich (1930); Gardiner (1984 and references therein); Pradel (2010); Pradel et al. (2011); Davis et al. (2012). 129 Jugular canal long, extends throughout most of otic capsule wall posterior to the postorbital process (0); short and/ or groove present on exterior of otic wall (1); absent, path of jugular re- moved from otic wall (2). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Giles et al. (2015c); Coates et al. (2017). 130 C-bout notch separates postorbital process from supraotic shelf: absent (0); present (1). Charac- teristic feature of Tristychius, present in Acronemus (Maisey 2011). 131 Postorbital fossa: absent (0); present (1). Zhu et al. (2013). 132 Hyoid ramus of facial nerve (N. VII) exits through posterior jugular opening: absent (0); pres- ent (1). Friedman (2007); Brazeau (2009); Friedman & Brazeau (2010); Davis et al. (2012); Zhu et al. (2013). 133 Periotic process: absent (0); present (1). Maisey (2007); Coates et al. (2017). 134 Articulation facet for hyomandibula: single-headed (0), double-headed (1). Zhu et al. (2009, 2013). 135 Relative position of jugular groove and hyomandibular articulation: hyomandibula dorsal or same level (i.e. on bridge) (0); jugular vein passing dorsal or lateral to hyomandibula (1). Brazeau & de Winter (2015). 136 Transverse otic process: absent (0); present (1). Lu et al. (2016); Giles et al. (2016) 137 Craniospinal process: absent (0); present (1). Giles et al. (2015); Lu et al. (2016). 138 Lateral otic process: absent (0); present (1). Schaeffer (1981); Coates & Sequeira (1998); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 139 Hyomandibula articulates with neurocranium beneath otic shelf: absent (0); present (1). 140 Sub-otic occipital fossa: absent (0); present (1). Coates et al. (2017, 2018).

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141 Postotic process: absent (0); present (1). Pradel et al. (2011); Coates et al. (2017). 142 Otic capsule extends posterolaterally relative to occipital arch: absent (0); present (1). Maisey (1985). 143 Otic capsules: widely separated (0); approaching dorsal midline (1). Coates et al. (2017). 144 Otic capsules project anteriorly between postorbital processes: absent (0); present (1). Coates et al. (2018). 145 Endocranial roof anterior to otic capsules dome-like, smoothly convex dorsally and anteriorly: absent (0); present (1). Coates et al. (2017). 146 Roof of skeletal cavity for cerebellum and mesencephalon signifi cantly higher than dorsal-most level of semicircular canals: absent (0); present (1). Coates et al. (2017). 147 Roof of the endocranial space for telencephalon and olfactory tracts offset ventrally relative to level of mesencephalon: absent (0); present (1). Coates et al. (2017). 148 Labyrinth cavity separated from the main neurocranial cavity by a cartilaginous or ossifi ed capsular wall (0); skeletal medial capsular wall absent (1). Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). 149 Double octaval nerve foramena in chondrifi ed mesial wall of otic capsule: absent (0); present (1). Coates et al. (2018). 150 External (horizontal) semicircular canal joins the vestibular region dorsal to posterior ampulla (0); joins level with posterior ampulla (1). Davis et al. (2012); Zhu et al. (2013). 151 Angle of external semicircular canal: in lateral view, straight line projected through canal in- tersects anterior ampulla, external ampullae, and base of foramen magnum: absent (0); present (1). Coates et al. (2017). 152 Left and right external semicircular canals approach or meet the posterodorsal midine of the hindbrain roof: absent (0); present (1). Coates et al. (2017). 153 Preampullary portion of posterior semicircular canal absent (0); present (1). Coates et al. (2017). 154 Crus commune connecting anterior and posterior semicircular canals present (0); absent (1). Coates et al. (2017). 155 Sinus superior: absent or indistinguishable from union of anterior and posterior canals with saccular chamber (0); present, elongate and nearly vertical (1). Davis et al. (2012); Zhu et al. (2013). 156 Lateral cranial canal: absent (0); present (1). Zhu et al. (2009, 2013); Lu et al. (2016). 157 Endolymphatic ducts: posteriodorsally angled tubes (0); tubes oriented vertically through endo- lymphatic fossa/posterior dorsal fontanelle (1). Schaeffer (1981); Coates & Sequeira (1998, 2001); Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 158 Posterior dorsal fontanelle connected to persistent otico-occipital fi ssure (0); posterior tectum separates fontanelle from fi ssure (1). Schaeffer (1981); Coates & Sequeira (1998); Pradel et al. (2011). 159 Subcircular endolymphatic foramen: absent (0); present (1). Pradel et al. (2015), Coates et al. 2017. 160 External opening for endolymphatic ducts anterior to crus commune: absent (0); present (1). Coates et al. (2017). 161 Supraotic shelf broad: absent (0); present (1). Coates et al. (2017). 162 Dorsal otic ridge: absent (0); present (1). Coates & Sequeira (1998, 2001); Maisey (2001); Davis (2002); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 163 Dorsal otic ridge forms a crest posteriorly: absent (0); present (1). Coates & Sequeira (1998, 2001); Pradel et al. (2011). 164 Endolymphatic fossa: absent (0); present (1). Pradel et al. (2011). 165 Endolymphatic fossa elongate (slot-shaped), dividing dorsal otic ridge along midline: absent (0); present (1). Coates et al. (2017). 166 Perilymphatic fenestra within the endolymphatic fossa: absent (0); present (1). Pradel et al. (2011); Coates et al. (2017). 167 Ventral cranial fi ssure: absent (0); present (1). Janvier (1996); Coates & Sequeira (2001); Maisey (2001); Davis (2002); Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). 168 Endoskeletal intracranial joint: absent (0); present (1). Janvier (1996); Davis et al. (2012); Zhu et al. (2013). 169 Metotic (otic-occipital) fi ssure: absent (0); present (1). Schaeffer (1981); Janvier (1996); Coates

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& Sequeira (1998); Maisey (2001); Davis (2002); Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). 170 Vestibular fontanelle: absent (0); present (1). Brazeau (2009); Friedman & Brazeau (2010). Davis et al. (2012); Zhu et al. (2013). 171 Hypotic lamina: absent (0); present (1). Schaeffer (1981); Maisey (1984, 2001); Brazeau (2009); Pradel et al. (2011, 2013); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2017). 172 Glossopharyngeal nerve path: directed laterally, across fl oor of the saccular chamber and exits via foramen in side wall of the otic capsule (0); directed posteriorly, and exits through metotic fi ssure or foramen in posteroventral wall of otic capsule (1); exits laterally through a canal con- tained ventrally (fl oored) by the hypotic lamina (2); exits through a foramen anterior to the pos- terior ampulla (3). Coates et al. (2017), adapted from Schaeffer (1981); Coates & Sequeira (1998, 2001); Brazeau (2009): Davis et al. (2012); Zhu et al. (2013); Pradel et al. (2011, 2013). 173 Glossopharyngeal and vagus nerves share common exit from neurocranium: absent (0); present (1). Coates et al. (2017). 174 Basicranial morphology: platybasic (0); tropibasic (1). Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Zhu et al. (2013). 175 Channel for dorsal aorta and/or lateral dorsal aortae passes through basicranium (0): exter- nal to basicranium (1). Schaeffer (1981); Coates & Sequeira (1998); Brazeau (2009); Pradel et al. (2011); Brazeau & Friedman (2014); Coates et al. (2017). 176 Dorsal aorta divides into lateral dorsal aortae posterior to occipital level (0); anterior to level of the occiput (1). Pradel et al. (2011); Giles et al. (2015); Coates et al. (2017). 177 Ventral portion of occipital arch wedged between rear of otic capsules: absent (0); present (1). Schaeffer (1981); Coates & Sequeira (1998); Maisey (2001a); Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Coates et al. (2017). 178 Dorsal portion of occipital arch wedged between otic capsules: absent (0); present (1). Schaeffer (1981); Coates & Sequeira (1998); Maisey (2001a); Brazeau (2009); Pradel et al. (2011); Davis et al. (2012); Coates et al. (2017). 179 Occipital crest anteroposteriorly elongate, and extends from the roof of the posterior tectum: absent (0); present (1). Coates et al. (2018).

Axial and appendicular skeleton 180 Calcifi ed vertebral centra: absent (0); present (1). Maisey (1985); Coates et al. (2017). 181 Chordacentra: absent (0); present (1). Stahl (1999); Coates and Sequeira (2001); Coates et al. (2017). 182 Chordacentra polyspondylous and consist of narrow closely packed rings: absent (0); present (1). Derived from Patterson (1965); Coates et al. (2017). 183 Synarcual: absent (0); present (1). Stahl (1999); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Coates et al. (2017). 184 Macromeric dermal pectoral girdle (0); micromeric or lacking dermal skeleton entirely (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 185 Macromeric dermal pectoral girdle composition: ventral and dorsal components (0); ventral components only (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 186 Macromeric pectoral dermal skeleton forms complete ring around the trunk: present (0); ab- sent (1). Goujet & Young (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 187 Median dorsal plate: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 188 Scapular process (dorsal) of shoulder endoskeleton: absent (0); present (1). Coates & Sequeira (2001a); Zhu & Schultze (2001); Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 189 Ventral margin of separate scapular ossifi cation: horizontal (0); deeply angled (1). Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 190 Cross sectional shape of scapular process: fl attened or strongly ovate (0); subcircular (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 191 Flange on trailing edge of scapulocoracoid: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 192 Scapular process with posterodorsal process: absent (0); present (1). Coates & Sequeira (2001a); Davis et al. (2012); Zhu et al. (2013).

159 Chapter IV: Functional Morphology of Symmoriid Jaws

193 Mineralisation of internal surface of scapular process: mineralised all around (0); un-min- eralised on internal face forming a hemicylindrical cross-section. Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Burrow et al. (2016). 194 Coracoid process: absent (0); present (1). Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 195 Procoracoid mineralisation: absent (0); present (1). Davis (2002); Hanke & Wilson (2004): Brazeau (2009). 196 Fin base articulation on scapulocoracoid: stenobasal, deeper than wide (0); eurybasal, wider than deep (1). Lu et al. (2016). 197 Pectoral fi n articulation monobasal (0); dibasal (1); three or more basals (2). 198 Metapterygium pectinate subtriangular plate or bar supporting numerous (six or more) radials along distal edge: absent (0); present (1). Coates et al. (2018). 199 Metapterygial whip: absent (0); present (1). Coates et al. (2017). 200 Biserial pectoral fi n endoskeleton: absent (0); present (1). Lu et al. (2016). 201 Propterygium perforated: absent (0); present (1). Rosen et al. (1981); Patterson (1982); Davis et al. (2012); Zhu et al. (2013). 202 Pelvic girdle with fused puboischiadic bar: absent (0); present (1). Maisey (1984); Coates & Se- queira (2001a); Coates et al. (2017). 203 Mixipterygial/ mixopterygial claspers: absent (0), present (1). Coates & Sequeira (2001a, b); Brazeau & Friedman (2014). 204 Pre-pelvic clasper or tenaculum: absent (0); present (1). After Patterson (1965); Coates et al. (2017). 205 Number of dorsal fi ns, if present: one (0); two (1); one, extending from pectoral to anal fi n level (2). Coates & Sequeira (2001a); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 206 Brush complex of bilaterally distributed calcifi ed tubes fl anking or embedded in calcifi ed carti- lage core: absent (0); present (1). Coates et al. (2017, 2018) 207 Posterior or pelvic-level dorsal fi n with calcifi ed base plate: absent (0); present (1). Coates & Sequeira (2001a, b). 208 Posterior dorsal fi n with delta-shaped cartilage: absent (0); present (1). Coates & Sequeira (2001a, b). 209 Posterior or pelvic-level dorsal fi n shape, base approximately as broad as tall and not broader than other median fi ns (0); base much longer than fi n height, substantially longer than other median fi ns (1). Brazeau & deWinter (2015); Lu et al. (2017). 210 Anal fi n: absent (0); present (1). Coates & Sequeira (2001); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 211 Anal fi n base narrow, posteriormost proximal segments radials broad: absent (0); present (1). Heidtke (1999). 212 Caudal radials restricted to axial lobe (0); extend beyond level of body wall and deep into hypo- chordal lobe (1). Davis et al. (2012); Zhu et al. (2013). 213 Caudal neural and/or supraneural spines or radials short (0); long, expanded, and supporting high aspect-ratio (lunate) tail with notochord extending to posterodorsal extremity (1); noto- chord terminates pre-caudal extremity, neural and heamal radial lengths near symmetrical and support epichordal and hypochordal lobes respectively (2). Coates & Sequeira (2001a, b).

Spines: fi ns, cranial and elsewhere 214 Dorsal fi n spine or spines: absent (0); present (1). Zhu et al. (2001); Zhu & Yu (2002); Friedman (2007); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013); Lu et al. (2016). 215 Dorsal fi n spine at anterior (pectoral level) location only: absent (0); present (1). Coates & Sequei- ra (2001a); Ginter et al. (2010). 216 Dorsal fi n spine cross section: horseshoe shaped (0); fl at sided, with rectangular profi le (1); sub- circular (2). Hampe (2003); Brazeau & de Winter (2015). 217 Anterior dorsal fi n spine leading edge concave in lateral view: absent (0); present (1). Lund (1985, 1986). 218 Anal fi n spine: absent (0); present (1). Maisey (1986); Davis (2002); Brazeau (2009). 219 Pectoral fi n spines: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 220 Pectoral fi n spine with denticles along posterior surface: absent (0); present (1). Burrow et al.

160 Chapter IV: Functional Morphology of Symmoriid Jaws

(2016). 221 Prepectoral fi n spines: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). Present in Doliodus (Maisey et al. 2017). 222 Admedian pectoral spines absent (0); present (1). Burrow et al. (2016); see also description of Doliodus pectoral girdle (Maisey et al. 2017). 223 Median fi n spine insertion: shallow, not greatly deeper than dermal bones/ scales (0); deep (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009). Davis et al. (2012); Zhu et al. (2013). 224 Intermediate (pre-pelvic) fi n spines: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 225 Fin spines with ridges: absent (0); present (1). Davis (2002); Brazeau (2009); Davis et al. (2012); Zhu et al. (2013). 226 Fin spines with nodes: absent (0); present (1). Davis (2002); Hanke & Wilson (2004); Brazeau (2009). Davis et al. (2012); Zhu et al. (2013). 227 Fin spines (dorsal) with rows of large denticles: absent (0); on posterior surface (1); on lateral surface (2). Maisey (1989b); Davis et al. (2012); Zhu et al. (2013); Brazeau & Friedman (2014). 228 Cephalic spines: absent (0); present (1). Maisey (1989); Coates et al. (2017)

4. References crossopterygian from Yunnan, south-western China. Doctor- al dissertation, Department of Geology, Stockholm University (1982). Arratia, G. & Cloutier, R. in Devonian Fishes and Plants of Migua- Chang, M. M. Head exoskeleton and shoulder girdle of Youngole- sha, Quebec, Canada (eds. Schultze, H.-P. & Cloutier, R.) 165- pis. In Early vertebrates and related problems of evolutionary 197 (Verlag Dr. Friedrich Pfeil, Munich, 1996). biology, M. M. Chang, Y. H. Liu & G. R. Zhang, eds. (Beijing: Bendix-Almgreen, S. E. The paired fi ns and shoulder girdle in Science Press), pp. 355-378 (1991). Cladoselache, their morphology and phyletic signifi cance. Chang, M. M. Synapomorphies and scenarios - more characters of Colloques Internationaux du Centre National de la Recherche Youngolepis betraying its affi nity to the Dipnoi. In Recent Ad- Scientifi que 218, 111-123 (1975). vances in the Origin and Early Radiation of Vertebrates, G. Ar- Bernacsek, G.M., & Dineley, D.L. New acanthodians from the Delo- ratia, M. V. H. Wilson & R. Cloutier, eds. (München: Verlag Dr. rme Formation (Lower Devonian) of N.W.T., Canada. Paleonto- Friedrich Pfeil), pp. 665-686 (2004). graphica Abt.A 158, 1-25 (1977). Chang, M.-M. & Yu, X.-B. A new crossopterygian, Youngolepis Brazeau, M. D. The braincase and jaws of a Devonian ‘acanthodian’ praecursor, gen. et sp. nov., from Lower Devonian of E. Yun- and modern gnathostome origins. Nature 457, 305-308 (2009). nan, China. Sci. Sin. 24, 89-97 (1981). Brazeau, M. D. A revision of the anatomy of the early Devonian Choo, B. Revision of the actinopterygian genus Mimipiscis (= jawed vertebrate Ptomacanthus anglicus Miles. Palaeontology Mimia) from the Upper Devonian Gogo Formation of West- 55, 355-367 (2012). ern Australia and the interrelationships of early Actinopterygii. Brazeau, M. D. & Friedman, M. The characters of Palaeozoic jawed Earth and Environmental Science Transactions of the Royal So- vertebrates. Zoological Journal of the Linnean Society, 170, ciety of Edinburgh, 102, 77-104 (2011) 779-821 (2014). Coates, M. I. Endocranial preservation of a Carboniferous actinopte- Brazeau, M. D. & de Winter, V. The hyoid arch and braincase anato- rygian from Lancashire, UK, and the interrelationships of prim- my of Acanthodes support chondrichthyan affi nity of ‘acantho- itive actinopterygians. Philosophical Transactions of the Royal dians’. Proc. R. Soc. B 282: 20152210 (2015). Society of London. Series B: Biological Sciences, 354 (1382), Brazeau, M. D., Friedman, M., Jerve, A., & Atwood, R. C. A 435-462 (1999). three-dimensional placoderm (stem-group gnathostome) pha- Coates, M.I., Finarelli, J.A., Sansom, I.J., Andreev, P.S., Criswell, ryngeal skeleton and its implications for primitive gnathostome K.E., Tietjen, K., Rivers, M.L. & La Riviere, P.J. An early pharyngeal architecture. Journal of Morphology. DOI: 10.1002/ chondrichthyan and the evolutionary assembly of a shark body jmor.20706 (2017). plan. Proceedings of the Royal Society B 285: 20172418. (2018) Burrow, C. J. A partial articulated acanthodian from the Silurian of http://dx.doi.org/10.1098/rspb.2017.2418 New Brunswick, Canada. Canadian Journal of Earth Sciences Coates, M.I., & Gess, R.W. A new reconstruction of Onychoselache 48(9), 1329–1341. doi:10.1139/e11-023 (2011). traquairi, comments on early chondrichthyan pectoral girdles Burrow, C. J., den Blaauwen, J., Newman, M. & Davidson, R. The and hybodontiform phylogeny. Palaeontology, 50(6), 1421- diplacanthid fi shes (Acanthodii, Diplacanthiformes, Diplacan- 1446 (2007). thidae) from the Middle Devonian of Scotland. Palaeontologica Coates, M. I., Gess, R. W., Finarelli, J. A., Criswell, K. E. & Tietjen, Electronica 19, 1-83 (2016). K. A symmoriiform chondrichthyan braincase and the origin of Burrow, C. J. & Rudkin, D. Oldest near-complete acanthodian: chimaeroid fi shes. Nature 541, 209-211 (2017). the fi rst vertebrate from the Silurian Bertie formation Konser- Coates, M. I., Sansom, I. J. & Smith, M. M. Spines and tissues of vat-Lagerstätte, Ontario. PLoS ONE 9(8), DOI:10.1371/journal. ancient sharks. Nature 396, 729-730 (1998). pone.0104171 (2014). Coates, M. I. & Sequeira, S. E. K. The braincase of a primitive shark. Burrow, C. J., Trinajstic, K. & Long, J. First acanthodian from the Trans. R. Soc. Edinb. (Earth Sci.) 89, 63-85 (1998). Upper Devonian (Frasnian) Gogo Formation, Western Austra- Coates, M. I. & Sequeira, S. E. K. A new stethacanthid chondrich- lia. Historical Biology 24, DOI:10.1080/08912963.2012.66015 thyan from the Lower Carboniferous of Bearsden, Scotland. J. 0 (2012). Vertebr. Paleontol. 21, 754-766 (2001a). Burrow, C. J. & Turner, S. Scale structure of the putative chondrich- Coates, M. I. & Sequeira, S. E. K. in Major Events in Early Verte- thyan Gladbachus adentatus Heidtke & Krätschmer, 2001 from brate Evolution (ed. Ahlberg, P. E.) 241-262 (Taylor and Fran- the Middle Devonian Rheinisches Schiefergebirge, Germany. cis, 2001b). Historical Biology 25, 385-390 (2013). Coates, M. I. & Tietjen, K. The neurocranium of the Lower Car- Carr, R. K., Johanson, Z. & Ritchie, A. The phyllolepid placoderm boniferous shark Tristychius arcuatus (Agassiz, 1837). Earth Cowralepis mclachlani: insights into the evolution of feed- and Environmental Science Transactions of the Royal Society ing mechanisms in jawed vertebrates. J. Morph. 270, 775-804 of Edinburgh (2018). (2009). Cole, F. J. On the cranial nerves of Chimaera monstrosa (Linn.); with Chang, M. M. The braincase of Youngolepis, a Lower Devonian a discussion of the lateral line system and of the morphology of

161 Chapter IV: Functional Morphology of Symmoriid Jaws

the chorda tympani. Trans. R. Soc. Edinb. 38, 631-680 (1896). Hist. (Geol.) 37, 173-428 (1984). Davis, S. P. Comparative anatomy and relationships of the acanthodi- Giles, S., Coates, M., Garwood, R. J., Brazeau, M. D., Atwood, R., an fi shes. Unpublished PhD thesis, Unv. London, 1-318. (2002). Johanson, Z. & Friedman, M. Enodskeletal structure in Cher- Davis, S. P., Finarelli, J. A., & Coates, M. I. Acanthodes and shark- olepis (Osteichthyes, Actinopterygii), an early ray-fi nned fi sh. like conditions in the last common ancestor of modern gnatho- Palaeontology 2015, DOI:10.1111/pala. 12182 (2015a). stomes. Nature 486, 247-250 (2012). Giles, S., Darras, L., Clément, G., Blieck, A. & Friedman, M. An ex- Dean, M. N. & Summers, A. P. Cartilage in the skeleton of cartilagi- ceptionally preserved Late Devonian actinopterygian provides nous fi shes. Zoology 109,164-168 (2006). a new model for primitive cranial anatomy in ray-fi nned fi shes. Dean, M. N., Mull, C. G., Gorb, S. N. & Summers, A. P. Ontogeny of Proc. R. Soc. B 282: 20151485 (2015b). the tessellated skeleton: insight form the skeletal growth of the Giles, S., Friedman, M. Virtual reconstruction of endocast anatomy round stingray Urobatis halleri. J. Anat. DOI:10.1111/j.1469- in early ray-fi nned fi shes (Osteichthyes, Actinopterygii). Jour- 7580.2009.01116x (2009). nal of Paleontology, 88(4), 636-651 (2014). Denison, R. in Handbook of Paleoichthyology Vol. 5 (ed. Schultze, Giles, S., Friedman, M. & Brazeau, M. D. Osteichthyan-like cranial H.-P.) (Gustav Fischer Verlag, Stuttgart, 1979). conditions in an Early Devonian stem gnathostome. Nature 520, Dick, J. R. F. On the Carboniferous shark Tristychius arcuatus Agas- 82-85 (2015c). siz from Scotland. Trans. R. Soc. Edinb. 70, 63-109 (1978). Ginter, M. Late Famennian shark teeth from the Holy Cross Mts, Dick, J. R. F. Diplodoselache woodi gen. et sp. nov., an early Car- Central Poland. Acta Geologica Polonica 40, 69-81 (1990). boniferous shark from the Midland Valley of Scotland. Trans. R. Ginter, M. Late Famennian pelagic shark assemblages. Acta Geolog- Soc. Edinb. 72, 99-113 (1981). ica Polonica 50(2), 369-386 (2000). Dick, J. R. F. & Maisey, J. G. The Scottish Lower Carboniferous Ginter, M., Hairapetian, V. & Klug, C. Famennian chondrichthyans shark Onychoselache traquairi. Palaeontology 23, 363-374 from the shelves of North Gondwana. Acta Geologica Polonica (1980). 52(2), 169-215 (2002). Didier, D. A. Phylogenetic systematics of extant chimaeroid fi sh- Ginter, M., Hampe, O. & Duffi n, C. J. Chondrichthyes: Paleozoic es (Holocephali, Chimaeroidei). Am. Mus. Novit. 3119, 1-86 Elasmobranchii: teeth, in: Schultze, H. (Ed.), Handbook of Pa- (1995). leoichthyology, 3D, 168 p. (2010). Didier, D. A., Kemper, J. M. & Ebert, D. A. in Biology of Sharks and Ginter, M. & Ivanov, A. Devonian phoebodont shark teeth. Acta Pa- Their Relatives (eds Carrier, J. C., Musick, J. & Heithaus, M. R.) laeontologica 97-122 (CRC Press, 2012). Polonica 37(1), 55-75 (1992). Didier, D. A., Stahl, B. J. & Zangerl R. Development and growth of Ginter, M. & Ivanov, A. Middle/Late Devonian Phoebodont-based compound tooth plates in Callorhinchus milii (Chondrichthyes, ichthyolith zonation. [Zonation ichthyologique du Dévonien Holocephali). Journal of Morphology 222, 73-89 (1994). moyen/supérieur fondée sur les Phoebodontes]. Geobios 19, Donoghue, P.C.J., & Aldridge, R. J. in Major events in early verte- 351-355 (1995). brate evolution: palaeontology, phylogeny, genetics and devel- Ginter, M. & Sun, Y. Chondrichthyan remains from the Lower Car- opment. (ed Ahlberg, P. E.) 85–105 (Taylor & Francis, 2001). boniferous of Muhua, southern China. Acta Palaeontologica Donoghue, P. C. J., Forey, P. L., & Aldridge, R. J. Conodont affi nity Polonica 52(4), 705-727 (2007). and chordate phylogeny. Biol. Rev.75, 191-251 (2000). Ginter, M. & Turner, S. The middle Paleozoic Selachian genus Thri- Dupret, V., Sanchez, S., Goujet, D., Tafforeau, P. & Ahlberg, P. E. nacodus. Journal of Vertebrate Paleontology 30(6), 1666-1672, A primitive placoderm sheds light on the origin of the jawed (2010), doi:10.1080/02724634.2010.520785. vertebrate face. Nature 507, 500-503 (2014). Goodrich E. S. Studies on the structure and development of verte- Eastman, C. R. Tamiobatis vetustus: a new form of fossil skate. brates (Univ. Chicago Press, 1930). American Journal of Science Goujet D, & Young G. C. in Recent Advances in the Origin and Early 4(4), 85-90 (1897A). Radiation of Vertebrates, (eds Arratia, G., Wilson, M. V. H. & Finarelli, J. A. & Coates, M. I. First tooth-set outside the jaws in a Cloutier, R.) 109-26 (Friedrich Pfeil, 2004). vertebrate. Proceedings of the Royal Society of London Series Grogan, E. D. and Lund, R. Debeerius ellefseni (Fam. Nov., Gen. B-Biological Sciences 279, 775-779 (2012). Nov., Sped. Nov.) an Autodiastylic Chondrichthyan From the Finarelli, J. A. & Coates, M. I. Chondrenchelys problematica (Tra- Mississippian Bear Gulch Limestone of Montana (USA), the quair, 1888) redescribed: a Lower Carboniferous, eel-like ho- Relationships of the Chondrichthyes, and Comments on Gna- locephalan from Scotland. Earth and Environmental Science thostome Evolution. J. Morphol. 243, 219-245 (2000). Transactions of the Royal Society of Edinburgh 105, 1-25 Grogan, E.D. & Lund, R. A basal elasmobranch, Thrinacoselache (2014). gracia n. gen & sp., (Thrinacodontidae, new family) from the Forey, P. L. Latimeria: a paradoxical fi sh. Proc. R. Soc. London, Ser. Bear Gulch Limestone, Serpukhovian of Montana, USA. Jour- B 208, 369-384 (1980). nal of Vertebrate Paleontology 28(4), 970-988 (2008). Friedman, M. Styloichthys as the oldest coelacanth: implications for Grogan, E. D., Lund, R. & Greenfest-Allen, E. in Biology of Sharks early osteichthyan interrelationships. J. Syst. Palaeontol. 5, 289- and Their Relatives (eds Carrier, J. C., Musick, J. A. & Heithaus, 343 (2007). M. R.) 3-29 (CRC Press, 2012). Friedman, M. & Brazeau, M. A reappraisal of the origin and basal Gross, W. Das Kopfskelett on Cladodus wildungensis Jaekel; 1. Teil. radiation of the Osteichthyes. J. Vertebr. Paleontol. 30, 36-56 Endocranium und Palatoquadratum. Senckenbergiana 19, 80- (2010). 107 (1937). Gans, C. & Parsons, T. S. A Photographic Atlas of Shark Anatomy Gross, W. Das Kopfskelett on Cladodus wildungensis Jaekel; 2. Teil. (Academic Press, New York, 1964). Der Kieferbogen. Anhang: Protractodus vetusus Jaekel. Senck- Gagnier, P. Y. in Devonian Fishes and Plants of Miguasha, Quebec, enbergiana 20, 123-145 (1938). Canada. (eds Schultze, H. P. & Cloutier, R.) 149-163 (Freidrich Hampe, O. Revision of the Xenacanthida (Chondrichthyes: Elasmo- Pfeil, 1996). branchii) from the Carboniferous of the British Isles. Trans. R. Gagnier, P. Y., Hanke, G. F. & Wilson, M. V. H. Tetanopsyrus lin- Soc. Edinb. (Earth Sci.) 93, 191-237 (2003). doei gen. et sp. nov., an Early Devonian acanthodian from the Hanke G. F. Promesacanthus eppleri n. gen., n. sp., a mesacanthid Northwest Territories, Canada. Acta Geologica Polonica 49, 81- (Acanthodii, Acanthodiformes) from the Lower Devonian of 96 (1999). northern Canada. Geodiversitas 30, 287-302 (2008). Gagnier, P. Y. & Wilson, M. V. H. New evidences on jaw bones and Hanke, G. F. & Davis, S. P. Redescription of the acanthodian Gladio- jaw articulations in acanthodians. Geobios 19 (1995). branchus probaton Bernacsek & Dineley, 1977, and comments Gagnier, P. Y. & Wilson, M. V. H. Early Devonian acanthodians from on diplacanthid relationships. Geodiversitas 30, 303-330 (2008). northern Canada. Palaeontology 39, 241-258 (1996a). Hanke, G. F. & Davis, S. P. A re-examination of Lupopsyrus pygmae- Gagnier P. Y. & Wilson M. V. H. An unusual acanthodian from us Bernacsek & Dineley, 1977 (Pisces, Acanthodii). Geodiversi- Northern Canada: revision of Brochoadmones milesi. Modern tas 34, 469-487 (2012). Geology 20, 235-251 (1996b). Hanke, G. F., Davis, S. P. & Wilson, M. V. H. A new species of Gardiner, B. G. The relationships of the palaeoniscoid fi shes, a re- the acanthodian genus Tetanopsyrus from Northern Canada, view based on new specimens of Mimia and Moythomasia from with comments on related taxa. J. Vert. Paleontol. 21, 740-753 the Upper Devonian of Western Australia. Bull. Br. Mus. Nat. (2001).

162 Chapter IV: Functional Morphology of Symmoriid Jaws

Hanke, G. F., & Wilson, M. V. H. in Recent Advances in the Origin tralia sheds new light on the development of tessellated calci- and Early Radiation of Vertebrates. (eds Arratia, G., Wilson, M. fi ed cartilage. PLoS ONE 10: e0126066 DOI:10.1371/journal. V. H., & Cloutier, R.) 189–216 (Freidrich Pfeil, 2004). pone.0126066 (2015). Hanke, G. F. & Wilson, M. V. H. Anatomy of the Early Devonian Lund, R. Harpagofututor volsellorhinus new genus and species Acanthodian Brochoadmones milesi based on nearly complete (Chondrichthyes, Chondrenchelyiformes) from the Namurian body fossils, with comments on the evolution and development Bear Gulch Limestone, Chondrenchelys problematica Traquair of paired fi ns. J. Vert. Paleontol. 26, 526-537 (2006). (Visean), and their sexual dimorphism. Journal of Paleontology Hanke, G. F., & Wilson, M. V. H. in Morphology, Phylogeny and 56, 938-958 (1982). Paleobiogeography of Fossil Fishes. (eds Elliot, D.K., Maisey, Lund, R.. Stethacanthid elasmobranch remains from the Bear Gulch J.G., Yu, X. & Miao, D.) 159-182 (Freidrich Pfeil, 2010). Limestone (Namurian E2b) of Montana. American Museum No- Harris, J. E. The dorsal fi n spine of Cladoselache. Scientifi c Pub- vitates 2828, 1-24 (1985a). lications of the Cleveland Museum of Natural History 8, 1-6 Lund, R. The morphology of Falcatus falcatus (St. John and Worth- (1938a). en), a Mississippian stethacanthid chndrichthyan from the Bear Harris, J. E. The neurocranium and jaws of Cladoselache. Scientif- Gulch Limestone of Montana. Journal of Vertebrate Paleontol- ic Publications of the Cleveland Museum of Natural History 8, ogy 5, 1-19 (1985b). 7-12 (1938b). Lund, R. On Damocles serratus nov. gen. et sp., (Elasmobranchii: Heidtke, U. H. J. Der Xenacanthide Orthacanthus senckenbergianus Cladodontida) from the Upper Mississippian Bear Gulch Lime- aus dem pfälzischen Rotliegenden (Unter-Perm). Pollichia 70, stone of Montana. Journal of Vertebrate Paleontology 6, 12-19 65-86 (1982). (1986). Heidtke, U. Studien über Acanthodes. 4. Acanthodes boyi n. sp., die Lund, R. & Grogan, E. D. Relationships of the Chimaeriformes and dritte Art der Acanthodier (Acanthodii: Pisces) aus dem Rotlie- the basal radiation of the Chondrichthyes. Reviews in Fish Biol- gend (Unterperm) des Saar-Nahe-Beckens (S-W-Deutschland. ogy and Fisheries 7, 65-123 (1997). Paläont. Z. 67, 331-341 (1993). Lund, R. & Grogan, E. D. in Recent Advances in the Origin and Ear- Heidtke, U. H. J. Orthacanthus (Lebachacanthus) senckenbergianus ly Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Fritsch 1889 (Xenacanthida: Chondrichthyes): revision, organi- Cloutier, R.) 171-187 (Friedrich Pfi el, 2004a). sation und phylogenie. Freiberger Forschungsheft 481, 63-106 Lund, R. & Grogan, E. D. in Recent Advances in the Origin and Ear- (1999). ly Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Heidtke, U. H. J. Gladbachus adentatus, die Geschichte des weltweit Cloutier, R.) 505-531 (Friedrich Pfi el, 2004b). ältesten Hais – untersucht und beschriebenaus dem AK Geowis- Maisey, J. G. The anatomy and interrelationships of Mesozoic hy- senschaften. Pollichia Kurrier 25, 24-26 (2009). bodont sharks. Am. Mus. Novit. 2724, 1-48 (1982). Heidtke, U. H. J. Neue Erkenntnisse über Acanthodes bronni Agassiz Maisey, J. G. Cranial anatomy of Hybodus basanus Egerton from 1833. Mitt. Pollichia 95, 1-14 (2011a). the Lower Cretaceous of England. Am. Mus. Novit. 2758, 1-64 Heidtke, U. H. J. Revision der unterpermischen Acanthodier (Acan- (1983). thodii: Pisces) des südwestdeutschen Saar-Nahe-Beckens. Mitt. Maisey, J. G. Cranial Morphology of the Fossil Elasmobranch Syn- Pollichia 95, 15-41 (2011b). echodus dubrisiensis. Am. Mus. Novit. 2804, 1-28 (1985). Heidtke, U. H. J. & Krätschmer K. Gladbachus adentatus nov. gen. Maisey, J. G. Visceral skeleton and musculature of a Late Devonian et sp., ein primitiver Hai aus dem Oberen Givetium (Oberes Mit- shark. J. Vertebr. Paleontol. 9, 174-190 (1989a). teldevon) der Bergisch Gladbach – Paffrath-Mulde (Rheinisches Maisey, J. G. Hamiltonichthys mapesi g. & sp. nov. (Chondrichthy- Schiefergebirge). Mainzer geowiss. Mitt. 30, 105-122 (2001). es; Elasmobranchii), from the Upper Pennsylvanian of Kansas. Heidtke, U. H. J., Schwind, C. & Krätschmer K. Über die Organisa- American Museum Novitates 2931, 1-42 (1989b). tion des Skelettes und die verwandschaftlichen Beziehungen der Maisey, J. G. in Major Events in Early Vertebrate Evolution (ed. Ahl- Gattung Triodus Jordan 1849 (Elasmobranchii: Xenacanthida). berg, P. E.) 263-288 (Taylor and Francis, 2001a). Mainzer geowiss. Mitt. 32, 9-54 (2004). Maisey, J. G. Remarks on the inner ear of elasmobranchs and its in- Hotton, N. Jaws and teeth of American xenacanth sharks. Journal of terpretation from skeletal labyrinth morphology. J. Morph. 250, Paleontology 26, 489-500 (1952). 236-264. (2001b). Howard, L. E., Holmes, W. M., Ferrando, S., Maclaine, J. S., Kelsh, Maisey, J. G. Braincase of the Upper Devonian shark Cladodoides R. N., Ramsey, A., Abel R. L. & Cox P. L. J. Functional nasal wildungensis (Chondrichthyes, Elasmobranchii), with observa- morphology of chimaeroid fi shes. Journal of Morphology 274: tions on the braincase in early chondrichthyans. Bull. Am. Mus. 987-1009 (2013). Nat. Hist. 288, 1-103 (2005). Janvier, P. Early Vertebrates (Oxford Univ. Press, 1996). Maisey, J. G. The braincase in Paleozoic symmoriiform and cladose- Janvier, P. & Maisey, J. G. (2010) in Morphology, Phylogeny and lachian sharks. Bull. Am. Mus. Nat. Hist. 307, 1-122 (2007). Paleobiogeography of Fossil Fishes. (eds Elliot, D.K., Maisey, Maisey, J. G. The braincase of the Middle Triassic shark Acronemus J.G., Yu, X. & Miao, D.) 431-459 (Freidrich Pfeil, 2010). tuberculatus (Bassani, 1886). Palaeontology 54, 417-428 Jarvik, E. in Problems in Vertebrate Evolution. (eds Andrews, S. M., (2011). Miles, R. S., Walker & A. D.) 199-225 (Linnean Symposium Maisey, J. G. The diversity of tessellated calcifi cation in modern and Series, London, 1977). extinct chondrichthyans. Revue de Paléobiologie, Geneve 32, Jarvik, E. Basic Structure and Evolution of Vertebrates (Academic, 355-371 (2013). 1980). Maisey, J. G. & Anderson, M. E. A primitive chondrichthyan brain- Kesteven, H. L. The anatomy of the head of Callorhynchus antarcti- case from the Early Devonian of South Africa. Journal of Verte- cus. Journal of Anatomy 67, 443-474 (1937). brate Paleontology 21, 702-713 (2001). Lane, J. A. Morphology of the braincase in the Cretaceous hybodont Maisey, J. G. & de Carvalho, M. R. A new look at old sharks. Nature shark Tribodus linnae (Chondrichthyes: Elasmobranchii), based 385, 779-780 (1997). on CT scanning. Amer. Mus. Novitates 2758, 1-70 (2010). Maisey, J. G. & Lane, J. A. Labyrinth morphology and the evolution Lane, J. A. & Maisey, J. G. Pectoral anatomy of Tribodus limae of low-frequency phonoreception in elasmobranchs. C. R. Pa- (Elasmobranchii: Hybodontiformes) from the Lower Cretaceous levol 9, 289-309. (2010) of Northeastern Brazil. Journal of Vertebrate Paleontology 29, Maisey, J. G., Miller, R. & Turner, S. The braincase of the chon- 25-38 (2009). drichthyan Doliodus from the Lower Devonian Campbellton Lane, J. A. & Maisey, J. G. The visceral skeleton and jaw suspension Formation of New Brunswick, Canada. Acta Zoologica 90 (sup- in the durophagous hybodontid shark Tribodus limae from the plement 1), 109-122 (2009). Lower Cretaceous of Brazil. Journal of Paleontology 86, 886- Maisey, J. G., Miller, R., Pradel, A., Denton, J. S. S., Bronson, A. & 905 (2012). Janvier, P. Pectoral morphology in Doliodus: bridging the ‘ac- Long, J. A. A new diplacanthoid acanthodian from the Late Devoni- anthodian’-chondrichthyan divide. American Museum Novitates an of Victoria. Memoirs of the Association of Australasian Pa- 3875, 1-15. (2017). laeontologists 1, 51-65 (1983). Maisey, J. G., Turner, S., Naylor, G. J. P. & Miller, R. F. Dental pat- Long, J. A., Burrow, C. J., Ginter, M., Maisey, J., Trinajstic, K. M., terning in the earliest sharks: implications for tooth evolution. Coates, M. I., Young, G. C. & Senden, T. J. First shark from Journal of Morphology. DOI:10.1002/jmor.20242 (2013) the Late Devonian (Frasnian) Gogo Formation, Western Aus- Marinelli, W. & Strenger, A. Vergleichende Anatomie und Morpholo-

163 Chapter IV: Functional Morphology of Symmoriid Jaws

gie der Wirbeltiere. III. 174-308 (Franz Deuticke, Wien, 1959). ONE 11, DOI:10.1371/journal.pone.0163157 (2016). Miles, R. S. Articulated acanthodian fi shes from the Old Red Sand- Reif, W. E. Types of morphogenesis of the dermal skeleton in fossil stone of England, with a review of the structure and evolution sharks. Paläont. Z. 52, 110-128 (1978). of the acanthodian shoulder- girdle. Bull. Br. Mus. Nat. Hist. Reif, W. E. Squamation and ecology of sharks. Cour. Forsch.-Inst. (Geol.) 24, 111-213 (1973a). Senckenberg 78, 1-255 (1985). Miles, R. S. in Interrelationships of Fishes (eds Greenwood, P. H., Rieppel, O. A new genus of shark from the Middle Triassic of Monte Miles, R. S. & Patterson, C.) 63-103 (Academic, 1973b). San Giorgio, Switzerland. Palaeontology 25, 399-412 (1982). Miller, R. F., Cloutier, R. & Turner, S. The oldest articulated chon- Schaeffer, B. The xenacanth shark neurocranium, with comments on drichthyan from the Early Devonian period. Nature 425, 501- elasmobranch monophyly. Bull. Am. Mus. Nat. Hist. 169, 1-66 504 (2003). (1981). Moy-Thomas, J. A. The structure and affi nities of Chondrenchelys Schultze, H.NP. & Zidek, J. Ein primitiver acanthodier (Pisces) aus problematica Tr. Proceedings of the Zoological Society, Lon- dem Unterdevon Lettlands. Paläontologische Zeitschrift 56, 95- don1935, 391-403 (1935). 105 (1982). Mutter, R. J., de Blanger, K., & Neuman, A. G. Elasmobranchs from Seidel, R., Lyons, K., Blumer, M., Zalansky, P., Fratzl, P., Weaver, J. the Lower Triassic Sulphur Mountain Formation near Wapiti C. & Dean, M. N. Ultrastructural and developmental features of Lake (BC, Canada). Zoological Journal of the Linnean Society the tessellated endoskeleton of elasmobranchs (sharks and rays). 149, 309-37 (2007). J. Anat. DOI:10.1111/joa.12508 (2016). Mutter, R. J., Neuman, A. G. & de Blanger, K. Homalodontus nom. Solér-Gijon, R. & Hampe, O. Evidence of Triodus Jordan 1849 nov. a replacement for Wapitiodus Mutter, de Blanger and Neu- (Elasmobranchii: Xenacanthidae) in the Lower Permian of the man 2007 (Homalodontidae nom. nov., ?Hybodontoidea), pre- Autun basin (Muse, France). N. Jb. Geol. Paläont. Mh. 1998, occupied by Wapitiodus Orchard, 2005. Zoological Journal of 335-348 (1998). the Linnean Society 154, 419-420 (2008). Stahl, B. J. in Handbook of Paleoichthyology Vol. 4 (ed. Schultze, Nelson, G. J. in Current problems of lower vertebrate phylogeny. H.-P.) (Friedrich Pfeil, München. 1999). (ed. T. Ørvig) 129-143 (Almqvist & Wiksell, Stockholm, 1968). Turner, S. Middle Palaeozoic elasmobranch remains from Australia. Newberry, J. S. The Paleozoic fi shes of North America, Monograph Journal of Vertebrate Paleontology 2, 117-131 (1982). of the U.S. Geological Survey 16, 1–340 (1889). Turner, S., Burrow, C. J. & Warren, A. Gyracanthides hawkinsi sp. Newman, M. J., Davidson, R. G., den Blaauwen, J. L. & Burrow, nov. (Acanthodii, Gyracanthidae) from the Lower Carbonifer- C. J. The Early Devonian acanthodian Uraniacanthus curtus ous of Queensland, Australia, with a review of gyracanthid taxa. (Powrie, 1870) n. comb., from the Midland Valley of Scotland. Palaeontology 48, 963-1006 (2005). Geodiversitas 34, 739-759 (2012). Valiukevicius, J. in Fossil Fishes as Living Animals (ed. Mark-Kurik, Oelofsen, B. W. A fossil shark neurocranium from the Permo-Car- E.) 193-213 (Academy of Sciences of Estonia, Tallinn, (1992). boniferous (lowermost Ecca Formation) of South Africa. In In- Warren, A., Currie, B. P., Burrow, C. & Turner, S. A redescription do-Pacifi c fi sh biology. Proceedings of the Second International and reinterpretation of Gyracanthides murrayi Woodward 1906 Conference on Indo-Pacifi c Fishes. Ichthyological Society of (Acanthodii, Gyracanthidae) from the Lower Carboniferous of Japan, Tokyo, pp. 107-124 (1986). the Mansfi eld Basin, Victoria, Australia. Journal of Vertebrate Patterson, C. The phylogeny of the chimaeroids. Philosophical Paleontology 20, 225-242 (2000). Transactions of the Royal Society of London, Series B 249, 101- Watson, D. M. S. The acanthodian fi shes. Philosophical Transac- 219 (1965). tions of the Royal Society of London B 228, 49-146 (1937). Patterson, C. Morphology and interrelationships of primitive acti- Williams, M. E. A new specimen of Tamiobatis vetustus (Chondrich- nopterygian fi shes. American Zoologist 22, 241-259 (1982). thyes, Ctenacanthoidea) from the Late Devonian Cleveland Patterson, C. Interpretation of the toothplates of chimaeroid fi shes. Shale of Ohio. Journal of Vertebrate Paleontology 18(2), 251- Zool. J. Linn. Soc. 106, 33-61 (1992). 260 (1998). Pearson, D. M. & Westoll, T. S. The Devonian actinopterygian Chei- Williams, M. E. Tooth retention in cladodont sharks: with a compar- rolepis Agassiz. Trans. R. Soc. Edinb. 70, 337-399 (1979). ison between primitive grasping and swallowing, and modern Pradel, A. Skull and brain anatomy of Late Carboniferous Siby- cutting and gouging feeding mechanisms. Journal of Vertebrate rhynchidae (Chondrichthyes, Iniopterygia) from Kansas and Paleontology 21, 214-226 (2001). Oklahoma (USA). Geodiversitas 32, 595-661 (2010). Woodward, A. S. & White, E. I. The dermal tubercles of the Upper Pradel A., Didier, D., Casane, D., Tafforeau, P. & Maisey J. G. Ho- Devonian shark, Cladoselache. Annals and Magazine of Natural locephalan embryo provides new information on the evolution History 11, 367-368 (1938). of the glossopharyngeal nerve, metotic fi ssure and parachordal Yu, X. A new porolepiform-like fi sh, Psarolepis romeri, gen. et sp. plate in gnathostomes. PLoS ONE 8: e66988 DOI:10.1371/jour- nov. (Sarcopterygii, Osteichthyes) from the Lower Devonian of nal.pone.0066988 (2013). Yunnan, China. J. Vertebr. Paleontol. 18, 261-264 (1998). Pradel A., Langer M., Maisey J. G., Geffard-Kuriyama D., Cloetens Zangerl, R. in Handbook of Paleoichthyology Vol. 3A (ed. Schultze, P., Janvier P., & Tafforeau P. Skull and brain of a 300 million- H.-P.) (Gustav Fischer Verlag, Stuttgart,1981). year-old chimaeroid fi sh revealed by synchrotron holotomog- Zangerl, R. & Case, G. R. Iniopterygia, a new order of chondrich- raphy. Proceedings of the National Academy of Sciences 106, thyan fi shes from the Pennsylvanian of North America. Fieldi- 5224-5228 (2009). ana: Geology 6, 1-67 (1973). Pradel, A., Maisey, J. G., Tafforeau, P., Mapes, R. H. & Mallatt, J. Zangerl, R. & Case, G. R. Cobelodus aculeatus (Cope), ananacan- A Palaeozoic shark with osteichthyan-like branchial arches. Na- thous shark from Pennsylvanian black shales of North America. ture 509, 608-611 (2014). Palaeontographica, A, 154, 107-157 (1976). Pradel, A., Tafforeau, P. & Janvier P. Study of the pectoral girdle and Zhu, M., Ahlberg, P., Pan, Z., Zhu, Y., Qiao, T., Zhao, W., Jia, L. & fi ns of the Late Carboniferous sibyrhynchid iniopterygians (Ver- Lu, J. A Silurian maxillate placoderm illuminates jaw evolution. tebrata, Chondrichthyes, Iniopterygia) from Kansas and Okla- Science 354, 334-336 (2016). homa (USA) by means of microtomography, with comments on Zhu, M. & Schultze, H. P. The oldest sarcopterygian fi sh. Lethaia iniopterygian relationships. Comptes Rendus Palevol 9, 377-387 30, 293-304 (1997). (2010). Zhu, M. & Schultze, H. P. in Major Events in Early Vertebrate Evo- Pradel A., Tafforeau P., Maisey J. G. & Janvier P. A new Paleo- lution (Palaeontology, phylogeny, genetics, and development). zoic Symmoriiformes (Chondrichthyes) from the Late Car- (ed. Ahlberg, P. E.) 289-314 (Taylor and Francis, 2001). boniferous of Kansas (USA) and Cladistic Analysis of Early Zhu, M & Yu, X. A primitive fi sh close to the common ancestor of Chondrichthyans. PLoS ONE 6: e24938 DOI:10.1371/journal. tetrapods and lungfi sh. Nature 418, 767-770 (2002). pone.0024938 (2011). Zhu, M., Yu, X, & Ahlberg, P. E. A primitive sarcopterygian fi sh with Qu, Q., M., Zhu, M. & Wang, W. Scales and dermal skeletal histolo- an eyestalk. Nature 410, 81-84 (2001). gy of an early bony fi sh Psarolepis romeri and their bearing on Zhu, M., Yu, X., Ahlberg, P. E., Choo, B., Lu, J., Qiao, Q., Zhao, the evolution of rhombic scales and hard tissues. PLoS One 8, L. J., Blom, H., & Zhu, Y. A Silurian placoderm with osteich- e61485 (2013). thyan-like marginal jaw bones. Nature 52, 188-193 (2013). Qiao, T., King B., Long J. A., Ahlberg P. E., & Zhu M. Early gnatho- Zhu, M., Yu, X. & Janvier, P. A primitive fossil fi sh sheds light on the stome phylogeny revisited: multiple method consensus. PLoS origin of bony fi shes. Nature 397, 607-610 (1999).

164 Chapter IV: Functional Morphology of Symmoriid Jaws

Zhu, M., Zhao, W., Jia, L., Lu, J., Qiao, T. & Qu, Q. The oldest artic- ta Moutains, New Mexico. In Geology and paleontology of the ulated osteichthyan reveals a mosaic of gnathostome characters. Kinney Brick Quarry, Late Pennsylvanian, central New Mexi- Nature 458, 469-474 (2009). co. J. Zidek ed. Bulletin 138, New Mexico Bureau of Mines & Zidek, J. Late Pennsylvanian Chondrichthyes, Acanthodii, and Mineral Resources (Socorro: New Mexico Bureau of Mines & deep-bodied Actinopterygii from the Kinney Quarry, Manzani- Mineral Resources), pp. 199-214. (1992).

165

CONCLUSIONS

Conclusions

Alpha diversity and palaeoecology of stomes (in the neighbouring Tafi lalt region, teeth the Maïder region of Morocco of 17 chondrichthyan taxa including pelagic and benthic taxa occur). The chondrichthyans of the Fammenian Fossillagerstätten of the Maïder re- Maïder are most abundant in the Thylacocephalan gion contain numerous gnathostome remains of at Layer with thylacocephalans as an important food least one sarcopterygian species, one actinoptery- source. gian species, four species of placoderms and fi ve species of chondrichthyans. Most of these gnatho- stome remains were excavated from the Thylaco- cephalan Layer, an argillaceous interval of about Taphonomy of the Moroccan Fossillag- two meter thickness with numerous small nodules erstätte containing mostly carapaces of thylacocephalan arthropods. This layer represents a Konservat-La- The mineral composition of fossils of some De- gerstätte (conservation deposit; see Chapter II). In vonian Fossillagerstätten of the eastern Anti-At- this chapter I, I analysed the faunal composition, las was analysed. Cephalopods, thylacoephalan trophic nucleus, alpha diversity and ecospace oc- and vertebrate skeletal remains contain calcite, cupation of 21 invertebrate associations of early goethite and sometimes haematite. Bones of plac- Famennian (17 from Madene el Mrakbib) to mid- oderms and the cartilage of chondrichthyans are dle Tournaisian age (4 from Aguelmous). The spe- preserved in hydroxyapatite and, muscle fi bres cies richness fl uctuated mostly between three and of the chondrichthyans contain goethite and hae- 14 taxa (rarely it comprised up to 24 taxa) and the matite among other iron minerals; these fossils ecospace occupation fl uctuated between one and were likely primarily preserved in pyrite that later 12 three-dimensional modes of life. Within the weathered into iron oxides and hydroxides. ecospace, the ratio between pelagic and benthic The occurrence of iron oxides and hydrox- modes of life varied signifi cantly. In the trophic ides (and possibly primary pyrite), the clayey fa- nucleus, there were mostly pelagic but also some cies and the few benthic invertebrate taxa (ben- benthic taxa. thic chondrichthyans are completely absent) in The mostly relatively low taxonomic di- the gnathostome bearing Thylacopehalan Layer versity and the dominance of pelagic or benthic suggests that the fossils were embedded under ox- taxa tolerating dysoxic conditions show that the ygen-depleted conditions. These low oxygen-con- environment of the Famennian and Tournaisian ditions might have been caused by the limited was characterised by often oxygen-depleted bot- water exchange due to the restricted palaeogeog- tom-waters in the Maïder Basin (at least in the raphy of the Maïder Basin, which was bordered studied localities). Some of the fl uctuations in by land and two pelagic submarine ridges. ecospace occupation and species richness cor- Because of the often exceptional fossil pres- relate with Famennian and Tournaisian bio-events ervation (including soft-tissue in, e.g., chondrich- of varying importance and changes in regional or thyans), the faunal composition (few benthos), global sea level including the consequences for the abundance of primary pyrite and phosphates oxygen supply to bottom waters. Since the fl ucta- and the palaeogeography of the Maïder region, tions in the associations in combination with the the Famennian Thylacocephala Layer represents changes in the sediment (varying content of clay the fi rst Devonian Konservat-Lagerstätte of North and carbonate), fi t reasonably well with the glob- Africa. al sea level curves, the regional sea level curve of the Maïder was probably more fl uctuant than reported by previous studies. The Famennian eco- space was also more depleted after the Kellwass- Famennian chondrichthyans of the er Event (late Frasnian) and during the Annulata Famennian Konservat-Lagerstätte of Event (middle Famennian). In general, the envi- ronment in which the gnathostomes of the Maïder the Maïder lived was not suitable for a highly diverse ecosys- Two of the at least fi ve chondrichthyan species tem (common hypoxic to dysoxic conditions, low discovered in the Famennian Konservat-Lager- taxonomic richness, scarcity of benthos, several stätte were described in the framework of this the- bio-events), which is also shown by the relatively sis. The Famennian Phoebodus saidselachus sp. low diversity of jawed fi sh (around 8, possibly 10 nov. is the fi rst Phoebodus specimen preserving species) and the complete lack of benthic gnatho- body remains (Chapter III). Before this discovery,

169 Conclusions this well-known geographically widely distribut- experiments with 3D-prints, the jaw function of ed Devonian taxon was exclusively based on teeth a symmoriid could be reconstructed for the fi rst and tentatively assigned isolated fi n spines. The time. Due to the confi guration of the articulation, anatomy of Phoebodus saidselachus sp. nov. and the lower jaw rotated laterally outward when the of the stratigraphically younger phoebodont Thr- mouth opened. As a result of this lateral rotation, inacodus gracia (Carboniferous of Bear Gulch) more teeth became exposed and thus functional show that phoebodontids are a chondrichthyan than originally thought. In contrast to the apheto- clade characterised by slender and elongate eel- hyoidean hypothesis (no suspensory function of shaped bodies. In the more derived genus Thrina- the hyoid) where a gap exists between the jaws codus, the degree of elongation is more extreme and branchial arches, the hyoid and ceratohyal are than in Phoebodus, which corroborates earlier tightly articulated with the jaws in Ferromirum. assumptions on the phylogenetic relationships Therefore, the hyoid functioned as a suspension between the two genera based on teeth. Addition- between the jaws and the neurocranium. The jaw ally, the phylogenetic analyses confi rmed that the function mentioned above and the suspensory Phoebodontidae are stem elasmobranchs, which function of the hyoid might have been common in encompasses both genera. Since phoebodontid symmoriiforms as their jaw-to-skull articulation teeth are known from the Givetian (Middle Devo- is a conservative feature in these chondrichthyans nian), the phoebodontids and in particular Phoe- (as has been shown by the perfect fi t of the up- bodus represent the earliest stem elasmobranchs per jaws of Ferromirum to the neurocranium of and also the oldest anguilliform chondrichthyans. Dwykaselachus).

The second chondrichthyan described from To conclude, the chondrichthyans preserved the Fossillagerstätte of the Maïder is the sym- in nodules of the Famennian Konservat-Lager- moriiform Ferromirum oukherbouchi gen. et sp. stätte of the Maïder Basin provided new insights nov (Chapter IV). It is a single specimen with into the morphological disparity of Devonian preserved body outline and visceral skeleton, chondrichthyans (in the case of Phoebodus said- shoulder girdles and fi n spine in three-dimension- selachus sp. nov) and they also allow us to recon- al preservation. The virtual 3D-reconstruction of struct the function of certain skeletal elements the specimen revealed that this specimen has the (suc h as in Ferromirum oukherbouchi gen. et sp. best preserved jaws of symmoriiform chondrich- nov.). thyans currently known. Based on mechanical

170 APPENDIX A

Collaborations with other projects

(abstracts)

Appendix A

[Palaeontology, 2016, pp. 1–19]

THE OLDEST GONDWANAN CEPHALOPOD MANDIBLES (HANGENBERG BLACK SHALE, LATE DEVONIAN) AND THE MID-PALAEOZOIC RISE OF JAWS by CHRISTIAN KLUG1,LINDAFREY1,DIETERKORN2, ROMAIN JATTIOT1 and MARTIN RUCKLIN€ 3 1Pal€aontologisches Institut und Museum, Universit€at Zurich,€ Karl Schmid-Strasse 4, CH-8006, Zurich,€ Switzerland; [email protected], [email protected], [email protected] 2Museum fur€ Naturkunde Berlin, Leibniz-Institut fur€ Evolutions- und Biodiversit€atsforschung, Invalidenstraße 43, D-10115, Berlin, Germany; [email protected] 3Naturalis Biodiversity Center, Postbus 9517, 2300 RA, Leiden, The Netherlands; [email protected]

Typescript received 4 April 2016; accepted in revised form 3 June 2016

Abstract: It is widely accepted that the effects of global Order Clymeniida and to the Suborder Tornoceratina. These sea-level changes at the transition from the Devonian to the findings imply that chitinous normal-type jaws were likely to Carboniferous are recorded in deposits on the shelf of north- have already been present at the origin of the whole clade ern Gondwana. These latest Devonian strata had been Ammonoidea, i.e. in the early Emsian (or earlier). Vertebrate thought to be poor in fossils due to the Hangenberg mass jaws probably evolved prior to the origin of ammonoids, in extinction. In the Ma’der (eastern Anti-Atlas), however, the the Early Devonian. The temporal succession of evolutionary Hangenberg Black Shale claystones (latest Famennian) are events suggests that it could have been the indirect positive rich in exceptionally preserved fossils displaying the remains selection pressure towards strong (and thus preservable) jaws of non-mineralized structures. The diversity in animal since defensive structures of potential prey animals would species of these strata is, however, low. Remarkably, the otherwise have made them inaccessible to jawless predators organic-rich claystones have yielded abundant remains of in the course of the mid-Palaeozoic marine revolution. In Ammonoidea preserved with their jaws, both in situ and iso- this respect, our findings reflect the macroecological changes lated. This is important because previously, the jaws of only that occurred in the Devonian. one of the main Devonian ammonoid clades had been found (Frasnian Gephuroceratina). Here, we describe four types of Key words: Cephalopoda, Ammonoidea, mass extinctions, jaws of which two could be assigned confidently to the macroecology, Devonian, Morocco.

173 Appendix A

Palaeozoic evolution of animal mouthparts

CHRISTIAN KLUG, LINDA FREY, ALEXANDER POHLE, KENNETH DE BAETS & DIETER KORN

During the Palaeozoic, a diversification in modes of life occurred that included a wide range of predators. Major macroecological events include the Cambrian Explosion (including the Agronomic Substrate Revolution and the here introduced ‘Ediacaran-Cambrian Mouthpart Armament’), the Great Ordovician Biodiversification Event, the Palaeozoic Plankton Revolution, the Siluro-Devonian Jaw Armament (newly introduced herein) and the Devonian Nekton Revolution. Here, we discuss the evolutionary advancement in oral equipment, i.e. the Palaeozoic evolution of mouthparts and jaws in a macroecological context. It appears that particularly the latest Neoproterozoic to Cambrian and the Silurian to Devonian were phases when important innovations in the evolution of oral structures occurred. • Key words: Gnathostomata, Cephalopoda, evolution, convergence, diversity, nekton, jaws.

CHRISTIAN KLUG,LINDA FREY,ALEXANDER POHLE,KENNETH DE BAETS &DIETER KORN 2017. Palaeozoic evolu- tion of animal mouthparts. Bulletin of Geosciences 92(4), 511–524 (4 figures, 1 table). Czech Geological Survey, Prague. ISSN 1214-1119. Manuscript received November 10, 2016; accepted in revised form September 22, 2017; pub- lished online December 6, 2017; issued December 31, 2017.

Christian Klug, Linda Frey & Alexander Pohle, Paläontologisches Institut und Museum, Universität Zürich, Karl Schmid-Strasse 4, 8006 Zürich, Switzerland; [email protected], [email protected], [email protected] • Kenneth De Baets, GeoZentrum Nordbayern, Fachgruppe PaläoUmwelt, Universität Erlangen, Loewenichstr. 28, 91054 Erlangen, Germany; [email protected] • Dieter Korn, Museum für Naturkunde, Leibniz-Institut für Evolu- tions- und Biodiversitätsforschung, Invalidenstraße 43, 10115 Berlin, Germany; [email protected]

174 APPENDIX B

Additional article published during doctoral studies

Intraspecifi c variation in fossil vertebrate populations: Fos- sil killifi shes (Actinopterygii: Cyprinodontiformes) from the Oligocene of the Central Europe

Linda Frey, Erin E. Maxwell and Marcelo R. Sánchez-Villagra

Published in: Palaeontologia Electronica, 19.2.14A: 1-27 palaeo-electronica.org/content/2016/1464-fossil-killifi shes-from-europe

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182 Appendix B

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183 Appendix B

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184 Appendix B

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185 Appendix B

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186 Appendix B

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187 Appendix B

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190 Appendix B

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191 Appendix B

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194 Appendix B

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196 Appendix B

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197 Appendix B

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198 Appendix B

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199 Appendix B

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200 Appendix B

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201

ACKNOWLEDGMENTS

203

Acknowledgments

I would like to show my greatest appreciation to my supervisor Prof. Dr. Christian Klug (University of Zurich) for his support, patience and encouragements and for sharing his knowledge about the palaeon- tology of Morocco during the work on my dissertation. Without his guidance, this dissertation would not have been possible.

I greatly thank Prof. Dr. Michael Coates (University of Chicago) and Dr. Martin Rücklin (Naturalis Bio- diversity Center, Leiden) for accepting to be committee members and for the illuminating discussions, inputs and feedbacks. Many thanks go to Prof. Dr. Marcelo Sánchez and to Prof. Dr. Hugo Bucher for providing me work space and constructive feedbacks during committee meetings.

During this dissertation, I received generous support from many colleagues and therefore, I would like to thank:

 The colleagues of the Ministère de l’Energie, des Mines, de l’Eau et de l’Environnement (Direction du Développement Minier, Division du Patrimoine, Rabat, Morocco) for providing working and sample export permits,  Said Oukherbouch (Tafraoute, Morocco) for his enormously important help and support during fi eld work,  Michał Ginter (University of Warsaw) and Vachik Hairapetian (Islamic Azad University of Isfahan) for sharing their knowledge o n early chondrichtyan teeth,  René Kindlimann (Aathal) and Jorge Carrillo-Briceño (University of Zurich) for sharing their exper- tise on fossil and recent cartilagenous fi sh,  Dieter Korn (Museum für Naturkunde, Berlin) for sharing his knowledge on the diversity of Devo- nian ammonoids, for providing data for palaeoecological analyses and for giving constructive feed- backs,  Michael R. W. Amler (University of Cologne) for helping in the determination of Devonian bivalves,  Per Ahlberg (University of Uppsala) for advice about 3D-reconstruction software,  Christina Brühwiler (Winterthur), Ben Pabst (Zurich), Claudine Misérez (Neuchâtel) and the Tahiri Museum (Erfoud) for their excellent fossil preparation,  Rosi Roth (University of Zurich) for preparing fossil material and for helping in the photo lab.  Markus Hebeisen (University of Zurich) for providing working space in his preparation lab and for introducing me into preparation with airscribes,  Alexander Pohle (University of Zurich) for conducting XRD-analyses,  Lydia Zehnder and Sebastian Cionoiu (both ETH Zurich) for their generous help with the XRD- and Raman-analyses,  Iwan Jerjen (ETH Zurich), Tom Davis (University of Bristol), Alexandra Wegemann (University of Zurich) and Anita Schweitzer (Zurich) for acquiring computer tomography scans of the specimens,  Thodoris Argyriou (Paris) for sharing his knowledge about fi shes, for CT-scanning and assisting during virtual 3D-reconstruction,  Amane Tajika (NHM, New York) and Tobias Reich (University of Zurich) for kindly providing help during segmentation of CT-scans,  Gabriel Aguirre-Fernández (University of Zurich) for introducing me into software used for phyloge- netic analysis,  Morgane Brosse (Zurich) for generously helping me to solve any problem concerning the layout of this disseration, and  Heike Götzmann as well as Heinrich Walter (both University of Zurich) for their administrative and technical support.

I would also like to thank all the colleagues of the Palaeontological Institute and Museum of the Univer- sity of Zurich not only for their scientifi c advices and support but also for their friendship. Moreover, I would like to show my appreciation to the people I met in Morocco for their hospitality, which made our fi eld trips very pleasant.

A big thank you goes to my family, especially to my parents Edith and Peter and to my grandmother Ma- rie Anne who always supported me during my studies.

205 Acknowledgments

Funding

 I greatly appreciate the fi nancial support of this dissertation by the Swiss National Science Founda- tion (No. 200021_156105)  The Swiss Geological Society supported the participation at 14th International Symposium on Early and Lower Vertebrates in Poland in 2017.

206 CURRICULUM VITAE

207 Curriculum Vitae

Name: Frey First name: Linda Date of birth: 10.07.1987 Nationality: Swiss Heimatort: St. Ursen (FR)

Education 2003 –2007 Kantonsschule Wettingen 2007 –2011 University of Zurich, Bachelor of Science Main subject: Biology 2012 –2013 University of Zurich, Master of Science Master thesis in Palaeontology: Alpha diversity and palaeoecology of invertebrate associations of the Early Devonian in the Moroccan Anti-Atlas (Grade: 5.7) Supervisor: Prof. Dr. Christian Klug Since 2014 PhD student in Palaeontology Palaeontological Institute and Museum, University of Zurich Supervisor: Prof. Dr. Christian Klug

Publications during doctoral studies Articles Frey, L., Rücklin, M., Korn, D. and Klug, C. (2018): Late Devonian and Early Carboniferous alpha diversity, ecospace occupation, vertebrate assemblages and bio-events of southeastern Morocco. Palaeogeography, Palaeoclimatology, Palaeoecology, 496 (1): 1-17; Klug, C., Frey, L., Pohle, A., De Baets, K. and Korn, D. (2017): Palaeozoic evolution of animal mouthparts. Bulletin of Geosciences, 92(4): 13 pp. Klug, C., Frey, L. Korn, D., Jattiot, R. and Rücklin, M. (2016). The oldest Gondwanan cephalopod mandibles (Hangenberg black shale, Late Devonian) and the mid-Palaeozoic rise of jaws. Palaeontology: 1-19 pp., doi: 10.1111/pala.12248 Frey, L., Maxwell, E., and Sánchez-Villagra, M. R. (2016): Intraspecifi c variation in fossil vertebrate populations: Fossil killifi shes (Actinopterygii: Cyprinodontiformes) from the Oligocene of Central Europe. Palaeontologia Electronica 19.2.14A: 1-27; palaeo-electronica. org/content/2016/1464-fossil-killifi shes-from-europe

Abstracts Klug, C., Frey, L., Pohle, A., De Beats, K. & Korn, D. (2018b): Palaeozoic evolution of cephalopod mouthparts. 10th International Symposium on Cephalopods - Present and Past: p. 2, Fez. Frey, L., Coates, M., Ginter, M., Klug, C. (2017): Skeletal Remains of Phoebodus politus Newberry 1889 (Chondrichthyes: Elasmobranchii) from a Famennian Konservatlagerstätte in the Eastern Anti-Atlas (Morocco) and its Ecology. 15th Annual Meeting of the European Association of Vertebrate Palaeontologists; p. 37, Munich.

208 Curriculum Vitae

Frey, L., Coates, M., Ginter, M., Klug, C. (2017): Skeletal remains of Phoebodus politus Newberry 1889 (Chondrichthyes: Elasmobranchii) from a Famennian Konservatlagerstätte in the eastern Anti-Atlas (Morocco) and its ecology. 14th International Symposium on Early and Lower Vertebrates : p. 36, Checiny, Poland. Klug, C., Frey, L., Pohle, A., Rücklin, M., (2017): Origin of the Konservatlagerstätten of the southern Maider (Morocco) and gnathostome preservation. 14th International Symposium on Early and Lower Vertebrates: p. 52, Checiny, Poland. Frey, L., Coates, M., Ginter, M., Klug, C. (2016): The fi rst skeletal remains of Phoebodus politus Newberry 1889 (Chondrichthyes: Elasmobranchii) and its ecology. 14th Swiss Geoscience Meeting, 4. Palaeontology: p. 147, Geneva. Klug, C., Frey, L., Korn, D., Jattiot, R., Rücklin, M. (2016): No fossil record? Yes fossil record! Konservat-Lagerstätten of the End-Devonian Hangenberg Black Shale in the eastern Anti- Atlas (Morocco). 14th Swiss Geoscience Meeting, 4. Palaeontology: p. 149, Geneva. Klug, C., Frey, L., De Baets, K., and Korn, D. (2016): Paleozoic Marine macroecology. 1st Meeting of Early Stage Researchers in Palaeontology: p. 1, Alpuente (Valencia). Frey, L., Rücklin, M., Kindlimann, R., and Klug, C. (2015): Alpha diversity and palaeoecology of a Late Devonian Fossillagerstätte from Morocco and its exceptionally preserved fi sh fauna. 13th Swiss Geoscience Meeting: p. 142, Basel, Klug, C., Frey, L. and Rücklin, M. (2015): Preservation and taphonomy of Famennian Fossillagerstätten in the eastern Anti-Atlas of Morocco. 13th Swiss Geoscience Meeting: p. 144, Basel. Frey, L., Rücklin, M., Kindlimann, R., and Klug, C. (2015): Alpha diversity and palaeoecology of a Late Devonian Fossillagerstätte from Morocco and its exceptionally preserved fi sh fauna. 13th International symposium on Early and Lower Vertebrates: p. 15, Melbourne Klug, C., Frey, L. and Rücklin, M. (2015): Preservation and taphonomy of Famennian Fossillagerstätten in the eastern Anti-Atlas of Morocco. 13th international Symposium on Early and Lower Vertebrates: p. 21, Melbourne.

209