Lampreys and gnathostomes, in possessing electroreceptors that are thought to be homologous, form an extant phylogenetic bracket (Witmer 1995 ). Fossil stem gnathostomes (closer to extant gnathostomes than to extant agnathans) fall within this bracket. The jawless arandaspids, anaspids, thelodonts, heterostracans, galeaspids, pituriaspids and osteostracans are considered to be stem gnathostomes (Janvier 1996 ; Donoghue et al . 2000 ; Sansom et al . 2010 ), as are the jawed placoderms (Young 1986 ; Goujet 2001 ; Brazeau 2009 ). All of these groups can therefore be assumed to have had electroreception, or to have secondarily lost it. The purpose of this review is to re‐examine the putative electroreceptors in fossil stem and early crown gnathostomes. CT scan data is presented on ‘cutaneous sense organs’, putative electectroreceptor pits on the cheeks of arthrodire placoderms, lungfish pore‐group pits and newly identified pits on the skull of the enigmatic early osteichthyan ‘Ligulalepis’ .

Electroreception has apparently been lost in hagfish, neopterygian fish (including teleosts), anurans (frogs) and amniotes (Fig. 1 ). However, it has subsequently been re‐gained at least twice in teleosts (in subgroups of Osteoglossomorpha and Ostariophysi) (Alves‐Gomes 2001 ) and twice in mammals (dolphins and monotremes) (Proske et al . 1998 ; Czech‐Damal et al . 2012 ). The electroreceptors of teleosts are not considered homologous with those of non‐teleosts (Bullock et al . 1983 ; Baker et al . 2013 ). This review will focus mainly on the vertebrate ‘ancestral‐type’ of electroreceptor (i.e. those of non‐teleosts).

Vertebrate phylogeny showing presence and absence of electroreception, and the position of key fossil taxa discussed during this review. Electroreception is inferred to be a primitive vertebrate feature as it is present across the phylogeny (blue branches). It has been lost four times (red branches). The asterisks indicate clades within which electroreception has evolved secondarily following loss (i.e. within teleosts and mammals). Key fossil groups that will be discussed in this review are shown on dotted black branches. All of these could be inferred to have had electroreception, or to have lost it, based on their relationships to living taxa with electroreception.

Passive electroreception was subsequently discovered in a broad range of vertebrates including basal actinopterygians (ray‐finned fish), sarcopterygians (lobe‐finned fish), amphibians, chimaeras (relatives of sharks and rays) and the jawless lampreys (Jørgensen et al . 1972 ; Roth 1973 ; Fields & Lange 1980 ; Teeter et al . 1980 ; Bodznick & Northcutt 1981 ; Münz et al . 1982 ; Watt et al . 1999 ). The presence of electroreception is distributed widely in phylogeny (Fig. 1 ) and is often regarded as a plesiomorphic feature of vertebrates (Bullock et al . 1983 ). The homology of electrosensory systems (excluding those of teleost fishes) is supported by shared features: activation by cathodal (outside negative) stimuli, innervation by the anterior lateral line nerve (ALLN: superficial ophthalmic, buccal, otic and mandibularis externus lateral line nerves) and projections to the dorsal octavolateralis nucleus (DON) in the medulla region of the hindbrain (Bullock et al . 1983 ). These electroreceptors also share a common embryonic origin, forming on the periphery of lateral line placodes, patches of thickened cranial ectoderm that also give rise to the mechanosensory lateral lines (Northcutt et al . 1995 ; Modrell et al . 2011 ; Gillis et al . 2012 ; Baker et al . 2013 ). For these reasons, there is a general consensus that the electroreceptors of non‐teleosts are homologous, although there are significant morphological differences between groups (see below).

Electroreception, the ability to detect electric fields, is the most recently discovered of the major sensory modalities. Lissmann ( 1951 ) and Lissmann & Machin ( 1958 ) discovered that African knifefish ( Gymnarchus ) could detect perturbations in electrical fields produced by their electric organs, allowing them to navigate their environment. Detecting electrical fields produced by an electric organ is known as active electroreception. Later, sensitivity to external electrical fields without use of an electric organ was demonstrated in sharks and rays (Murray 1960 , 1962 ; Bennett 1971 ). Experiments on the catshark Scyliorhinus canicula showed that passive electroreception functions in the detection of naturally‐occurring electric fields surrounding prey items (Kalmijn 1971 ).

SAM P53772 and SAM P50606 were scanned together in a 25 mm jar on a double helix HeliScan CT Scanner. A 2.2 mm aluminium filter was used, with specimen distance 18.5 mm from the source, and detector position 300 mm from the source. Accelerating voltage of the electron beam generating the Bremsstrahlung radiation was 100 kV with a current of 80 μA. Reconstruction was based on 3600 radiographic projections formed on a 1536 × 2048 Varian flat panel camera (Varex Imaging).

ANU V79 was scanned on a double helix HeliScan CT Scanner. A 3 mm aluminium filter was used, with specimen distance 128 mm from the source, and detector position 672 mm from the source. Accelerating voltage of the electron beam generating the Bremsstrahlung radiation was 110 kV with a current of 120 μA. Reconstruction was based on 3600 radiographic projections formed on a 2840 × 2872 Pixium flat panel camera (Thales).

All CT scans (with the exception of ANU V3628) were done on instruments developed and built at the ANU CT Lab ( https://ctlab.anu.edu.au/ ), Department of Applied Mathematics, Research School of Physics and Engineering, Australian National University. ANU V244 was scanned in 2011; see Hu et al . ( 2017 ) for information. ANU 49340 was scanned in 2004, and ANU V1710 in 2005. For more information about these specimens, see Campbell et al . ( 2010 ). For further technical information about the CT Scanner, see Sakellariou et al . ( 2004 ).

Some specimens (Table 1 ) were scanned at the medical imaging beamline of the Australian Synchrotron, Victoria, Australia ( http://www.synchrotron.org.au/index.php/home ). Scans used a monochromatic beam with a photon energy of 30 keV, sample to detector distance of 325 mm and an nRuby detector. A total of 1800 projections over 180° were taken. Raw data was processed using the X‐TRACT software ( https://www.ts-imaging.net/Services/AppInfo/X-TRACT.aspx ). The images from the overlapping 3 mm slices were concatenated for segmentation. 3‐D segmentation of the bone and internal canals was performed using MIMICS 17.0 and 18.0 ( http://www.materialise.com ). Additional renderings were performed in Blender ( http://www.blender.org ) and Drishti (Limaye 2012 ).

In lampreys and lungfish, which possess trunk electroreceptors, these are innervated by a recurrent ramus of the ALLN (Bodznick & Preston 1983 ; Northcutt 1986a ). This nerve courses around the otic capsule and runs posteriorly to join the posterior lateral line nerve, which innervates trunk mechanoreceptors. Since this nerve exclusively innervates trunk electroreceptors, its presence in a fossil is likely to indicate the presence of electroreception.

The dorsal octavolateralis nucleus in the medulla is thought to be exclusively involved in electroreception (Bodznick & Northcutt 1980 , 1981 ; Bullock et al . 1983 ). However, presence of such a nucleus cannot be ascertained in fossil endocasts. In fact, the dorsal hindbrain has a particularly poor fit to the endocast in the lungfish Neoceratodus (Clement et al . 2015 ).

Non‐teleost electroreceptors are innervated by branches of the anterior lateral line nerve (ALLN) which project to the dorsal octavolateralis nucleus (DON) in the medulla (Bullock et al . 1983 ). In marine chondrichthyans, in which the ampullary bulbs are clustered into a number of discrete capsules, each capsule is innervated by a branch of the ALLN: the superficial ophthalmic, outer buccal, inner buccal, hyomandibular and mandibular branches (Raschi 1986 ).

Ampullary electroreceptors develop from the periphery of lateral line placodes (Northcutt et al . 1995 ; Modrell et al . 2011 ; Gillis et al . 2012 ). This is reflected in the distribution of pores in the adult: ampullary organs occur in fields alongside the latero‐sensory canals (e.g. Norris 1929 ; Fields et al . 1993 ).

Some electroreceptive species have evolved specialized morphologies associated with enhanced electroreceptive abilities. The elongate snouts of rhinochimaerid holocephalans have an increased density of electroreceptive pores on their ventral surface (Lisney 2010 ), as do the wide heads of hammerhead sharks (Kajiura 2001 ). The elongate bill of the paddlefish acts as an electroreceptive antenna aiding capture of plankton in murky water (Wilkens et al . 1997 ).

Ampullary pores are generally most densely distributed at the anterior end of the snout in sharks (e.g. Norris 1929 ; Kajiura 2001 ; Winther‐Janson et al . 2012 ). Whether pores are primarily found on the dorsal or ventral surface appears to depend on ecology (Raschi 1986 ). Pores primarily on the dorsal surface are indicative of a vertical ambush predatory lifestyle (Theiss et al . 2011 ; Moore & McCarthy 2014 ), whereas having pores primarily on the ventral surface is characteristic of species that feed on bottom‐dwelling prey (Raschi 1978 , 1986 ). Pelagic forms have more evenly distributed pores (Raschi 1986 ; Kajiura 2001 ). In holocephalans, the highest pore densities are also on the snout anterior to the eyes (Fields et al . 1993 ), and the same is true in general for osteichthyans (Northcutt 1986b ).

In chondrichthyans, each ampullary organ is most sensitive to voltage gradients that are parallel to canal direction (Murray 1962 ). In many species, ampullary canals radiate out in many directions, to enable sensitivity to electric fields in various orientations (Kramer 1996 ; Tricas 2001 ).

In the majority of non‐teleosts with electroreceptors, they are confined to the head. However, in lampreys, they are also distributed widely over the body and branchial region (Bodznick & Preston 1983 ). Trunk electroreceptors are also found in lungfish (Northcutt 1986a ), and ampullary organs are found on the pectoral fins of rays and skates (Raschi 1978 ).

The morphological difference between electroreceptors of living freshwater and saltwater species is consistent across multiple groups, and is associated with the biophysical properties of the water. Therefore, similar morphological differences should be applicable in fossils from freshwater and marine deposits.

Marine species have long ampullary canals to get sufficient voltage difference across the receptor membrane in the ampullae, whereas freshwater species have sufficient voltage difference across the skin and only require short canals. The background gradient represents an imposed electric field. In marine species (represented by a shark), skin resistance is low and voltage gradients extend through the body. Long canals with high‐resistance walls allow the voltage at the pore opening to extend to the ampulla, where there is sufficient voltage difference with the surrounding tissues to allow detection. In freshwater species (represented by a sturgeon), skin resistance is high, so voltage gradients do not extend through the body. The inside of the fish is instead relatively isopotential (apparent reverse gradient in the figure is an optical illusion). The voltage difference across the skin is sufficient that only short canals are required. Based on similar figures in Kramer () and Kalmijn ().

The difference in electroreceptor morphology between marine and freshwater species has been attributed to the biophysical properties of these two media (Szabo et al . 1972 ; Kalmijn 1974 ; Fig. 3 ). In saltwater, skin resistance is low and the body fluids are less conductive than the surrounding water, so voltage gradients extend throughout the body in marine vertebrates (Fig. 3 A). There is little voltage difference across the skin so marine vertebrates require long canals filled with a highly conductive jelly to produce sufficient voltage differences across the receptor membrane. The long canals effectively focus the voltage difference between the canal pore and the body fluids surrounding the ampulla onto the receptor membrane. Freshwater species have a higher skin resistance and relatively conductive body fluids, and therefore the voltage difference across the skin is sufficient for detection (Fig. 3 B), without requiring long canals. Szabo et al . ( 1972 ) suggested that short canals in freshwater species are an adaptation to minimize loss of ions by outward diffusion from the canal jelly.

The morphology of electroreceptors differs between marine and freshwater species, with long canals characterizing marine species and short canals characterizing freshwater species (Kramer 1996 ). Long canals characterize the majority of chondrichthyans, but short ampullary canals are known in the freshwater rays Potamotrygon and Himantura (Szabo et al . 1972 ; Raschi et al . 1997 ). This difference also occurs in the electroreceptors of catfish, although teleost electroreceptors are probably not homologous to vertebrate ancestral‐type electroreceptors (Bullock et al . 1983 ; Baker et al . 2013 ). Marine catfish Plotosus have long canals that penetrate deep into the dermis (Obara 1976 ). A freshwater member of the same genus has short canals (Whitehead et al . 2003 ). Euryhaline populations of the catfish Arius graeffi have intermediate canal length between marine and freshwater catfish (Whitehead et al . 1999 ) and freshwater populations of the same species have short canals (Whitehead et al . 2000 ).

Coelacanths, the sister group to other living sarcopterygians, have an electroreceptor system with a unique morphology, called the rostral organ. This is a subdermal chamber enclosed in the ethmoid region of the braincase, and connected to the outside by three pairs of jelly‐filled canals (Millot & Anthony 1965 ; Bemis & Hetherington 1982 ). This highly specialized system is sensitive only in a small region directly in front of the mouth, and is thought to function solely in the feeding strike (Berquist et al . 2015 ).

Within sarcopterygians (lobe‐finned fish), the electroreceptors of lungfish are superficial tube‐like structures embedded in the epidermis with ampullae at the base (Roth & Tscharntke 1976 ; Jørgensen 2011 ). The electroreceptors of both caecilian and urodele amphibians are likewise simple structures confined to the epidermis (Hetherington & Wake 1979 ; Istenič & Bulog 1984 ).

In actinopterygians (ray‐finned fish), electroreceptors are present in the two most basal lineages: polypteriforms (bichirs and reedfish), and acipenseriforms (paddlefish and sturgeons) (Jørgensen et al . 1972 ; Roth 1973 ). Ampullae of polypteriformes are superficial structures with short canals (Roth & Tscharntke 1976 ; Jørgensen 1982 ), particularly in Polypterus where they are confined to the epidermis of the skin. In sturgeons, electroreceptors are also superficial structures, although ampullae are sunken into the dermis (Jørgensen 1980 ; Teeter et al . 1980 ). Canals in sturgeons have a diameter of 30–40 μm at the surface, widening basally to 60–70 μm. Ampullae are clustered into groups of 4–85, and pairs of ampullae sometimes share common pores (Weisel 1978 ).

The other major lineage of cartilaginous fish, the chimaeras or Holocephali, also have electroreceptors (Fields & Lange 1980 ). In the spotted ratfish Hydrolagus colliei , ampullae are largely similar to those in elasmobranchs (Fields et al . 1993 ): alveolate and grouped in connective tissue capsules. The density of pores falls within the lower end of the range seen in elasmobranchs (Lisney 2010 ). In addition to ‘macro‐ampullae’, Holocephali have ‘micro‐ampullae’, with pores of 80–100 μm in diameter on the surface of the rostrum (Andres & Von Düring 1988 ).

In elasmobranchs (sharks and rays), electroreceptors are called ampullae of Lorenzini (Fig. 2 ). These are jelly‐filled canals, c . 1 mm in diameter, ending in small sacs known as ampullae (Lorenzini 1678 ). A series of experiments showed these to be electroreceptors (Murray 1960 , 1962 ; Dijkgraaf & Kalmijn 1963 ). Elasmobranch ampullae are grouped into clusters surrounded by connective tissue beneath the dermis, with long subdermal canals penetrating the dermis and opening into pores on the external surface (Tricas & Sisneros 2004 ; Wueringer & Tibbetts 2008 ). The ampullae have a range of morphologies, from simple tubes with an enlarged chamber at the base (e.g. in Torpedo rays) to ‘lobular’ or ‘alveolate’ ampullae with diverticulae emanating from a central chamber (Jørgensen 2005 ). The total number of ampullary organs varies between species, from the 148 to over 2000 (Bodznick & Boord 1986 ).

Adult lamprey electroreceptors are called ‘end buds’ (Ronan & Bodznick 1986 ). These are goblet shaped organs, 25–60 μm in diameter, found in groups of two to eight in the epidermis over the head and trunk on the surface of the skin. End buds are absent in larval lampreys (ammocetes), although ammocetes are known to be electroreceptive (Ronan 1988 ). Likely candidates for larval electroreceptors are multivillous cells found scattered throughout the epidermis in both ammocetes and adults (Whitear & Lane 1983 ). End buds are indistinguishable from the surrounding epidermis unless stained (Ronan & Bodznick 1986 ) and have no potential for preservation in the fossil record, even in lamprey fossils with good soft tissue preservation (Bardack & Zangerl 1968 ; Chang et al . 2006 ; Gess et al . 2006 ).

Electroreceptor structure and morphology in each group of vertebrates has been reviewed elsewhere (Jørgensen 2005 ; Baker et al . 2013 ). This section will focus on aspects of electroreception that are important for the recognition of electroreception in fossils: gross morphology, innervation and distribution.

Janvier ( 1974 ) interpreted a groove over the labyrinth cavity in the wax model of Stensiö ( 1927 ) as a possible ramus recurrens, connecting the preotic and postotic ganglia. A small canal in Benneviaspis , piercing the labyrinth cavity antero‐dorsal to the acoustic and facial nerves, is thought to have carried the ramus recurrens (Janvier 1985 ); it probably rejoined the postotic ganglion via the glossopharyngeal canal. As discussed above, the ramus recurrens is thought to be exclusively involved in innervation of trunk electroreceptors. This would indicate that osteostracans had electroreceptors, despite lack of convincing evidence for preservation of the electroreceptors themselves.

Despite these arguments, the morphology and innervation of the lateral fields is consistent with the electric organs of certain catfish (Janvier 1985 ) . Malapterurus catfish have thin electric organs, which may be derived from muscle despite their superficial position (Johnels 1956 ). Both an electric organ and a vibration sensor remain plausible possibilities for the function of the lateral and dorsal fields. They are unlikely to have housed electroreceptors.

Bohlin ( 1941 ) compared the dorsal and lateral fields of osteostracans with the ampullae of Lorenzini of elasmobranchs, at that time thought to be thermoreceptors (Sand 1938 ). Bohlin ( 1956 ) dismissed this idea, and suggested the fields were specialized hearing organs or mechanoreceptors. In this hypothesis, the canals connecting the fields to the labyrinth would have been filled with endolymph, and the roof of the cavity, formed from a mosaic of small plates, would have acted in a manner analogous to an eardrum. This idea was first put forward by Watson ( 1954 ), who argued that the canals leading to the lateral fields were far too wide to carry nerves, being much wider than the entry foramina for nerves VII and VIII into the labyrinth. Jarvik ( 1965 ) reinforced this interpretation of the lateral fields. Additionally, he identified one dorsal and five ventral protruberances in the labyrinth of lampreys, which might be vestiges of the SEL canals in osteostracans. Northcutt ( 1985 ) also considered the electric organ hypothesis unlikely, as the electric organs of modern species are innervated by postotic branchiomeric nerves and have associated expanded brain stem areas. He agreed with Jarvik ( 1965 ), arguing that the fields could be evaginations of the labyrinth homologous with the ciliated dorsal and lateral chambers of the lamprey labyrinth.

The electric organ interpretation was challenged based on comparison with electric organs in living species (Bohlin 1941 ; Wängsjö 1952 ), as the volume of the fields was too small and the nerves disproportionately large to support it. Wängsjö ( 1952 ) instead interpreted the lateral and dorsal fields as housing lateral line organs, and suggested that the well‐developed cerebellum of osteostracans was associated with this.

The dorsal and lateral fields (Fig. 4 C) were first suggested to be electric organs (i.e. for generating electric fields or shocking prey) by Stensiö ( 1927 ). Due to their superficial position he argued that they were unlikely to be derived from muscle (electric organs of modern species are derived from muscle). These ‘fields’ are connected to the labyrinth (inner ear cavity) by large canals (termed sinus expansions of the labyrinth or SEL) (Fig. 4 B). These were thought to provide nerves (Stensiö 1927 ). Electroreception was unknown at the time, but electric organs for stunning prey were well known. Living species with electric organs mostly also possess electroreceptors, although stargazers (Uranoscopidae) are an exception to this rule, having electric organs but no electroreceptors (Baron 2009 ).

Some tremataspid osteostracans have ‘porous fields’, clusters of microscopic pits that occur between tubercles (Afanassieva 2004 ; Märss et al . 2014 ). However, these have not been suggested to be electroreceptors, and they are smaller than any known electroreceptors.

Denison ( 1964 ) suggested that the ‘intercostal grooves’ of heterostracans (separating dentine ridges or tubercles) were homologous to the pore canal system of osteostracans. No electroreceptive function has been suggested for this system in heterostracans.

The argument for an electroreceptive function in osteostracans rests on extrapolation from the pore canal system in sarcopterygians (Thomson 1977 ), but the two systems may not be homologous (Meinke 1984 ). The sarcopterygian pore canal system is within a dentinous layer. In osteostracans it underlies the dentine layer, although it occurs in a lamellar layer resembling elasmodine, a hard tissue with plywood‐like structure which is putatively a form of dentine (Sire et al . 2009 ). Furthermore, the pore canal system in sarcopterygians may not be involved in electroreception (New 1997 , and see Discussion below).

In a detailed treatment of the pore canal system in sarcopterygians (lobe‐finned fish), Thomson ( 1977 ) extrapolated the proposed electroreceptive function of this system to osteostracans (see below for full discussion of sarcopterygian pore canal system). Stensiö ( 1927 ) initially suggested that the osteostracan pore canal system housed mucous canals. However, the pore canal system is connected to, and in cross‐section is indistinguishable from, the lateral line canals (Denison 1947 ). A mechanoreceptive function was therefore proposed. A mechanoreceptive function was further supported on the basis of synchrotron X‐ray microtomography (Qu et al . 2015 ). The mesh canals in Oeselaspis , which lack a horizontal dividing septum, connect to the outside via ‘polyp‐like’ structures resembling the nerve supply of neuromasts. In the divided mesh canals of Tremataspis , the upper portion was suggested to house epithelial invaginations, perhaps representing a more sophisticated version of the same sensory system (Qu et al . 2015 ).

The pore canal system of osteostracans is a polygonal network of ‘mesh canals’ in the middle layer of the exoskeleton connecting to the outside through ‘pore canals’ (Denison 1966 ; Sire et al . 2009 ; Fig. 4 A). The mesh canals are divided into dorsal and ventral halves by a thin, perforated bony septum in Tremataspis (Denison 1947 , 1966 ).

Structures in osteostracans that have been suggested to be electroreceptors or electric organs. A, dermal bone structure in, showing the pore canal system (highlighted in blue). B, ventral view of the internal cavities of the neurocranium in; sinus expansions of the labyrinth, canals that connect the inner ear to the lateral fields, are highlighted in yellow. C, dorsal surface of the head in; lateral fields, shallow troughs in the dermal bone, are highlighted in yellow. A, redrawn based on Denison (); B–C, redrawn based on Janvier ().

There are a number of jawless fish groups that may be more closely related to crown gnathostomes than extant jawless fish (Janvier 1996 ; Donoghue et al . 2000 ; Sansom et al . 2010 ). These are the arandaspids, anaspids, thelodonts, heterostracans, galeaspids, pituriaspids and osteostracans (Fig. 1 ). Of these groups, only osteostracans have morphological structures that have been suggested to represent electroreceptors (Bohlin 1941 ; Thomson 1977 ; Janvier 1985 ). Their bones contain a network of canals linked to the exterior via pores termed the ‘pore‐canal system’ (Denison 1964 ; Fig. 4 A), which has been suggested to house electroreceptors (Thomson 1977 ). Importantly, osteostracans also have shallow depressed areas along the edges of the head shield and posterior to the pineal opening (dorsal and lateral fields, Fig. 4 B), for which a number of functions have been suggested including both detection and generation of electric fields (Stensiö 1927 ; Bohlin 1941 ). For heterostracans, Ørvig ( 1989 ) came to the conclusion that electroreceptors must be absent, as no trace of them could be found in the dermal skeleton.

The yunnanolepidid antiarchs Yunnanolepis and Phymolepis have a pore and cavity on the trunk shield called the Chang's apparatus (Zhu 1996 ). The Chang's apparatus occurs at the junction of the anterior ventrolateral plate and the anterior dorsolateral plates, on a vertical ridge at the anterior edge of the trunk armour; internally it forms a blind‐ending tube. A small anterior lateral plate covers the opening for the Chang's apparatus in Phymolepis , so that the opening is obscured in lateral view. Zhu ( 1996 ) suggested that the Chang's apparatus housed ampullary electroreceptors, or that it was glandular and performed a role in mucus secretion. The function of the Chang's apparatus remains open to interpretation, although the position of this apparatus is not consistent with an electroreceptor identification.

The interolateral plates of many arthrodires possess a ventral sulcus (Fig. 14 ), a transverse groove on the ventral lamina. Ventral sulci are present in most basal arthrodires, but are only known in coccosteids within the eubrachythoracids (Zhu et al . 2015 , character 121). Miles ( 1965 ) suggested these may contain neuromasts or cutaneous sense organs analogous with cu.so pits of arthrodire cheek plates. However, as discussed above, there is little evidence to support an electroreceptor identity for cu.so pits. In addition, the position of these sulci (posterior to the branchial chamber on the ventral surface), would be highly unusual for a group of electroreceptors. We consider it highly unlikely that the ventral sulci of arthordires contained electroreceptors.

The Young's apparatus lacks an obvious analogue in living fish, hindering functional interpretations, but the large canals (perhaps for nerves) joining the base, principally in two positions, might suggest a sensory function. Possible comparisons are with various specialized mechanoreceptor systems, such as the vesicles of Savi of various dorsoventrally flattened elasmobranchs (Barry & Bennett 1989 ), or the submandibular organ of Potamotrygon (Szabo et al . 1972 ). Structurally, vesicles of Savi are pits with neuromast organs sitting in depressions at their base and, by comparison, the two depressions at the base of the Young's apparatus may have held neuromast organs. The position of the Young's apparatus on the skull suggests that possible functional roles may have been to detect movement of the cheek relative to the skull roof or movement of the cranial‐thoracic joint, through pressure changes on the apparatus that occur during joint movement. As with other structures reviewed for placoderms, the position of the Young's apparatus makes an electroreceptor interpretation difficult to support.

The Young's apparatus crosses almost the entire thickness of the plate in ANU V79 and V244. The histology of ANU V79 is different to that of the eubrachythoracid arthrodires shown in Figure 5 : rather than a laminar layer, the superficial layer consists of stacked tubercle generations, as reported for some buchanosteids (Burrow & Turner 1998 ; Giles et al . 2013 ). The cu.so pits penetrate approximately half the thickness of the plate, but still appear to penetrate deeper than the oldest generation of overgrown tubercles (Fig. 13 F).

The Young's apparatus in ANU V79 can be interpreted in light of the information from the quadrate of ANU V244. Although the quadrate is not preserved in ANU V79, the bone directly below the apparatus is highly cancellar (Fig. 13 A, B, D), and is probably the point of contact of the perichondral bone of the quadrate with the dermal bone. A small portion of the quadrate may be present below the Young's apparatus (Fig. 13 A, B), an interpretation supported by the canals that pierce this space (Fig. 13 B, arrows). Long canals, curving in a similar shape to the postsuborbital sensory line, connect the Young's apparatus and the posterior cu.so (Fig. 13 E). Above the posterior cu.so are two smaller pits (Fig. 13 E, acc.cu.so). One of these is continuous with the postsuborbital sensory canal.

The Young's apparatus in ANU V244 is closely associated positionally with the quadrate and jaw joint (Fig. 12 ). Hu et al . ( 2017 ) identified a separate interhyal element seated behind the quadrate in ANU V244. Revisiting the scans shows that the quadrate and interhyal are continuous, although there is a constriction in the quadrate behind the mandibular joint. Posterior to this constriction the ‘interhyal’ portion of the quadrate enters a tunnel in the dermal bone that is continuous with the submarginal process, as described by Hu et al . ( 2017 ). The Young's apparatus sits directly above the mandibular joint (Fig. 12 A, C). Various canals from the base of the apparatus and the posterior cu.so run around the quadrate or run at the interface of the quadrate and the dermal bone (Fig. 12 A). One canal from the Young's apparatus pierces the constricted portion of the quadrate behind the mandibular joint (Fig. 12 A).

ANU V79 internal structure of Young's apparatus and cutaneous sense organs. A–B, the Young's apparatus (dark green) sits above a region of highly cancellar bone with many canals (navy blue); a space within the bone may represent part of the quadrate (turquoise), and canals pierce this space (B, arrows). C, the Young's apparatus (posterior to the right); canals join to the ventral recesses in the centre and anterior of the pit; there is also a posteriorly directed recess. D, cross‐section of the Young's apparatus. E, lateral view of the postsuborbital plate showing Young's apparatus, posterior cu.so and their connections; bone in transparent beige, postsuborbital sensory canal in light blue; canals (navy blue) connect the Young's apparatus with the posterior cutaneous sense organ; two smaller pits are present dorsal to the cu.so (acc.cu.so). F, cross‐section of the posterior cutaneous sense organ; stacked tubercle generations are visible in the upper part of the bone. Abbreviations : acc.cu.so, accessory cutaneous sense organs; cu.so, cutaneous sense organs; psoc, postsuborbital sensory canal; Y.app, Young's apparatus. All scale bars represent 1 mm.

Internal structure of the Young's apparatus in ANU V244, showing the close association with the quadrate. Dermal bone in beige, transparent. Quadrate in turquoise, transparent. Young's apparatus and posterior cutaneous sense organ in dark green (opaque). Canals in navy blue (opaque). A, visceral view of the posterior part of the suborbital–postsuborbital complex. B, the Young's apparatus and posterior cu.so, with connecting canals. C, lateral view of the plate, showing the positions of the structures discussed. Abbreviations : cu.so, cutaneous sense organs; pr.sm, submarginal process; Y.app, Young's apparatus. Scale bars represent 1 mm (A, B) and 3 mm (C).

Externally the Young's apparatus is an elongate pit with a constriction, giving it a peanut‐like shape (Fig. 11 ). In both ANU V79 and V244 there are two recesses at the base of the apparatus, at the anterior and the middle, which connect to canals in the underlying bone (Figs 12 B, 13 A–C).

ANU V79 was initially suggested to belong to a heterostiid (Young 2011 ), but the suborbital plate of the recently described heterostiid Herasmius dayi (Schultze & Cumbaa 2017 ) has very different proportions from ANU V79. ANU V79 has several features in common with ANU V244, suggesting that it may instead be a ‘buchanosteid’. These features include a horizontal canal, a supraoral canal that does not contact the infraorbital canal, no clear suture between the postsuborbital and suborbital plates, presence of two cu.so pits and a strongly curved ventral margin. On the posterior part of the plate, on the visceral surface, is a dermal process (Fig. 10 , pr.sm). A similar process occurs in ANU V244, where it is associated with a possible interhyal element (but see below for an alternative interpretation), and braces the submarginal plate (Hu et al . 2017 ). The dermal process and Young's apparatus are only known in these two specimens, while they are absent in Parabuchanosteus (Young 1979 ), suggesting that ANU V79 and ANU V244 belong to a subgroup of ‘buchanosteids’. Although the orbital area of ANU V79 is broken, the curvature of the preserved portion suggests small orbits, such that ANU V79 has an unusual morphology relative to other ‘buchanosteids’.

The Young's apparatus in two ‘buchanosteid’ suborbital–postsuborbital plates. This unusual structure has so far only been found in these two specimens. A, ANU V244. B, ANU V79 in posterior ventral view. Abbreviations : acc.cu.so, accessory cutaneous sense organs; cu.so, cutaneous sense organ; hc, horizontal sensory canal; ioc, infraorbital sensory canal; psoc, postsuborbital sensory canal; sorc, supraoral canal; Y.app, Young's apparatus. Scale bars represent 5 mm (A) and 20 mm (B).

A distinct type of pit structure is found on the suborbital–postsuborbital complex of two specimens from Taemas‐Wee Jasper: an isolated arthrodire suborbital–postsuborbital (ANU V79; Figs 10 , 11 ), and the ‘buchanosteid’ ANU V244 (Young et al . 2001 ; Hu et al . 2017 ; Fig. 11 ). This structure is distinct from the cu.so in being larger, having a more complex shape and penetrating almost the entire thickness of the bone. Here we erect the name ‘Young's apparatus’ for these unusual structures, in honour of Gavin C. Young, the world's leading authority on buchanosteid placoderms and Taemas‐Wee Jasper fossils. The Young's apparatus was labelled as a ‘sensory sulcus’ in ANU V244 by Hu et al . ( 2017 ).

However, the presence of canals joining the cu.so in Romundina and some buchanosteid arthrodires (see below) might suggest a sensory function, although only in Romundina can these canals be traced back to cranial nerves (Dupret et al . 2017b ). They may have housed an adirectional pressure detector, but their function cannot be determined with confidence.

Finally, the presence of long cu.so grooves in the presumed freshwater Wuttagoonaspis is also inconsistent with an electroreceptor identity. As discussed above, in living freshwater electroreceptive species, ampullae lie at the base of very short canals. The 10 mm groove in Wuttagoonaspis is therefore unlikely to represent an electroreceptor. The combination of the low number, orientation, association with bone growth and presence of long canals in freshwater species all suggest that cu.so pits are not electroreceptors.

The CT scans reveal that the orientation of the pits is influenced by growth. The depth of the superficial layer of exoskeleton determines the depth of the cu.so. Vertical pits occur when the superficial layers are also vertical, which may be indicative of rapid growth (de Boef & Larsson 2007 ; Giles et al . 2013 ). The groove‐like pits may occur in slow growing plates, with their orientation determined by the relative position of the cu.so to the growth centre. The intimate association of the cu.so pits with the growth of the plate suggests that they are not directional sense organs. In particular, the posteriorly orientated, dorsal cu.so of Wuttagoonaspis is inconsistent with electroreceptors in living species, in which they are most densely distributed around the snout and mouth.

Cutaneous sense organs of placoderms do not demonstrate any of the criteria outlined above that would allow a positive identification of electroreceptors. The diameter of cu.so pits is consistent with the size of a single ampullary canal, rather than a capsule containing multiple canals as suggested by Ørvig ( 1960 ). The low number of cu.so pits stands in contrast to the generally hundreds of ampullary organs in extant vertebrates. There is no expanded ampullary bulb at the base of the cu.so pits.

Plates without cutaneous sense organs still have thick superficial laminar layers. A, Camuropiscis sp. suborbital plate (SAM P53772). B, torosteid sp. postsuborbital plate (SAM P50606). The internal spaces within the superficial laminar layer are shown in blue. This layer was still substantial in these plates that lack cutaneous sense organs, suggesting that lack of these structures is not simply a result of a thin or absent superficial layer. Both scale bars represent 10 mm.

Since cu.so pits appear to be confined to the superficial layer of the dermal bone in eubrachythoracid arthrodires, the question arises of whether the absence of pits in some taxa simply reflects a very shallow or absent superficial layer. Scans of arthrodire cheek plates that lack pits (Fig. 9 ), demonstrate that this is not the case. A superficial layer is present despite the lack of a cu.so, suggesting that absence of a cu.so may be phylogenetically informative.

Posteriorly orientated cutaneous sense organs in the unusual anteriorly positioned suborbital plate of. A, dorsal view of the right side of the skull of; suborbital and postsuborbital plates highlighted in red; note the anterior position of the junction between the infraorbital and supraoral canals (and presumably therefore the growth centre). B, natural mould of the anterior dorsal right part of the skull, showing sensory canals and cu.so in positive relief; the cu.so in this specimen (AM F53628) is a particularly long groove, orientated posteriorly away from the presumed growth centre at the extreme anterior part of the plate. A is redrawn based on Miles & Young (). Scale bar represents 10 mm.: cu.so, cutaneous sense organ; ioc, infraorbital sensory canal; orb, orbit; soc, supraorbital canal; sorc, supraoral canal.

The unusual morphology of the arthrodire Wuttagoonaspis , which has an elongate suborbital plate facing dorsally and firmly united with the skull roof, makes its cutaneous sense organs an interesting case study (Fig. 8 ). The cu.so can be studied in specimens which preserve the suborbital plates as natural moulds, thus revealing the internal morphology of the pit in positive relief (Fig. 8 B). The cu.so is an elongate groove, but the angle and length of the groove varies considerably between specimens. The specimen shown in Figure 8 B (AMF 53628) is the most extreme example: other specimens have shorter grooves. The cu.so is always orientated posteriorly, consistent with an elongate suborbital plate with the growth centre (assumed to lie near the confluence of the infraorbital and supraoral sensory lines) placed at the extreme anterior end of the bone.

The orientation of the pits also follows the orientation of the canals in the superficial layer. In the Kimberleyichthys and Torosteus postsuborbitals, in which the pits form elongate grooves, canals within the superficial layer are orientated almost parallel to the surface, and radiate out from the growth centre of the plate (Fig. 7 E–G). The groove‐like cutaneous sense organs run parallel to these superficial layer canals, and appear to project away from the growth centre of the plate (Fig. 7 G). In the Eastmanosteus postsuborbital plate, the canals in the superficial layer are vertical, and therefore so is the pit (Fig. 7 B). In the Torosteus suborbital, the pit is again parallel to the canals in the superficial layer, this time at a slight angle to the vertical (Fig. 7 D).

Relationship of cutaneous sense organs with the underlying bone structure. Spaces within the basal laminar (purple), middle cancellar (green) and superficial laminar (blue) layers are coloured separately. The cutaneous sense organs (dark green) are found in the superficial layer. When canals in the superficial layer are predominantly vertical, the pits are also vertical (A–D). The groove‐like pits occur when the canals in the superficial layer are near horizontal (E–G). The groove‐like pits also follow the direction of the superficial layer canals, radiating out from the growth centre of the plate (G). A–B, Eastmanosteus calliaspis postsuborbital plate (MVP231104). C–D, Torosteus tuberculatus suborbital plate (MV P230808). E, Torosteus tuberculatus postsuborbital plate (MV P230808). F–G, Kimberleyichthys bispicatus postsubobital plate (ANU V1686). All scale bars represent 1 mm.

The CT scans allow the spatial relationship of these pits with the underlying structure of the dermal bone to be investigated (Fig. 7 ). Placoderm dermal bones typically have a three‐layer structure, with basal laminar and middle cancellar layers overlain by a superficial layer of either semidentine tubercles or laminar bone (Giles et al . 2013 ). These layers are easily distinguished from each other when the internal vascular canals are segmented and viewed in three dimensions (Fig. 7 ). The cutaneous sense organs (dark green, Figs 6 , 7 ) are mostly confined to the superficial layer, although in all cases they dip into the middle layer (Fig. 7 ). The depth of the pit therefore seems to depend on the depth of the superficial layer. In Eastmanosteus , which has a very deep pit, the superficial layer is also very deep (Fig. 7 A, B).

The morphology of cutaneous sense organ pits, as shown by CT scans, varies from deep pits to shallow grooves (Fig. 6 ). The postsuborbital plate of Eastmanosteus callispis has a deep, vertical, funnel‐shaped pit (Fig. 6 A), whereas the postsuborbital plates of Torosteus and Kimberleyichthys have cutaneous sense organs that form grooves, with that in Kimberleyichthys being particularly elongate (Fig. 6 D, E). The suborbital of Parabuchanosteus has a shallow, rounded, vertical pit (Fig. 6 B). The Torosteus suborbital plate has a pit that is inclined at a slight angle, and is intermediate between the vertical pits and groove‐like pits (Fig. 6 C). The groove‐like pits have the appearance of being blind‐ending tubes projecting almost horizontally.

Outside the arthrodires, cutaneous sensory organs are known from the skull roofs of the acanthothoracid placoderms Romundina and Brindabellaspis , situated behind the orbit near the confluence of the main lateral line canal and the infraorbital canal (Ørvig 1975 ; Young 1980 ). Dupret et al . ( 2017b ) described two pairs of sensory pits behind the orbit of a different specimen of Romundina . Both pits in Romundina are innervated by a nerve that emanates from the confluence of the trigeminal and facial nerves behind the orbit (Dupret et al . 2017b ). The petalichthyid placoderm Eurycaraspis possesses a group of three foramina towards the posterior of the skull roof, near the confluence of the main lateral line canal and the posterior pit line (Liu 1991 ). Ørvig ( 1971 ) described multiple cutaneous sensory organs surrounding sensory lines in skull bones of the ptyctodontid Ctenurella , but material from Gogo, preserved in three dimensions, shows no evidence for the presence of sensory pits (Long 1997 ; Trinajstic et al . 2012 ). As with Rhachiosteus these ‘pits’ in ptyctodontids are likely to simply be open bone structure around the edges of plates. Cutaneous sensory organs have been described in the yunnanolepid antiarch Phymolepis on the suborbital plate (Young & Zhang 1996 ). Cutaneous sense organs are therefore known from three major placoderm groups (arthrodires, antiarchs and acanthothoracids).

In non‐brachythoracid arthrodires, preservation of cheek plates is relatively rare. Cutaneous sense organ pits are absent in Holonema (Miles 1971 ) and Dicksonosteus (Goujet 1975 ). However a pit is found on the suborbital plate of Wuttagoonaspis (Ritchie 1973 ; Miles & Young 1977 ; Young & Goujet 2003 ), which occupies a very basal position in arthrodire phylogeny (Dupret et al . 2009 , 2017a ).

In more basal brachythoracid arthrodires, pits are found on the suborbital plates of Parabuchanosteus (White & Toombs 1972 ; Young 1979 ), Gemuendenaspis (Miles 1962 ), Atlantidosteus (Young 2003 ; Fig. 5 D) and Urvaspis (Long et al . 2014 ). Atlantidosteus has a large cutaneous sense organ and a group of smaller pits at the confluence of the supraoral and infraorbital sensory lines (Young 2003 ; Fig. 5 D).

These pits are not so well known in the dunkleosteoid and aspinothoracid ( sensu Zhu & Zhu ( 2013 )) eubrachythoracid arthrodires. However, postsuborbital pits are known in Eastmanosteus calliaspis (Dennis‐Bryan 1987 ). Miles ( 1966 ) described a number of pits in Rhachiosteus , which has recently been placed within the Dunkleosteoidea (Zhu et al . 2015 ), but these appear to be unrelated to the cheek plate ‘cu.so pits’ of other arthrodires, and may simply be due to the bone structure becoming more open and porous toward the edge of plates, as in many other placoderms (pers. obs.).

Within arthrodires, cutaneous sensory organ pits are most commonly found on the suborbital and postsuborbital plates of eubrachythoracid arthrodires: the suborbital and postsuborbital plates of Coccosteus (Stensiö 1963 ; Fig. 5 B), Watsonosteus (Miles & Westoll 1962 ), Goodradigbeeon (White 1978 ), Torosteus (Gardiner & Miles 1990 ) and Plourdosteus (Ørvig 1960 ) and the postsuborbital plate of Harrytoombsia (Miles & Dennis 1979 ), Mcnamaraspis (Long 1995 ), Simosteus (Dennis & Miles 1982 ), Compagopiscis (Gardiner & Miles 1994 ), Dickosteus (Miles & Westoll 1962 ) and Kimberleyichthyes (Dennis‐Bryan & Miles 1983 ). These pits therefore appear to have been a widespread feature in coccosteomorph ( sensu Carr & Hlavin ( 2010 )) arthrodires, although they are absent in Incisoscutum , Camuropiscis , Tubonasus , Latocamurus and Rolfosteus (Dennis & Miles 1979a , b ; Long 1988a ). The latter taxa are deeply nested within coccosteomorphs (Zhu & Zhu 2013 ), suggesting secondary loss.

Placoderm cutaneous sense organs. A, diagram ofskeleton in left lateral view, with the suborbital and postsuborbital plates highlighted in red. B, diagram of the suborbital and postsuborbital plates of, showing positions of the anterior and posterior cu.so pits. C,postsuborbital plate with cu.so pits (NMS 1859.33.620). D,suborbital plate with multiple small cu.so pits (ANU V1033). E,suborbital and postsuborbital plates, with cu.so pits (NHMUK P44544). A–B, redrawn based on Gardiner & Miles (). All scale bars represent 10 mm.: cu.so, cutaneous sense organ; ioc, infraorbital canal; psoc, postsuborbital canal; sorc, supraoral canal.

In some arthrodire placoderms, large ( c . 1 mm) isolated pits in the cheek plates, called cutaneous sense organs (cu.so), are putative electroreceptors (Ørvig 1960 ; Fig. 5 ). They were compared to the clusters of ampullae of Lorenzini of elasmobranchs, a short time before they were shown to be electroreceptors in sharks (Murray 1960 , 1962 ).

Osteichthyans (bony fish)

The pore canal system and cosmine The dermal skeleton of many early sarcopterygians is characterized by cosmine, a covering of dentine and enamel containing a pore canal system (Ørvig 1969; Thomson 1975; Meinke 1984). The pore canal system involves a horizontal network of mesh canals in the dentinous layer, with vertical pore canals opening to the surface (Fig. 15A, B). Thomson (1977) suggested an electroreceptive function for the pore canal system, based on a detailed study of cosmine in Ectosteorhachis (Thomson 1975). He argued that since sensory lines are well developed in the fossils, the pore canal system was unlikely to have also housed neuromasts. While the structure of the pore canal system was acknowledged to be significantly different from that of the ampullae of Lorenzini, the size and spacing of electroreceptors in freshwater teleosts was considered comparable. Furthermore, it was suggested that the pore canal system housed tonic electroreceptors (= ampullary receptors, sensitive to low frequency AC and DC fields), while the larger ‘pore group’ receptors of osteolepids (discussed in the next section) housed phasic electroreceptors (= tuberous receptors, sensitive to high frequency AC fields used for communication). In modern mormyrids, tuberous receptors are indeed larger than the ampullary organs (Bennett 1971), but the identification of tuberous receptors in osteolepids remains largely speculative. Figure 15 Open in figure viewer PowerPoint 1969 Megalichthys hibberti (NMS 1957.1.5688). C, incomplete covering of cosmine on the right squamosal and right‐hand side of the postparietal shield in Megalichthys hibberti (NHMUK P11554). Scale bars represent 2 mm (B) and 10 mm (C). Cosmine and cosmine resorption. A, cross‐sectional structure of cosmine, after Ørvig (); the pore canal system is highlighted in blue; a horizontal mesh of canals in the dentine layer joins to the surface via pore canals. B, cosmine pores on the skull of(NMS 1957.1.5688). C, incomplete covering of cosmine on the right squamosal and right‐hand side of the postparietal shield in(NHMUK P11554). Scale bars represent 2 mm (B) and 10 mm (C). Against the idea of the pore canal system being electroreceptive is the fact that the pores are more densely spaced posteriorly (Thomson 1977), in direct opposition to the pattern seen in all modern electroreceptive vertebrates (Borgen 1992). In addition, as pointed out by New (1997), connections between adjacent ampullae, as seen in the pore canal system, would nullify the spatial resolution of the system. This is because each canal would no longer be insulated from the rest, so that the whole network would become isopotential. Studies on the living lungfish Neoceratodus do not support an electroreceptive function for the pore canal system (Bemis & Northcutt 1992). Although Neoceratodus lacks cosmine, Bemis & Northcutt (1992) described a rich array of cutaneous blood vessels in the epidermis of the snout, supplying dermal papillae (capillary loops in connective tissue). Similar capillary loops were found in the hypermineralized tooth plates of Neoceratodus. On this basis, they argued that dermal papillae are vestigial organs involved in the deposition of dentine. Under this hypothesis this process is halted in an early stage of development in modern lungfish, before the deposition of mineralized tissues (Bemis & Northcutt 1992). The hypothesis that the pore canal system is involved in deposition of mineralized tissue perhaps fits better with certain observations on cosmine development. Cosmine bears no developmental relation to the underlying dermal bone and is uninterrupted across sutures between bones. This causes problems with growth and it is generally thought that cosmine went through cycles of resorption and redeposition (Westoll 1936; Gross 1956; Fig. 15C). Resorption may start at the cosmine pores (Borgen 1989). Based on the incomplete covering of cosmine in larger individuals of Ectosteorhachis (see also Fig. 15C for Megalichthys) it was suggested that cosmine acts as a store for excess phosphates that could be mobilized at certain times, perhaps during the breeding season (Thomson 1975). If this is the case then an efficient system for deposition and resorption as proposed by Bemis and Northcutt would be expected, and the pore canal system may be associated with this function. Overall, it appears unlikely that the pore canal system housed electroreceptors.

Rostral tubuli in lungfish The rostral and symphysial tubuli of fossil lungfish (Fig. 16) were first identified by Thomson & Campbell (1971) in Dipnorhynchus. Rostral tubuli occur in the snout and mandible, and consist of a series of mineralized, branching tubules forming a plexus beneath the dermal exoskeleton (Thomson & Campbell 1971; Fig. 16A, B). They connect with the pore canal system and also extend internally to open into the nasal capsule or meckelian cavity (Miles 1977; Cheng 1989). Recently, rostral tubuli have also been found in the non‐Dipnoan taxa Gogonasus and Qingmenodus (Holland 2014; Lu et al. 2016). Figure 16 Open in figure viewer PowerPoint Rostral tubuli on the snout of Devonian lungfish. A, Dipnorhynchus kurikae (ANU V48676), anterior part of skull in left lateral view (dermal bones not preserved) revealing rostral tubuli in the anterior part of the snout; note the sharp discontinuity between the rostral tubuli and the dermal bone. B, Chirodipterus australis (NHMUK P50101), inside of dermal snout bones in posteroventral view showing rostral tubuli. Both scale bars represent 10 mm. Colour online. Although it has been proposed that rostral tubuli housed ampullae of Lorenzini (Thomson & Campbell 1971; Campbell & Barwick 1986) the branching structure of the tubules, forming a plexus, does not fit this hypothesis. Alternatively, Cheng (1989) proposed that the tubuli were a part of the lateral line system, in part because they have a similar histological structure to the lateral line canals. However, the rostral tubuli appear to carry nerves: specifically, the profundus, superficial ophthalmic and buccal nerves (Miles 1977; Challands 2015). Campbell et al. (2010) also argued that rostral tubuli carried nerves, as they connect with the lateral line canals, and some tubules open through the dorsal wall of the nasal cavity as found for nerve bundles in Neoceratodus (Bartsch 1993). Although it is unlikely that the rostral tubuli themselves housed electroreceptors, they may have supplied nerves to electroreceptors (see below). An alternative view is that the rostral tubuli carried lymphatic vessels (Bemis & Northcutt 1992; Kemp 2014, 2017). The snout of Neoceratodus, the Australian lungfish, has unmineralized tubules that form a double plexus in the dermis which may be comparable to rostral tubuli, first interpreted as blood vessels (Bemis & Northcutt 1992), but later found to be lymphatics (Kemp 2014, 2017). At present it is difficult to reconcile the data from living lungfish (suggesting that rostral tubuli are lymphatics) and fossil lungfish (suggesting that they are nerves). However, given the clear connections with the neurocranium and sensory line canals (Campbell et al. 2010; Challands 2015), we assume that at least part of the rostral tubuli carried nerves for our interpretation of the pore‐group pits (see below).

Pore‐group clusters in sarcopterygians A more likely candidate for electroreceptors in sarcopterygians are the ‘pore groups’, first identified by Jarvik (1948), who compared them to ampullae of Lorenzini. He identified clusters of pits near sensory canals or pit‐lines on the lower jaw, lacrymal, jugal, postorbital, squamosal, fronto‐ethmoidal shield and the branchiostegal rays of the osteolepid tetrapodomorph fishes Osteolepis, Gyroptychius and Thursius (Fig. 17A, B). The pores are intermediate in size between those of the sensory canals and the cosmine pores, and fine canals lead from their bases (Jarvik 1948). Similar pores have been found in a number of basal tetrapodomorph fishes, including Kenichthys (Chang & Zhu 1993), Tungsenia (Lu et al. 2012), the canowindrid Koharalepis (Young et al. 1992; Fig. 17D) and the megalichthyids Megalichthys (Bjerring 1972; Fig. 17C), Mahalalepis (Young et al. 1992) and Cladarosymblema (Fox et al. 1995). Pore‐group clusters resembling those of osteolepiforms have also been found in the early Devonian Powichthys (Jessen 1975) and Youngolepis (Zhang & Yu 1981), which are basal dipnomorphs, the lineage that includes lungfish (Lu et al. 2012). Figure 17 Open in figure viewer PowerPoint 1948 Gyroptychius milleri (NMS 1895.185.25). C, pore‐group cluster in Megalichthys intermedius (NHMUK P3303). D, pore‐group clusters in Koharalepis (AM F54325). E, electroreceptor pore cluster in the paddlefish Polyodon spathula (from Jørgensen et al. 1972 Megalichthys; the sensory canal is in blue, and the dorsally branching canal at the base of the pore‐group cluster in red (redrawn and adapted from Bjerring 1972 Abbreviations: ot.lat, branches of the otic lateralis nerve; ST, supratemporal bone. Scale bars represent 1 mm (B, C) and 10 mm (D). Pore‐group clusters in fossil sarcopterygians, compared with the electroreceptor clusters of the extant paddlefish. A, diagram of dorsal skull roof of a generalized osteolepidid, after Jarvik (), showing locations of pore‐group clusters; these are closely associated with sensory lines. B, pore‐group cluster on snout region of(NMS 1895.185.25). C, pore‐group cluster in(NHMUK P3303). D, pore‐group clusters in(AM F54325). E, electroreceptor pore cluster in the paddlefish(from Jørgensen; re‐used with permission). F, dorsal (left) and ventral (right) view of canals within the supratemporal bone of the tetrapodomorph; the sensory canal is in blue, and the dorsally branching canal at the base of the pore‐group cluster in red (redrawn and adapted from Bjerring).: ot.lat, branches of the otic lateralis nerve; ST, supratemporal bone. Scale bars represent 1 mm (B, C) and 10 mm (D). Pore‐group clusters are good candidates for electroreceptors. They occur close to sensory lines and are particularly densely distributed around the snout (Fig. 17A). They occur in fossil sarcopterygians with cosmine. Cosmine, with its covering layer of enamel, may allow superficial structures that do not typically leave an impression in dermal bone to be preserved. The pit clusters, including the variability in the size of the pits, resemble the electroreceptor pit clusters in the paddlefish Polyodon (Jørgensen et al. 1972; Fig. 17E). The internal structure of the pore‐group clusters has been investigated in the tetrapodomorph Megalichthys using serial grinding techniques (Bjerring 1972). This revealed that the pore group on the supratemporal bone is connected to a dorsally branching canal that pierces the ventral surface of the bone (Fig. 17F). The canal at the base of the pore groups lies in close proximity to canals at the base of the sensory canal (Fig. 17F, ot.lat) and on this basis was inferred to have carried a branch of the otic lateral line nerve (Bjerring 1972). Although Bjerring's suggestion was that the pore groups might supply thermoreceptors, the available evidence suggests that pore groups may be electroreceptors. The results from serial grinding of Megalichthys are consistent with results from CT scanning pore‐group pits in lungfish, presented in the next section, which provide additional evidence that pore‐group pits are electroreceptors. The cosmine‐coated osteolepiform Gogonasus does not have pit clusters (Long et al. 1997), and it was suggested that this may be due to water salinity, although this interpretation does not fit with comparisons of marine and freshwater species in extant taxa (see above). The presence of pore groups in Powichthys and Youngolepis shows that these clusters can be found in marine species. Gogonasus also has a cavity in the neurocranium that has been compared to the rostral organ of coelacanths (Holland 2014), but this lacks connections to the surface.

New information on lungfish pore‐group pits Pore‐group pits are also known from the skulls of lungfish where they are often so numerous on the snout that they do not form obvious clusters (Jarvik 1950; Ørvig 1961; Bemis & Northcutt 1992). In some specimens of Chirodipterus, many of the pores on the snout appear to occur in pairs (Campbell et al. 2010). In Rhinodipterus, pore clusters are found on the jaw and gular bones in addition to the skull (Ørvig 1961), and clusters of pits occur on the operculum of the lungfishes Howdipterus and Barwickia (Long 1992). The pore‐group pits are intermediate in size between the cosmine pores and the lateral line pores and are densely distributed on the snout alongside the lateral line pores (Ørvig 1961; Bemis & Northcutt 1992; Fig. 18). The pores are variable in size: those on the downturned tip of the snout are larger than those further dorsally (Ørvig 1961; Gross 1965; Bemis & Northcutt 1992; Fig. 18C). The smaller cosmine pores are less abundant or absent anteriorly (Bemis & Northcutt 1992). The size, distribution and number of pore‐group pits in fossil lungfish are consistent with their identification as electroreceptors (Bemis & Northcutt 1992). In extant lungfishes, electroreceptor pores also increase in size at the tip of the snout (Kemp 2014). Figure 18 Open in figure viewer PowerPoint Numerous pore‐group pits on the snouts of Devonian lungfishes. A, Chirodipterus australis (ANU 21634a), skull in left antero‐dorsal view; pores on the snout are densely distributed around the lateral line pores, and some appear paired. B, Chirodipterus australis (NHMUK P50101) in dorso‐lateral view, showing pore groups clustered around sensory line canals. C, same specimen as B; anterior view showing enlarged pores, with highest density around the sensory lines. All scale bars represent 10 mm. Colour online. CT scans reveal new information on the internal structure of the pore‐group pits in the lungfish Speonesydrion (Figs 19-21). As with other fossil lungfish snouts, cosmine pores are numerous at the posterior of the specimen but are rare or absent anteriorly. Pore‐group pits are most densely distributed around the lateral line pores anteriorly (Fig. 19). Figure 19 Open in figure viewer PowerPoint Speonesydrion iani showing pore groups. A, dorsal view of specimen ANU 49340. B, anterior view of same specimen. Area with dashed white border indicates the segmented regions (see Fig. The snout of the lungfishshowing pore groups. A, dorsal view of specimen ANU 49340. B, anterior view of same specimen. Area with dashed white border indicates the segmented regions (see Fig. 20 ). Images from Drishti. Both scale bars represent 10 mm. Colour online. Figure 20 Open in figure viewer PowerPoint Speonesydrion iani ANU 49340 (imaged in Mimics), and their connections to rostral tubuli. A, internal model of a dorsal region of the snout (outlined in Fig. Internal structure of pore‐group pits in the lungfishANU 49340 (imaged in Mimics), and their connections to rostral tubuli. A, internal model of a dorsal region of the snout (outlined in Fig. 19 A); cosmine pores (burgundy) become less common anteriorly, while pore‐group pits (light red) become more common; rostral tubuli are in lavender colour and sensory lines and pores in blue. B, two individual clusters of pore‐group pits from A, showing their connections to a single opening of the rostral tubuli (arrows). C, internal model of a region of the anterior part of the snout (outlined in Fig. 19 B); connection of a cluster of pore‐group pits to an opening of the rostral tubuli is indicated with an arrow. D, cross‐section of the dorsal part of the snout (through A); connection of the rostral tubuli to canals joining the base of a pore‐group cluster is indicated with an arrow (equivalent to right‐hand arrow in B). All scale bars represent 1 mm. Figure 21 Open in figure viewer PowerPoint Speonesydrion iani (ANU 49340); pore‐group pits from anterior region of snout (outlined region in Fig. Chirodipterus australis (ANU V1710); pair of pore‐group pits indicating flask‐like shape (possible ampullae) and connections to underlying rostral tubule (lavender). Scale bars represent 200 μm (A) and 500 μm (B). Possible ampullae at the base of pore‐group pits in fossil lungfish. A,(ANU 49340); pore‐group pits from anterior region of snout (outlined region in Fig. 19 B); arrows indicate possible ampullae with canals continuing into the underlying bone. B,(ANU V1710); pair of pore‐group pits indicating flask‐like shape (possible ampullae) and connections to underlying rostral tubule (lavender). Scale bars represent 200 μm (A) and 500 μm (B). Internally, the structure of the dermal bone is as reported by Cheng (1989) for the snout of Chirodipterus: the cosmine layer is underlain by cancellar bone, and a basal laminar layer is absent. There is a sharp discontinuity between the underlying rostral tubuli and the dermal bone, as previously reported (Cheng 1989; Campbell & Barwick 2000; Campbell et al. 2010). The shape of the pore‐group pits is suggestive of an electroreceptive function. The external part of the pore‐group pits, within the cosmine layer of the dermal bones, resembles that of the smaller cosmine pores. They are constricted dorsally, appearing triangular in cross‐section. The pore‐group pits differ from the cosmine pores in that each one continues into the upper part of the cancellar bone (Gross 1965; Schultze 2016; Fig. 20A, D). The combination of the dorsally constricted part in the cosmine and the canal in the cancellar bone gives the pore‐group pits the overall shape of an arrow (Figs 20, 21). The pore‐group pits show evidence for ampullae at the base; some of the clearer examples for Speonesydrion are shown in Figure 21A. These ampullae sit in the cancellar bone layer. The depth from the surface to the base of the ampullae is c. 500–720 μm (n = 7 pits). The diameter of the canals in the constricted part above the ampullae is 170–280 μm on the anterior part and 110–250 μm posteriorly. Chirodipterus also shows evidence for ampullae, giving the pits a flask‐shape (Fig. 21B). The flask shape of the pores in Speonesydrion, Chirodipterus and Griphognathus is also clearly visible in figures 8, 13, 15 and 17 of Campbell et al. (2010). Canals connect the rostral tubuli with clusters of pore‐group pits (Figs 20B–D, 21B). Clusters of pits are supplied by an upwardly branching system of canals emanating from a single opening of a rostral tubule. These clusters vary in number: clusters with between two and six pits have been observed but larger clusters may exist. In Chirodipterus, many of the pores are paired (Campbell et al. 2010; Fig. 18A), but pore groups are not universally paired in Chirodipterus or Speonesydrion (Figs 18B, 19). As previously reported (Campbell et al. 2010), some of the rostral tubuli cross the discontinuity between the dermal bone and the underlying neurocranium. The upwardly branching system of canals at the base of the pore‐group pits may have housed a nerve supply from the rostral tubuli, although it should be noted that these have also been suggested to carry vessels (see above). In summary, the morphological evidence presented here supports the identification (based on size and distribution) presented by Bemis & Northcutt (1992) that the pore‐group pits are electroreceptors. They meet the criteria listed above for the identification of electroreceptors in fossils. The size, distribution (concentrated on the snout and around lateral line canals) and the possible presence of ampullae are all consistent with electroreceptor identification. As noted by Campbell et al. (2010), the pore‐group pits have differing orientations, as do the electroreceptors of modern species. Rostral tubuli communicate with the lateral lines and presumably carried nerves (Miles 1977; Campbell et al. 2010; Challands 2015, but see discussion on rostral tubuli above), and it is likely that lateral line nerves also innervated the pore‐group clusters via the rostral tubuli. Finally, although the depth and diameter of the pore group pits is larger than the values reported for living lungfish (Roth & Tscharntke 1976; Kemp 2014), this might be expected given that the fossils dealt with here are marine species (see above for explanation of differences between electroreceptors in marine and freshwater species).

The rostral organ in coelacanths The presence of a rostral organ in fossil coelacanths can be inferred from the presence of large foramina in the skull bones, similar to the pores for the rostral organ in the extant Latimeria (Forey 1998; Fig. 22A). These are present in coelacanths of Devonian age: Miguashaia, Gavinia, Euporosteus and Diplocercides (Cloutier 1996; Forey 1998; Long 1999; Fig. 22B). These taxa are the earliest coelacanths known from relatively complete remains, and they are also the most basal taxa in coelacanth phylogeny (Zhu et al. 2012). In addition to openings through the dermal bones, Euporosteus also preserves the anterior portion of the neurocranium, in which a median cavity for the rostral organ has been reconstructed (Jarvik 1942), and rostral organ pores are visible on the external surface (Jarvik 1942; Forey 1998; Fig. 22B). Although the anterior part of the neurocranium of Diplocercides (= Nesides) is incomplete, there is a notch which has been interpreted as the opening for the posterior inferior rostral organ tube (Jarvik 1980; Forey 1998). In contrast to modern coelacanths, in which the anterior rostral organ pore passes through the median rostral bone and the posterior pores lie ventral to the posterior tectal (Forey 1998), those in early fossil coelacanths pass through the premaxilla and preorbital respectively (Cloutier 1996; Forey 1998; Long 1999). However, although the association of rostral organ pores with particular dermal bones has changed, the number and position of these rostral organ pores has apparently remained constant for nearly 400 million years of evolution, and a rostral organ was present in the earliest recognizable coelacanths. Figure 22 Open in figure viewer PowerPoint Latimeria chalumnae showing the two posterior openings for the rostral organ (reproduced with permission from the Digital Fish Library, Euporosteus eifeliensis in left lateral view, showing openings for the rostral organ (redrawn after Forey 1998 The rostral organ in living and fossil coelacanths. A, head ofshowing the two posterior openings for the rostral organ (reproduced with permission from the Digital Fish Library, http://www.digitalfishlibrary.org ). B, drawing of the ethmosphenoid ofin left lateral view, showing openings for the rostral organ (redrawn after Forey). Colour online.

Early actinopterygians and a possible stem osteichthyan In early actinopterygians, potential electroreceptor pits have been identified on skull bones in Howqualepis (Long 1988b). The enigmatic early osteichthyan ‘Ligulalepis’ (Basden et al. 2000; Basden & Young 2001) has similar structures above the orbits (Fig. 23). The phylogenetic position of ‘Ligulalepis’ is uncertain, and it may be a stem osteichthyan rather than an actinopterygian (Friedman 2007; Friedman & Brazeau 2010). Here it is discussed alongside Howqualepis for convenience and due to the similarity of the structures under discussion. Figure 23 Open in figure viewer PowerPoint Possible electrosensory pits in the early osteichthyan ‘Ligulalepis’ (ANU V3628; A–D) and the early actinopterygian Howqualepis (NMV P160780; E). A, right lateral view of the skull of ‘Ligulalepis’; dermal bone transparent, showing an irregular series of pores above the orbit (red) alongside sensory line canals (blue). B, visceral view of dermal skull roof, showing openings on the right‐hand side of the skull. C, internal structure above the orbit on the left side of the skull, in posterior‐mesial view; one of the pit structures is connected via a canal at its base (arrow 1) to a branch of the otic nerve, which innervates the sensory canals; the most posterior pit also has a canal at its base (arrow 2); although this is incomplete ventrally, it may be a dorsal branch of the superficial ophthalmic nerve. D, internal model and cross section of a pit from the left‐hand side of the skull, anterior view, showing the expanded base. E, series of pits above the orbit in the actinopterygian Howqualepis rostridens (latex peel, whitened with ammonium chloride). Scale bars represent 1 mm (A–C, E) and 200 μm (D). Abbreviations: ioc, infraorbital sensory canal; ot.lat, branches of the otic lateralis nerve; soc, supraorbital sensory canal; soph, superficial ophthalmic nerve. In ‘Ligulalepis’, the pits are found on both sides of the skull above the orbits (Fig. 23A), although the distribution is not strictly symmetrical. There are two main groups: a line alongside the supraorbital sensory canal, and a second group around the intersection of the otic and infraorbital sensory canals (Fig. 23A). The size and shape of individual pits are variable. In ‘Ligulalepis’ some of the pits, particularly the posterior group, have very small openings, and are barely visible in dorsal view. The pits fully penetrate the bone (Fig. 23B) and their bases are expanded (Fig. 23D), which may hint at the presence of ampullae. Two of the pits on the left‐hand side have connecting canals at their base (Fig. 23C). One connects to a branch of the otic nerve that also innervates the sensory line (Fig. 23C, arrow 1). The other (arrow 2) runs mesially, and although it cannot be followed through, it may arise at the base of the superficial ophthalmic nerve. It is therefore likely that lateral line nerves innervated these pits. The pits of Howqualepis also vary in size (Fig. 23E) and in distribution between specimens (Long 1988b). They do not appear to have expanded bases (Fig. 23E), but the nature of the material (latex peels from natural moulds) makes this hard to judge. The distribution of the pits in both Howqualepis and Ligulalepis alongside sensory line canals, the expanded bases of the pits in Ligulalepis and the likely innervation by lateral line nerves suggest that they may house electroreceptors. This was originally suggested for Howqualepis by comparison with the sturgeon Scaphirhynchus (Weisel 1978; Long 1988b). A caveat is that these structures are mainly present on the dorsal skull roof, and are not found on the anterior part of the snout, although this is incomplete ventrally and no lower jaw is known for ‘Ligulalepis’.