The slime canals

"Dear frog and fish, or newt and shark,
you needn’t worry when it’s dark;
you’ll escape or dine just fine,
svenning with your lateral line."
(Platt et al., 1989)

​What is it?
A lateral line system is a sensory system found only in aquatic vertebrates, more specifically to fish and some amphibians in the modern day (animals like whales, sea turtles, and penguins lack this system). This does include the aquatic larvae of amphibians that metamorphose into terrestrial adults, as well as temnospondyls. Particularly in extinct tetrapods, this system goes by many other names, including "sensory grooves," "mucous canals," "lyra(e) / lyre," and my personal favourite, "slime canals." The lateral line system is a fundamentally mechanoreceptor sensory system and should not be confused with electroreceptive ampullary organs, which also occur in many fish, caecilians, and caudates (salamanders + newts). It helps the animal to detect vibrations, movement, and pressure, all of which are important for feeding, predator avoidance, social behaviours, etc. This feature is what allows a fish to detect you, even if you try to sneak up behind it where its range of vision is very limited.

​As a disclaimer, there is a TON of research on lateral lines, both from paleontological and modern biological perspectives. I cover some of the basics mostly to introduce it for temnos, but I hardly claim to be an expert on the topic or to have read even a small minority of the full breadth of literature. 

Stained neuromasts in a threespine stickleback (Gasterosteus aculeatus), distributed on Wikimedia Commons by Abigail Wark under a Attribution 2.5 Generic (CC BY 2.5) license.

Stained neuromasts in the blind Mexican cave fish (Astyanax mexicanus). A, full body photograph; B, close-up of head; C-D, schematic drawings of superficial and canal neuromasts. Figure from Windsor & McHenry (2009).

There are several types of lateral line organs, including superficial neuromasts that are found externally, canal neuromasts that are found within canals, spiracular organs, and vesicles of Savi. Neuromasts are organs made of receptive "hair" cells (these are not actual hairs like in mammals) that are covered by the cupula, a flexible semi-solid (jelly-like to be scientific) substance that can be displaced with the movement of water around it. The "hairs" are organized from tallest to shortest (like a staircase). The cupula will be displaced to a degree that is proportional to the strength of the stimulus (i.e. stronger flow will create more shear), causing the sensory "hairs" to also shear or deflect. This can produce either depolarization and increased neurotransmitter release and signal transduction (shear toward longest hair) or hyperpolarization and decreased release and transduction (shear toward shortest hair). These signals are then sent off to the brain to be interpreted.

Schematic diagram of a generic lateral line system, showing canal neuromasts, distributed on Wikimedia Commons by u/Thomas.haslwanter under a Creative Commons Attribution-Share Alike 3.0 Unported license.

Superficial neuromasts are found at the surface and are broadly equipped to detect a wide range of stimuli externally. The canal neuromasts are open to the external environment through pores and are arranged in a more orderly network that can better detect gradients and directional spread of a stimulus (e.g., pressure). As water moves over the pores, it creates a pressure difference between pores that leads to flow of fluid within the canal that deflects the "hair" cells. Because the current will exert difference pressure on different pores, the animal can detect direction of flow, rather than just the presence of a current. The mechanism seen in neuromasts is similar to the auditory (hearing) and vestibular (balance) systems, which also utilize the movement of mechanosensitive "hairs" to send sensory information to the brain.

Schematic diagram showing the mechanics of superficial and canal neuromasts in a fish. Figure from Windsor & McHenry (2009).

Spiracular organs are associated with the spiracle, a circular opening found in most cartilaginous fish and some primitive bony fish like the coelacanth. Its function is fairly well-constrained to be for mechanoreception. Perhaps the most interesting thing is that the spiracular organ has been homologized with the paratympanic organ (associated with pressure and altitude detection) of the middle ear in amniotes like birds (e.g., von Bartheld & Giannessi, 2011; O'Neill et al., 2012). The vesicles of Savi are found only in a few genera of rays belonging to the Torpediniformes, which are commonly referred to as "electric rays" or "torpedo rays" (e.g., Nickel & Fuchs, 1974; Shibuya et al., 2010). As an aside, the Romans used to use live electric rays for medicinal purposes to try and cure things like headaches by putting the ray on top of someone's head (Winter, 1976)! The vesicles of Savi are concentrated on the underside of the snout and around the margins of the large electric organs that give these fish their name. There seems to be some debate over their function, mostly about whether they are primarily mechanoreceptors similar to other lateral line organs or whether they play an important role in the electric organs' function.

Anyone interested in the deep history of electric fishes' relationship with humans should check out this paper!

The marbled torpedo ray (Torpedo marmorata), distributed on Flickr by Philippe Guillaume under a Attribution 2.0 Generic (CC BY 2.0) license.

The eye (left) and spiracle (right) of the zebra shark (Stegostoma fasciatum). Distributed on Wikimedia Commons by Jean-Lou Justine under a Creative Commons Attribution-Share Alike 3.0 Unported license.

Distribution of the spiracular organ among vertebrates paired with schematic illustrations showing the development of the organ in different species. From O'Neill et al. (2012): Dark blue, inner ear epithelium; green, geniculate ganglion; red, spiracular organ/PTO; pink, pharyngeal endoderm; purple, neural tube.

​The lateral line in temnospondyls

The lateral line occurs in many, but hardly most, temnospondyls. It is formed by typically deep and conspicuous grooves running along the ornamented surfaces of bones, disrupting the various patterns of ornamentation. Whether these are better referred to as 'grooves' or as 'canals' is a semantics argument that I'm not really interested in having; canals architecturally are not enclosed, but often times the term is implied as such in biological systems. 'Sulcus' is another term that's more along the line of 'groove.' Terminology for identifying the canals is typically pretty standard; as in modern vertebrates, the infraorbital canal runs beneath (in tall skulls) or lateral (in flat skulls) to the orbit, while the supraorbital canal runs above or medial to the orbit. The postorbital canal (sometimes called the temporal canal because it occurs on the temporal region [cheek]) extends from the posterolateral corners of the skull up towards the eye, then curves behind it and loops back down toward the back of the skull. 

Reconstruction of the Permian dvinosaur Dvinosaurus by Bystrow (1939), labels added to show the infraorbital (io), postorbital (po), and the supraorbital (so) canals.

Skull of the metoposaurid Koskinonodon on display at the American Museum of Natural History, arrows pointing to the lateral line grooves. Photograph by Bryan Gee.

Generally speaking, the lateral line arrangement is pretty consistent across the skulls temnospondyls and across aquatic early tetrapods. For example, the supraorbital canal cuts across many of the same elements (e.g., pre- and postfrontals, frontals) in many temnospondyls. The arrangement can look quite different between taxa, but this is often because there is a tight correlation between the grooves and the elements that they cut across; in other words, noticeable changes to proportions of elements will lead to correlated changes in the grooves. The infra- and supraorbital grooves are very long in taxa with long snouts, for example. There is some disparity in whether the postorbital groove is a single groove or formed by at least two distinct grooves (usually divided into the temporal [going toward the midline] and the jugal [going toward the edge of the skull] grooves in that case). The curvature of the grooves is also pretty consistent as a result; the term 'lyra / lyre' that was sometimes used to describe the grooves comes from the U-shaped inflection of mainly the supraorbital groove between the nose and the orbit (but the infraorbital groove can also be inflected, and the postorbital groove is a 'U' in its entirety). The name is after the U-shaped instrument of Greek antiquity (not the constellation Lyra, which does derive etymologically from the same origin). There can also be an occipital groove (green below) that is short and mostly transverse (side-to-side) in orientation along the back of the skull. 

An interesting feature that has received little attention to date is the presence or absence of a lateral line groove on the clavicles. This is rarely found among temnospondyls, which probably explains why it is rarely remarked on. In a few metoposaurids, the groove is a relatively simple curvature along the anterolateral margin on the ornamented ventral surface near the centre of ossification, incising through the ornamentation as on the skull (Dutuit, 1976). This should not be confused with a feature typically identified as the clavicular groove (a name that would make a lot of sense for a sensory groove), which is a non-sensory groove more along the anterolateral margin of the clavicle. Because it occurs sporadically and inconsistently within temnospondyl clades, it may represent nothing more than slight variation in the course of the lateral line. The fact that the grooves can develop within the ornamented bone of the skull suggests that it was feasible on the clavicles as well.

The ornamented pectoral girdle of the metoposaurid Dutuitosaurus ouazzoui, figure modified from Dutuit (1976).

The lateral line in lissamphibians
​​
All three groups of lissamphibians, anurans (toads + frogs), caudates (salamanders + newts), and caecilians have lateral line systems with neuromasts, as in other vertebrates (Fritzsch, 1989). Compared to temnospondyls, lissamphibians have shifted toward neuromasts embedded in the epidermis rather than in the bone; when exactly this occurred is unknown. Caudates and caecilians also have ampullary electroreceptors. The developmental relationship of neuromasts and ampullary organs remains poorly resolved in amphibians. There are typically three lines (dorsal, medial, ventral) on the trunk of the body, but there are the usual exceptions (the aquatic salamander Siren has four) and reductions (the tailed frog Ascaphus has two). The presence of four lines in some lungfish suggests that the primitive condition is four lines, with subsequent reductions in tetrapods (possibly due to pedomorphosis in lissamphibians). There are typically four lines on the head, all supplied by the trigeminal nerve (cranial nerve V). These are the supraorbital line (above / medial to the eye), the infraorbital eye (below / lateral to the eye), the jugular / angular / oral line (on the jaw), and the postorbital / gular line (behind the eye). This terminology is not always consistently used, as there is sometimes further division of the lines. The supraorbital and the infraorbital lines are commonly used terms in temnospondyls and are considered homologous to those in fish (and are sometimes used to attempt to infer homologies of skull bones) (e.g., Moodie, 1908). 

Distribution of lateral line organs in an anuran tadpole, figure from Wright (1951).

​During metamorphosis, the lateral line system and the ampullary organs are frequently lost (e.g., Wahnschaffe et al., 1987). However, many salamanders only cover the lateral line system with the epidermis during metamorphosis; this retention is similar to what lungfish do during aestivation to wait out the dry season. There is some evidence to suggest that the retention is also associated with the aquatic breeding habits of many caudates and anurans. Caudates shed their skin when they enter the water to breed, exposing the neuromasts (e.g., Fritzsch & Wahnschaffe, 1983), and many semi-aquatic anurans retain some of the non-tail neuromasts, though to differing degrees that probably reflects their degree of terrestriality (e.g., Fritzsch et al., 1987). Second-order neurons associated with the neuromasts are typically lost, although there is a less common phenomenon where the neuromasts are degraded but the neurons remain.

Refs

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