Barbara E. Wueringer

Comparison of the lateral line and ampullary systems of two species of shovelnose ray

The anatomical characteristics of the mechanoreceptive lateral line system and electrosensory ampullae of Lorenzini of Rhinobatos typus and Aptychotrema rostrata are compared. The spatial distribution of somatic pores of both sensory systems is quite similar, as lateral line canals are bordered by electrosensory pore fields. Lateral line canals form a sub-epidermal, bilaterally symmetrical net on the dorsal and ventral surfaces; canals contain a nearly continuous row of sensory neuromasts along their length and are either non-pored or pored. Pored canals are connected to the surface through a single terminal pore or additionally possess numerous tubules along their length. On the dorsal surface of R. typus, all canals of the lateral line occur in the same locations as those of A. rostrata. Tubules branching off the lateral line canals of R. typus are ramified, which contrasts with the straight tubules of A. rostrata. The ventral prenasal lateral line canals of R. typus are pored and possess branched tubules in contrast to the non-pored straight canals in A. rostrata. Pores of the ampullae of Lorenzini are restricted to the cephalic region of the disk, extending only slightly onto the pectoral fins in both species. Ampullary canals penetrate subdermally and are detached from the dermis. Ampullae occur clustered together, and can be surrounded by capsules of connective tissue. We divided the somatic pores of the ampullae of Lorenzini of R. typus into 12 pore fields (10 in A. rostrata), corresponding to innervation and cluster formation. The total number of ampullary pores found on the ventral skin surface of R. typus is approximately six times higher (four times higher in A. rostrata) than dorsally. Pores are concentrated around the mouth, in the abdominal area between the gills and along the rostral cartilage. The ampullae of both species of shovelnose ray are multi-alveolate macroampullae, sensu Andres and von Düring (1988). Both the pore patterns and the distribution of the ampullary clusters in R. typus differ from A. rostrata, although a basic pore distribution pattern is conserved.

The function of the sawfish's saw

Summary Jawed fishes that possess an elongated rostrum use it to either sense prey or to manipulate it, but not for both. The billfish rostrum, for instance, lacks any sensory function and is used to stun prey [1], while paddlefishes use their rostrum to detect and orient towards electric fields of plankton [2]. Sturgeons search through the substrate with their electroreceptive rostrum, and engulf prey by oral suction [2]. Here, we show that juvenile freshwater sawfish Pristis microdon are active predators that use their toothed rostrum — the saw — to both sense prey-simulating electric fields and capture prey. Prey encountered in the water column is attacked with lateral swipes of the saw that can stun and/or impale it. We compare sawfish to shovelnose rays, which share a common shovelnose ray-like ancestor [3] and lack a saw.

Sensory systems in sawfishes. 1. The ampullae of Lorenzini

The distribution and density of the ampullary electroreceptors in the skin of elasmobranchs are influenced by the phylogeny and ecology of a species. Sensory maps were created for 4 species of pristid sawfish. Their ampullary pores were separated into pore fields based on their innervation and cluster formation. Ventrally, ampullary pores are located in 6 areas (5 in Pristis microdon), covering the rostrum and head to the gills. Dorsally, pores are located in 4 areas (3 in P. microdon), which cover the rostrum, head and may extend slightly onto the pectoral fins. In all species, the highest number of pores is found on the dorsal and ventral sides of the rostrum. The high densities of pores along the rostrum combined with the low densities around the mouth could indicate that sawfish use their rostrum to stun their prey before ingesting it, but this hypothesis remains to be tested. The directions of ampullary canals on the ventral side of the rostrum are species specific. P. microdon possesses the highest number of ampullary pores, which indicates that amongst the study species this species is an electroreception specialist. As such, juvenile P. microdon inhabit low-visibility freshwater habitats.

Electric field detection in sawfish and shovelnose rays

In the aquatic environment, living organisms emit weak dipole electric fields, which spread in the surrounding water. Elasmobranchs detect these dipole electric fields with their highly sensitive electroreceptors, the ampullae of Lorenzini. Freshwater sawfish, Pristis microdon, and two species of shovelnose rays, Glaucostegus typus and Aptychotrema rostrata were tested for their reactions towards weak artificial electric dipole fields. The comparison of sawfishes and shovelnose rays sheds light on the evolution and function of the elongated rostrum (‘saw’) of sawfish, as both groups evolved from a shovelnose ray-like ancestor. Electric stimuli were presented both on the substrate (to mimic benthic prey) and suspended in the water column (to mimic free-swimming prey). Analysis of around 480 behavioural sequences shows that all three species are highly sensitive towards weak electric dipole fields, and initiate behavioural responses at median field strengths between 5.15 and 79.6 nVcm−1. The response behaviours used by sawfish and shovelnose rays depended on the location of the dipoles. The elongation of the sawfish’s rostrum clearly expanded their electroreceptive search area into the water column and enables them to target free-swimming prey.

Description of the mechanoreceptive lateral line and electroreceptive ampullary systems in the freshwater whipray, Himantura dalyensis

Mechanoreceptive and electroreceptive anatomical specialisations in freshwater elasmobranch fishes are largely unknown. The freshwater whipray, Himantura dalyensis, is one of a few Australian elasmobranch species that occur in low salinity (oligohaline) environments. The distribution and morphology of the mechanoreceptive lateral line and the electroreceptive ampullae of Lorenzini were investigated by dissection and compared with previous studies on related species. The distribution of the pit organs resembles that of a marine ray, Dasyatis sabina, although their orientation differs. The lateral line canals of H. dalyensis are distributed similarly compared with two marine relatives, H. gerrardi and D. sabina. However, convolutions of the ventral canals and proliferations of the infraorbital canal are more extensive in H. dalyensis than H. gerrardi. The intricate nature of the ventral, non-pored canals suggests a mechanotactile function, as previously demonstrated in D. sabina. The ampullary system of H. dalyensis is not typical of an obligate freshwater elasmobranch (i.e. H. signifer), and its morphology and pore distribution resembles those of marine dasyatids. These results suggest that H. dalyensis is euryhaline, with sensory systems adapted similarly to those described in marine and estuarine species.

Sensory systems in sawfishes. 2. The lateral line

The lateral line system allows elasmobranchs to detect hydrodynamic movements in their close surroundings. We examined the distribution of pit organs and lateral line canals in 4 species of sawfish (Anoxypristis cuspidata, Pristis microdon, P. clavata and P. zijsron). Pit organs could only be located in A. cuspidata, which possesses elongated pits that are lined by dermal denticles. In all 4 pristid species, the lateral line canals are well developed and were separated into regions of pored and non-pored canals. In all species the tubules that extend from pored canals form extensive networks. In A. cuspidata, P. microdon and P. clavata, the lateral line canals on both the dorsal and ventral surfaces of the rostrum possess extensively branched and pored tubules. Based on this morphological observation, we hypothesized that these 3 species do not use their rostrum to search in the substrate for prey as previously assumed. Other batoids that possess lateral line canals adapted to perceive stimuli produced by infaunal prey possess non-pored lateral line canals, which also prevent the intrusion of substrate particles. However, this hypothesis remains to be tested behaviourally in pristids. Lateral line canals located between the mouth and the nostrils are non-pored in all 4 species of sawfish. Thus this region is hypothesized to perceive stimuli caused by direct contact with prey before ingestion. Lateral line canals that contain neuromasts are longest in P. microdon, but canals containing neuromasts along the rostrum are longest in A. cuspidata.

Electroreceptive and Mechanoreceptive Anatomical Specialisations in the Epaulette Shark (Hemiscyllium ocellatum)

The arrangement of the electroreceptive ampullary system and closely related mechanoreceptive lateral line canal system was investigated in the epaulette shark, Hemiscyllium ocellatum. The lateral line canals form an elaborate network across the head and are continuously punctuated by pores. Ampullary pores are distributed in eleven distinct pore fields, and associated ampullary bulbs are aggregated in five independent ampullary clusters on either side of the head. Pores are primarily concentrated around the mouth and across the snout of the animal. We provide the anatomical basis for future behavioural studies on electroreception and mechanoreception in epaulette sharks, as well as supporting evidence that the electroreceptive ampullary system is specialised to provide behaviourally relevant stimuli. In addition, we describe ampullary pores distributed as far posteriorly as the dorsal fin and thus reject the assumption that ampullary pores are restricted to the cephalic region in sharks.

Electroreception in Elasmobranchs: Sawfish as a Case Study

The ampullae of Lorenzini are the electroreceptors of elasmobranchs. Ampullary pores located in the elasmobranch skin are each connected to a gel-filled canal that ends in an ampullary bulb, in which the sensory epithelium is located. Each ampulla functions as an independent receptor that measures the potential difference between the ampullary pore opening and the body interior. In the elasmobranch head, the ampullary bulbs of different ampullae are aggregated in 3–6 bilaterally symmetric clusters, which can be surrounded by a connective tissue capsule. Each cluster is innervated by one branch of the anterior lateral line nerve (ALLN). Only the dorsal root of the ALLN carries electrosensory fibers, which terminate in the dorsal octavo-lateral nucleus (DON) of the medulla. Each ampullary cluster projects into a distinctive area in the central zone of the DON, where projection areas are somatotopically arranged. Sharks and rays can possess thousands of ampullae. Amongst other functions, the use of electroreception during prey localization is well documented. The distribution of ampullary pores in the skin of elasmobranchs is influenced by both the phylogeny and ecology of a species. Pores are grouped in distinct pore fields, which remain recognizable amongst related taxa. However, the density of pores within a pore field, which determines the electroreceptive resolution, is influenced by the ecology of a species. Here, I compare the pore counts per pore field between rhinobatids (shovelnose rays) and pristids (sawfish). In both groups, the number of ampullary pores on the ventral side of the rostrum is similar, even though the pristid rostrum can comprise about 20% of the total length. Ampullary pore numbers in pristids are increased on the upper side of the rostrum, which can be related to a feeding strategy that targets free-swimming prey in the water column. Shovelnose rays pin their prey onto the substrate with their disk, while repositioning their mouth for ingestion and thus possess large numbers of pores ventrally around the mouth and in the area between the gills.

Morphometry and microanatomy of the barbels of the common sawshark Pristiophorus cirratus (Pristiophoridae): implications for pristiophorid behaviour

The internal anatomy of the barbels of the common sawshark Pristiophorus cirratus was examined with light microscopy to clarify their sensory role. No sensory structures such as taste buds (chemoreception), ampullae of Lorenzini (electroreception) or free neuromasts (lateral line mechanoreception) could be located in the barbels. The presence of bundles of nerve fibres, however, indicates a tactile function for the barbels. Conveyance of information regarding potentially damaging stimuli (nociception) and temperature (thermoception) cannot be excluded at this stage. It is hypothesized that the barbels are used by P. cirratus to locate prey in both the water column and on the substratum via wake detection and sensing changes in surface texture. The barbels may also be involved in the detection of water currents for rheotaxis. Regression analyses on P. cirratus morphometric data showed that the width of the rostrum at two sections (the barbels and the rostrum tip) does not significantly correlate with total length. The regression analyses also suggested that the barbels of P. cirratus may be lateralised.

First insights into the function of the sawshark rostrum through examination of rostral tooth microwear

Potential roles of the rostrum of sawsharks (Pristiophoridae), including predation and self-defence, were assessed through a variety of inferential methods. Comparison of microwear on the surface of the rostral teeth of sawsharks and sawfishes (Pristidae) show that microwear patterns are alike and suggest that the elongate rostra in these two elasmobranch families are used for a similar purpose (predation). Raman spectroscopy indicates that the rostral teeth of both sawsharks and sawfishes are composed of hydroxyapatite, but differ in their collagen content. Sawfishes possess collagen throughout their rostral teeth whereas collagen is present only in the centre of the rostral teeth of sawsharks, which may relate to differences in ecological use. The ratio of rostrum length to total length in the common sawshark Pristiophorus cirratus was found to be similar to the largetooth sawfish Pristis pristis but not the knifetooth sawfish Anoxypristis cuspidata. Analysis of the stomach contents of P. cirratus indicates that the diet consists of demersal fishes and crustaceans, with shrimp from the family Pandalidae being the most important dietary component. No prey item showed evidence of wounds inflicted by the rostral teeth. In light of the similarities in microwear patterns, rostral tooth chemistry and diet with sawfishes, it is hypothesised that sawsharks use their rostrum in a similar manner for predation (sensing and capturing prey) and possibly for self-defence.