Anatomy of the mechanosensory lateral line canal system and electrosensory ampullae of Lorenzini in two species of sawshark (fam. Pristiophoridae)

It has long been assumed that the elongated rostra (the saws) of sawsharks (family: Pristiophoridae) and sawfish (family: Pristidae) serve a similar function. Recent behavioural and anatomical studies have shed light on the dual function of the pristid rostrum in mechanosensory and electrosensory prey detection and prey manipulation. Here, the authors examine the distributions of the mechanosensory lateral line canals and electrosensory ampullae of Lorenzini in the southern sawshark, Pristiophorus nudipinnis and the longnose sawshark, Pristiophorus cirratus. In both species, the receptive fields of the mechano- and electrosensory systems extend the full length of the rostrum indicating that the sawshark rostrum serves a sensory function. Interestingly, despite recent findings suggesting they feed at different trophic levels, minimal interspecific variation between the two species was recorded. Nonetheless, compared to pristids, the pristiophorid rostrum possesses a reduced mechanosensory sampling field but higher electrosensory resolution, which suggests that pristiophorids may not use their rostrums to disable large prey like pristids do.     

Sawfishes stealth revealed using computational fluid dynamics

Detailed computational fluid dynamics simulations for the rostrum of three species of sawfish (Pristidae) revealed that negligible turbulent flow is generated from all rostra during lateral swipe prey manipulation and swimming. These results suggest that sawfishes are effective stealth hunters that may not be detected by their teleost prey's lateral line sensory system during pursuits. Moreover, during lateral swipes, the rostra were found to induce little velocity into the surrounding fluid. Consistent with previous data of sawfish feeding behaviour, these data indicate that the rostrum is therefore unlikely to be used to stir up the bottom to uncover benthic prey. Whilst swimming with the rostrum inclined at a small angle to the horizontal, the coefficient of drag of the rostrum is relatively low and the coefficient of lift is zero.     

Behavioral stochastic resonance: how the noise from a Daphnia swarm enhances individual prey capture by juvenile paddlefish.

Zooplankton emit weak electric fields into the surrounding water that originate from their own muscular activities associated with swimming and feeding. Juvenile paddlefish prey upon single zooplankton by detecting and tracking these weak electric signatures. The passive electric sense in this fish is provided by an elaborate array of electroreceptors, Ampullae of Lorenzini, spread over the surface of an elongated rostrum. We have previously shown that the fish use stochastic resonance to enhance prey capture near the detection threshold of their sensory system. However, stochastic resonance requires an external source of electrical noise in order to function. A swarm of plankton, for example Daphnia, can provide the required noise. We hypothesize that juvenile paddlefish can detect and attack single Daphnia as outliers in the vicinity of the swarm by using noise from the swarm itself. From the power spectral density of the noise plus the weak signal from a single Daphnia, we calculate the signal-to-noise ratio, Fisher information and discriminability at the surface of the paddlefish's rostrum. The results predict a specific attack pattern for the paddlefish that appears to be experimentally testable.     

Behavioral responses of batoid elasmobranchs to prey-simulating electric fields are correlated to peripheral sensory morphology and ecology

Electrosensory pore number, distribution, and sensitivity to prey-simulating electric fields have been described for many shark species. Electrosensory systems in batoids have received much less attention. Pore number and distribution have yet to be correlated to differences in sensitivity. However, pore number, pore distribution and sensitivity have been linked to behavior, diet, and morphology and follow species-specific trends. We report here that cownose rays have a greater number of pores than the yellow stingray, most of which are concentrated on the anterior ventral surface for both species. However, yellow stingrays have a broader arrangement of pores on both their dorsal and ventral surfaces than the cownose rays. Yellow stingrays demonstrated a median behavioral sensitivity to weak electric fields of 22 nV cm⁻¹ and are among the most highly sensitive batoids studied to date. Cownose rays are less sensitive than all other elasmobranch species with a median sensitivity of 107 nV cm⁻¹. As reported in previous studies, a higher pore number did not result in greater sensitivity. Cownose rays are benthopelagic schooling rays and may benefit from reduced sensitivity to bioelectric fields when they are surrounded by the bioelectric fields of conspecifics. Yellow stingrays, on the other hand, are typically solitary and bury in the substrate. A greater number of pores on their dorsal surface might improve detection of predators above them. Also, increased sensitivity and a broader distribution of pores may be beneficial as small prey items move past a buried ray.     

The paddlefish rostrum functions as an electrosensory antenna in plankton feeding

A novel electrosensory function is presented for the large, plankton-feeding, freshwater paddlefish, Polyodon spathula, along with a hypothesis which accounts for the distinctive, elongated rostrum of this unusual fish. Behavioural experiments conducted in the ''dark'' (under infrared illumination), to eliminate vision, show that paddlefish efficiently capture planktonic prey to distances up to 80–90 mm. They make feeding strikes at dipole electrodes in response to weak low-frequency electrical currents. Fish also avoid metal obstacles placed in the water, again in the dark. Electrophysiological experiments confirm that the Lorenzinian ampullae of paddlefish are sensitive to weak, low-frequency electrical signals, and demonstrate unequivocally that they respond to the very small electrical signals generated by their natural zooplankton prey (Daphnia sp.). We propose that the rostrum constitutes the biological equivalent of an electrical antenna, enabling the fish to accurately detect and capture its planktonic food in turbid river environments where vision is severely limited. The electrical sensitivity of paddlefish to metallic substrates may interfere with their migrations through locks and dams.     

Prey handling using whole-body fluid dynamics in batoids

Fluid flow generated by body movements is a foraging tactic that has been exploited by many benthic species. In this study, the kinematics and hydrodynamics of prey handling behavior in little skates, Leucoraja erinacea, and round stingrays, Urobatis halleri, are compared using kinematics and particle image velocimetry. Both species use the body to form a tent to constrain the prey with the pectoral fin edges pressed against the substrate. Stingrays then elevate the head, which increases the volume between the body and the substrate to generate suction, while maintaining pectoral fin contact with the substrate. Meanwhile, the tip of the rostrum is curled upwards to create an opening where fluid is drawn under the body, functionally analogous to suction-feeding fishes. Skates also rotate the rostrum upwards although with the open rostral sides and the smaller fin area weaker fluid flow is generated. However, skates also use a rostral strike behavior in which the rostrum is rapidly rotated downwards pushing fluid towards the substrate to potentially stun or uncover prey. Thus, both species use the anterior portion of the body to direct fluid flow to handle prey albeit in different ways, which may be explained by differences in morphology. Rostral stiffness and pectoral fin insertion onto the rostrum differ between skates and rays and this corresponds to behavioral differences in prey handling resulting in distinct fluid flow patterns. The flexible muscular rostrum and greater fin area of stingrays allow more extensive use of suction to handle prey while the stiff cartilaginous rostrum of skates lacking extensive fin insertion is used as a paddle to strike prey as well as to clear away sand cover.     

The biology of extinct and extant sawfish (Batoidea: Sclerorhynchidae and Pristidae)

Sclerorhynchids (extinct sawfishes, Batoidea), pristids (extant sawfish, Batoidea) and pristiophorids (sawsharks, Squalomorphi) are the three elasmobranch families that possess an elongated rostrum with lateral teeth. Sclerorhynchids are the extinct sawfishes of the Cretaceous period, which reached maximum total lengths of 100 cm. The morphology of their rostral teeth is highly variable. Pristid sawfish occur circumtropically and can reach maximum total lengths of around 700 cm. All pristid species are globally endangered due to their restricted habitat inshore. Pristiophorid sawsharks are small sharks of maximum total lengths below 150 cm, which occur in depths of 70–900 m. Close examination of the morphology of pectoral fin basals and the internal structure of the rostrum reveals that sclerorhynchids and pristids evolved independently from rhinobatids, whereas pristiophorids are squalomorph sharks. The elongation of the rostrum may be an adaptation for feeding, as all marine vertebrate taxa that possess this structure are said to use it in the context of feeding.     

The physical nature of life.

Life evolved from the primeval world of physics. Sensory systems inform animals of the natural environment, enabling them to conduct responsively. The discovery of weak, DC bioelectric fields in the vicinity of aquatic organisms and the role they play in guiding sharks and rays to their prey have led to the recognition of fundamental, hitherto less well known, physical aspects of sensory biology. The inferred cybernetic algorithm of electric-field orientation in sharks and rays is highly effective and extremely robust. In orienting to the weak DC electric fields of ocean currents and to the earth's magnetic field, sharks and rays unwittingly practise the motional-electric principles that Einstein had in mind when he introduced the special theory of relativity. At the sense-organ, receptor-membrane, and ion-channel levels, the elasmobranch ampullae of Lorenzini operate on the basis of graded positive feedback driven by negative conductance, supposedly employing voltage-sensitive ion channels as the active, excitable elements. The electric sense of sharks and rays presents an exquisite implementation of the very biophysical principles that also govern the graded, much richer than all-or-none, integrative brain processes of animal and man.     

Electrosensitive spatial vectors in elasmobranch fishes: implications for source localization

The electrosense of sharks and rays is used to detect weak dipole-like bioelectric fields of prey, mates and predators, and several models propose a use for the detection of streaming ocean currents and swimming-induced fields for geomagnetic orientation. We assessed pore distributions, canal vectors, complementarity and possible evolutionary divergent functions for ampullary clusters in two sharks, the scalloped hammerhead (Sphyrna lewini) and the sandbar shark (Carcharhinus plumbeus), and the brown stingray (Dasyatis lata). Canal projections were determined from measured coordinates of each electrosensory pore and corresponding ampulla relative to the body axis. These species share three ampullary groups: the buccal (BUC), mandibular (MAN) and superficial ophthalmic (SO), which is subdivided into anterior (SOa) and posterior (SOp) in sharks. The stingray also has a hyoid (HYO) cluster. The SOp in both sharks contains the longest (most sensitive) canals with main projections in the posterior-lateral quadrants of the horizontal plane. In contrast, stingray SO canals are few and short with the posterior-lateral projections subsumed by the HYO. There was strong projection coincidence by BUC and SOp canals in the posterior lateral quadrant of the hammerhead shark, and laterally among the stingray BUC and HYO. The shark SOa and stingray SO and BUC contain short canals located anterior to the mouth for detection of prey at close distance. The MAN canals of all species project in anterior or posterior directions behind the mouth and likely coordinate prey capture. Vertical elevation was greatest in the BUC of the sandbar shark, restricted by the hammerhead cephalofoil and extremely limited in the dorsoventrally flattened stingray. These results are consistent with the functional subunit hypothesis that predicts specialized ampullary functions for processing of weak dipole and geomagnetic induced fields, and provides an anatomical basis for future experiments on central processing of different forms of relevant electric stimuli.     

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.     

Prey detection mechanism of elasmobranchs

Elasmobranchs can detect a little amount of electric fields and they have characteristic approach strategies to find an electric dipole source generated by prey or conspecifics. They appear to align the body at a constant angle with the current flow line of the electric field while swimming towards prey. However, it has not been studied how they process the perception of electric fields for the approach behaviour or what kind of neural mechanism is used. We use a model of electrosensory perception with electrodynamics and explore a possible approach mechanism based on the sensory landscape distributed on electroreceptors. This paper presents that elasmobranchs can estimate the direction of the electric field by swaying their head, which will be a basis information for their particular approach behaviour. A velocity profile of voltage gradients and intensity difference among the ampullary clusters can be another cues to detect a prey source.     

Receptive field organization of electrosensory neurons in the paddlefish (Polyodon spathula)

Paddlefish use their electrosense to locate small water fleas (daphnia), their primary prey, in three-dimensional space. High sensitivity and a representation of object location are essential for this task. High sensitivity can be achieved by convergence of information from a large number of receptors and object location is usually represented in the nervous system by topographic maps. However the first electrosensory center in the brain, the dorsal octavolateral nucleus in the hindbrain, is neither topographically organized nor does it show a higher sensitivity than primary afferent fibers. Here, we investigated the response properties of electrosensory neurons in the dorsal octavolateral nucleus (DON), the lateral mesencephalic nucleus (LMN) and the tectum mesencephali (TM). LMN units are characterized by large receptive fields, which suggest a high degree of convergence. TM units have small receptive fields and are topographically arranged, at least in the rostro-caudal axis, the only dimension we could test. Well-defined receptive fields, however, could only be detected in the TM with a moving DC stimulus. The receptive fields of TM units, as determined by slowly scanning the rostrum and head with a 5 Hz stimulus, were very large and frequently two or more receptive fields were present. The receptive fields for LMN units were located in the anterior half of the rostrum whereas TM units had receptive fields predominantly on the head and at the base of the rostrum. A detailed analysis of the prey catching behavior revealed that it consists of two phases that coincide with the location of the receptive fields in LMN and TM, respectively. This suggests that LMN units are responsible for the initial orienting response that occurs when the prey is alongside the anterior first half of the rostrum. TM units, in contrast, had receptive fields at locations where the prey is located when the fish opens its mouth and attempts the final strike.     

A laboratory examination of substrate, water depth, and light use at two water velocity levels by individual juvenile pallid (Scaphirhynchus albus) and shovelnose (Scaphirhynchus platorynchus) sturgeon

We investigated the influence of substrate type, water depth, light, and relative water velocity on microhabitat selection in juvenile pallid (Scaphirhynchus albus) and shovelnose (Scaphirhynchus platorynchus) sturgeon. Individual sturgeon were placed in an 18 927 L elliptical flume, and their location was recorded after a 2‐h period. Data were analyzed using exact chi‐square goodness of fit tests and exact tests of independence. Both sturgeon species used substrate, depth, and light in similar proportions. (all comparisons; P > 0.05). Specifically, pallid and shovelnose sturgeon did not use substrate in proportion to its availability (pallid: P = 0.0026; shovelnose: P = 0.0199). Each species used sand substrate more and gravel substrate less than expected based on availability. Additionally, neither species used woody structure. Both species used deep areas in greater proportion than availability while shallow areas were used less than expected based on availability (pallid; P < 0.0001; shovelnose; P = 0.0335). Pallid and shovelnose sturgeon used very dark areas in greater proportion than expected based on availability; however, very light areas were used in lower proportion than expected (P < 0.0001). Overall, neither species changed their use of habitat in relation to a change in water velocity (pallid, all comparisons P > 0.05; shovelnose, all comparisons P > 0.05). This study is the first investigation of juvenile pallid and shovelnose sturgeon habitat selection in a large‐scale artificial stream system. Field studies of microhabitat selection by juvenile pallid and shovelnose sturgeon should be carried out to substantiate the results of this study, and to identify critical habitat for recovery and management of sturgeon species. Due to the extensive range, longevity, and migratory behavior of these fishes, proper management likely requires river improvements that provide sturgeon with access to a broad range of habitat conditions over time, including system‐wide habitat diversity; natural variation in flow, velocity, temperature, and turbidity; high water quality; a broad prey base; free‐flowing river sections which provide suitable spawning and rearing sites, as well as protection from recreational and commercial harvesting.     

Response of juvenile scalloped hammerhead sharks to electric stimuli

Sharks can use their electrosensory system to detect electric fields in their environment. Measurements of their electrosensitivity are often derived by calculating the voltage gradient from a model of the charge distribution for an ideal dipole. This study measures the charge distribution around a dipole in seawater and confirms the close correspondence with the model. From this, it is possible to predict how the sharks will respond to dipolar electric fields comprised of differing parameters. We tested these predictions by exposing sharks to different sized dipoles and levels of applied current that simulated the bioelectric fields of their natural prey items. The sharks initiated responses from a significantly greater distance with larger dipole sizes and also from a significantly greater distance with increasing levels of electric current. This study is the first to provide empirical evidence supporting a popular theoretical model and test predictions about how sharks will respond to a variety of different electric stimuli.     

Feeding currents facilitate a mixotrophic way of life

Mixotrophy is common, if not dominant, among eukaryotic flagellates, and these organisms have to both acquire inorganic nutrients and capture particulate food. Diffusion limitation favors small cell size for nutrient acquisition, whereas large cell size facilitates prey interception because of viscosity, and hence intermediately sized mixotrophic dinoflagellates are simultaneously constrained by diffusion and viscosity. Advection may help relax both constraints. We use high-speed video microscopy to describe prey interception and capture, and micro particle image velocimetry (micro-PIV) to quantify the flow fields produced by free-swimming dinoflagellates. We provide the first complete flow fields of free-swimming interception feeders, and demonstrate the use of feeding currents. These are directed toward the prey capture area, the position varying between the seven dinoflagellate species studied, and we argue that this efficiently allows the grazer to approach small-sized prey despite viscosity. Measured flow fields predict the magnitude of observed clearance rates. The fluid deformation created by swimming dinoflagellates may be detected by evasive prey, but the magnitude of flow deformation in the feeding current varies widely between species and depends on the position of the transverse flagellum. We also use the near-cell flow fields to calculate nutrient transport to swimming cells and find that feeding currents may enhance nutrient uptake by ≈75% compared with that by diffusion alone. We argue that all phagotrophic microorganisms must have developed adaptations to counter viscosity in order to allow prey interception, and conclude that the flow fields created by the beating flagella in dinoflagellates are key to the success of these mixotrophic organisms.     

Using cone beam CT scans to reveal headfirst ingestion and possible prey manipulation tactics in sawsharks

Prey manipulation through headfirst ingestion is a common foraging tactic in predatory taxa. Sawsharks possess a toothed rostrum that is thought to assist in prey capture, but the process from prey contact to ingestion is unknown. This study provides evidence of headfirst ingestion and possible prey orientation in situ through the use of cone beam CT scans in the common sawshark (Pristiophorus cirratus). CT scans provide an efficient method for assessing ingestion and proposing plausible behavioural tactics for food manipulation in a species difficult to observe in the wild or maintain in captivity.     

Dichromatism in relation to the trophic biology of predatory cichlid fishes in Lake Tanganyika, East Africa

A population of the piscivorous Tanganyikan cichlid, Lepidiolamprologus profundicola contains individually distinct pale and dark colour morphs: a dichromatism not related to age or sex. The 'dark form' frequently targets prey from the shaded space under rocks, while the 'plae form' targets prey in well-iluminated open water. This hunting site specialization is not ascribable to the differences of microhabitat that the predators of each form encounter. The main function of the dichromatism is apparently cryptic, as a camouflage for hunting. Interspecific comparisons among 19 species of carnivorous Tanganyikan cichlid fishes reveal that dichromatic taxa generally chase an active prey: fishes, scales of fishes or highly mobile free-swimming crustacea. In contrast, cichlid species foraging on a sessile or sluggish prey are monochromatic. This finding strongly supports the hypothesis that a pale-dark dichromatism serves to optimize foraging efficiency in predatory cichlids hunting an active prey.     

Microhabitat Selection by Marine Mesoconsumers in a Thermally Heterogeneous Habitat: Behavioral Thermoregulation or Avoiding Predation Risk?

Habitat selection decisions by consumers has the potential to shape ecosystems. Understanding the factors that influence habitat selection is therefore critical to understanding ecosystem function. This is especially true of mesoconsumers because they provide the link between upper and lower tropic levels. We examined the factors influencing microhabitat selection of marine mesoconsumers – juvenile giant shovelnose rays (Glaucostegus typus), reticulate whiprays (Himantura uarnak), and pink whiprays (H. fai) – in a coastal ecosystem with intact predator and prey populations and marked spatial and temporal thermal heterogeneity. Using a combination of belt transects and data on water temperature, tidal height, prey abundance, predator abundance and ray behavior, we found that giant shovelnose rays and reticulate whiprays were most often found resting in nearshore microhabitats, especially at low tidal heights during the warm season. Microhabitat selection did not match predictions derived from distributions of prey. Although at a course scale, ray distributions appeared to match predictions of behavioral thermoregulation theory, fine-scale examination revealed a mismatch. The selection of the shallow nearshore microhabitat at low tidal heights during periods of high predator abundance (warm season) suggests that this microhabitat may serve as a refuge, although it may come with metabolic costs due to higher temperatures. The results of this study highlight the importance of predators in the habitat selection decisions of mesoconsumers and that within thermal gradients, factors, such as predation risk, must be considered in addition to behavioral thermoregulation to explain habitat selection decisions. Furthermore, increasing water temperatures predicted by climate change may result in complex trade-offs that might have important implications for ecosystem dynamics.     

The rostral micro-tooth morphology of blue marlin,Makaira nigricans

Billfish rostra potentially have several functions; however, their role in feeding is unequivocal in some species. Recent work linked morphological variation in rostral micro-teeth to differences in feeding behavior in two billfish species, the striped marlin (Kajikia audax) and the sailfish (Istiophorus platypterus). Here, we present the rostral micro-tooth morphology for a third billfish species, the blue marlin (Makaira nigricans), for which the use of the rostrum in feeding behavior is still undocumented from systematic observations in the wild. We measured the micro-teeth on rostrum tips of blue marlin, striped marlin, and sailfish using a micro–computed tomography approach and compared the tooth morphology among the three species. This was done after an analysis of video-recorded hunting behavior of striped marlin and sailfish revealed that both species strike prey predominantly with the first third of the rostrum, which provided the justification to focus our analysis on the rostrum tips. In blue marlin, intact micro-teeth were longer compared to striped marlin but not to sailfish. Blue marlin had a higher fraction of broken teeth than both striped marlin and sailfish, and broken teeth were distributed more evenly on the rostrum. Micro-tooth regrowth was equally low in both marlin species but higher in sailfish. Based on the differences and similarities in the micro-tooth morphology between the billfish species, we discuss potential feeding-related rostrum use in blue marlin. We put forward the hypothesis that blue marlin might use their rostra in high-speed dashes as observed in striped marlin, rather than in the high-precision rostral strikes described for sailfish, possibly focusing on larger prey organisms.     

Response properties of electrosensory neurons in the lateral mesencephalic nucleus of the paddlefish

Many fishes and amphibians are able to sense weak electric fields from prey animals or other sources. The response properties of primary afferent fibers innervating the electroreceptors and information processing at the level of the hindbrain is well investigated in a number of taxa. However, there are only a few studies in higher brain areas. We recorded from electrosensory neurons in the lateral mesencephalic nucleus (LMN) and from neurons in the dorsal octavolateral nucleus (DON) of the paddlefish. We stimulated with sine wave stimuli of different amplitudes and frequencies and with moving DC stimuli. During sinusoidal stimulation, DON units increased their firing rate during the negative cycle of the sine wave and decreased their firing rate to the positive cycle. Lateral mesencephalic nucleus units increased their rate for both half cycles of the sine wave. Lateral mesencephalic nucleus units are more sensitive than DON units, especially to small moving dipoles. Dorsal octavolateral nucleus units respond to a moving DC dipole with an increase followed by a decrease in spike rate or vice versa, depending on movement direction and dipole orientation. Lateral mesencephalic nucleus units, in contrast, increased their discharge rate for all stimuli. Any change in discharge rate of DON units is converted in the LMN to a discharge rate increase. Lateral mesencephalic nucleus units therefore appear to code the presence of a stimulus regardless of orientation and motion direction.