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.     

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.     

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.     

Perception of local DC and AC electric fields in humans

The goal of this study was to address some of the factors that contribute to the human ability to detect the presence of weak electric fields generated by direct current (DC) and alternating current (AC) sources. An exposure chamber allowed us to expose a limited surface of the body (forearm and hand) to DC fields of up to 65 kV/m and AC fields up to a maximum of 35 kV/m (frequency 60 Hz). Perception was examined using a staircase procedure and a rating procedure derived from signal detection theory. Sixteen subjects participated in the experiments, and none detected the local DC fields. In contrast, 9/16 subjects were sensitive to local AC electric fields, although detection thresholds (index of sensitivity, d' = 1.0) were widely variable between subjects. When regional exposure was limited to the dorsal forearm, performance was similar to that seen when the forearm and hand were exposed. In contrast, subjects did not reliably detect the AC electric fields when exposure was limited to the hand (either hairy or glabrous skin), although a minority of subjects (3/9) showed some evidence of detecting fields presented to the glabrous palm. Subjects were unable to detect AC electric fields when the hair was removed from the forearm and hand, suggesting that the evoked sensation is mainly dependent on movement of hair located in the exposed region.     

Electrotropism of Maize (Zea mays L.) Roots (Facts and Artifacts)

Intact and decapped primary roots of maize (Zea mays L.) were exposed to DC electric fields of 0.5 to 8.0 V/cm in low-salinity media to resolve conflicting results about the direction of electrotropism. In DC fields of 0.5 V/cm or 1.0 V/cm, intact roots always curved toward the cathode. In a field of 8.0 V/cm, intact roots curved toward the anode and stopped growth. Decapped roots also curved toward the anode both in weak and strong fields. The results indicate that growth toward the cathode is the true response of healthy roots.     

Neuroethology and life history adaptations of the elasmobranch electric sense.

The electric sense of elasmobranch fishes (sharks and rays) is an important sensory modality known to mediate the detection of bioelectric stimuli. Although the best known function for the use of the elasmobranch electric sense is prey detection, relatively few studies have investigated other possible biological functions. Here, we review recent studies that demonstrate the elasmobranch electrosensory system functions in a wide number of behavioral contexts including social, reproductive and anti-predator behaviors. Recent work on non-electrogenic stingrays demonstrates that the electric sense is used during reproduction and courtship for conspecific detection and localization. Electrogenic skates may use their electrosensory encoding capabilities and electric organ discharges for communication during social and reproductive interactions. The electric sense may also be used to detect and avoid predators during early life history stages in many elasmobranch species. Embryonic clearnose skates demonstrate a ventilatory freeze response when a weak low-frequency electric field is imposed upon the egg capsule. Peak frequency sensitivity of the peripheral electrosensory system in embryonic skates matches the low frequencies of phasic electric stimuli produced by natural fish egg-predators. Neurophysiology experiments reveal that electrosensory tuning changes across the life history of a species and also seasonally due to steroid hormone changes during the reproductive season. We argue that the ontogenetic and seasonal variation in electrosensory tuning represent an adaptive electrosensory plasticity that may be common to many elasmobranchs to enhance an individual's fitness throughout its life history.     

Influence of a weak DC electric field on root meristem architecture

BACKGROUND AND AIMS: Electric fields are an important environmental factor that can influence the development of plants organs. Such a field can either inhibit or stimulate root growth, and may also affect the direction of growth. Many developmental processes directly or indirectly depend upon the activity of the root apical meristem (RAM). The aim of this work was to examine the effects of a weak electric field on the organization of the RAM. METHODS: Roots of Zea mays seedlings, grown in liquid medium, were exposed to DC electric fields of different strengths from 0.5 to 1.5 V cm(-1), with a frequency of 50 Hz, for 3 h. The roots were sampled for anatomical observation immediately after the treatment, and after 24 and 48 h of further undisturbed growth. KEY RESULTS: DC fields of 1 and 1.5 V cm(-1) resulted in noticeable changes in the cellular pattern of the RAM. The electric field activated the quiescent centre (QC): the cells of the QC penetrated the root cap junction, disturbing the organization of the closed meristem and changing it temporarily into the open type. CONCLUSIONS: Even a weak electric field disturbs the pattern of cell divisions in plant root meristem. This in turn changes the global organization of the RAM. A field of slightly higher strength also damages root cap initials, terminating their division.     

Incorporating movement in the modelling of shark and ray population dynamics: approaches and management implications

The explicit incorporation of movement in the modelling of population dynamics can allow improved management of highly mobile species. Large-scale movements are increasingly being reported for sharks and rays. Hence, in this review we summarise the current understanding of long-scale movement patterns of sharks and rays and then present the different methods used in fisheries science for modelling population movement with an emphasis on sharks and rays. The use of movement data for informing population modelling and deriving management advice remains rare for sharks and rays. In the few cases where population movement was modelled explicitly, movement information has been solely derived from conventional tagging. Though shark and ray movement has been increasingly studied through a range of approaches these different sources of information have not been used in population models. Integrating these multiple sources of movement information could advance our understanding of shark and ray dynamics. This, in turn, would allow the use of more adequate models for assessing stocks and advising management and conservation effort.     

An integrated risk assessment for climate change: analysing the vulnerability of sharks and rays on Australia's Great Barrier Reef

An Integrated Risk Assessment for Climate Change (IRACC) is developed and applied to assess the vulnerability of sharks and rays on Australia's Great Barrier Reef (GBR) to climate change. The IRACC merges a traditional climate change vulnerability framework with approaches from fisheries ecological risk assessments. This semi‐quantitative assessment accommodates uncertainty and can be applied at different spatial and temporal scales to identify exposure factors, at‐risk species and their key biological and ecological attributes, critical habitats a`nd ecological processes, and major knowledge gaps. Consequently, the IRACC can provide a foundation upon which to develop climate change response strategies. Here, we describe the assessment process, demonstrate its application to GBR shark and ray species, and explore the issues affecting their vulnerability to climate change. The assessment indicates that for the GBR, freshwater/estuarine and reef associated sharks and rays are most vulnerable to climate change, and that vulnerability is driven by case‐specific interactions of multiple factors and species attributes. Changes in temperature, freshwater input and ocean circulation will have the most widespread effects on these species. Although relatively few GBR sharks and rays were assessed as highly vulnerable, their vulnerability increases when synergies with other factors are considered. This is especially true for freshwater/estuarine and coastal/inshore sharks and rays. Reducing the impacts of climate change on the GBR's sharks and rays requires a range of approaches including mitigating climate change and addressing habitat degradation and sustainability issues. Species‐specific conservation actions may be required for higher risk species (e.g. the freshwater whipray, porcupine ray, speartooth shark and sawfishes) including reducing mortality, preserving coastal catchments and estuarine habitats, and addressing fisheries sustainability. The assessment identified many knowledge gaps concerning GBR habitats and processes, and highlights the need for improved understanding of the biology and ecology of the sharks and rays of the GBR.     

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 phylogenetic placement of Chondrichthyes: inferences from analysis of multiple genes and implications for comparative studies

Elasmobranch fishes (sharks and rays) have proven valuable for inferring general and specific properties of molecular evolution through comparative studies with crown group vertebrates because they are the most ancient group of gnathostomes. Recent studies have questioned the conventional phylogenetic placement of sharks in the vertebrate tree, however. In this paper I review the importance of the basal position of Chondrichthyes for comparative biology and compile evidence from multiple, independent genes to evaluate the phylogenetic placement of sharks. The results suggests that alternative phylogenetic hypotheses of the relationships among the Chondrichthyes, Actinopterygii and Sarcopterygii can not be refuted with available data, implying that the assumption of the basal placement of sharks in the vertebrate tree is suspect. Resolving the phylogeny of basal vertebrates is important for testing hypotheses about the evolution of vertebrates, and the current lack of a robust phylogeny limits evolutionary inferences that can be gained from comparative studies that include sharks and rays.     

Phyletic Relationships of Living Sharks and Rays

A set of hypotheses are developed for the origin of living sharksand rays and the interrelationships of their major groups, usingsome methods of cladistic analysis to relate groups with sharedderived characters. Comparative studies on living sharks andrays combined with new data on fossil sharks suggests that theliving groups ultimately stem from a common ancestral groupof "neoselachian" sharks with many modern characters. Reinterpretationsof "amphistyly" in modern sharks is presented on new data.     

Electroreception in marine fishes: chondrichthyans

Electroreception in marine fishes occurs across a variety of taxa and is best understood in the chondrichthyans (sharks, skates, rays, and chimaeras). Here, we present an up-to-date review of what is known about the biology of passive electroreception and we consider how electroreceptive fishes might respond to electric and magnetic stimuli in a changing marine environment. We briefly describe the history and discovery of electroreception in marine Chondrichthyes, the current understanding of the passive mode, the morphological adaptations of receptors across phylogeny and habitat, the physiological function of the peripheral and central nervous system components, and the behaviours mediated by electroreception. Additionally, whole genome sequencing, genetic screening and molecular studies promise to yield new insights into the evolution, distribution, and function of electroreceptors across different environments. This review complements that of electroreception in freshwater fishes in this special issue, which provides a comprehensive state of knowledge regarding the evolution of electroreception. We conclude that despite our improved understanding of passive electroreception, several outstanding gaps remain which limits our full comprehension of this sensory modality. Of particular concern is how electroreceptive fishes will respond and adapt to a marine environment that is being increasingly altered by anthropogenic electric and magnetic fields.     

Edgeworth's legacy of cranial muscle development with an analysis of muscles in the ventral gill arch region of batoid fishes (Chondrichthyes: Batoidea).

A series of studies by Edgeworth demonstrated that cranial muscles of gnathostome fishes are embryologically of somitic origin, originating from the mandibular, hyoid, branchial, epibranchial, and hypobranchial muscle plates. Recent experimental studies using quail-chick chimeras support Edgeworth's view on the developmental origin of cranial muscles. One of his findings, the existence of the premyogenic condensation constrictor dorsalis in teleost fishes, has also been confirmed by molecular developmental studies. Therefore, developmental mechanisms for patterning of cranial muscles, as described and implicated by Edgeworth, may serve as structural entities or regulatory phenomena responsible for developmental and evolutionary changes. With Edgeworth's and other studies as background, muscles in the ventral gill arch region of batoid fishes are analyzed and compared with those of other gnathostome fishes. The spiracularis is regarded as homologous at least within batoid fishes, but its status within elasmobranchs remains unclear; developmental modifications of the spiracularis proper are evident in some batoid fishes and in several shark groups. The peculiar ventral extension of the spiracularis in electric rays and some stingrays may represent convergence, probably facilitating ventilation and/or feeding in both groups. The evolutionary origin of the "internus" and "externus" remains uncertain, despite the fact that a variety of forms of the constrictor superficiales ventrales in batoid fishes indicates an actual medio-ventral extension of the "externus." The intermandibularis is probably present only in electric rays. The "X" muscle occurs only in electric rays and is considered to be Edgeworth's intermandibularis profundus. Its association with the adductor mandibular complex in narkinidid and narcinidid electric rays may relate to its functional role in lower jaw movement. Contrary to common belief, in most batoid fishes as well as some sharks, muscles that originate from the branchial muscle plate and extend medially in the ventral gill arches do exist: the medial extension of the interbranchiales in most batoid fishes and some sharks and the "Y" muscle in the pelagic stingrays Myliobatos and Rhinoptera. The latter is another example of the medial extension of the "internus." Whether the interbranchiales and "Y" muscle are homologous within elasmobranchs and whether homologous with the obliques ventrales and/or transversi ventrales of osteichthyan fishes await further research. Four hypobranchial muscles are recognized in batoid fishes: the coracomandibularis, coracohyoideus, coracoarcualis, and coracohyomandibularis. The coracohyoideus is discrete from the coracoarcualis; its complete structural separation from the latter occurs in several groups of batoid fishes.(ABSTRACT TRUNCATED AT 400 WORDS)     

Inter- and intraspecific variation in the distribution and number of pit organs (free neuromasts) of sharks and rays

The distribution of pit organs (free neuromasts) has previously been documented for several species of pelagic sharks, but is relatively poorly known for rays and bottom-dwelling (demersal) sharks. In the present study, the complete distribution of pit organs was mapped in the demersal sharks Heterodontus portusjacksoni, Orectolobus maculatus, Hemiscyllium ocellatum, Chiloscyllium punctatum, and Asymbolus analis, and the rays Rhinobatos typus, Aptychotrema rostrata, Trygonorrhina sp. A, Raja sp. A, and Myliobatis australis. All of these species had pit organs scattered over the dorsolateral surface. The sharks also had "mandibular" pit organs (and "umbilical" pit organs in C. punctatum and A. analis) on the ventral surface, while pit organs were sparse or absent on the ventral surface of rays. All of the species examined here, except for M. australis, also had a "spiracular" group of pit organs adjacent to the eye and/or spiracle. Spiracular pit organs were also recorded for the sawshark Pristiophorus sp. A and the skate Pavoraja nitida, although the remainder of pit organs were not mapped in these species. The distribution and number of pit organs varied both within and among species. Pit organ distribution was asymmetrical in each individual examined, but no particular trend towards left or right "handedness" was observed in any species. Although rays have been thought to have fewer pit organs than sharks in general, this was not the case in the present study. All of the species examined here had few pit organs compared to the pelagic sharks previously documented, but it is not clear whether this is due to ecological or phylogenetic causes.     

Extremely low frequency electromagnetic fields do not interact directly with DNA

Blank and Goodman [(1997): Bioelectromagnetics 18:111–115] suggest that weak extremely low frequency (ELF) electric and magnetic fields affect intracellular DNA directly. We show that such a conclusion is not in accord with physical principles. Bioelectromagnetics 19: 136–137, 1998. © 1998 Wiley-Liss, Inc.     

Sturgeons,sharks, and rays have multifocal crystalline lenses and similar lens suspension apparatuses

Crystalline lenses with multiple focal lengths in monochromatic light (multifocal lenses) are present in many vertebrate groups. These lenses compensate for chromatic aberration and create well‐focused color images. Stabilization of the lens within the eye and the ability to adjust focus are further requirements for vision in high detail. We investigated the occurrence of multifocal lenses by photorefractometry and lens suspension structures by light and electron microscopy in sturgeons (Acipenseriformes, Chondrostei) as well as sharks and rays (Elasmobranchii, Chondrichthyes). Multifocal lenses were found in two more major vertebrate groups, the Chondrostei represented by Acipenseriformes and Chondrichthyes represented by Elasmobranchii. The lens suspension structures of sturgeons, sharks, and rays are more complex than described previously. The lens is suspended by many delicate suspensory fibers in association with a ventral papilla in all groups studied. The arrangements of the suspensory fibers are most similar between sturgeons and sharks. In rays, the lens is suspended by a smaller ventral papilla and the suspensory fibers are arranged more concentrically to the lens. J. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

Lymphocyte electrotaxis in vitro and in vivo

Electric fields are generated in vivo in a variety of physiologic and pathologic settings, including penetrating injury to epithelial barriers. An applied electric field with strength within the physiologic range can induce directional cell migration (i.e., electrotaxis) of epithelial cells, endothelial cells, fibroblasts, and neutrophils suggesting a potential role in cell positioning during wound healing. In the present study, we investigated the ability of lymphocytes to respond to applied direct current (DC) electric fields. Using a modified Transwell assay and a simple microfluidic device, we show that human PBLs migrate toward the cathode in physiologically relevant DC electric fields. Additionally, electrical stimulation activates intracellular kinase signaling pathways shared with chemotactic stimuli. Finally, video microscopic tracing of GFP-tagged immunocytes in the skin of mouse ears reveals that motile cutaneous T cells actively migrate toward the cathode of an applied DC electric field. Lymphocyte positioning within tissues can thus be manipulated by externally applied electric fields, and may be influenced by endogenous electrical potential gradients as well.     

Estimating the potential impacts of large mesopredators on benthic resources: integrative assessment of spotted eagle ray foraging ecology in Bermuda

Declines of large sharks and subsequent release of elasmobranch mesopredators (smaller sharks and rays) may pose problems for marine fisheries management as some mesopredators consume exploitable shellfish species. The spotted eagle ray (Aetobatus narinari) is the most abundant inshore elasmobranch in subtropical Bermuda, but its predatory role remains unexamined despite suspected abundance increases and its hypothesized specialization for mollusks. We utilized a combination of acoustic telemetry, benthic invertebrate sampling, gut content analysis and manipulative experiments to assess the impact of spotted eagle rays on Bermudian shellfish resources. Residency and distribution of adult spotted eagle rays was monitored over two consecutive summers in Harrington Sound (HS), an enclosed inshore lagoon that has historically supported multiple recreational and commercial shellfish species. Telemetered rays exhibited variable fidelity (depending on sex) to HS, though generally selected regions that supported relatively high densities of potential mollusk prey. Gut content analysis from rays collected in HS revealed a diet of mainly bivalves and a few gastropods, with calico clam (Macrocallista maculata) representing the most important prey item. Manipulative field and mesocosm experiments with calico clams suggested that rays selected prey patches based on density, though there was no evidence of rays depleting clam patches to extirpation. Overall, spotted eagle rays had modest impacts on local shellfish populations at current population levels, suggesting a reduced role in transmitting cascading effects from apex predator loss. However, due to the strong degree of coupling between rays and multiple protected mollusks in HS, ecosystem-based management that accounts for ray predation should be adopted.