Neuroethology and life history adaptations of the elasmobranch electric sense.
TL;DR: It is argued 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.
Abstract: 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.
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TL;DR: The role of learning in behaviour is well known for many animal taxa, including teleost fishes, insects, birds and mammals as discussed by the authors, however, its importance to sharks in everyday behavioural processes has rarely been considered.
Abstract: The role of learning in behaviour is well known for many animal taxa, including teleost fishes, insects, birds and mammals. However, its importance to sharks in everyday behavioural processes has rarely been considered. Almost 50 years ago the first learning experiments on sharks were conducted; our first section discusses these studies and places them in a framework of associative and non-associative learning. These experiments showed that sharks were capable of different forms of learning, such as operant and classical conditioning and habituation. Sharks could learn associations as rapidly as other vertebrates and also remember training regimes for several months. However, much of this experimental evidence was based on small sample sizes and few shark orders, such as Carcharhiniformes and Orectobliformes, leaving large gaps in our knowledge of the general learning capabilities of other shark orders. We also examine recent research that has tested for, or inferred learning in behavioural processes. This section reveals that sharks, like teleost fishes use learning to improve prey search and capture to potentially navigate and orientate in their home range and recognize conspecifics, heterospecifics and mates. Learning is also discussed in relation to ecotourism and fisheries. Findings indicated that these activities may lead to conditioning of sharks and that considerable effort should go into investigating what impact this could have on the shark species involved. Finally, we discuss the importance of combining laboratory experiments with field studies, the use of new experimental techniques, the role of model species and research priorities for future work.
93 citations
Additional excerpts
...Male stingrays were shown to use their electrosense to detect and locate buried females, whereas females used their sense to locate other females to refuge with them (Tricas et al. 1995; Sisneros and Tricas 2002)....
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TL;DR: This review has two aims: to synthesise the knowledge of the functional biology and phylogenetic distribution of electroreception and electrogenesis in fishes, with a focus on freshwater taxa and on the proximate bases of EOD and electroreceptor diversity, and to describe the diversity, biogeography, ecology and electric signal diversity of the mormyroids and gymnotiforms.
Abstract: Electroreception, the capacity to detect external underwater electric fields with specialised receptors, is a phylogenetically widespread sensory modality in fishes and amphibians. In passive electroreception, a capacity possessed by c. 16% of fish species, an animal uses low-frequency-tuned ampullary electroreceptors to detect microvolt-range bioelectric fields from prey, without the need to generate its own electric field. In active electroreception (electrolocation), which occurs only in the teleost lineages Mormyroidea and Gymnotiformes, an animal senses its surroundings by generating a weak ( 50 V) EODs that facilitate communication or predation, but not electrolocation. Approximately 1.5% of fish species possess electric organs. This review has two aims. First, to synthesise our knowledge of the functional biology and phylogenetic distribution of electroreception and electrogenesis in fishes, with a focus on freshwater taxa and with emphasis on the proximate (morphological, physiological and genetic) bases of EOD and electroreceptor diversity. Second, to describe the diversity, biogeography, ecology and electric signal diversity of the mormyroids and gymnotiforms and to explore the ultimate (evolutionary) bases of signal and receptor diversity in their convergent electrogenic-electrosensory systems. Four sets of potential drivers or moderators of signal diversity are discussed. First, selective forces of an abiotic (environmental) nature for optimal electrolocation and communication performance of the EOD. Second, selective forces of a biotic nature targeting the communication function of the EOD, including sexual selection, reproductive interference from syntopic heterospecifics and selection from eavesdropping predators. Third, non-adaptive drift and, finally, phylogenetic inertia, which may arise from stabilising selection for optimal signal-receptor matching.
75 citations
TL;DR: Case studies in vocal species where well-delineated sensory and motor pathways underlying reproductive-related behaviors illustrate the diversity and evolution of brain mechanisms driving sexual motivation between (and within) sexes are highlighted.
68 citations
Cites background from "Neuroethology and life history adap..."
...Unreceptive female round stingrays also use electroreception to find each other, as they are found buried in groups for refuge late in themating season (Sisneros and Tricas, 2002; Tricas et al., 1995)....
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TL;DR: Morphological misidentifications were found across most orders, further confirming the need for a comprehensive DNA barcoding library as a valuable tool for the reliable identification of specimens in support of taxonomist who are reviewing current identification keys.
Abstract: Cartilaginous fish are particularly vulnerable to anthropogenic stressors and environmental change because of their K-selected reproductive strategy. Accurate data from scientific surveys and landings are essential to assess conservation status and to develop robust protection and management plans. Currently available data are often incomplete or incorrect as a result of inaccurate species identifications, due to a high level of morphological stasis, especially among closely related taxa. Moreover, several diagnostic characters clearly visible in adult specimens are less evident in juveniles. Here we present results generated by the ELASMOMED Consortium, a regional network aiming to sample and DNA-barcode the Mediterranean Chondrichthyans with the ultimate goal to provide a comprehensive DNA barcode reference library. This library will support and improve the molecular taxonomy of this group and the effectiveness of management and conservation measures. We successfully barcoded 882 individuals belonging to 42 species (17 sharks, 24 batoids and one chimaera), including four endemic and several threatened ones. Morphological misidentifications were found across most orders, further confirming the need for a comprehensive DNA barcoding library as a valuable tool for the reliable identification of specimens in support of taxonomist who are reviewing current identification keys. Despite low intraspecific variation among their barcode sequences and reduced samples size, five species showed preliminary evidence of phylogeographic structure. Overall, the ELASMOMED initiative further emphasizes the key role accurate DNA barcoding libraries play in establishing reliable diagnostic species specific features in otherwise taxonomically problematic groups for biodiversity management and conservation actions.
68 citations
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TL;DR: Direct evidence is presented that the only electrogenically reactive membrane of the cells is on the innervated surface and that this membrane is electrically inexcitable.
Abstract: Single electroplaques of Torpedo nobiliana have been studied with microelectrode recording Direct evidence is presented that the only electrogenically reactive membrane of the cells is on the innervated surface and that this membrane is electrically inexcitable Responses are not evoked by depolarizing currents applied to this membrane, but only by stimulating the innervating nerve fibers The responses arise after a latency of 1 to 3 msec This latency is not affected by large depolarizing or hyperpolarizing changes in membrane potential Various properties that have been theoretically associated with electrically inexcitable responses have been also demonstrated to occur in the electroplaques The neurally evoked response is not propagated actively in the membrane and may have different amplitudes and forms in closely adjacent regions The maximal responses frequently are slightly larger than the recorded resting potential but the apparent small overshoot may be due to difficulty in recording the full resting potential The responses are subject to electrochemical gradation and appear inverted in sign on applying strong outward currents across the innervated membrane This membrane is cholinoceptive and shows marked desensitization The membrane of the uninnervated surface has a very low resistance, a factor that aids maximum output of current during the discharge of the electric organ
81 citations
TL;DR: It is found that inactivation time constants were significantly slower in DHT implanted, but not control, fish, the first observation of functionally relevant individual variation in the kinetic properties of a Na+ current and the first demonstration that the kinetics of aNa+ current may be modulated by an androgen.
Abstract: Electric fish of the genus Sfernopygus produce a sinusoidal electric organ discharge (EOD) of low frequencies in males, high frequencies in females, and overlapping and intermediate frequencies in juveniles. Correspondingly, the cells of the electric organ, the electrocytes, generate action potentials which are of long duration in mature males, short duration in females, and intermediate duration in immatures. The androgen dihydrotestosterone (DHT) lowers EOD frequency and increases electrocyte action potential duration. We examined the electrocytes under voltage clamp to determine whether variations in the kinetic properties of the Na+ current might underlie these phenomena. We found that the fast inactivation time constants of the peak Na+ current (0 mV) ranged from 0.5 to 4.7 msec and varied systematically with EOD frequency and action potential duration. Voltage dependence of steady-state inactivation also varied with EOD frequency with the midpoint of inactivation being more positive in fish with low EOD frequencies. There was no correlation between the voltage at which the Na+ current activates, voltage at peak current, reversal potential, rate of recovery from inactivation, or TTX sensitivity and EOD frequency. We tested whether DHT influenced Na+ current inactivation by recording from electrocytes before and after juvenile fish of both sexes were implanted with a DHT-containing or empty capsule. We found that inactivation time constants were significantly slower in DHT implanted, but not control, fish. This is the first observation of functionally relevant individual variation in the kinetics of a Na+ current and the first demonstration that the kinetics of a Na+ current may be modulated by an androgen.
79 citations
TL;DR: A comparison of the ampullae of Lorenzini among 40 species of skates (Rajoidei) demonstrates a close relationship between inferred electroreceptive capabilities and feeding mechanisms.
Abstract: A comparison of the ampullae of Lorenzini among 40 species of skates (Rajoidei) demonstrates a close relationship between inferred electroreceptive capabilities and feeding mechanisms. Three general lines of morphological modifications are noted. (1) Whereas the majority of ampullary pores are located on the ventral surface of the dorsoventrally flattened body, the relative proportion of ventral pores is significantly lower on species inhabiting aphotic waters. (2) The ventral pores on more piscivorous species are distributed over a larger portion of body surface than they are on those species that feed primarily on invertebrates. Ventral pores in this latter group are more noticeably concentrated around the mouth and their densities on the adult are inversely related to the overall mobility of preferred prey species. (3) The size of each ampulla and the number of alveoli associated with it are directly related to the habitat depth occupied by each species. Shallow-water species have smaller ampullae with fewer alveoli than deeper-dwelling (> 1,000 m) species. The general distribution of ampullary pores on deep dwelling rajoids appears to compensate for reduced visual input, whereas their relative densities are a measure of the system's resolution and reflect major differences in feeding strategies. The increased ampullary size and complexity observed in deep-sea rajoids provides mechanisms to increase both the sensitivity and signal-to-noise ratios.
76 citations
Additional excerpts
...LL=lateral line (modified from Raschi [50])....
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75 citations
"Neuroethology and life history adap..." refers background in this paper
...Prey detection [28,63] Social communication [13,14,55] Detection of mates [65] Detection of predators [55]...
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01 Mar 1983-Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology
TL;DR: Sternopygus dariensis, a weakly electric gymnotiform fish, possesses sexually different electric organ discharges, with females emitting EODs at higher frequencies than males, which can be accounted for by the effects of gonadal steroids.
Abstract: Sternopygus dariensis, a weakly electric gymnotiform fish, possesses sexually different electric organ discharges (EODs), with females emitting EODs at higher frequencies than males. This difference can be accounted for by the effects of gonadal steroids: laboratory experiments indicate that daily injections (0.25 to 20 μg/g body weight) of androgens lower discharge frequencies while injections of estrogens raise discharge frequencies. Clear changes in discharge frequencies can be noted over the course of days, and persist until several days after injections are terminated. These effects are noted irrespective of age or sex, and can be seen in both intact and gonadectomized animals. The discharge frequencies of these animals are established by a neuronal oscillator, the medullary pacemaker nucleus. Thus, the steroid-elicited changes in discharge frequencies are indicative of changes in the activity of the pacemaker nucleus. Steroids may be exerting their effects either through indirect effects upon those neurons which provide input to the pacemaker, or through direct effects upon the spontaneous depolarizations of the pacemaker itself.
75 citations