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
References
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TL;DR: Attacks by rays on energized electrodes provide the first evidence that electric rays use electroreceptors to detect their prey, however, the lack of clear differences among the four prey treatments in five characteristics of the initial pulse train suggests that a suite of sensory stimuli cooperate in triggering an attack and regulating the electrical output during the attack.
Abstract: The predatory behavior of 74 Pacific electric rays (Torpedo californica), studied between August and December during 1988 through 1991 in situ off the Palos Verdes Peninsula, southern California, consisted of two feeding modes: an ambush from the substratum during the day and a more vigorous attack from the water column at night. Predatory motor patterns and electric organ discharges (EODs) were recorded on the video and audio channels of a housed camcorder. Predatory motor patterns included four phases: (1) jump (simultaneous with EOD initiation), (2) pectoral-fin cupping, (3) orientation to prey, and (4) ingestion. The initial electrical activity of the rays was a train of 46 to 414 5-ms monophasic EODs that lasted 0.45 to 7.06 s; the maximum number of EODs produced during an attack was >1200. Maximum output, measured on only one ray, was 45 V. Fifty-five rays were presented one of four types of prey stimuli: live fish (LF), freshly-speared fish (FSF), frozen fish (FF), or a simulated bioelectric field (SBF). The percent frequency of attacks for the LF, FSF, and FF treatments ranged from 70 to >90%, but was <30% for the SBF. The interval between prey presentation and attack was ≃30 s for the LF, FSF, and FF and over five times longer for the SBF; intervals averaged <4 s for the three rays tested at night. Attacks by rays on energized electrodes provide the first evidence that electric rays use electroreceptors to detect their prey. However, the lack of clear differences among the four prey treatments in five characteristics of the initial pulse train suggests that a suite of sensory stimuli cooperate in triggering an attack and regulating the electrical output during the attack.
46 citations
TL;DR: Frequency characteristics of the electroreceptive system in Scyliorhinus canicula were determined both by electrophysiological recording of the primary afferent responses and by optical recording of respiratory reflexes after electrical stimulation, concluding that the low pass filter properties are not imposed by the time constant of the ampulla wall.
Abstract: 1. Frequency characteristics of the electroreceptive system in Scyliorhinus canicula were determined both by electrophysiological recording of the primary afferent responses and by optical recording of respiratory reflexes after electrical stimulation. 2. The frequency response of the primary afferents shows a maximum gain at about 5 Hz, with slopes of +2.3 and −3.4 dB octave −1 at the low and high frequency side respectively. The phase changes from +60° at 0.03 Hz to −120° at 15 Hz. 3. The sensitivity curve determined by recording the respiratory reflex has a plateau from 0.1 to 1 Hz, with slopes of +2.8 and -;11.4dB octave −1 . The highest sensitivity for sinusoidal electrical stimuli was 40nV cm −1 peak-to-peak, in the frequency range 0.1 to 1 Hz. 4. We suggest that the difference between the two curves reflects the convergence of primary afferents on to secondary neurones. 5. We conclude that the low pass filter properties are not imposed by the time constant of the ampulla wall. 6. The low frequency slope found in the behavioural curve presumably represents the slope of the receptor-cell-synapse complex. 7. The Lorenzinian ampullae apparently act as peripheral filters with different tuning curves; these must play a part in frequency discrimination.
46 citations
"Neuroethology and life history adap..." refers background in this paper
...1–1 Hz are also known to interrupt the respiratory movements of newly post-hatched dogfish, Scyliorhinus canicula, [49] and may reflect the perceived low frequency modulation of a d....
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01 Jul 1990-Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology
TL;DR: Responses of ALLN fibers and DON neurons to weak sinusoidal stimuli demonstrated very similar frequency response characteristics for all cell types, with peak sensitivity of electrosensory neurons between 5–10 Hz.
Abstract: 1.
Previous studies have demonstrated that the resting activity of electrosensory ALLN fibers is modulated by the animal's own respiratory activity and that all fibers innervating a single ampullary cluster are modulated with the same amplitude and phase relationship to ventilation. We demonstrate that ALLN fibers in the skate are modulated in this common-mode manner bilaterally, regardless of receptor group, orientation, or position of the receptor pore on the body surface (Fig. 2).
2.
Ascending efferent neurons (AENs), which project to the electrosensory midbrain from the DON, are modulated through a much smaller portion of their dynamic range. AENs give larger responses to an extrinsic local electric field than to the respiratory driving, indicating that a mechanism exists for suppressing ventilatory electrosensory reafference.
3.
In paralyzed animals no modulation of resting activity or of responses of extrinsic electric fields could be observed with respect to the animal's respiratory motor commands in the absence of electrosensory reafference.
4.
Cells of the dorsal granular ridge (DGR) project to medullary AENs via the DON molecular layer. A majority of proprioceptive DGR neurons are modulated by ventilatory activity, however, in a given fish the modulation is not in the same phase relationship to ventilation among DGR units.
5.
The modulation of AENs during respiration was increased following transection of the contralateral ALLN (Fig. 9). Resting activity and responses to excitatory stimuli were inhibited by simultaneous stimulation of the transected contralateral ALLN indicating that a common-mode rejection mechanism is mediated via the commissural interconnections of the DONs.
41 citations
"Neuroethology and life history adap..." refers background in this paper
...Similarly, the peak frequency sensitivity (5–7 Hz) of electrosensory primary afferents in the adult little skate (Raja erinacea) [46] is also aligned with the EOD pulse rate (about 5 Hz) produced during interactions with conspecifics [13]....
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01 Oct 1986-Journal of Comparative Physiology A-neuroethology Sensory Neural and Behavioral Physiology
TL;DR: It is shown, using biochemical techniques, that the steroid-sensitivity of the myogenic electric organ correlates with the presence of comparatively high levels of androgen-binding activity in the cytosol of electrocytes, which suggests that the electric organ has evolved a sensitivity to gonadal steroid hormones that may underlie the development of known sex differences in the EOD waveform.
Abstract: The mormyrid fish of Africa produce a weak electric pulse called an Electric Organ Discharge (EOD) that functions in electrical guidance and communication. TheEOD waveform describes the appearance of a single pulse which is produced by the electric organ's excitable cells, the electrocytes. For some species, there is a sex difference in the appearance and duration of the EOD waveform, which is under the control of gonadal steroid hormones. We now show, using biochemical techniques, that the steroid-sensitivity of the myogenic electric organ correlates with the presence of comparatively high levels of androgen-binding activity in the cytosol of electrocytes. TheEOD rhythm describes the rate at which the electric organ fires and is under the control of a central electromotor pathway. Sex differences have also been described for the EOD rhythm. Using steroid autoradiographic techniques, we found uptake of tritium-labelled dihydrotestosterone (3H-DHT) by cells within the reticular formation that lie adjacent to the medullary ‘relay nucleus’ which innervates the spinal electromotoneurons that excite the electric organ. However, no DHT-binding was observed in the relay or electromotor nuclei. Steroid-concentrating cells were also found in several other brainstem regions, the hypothalamus, and the thalamus. In particular, a group of DHT-concentrating, motoneuron-like cells were observed in the caudal medulla and were identified as aswimbladder orsonic motor nucleus. The biochemical data suggest that the electric organ has evolved a sensitivity to gonadal steroid hormones that may underlie the development of known sex differences in the EOD waveform. The autoradiographic results suggest that if steroids do affect the development of sex differences in the EOD rhythm, it is at some level removed from known spinal and medullary electromotor nuclei.
37 citations
"Neuroethology and life history adap..." refers background in this paper
...Recent evidence indicates that the steroid-induced changes in the electromotor system are mediated by steroid receptors within the electrocytes [7,19,20,25]....
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TL;DR: Analysis of sevengill shark stomachs from four different regions off southern Africa reveal that chondrichthyan, teleost and marine mammal species were the major prey categories and lead to the conclusion that theSevengill is an apex predator in that nearshore marine ecosystem.
Abstract: The sevengill shark Notorynchus cepedianus is a large, common species of most coastal temperate waters that has often been overlooked as an important marine predator It is a eurytrophic predator that optimizes the available resources Analysis of sevengill shark stomachs from four different regions off southern Africa reveal that chondrichthyan, teleost and marine mammal species were the major prey categories and lead to the conclusion that the sevengill is an apex predator in that nearshore marine ecosystem Other than the great white shark, the sevengill shark has no trophic equivalents in those areas where it occurs, particularly among carcharhinoids
37 citations
"Neuroethology and life history adap..." refers background in this paper
...Embryos of egg-laying elasmobranchs spend their embryonic life in an oviposited egg case on or near the benthic substrate where they are vulnerable to egg predators, which include other elasmobranchs (sharks, rays and skates), teleost fishes, marine mammals and molluscan gastropods [17,21,37,58,59,62]....
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