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Journal ArticleDOI

Neuroethology and life history adaptations of the elasmobranch electric sense.

01 Sep 2002-Journal of Physiology-paris (Elsevier)-Vol. 96, Iss: 5, pp 379-389
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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Citations
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Journal ArticleDOI
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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Journal ArticleDOI
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

Journal ArticleDOI
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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Journal ArticleDOI
20 Jan 2017-PLOS ONE
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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Journal ArticleDOI
TL;DR: Small doses of dihydrotestosterone were implanted in the electric organ to determine whether androgens can alter pulse duration despite a stable pacemaker nucleus firing frequency, and found that androgen implants increased EOD pulse duration, but did not influence EOD frequency.

31 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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Journal ArticleDOI
TL;DR: The sensory epithelium lining the ampulla of Lorenzini in the skate was examined by the freeze-fracture technique and it is suggested that the co-extensive arrays of particles at the tip of the ribbon synapse is an intercellular junction; that the active zone of the synapses is at or above the constriction; and that membrane retrieval occurs in the synaptic arch region.
Abstract: The sensory epithelium lining the ampulla of Lorenzini in the skate was examined by the freeze-fracture technique. Anastomosing tight junctions (zonula occludens) completely encircle the apex of each receptor cell joining it to neighbouring support cells. The tight junctions separate two distinctly different regions of the receptor-cell surface. The apical P-face has numerous large particles while just below the tight junctions of the lateral surface have many smaller particles. On its basal surface each receptor cell makes several evaginating ribbon synapses with an afferent nerve. Three regions of the synaptic evagination can be distinguished on the basis of membrane specializations: 1. At the tip of the evagination a regular array of large particles is found on the P-face of the receptor cell directly opposite a similar regular array of large particles on the P-face of the afferent nerve; 2. just above the tip at a narrow constriction, below which vesicles are not found, a population of large particles on the P-face of the receptor cell opposes a well-defined strip of large particles that cleaves with the E-face of the nerve fibre; 3. at the arch of the synaptic evagination randomly occurring dimples are found on the P-face and protrusions on the E-face of the receptor cell. The density of these protrusions increased in skates that were electrically stimulated. We suggest that the co-extensive arrays of particles at the tip of the ribbon synapse is an intercellular junction; that the active zone of the synapse is at or above the constriction; and that membrane retrieval occurs in the synaptic arch region.

29 citations

Journal ArticleDOI
TL;DR: Occurrence of ripe ova or egg cases in females and presence of semen in the seminal vesicle of males throughout the year, as well as the lack of seasonal changes in male gonad indices indicate that C. umbratile does not have a well-defined reproductive season.
Abstract: I examined 356 specimens of the Japanese swellshark caught off Choshi, near Tokyo, Japan. The Japanese swellshark Cephaloscyllium umbratile attained maturity at a total length of 861-880mm size class for males and 921-940mm for females. All males over 960mm and females over 1040mm were mature. The largest male (1140mm) was only slightly smaller than the largest female (1145mm). In males, both clasper length and testes weight increased rapidly with the onset of maturity. Occurrence of ripe ova or egg cases in females and presence of semen in the seminal vesicle of males throughout the year, as well as the lack of seasonal changes in male gonad indices indicate that C. umbratile does not have a well-defined reproductive season. Food items of the shark consisted of at least 71 prey species, principally fishes. Pacific mackerel and Japanese sardine were the dominant prey. Ten species of Chondrichthyan fishes were also important in their diet.

27 citations

Journal ArticleDOI
TL;DR: This study measured the strength and nature of the response of the skate electrosensory system to electric organ discharge via electrical stimulation of the medullary command nucleus in two species of skates and found that EODs serve as a communicative signal over moderate distances.
Abstract: Skates possess bilateral electric organs that produce intermittent, weak discharges of relatively long duration compared to the discharges ofother weakly elec tric fish. They, like all elasmobranchs, also have an elec trosensory system capable of detecting weak, low-fre quency electric fields. Several studies have suggested that the discharge is used in some type of social communi cation. This study measured the strength and nature of the response ofthe skate electrosensory system to electric organ discharge. Electric organ discharge (EOD) waselicited via electrical stimulation of the medullary command nucleus in two species ofskates. The temporal structure and power spec tra ofthe EODS demonstrated that they should be effective stimuli for the skate electrosensory system. The responses ofelectrosensory afferent fibers in the anterior lateral line nerve (ALLN) to EODS were variable depending upon the location and orientation ofthe receptor. The responses of most ALLN fibers were very weak compared to the strong reafference produced by the skate's ventilatory ac tivity. Unlike the common-mode ventilatory reafference, EOD reafference was variable in terms of excitation or inhibition, depending upon receptor orientation. Despite the low signal-to-noise ratio observed in ALLN responses to EODS,it is likely that EODSserve as a communicative signal over moderate distances.

19 citations


"Neuroethology and life history adap..." refers background in this paper

  • ...erinacea is also well suited to detect the spectral components of individual EOD pulses [47]....

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Journal ArticleDOI
TL;DR: Sets of electric organ discharges (EODs), which accompany the defensive responses and certain predatory responses, show a stereotyped pattern, characteristic for each EOD motor act.
Abstract: 1. Predation and defence of Torpedo marmorata , elicited with biological and inanimate stimuli, were studied in experimental conditions. 2.Patterns of responses of neonates and adults are described, and chains of separate, coordinated motor acts are defined. 3.Jumping predation, creeping predation, defence of the disc and defence of the tail are distinguished. Each predatory behaviour consists of stimulus reaction chains, whereas defensive types of behaviour involve single stimulus reactions. 4.During jumping behaviour, tail strokes provoked by the initial response in the chain are displayed during the whole period of predation; these ‘delayed’ tail strokes provoke displacements of the prey, thus probing the substrate and furnishing biological cues. 5.Large behavioural variations are reported, including incomplete chains of responses, repetition of responses, oriented responses, stimulus intensity/response magnitude relationships and missing of certain motor acts. 6.Ontogenetic maturation of the behaviour patterns is observed in embryos and in immature neonates. 7.Sets of electric organ discharges (EODs), which accompany the defensive responses and certain predatory responses, show a stereotyped pattern, characteristic for each EOD motor act. Variations found in the EOD pattern are often related to the effects of fatigue on the EOD rate. Electric shock provokes the immobilization of the prey, or the flight of the aggressor. Effective use of the EOD by neonates as a weapon against prey is reported. 8.The possible neuronal basis of the sensorimotor organization which may account for the results is discussed.

18 citations