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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: It is proposed that the production of male androgens across the full seven-month preovulatory mating period promotes their aggressive reproductive behavior and drives the protracted mating season of this species.

108 citations


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

  • ...sabina exhibit a 9month protracted mating season from August through April [36] during which male stingrays exhibit distinct reproductive activities associated with varying serum androgen levels [66]....

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Journal ArticleDOI
27 May 1983-Science
TL;DR: In this paper, it was shown that androgens affect the electric organ of mormyrid electric fishes and not only the electrophoresis, but also the waveform and duration of electric organ discharge.
Abstract: Males and females of some mormyrid electric fishes generate electrical pulses that differ in waveform and duration. For one such species, testosterone or dihydrotestosterone induces females and immature males to produce the mature male electric organ discharge which is two times the duration of the female or immature discharge. Estradiol has only a weak effect. For a second species where males and females have similar electric organ discharges, testosterone produces no effect. The data suggest that androgens affect the electric organ itself.

107 citations

Journal ArticleDOI
TL;DR: It is suggested that life-history-dependent functions such as these may shape the evolution of the low-frequency response properties for the elasmobranch electrosensory system.
Abstract: This study examined the response properties of skate electrosensory primary afferent neurons of pre-hatch embryo (8-11 weeks), post-hatch juvenile (1-8 months), and adult (> 2 year) clearnose skates (Raja eglanteria) to determine whether encoding of electrosensory information changes with age, and if the electrosense is adapted to encode natural bioelectric stimuli across life history stages. During ontogeny, electrosensory primary afferents increase resting discharge rate, spike regularity, and sensitivity at best frequency. Best frequency was at 1-2 Hz for embryos, showed an upwards shift to 5 Hz in juveniles, and a downward shift to 2-3 HZ in adults. Encapsulated embryos exhibit ventilatory movements that are interrupted by a "freeze response" when presented with weak uniform fields at 0.5 and 1 Hz. This phasic electric stimulus contains spectral information found in potentials produced by natural fish predators, and therefore indicates that the embryo electrosense can efficiently mediate predator detection and avoidance. In contrast, reproductively active adult clearnose skates discharge their electric organs at rates near the peak frequency sensitivity of the adult electrosensory system, which; facilitates electric communication during social behavior. We suggest that life-history-dependent functions such as these may shape the evolution of the low-frequency response properties for the elasmobranch electrosensory system.

103 citations


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

  • ...eglanteria) [55], and 1–5 Hz in the little skate (R....

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  • ...This behavior results in the streaming of water from one horn of the egg case at velocities of approximately 7 cm s 1 [55] and creates a localized vortex near the egg which may provide olfactory, electrosensory and mechanosensory cues that facilitate the detection and location of the skate by potential predators....

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  • ...Work on the clearnose skate (Raja eglanteria) shows that the electrosensory system of egg-encapsulated embryonic skates is well suited to detect potential egg predators [55]....

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  • ...Prey detection [28,63] Social communication [13,14,55] Detection of mates [65] Detection of predators [55]...

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Journal ArticleDOI
19 Jun 1961-Copeia

98 citations


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

  • ...Skate electric organs also differ in length among species and may be sexually dimorphic [26,27]....

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Journal ArticleDOI
13 Aug 1982-Science
TL;DR: Findings indicate that the tuning of electroreceptors is dynamic and that it parallels natural shifts in electric organ discharge frequency.
Abstract: Weakly electric fish possess electroreceptors that are tuned to their individual electric organ discharge frequencies. One genus, Sternopygus, displays both ontogenetic and seasonal shifts in these frequencies, possibly because of endocrine influences. Systemic treatment with androgens lowers the discharge frequencies in these animals. Concomitant with these changes in electric organ discharge frequencies are decreases in electroreceptor best frequencies; hence the close match between discharge frequency and receptor tuning is maintained. These findings indicate that the tuning of electroreceptors is dynamic and that it parallels natural shifts in electric organ discharge frequency.

88 citations