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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01 Jan 1988
TL;DR: For example, the authors found that weakly electric fishes, such as the common catfish, are particularly sensitive to electric fields, but the more primitive fishes are also known for their keen electric sense.
Abstract: Electric fields in natural waters present a wealth of sensory information. Bioelectric fields direct electrosensitive fishes to their prey, environmental fields provide important orientational cues, and the fields induced by the animals’ motion through the earth’s magnetic field offer oceanic species complete compass data. Particularly sensitive to electric fields are the marine sharks, skates, and rays, but the weakly electric fishes, the common catfishes, and several of the more primitive fishes are also known for their keen electric sense.
148 citations
"Neuroethology and life history adap..." refers background in this paper
...field produced by an approaching predator as it moves relative to the embryo [30]....
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...The static portion of the dc field can also provides an adequate stimulus because it will appear to vary at low frequency as the stingray electroreceptor system passes through it (sensu Kalmijn [30])....
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Journal Article•
139 citations
"Neuroethology and life history adap..." refers background in this paper
...The wall of the ampulla is composed of a single-layer sensory epithelium that contains hundreds of sensory receptor and support cells [51,67] with only the apical surface of the receptors exposed to the ampulla chamber (Fig....
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...Tight junctions unite receptor and support cells to form a high resistance separation of apical and basal surfaces of the sensory epithelium [53,67]....
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...The canal lumen and ampullary chamber are filled with a conductive low-resistance mucopolysaccharide to form an electrical core conductor such that the ampullary chamber is isopotential with a charge at the skin pore [18,45,67]....
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TL;DR: The match between primary afferent frequency sensitivity and the ventilatory phasic signals produced by conspecifics indicates that the electrosensory system serves an important biological function in the social behavior of elasmobranchs.
124 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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...Both male and female round stingrays in the wild use the electrosense to detect and locate conspecifics during the mating season [65]....
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...field that is partially modulated by the ventilatory movements of the mouth and gill slits [29,65]....
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...Courtship and mating among many individuals of this species can readily be observed during the winter months (January–March) in the clear shallow waters near Bahia Kino, Mexico [48,65]....
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TL;DR: It is suggested the protracted mating period of the Atlantic stingray serves some currently undetermined function such as induction of steroidogenesis, oocyte growth, or ovulation in females.
Abstract: Temporal patterns of gonad development are determined by environmental cues that regulate hormonal cycles and ultimately affect a population's mating system. Annual periodicity of gonad histology is essentially unknown for the more than 450 species of batoid elasmobranchs. Temporal periodicity in spermatogenic activity and ova production in the Atlantic stingray (Dasyatis sabina) were examined by histology over a consecutive 20 month period. Gonadosomatic index (GSI) shows three distinct phases associated with structural changes at the cellular level. Testes in the inactive phase occur from March through July, have a low GSI, and are represented only by germinal (SI) and early spermatocyst (SII) stages. The enlargement phase begins in mid-August, followed by rapid testicular growth that peaks in October. Testicular recrudescence is characterized by a decline in the proportion of early stage spermatocysts (SI, II) and a sequential maturation of cells to the spermatocyte (SIII), spermatid (SIV), immature sperm (SV), and mature spermatozoa (SVI) stages. The measure of absolute spermatogenic production (ASP) is maximum from about August through January. The diminution phase is characterized by a decrease in male GSI from October through April associated with a reduced tissue biomass and predominance of early spermatogenic stages. The annual succession of peaks in sperm formation indicates continuous spermatogenesis through the fall-winter and shows that peak sperm production lags maximum GSI by approximately 3–4 months. Further, seminal vesicle diameter peaks in February, which also lags maximum GSI by 4 months. Egg growth in females is a periodic process of 5–6 months duration that involves vitellogenesis of 2–4 oocytes. Maximum ova diameter increases after mid-September, peaks in March (x¯ = 10.62 mm), and covaries with the increase in female GSI. Despite the brief period of ovulation and fertilization in March-April, fresh mating scars and sperm in the lower reproductive tract of females confirm a protracted mating period from October through April-May. Thus, mating begins in the population at least 7 months prior to ovulation and fertilization. Current evidence indicates this protracted mating period is not explained by female sperm storage or arrested embryonic development. We suggest the protracted mating period serves some currently undetermined function such as induction of steroidogenesis, oocyte growth, or ovulation in females. © 1996 Wiley-Liss, Inc.
121 citations
"Neuroethology and life history adap..." refers background in this paper
...Populations of D. sabina exhibit a 9- month 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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...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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TL;DR: Food habits of two sympatric species-pairs of skates (Raja erinacea-R. ocellata and R. senta), which occur off the east coast of North America were investigated, found that food preferences of the two species may be correlated to the difference in shape of the mouth and number of tooth rows.
Abstract: Food habits of two sympatric species-pairs of skates (Raja erinacea-R. ocellata and R. radiata-R. senta), which occur off the east coast of North America were investigated. Stomachs from over 1600 specimens of the 4 species were collected during winter, summer, and autumn of 1969 and the winter of 1970. Diets of R. erinacea and R. ocellata consisted largely of amphipods, decapod crustaceans and polychaetes. However, R. ocellata consumed relatively more fishes and polychaetes and less decapods than R. erinacea. These two skates ate many of the same species but in different proportions; R. ocellata tended to feed on infauna and R. erinacea tended to feed on epifauna. Food preferences of the two species may be correlated to the difference in shape of the mouth and number of tooth rows. R. radiata and R. senta both fed heavily on decapod crustaceans and euphausids, but polychaetes were relatively more important to R. radiata and mysids were relatively more important to R. senta. R. radiata had a very diversified diet and fed on both epifauna and infauna. The diet of R. senta was very restricted and consisted almost entirely of epifauna. Diets of the two species-pairs were similar, but isopods and bivalves were more important to the R. erinacea-R. ocellata pair and euphausids and mysids were more important to the R. radiata-R. senta pair. These differences may reflect differences in the benthic communities with which the species-pairs are associated. Amount of overlap in resource utilization of the pairs of skates was compared with that of some other congeneric organisms.
108 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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