The functional roles of passive electroreception in non-electric fishes

Passive electroreception is a complex and specialised sense found in a large range of aquatic vertebrates primarily designed for the detection of weak bioelectric fields. Particular attention has traditionally focused on cartilaginous fishes, but a range of teleost and non-teleost fishes from a diversity of habitats have also been examined. As more species are investigated, it has become apparent that the role of electroreception in fishes is not restricted to locating prey, but is utilised in other complex behaviours. This paper presents the various functional roles of passive electroreception in non-electric fishes, by reviewing much of the recent research on the detection of prey in the context of differences in species' habitat (shallow water, deep-sea, freshwater and saltwater). A special case study on the distribution and neural groupings of ampullary organs in the omnihaline bull shark, Carcharhinus leucas, is also presented and reveals that prey-capture, rather than navigation, may be an important determinant of pore distribution. The discrimination between potential predators and conspecifics and the role of bioelectric stimuli in social behaviour is discussed, as is the ability to migrate over short or long distances in order to locate environmentally favourable conditions. The various theories proposed regarding the importance and mediation of geomagnetic orientation by either an electroreceptive and/or a magnetite-based sensory system receives particular attention. The importance of electroreception to many species is emphasised by highlighting what still remains to be investigated, especially with respect to the physical, biochemical and neural properties of the ampullary organs and the signals that give rise to the large range of observed behaviours.

A comparison of the electrosensory morphology of a euryhaline and a marine stingray

The electrosensory system is found in all chondrichthyan fishes and is used for several biological functions, most notably prey detection. Variation in the physical parameters of a habitat type, i.e. water conductivity, may influence the morphology of the electrosensory system. Thus, the electrosensory systems of freshwater rays are considerably different from those of fully marine species; however, little research has so far examined the morphology and distribution of these systems in euryhaline elasmobranchs. The present study investigates and compares the morphology and distribution of electrosensory organs in two sympatric stingray species: the (euryhaline) estuary stingray, Dasyatis fluviorum, and the (marine) blue-spotted maskray, Neotrygon kuhlii. Both species possess a significantly higher number of ventral electrosensory pores than previously assessed elasmobranchs. This correlates with a diet consisting of benthic infaunal and epifaunal prey, where the electrosensory pore distribution patterns are likely to be a function of both ecology and phylogeny. The gross morphology of the electrosensory system in D. fluviorum is more similar to that of other marine elasmobranch species, rather than that of freshwater species. Both D. fluviorum and N. kuhlii possess 'macro-ampullae' with branching canals leading to several alveoli. The size of the pores and the length of the canals in D. fluviorum are smaller than in N. kuhlii, which is likely to be an adaptation to habitats with lower conductivity. This study indicates that the morphology of the electrosensmy system in.a euryhaline elasmobranch species seems very similar to that of their fully marine counterparts. However, some morphological differences are present between these two sympatric species, which are thought to be linked to their habitat type. (C) 2013 Elsevier GmbH. All rights reserved.

The distribution and abundance of electrosensory pores in two benthic sharks: a comparison of the wobbegong shark, Orectolobus maculatus, and the angel shark, Squatina australis

Electroreception is an ancient sense found in many aquatic animals, including sharks, which may be used in the detection of prey, predators and mates. Wobbegong sharks (Orectolobidae) and angel sharks (Squatinidae) represent two distantly related families that have independently evolved a similar dorso-ventrally compressed body form to complement their benthic ambush feeding strategy. Consequently, these groups represent useful models in which to investigate the specific morphological and physiological adaptations that are driven by the adoption of a benthic lifestyle. In this study, we compared the distribution and abundance of electrosensory pores in the spotted wobbegong shark (Orectolobus maculatus) with the Australian angel shark (Squatina australis) to determine whether both species display a similar pattern of clustering of sub-dermal electroreceptors and to further understand the functional importance of electroreception in the feeding behaviour of these benthic sharks. Orectolobus maculatus has a more complex electrosensory system than S. australis, with a higher abundance of pores and an additional cluster of electroreceptors positioned in the snout (the superficial ophthalmic cluster). Interestingly, both species possess a cluster of pores (the hyoid cluster, positioned slightly posterior to the first gill slit) more commonly found in rays, but which may be present in all benthic elasmobranchs to assist in the detection of approaching predators.

A sensory brain map for each behavior?

Multiple brain maps are commonly found in virtually every vertebrate sensory system. Although their functional significance is generally relatively little understood, they seem to specialize in processing distinct sensory parameters. Nevertheless, to yield the stimulus features that ultimately elicit the adaptive behavior, it appears that information streams have to be combined across maps. Results from current lesion experiments in the electrosensory system, however, suggest an alternative possibility. Inactivations of different maps of the first-order electrosensory nucleus in electric fish, the electrosensory lateral line lobe, resulted in markedly different behavioral deficits. The centromedial map is both necessary and sufficient for a particular electrolocation behavior, the jamming avoidance response, whereas it does not affect the communicative response to external electric signals. Conversely, the lateral map does not affect the jamming avoidance response but is necessary and sufficient to evoke communication behavior. Because the premotor pathways controlling the two behaviors in these fish appear to be separated as well, this system illustrates that sensory–motor control of different behaviors can occur in strictly segregated channels from the sensory input of the brain all through to its motor output. This might reflect an early evolutionary stage where multiplication of brain maps can satisfy the demand on processing a wider range of sensory signals ensuing from an enlarged behavioral repertoire, and bridging across maps is not yet required.

Spatio-temporal filtering properties of a dendritic cable with active spines: a modeling study in the spike-diffuse-spike framework

The spike-diffuse-spike (SDS) model describes a passive dendritic tree with active dendritic spines. Spine-head dynamics is modeled with a simple integrate-and-fire process, whilst communication between spines is mediated by the cable equation. In this paper we develop a computational framework that allows the study of multiple spiking events in a network of such spines embedded on a simple one-dimensional cable. In the first instance this system is shown to support saltatory waves with the same qualitative features as those observed in a model with Hodgkin-Huxley kinetics in the spine-head. Moreover, there is excellent agreement with the analytically calculated speed for a solitary saltatory pulse. Upon driving the system with time varying external input we find that the distribution of spines can play a crucial role in determining spatio-temporal filtering properties. In particular, the SDS model in response to periodic pulse train shows a positive correlation between spine density and low-pass temporal filtering that is consistent with the experimental results of Rose and Fortune [1999, Mechanisms for generating temporal filters in the electrosensory system. The Journal of Experimental Biology 202, 1281-1289]. Further, we demonstrate the robustness of observed wave properties to natural sources of noise that arise both in the cable and the spine-head, and highlight the possibility of purely noise induced waves and coherent oscillations.

Urea based osmoregulation and endocrine control in elasmobranch fish with special reference to euryhalinity

Since the landmark contributions of Homer Smith and co-workers in the 1930s there has been a considerable advance in our knowledge regarding the osmoregulatory strategy of elasmobranch fish. Smith recognised that urea was retained in the body fluids as part of the 'osmoregulatory ballast' of elasmobranch fish so that body fluid osmolality is raised to a level that is iso- or slightly hyper-osmotic to that of the surrounding medium. From studies at that time he also postulated that many marine dwelling elasmobranchs were not capable of adaptation to dilute environments. However, more recent investigations have demonstrated that, at least in some species, this may not be the case. Gradual acclimation of marine dwelling elasmobranchs to varying environmental salinities under laboratory conditions has demonstrated that these fish do have the capacity to acclimate to changes in salinity through independent regulation of Na+, Cl- and urea levels. This suggests that many of the presumed stenohaline marine elasmobranchs could in fact be described as partially euryhaline. The contributions of Thomas Thorson in the 1970s demonstrated the osmoregulatory strategy of a fully euryhaline elasmobranch, the bull shark, Carcharhinus leucas, and more recent investigations have examined the mechanisms behind this strategy in the euryhaline elasmobranch, Dasyatis sabina. Both partially euryhaline and fully euryhaline species utilise the same physiological processes to control urea, Na+ and Cl- levels within the body fluids. The role of the gills, kidney, liver, rectal gland and drinking process is discussed in relation to the endocrine control of urea, Na+ and Cl- levels as elasmobranchs acclimate to different environmental salinities. (C) 2003 Elsevier Inc. All rights reserved.

Sequence, circulating levels, and expression of C-type natriuretic peptide in a euryhaline elasmobranch, Carcharhinus leucas

The present study has examined expression and circulating levels of C-type natriuretic peptide (CNP) in the euryhaline bull shark, Carcharhinus leucas. Complementary DNA and deduced amino acid sequence for CNP in C leucas were determined by RACE methods. Homology of CNP amino acid sequence in C. leucas was high both for proCNP and for mature CNP when compared with previously identified elasmobranch CNPs. Mature CNP sequence in C. leucas was identical to that in Triakis seyllia and Seyliorhinus canicula. Levels of expression of CNP mRNA were significantly decreased in the atrium but did not change in either the brain or ventricle following acclimation to a SW environment. However, circulating levels of CNP significantly increased from 86.0 +/- 7.9 fmol ml(-1) in FW to 144.9 +/- 19.5 fmol ml(-1) in SW. The results presented demonstrate that changes in environmental salinity influences both synthesis of CNP from the heart and also circulating levels in C. leucas. Potential stimulus for release and modes of action are discussed. (c) 2005 Elsevier Inc. All rights reserved.

Diel and seasonal variation in the use of a nearshore sandflat by a ray community in a near pristine system

Knowledge of movements and habitat use is necessary to assess a species’ ecological role and is especially important for mesopredators because they provide the link between upper and lower trophic levels. Using acoustic telemetry, we examined coarse-scale diel and seasonal movements of elasmobranch mesopredators on a shallow sandflat in Shark Bay, Western Australia. Giant shovelnose rays (Glaucostegus typus) and reticulate whiprays (Himantura uarnak) were most often detected in nearshore microhabitats and were regularly detected throughout the day and year, although reticulate whiprays tended to frequent the monitored array over longer periods. Pink whiprays (H. fai) and cowtail stingrays (Pastinachus atrus) were also detected throughout the day, but were far less frequently detected. Overall, there was no apparent spatial or temporal partitioning of the sandflats, but residency to the area varied between species. In addition, ray presence throughout the year suggests that previously observed differences in seasonal abundance are likely because of seasonal changes in habitat use rather than large-scale migrations. Continuous use of the sandflats and limited movements within this ray community suggests that rays have the potential to be a structuring force on this system and that focusing on nearshore habitats is important for managing subtropical ray populations.