Electroreception in the obligate freshwater stingray, Potamotrygon motoro

Abstract

Elasmobranch fishes use electroreception to detect electric fields in the environment, particularly minute bioelectric fields of potential prey. A single family of obligate freshwater stingrays, Potamotrygonidae, endemic to the Amazon River, demonstrates morphological adaptations of their electrosensory system due to characteristics of a high impedance freshwater environment. Little work has investigated whether the reduced morphology translates to reduced sensitivity because of the electrical properties of freshwater, or because of a marine-tuned sensory system attempting to function in freshwater. The objective of the present study was to measure electric potential from prey of Potamotrygon motoro and replicate the measurements in a behavioural assay to quantify P. motoro electrosensitivity. Median orientation distance to prey-simulating electric fields was 2.73 cm, and the median voltage gradient detected was 0.20 mV cm À1 . This sensitivity is greatly reduced compared with marine batoids. A euryhaline species with marine-type ampullary morphology was previously tested in freshwater and demonstrated reduced sensitivity compared with when it was tested in seawater (0.2 mV cm À1 v. 0.6 nV cm À1 ). When the data were adjusted with a modified ideal dipole equation, sensitivity was comparable to P. motoro. This suggests that the conductivity of the medium, more so than ampullary morphology, dictates the sensitivity of elasmobranch electroreception.

Electroreception in marine fishes: chondrichthyans

“…Laboratory‐based behavioural choice assays later confirmed the preferential bite response to active electrodes emitting prey‐simulating stimuli over control electrodes in the bonnethead shark, Sphyrna tiburo (L. 1758) (Kajiura, ), S. lewini (Kajiura & Fitzgerald, ), C. plumbeus (Kajiura & Holland, ), blacktip reef shark, Carcharhinus melanopterus (Quoy & Gaimard 1824) (Haine et al, ), H. portjacksonii and shovelnose ray Aptychotrema vincentiana (Haacke 1885) (Kempster et al, ), H. sabinus (McGowan et al, ), Myliobatis californica Gill 1865, U. halleri and P. violacea , (Jordan & Kajiura, 2009), U. jamaicensis and R. bonasus (Bedore et al, ), P. motoro (Harris et al, ), P. microdon and G. typus and A. rostrata (Wueringer et al ., 2012). The median behavioural sensitivity of elasmobranchs to prey simulating electrical stimuli ranges from 5–107 nV cm −1 at distances of 22–44 cm (Jordan et al, , ; Kajiura, ; Kajiura & Holland, ; McGowan & Kajiura, ; Bedore et al, ; Wueringer et al ., 2012), which corresponds to the bioelectric potentials produced at the mouth, gills and cloaca (Figure ) of common invertebrate (14–28 μV cm −1 ), teleost (39–319 μV cm −1 ) and small elasmobranch (18–30 μV cm −1 ) prey species (Bedore & Kajiura, ).…”

“…The influence of environment on behavioural electrosensitivity is best illustrated in the transition from marine to freshwater habitats. For example, the euryhaline H. sabinus in seawater (salinity 35) has a detection threshold of 0.6 nV cm −1 but the threshold rises to 2 nV cm −1 in brackish water (salinity 15) and up to 3 μV cm −1 in fresh water (McGowan & Kajiura, ; freshwater value corrected by Harris et al, ). The freshwater sensitivity is commensurate with that of the obligate freshwater P. motoro , which can detect voltages as weak as 5 μV cm −1 (Harris et al, ).…”

“…The freshwater sensitivity is commensurate with that of the obligate freshwater P. motoro , which can detect voltages as weak as 5 μV cm −1 (Harris et al, ). This suggests that a reduced sensitivity and detection range of electrical stimuli in freshwater species (Crampton, ) occurs due to the lower conductivity and higher resistivity of fresh water compared with seawater and not the morphological adaptations of thicker skin and shorter ampullary canals seen in obligate freshwater elasmobranchs (Harris et al, ).…”

“…The electroreceptors of obligate marine chondrichthyans detect very weak bioelectric potentials of c . 1 nV cm −1 (Jordan et al, , ; Kajiura, ; Kalmijn, ), but behavioural sensitivity declines by three orders of magnitude for euryhaline species in fresh water (McGowan & Kajiura, ) and by five orders of magnitude for obligate freshwater species (Harris et al, ). The behaviours mediated by the electrosensory system include: orientation to prey‐simulating electrical fields (Kalmijn, , ; Pal et al ., 1982; Kimber et al, ), foraging and prey capture (Bedore et al ., 2014, Blonder & Alevizon, ; Jordan et al, , ; Kajiura, ; Kajiura & Fitzgerald, , Kalmijn, , ; Tricas, ), conspecific detection (Tricas et al, ), predator avoidance (Ball et al, ; Kempster et al, ; Sisneros et al, ), learning and habituation (Kimber et al, ), and possibly for navigation using the geomagnetic field (Anderson et al, ; Kalmijn, , , , ; Newton, ; Newton & Kajiura, ; Paulin, ).…”

Freezing behaviour facilitates bioelectric crypsis in cuttlefish faced with predation risk

“…However, voltage does not arise from active ventilation itself; rather, it is a product of osmoregulation at the gill surface, and the resulting charge is then propagated away from the gills in water currents resulting from the pumping behaviour during ventilation. In previous work that quantified electric potentials of aquatic invertebrates and fishes [28,40], data were carefully inspected for interactions among voltage, frequency and stress level (indicated by ventilatory rate). Data for the current work were subjected to similar scrutiny.…”