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Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus)

Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau... The Journal of Experimental Biology 208, 3441-3450 Published by The Company of Biologists 2005 doi:10.1242/jeb.01766 Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus) 1,2 2,3 1,2, Lucy M. Palmer , Max Deffenbaugh and Allen F. Mensinger * 1 2 Biology Department, University of Minnesota Duluth, Duluth, MN 55812, USA, Marine Biological Laboratory, Woods Hole, MA 02543, USA and ExxonMobil Upstream Research Company, PO Box 2189, Houston, TX 77252, USA *Author for correspondence (e-mail: [email protected]) Accepted 28 June 2005 Summary Inductive neural telemetry was used to record from toadfish (28·cm standard length; 33·cm total length) were microwire electrodes chronically implanted into the only able to detect mobile prey that approached within anterior lateral line nerve of the oyster toadfish, Opsanus approximately 40% of their body length. Both tau (L.). The lateral lines of free-ranging toadfish were spontaneously active and silent afferent fibers also stimulated by the swimming movements of a prey fish experienced a dramatic increase in firing during (Fundulus heteroclitus), and the corresponding neural predatory strikes, indicating that the fibers were not activity was quantified. Both spontaneously active and inhibited during rapid body movement. This study silent afferent fibers experienced an increase in neural investigates, for the first time, the neural response of the firing as the prey approached the lateral line. Activity was anterior lateral line to prey stimuli in free-ranging fish. evoked when the prey fish approached to within 8–12·cm of the neuromast, with increases in nerve firing rates directly correlated with diminishing distance. Thus, adult Key words: lateral line, telemetry, prey, toadfish, Opsanus tau. Introduction To enhance the interpretation of their environment, fish and distributions of local particle activity, alternating eddies and aquatic amphibians have evolved a lateral line system that slightly deformed vortex rings (Blickhan et al., 1992; Muller, detects displacements in the local water field. Neuromasts are 1996). Information about the direction and temporal scale of the basic unit of the lateral line system and consist of bundles fish movement can be contained in these trails (Hanke et al., of mechanoreceptive hair cells, which are comprised of a single 2000), which can persist in the water column for several kinocilium and numerous stereovilli protruding into a minutes (Hanke and Bleckmann, 2004). However, since the gelatinous cupula. The hydrodynamic properties of the chain of vortices generated by fish movement is difficult to neuromast act as a mechanical filter for sensory hair cells (van recreate and/or present during standard neurophysiological Netten, 1991). Hair cells are grouped into neuromasts located preparations, the activity of the lateral line in response to free- either upon the skin surface (superficial neuromasts) or swimming prey has been difficult to quantify. Instead, enclosed within subdermal canals (canal neuromasts). Canal vibrating spheres have been used historically as stimuli for the neuromasts function as water acceleration detectors, and lateral line (Wubbels et al., 1993; Muller, 1996; Coombs, 1999; superficial neuromasts act to determine water velocity (Kroese Kanter and Coombs, 2003). While instrumental in determining and Schellart, 1992). neuromast characteristics (frequency and directional Behavioral and electrophysiological experiments have sensitivity), pure stationary dipole-like stimuli are rarely illustrated that the lateral line functions in schooling behavior encountered in nature. (Partridge and Pitcher, 1980), rheotaxis (Montgomery et al., The detection of biologically relevant stimuli must often be 1997) and localization of underwater objects (Weissert and von accomplished during self-generated movement (e.g. Campenhausen, 1981). The lateral line has also been shown to swimming, ventilation). Recent studies conducted by Palmer receive water displacements generated by moving prey et al. (2003) indicate that the primary afferents of the anterior (Saunders and Montgomery, 1985; Montgomery and lateral line were stimulated during swimming and ventilatory Macdonald, 1987; Montgomery et al., 1988; Bleckmann and movements. Various studies have shown that lateral line Topp, 2003; Pohlmann et al., 2004). The great diversity in fish filtering during intense stimuli may be performed in higher body plan and swimming strategies can generate extremely brain regions. Tricas and Highstein (1990, 1991) identified complex hydrodynamic trails consisting of unpredictable efferent modulation of lateral line activity when toadfish THE JOURNAL OF EXPERIMENTAL BIOLOGY 3442 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger viewed live prey, and Montgomery and Bodznick (1994) and paralyzed with an intramuscular injection of a 0.01% –1 indicated that the lateral line medullary nuclei contain an solution of pancuronium bromide (600·g·kg ; Sigma). An adaptive filter capability that cancels input consistently incision was made through the dorsal musculature overlying associated with an animal’s own movements. the sagittal crest, and the muscle was retracted. A small The operating range of the lateral line system has been craniotomy was performed lateral to the sagittal crest and reported to be one to two body lengths (Denton and Gray, posterior to the transverse crest to expose the anterior ramus 1983; Kalmijn, 1988; Coombs, 1999; Braun and Coombs, of the anterior lateral line nerve. The electrode was inserted 2000). However, to accurately quantify the range and into the nerve just prior to its exit from the braincase. Potentials sensitivity of the lateral line to natural stimuli, neural activity were differentially amplified (Dagan, Minneapolis, MN, USA) must be monitored from an unconstrained teleost in quasi- and monitored on a portable computer using Chart5 for natural settings. Recording neural activity from free-swimming Windows software (ADInstruments, Colorado Springs, CO, fish has been complicated by the need for electrode stability USA). The two channels that provided the highest fidelity and/or a suitable telemetry device. Terrestrial telemetry modes signal were chosen for the experiments. Once a candidate fiber such as infrared light or radio waves are rapidly attenuated in was located, the fish was left undisturbed for 30·min to ensure seawater and are ineffective. The development of an inductive fiber stability. neural telemetry system allows the recording of neural Cyanoacrylate gel (Pacer Technology, Rancho Cucamonga, responses from free-ranging toadfish (Mensinger and CA, USA) was used to affix the electrode to the skull and seal Deffenbaugh, 1998, 2000; Palmer and Mensinger, 2004). This the craniotomy. The muscle was restored to its original study reports the activity of the lateral line in response to free- position, and the muscle, faschia and epidermis were swimming prey. individually sutured to provide a watertight seal over the craniotomy and around the transdermal electrode lead. The differential amplifier was disconnected from the electrode, and Materials and methods the cylindrical telemetry tag (15·mm38·mm, diameter Animal care length; 8·g) was inserted into the waterproof electrode Adult toadfish [~33·cm total length (TL); 28±1.4·cm connector. The tag was sutured parallel to the dorsal fin on the standard length (SL); 675±46·g wet mass; means ± S.E.M.] of dorsal surface of the fish. either sex were obtained from the Marine Biological Neural recordings Laboratory (MBL), Woods Hole, MA, USA. Fish were housed in large flow-through seawater tanks maintained at 20°C and Chronic extracellular recordings from lateral line primary fed squid and bait fish. All animal care and experimental afferent fibers were obtained using an inductive telemetry procedures conformed to institutional animal care protocols. system (Mensinger and Deffenbaugh, 1998, 2000; Palmer and Mensinger, 2004). In brief, the inductive telemetry system Microwire electrode consists of a transmitter tag and receiver coils. The tag Microwire electrodes consisting of three strands of insulated transmits the neural signal as a frequency-modulated magnetic 20·m-diameter 10% platinum/iridium wire (Sigmund Cohn field (90·kHz carrier, 20·kHz bandwidth), which is detected by Corp., Mt Vernon, NY, USA) were custom fabricated for each receiver coils embedded in a recharging habitat and stage implantation. Each microwire strand was affixed to hard silver- (RECHABS). To recharge the tag, the RECHABS produces an plated copper multistranded wire (25·m diameter) with oscillating magnetic field (50·T, 200·kHz), and the tag stores conductive silver paint (Silver Print Paint, GC Electronics, energy from this field in its capacitors. The RECHABS Rockford, IL, USA). The multistranded wire was attached to consists of a cylindrical habitat (12·cm30·cm, internal silver wire (320·m) that terminated into a multipin underwater diameter  length) that opens onto an octagonal stage (16·cm connector. The anterior portion of the microwires was threaded per side; Fig.·1). The RECHABS can both receive the through a 1·mm length of polymide tubing (180·m outer telemetry signal from the tag and recharge the tag when the tag diameter; A-M Systems Inc., Carlsborg, WA, USA) to maintain is within the habitat or up to a height of approximately 15·cm the recording sites in proximity. Any exposed wire/connections above the stage. The tag can be fully charged in less than 30·s were encased in medical device adhesive (Loctite 3341; Henkel and will provide telemetry for 5·min. Loctite Corp., Rocky Hill, CT, USA) and cured with ultraviolet Immediately after surgery, the fish were placed in an opaque light (ELC #660; Electro-lite Corp., Danbury, CT, USA). The fiberglass experimental tank (90·cm45·cm, width  length; impedance of each electrode channel was determined with an 15·cm water depth) and left undisturbed for a minimum of impedance-test unit (FHC; Bowdoinham, ME, USA) using 90·min. The innervated neuromast location was determined by 1·kHz input frequency. Only electrodes with impedances monitoring neural activity while a small brush was gently run between 0.5 and 1.2·M were used. along the supraorbital or infraorbital lateral line. This allowed the innervated neuromast to be localized to within two or three Electrode implant end organs, or an area of approximately one cm . Fish were anesthetized by immersion in 0.005% tricaine (3- Killifish (Fundulus heteroclitus; 6–8·cm SL) were used as aminobenzoic acid ethyl ester; Sigma, St Louis, MO, USA) prey. To maximize predator–prey encounters, a circular THE JOURNAL OF EXPERIMENTAL BIOLOGY Lateral line sensitivity in toadfish 3443 distance between the neuromast and the intersection point of the nearside killifish pectoral fin with its body axis. A trial consisted of placing a free-swimming or tethered Fundulus into the arena and monitoring its swimming movements while concurrently recording toadfish lateral line activity for up to 10·min. An encounter consisted of a Fundulus hovering for >500·ms in the same position that was within 20·cm of the innervated neuromast during a trial. Five to 12 trials were conducted per toadfish, with up to 119 encounters recorded per trial. To compare activity between H fibers, firing rates were normalized according to the maximum firing rate elicited by prey movements that was recorded in each trial. Although the microwires often yielded multiunit activity, fiber discrimination was usually limited to a single unit that yielded the greatest action potential amplitude and was clearly 45 cm discernible from other units. To verify that the same unit was consistently recorded during an experiment, individual fibers were distinguished using rigorous waveform analysis (Spike2) in addition to spike amplitude. During one implant, two units Fig.·1. Dorsal view of the experimental arena. The recharging habitat were discovered to be clearly distinguishable based on and stage (RECHABS) consists of the cylindrical habitat (H) and amplitude and waveform analysis, and both fibers were octagonal stage (S). Neural telemetry and tag recharging could individually analyzed during the trial. transpire when the fish was in the habitat or over the stage. The black The streamlined telemetry tag only added 1% to toadfish circle (arrow) represents an opaque barricade that restricted the prey body mass and its attachment did not have noticeable effects and the toadfish to the stage area. Fish movements were recorded with on behavior. Normal ventilation rates and equilibrium returned an overhead video camera (C). Drawing is not to scale. within 30·min of anesthetic withdrawal, and swimming activity resumed within two hours post-surgery. Recent work has plastic barricade surrounded the stage and restricted the shown that the sensitivity of the anterior lateral line to killifish to the RECHABS area. Prey that did not approach the mechanical stimuli is restored within 90·min of anesthetic toadfish within 15·min were anesthetized (0.0001% MS-222), withdrawal (Palmer and Mensinger, 2004), and therefore and a barbless fish hook (size 6) attached to monofilament experiments were not initiated until a minimum of two hours (1·kg test) was inserted between the premaxilla and maxilla following anesthetic removal. During all trials, toadfish were bone of the killifish. Once the tethered Fundulus recovered monitored for abnormal physiological (respiration rate) and normal swimming activity, they were placed in the behavioral (sudden movement, tail contraction) changes experimental tank. Sufficient slack was maintained in the before, during and after the application of the magnetic field, tether to allow normal swimming movements; however, the and no discernible effects were observed. Previous studies tether allowed the fish to be directed towards the toadfish (Mensinger and Deffenbaugh, 1998, 2000; Palmer and when necessary. Mensinger, 2004) demonstrated that the magnetic field does The telemetry signals were recorded up to four days post not affect neural activity or behavior in the toadfish. electrode implantation and stored on a portable computer using Prey stimulus Chart5 software and analyzed offline with Spike2 software (Cambridge Electronic Design, Cambridge, UK). Still-water trials were conducted with 8·cm SL Fundulus in Predator–prey interactions were simultaneously recorded on a large rectangular tank (2.5·m1.2·m0.5·m) with water –1 videotape (30·frames·s ; Sony Digital Handycam, Sony depth maintained at 20·cm. Water velocities generated by Electronics USA, Oradell, NJ, USA) that was synchronized hovering Fundulus were calculated by digital particle tracking with the neural telemetry system and analyzed frame by frame velocimetry. Fluid flow around the fish was illuminated by a using DV Shelf video frame capture and Scion Imaging horizontal laser sheet, 0.5·mm thick, and imaged from above software (Scion Corp., Frederick, MD, USA). Killifish with a high-resolution digital video camera (Kodak ES 1.0, movement alternated between caudal-fin-mediated forward 1008·pixels1018·pixels). The flow was seeded with swimming and stationary positioning via 2–3·Hz oscillation of 20–40·m-diameter neutrally buoyant fluorescent particles. the pectoral fins. Because the various fins and swimming For further details, refer to Anderson et al. (2001). motions of fish produce differing stimuli of varying intensity Statistical analysis (Gibb et al., 1994; Drucker and Lauder, 2001), neural activity was only quantified when the prey hovered in the same location All statistical analysis was performed using GraphPad for greater than 500·ms. Prey distance was defined as the Software (San Diego, CA, USA) or SigmaStat for Windows THE JOURNAL OF EXPERIMENTAL BIOLOGY 3444 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger version 3.10 (Systat Software, Inc., Richmond, CA, USA). All data represent mean values ± 1 S.E.M. unless otherwise indicated. Fiber activity during an encounter was binned into 2·cm intervals (distance of Fundulus fin origin to innervated neuromast). As the range of activity for the silent fibers was moderate (0–17·Hz), a one-way analysis of variance (ANOVA) was used to determine differences in spike activity among the four fibers during prey encounters. For the * spontaneous active fibers, firing rates were normalized according to the maximum firing rate elicited by prey movements that was recorded in each fiber during a trial. The 2D Graph 5 resulting percentages were transformed using the arcsine function (Zar, 1984), and a one-way ANOVA was used to determine differences in the transformed data for fiber activity for the combined five spontaneous active fibers. Samples were tested for normality using the method of Kolmogorov and Smirnov. Bartlett’s test was used to determine the use of parametric or non-parametric testing. Results Two types of lateral line fibers were identified. Silent fibers (N=4) did not display any spontaneous activity and were only activated by water movement. Their average sustained firing rate to prey movement ranged from 3 to 5·Hz, which was ~27% of the fibers’ maximal evoked response. Spontaneous active fibers (N=5) were of the irregular type (Tricas and Highstein, Control <2 2–4 4–6 6–8 8–10 10–12 12–14 1991) and had an average discharge rate of ~47·Hz in the Distance (cm) absence of stimulation. Prey movements stimulated these fibers Fig.·2. The mean normalized neural firing rates of (A) silent (N=4) to firing frequencies approximately 65% of their maximum and (B) spontaneously active afferent fibers (N=5) of the anterior firing rate. lateral line are plotted versus the distance of the innervated As the distance between the prey and neuromast diminished, neuromasts to the prey. All firing rates were normalized according to silent fibers were stimulated to fire (Fig.·2A). The greatest range the maximum firing rate recorded during each trial. Neural activity at which prey stimulated a silent fiber was 11·cm. Spontaneous was analyzed only when the prey fish was at the same location for fibers showed similar characteristics, with activity significantly greater than 500·ms. All distances were measured from the insertion increasing (ANOVA, P<0.05) above resting background levels point of the nearside prey pectoral fin to the neuromast that was at prey distances of up to 4·cm from the neuromasts (Fig.·2B). innervated by the recording. Asterisks indicate significantly different Prey at distances between 4 and 8·cm stimulated firing rates means from controls (ANOVA). The broken horizontal line in B above background levels; however, at distances greater than represents the mean normalized spontaneous firing rate from spontaneously active fibers. 8·cm, the presence of prey did not lead to elevated rates. Fig.·3. The probability of a silent fiber (triangles) firing during a prey encounter and the probability of a spontaneously active fiber 100 Spont. >1 S.D. increasing its discharge rate one (filled circle) or two (open circle) Spont. >2 S.D. standard deviations above its spontaneous discharge rate during Silent a prey encounter is plotted versus prey distance. If the silent fiber fired during the event, it was considered stimulated, and the 60 probability of the silent fibers firing was calculated as: (stimulated encounters/total encounters)100. If the firing activity of the spontaneously active fibers firing increased one and/or two standard deviations above its mean resting discharge rate it was considered stimulated and the probability was calculated as: (stimulated encounters >1·S.D./total encounters)100 and (stimulated encounters >2·S.D./total encounters)100. The data represent the summary of all trials for each fiber class, and each <2 2–4 4–6 6–8 8–10 10–12 12–14 >14 point represents a minimum of 15 trials at each distance. Prey Distance (cm) distance was binned into 2·cm segments. THE JOURNAL OF EXPERIMENTAL BIOLOGY Probability of firing (%) Normalized firing rate (% of maximum) Lateral line sensitivity in toadfish 3445 20 A Fig.·4. The activity of a silent, afferent fiber innervating a superficial neuromast on the infraorbital lateral line, as monitored during prey movement. (A) The distance (cm) of the prey fish from the recorded neuromast. (B) The full neural waveform from the anterior lateral line nerve that was transmitted via inductive telemetry. Although multiunit activity is visible in the trace, only the fiber with the greatest amplitude of action potential was used for data analysis. The fiber had no spontaneous activity 25 μV and exhibited maximum firing (~10·Hz) when the prey 20 s fish was within 1·cm of the neuromast. Small fluctuations in action potential frequency may be more valuable for prey detection for the toadfish than statistically significant changes. For silent fibers, the probability of a silent fiber firing during an encounter was plotted versus prey distance (Fig.·3). Silent fibers fired greater than 60% of the time when prey was located within 4·cm of the neuromast. This probability decreased to approximately 20% between 6 and 12·cm, and prey located further than Toadfish 12·cm failed to stimulate silent fibers. For spontaneous fibers, determining small fluctuations in action potential frequency was not as clear, as spontaneous discharge rates could drift by 5–10% during a trial. Therefore, Fig.·3 includes the probability of spontaneous fibers firing one and/or two standard deviations above their resting discharge rate during an encounter versus prey distance. Thus, even after including a less rigorous benchmark (1 S.D.), the probability of a spontaneous fiber reacting to the prey during an encounter continues to decline sharply with distance. Fig.·4 shows the neural activity in a silent lateral line fiber correlated with the position of a free-swimming Fundulus during a 5·min trial. Both transient swimming and hovering evoked a neural response when the prey fish approached within 6·cm of the neuromast; however, movement outside this range did not induce firing. Activity for a silent anterior lateral line fiber innervating a superficial neuromast on the right infraorbital lateral line of a toadfish is illustrated in Fig.·5. The fiber was unresponsive at prey distances greater 33 µV 100 ms than 10·cm; however, activity was evoked (~5·Hz) when the prey approached to within 3.5·cm of the neuromasts. As Fig.·5. Neural activity during the approach of a single prey fish. The the prey closed to within 1·cm, firing rate increased to ~10·Hz. diagram depicts the head of the toadfish projecting out of its habitat The neural response of a spontaneously active fiber and a and the sequential positions of the approaching prey: (A) 10·cm; (B) silent fiber to hovering prey is illustrated in Fig.·6. Both fibers 3.5·cm; (C) 1.0·cm. Images were reconstructed from single video innervated superficial neuromasts located on the infraorbital frames. The letter next to the prey fish corresponds to neural activity line of the anterior lateral line. As prey approached within from a superficial neuromast on the suborbital portion of the 8·cm, both fibers experienced an increase in neural activity. infraorbital lateral line. Although multiunit activity is visible in the The neural activity during predatory strikes was recorded in trace, data analysis was restricted to the fiber with the greatest four fibers from three fish during 20 prey strikes. The firing amplitude of action potential. THE JOURNAL OF EXPERIMENTAL BIOLOGY Distance (cm) Telemetry Habitat 3446 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger (7) (7) (1) (6) SP1 SP2 SP3 SL1 0 5 10 15 20 25 30 Fig.·7. Mean firing rate (± 1 S.E.M.) of four anterior lateral line afferents fibers [three spontaneous (SP) and one silent (SL)] immediately before (open) and during (filled) a toadfish prey strike. 80 Numbers above the bars represent the number of prey strikes that were averaged for each fiber. The water velocities generated by pectoral and caudal fin movement of 8·cm SL Fundulus were extremely complex (Fig.·9). Maximum water velocities generated by the pectoral –1 fins during hovering were approximately 5·cm·s , with water displacement rapidly attenuating with distance from the body –1 axis. Velocities between 2 and 3·cm·s were often detectable within 2–3·cm of the fin’s insertion; however, at distances 0 5 10 15 20 –1 greater than 5·cm, water movement remained less than 1·cm·s . Distance (cm) Fig.·6. Firing rates of (A) a spontaneously active afferent fiber and (B) a silent fiber in response to a prey fish located at variable distances Discussion from the neuromast. Both fibers innervated superficial neuromasts. All Oyster toadfish are benthic fish that inhabit most estuaries distances were measured from the insertion point of the nearside prey along the Atlantic Coast of the USA (Gudger, 1910). They are pectoral fin to the neuromast that was innervated by the recording. The broken horizontal line in A represents the mean spontaneous activity. All firing rates were normalized according to the maximum firing rate elicited by prey movements during each trial. Neural activity was analyzed only when the prey fish was at the same location for greater than 500·ms. activity of the fibers increased during all strikes (Fig.·7). The 1 s spontaneously active fibers (N=3) experienced a 9-fold average increase in firing activity above resting discharge rates. These B increases were much greater than the maximum firing activity Strike Retained Expelled evoked by prey movements in the same fibers. Neural activity from a single fiber during a prey strike is illustrated in Fig.·8. The killifish approached the toadfish at a constant velocity –1 (2·cm·s ) from the contralateral side of the neuromast, and the toadfish struck when the prey was directly in front of the 100 ms mouth, 2·cm from the premaxilla (Fig.·8B). During the strike, Fig.·8. Neural activity from an afferent anterior lateral line fiber the toadfish moved forward slightly (1·cm) and opened its before, during and after a prey strike. Vertical lines on the trace mouth to engulf the prey fish. The prey was retained in the indicate individual action potentials from a single fiber that were toadfish’s mouth for 1300·ms before being expelled. discriminated based on spike amplitude. The arrows indicate initiation Both silent and spontaneously active fibers were observed of opercular contraction for each ventilation cycle. The time during to continually fire in phase with the toadfish’s ventilation cycle. the strike, capture and subsequent expulsion of the prey is boxed in The fibers fired regularly with each ventilation cycle and were A, and this interval is expanded in B. The prey was retained in the never observed to become habituated (Fig.·8). mouth of the toadfish for approximately 1·s before being expelled. THE JOURNAL OF EXPERIMENTAL BIOLOGY Normalized firing rates (% of maximum) Firing rate (Hz) Lateral line sensitivity in toadfish 3447 Fig.·9. The picture shows the water movements produced by an 8·cm SL Fundulus heteroclitus taken with a digital video camera at 10001000 pixel resolution. Each velocity vector represents the average of a 32·pixel32·pixel window, and the center of each window is spaced 16·pixels apart. Velocities are presented by pseudo color images. Scale bar, 2·cm. predominately ambush predators that prey largely upon limit the disparity in Fundulus swimming characteristics, data crustaceans and small fish (Chrobot, 1959; Schwartz and analysis was restricted to periods when prey were hovering in Dutcher, 1963; McDermott, 1964; Phillips and Swears, 1979; the same location for greater than 500·ms. Consequently, much Wilson et al., 1982; Price and Mensinger, 1999; Mensinger et of the data analysis characterizes lateral line activity in al., 2003). Field and laboratory observations indicate that response to oscillation (3·Hz) of the killifish pectoral fin. toadfish spend the majority of their time in small caves or Digital particle tracking velocimetry allowed analysis of the crevices with their head facing outward and will often remain water velocities generated by hovering Fundulus. Retraction of motionless prior to launching a ballistic strike at nearby prey. the pectoral fins in hovering killifish produced maximum water –1 Therefore, with the exception of water currents generated by velocities of approximately 5·cm·s within the arc traveled by respiratory activity and prey strikes, there exists little self- the fin. These velocities rapidly attenuated with distance from –1 generated interference for their lateral line. the fin’s origin. Velocities between 2 and 3·cm·s were often As fish swimming combines the locomotion of several detectable within 3·cm of the fin; however, at distances greater independent fin systems (Drucker and Lauder, 2001), the than 5·cm from the fin’s origin, water movement declined to –1 generated hydrodynamics can be complex. A swimming fish less than 1·cm·s before fading into the background –1 leaves a hydrodynamic trail in the water that can persist several (0.1·cm·s ). Caudal fin motion disrupted a larger volume of minutes after its passage (Hanke et al., 2000; Hanke and water over greater distances. However, as these deflections Bleckmann, 2004). Experiments conducted by Enger et al. were lateral and posterior to the pectoral fin currents, there (1989) concluded that the lower-frequency accelerations appeared to be little potential for constructive inference resulting from the prey’s motion are biologically of utmost between the two sources. As data analysis was restricted to importance in lateral line detection. The killifish was chosen hovering, during which the caudal fin remained relatively for these experiments as it is natural prey for the toadfish stationary, pectoral fin movements were the primary stimulus (Chrobot, 1959). Its swimming behavior alternates between source. forward propulsion mediated by body and caudal fin Previous studies have indicated the persistence of movement, and stationary hovering using pectoral fin hydrodynamic trails several minutes following fish passage oscillation. Caudal fin movement generally creates greater (Hanke et al., 2000; Hanke and Bleckmann, 2004). Slowly water displacement and may consequently provide a larger decaying wakes could complicate determining if the lateral line stimulus for the lateral line. However, as toadfish is reacting to current prey motion or residual wakes. Fig.·4 predominantly strike at approaching prey, bow waves or illustrates a typical trial during which the prey moved forward fin (pectoral and/or pelvic) displacement may be more throughout the arena. The silent fiber ceased to fire when the important than caudal movements or subsequent wakes. To prey moved greater than 10·cm away from the toadfish. If the THE JOURNAL OF EXPERIMENTAL BIOLOGY 3448 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger hydrodynamic trails continued to persist at a physiological level, the fiber should have continued to fire after the prey vacated the area. However, the previous studies examined wakes generated by rapidly swimming fish which would create greater and more persistent, water disturbance than Fundulus. 30 Alternatively, the lateral line fibers could have become habituated to a persistence stimulus and ceased to respond. However, when lateral line fibers were stimulated for up to 60·s with continuous water flow, habituation was not evident (Palmer and Mensinger, 2004), indicating that a dispersing stimulus and not habituation was responsible for the return of <1 1–2 2–3 3–4 4–5 >5 lateral line activity to baseline levels. Distance (cm) Several studies have suggested that the lateral line detects Fig.·10. The frequency of attacks by 8·cm SL toadfish at 2·cm SL prey up to a distance of 1–2 body lengths (Denton and Gray, guppies is plotted versus the distance between the two fish at the time 1983; Kalmijn, 1988; Coombs, 1999; Braun and Coombs, the toadfish launched its attack. The total number of attacks analyzed 2000). However, many lateral line studies have been performed was 78. Modified from Price and Mensinger (1999). with vibrating probes, which may generate a stronger stimulus than prey and do not reflect the complexity of water currents generated by natural stimuli. The neural telemetry system allowed lateral line activity to be monitored in the presence of reacts to the prey rather than when detection occurs, they provide free-swimming prey. The distance at which prey movement further support for close-range detection. Year one toadfish modulated the toadfish lateral line was shorter than the range (8·cm SL; 10·cm TL) feeding on small guppies (2·cm SL) during usually proposed for other species. Both spontaneous and silent daylight trials did not launch strikes at prey that were greater fibers of the toadfish anterior lateral line were stimulated by than 5·cm from the toadfish (Fig.·10; Price and Mensinger, prey pectoral fin oscillation at distances from the sensory 1999). These attacks were probably mediated by both visual and neuromast of less than half the toadfish body length. The mechanical cues, and reaction distances under low light detection range represented the distance between neuromast conditions would be predicted to be shorter and more accurate location and pectoral fin insertion; however, the nearest distance indicators of lateral line range. Ongoing studies in juvenile between predator and prey (often the head of the killifish and toadfish indicate that both reaction distance and attack range are the body of the toadfish) was frequently 2·cm closer. less in the dark than the light (L. Lundeen and A. F. Mensinger, Caution must be applied in two areas of our data unpublished) and are consistent with studies by Enger et al. interpretation. As the recordings were restricted to individual (1989), New and Kang (2000) and Richmond et al. (2004) that fibers in a localized region of the anterior lateral line, it is found that predatory fish without visual cues reacted to prey at possible that other regions may contain neuromasts more distances of less than 50% of the predator’s body length. sensitive to prey movements. Alternatively, central integration Although the lateral line can contribute significant from multiple neuromasts may function to increase resolution information for prey localization, due to its short range it is and sensitivity and project the detection distance further than evident that other systems are important in locating distant an individual neuromast. Additionally, slight changes in firing prey. The far hydrodynamic fields of moving objects are frequency may provide important information for the fish but hypothesized to be mediated by the inner ear (Kalmijn, 1988). fail to be statistically significant, especially when averaged Additionally, behavioral and physiological experiments have over different neurons and fish, as in the current study. For illustrated that tactile, chemosensory, hydrodynamic and visual example, in the 4–8·cm range for spontaneous fibers, the fibers stimuli are capable of guiding prey capture (Montgomery et fired well above background discharges and undoubtedly al., 2002). provided information about the prey. However, using less The oyster toadfish possesses an anterior lateral line rigorous statistical analysis (1 S.D. above spontaneous rate) did dominated by superficial neuromasts (Clapp, 1898). Although not greatly extend the maximum detection distance. It remains behavioral experiments in other species have indicated that possible that small, transient fluctuations in lateral line activity prey detection and localization is mediated by canal that were outside our resolution ability encode for prey neuromasts (Coombs et al., 2001), it appears that the afferent distance and extend detection distance. However, the response fibers innervating the superficial neuromasts of the toadfish dynamics of the silent fibers, which did not fire in the absence anterior lateral line are responsive to the stimuli produced by of stimulus, provide support for the limited range of the lateral prey. Consequently, although canal neuromasts may provide line as these fibers failed to fire until the prey approached important prey localization information, superficial neuromasts within 11·cm. are able to detect the low-frequency water displacements Predator–prey interactions are also consistent with lateral line generated by prey and contribute to near-field prey detection. sensitivity recorded in toadfish. Although behavioral Efferent innervation of lateral line hair cells has been observations are limited to discerning when the predator visibly hypothesized to inhibit afferent firing (Russell and Roberts, THE JOURNAL OF EXPERIMENTAL BIOLOGY Attack frequency (%) Lateral line sensitivity in toadfish 3449 1974) and prevent depletion of transmitter from lateral line hair line organs of the top minnow Aplocheilus lineatus. Naturwissenschaften 68, 624-625. cells during locomotion or rapid movements (Russell, 1971). Blickhan, R., Krick, C., Zehren, D., Nachtigall, W. and Breithaupt, T. Tricas and Highstein (1990) illustrated that the lateral line (1992). Generation of a vortex chain in the wake of a subundulatory experienced transient inhibition when toadfish were allowed to swimmer. Naturwissenschaften 79, 220-221. Braun, C. B. and Coombs, S. (2000). The overlapping roles of the inner ear view live Fundulus in an adjacent aquarium and that in a and lateral line: the active space of dipole source detection. Phil. Trans. R. minority of fibers there was a decrease in neural activity in Soc. Lond. B 355, 1115-1119. anterior lateral line afferent fibers during a predatory strike. Chrobot, R. J. (1959). The feeding habits of the toadfish (Opsanus tau) based on an analysis of the contents of the stomach and intestine. Master’s thesis. However, recent studies have illustrated the ability of hair cells University of Maryland. to release neurotransmitters for prolonged periods with little Clapp, C. (1898). The lateral line system of Batrachus tau. J. Morph. 15, 223- exhaustion (Moser and Beutner, 2000; Trussell, 2002). 265. Coombs, S. (1999). Signal detection theory, lateral-line excitation patterns and Evidence of efferent modulation (reduction or cessation of prey capture behaviour of mottled sculpin. Anim. Behav. 58, 421-430. nerve activity) was not observed during any trial. The length Coombs, S., Braun, C. B. and Donovan, B. (2001). The orienting response of our trials and the inclusion of intermittent mechanosensory of Lake Michigan mottled sculpin is mediated by canal neuromasts. J. Exp. Biol. 204, 337-348. stimulation may have occluded our ability to detect efferent Denton, E. J. and Gray, J. (1983). Mechanical factors in the excitation of modulation. However, the lack of inhibition of toadfish clupeid lateral lines. Proc. R. Soc. Lond. B. 218, 1-26. neuromasts located near the operculum that were continually Drucker, E. G. and Lauder, G. V. (2001). Locomotor function of the dorsal fin in teleost fishes: experimental analysis of wake forces in sunfish. J. Exp. stimulated by opercular displacement (present study) or Biol. 204, 2943-2958. prolonged water current (Palmer and Mensinger, 2004) appears Enger, P. S., Kalmijn, A. J. and Sand, O. (1989). Behavioral investigations to indicate that efferent modulation was not common in our on the functions of the lateral line and inner ear in predation. In The Mechanosensory Lateral Line – Neurobiology and Evolution (ed. S. Coombs, sample population. H. Munz and P. Gorner), pp. 265-285. New York: Springer-Verlag. Both silent and irregular fibers experienced a dramatic Gibb, A. C., Jayne, B. C. and Lauder, G. V. (1994). Kinematics of pectoral increase in firing during a predatory strike. It is possible that fin locomotion in the bluegill sunfish Lepomis macrochirus. J. Exp. Biol. 189, 133-161. self-generated noise created during a predatory strike may be Gudger, E. W. (1910). Habits and life history of the toadfish (Opsanus tau). filtered by higher order neurons. Montgomery and Bodznick Bull. U.S. Bur. Fish. 28, 1071-1099. (1994) indicate that the lateral line medullary nuclei contain an Hanke, W. and Bleckmann, H. (2004). The hydrodynamic trails of Lepomis gibbosus (Centrarchidae), Colomesus psittacus (Tetraodontidae) and adaptive filter capability that cancels inputs consistently Thysochromis ansorgii (Cichlidae) investigated with scanning particle associated with an animal’s own movements. Further image velocimetry. J. Exp. Biol. 207, 1585-1596. experiments are required to determine decisively whether the Hanke, W., Brucker, C. and Bleckmann, H. (2000). The ageing of the low- frequency water disturbances caused by swimming goldfish and its possible lateral line conveys self-regulatory information during a relevance to prey detection. J. Exp. Biol. 203, 1193-1200. predatory strike. Kalmijn, A. J. (1988). Hydrodynamic and acoustic field detection. In Sensory In summary, the toadfish lateral line can detect transient Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp. 83-130. New York: Springer-Verlag. water displacement generated by natural prey. The distance at Kanter, M. J. and Coombs, S. (2003). Rheotaxis and prey detection in which stimulation occurred was less than 40% of toadfish body uniform currents by Lake Michigan mottled sculpin (Cottus bairdi). J. Exp. length. This is the first study that investigates the neural Biol. 206, 59-70. Kroese, A. B. and Schellart, N. A. (1992). Velocity- and acceleration- response of the anterior lateral line to prey stimuli in free- sensitive units in the trunk lateral line of the trout. J. Neurophysiol. 68, 2212- ranging fish and highlights the importance of the lateral line in near-field prey detection. McDermott, J. J. (1964). Food habits of the toadfish, Opsanus tau (L.), in New Jersey waters. J. Penn. Acad. Sci. 38, 64-71. Mensinger, A. F. and Deffenbaugh, M. (1998). Prototype rechargeable tag The authors wish to thank Tom Hrabik and John Nicols for for acoustical neural telemetry. Biol. Bull. 195, 194-195. helpful criticisms of the manuscript, and Beth Giuffrida for Mensinger, A. F. and Deffenbaugh, M. (2000). Anechoic aquarium for ultrasonic neural telemetry. Phil. Trans. R. Soc. Lond. B 355, 1305-1308. her analysis assistance. We are especially indebted to Mark Mensinger, A. F., Price, N. N., Richmond, H. E., Forsythe, J. W. and Grosenbaugh for his assistance with the digital particle Hanlon, R. T. (2003). Mariculture of the oyster toadfish: juvenile growth tracking velocimetry. This work was supported by a and survival. N. Am. J. Aquacult. 65, 289-299. Montgomery, J. C. and Bodznick, D. (1994). An adaptive filter that cancels University of Minnesota Grant in Aid and by the Minnesota self-induced noise in the electrosensory and lateral line mechanosensory Sea Grant College Program supported by the NOAA Office of systems of fish. Neurosci. Lett. 174, 145-148. Sea Grant, United States Department of Commerce, under Montgomery, J. C. and Macdonald, J. A. (1987). Sensory tuning of lateral line receptors in Antarctic fish to the movements of planktonic prey. Science grant No. NOAA-NA16-RG1046. The U.S. Government is 235, 195-196. authorized to reproduce and distribute reprints for government Montgomery, J. C., Macdonald, J. A. and Housley, G. D. (1988). Lateral purposes, not withstanding any copyright notation that may line function in an Antarctic fish related to the signals produced by planktonic prey. J. Comp. Physiol. A 163, 827-833. appear hereon. This paper is journal reprint (512) of the Montgomery, J. C., Baker, C. and Carton, A. (1997). The lateral line can Minnesota Sea Grant College Program. mediate rheotaxis in fish. Nature 389, 960-963. Montgomery, J. C., Macdonald, F., Baker, C. F. and Carton, A. G. (2002). Hydrodynamic contributions to multimodal guidance of prey capture References behavior in fish. Brain Behav. Evol. 59, 190-198. Anderson, E. J., McGillis, W. R. and Grosenbaugh, M. A. (2001). The Moser, T. and Beutner, D. (2000). Kinetics of exocytosis and endocytosis at boundary layer of swimming fish. J. Exp. Biol. 204, 81-102. the cochlear inner hair cell afferent synapse of the mouse. Proc. Natl. Acad. Bleckmann, H. and Topp, G. (2003). Surface wave sensitivity of the lateral Sci. USA 97, 883-888. THE JOURNAL OF EXPERIMENTAL BIOLOGY 3450 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger Muller, H. M. (1996). Indications for feature detection with the lateral line Saunders, A. J. and Montgomery, J. C. (1985). Field and laboratory studies organ in fish. Comp. Biochem. Physiol. 114A, 257-263. of the feeding behaviour of the piper Hyporhamphus ihi with reference to New, J. G. and Kang, P. Y. (2000). Multimodal sensory integration in the the role of the lateral line in feeding. Proc. R. Soc. Lond B 224, 209-221. strike-feeding behaviour of predatory fishes. Phil. Trans. R. Soc. Lond. B Schwartz, F. J. and Dutcher, B. W. (1963). Age, growth and food of the 355, 1321-1324. oyster toadfish near Solomons, Maryland. Trans. Am. Fish. Soc. 92, 170- Palmer, L. M. and Mensinger, A. F. (2004). The effect of the anesthetic 173. tricaine (MS-222) on nerve activity in the anterior lateral line of the oyster Tricas, T. C. and Highstein, S. M. (1990). Visually mediated inhibition of toadfish, Opsanus tau. J. Neurophysiol. 92, 1034-1041. lateral line primary afferent activity by the octavolateralis efferent system Palmer, L. M., Giuffrida, B. A. and Mensinger, A. F. (2003). Neural during predation in the free- swimming toadfish, Opsanus tau. Exp. Brain recordings from the lateral line in free-swimming toadfish, Opsanus tau. Res. 83, 233-236. Biol. Bull. 205, 216-218. Tricas, T. C. and Highstein, S. M. (1991). Action of the octavolateralis Partridge, B. L. and Pitcher, T. J. (1980). The sensory basis of fish schools: efferent system upon the lateral line of free-swimming toadfish, Opsanus relative roles of lateral line and vision. J. Comp. Physiol. 135, 315-325. tau. J. Comp. Physiol. A 169, 25-37. Phillips, R. R. and Swears, S. B. (1979). Social hierarchy, shelter use, and Trussell, L. O. (2002). Transmission at the hair cell synapse. Nature Neurosci. avoidance of predatory toadfish (Opsanus tau) by the striped blenny 5, 85-86. (Chasmodes bosquianus). Anim. Behav. 27, 1113-1121. van Netten, S. M. (1991). Hydrodynamics of the excitation of the cupula in Pohlmann, K., Atema, J. and Breithaupt, T. (2004). The importance of the the fish canal lateral line. J. Acoust. Soc. Am. 89, 310-319. lateral line in nocturnal predation of piscivorous catfish. J. Exp. Biol. 207, Weissert, R. and von Campenhausen, C. (1981). Discrimination between 2971-2978. stationary objects by the blind cave fish Anoptichthys jordani (Characidae). Price, N. N. and Mensinger, A. F. (1999). Predator–prey interactions of J. Comp. Physiol. 143, 375-381. juvenile toadfish, Opsanus tau. Biol. Bull. 197, 246-247. Wilson, C. A., Dean, J. M. and Radtke, R. (1982). Age, growth rate and Richmond, H. E., Hrabik, T. and Mensinger, A. F. (2004). Light intensity, feeding habits of the oyster toadfish, Opsanus tau (Linnaeus) in South prey detection and foraging mechanisms of age-0 year yellow perch. J. Fish Carolina. J. Exp. Mar. Biol. Ecol. 62, 251-259. Biol. 65, 195-205. Wubbels, R. J., Kroese, A. B. and Schellart, N. A. (1993). Response Russell, I. J. (1971). The role of the lateral-line efferent system in Xenopus properties of lateral line and auditory units in the medulla oblongata of the laevis. J. Exp. Biol. 54, 621-641. rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 179, 77-92. Russell, I. J. and Roberts, B. L. (1974). Active reduction of lateral-line Zar, J. H. (1984). Biostatistical Analysis. Englewood Cliffs, NJ: Prentice- sensitivity in swimming dogfish. J. Comp. Physiol. 94, 7-15. Hall. THE JOURNAL OF EXPERIMENTAL BIOLOGY http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Experimental Biology The Company of Biologists

Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus)

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0022-0949
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10.1242/jeb.01766
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The Journal of Experimental Biology 208, 3441-3450 Published by The Company of Biologists 2005 doi:10.1242/jeb.01766 Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus) 1,2 2,3 1,2, Lucy M. Palmer , Max Deffenbaugh and Allen F. Mensinger * 1 2 Biology Department, University of Minnesota Duluth, Duluth, MN 55812, USA, Marine Biological Laboratory, Woods Hole, MA 02543, USA and ExxonMobil Upstream Research Company, PO Box 2189, Houston, TX 77252, USA *Author for correspondence (e-mail: [email protected]) Accepted 28 June 2005 Summary Inductive neural telemetry was used to record from toadfish (28·cm standard length; 33·cm total length) were microwire electrodes chronically implanted into the only able to detect mobile prey that approached within anterior lateral line nerve of the oyster toadfish, Opsanus approximately 40% of their body length. Both tau (L.). The lateral lines of free-ranging toadfish were spontaneously active and silent afferent fibers also stimulated by the swimming movements of a prey fish experienced a dramatic increase in firing during (Fundulus heteroclitus), and the corresponding neural predatory strikes, indicating that the fibers were not activity was quantified. Both spontaneously active and inhibited during rapid body movement. This study silent afferent fibers experienced an increase in neural investigates, for the first time, the neural response of the firing as the prey approached the lateral line. Activity was anterior lateral line to prey stimuli in free-ranging fish. evoked when the prey fish approached to within 8–12·cm of the neuromast, with increases in nerve firing rates directly correlated with diminishing distance. Thus, adult Key words: lateral line, telemetry, prey, toadfish, Opsanus tau. Introduction To enhance the interpretation of their environment, fish and distributions of local particle activity, alternating eddies and aquatic amphibians have evolved a lateral line system that slightly deformed vortex rings (Blickhan et al., 1992; Muller, detects displacements in the local water field. Neuromasts are 1996). Information about the direction and temporal scale of the basic unit of the lateral line system and consist of bundles fish movement can be contained in these trails (Hanke et al., of mechanoreceptive hair cells, which are comprised of a single 2000), which can persist in the water column for several kinocilium and numerous stereovilli protruding into a minutes (Hanke and Bleckmann, 2004). However, since the gelatinous cupula. The hydrodynamic properties of the chain of vortices generated by fish movement is difficult to neuromast act as a mechanical filter for sensory hair cells (van recreate and/or present during standard neurophysiological Netten, 1991). Hair cells are grouped into neuromasts located preparations, the activity of the lateral line in response to free- either upon the skin surface (superficial neuromasts) or swimming prey has been difficult to quantify. Instead, enclosed within subdermal canals (canal neuromasts). Canal vibrating spheres have been used historically as stimuli for the neuromasts function as water acceleration detectors, and lateral line (Wubbels et al., 1993; Muller, 1996; Coombs, 1999; superficial neuromasts act to determine water velocity (Kroese Kanter and Coombs, 2003). While instrumental in determining and Schellart, 1992). neuromast characteristics (frequency and directional Behavioral and electrophysiological experiments have sensitivity), pure stationary dipole-like stimuli are rarely illustrated that the lateral line functions in schooling behavior encountered in nature. (Partridge and Pitcher, 1980), rheotaxis (Montgomery et al., The detection of biologically relevant stimuli must often be 1997) and localization of underwater objects (Weissert and von accomplished during self-generated movement (e.g. Campenhausen, 1981). The lateral line has also been shown to swimming, ventilation). Recent studies conducted by Palmer receive water displacements generated by moving prey et al. (2003) indicate that the primary afferents of the anterior (Saunders and Montgomery, 1985; Montgomery and lateral line were stimulated during swimming and ventilatory Macdonald, 1987; Montgomery et al., 1988; Bleckmann and movements. Various studies have shown that lateral line Topp, 2003; Pohlmann et al., 2004). The great diversity in fish filtering during intense stimuli may be performed in higher body plan and swimming strategies can generate extremely brain regions. Tricas and Highstein (1990, 1991) identified complex hydrodynamic trails consisting of unpredictable efferent modulation of lateral line activity when toadfish THE JOURNAL OF EXPERIMENTAL BIOLOGY 3442 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger viewed live prey, and Montgomery and Bodznick (1994) and paralyzed with an intramuscular injection of a 0.01% –1 indicated that the lateral line medullary nuclei contain an solution of pancuronium bromide (600·g·kg ; Sigma). An adaptive filter capability that cancels input consistently incision was made through the dorsal musculature overlying associated with an animal’s own movements. the sagittal crest, and the muscle was retracted. A small The operating range of the lateral line system has been craniotomy was performed lateral to the sagittal crest and reported to be one to two body lengths (Denton and Gray, posterior to the transverse crest to expose the anterior ramus 1983; Kalmijn, 1988; Coombs, 1999; Braun and Coombs, of the anterior lateral line nerve. The electrode was inserted 2000). However, to accurately quantify the range and into the nerve just prior to its exit from the braincase. Potentials sensitivity of the lateral line to natural stimuli, neural activity were differentially amplified (Dagan, Minneapolis, MN, USA) must be monitored from an unconstrained teleost in quasi- and monitored on a portable computer using Chart5 for natural settings. Recording neural activity from free-swimming Windows software (ADInstruments, Colorado Springs, CO, fish has been complicated by the need for electrode stability USA). The two channels that provided the highest fidelity and/or a suitable telemetry device. Terrestrial telemetry modes signal were chosen for the experiments. Once a candidate fiber such as infrared light or radio waves are rapidly attenuated in was located, the fish was left undisturbed for 30·min to ensure seawater and are ineffective. The development of an inductive fiber stability. neural telemetry system allows the recording of neural Cyanoacrylate gel (Pacer Technology, Rancho Cucamonga, responses from free-ranging toadfish (Mensinger and CA, USA) was used to affix the electrode to the skull and seal Deffenbaugh, 1998, 2000; Palmer and Mensinger, 2004). This the craniotomy. The muscle was restored to its original study reports the activity of the lateral line in response to free- position, and the muscle, faschia and epidermis were swimming prey. individually sutured to provide a watertight seal over the craniotomy and around the transdermal electrode lead. The differential amplifier was disconnected from the electrode, and Materials and methods the cylindrical telemetry tag (15·mm38·mm, diameter Animal care length; 8·g) was inserted into the waterproof electrode Adult toadfish [~33·cm total length (TL); 28±1.4·cm connector. The tag was sutured parallel to the dorsal fin on the standard length (SL); 675±46·g wet mass; means ± S.E.M.] of dorsal surface of the fish. either sex were obtained from the Marine Biological Neural recordings Laboratory (MBL), Woods Hole, MA, USA. Fish were housed in large flow-through seawater tanks maintained at 20°C and Chronic extracellular recordings from lateral line primary fed squid and bait fish. All animal care and experimental afferent fibers were obtained using an inductive telemetry procedures conformed to institutional animal care protocols. system (Mensinger and Deffenbaugh, 1998, 2000; Palmer and Mensinger, 2004). In brief, the inductive telemetry system Microwire electrode consists of a transmitter tag and receiver coils. The tag Microwire electrodes consisting of three strands of insulated transmits the neural signal as a frequency-modulated magnetic 20·m-diameter 10% platinum/iridium wire (Sigmund Cohn field (90·kHz carrier, 20·kHz bandwidth), which is detected by Corp., Mt Vernon, NY, USA) were custom fabricated for each receiver coils embedded in a recharging habitat and stage implantation. Each microwire strand was affixed to hard silver- (RECHABS). To recharge the tag, the RECHABS produces an plated copper multistranded wire (25·m diameter) with oscillating magnetic field (50·T, 200·kHz), and the tag stores conductive silver paint (Silver Print Paint, GC Electronics, energy from this field in its capacitors. The RECHABS Rockford, IL, USA). The multistranded wire was attached to consists of a cylindrical habitat (12·cm30·cm, internal silver wire (320·m) that terminated into a multipin underwater diameter  length) that opens onto an octagonal stage (16·cm connector. The anterior portion of the microwires was threaded per side; Fig.·1). The RECHABS can both receive the through a 1·mm length of polymide tubing (180·m outer telemetry signal from the tag and recharge the tag when the tag diameter; A-M Systems Inc., Carlsborg, WA, USA) to maintain is within the habitat or up to a height of approximately 15·cm the recording sites in proximity. Any exposed wire/connections above the stage. The tag can be fully charged in less than 30·s were encased in medical device adhesive (Loctite 3341; Henkel and will provide telemetry for 5·min. Loctite Corp., Rocky Hill, CT, USA) and cured with ultraviolet Immediately after surgery, the fish were placed in an opaque light (ELC #660; Electro-lite Corp., Danbury, CT, USA). The fiberglass experimental tank (90·cm45·cm, width  length; impedance of each electrode channel was determined with an 15·cm water depth) and left undisturbed for a minimum of impedance-test unit (FHC; Bowdoinham, ME, USA) using 90·min. The innervated neuromast location was determined by 1·kHz input frequency. Only electrodes with impedances monitoring neural activity while a small brush was gently run between 0.5 and 1.2·M were used. along the supraorbital or infraorbital lateral line. This allowed the innervated neuromast to be localized to within two or three Electrode implant end organs, or an area of approximately one cm . Fish were anesthetized by immersion in 0.005% tricaine (3- Killifish (Fundulus heteroclitus; 6–8·cm SL) were used as aminobenzoic acid ethyl ester; Sigma, St Louis, MO, USA) prey. To maximize predator–prey encounters, a circular THE JOURNAL OF EXPERIMENTAL BIOLOGY Lateral line sensitivity in toadfish 3443 distance between the neuromast and the intersection point of the nearside killifish pectoral fin with its body axis. A trial consisted of placing a free-swimming or tethered Fundulus into the arena and monitoring its swimming movements while concurrently recording toadfish lateral line activity for up to 10·min. An encounter consisted of a Fundulus hovering for >500·ms in the same position that was within 20·cm of the innervated neuromast during a trial. Five to 12 trials were conducted per toadfish, with up to 119 encounters recorded per trial. To compare activity between H fibers, firing rates were normalized according to the maximum firing rate elicited by prey movements that was recorded in each trial. Although the microwires often yielded multiunit activity, fiber discrimination was usually limited to a single unit that yielded the greatest action potential amplitude and was clearly 45 cm discernible from other units. To verify that the same unit was consistently recorded during an experiment, individual fibers were distinguished using rigorous waveform analysis (Spike2) in addition to spike amplitude. During one implant, two units Fig.·1. Dorsal view of the experimental arena. The recharging habitat were discovered to be clearly distinguishable based on and stage (RECHABS) consists of the cylindrical habitat (H) and amplitude and waveform analysis, and both fibers were octagonal stage (S). Neural telemetry and tag recharging could individually analyzed during the trial. transpire when the fish was in the habitat or over the stage. The black The streamlined telemetry tag only added 1% to toadfish circle (arrow) represents an opaque barricade that restricted the prey body mass and its attachment did not have noticeable effects and the toadfish to the stage area. Fish movements were recorded with on behavior. Normal ventilation rates and equilibrium returned an overhead video camera (C). Drawing is not to scale. within 30·min of anesthetic withdrawal, and swimming activity resumed within two hours post-surgery. Recent work has plastic barricade surrounded the stage and restricted the shown that the sensitivity of the anterior lateral line to killifish to the RECHABS area. Prey that did not approach the mechanical stimuli is restored within 90·min of anesthetic toadfish within 15·min were anesthetized (0.0001% MS-222), withdrawal (Palmer and Mensinger, 2004), and therefore and a barbless fish hook (size 6) attached to monofilament experiments were not initiated until a minimum of two hours (1·kg test) was inserted between the premaxilla and maxilla following anesthetic removal. During all trials, toadfish were bone of the killifish. Once the tethered Fundulus recovered monitored for abnormal physiological (respiration rate) and normal swimming activity, they were placed in the behavioral (sudden movement, tail contraction) changes experimental tank. Sufficient slack was maintained in the before, during and after the application of the magnetic field, tether to allow normal swimming movements; however, the and no discernible effects were observed. Previous studies tether allowed the fish to be directed towards the toadfish (Mensinger and Deffenbaugh, 1998, 2000; Palmer and when necessary. Mensinger, 2004) demonstrated that the magnetic field does The telemetry signals were recorded up to four days post not affect neural activity or behavior in the toadfish. electrode implantation and stored on a portable computer using Prey stimulus Chart5 software and analyzed offline with Spike2 software (Cambridge Electronic Design, Cambridge, UK). Still-water trials were conducted with 8·cm SL Fundulus in Predator–prey interactions were simultaneously recorded on a large rectangular tank (2.5·m1.2·m0.5·m) with water –1 videotape (30·frames·s ; Sony Digital Handycam, Sony depth maintained at 20·cm. Water velocities generated by Electronics USA, Oradell, NJ, USA) that was synchronized hovering Fundulus were calculated by digital particle tracking with the neural telemetry system and analyzed frame by frame velocimetry. Fluid flow around the fish was illuminated by a using DV Shelf video frame capture and Scion Imaging horizontal laser sheet, 0.5·mm thick, and imaged from above software (Scion Corp., Frederick, MD, USA). Killifish with a high-resolution digital video camera (Kodak ES 1.0, movement alternated between caudal-fin-mediated forward 1008·pixels1018·pixels). The flow was seeded with swimming and stationary positioning via 2–3·Hz oscillation of 20–40·m-diameter neutrally buoyant fluorescent particles. the pectoral fins. Because the various fins and swimming For further details, refer to Anderson et al. (2001). motions of fish produce differing stimuli of varying intensity Statistical analysis (Gibb et al., 1994; Drucker and Lauder, 2001), neural activity was only quantified when the prey hovered in the same location All statistical analysis was performed using GraphPad for greater than 500·ms. Prey distance was defined as the Software (San Diego, CA, USA) or SigmaStat for Windows THE JOURNAL OF EXPERIMENTAL BIOLOGY 3444 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger version 3.10 (Systat Software, Inc., Richmond, CA, USA). All data represent mean values ± 1 S.E.M. unless otherwise indicated. Fiber activity during an encounter was binned into 2·cm intervals (distance of Fundulus fin origin to innervated neuromast). As the range of activity for the silent fibers was moderate (0–17·Hz), a one-way analysis of variance (ANOVA) was used to determine differences in spike activity among the four fibers during prey encounters. For the * spontaneous active fibers, firing rates were normalized according to the maximum firing rate elicited by prey movements that was recorded in each fiber during a trial. The 2D Graph 5 resulting percentages were transformed using the arcsine function (Zar, 1984), and a one-way ANOVA was used to determine differences in the transformed data for fiber activity for the combined five spontaneous active fibers. Samples were tested for normality using the method of Kolmogorov and Smirnov. Bartlett’s test was used to determine the use of parametric or non-parametric testing. Results Two types of lateral line fibers were identified. Silent fibers (N=4) did not display any spontaneous activity and were only activated by water movement. Their average sustained firing rate to prey movement ranged from 3 to 5·Hz, which was ~27% of the fibers’ maximal evoked response. Spontaneous active fibers (N=5) were of the irregular type (Tricas and Highstein, Control <2 2–4 4–6 6–8 8–10 10–12 12–14 1991) and had an average discharge rate of ~47·Hz in the Distance (cm) absence of stimulation. Prey movements stimulated these fibers Fig.·2. The mean normalized neural firing rates of (A) silent (N=4) to firing frequencies approximately 65% of their maximum and (B) spontaneously active afferent fibers (N=5) of the anterior firing rate. lateral line are plotted versus the distance of the innervated As the distance between the prey and neuromast diminished, neuromasts to the prey. All firing rates were normalized according to silent fibers were stimulated to fire (Fig.·2A). The greatest range the maximum firing rate recorded during each trial. Neural activity at which prey stimulated a silent fiber was 11·cm. Spontaneous was analyzed only when the prey fish was at the same location for fibers showed similar characteristics, with activity significantly greater than 500·ms. All distances were measured from the insertion increasing (ANOVA, P<0.05) above resting background levels point of the nearside prey pectoral fin to the neuromast that was at prey distances of up to 4·cm from the neuromasts (Fig.·2B). innervated by the recording. Asterisks indicate significantly different Prey at distances between 4 and 8·cm stimulated firing rates means from controls (ANOVA). The broken horizontal line in B above background levels; however, at distances greater than represents the mean normalized spontaneous firing rate from spontaneously active fibers. 8·cm, the presence of prey did not lead to elevated rates. Fig.·3. The probability of a silent fiber (triangles) firing during a prey encounter and the probability of a spontaneously active fiber 100 Spont. >1 S.D. increasing its discharge rate one (filled circle) or two (open circle) Spont. >2 S.D. standard deviations above its spontaneous discharge rate during Silent a prey encounter is plotted versus prey distance. If the silent fiber fired during the event, it was considered stimulated, and the 60 probability of the silent fibers firing was calculated as: (stimulated encounters/total encounters)100. If the firing activity of the spontaneously active fibers firing increased one and/or two standard deviations above its mean resting discharge rate it was considered stimulated and the probability was calculated as: (stimulated encounters >1·S.D./total encounters)100 and (stimulated encounters >2·S.D./total encounters)100. The data represent the summary of all trials for each fiber class, and each <2 2–4 4–6 6–8 8–10 10–12 12–14 >14 point represents a minimum of 15 trials at each distance. Prey Distance (cm) distance was binned into 2·cm segments. THE JOURNAL OF EXPERIMENTAL BIOLOGY Probability of firing (%) Normalized firing rate (% of maximum) Lateral line sensitivity in toadfish 3445 20 A Fig.·4. The activity of a silent, afferent fiber innervating a superficial neuromast on the infraorbital lateral line, as monitored during prey movement. (A) The distance (cm) of the prey fish from the recorded neuromast. (B) The full neural waveform from the anterior lateral line nerve that was transmitted via inductive telemetry. Although multiunit activity is visible in the trace, only the fiber with the greatest amplitude of action potential was used for data analysis. The fiber had no spontaneous activity 25 μV and exhibited maximum firing (~10·Hz) when the prey 20 s fish was within 1·cm of the neuromast. Small fluctuations in action potential frequency may be more valuable for prey detection for the toadfish than statistically significant changes. For silent fibers, the probability of a silent fiber firing during an encounter was plotted versus prey distance (Fig.·3). Silent fibers fired greater than 60% of the time when prey was located within 4·cm of the neuromast. This probability decreased to approximately 20% between 6 and 12·cm, and prey located further than Toadfish 12·cm failed to stimulate silent fibers. For spontaneous fibers, determining small fluctuations in action potential frequency was not as clear, as spontaneous discharge rates could drift by 5–10% during a trial. Therefore, Fig.·3 includes the probability of spontaneous fibers firing one and/or two standard deviations above their resting discharge rate during an encounter versus prey distance. Thus, even after including a less rigorous benchmark (1 S.D.), the probability of a spontaneous fiber reacting to the prey during an encounter continues to decline sharply with distance. Fig.·4 shows the neural activity in a silent lateral line fiber correlated with the position of a free-swimming Fundulus during a 5·min trial. Both transient swimming and hovering evoked a neural response when the prey fish approached within 6·cm of the neuromast; however, movement outside this range did not induce firing. Activity for a silent anterior lateral line fiber innervating a superficial neuromast on the right infraorbital lateral line of a toadfish is illustrated in Fig.·5. The fiber was unresponsive at prey distances greater 33 µV 100 ms than 10·cm; however, activity was evoked (~5·Hz) when the prey approached to within 3.5·cm of the neuromasts. As Fig.·5. Neural activity during the approach of a single prey fish. The the prey closed to within 1·cm, firing rate increased to ~10·Hz. diagram depicts the head of the toadfish projecting out of its habitat The neural response of a spontaneously active fiber and a and the sequential positions of the approaching prey: (A) 10·cm; (B) silent fiber to hovering prey is illustrated in Fig.·6. Both fibers 3.5·cm; (C) 1.0·cm. Images were reconstructed from single video innervated superficial neuromasts located on the infraorbital frames. The letter next to the prey fish corresponds to neural activity line of the anterior lateral line. As prey approached within from a superficial neuromast on the suborbital portion of the 8·cm, both fibers experienced an increase in neural activity. infraorbital lateral line. Although multiunit activity is visible in the The neural activity during predatory strikes was recorded in trace, data analysis was restricted to the fiber with the greatest four fibers from three fish during 20 prey strikes. The firing amplitude of action potential. THE JOURNAL OF EXPERIMENTAL BIOLOGY Distance (cm) Telemetry Habitat 3446 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger (7) (7) (1) (6) SP1 SP2 SP3 SL1 0 5 10 15 20 25 30 Fig.·7. Mean firing rate (± 1 S.E.M.) of four anterior lateral line afferents fibers [three spontaneous (SP) and one silent (SL)] immediately before (open) and during (filled) a toadfish prey strike. 80 Numbers above the bars represent the number of prey strikes that were averaged for each fiber. The water velocities generated by pectoral and caudal fin movement of 8·cm SL Fundulus were extremely complex (Fig.·9). Maximum water velocities generated by the pectoral –1 fins during hovering were approximately 5·cm·s , with water displacement rapidly attenuating with distance from the body –1 axis. Velocities between 2 and 3·cm·s were often detectable within 2–3·cm of the fin’s insertion; however, at distances 0 5 10 15 20 –1 greater than 5·cm, water movement remained less than 1·cm·s . Distance (cm) Fig.·6. Firing rates of (A) a spontaneously active afferent fiber and (B) a silent fiber in response to a prey fish located at variable distances Discussion from the neuromast. Both fibers innervated superficial neuromasts. All Oyster toadfish are benthic fish that inhabit most estuaries distances were measured from the insertion point of the nearside prey along the Atlantic Coast of the USA (Gudger, 1910). They are pectoral fin to the neuromast that was innervated by the recording. The broken horizontal line in A represents the mean spontaneous activity. All firing rates were normalized according to the maximum firing rate elicited by prey movements during each trial. Neural activity was analyzed only when the prey fish was at the same location for greater than 500·ms. activity of the fibers increased during all strikes (Fig.·7). The 1 s spontaneously active fibers (N=3) experienced a 9-fold average increase in firing activity above resting discharge rates. These B increases were much greater than the maximum firing activity Strike Retained Expelled evoked by prey movements in the same fibers. Neural activity from a single fiber during a prey strike is illustrated in Fig.·8. The killifish approached the toadfish at a constant velocity –1 (2·cm·s ) from the contralateral side of the neuromast, and the toadfish struck when the prey was directly in front of the 100 ms mouth, 2·cm from the premaxilla (Fig.·8B). During the strike, Fig.·8. Neural activity from an afferent anterior lateral line fiber the toadfish moved forward slightly (1·cm) and opened its before, during and after a prey strike. Vertical lines on the trace mouth to engulf the prey fish. The prey was retained in the indicate individual action potentials from a single fiber that were toadfish’s mouth for 1300·ms before being expelled. discriminated based on spike amplitude. The arrows indicate initiation Both silent and spontaneously active fibers were observed of opercular contraction for each ventilation cycle. The time during to continually fire in phase with the toadfish’s ventilation cycle. the strike, capture and subsequent expulsion of the prey is boxed in The fibers fired regularly with each ventilation cycle and were A, and this interval is expanded in B. The prey was retained in the never observed to become habituated (Fig.·8). mouth of the toadfish for approximately 1·s before being expelled. THE JOURNAL OF EXPERIMENTAL BIOLOGY Normalized firing rates (% of maximum) Firing rate (Hz) Lateral line sensitivity in toadfish 3447 Fig.·9. The picture shows the water movements produced by an 8·cm SL Fundulus heteroclitus taken with a digital video camera at 10001000 pixel resolution. Each velocity vector represents the average of a 32·pixel32·pixel window, and the center of each window is spaced 16·pixels apart. Velocities are presented by pseudo color images. Scale bar, 2·cm. predominately ambush predators that prey largely upon limit the disparity in Fundulus swimming characteristics, data crustaceans and small fish (Chrobot, 1959; Schwartz and analysis was restricted to periods when prey were hovering in Dutcher, 1963; McDermott, 1964; Phillips and Swears, 1979; the same location for greater than 500·ms. Consequently, much Wilson et al., 1982; Price and Mensinger, 1999; Mensinger et of the data analysis characterizes lateral line activity in al., 2003). Field and laboratory observations indicate that response to oscillation (3·Hz) of the killifish pectoral fin. toadfish spend the majority of their time in small caves or Digital particle tracking velocimetry allowed analysis of the crevices with their head facing outward and will often remain water velocities generated by hovering Fundulus. Retraction of motionless prior to launching a ballistic strike at nearby prey. the pectoral fins in hovering killifish produced maximum water –1 Therefore, with the exception of water currents generated by velocities of approximately 5·cm·s within the arc traveled by respiratory activity and prey strikes, there exists little self- the fin. These velocities rapidly attenuated with distance from –1 generated interference for their lateral line. the fin’s origin. Velocities between 2 and 3·cm·s were often As fish swimming combines the locomotion of several detectable within 3·cm of the fin; however, at distances greater independent fin systems (Drucker and Lauder, 2001), the than 5·cm from the fin’s origin, water movement declined to –1 generated hydrodynamics can be complex. A swimming fish less than 1·cm·s before fading into the background –1 leaves a hydrodynamic trail in the water that can persist several (0.1·cm·s ). Caudal fin motion disrupted a larger volume of minutes after its passage (Hanke et al., 2000; Hanke and water over greater distances. However, as these deflections Bleckmann, 2004). Experiments conducted by Enger et al. were lateral and posterior to the pectoral fin currents, there (1989) concluded that the lower-frequency accelerations appeared to be little potential for constructive inference resulting from the prey’s motion are biologically of utmost between the two sources. As data analysis was restricted to importance in lateral line detection. The killifish was chosen hovering, during which the caudal fin remained relatively for these experiments as it is natural prey for the toadfish stationary, pectoral fin movements were the primary stimulus (Chrobot, 1959). Its swimming behavior alternates between source. forward propulsion mediated by body and caudal fin Previous studies have indicated the persistence of movement, and stationary hovering using pectoral fin hydrodynamic trails several minutes following fish passage oscillation. Caudal fin movement generally creates greater (Hanke et al., 2000; Hanke and Bleckmann, 2004). Slowly water displacement and may consequently provide a larger decaying wakes could complicate determining if the lateral line stimulus for the lateral line. However, as toadfish is reacting to current prey motion or residual wakes. Fig.·4 predominantly strike at approaching prey, bow waves or illustrates a typical trial during which the prey moved forward fin (pectoral and/or pelvic) displacement may be more throughout the arena. The silent fiber ceased to fire when the important than caudal movements or subsequent wakes. To prey moved greater than 10·cm away from the toadfish. If the THE JOURNAL OF EXPERIMENTAL BIOLOGY 3448 L. M. Palmer, M. Deffenbaugh and A. F. Mensinger hydrodynamic trails continued to persist at a physiological level, the fiber should have continued to fire after the prey vacated the area. However, the previous studies examined wakes generated by rapidly swimming fish which would create greater and more persistent, water disturbance than Fundulus. 30 Alternatively, the lateral line fibers could have become habituated to a persistence stimulus and ceased to respond. However, when lateral line fibers were stimulated for up to 60·s with continuous water flow, habituation was not evident (Palmer and Mensinger, 2004), indicating that a dispersing stimulus and not habituation was responsible for the return of <1 1–2 2–3 3–4 4–5 >5 lateral line activity to baseline levels. Distance (cm) Several studies have suggested that the lateral line detects Fig.·10. The frequency of attacks by 8·cm SL toadfish at 2·cm SL prey up to a distance of 1–2 body lengths (Denton and Gray, guppies is plotted versus the distance between the two fish at the time 1983; Kalmijn, 1988; Coombs, 1999; Braun and Coombs, the toadfish launched its attack. The total number of attacks analyzed 2000). However, many lateral line studies have been performed was 78. Modified from Price and Mensinger (1999). with vibrating probes, which may generate a stronger stimulus than prey and do not reflect the complexity of water currents generated by natural stimuli. The neural telemetry system allowed lateral line activity to be monitored in the presence of reacts to the prey rather than when detection occurs, they provide free-swimming prey. The distance at which prey movement further support for close-range detection. Year one toadfish modulated the toadfish lateral line was shorter than the range (8·cm SL; 10·cm TL) feeding on small guppies (2·cm SL) during usually proposed for other species. Both spontaneous and silent daylight trials did not launch strikes at prey that were greater fibers of the toadfish anterior lateral line were stimulated by than 5·cm from the toadfish (Fig.·10; Price and Mensinger, prey pectoral fin oscillation at distances from the sensory 1999). These attacks were probably mediated by both visual and neuromast of less than half the toadfish body length. The mechanical cues, and reaction distances under low light detection range represented the distance between neuromast conditions would be predicted to be shorter and more accurate location and pectoral fin insertion; however, the nearest distance indicators of lateral line range. Ongoing studies in juvenile between predator and prey (often the head of the killifish and toadfish indicate that both reaction distance and attack range are the body of the toadfish) was frequently 2·cm closer. less in the dark than the light (L. Lundeen and A. F. Mensinger, Caution must be applied in two areas of our data unpublished) and are consistent with studies by Enger et al. interpretation. As the recordings were restricted to individual (1989), New and Kang (2000) and Richmond et al. (2004) that fibers in a localized region of the anterior lateral line, it is found that predatory fish without visual cues reacted to prey at possible that other regions may contain neuromasts more distances of less than 50% of the predator’s body length. sensitive to prey movements. Alternatively, central integration Although the lateral line can contribute significant from multiple neuromasts may function to increase resolution information for prey localization, due to its short range it is and sensitivity and project the detection distance further than evident that other systems are important in locating distant an individual neuromast. Additionally, slight changes in firing prey. The far hydrodynamic fields of moving objects are frequency may provide important information for the fish but hypothesized to be mediated by the inner ear (Kalmijn, 1988). fail to be statistically significant, especially when averaged Additionally, behavioral and physiological experiments have over different neurons and fish, as in the current study. For illustrated that tactile, chemosensory, hydrodynamic and visual example, in the 4–8·cm range for spontaneous fibers, the fibers stimuli are capable of guiding prey capture (Montgomery et fired well above background discharges and undoubtedly al., 2002). provided information about the prey. However, using less The oyster toadfish possesses an anterior lateral line rigorous statistical analysis (1 S.D. above spontaneous rate) did dominated by superficial neuromasts (Clapp, 1898). Although not greatly extend the maximum detection distance. It remains behavioral experiments in other species have indicated that possible that small, transient fluctuations in lateral line activity prey detection and localization is mediated by canal that were outside our resolution ability encode for prey neuromasts (Coombs et al., 2001), it appears that the afferent distance and extend detection distance. However, the response fibers innervating the superficial neuromasts of the toadfish dynamics of the silent fibers, which did not fire in the absence anterior lateral line are responsive to the stimuli produced by of stimulus, provide support for the limited range of the lateral prey. Consequently, although canal neuromasts may provide line as these fibers failed to fire until the prey approached important prey localization information, superficial neuromasts within 11·cm. are able to detect the low-frequency water displacements Predator–prey interactions are also consistent with lateral line generated by prey and contribute to near-field prey detection. sensitivity recorded in toadfish. Although behavioral Efferent innervation of lateral line hair cells has been observations are limited to discerning when the predator visibly hypothesized to inhibit afferent firing (Russell and Roberts, THE JOURNAL OF EXPERIMENTAL BIOLOGY Attack frequency (%) Lateral line sensitivity in toadfish 3449 1974) and prevent depletion of transmitter from lateral line hair line organs of the top minnow Aplocheilus lineatus. Naturwissenschaften 68, 624-625. cells during locomotion or rapid movements (Russell, 1971). Blickhan, R., Krick, C., Zehren, D., Nachtigall, W. and Breithaupt, T. Tricas and Highstein (1990) illustrated that the lateral line (1992). Generation of a vortex chain in the wake of a subundulatory experienced transient inhibition when toadfish were allowed to swimmer. Naturwissenschaften 79, 220-221. Braun, C. B. and Coombs, S. (2000). The overlapping roles of the inner ear view live Fundulus in an adjacent aquarium and that in a and lateral line: the active space of dipole source detection. Phil. Trans. R. minority of fibers there was a decrease in neural activity in Soc. Lond. B 355, 1115-1119. anterior lateral line afferent fibers during a predatory strike. Chrobot, R. J. (1959). The feeding habits of the toadfish (Opsanus tau) based on an analysis of the contents of the stomach and intestine. Master’s thesis. However, recent studies have illustrated the ability of hair cells University of Maryland. to release neurotransmitters for prolonged periods with little Clapp, C. (1898). The lateral line system of Batrachus tau. J. Morph. 15, 223- exhaustion (Moser and Beutner, 2000; Trussell, 2002). 265. Coombs, S. (1999). Signal detection theory, lateral-line excitation patterns and Evidence of efferent modulation (reduction or cessation of prey capture behaviour of mottled sculpin. Anim. Behav. 58, 421-430. nerve activity) was not observed during any trial. The length Coombs, S., Braun, C. B. and Donovan, B. (2001). The orienting response of our trials and the inclusion of intermittent mechanosensory of Lake Michigan mottled sculpin is mediated by canal neuromasts. J. Exp. Biol. 204, 337-348. stimulation may have occluded our ability to detect efferent Denton, E. J. and Gray, J. (1983). Mechanical factors in the excitation of modulation. However, the lack of inhibition of toadfish clupeid lateral lines. Proc. R. Soc. Lond. B. 218, 1-26. neuromasts located near the operculum that were continually Drucker, E. G. and Lauder, G. V. (2001). Locomotor function of the dorsal fin in teleost fishes: experimental analysis of wake forces in sunfish. J. Exp. stimulated by opercular displacement (present study) or Biol. 204, 2943-2958. prolonged water current (Palmer and Mensinger, 2004) appears Enger, P. S., Kalmijn, A. J. and Sand, O. (1989). Behavioral investigations to indicate that efferent modulation was not common in our on the functions of the lateral line and inner ear in predation. In The Mechanosensory Lateral Line – Neurobiology and Evolution (ed. S. Coombs, sample population. H. Munz and P. Gorner), pp. 265-285. New York: Springer-Verlag. Both silent and irregular fibers experienced a dramatic Gibb, A. C., Jayne, B. C. and Lauder, G. V. (1994). Kinematics of pectoral increase in firing during a predatory strike. It is possible that fin locomotion in the bluegill sunfish Lepomis macrochirus. J. Exp. Biol. 189, 133-161. self-generated noise created during a predatory strike may be Gudger, E. W. (1910). Habits and life history of the toadfish (Opsanus tau). filtered by higher order neurons. Montgomery and Bodznick Bull. U.S. Bur. Fish. 28, 1071-1099. (1994) indicate that the lateral line medullary nuclei contain an Hanke, W. and Bleckmann, H. (2004). The hydrodynamic trails of Lepomis gibbosus (Centrarchidae), Colomesus psittacus (Tetraodontidae) and adaptive filter capability that cancels inputs consistently Thysochromis ansorgii (Cichlidae) investigated with scanning particle associated with an animal’s own movements. Further image velocimetry. J. Exp. Biol. 207, 1585-1596. experiments are required to determine decisively whether the Hanke, W., Brucker, C. and Bleckmann, H. (2000). The ageing of the low- frequency water disturbances caused by swimming goldfish and its possible lateral line conveys self-regulatory information during a relevance to prey detection. J. Exp. Biol. 203, 1193-1200. predatory strike. Kalmijn, A. J. (1988). Hydrodynamic and acoustic field detection. In Sensory In summary, the toadfish lateral line can detect transient Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp. 83-130. New York: Springer-Verlag. water displacement generated by natural prey. The distance at Kanter, M. J. and Coombs, S. (2003). Rheotaxis and prey detection in which stimulation occurred was less than 40% of toadfish body uniform currents by Lake Michigan mottled sculpin (Cottus bairdi). J. Exp. length. This is the first study that investigates the neural Biol. 206, 59-70. Kroese, A. B. and Schellart, N. A. (1992). Velocity- and acceleration- response of the anterior lateral line to prey stimuli in free- sensitive units in the trunk lateral line of the trout. J. Neurophysiol. 68, 2212- ranging fish and highlights the importance of the lateral line in near-field prey detection. McDermott, J. J. (1964). Food habits of the toadfish, Opsanus tau (L.), in New Jersey waters. J. Penn. Acad. Sci. 38, 64-71. Mensinger, A. F. and Deffenbaugh, M. (1998). Prototype rechargeable tag The authors wish to thank Tom Hrabik and John Nicols for for acoustical neural telemetry. Biol. Bull. 195, 194-195. helpful criticisms of the manuscript, and Beth Giuffrida for Mensinger, A. 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