Lateral line stimulation patterns and prey orienting behavior in the Lake Michigan mottled sculpin (Cottus bairdi)

Information contained in the spatial excitation pattern along arrayed sensors in the lateral line system of Lake Michigan mottled sculpin, as well as other surface-feeding fish and amphibians, is thought to play a fundamental role in guiding prey-orienting behaviors. However, the way in which prey location is encoded by the excitation pattern and used by the nervous system to direct orienting behaviors is largely unknown. In this study, we test the hypothesis that mottled sculpin use excitation peaks (local ‘hot spots’) to determine the somatotopic location of an artificial prey (vibrating sphere/dipole source) along the body surface. Dipole orientation (axis of sphere vibration re: long axis of the fish) is manipulated to produce excitatory peaks in different body locations without changing the actual sphere location. Our results show that orienting accuracy is largely independent of source orientation, but not source distance and that turning directions are not guided by local hot spots in the somatotopic activation pattern of the lateral line.     

Mechanosensory‐based orientation to elevated prey by a benthic fish

Lake Michigan mottled sculpin, Cottus bairdi, respond to both live and artificial (e.g., vibrating sphere) prey with an unconditioned movement towards the source of vibration, followed by a step‐by‐step approach and final strike at the source. In addition to these well‐studied, whole‐body movements along the horizontal plane of the substrate, sculpin exhibit a little‐studied behavior in which the vertical position of the fish's head can vary from being flush with the substrate to several cm's above the substrate. To test the hypothesis that sculpin can determine source elevation via mechanosensory cues, we measured head elevation of blinded fish as a function of source elevation and distance as fish approached a small (3 mm radius), 50 Hz vibrating sphere. At distances associated with pre‐strike positions (< 2 cm), head elevations were positively correlated with source elevation before but not after pharmacological blocking of the lateral line with CoCl₂. These results demonstrate that sculpin are able to determine source elevation using mechanosensory cues alone and that in the absence of visual and olfactory cues, vertical orientation of the head towards the source requires the lateral line system.     

Mechanosensory based orienting behaviors in fluvial and lacustrine populations of mottled sculpin ( Cottus bairdi )

We compared prey-orienting and rheotactic behaviors in a fluvial (Coweeta Creek) and lacustrine (Lake Michigan) population of mottled sculpin. Blinded sculpin from both populations exhibited unconditioned, mechanosensory based rheotaxis to low velocity flows. Whereas Lake Michigan sculpin generally showed increasing levels of positive rheotaxis to increasing velocities, Coweeta Creek sculpin show varying levels of positive rheotaxis at low to intermediate velocities and often reduced positive rheotaxis or even negative rheotaxis at the highest velocities (12?cm?s^?1). Blinded Lake Michigan, but not Coweeta Creek mottled sculpin exhibited an orienting response to a small (3?mm diameter) artificial prey (50?Hz vibrating sphere). In conclusion, the two populations differed in the strength and polarity of the rheotactic response at higher velocities and in their responsiveness to mechanosensory cues from epibenthic prey sources. These behavioral differences have most likely arisen from different learning experiences in different habitats and from the greater importance of visual cues to the Coweeta Creek mottled sculpin and mechanosensory cues to Lake Michigan mottled sculpin in the sensory guidance of orienting behaviors.     

Mechanosensory based orienting behaviors in fluvial and lacustrine populations of mottled sculpin (Cottus bairdi)

We compared prey-orienting and rheotactic behaviors in a fluvial (Coweeta Creek) and lacustrine (Lake Michigan) population of mottled sculpin. Blinded sculpin from both populations exhibited unconditioned, mechanosensory based rheotaxis to low velocity flows. Whereas Lake Michigan sculpin generally showed increasing levels of positive rheotaxis to increasing velocities, Coweeta Creek sculpin show varying levels of positive rheotaxis at low to intermediate velocities and often reduced positive rheotaxis or even negative rheotaxis at the highest velocities (12 cm s^-1). Blinded Lake Michigan, but not Coweeta Creek mottled sculpin exhibited an orienting response to a small (3 mm diameter) artificial prey (50 Hz vibrating sphere). In conclusion, the two populations differed in the strength and polarity of the rheotactic response at higher velocities and in their responsiveness to mechanosensory cues from epibenthic prey sources. These behavioral differences have most likely arisen from different learning experiences in different habitats and from the greater importance of visual cues to the Coweeta Creek mottled sculpin and mechanosensory cues to Lake Michigan mottled sculpin in the sensory guidance of orienting behaviors.     

Dipole source localization by mottled sculpin. I. Approach strategies

Lake Michigan mottled sculpin respond to a chemically-inert vibrating sphere (a dipole source) with an initial orientation towards the source followed by a step-wise progression towards and final strike at the source. An analysis of videotape recordings of this behavior indicate that although pathways to the source varied, they tended to be influenced by the fish's position at signal onset. Fish heading toward the source at signal onset approached the source in an indirect fashion by either (a) keeping the source to one side in a smoothly arching path to the source or (b) alternating between keeping the source to the left and to the right. When the source was to the side of the fish at the time of stimulus onset, fish tended to approach the source in a more direct path. Most (79%) initial orienting responses placed the fish within 45° of the source, but response angles were not strongly correlated with initial source angle. Most (83%) unsuccessful strikes (misses) occurred when the source was directly in front of the fish (± 20°) and source angles associated with misses were significantly smaller than source angles associated with successful strikes. Approach strategies used by mottled sculpin in finding dipole sources appear to include (1) moving in a direction that increases the pressure difference along the head while keeping it consistently low (between 1 and 10 Pa) across the head, (2) narrowing the fish-to-source gap with each successive step in the pathway, (3) keeping the source lateralized (on average, 30° to one or the other side of the head) and (4) avoiding approach positions that are perpendicular to the flow line or that place the fish in the pressure null area of the dipole field. These results are consistent with the hypothesis that spatial excitation patterns along the lateral line system play a major role in encoding both source direction and distance. Accepted: 23 October 1996     

Non-visual feeding behavior of the mottled sculpin,Cottus bairdi,in Lake Michigan

Synopsis Field and laboratory experiments indicate that the mottled sculpin, Cottus bairdi, feed in the dark. Blinded sculpins feed on a variety of motile prey in the laboratory and show stereotyped responses to prey stimuli. The sculpins bite at moving inert objects, even if buried in substratum, indicating that they use their lateral line system to detect prey. Covering portions of the lateral line with an inert paste eliminates response to objects near the covered region of the lateral line. The sculpins can also detect prey (including inert objects) in a stream if the prey is upstream. Collection from two series of presunset, postsunset, presunrise, postsunrise, dives in Lake Michigan indicate nocturnal feeding by the mottled sculpin.     

Dipole source localization by the mottled sculpin II. The role of lateral line excitation patterns

Extracellular, single unit recording techniques were used to measure the responses of posterior lateral line nerve fibers to a 50-Hz dipole source that slowly changed its location along the length of the fish. The flow-field equations for a dipole source were used to model the pressure gradient pattern and thus, the expected excitation pattern along a linear array of lateral line receptor organs for different source locations. Finally, excitation patterns were similarly modeled along the left and right side of the fish's head for actual steps taken by sculpin in approach pathways to the 50-Hz dipole source. Spatial histograms of posterior lateral line nerve fiber responses to different locations of the dipole source could be predicted from pressure gradient patterns modeled from the flow-field equations, confirming that the modeling approach applied to behavioral results was a good predictor of excitation patterns likely to be encoded by the lateral line periphery. An examination of how modeled excitation patterns changed from one position to the next in typical approach pathways and how patterns differed between positions from which successful and unsuccessful strikes were launched suggests that approach and strike strategies can indeed be explained by the information available in excitation patterns. In particular, changes in the spatial distribution of pressure gradient directions (polarities), available only when the source is lateral (as opposed to directly in front of the fish), appear to enhance the ability of sculpin to determine source distance. Without such information, misses are more likely to occur and successful strikes are more likely to be launched from short distances only. Accepted: 23 October 1996     

Dipole source localization by mottled sculpin. III. Orientation after site-specific, unilateral denervation of the lateral line system

To test the hypothesis that spatial excitation patterns along the lateral-line system underlie source localization, we videotaped the orientation behavior of blinded mottled sculpin in response to a small dipole source (50-Hz vibrating sphere) before and after unilateral denervation of the lateral line system on different body regions (head, trunk and head + trunk). Approach pathways were qualitatively similar to those followed by normal intact animals. Abnormal behavior (turning in circles) was not observed. However, the frequency with which fish placed their intact side facing the source increased by 12–89%, depending on the denervation site. The angular accuracy of orientation decreased by 20° to 60° (100% to 370% change) depending on source location and region of lateral line denervated. Deficits tended to be site-specific. For example, unilaterally denervating lateral-line organs on the head resulted in less accurate orienting responses when the source was located on the denervated side of the head, but not on the opposite side of the head or on either side of the trunk. Site-specific deficits and the absence of abnormal approach pathways argue that animals are relying on a point-by-point spatial representation of source location along the sensory surface rather than computations based on bilateral comparisons. Accepted: 28 May 1998     

Comparisons of aquatic versus terrestrial predatory strikes in the pitviper, Agkistrodon piscivorus

Recent studies comparing terrestrial versus aquatic locomotion in animals have shown that changes in kinematics, muscular activation patterns, and performance across media are often dramatic. Surprisingly, however, despite the importance of feeding to the survival of most animals, few studies have compared differences in feeding behaviour between media. The present study compares prey-capture behaviour, strike success, strike velocity and acceleration, and prey-capture kinematics in a semi-aquatic pitviper (Agkistrodon piscivorus) when capturing both terrestrial (mice) and aquatic (fish) prey in a standardized laboratory setting. Strike velocity and acceleration did not differ significantly between media, but instead were positively correlated with initial prey distance. By contrast, the kinematics of terrestrial and aquatic strikes differed significantly in several aspects: max gape angle during the retraction phase, angular velocity of mouth closing during the strike, and the initial head angle before the strike. Terrestrial strikes were associated with higher gape angles during the retraction phase, higher angular velocities of mouth closure, and a more inclined head angle at the onset of the strike. Finally, strike success differed significantly between strike types, with terrestrial strikes being considerably more successful than aquatic strikes. Strike success likely differed due to the relatively slow mouth-closing velocity of aquatic strikes.     

Giving‐up densities and ideal pre‐emptive patch use in a predatory benthic stream fish

1. We used observational and experimental field studies together with an individual‐based simulation model to demonstrate that behaviours of mottled sculpin (Cottus bairdi) were broadly consistent with the expectations of Giving‐Up Density theory and an Ideal Pre‐emptive Distribution habitat selection model. 2. Specifically we found that: (i) adult mottled sculpin established territories within patches characterised by significantly higher prey densities and prey renewal rates than patches occupied by juveniles or randomly selected patches; (ii) patches abandoned by adult sculpin possessed significantly lower prey densities than newly occupied patches, although this was not true for juveniles; (iii) the observed giving‐up density (GUD) for adult sculpin (i.e. average prey density in patches recently abandoned) increased linearly with increasing fish size up to the average prey density measured in randomly selected patches (i.e. 350 prey items per 0.1 m²) and decreased with increasing sculpin density and (iv) juveniles rapidly shifted their distribution towards the highest quality patches following removal of competitively dominant adult sculpin. 3. These results provide the first evidence of the applicability of GUD theory to a stream‐dwelling organism, and they elucidate the underlying factors influencing juvenile and adult sculpin habitat selection and movement behaviours. Furthermore, optimal patch use, ideal pre‐emptive habitat selection and juvenile ‘floating’ provide behavioural mechanisms linking environmental heterogeneity in the stream benthos to density‐dependent regulation of mottled sculpin populations in this system.     

Toral lateral line units of goldfish, Carassius auratus, are sensitive to the position and vibration direction of a vibrating sphere

We recorded the responses of lateral line units in the midbrain torus semicircularis of goldfish, Carassius auratus, to a 50-Hz vibrating sphere and determined the unit's spatial receptive fields for various distances between fish and sphere and for different directions of sphere vibration. All but one unit responded to the vibrating sphere with an increase in discharge rate. Only a proportion (25?%) of the units exhibited phase-locked responses. Receptive fields were narrow or broad and contained one, two or more areas of increased discharge rate. The data show that the receptive fields of toral lateral line units are in many respects similar to those of brainstem units but differ from those of afferent nerve fibres. The responses of primary afferents represent the pressure gradient pattern generated by a vibrating sphere and provide information about sphere location and vibration direction. Across the array of lateral line neuromasts, the fish brain in principle can derive this information. Nevertheless, toral units tuned to a distinct sphere location or sensitive to a distinct sphere vibration direction were not found. Therefore, it is conceivable that the torus semicircularis uses a population code to determine spatial location and vibration direction of a vibrating sphere.     

Which way to turn? Effect of direction of body asymmetry on turning and prey strike orientation in starry flounder Platichthys stellatus (Pallas) (Pleuronectidae)

Starry flounder Platichthys stellatus , a rare polymorphic flatfish exhibiting a large-scale geographic cline in the frequency of right-eyed (dextral) and left-eyed (sinistral) morphs, was studied to investigate whether foraging behaviour (turning angle and prey strike orientation) differed between dextral and sinistral laboratory-raised juveniles. Platichthys stellatus foraging on brine shrimp Artemia sp. nauplii tended to strike dorsally at prey ('left' to an observer for dextral flounder and 'right' to an observer for sinistral flounder), although this effect was stronger for sinistral fish. This dorsal tendency also increased with body size. Non-strike behaviours (movements between strikes) were ventrally biased for both morphs. Maximum turn angles were larger for both morphs towards the dorsal side than the ventral side during prey strikes but were the same during non-strike behaviours. The positioning of the eyes of the juvenile starry flounder was skewed towards the dorsal midline rather than being symmetrically placed between dorsal and ventral margins on the eyed side of each fish. The migrating eyes of dextral fish, however, were significantly closer to the dorsal midline than in sinistral fish. This, in addition to the more dorsally oriented prey strikes in sinistral fish, suggests that the morphs are not simple behavioural mirror images of one another and therefore may differ ecologically.     

Influence of cruising and ambush predators on 3-dimensional habitat use in age 0 juvenile Atlantic cod Gadus morhua

Predators and prey often co-exist at high densities within the same habitat, yet the behavioural and spatial dynamics underlying this co-existence are not well known. To better understand small-scale, predator-prey co-occurrence, the spatial patterns and behaviour of age 0 juvenile cod Gadus morhua 75-88 mm SL and two of their known predators, age 2+ cod and short-horn sculpin Myoxocephalus scorpinus, were examined in two habitats (i.e., sand and eelgrass) using three-dimensional video analysis. Both habitat and predator type interacted to result in unique spatial patterns of prey. Spatial overlap between predators and prey was highest in open habitat in the presence of the cruising predator but lowest in the presence of sculpin in the same habitat. In eelgrass, age 0 cod avoided predators primarily along the vertical axis (i.e., distance off bottom). Age 0 cod stayed above eelgrass in the presence of sculpin but lowered themselves into the eelgrass while in the presence of predator cod. Anti-predator behaviour (i.e., predator-prey distance, prey cohesion and freezing) was significantly reduced over eelgrass compared to sand, suggesting eelgrass has lower ‘inherent risk’ than open habitats. However, predator consumption was similar across all treatments, suggesting that, 1) complex habitat also impairs the visual cues needed for anti-predator behaviour (e.g., schooling) and assessing the location of predators, and 2) predators change their behaviour with habitat to enhance their opportunities for finding and capturing prey.     

Seasonal feeding ecology of co-existing native and invasive benthic fish along a nearshore to offshore gradient in Lake Michigan

Relative abundance, diet composition and feeding strategy were determined for three benthic fish, the native deepwater sculpin Myoxocephalus thompsonii (Girard, 1851) and slimy sculpin Cottus cognatus (Richardson, 1836), and the invasive round goby Neogobius melanostomus (Pallas, 1814), along a nearshore to offshore gradient in southeastern Lake Michigan during March–December 2010, 2015, and 2016. Round goby were most abundant in the nearshore (<25 m), slimy sculpin were most abundant in the transitional zone (35–65 m), and deepwater sculpin were most abundant in the offshore zone (>75 m). Despite a large degree of spatial separation, some species did overlap, with slimy and deepwater sculpin occurring in sympatry throughout the year in the offshore and transitional zones, and round goby overlapping with both sculpin species seasonally in the transitional zone. Deepwater sculpin exhibited specialization on Mysis diluviana in all depth regions. Slimy sculpin in the offshore reduced diet overlap with deepwater sculpin by specializing on fish eggs during spring and fall, whereas in the transitional depth zone, there was considerable overlap between sculpin species due to the high importance of Mysis in diets. The invasive round goby had a mixed diet, with some diet overlap with native sculpin, especially slimy sculpin, in the transitional zone. In the nearshore zone, round goby displayed a generalized diet with many prey contributing to the diet, but the average contribution of any prey was generally low. Spatial separation and variable feeding strategies help reduce, but not eliminate shared resource use amongst these benthic fish in Lake Michigan.     

Transformation of peripheral inputs by the first-order lateral line brainstem nucleus

Extracellular recording techniques were used to record the responses of medial nucleus cells and posterior lateral line nerve fibers in mottled sculpin, Cottus bairdi, and goldfish, Carassius auratus, to a 50-Hz dipole source (vibrating sphere). Responses were characterized in terms of (1) receptive fields that relate responsiveness (spike rate and phase-locking) to the location of the source along the length of the fish, (2) input-output functions that relate responsiveness to vibration amplitude for a fixed source location, and (3) peri-stimulus time histograms that relate responsiveness to time during a sustained period of vibration. Relative to posterior lateral line nerve fibers, medial nucleus cells in both species were similar in showing (1) lower spontaneous and evoked rates of spike activity, (2) greater degrees of adaptation, (3) greater heterogeneity in all response characteristics, and (4) evidence for inhibitory/excitatory interactions. Whereas receptive fields of nerve fibers in both species faithfully reflect both pressure gradient amplitudes (with rate changes) and directions (with phase-angle changes) in the stimulus field, receptive fields of medial nucleus were more difficult to relate to the stimulus field. Some, but not all, receptive fields could be modeled with excitatory center/inhibitory surround and inhibitory center/excitatory surround organizations. Accepted: 26 November 1997     

Behavioral and neurophysiological assessment of lateral line sensitivity in the mottled sculpin,Cottus bairdi

1. The unconditioned feeding response of the mottled sculpin, Cottus bairdi, was used to measure threshold sensitivity of the lateral line system to a vibrating sphere as a function of stimulus position (i.e., sphere near head, trunk or tail) and vibration frequency. In addition, extracellular recording techniques were used to measure threshold sensitivity curves for posterior lateral line nerve fibers for the same stimulus positions used for measuring trunk sensitivity in behavioral measurements. 2. For all stimulus positions, behaviorally-measured threshold sensitivity was relatively independent of vibration frequency from 10 to 100 Hz when defined in terms of water acceleration, rather than velocity or displacement. Best thresholds for stimuli placed 15 mm away from the head were around -75 dB re: 1m/s(2), approximately 20 dB less than that for stimuli placed at the same distance near the tail. Trunk sensitivity was intermediate. 3. Physiologically-measured threshold sensitivity, in terms of acceleration, was also relatively independent of of frequency from 10 to 100 Hz in most fibers. A smaller number of fibers showed a decline in acceleration sensitivity after 10-30 Hz, with the rate of decline being equivalent to equal velocity sensitivity. Best sensitivity of all fibers fell between -40 and -70 dB re: 1m/s (2). 4. These results indicate that (a) behavioral thresholds are based on acceleration-sensitive endorgans--most likely lateral line canal (rather than superficial) neuromasts, (b) behavioral performance can be accounted for on the basis of information from a single population of fibers, and (c) sensitivity varies along the fish's body in a manner that corresponds to the size and distribution of neuromasts.     

Two-dimensional receptive fields of midbrain lateral line units in the goldfish, <Emphasis Type="Italic">Carassius auratus</Emphasis>

We determined the receptive fields of midbrain lateral line units in goldfish, Carassius auratus, with a 50 Hz vibrating sphere placed at various azimuths and elevations alongside the fish and studied how responses were affected by different directions of sphere vibration. The receptive fields of toral lateral line units, in contrast to those of primary afferent nerve fibers, did not represent the pressure gradient pattern generated by a vibrating sphere. Thus, unlike primary afferents, single toral lateral line units did not code for source location in their spatial discharge patterns. The two-dimensional receptive fields were round, horizontally or vertically stretched, or complex. While some toral lateral line units were sensitive to the direction of sphere vibration others were not.     

Same habitat,different species: otolith microchemistry relationships between migratory and resident species support interspecific natal source classification

We tested the hypothesis that otolith trace elemental signatures (microchemistries) of mottled sculpin Cottus bairdi, slimy sculpin C. cognatus, and juvenile coho salmon Oncorhynchus kisutch were predictive of those of juvenile steelhead O. mykiss across many sites within the Lake Michigan basin. Laser ablation inductively coupled plasma mass spectrometry was used to generate otolith microchemistry signatures for each individual fish. For each species pair, statistical correlations of mean otolith concentrations of Mg, Mn, Cu, Zn, Sr, Ba, and Pb for each site were estimated. Linear equations describing these relationships were used to transform juvenile steelhead otolith microchemistry data to those of each of the other species. Transformed otolith microchemistry data were subjected to random forest classifications developed for mottled sculpin, slimy sculpin, and juvenile coho salmon to assess interspecific natal source assignment accuracies. Steelhead otolith concentrations of Sr were significantly correlated with those of each of the other species, whereas otolith concentrations of Ba and Mn were significantly correlated among some species pairs, but not others. Natal source assignment accuracies of juvenile steelhead to site and watershed generally decreased when otolith microchemistry data were transformed to those of mottled sculpin, slimy sculpin, and coho salmon. Miss-assigned fish often classified into nearby watersheds within larger hydrologic units, leading to higher assignment accuracies at coarser geographical resolutions (75–97% correct assignment to hydrologic unit for each species). These findings suggest that applications of otolith microchemistry data may extend beyond the species from which they are collected.     

The Feeding Behaviour of a Sit-and-Wait Predator,Ranatra dispar (Heteroptera: Nepidae): The Combined Effect of Food Deprivation and Prey Size on the Behavioural Components of Prey Capture

Previous work has shown a significant effect of hunger on the predatory behaviour in a sit-and-wait predator Ranatra dispar, the water stick insect (Bailey 1986 a). The experiments reported here were designed to investigate the combined effect of prey size and hunger on the predatory behaviour in order to identify which behavioural components are effected. It was found that the hunger level determines whether R. dispar will initially be aroused or not but the distance at which the arousal takes place is influenced by the size of the prey. This is believed to reflect the capacity and interrelation between visual and mechanoreceptor, sensory organs. The decision to strike at a prey is, although again influenced by hunger, significantly affected by prey size. The distance of the prey when the strike takes place is affected by hunger not the size of the prey. The outcome of the strike is determined by the size of the prey, not the hunger level of the predator. This is believed to reflect the relationship between strike trajectory, leg morphology and prey size. Food deprivation affects all components of predatory behaviour of R. dispar leading up to prey capture, by increasing not only distance of response but also the number of strikes, hits, and captures per unit presentation of prey. It does not affect capture efficiency which remains at about 70 to 80 %. Food deprivation also increases the range of prey sizes that R. dispar responds to and attempts to capture. The effect of food deprivation is considered to reflect a motivational change in responsiveness to particular prey stimuli usually described as a sensitization of particular stimulus-response relations rather than the food deprivation affecting the sensory mechanisms. The predatory success in relation to size of model prey suggested a hypothetical size that could be captured, irrespective of predator motivational level, which is based primarily on the relationship between the shape of the grasping leg and size of prey.     

Complex postglacial recolonization inferred from population genetic structure of mottled sculpin Cottus bairdii in tributaries of eastern Lake Michigan,U.S.A.

This study used analyses of the genetic structure of a non‐game fish species, the mottled sculpin Cottus bairdii to hypothesize probable recolonization routes used by cottids and possibly other Laurentian Great Lakes fishes following glacial recession. Based on samples from 16 small streams in five major Lake Michigan, U.S.A., tributary basins, significant interpopulation differentiation was documented (overall F_ST = 0·235). Differentiation was complex, however, with unexpectedly high genetic similarity among basins as well as occasionally strong differentiation within basins, despite relatively close geographic proximity of populations. Genetic dissimilarities were identified between eastern and western populations within river basins, with similarities existing between eastern and western populations across basins. Given such patterns, recolonization is hypothesized to have occurred on three occasions from more than one glacial refugium, with a secondary vicariant event resulting from reduction in the water level of ancestral Lake Michigan. By studying the phylogeography of a small, non‐game fish species, this study provides insight into recolonization dynamics of the region that could be difficult to infer from game species that are often broadly dispersed by humans.