The paddlefish rostrum functions as an electrosensory antenna in plankton feeding

A novel electrosensory function is presented for the large, plankton-feeding, freshwater paddlefish, Polyodon spathula, along with a hypothesis which accounts for the distinctive, elongated rostrum of this unusual fish. Behavioural experiments conducted in the ''dark'' (under infrared illumination), to eliminate vision, show that paddlefish efficiently capture planktonic prey to distances up to 80–90 mm. They make feeding strikes at dipole electrodes in response to weak low-frequency electrical currents. Fish also avoid metal obstacles placed in the water, again in the dark. Electrophysiological experiments confirm that the Lorenzinian ampullae of paddlefish are sensitive to weak, low-frequency electrical signals, and demonstrate unequivocally that they respond to the very small electrical signals generated by their natural zooplankton prey (Daphnia sp.). We propose that the rostrum constitutes the biological equivalent of an electrical antenna, enabling the fish to accurately detect and capture its planktonic food in turbid river environments where vision is severely limited. The electrical sensitivity of paddlefish to metallic substrates may interfere with their migrations through locks and dams.     

Behavioral stochastic resonance: how the noise from a Daphnia swarm enhances individual prey capture by juvenile paddlefish.

Zooplankton emit weak electric fields into the surrounding water that originate from their own muscular activities associated with swimming and feeding. Juvenile paddlefish prey upon single zooplankton by detecting and tracking these weak electric signatures. The passive electric sense in this fish is provided by an elaborate array of electroreceptors, Ampullae of Lorenzini, spread over the surface of an elongated rostrum. We have previously shown that the fish use stochastic resonance to enhance prey capture near the detection threshold of their sensory system. However, stochastic resonance requires an external source of electrical noise in order to function. A swarm of plankton, for example Daphnia, can provide the required noise. We hypothesize that juvenile paddlefish can detect and attack single Daphnia as outliers in the vicinity of the swarm by using noise from the swarm itself. From the power spectral density of the noise plus the weak signal from a single Daphnia, we calculate the signal-to-noise ratio, Fisher information and discriminability at the surface of the paddlefish's rostrum. The results predict a specific attack pattern for the paddlefish that appears to be experimentally testable.     

Resonant properties in the paddlefish electrosensory system caused by delayed feedback

Introduction The paddlefish electrosensory system consists of receptor cells in the skin that sense minute electric fields from their prey, small water fleas. The receptors thereby measure the difference of the voltage at the skin surface against the voltage inside the animal. Due to a high skin impedance, this internal voltage is considered to be relatively fixed. Results We found, however, that this internal voltage can fluctuate. It shows damped oscillations to a single short electric field pulse and changes, with some time delay, according to the previous history of stimulation, and shows resonance at a certain frequency. Conclusions Computer simulations show that these phenomena can be explained by the presence of delayed feedback where the internal voltage is part of the feedback loop.     

Development of the jamming avoidance response and its morphological correlates in the gymnotiform electric fish, Eigenmannia.

The electric fish, Eigenmannia, will smoothly shift the frequency of its electric organ discharge away from an interfering electric signal. This shift in frequency is called the jamming avoidance response (JAR). In this article, we analyze the behavioral development of the JAR and the anatomical development of structures critical for the performance of the JAR. The JAR first appears when juvenile Eigenmannia are approximately 1 month old, at a total length of 13-18 mm. We have found that the establishment of much of the sensory periphery and of central connections precedes the onset of the JAR. We describe three aspects of the behavioral development of the JAR: (a) the onset and development of the behavior is closely correlated with size, not age; (b) the magnitude (in Hz) of the JAR increases with size until the juveniles display values within the adult range (10-20 Hz) at a total length of 25-30 mm; and (3) the JAR does not require prior experience or exposure to electrical signals. Raised in total electrical isolation from the egg stage, animals tested at a total length of 25 mm performed a correct JAR when first exposed to the stimulus. We examine the development of anatomical areas important for the performance of the JAR: the peripheral electrosensory system (mechano- and electroreceptors and peripheral nerves); and central electrosensory pathways and nuclei [the electrosensory lateral line lobe (ELL), the lateral lemniscus, the torus semicircularis, and the pace-maker nucleus]. The first recognizable structures in the developing electrosensory system are the peripheral neurites of the anterior lateral line nerve. The afferent nerves are established by day 2, which is prior to the formation of receptors in the epidermis. Thus, the neurites wait for their targets. This sequence of events suggests that receptor formation may be induced by innervation of primordial cells within the epidermis. Mechanoreceptors are first formed between day 3 and 4, while electroreceptors are first formed on day 7. Electroreceptor multiplication is observed for the first time at an age of 25 days and correlates with the onset of the JAR. The somata of the anterior lateral line nerve ganglion project afferents out to peripheral electroreceptors and also send axons centrally into the ELL. The first electroreceptive axons invade the ELL by day 6, and presumably a rough somatotopic organization and segmentation within the ELL may arise as early as day 7. Axonal projections from the ELL to the torus develop after day 18.(ABSTRACT TRUNCATED AT 400 WORDS)     

Two modes of information processing in the electrosensory system of the paddlefish (Polyodon spathula)

Paddlefish are uniquely adapted for the detection of their prey, small water fleas, by primarily using their passive electrosensory system. In a recent anatomical study, we found two populations of secondary neurons in the electrosensory hind brain area (dorsal octavolateral nucleus, DON). Cells in the anterior DON project to the contralateral tectum, whereas cells in the posterior DON project bilaterally to the torus semicircularis and lateral mesencephalic nucleus. In this study, we investigated the properties of both populations and found that they form two physiologically different populations. Cells in the posterior DON are about one order of magnitude more sensitive and respond better to stimuli with lower frequency content than anterior cells. The posterior cells are, therefore, better suited to detect distant prey represented by low-amplitude signals at the receptors, along with a lower frequency spectrum, whereas cells in the anterior DON may only be able to sense nearby prey. This suggests the existence of two distinct channels for electrosensory information processing: one for proximal signals via the anterior DON and one for distant stimuli via the posterior DON with the sensory input fed into the appropriate ascending channels based on the relative sensitivity of both cell populations.     

Developmental origin of shark electrosensory organs

Vertebrates have evolved electrosensory receptors that detect electrical stimuli on the surface of the skin and transmit them somatotopically to the brain. In chondrichthyans, the electrosensory system is composed of a cephalic network of ampullary organs, known as the ampullae of Lorenzini, that can detect extremely weak electric fields during hunting and navigation. Each ampullary organ consists of a gel-filled epidermal pit containing sensory hair cells, and synaptic connections with primary afferent neurons at the base of the pit that facilitate detection of voltage gradients over large regions of the body. The developmental origin of electroreceptors and the mechanisms that determine their spatial arrangement in the vertebrate head are not well understood. We have analyzed electroreceptor development in the lesser spotted catshark (Scyliorhinus canicula) and show that Sox8 and HNK1, two markers of the neural crest lineage, selectively mark sensory cells in ampullary organs. This represents the first evidence that the neural crest gives rise to electrosensory cells. We also show that pathfinding by cephalic mechanosensory and electrosensory axons follows the expression pattern of EphA4, a well-known guidance cue for axons and neural crest cells in osteichthyans. Expression of EphrinB2, which encodes a ligand for EphA4, marks the positions at which ampullary placodes are initiated in the epidermis, and EphA4 is expressed in surrounding mesenchyme. These results suggest that Eph-Ephrin signaling may establish an early molecular map for neural crest migration, axon guidance and placodal morphogenesis during development of the shark electrosensory system.     

Role of the daily food ration of perch fry (Perca fluvialis) in infestation with Bunodera luciopercae (Trematoda, Allocreadiidae)

The list of intermediate hosts of Bunodera luciopercae is given. In Lake Syamozero they are represented by crustaceans Heterocope, Ophryoxus. Data on their role in the ration of juvenile perch are given. Diurnal dynamics of the ratio between infected and noninfected plankton in feeding and the process of the formation of fish infection have been studied.     

FORAGING OF JUVENILE MONK SEALS AT FRENCH FRIGATE SHOALS, HAWAII

Emaciation and poor survivorship of juvenile Hawaiian monk seals at French Frigate Shoals atoll prompted a study of their foraging, using video camera technology ( crittercam ). Nine juveniles between the ages of 1 and 3 yr (six males, three females) were fitted with crittercam to identify their foraging habitat and feeding behavior. All feeding was directed at small (≤ 10 cm), cryptic, benthic prey. Older seals (ages 2 and 3), varied in their foraging intensity with most of their attention directed at shallow atoll depths (10–30 m). In contrast, the three yearlings focused all their feeding in the sand fields (50–100 m) on the atoll's outer slope. Bottom trawls were used to assess the prey abundance of the sand habitat and found 70% of the numerical catch was flounder ( Bothidae ). Extrapolating the yearlings' prey capture rate (0.13/min, derived from the crittercam video) over their total bottom time yielded an estimated 1–1.3 kg/day of flounder. The mean size of flounder (5 ± 1.7 cm) caught in the bottom trawls was close to the size at which larval flounder settle from the plankton (3 cm), suggesting that localized changes in oceanography could directly impact the seals' prey supply. Extensive use of sand communities by young seals may be the strongest link yet identified between juvenile survivorship and oceanographic dynamics.     

The effects of intraspecific competition on the prey capture behavior and kinematics of the bluegill sunfish, Lepomis macrochirus

Competition has broad effects on fish and specifically the effects of competition on the prey capture kinematics and behavior are important for the assessment of future prey capture studies in bony fishes. Prey capture kinematics and behavior in bony fishes have been shown to be affected by temperature and satiation. The densities at which bony fish are kept have also been shown to affect their growth, behavior, prey selection, feeding and physiology. We investigated how density induced intraspecific competition for food affects the prey capture kinematics of juvenile bluegill sunfish, Lepomis macrochirus. High speed video was utilized to film five bold individuals feeding at three different densities representing different levels of intraspecific competition. We hypothesized that: (1) the feeding kinematics will be faster at higher levels of competition compared to lower levels of competition, and (2) bluegill should shift from more suction-based feeding towards more ram-based feeding with increasing levels of competition in order to outcompete conspecifics for a prey item. We found that, with increased intraspecific competition, prey capture became faster, involving more rapid jaw opening and therefore greater inertial suction, shorter mouth closing times, and shorter gape cycles. Furthermore, the attack velocity of the fish increased with increasing competition, however a shift towards primarily ram based feeding was not confirmed. Our study demonstrates that prey capture kinematics are affected by the presence of conspecifics and future studies need to consider the effects of competition on prey capture kinematics.     

Energy acquisition and retention by age‐0 and age‐1 paddlefish Polyodon spathula (Walbaum, 1792) in relation to size,growth, and rearing conditions in two Great Plains reservoirs and hatchery ponds

The objective of this study was to investigate lipid accumulation and storage in age‐0 and age‐1 paddlefish Polyodon spathula (Walbaum, 1792) in relation to age, stock, year, and growth. Juvenile paddlefish were collected from three locations in North Dakota and Montana, USA, during July and August of 2011 and 2012 and proximate analysis was used to determine lipid content. RNA/DNA ratios were used as an index of growth rates. Differences in age‐based lipid accumulation and storage in juvenile paddlefish suggest a split allocation between growth and lipid storage, with growth being the highest initial priority and emphasis on energy storage occurring at a larger size, later in life. Differences in lipid allocation between stocks indicate that allocation is influenced by hatchery/wild rearing conditions. Differences within and between year‐classes are consistent with field evidence observed in 2012 of a strong 2011 year‐class, and indicate that during productive times, paddlefish may allocate energy to both body growth and lipid reserves, and that allocation differs among years. The lack of a relationship between RNA/DNA ratio and lipid does not support a physiologically exclusive allocation strategy between growth and lipid. Evidence from this and other studies suggests rather that an emphasis on growth, some energy storage, and a large rostrum size in relation to overall fish length in age‐0 and age‐1 fish, may be adaptive in avoiding predation while accruing necessary energy reserves for overwintering. Although this study also provides reference information regarding proximate composition of wild and hatchery origin juvenile paddlefish, much more study is needed into the relationships among growth, low and high lipid groups, lipid allocation in juvenile paddlefish as well as the existence and timing of allocation changes between growth and storage. To aid in understanding paddlefish survival and year‐class strengths, these relationships also need to be linked to inter‐annual differences in early rearing environments for age‐0 and age‐1 fish.     

Food habits and trophic status of Limanda sakhalinensis (Pleuronectidae) on the western Kamchatka shelf in the summer period

Based on materials of expeditions of TINRO-Center on the western Kamchatka shelf in July 2005, 2008, and 2010, we analyze data on feeding of Sakhalin flounder. Sakhalin flounders are consumers of euphausiids, copepods, amphipods, polychaetes, and juvenile fish. The calculated values of the trophic levels are 3.58–3.95. Consumption of maturing and mature Sakhalin flounder primarily plankton prey leads to divergence of ecological niches with morphologically close yellowfin sole, extends prey species, and apparently provides the basis for the dominance of the western Kamchatka shelf community. Mature and maturing Sakhalin flounders feed predominantly on plankton prey, which leads to a divergence of their ecological niche with morphologically close yellowfin sole and expanding food supply and apparently is the basis of the dominance of flatfish community of the western Kamchatka shelf.     

Development of the jamming avoidance response and its morphological correlates in the gymnotiform electric fish,Eigenmannia

The electric fish, Eigenmannia, will smoothly shift the frequency of its electric organ discharge away from an interfering electric signal. This shift in frequency is called the jamming avoidance response (JAR). In this article, we analyze the behavioral development of the JAR and the anatomical development of structures critical for the performance of the JAR. The JAR first appears when juvenile Eigenmannia are approximately 1 month old, at a total length of 13–18 mm. We have found that the establishment of much of the sensory periphery and of central connections precedes the onset of the JAR. We describe three aspects of the behavioral development of the JAR: (a) the onset and development of the behavior is closely correlated with size, not age; (b) the magnitude (in Hz) of the JAR increases with size until the juveniles display values within the adult range (10–20 Hz) at a total length of 25–30 mm; and (3) the JAR does not require prior experience or exposure to electrical signals. Raised in total electrical isolation from the egg stage, animals tested at a total length of 25 mm performed a correct JAR when first exposed to the stimulus. We examine the development of anatomical areas important for the performance of the JAR: the peripheral electrosensory system (mechano- and electroreceptors and peripheral nerves); and central electrosensory pathways and nuclei [the electrosensory lateral line lobe (ELL), the lateral lemniscus, the torus semicircularis, and the pacemaker nucleus]. The first recognizable structures in the developing electrosensory system are the peripheral neurites of the anterior lateral line nerve. The afferent nerves are established by day 2, which is prior to the formation of receptors in the epidermis. Thus, the neurites wait for their targets. This sequence of events suggests that receptor formation may be induced by innervation of primordial cells within the epidermis. Mechanoreceptors are first formed between day 3 and 4, while electroreceptors are first formed on day 7. Electroreceptor multiplication is observed for the first time at an age of 25 days and correlates with the onset of the JAR. The somata of the anterior lateral line nerve ganglion project afferents out to peripheral electroreceptors and also send axons centrally into the ELL. The first electroreceptive axons invade the ELL by day 6, and presumably a rough somatotopic organization and segmentation within the ELL may arise as early as day 7. Axonal projections from the ELL to the torus develop after day 18. Within the torus semicircularis, giant cells are necessary for the performance of the JAR. Giant cell numbers increase exponentially during development and the onset of the JAR coincides with a minimum of at least 150 giant cells and the attainment of a total length of at least 15 mm and at least 150 giant cells. Pacemaker and relay cells comprise the adult Eigenmannia pacemaker nucleus. The growth and differentiation of these cell types also correlates with the onset of the JAR in developing animals. We describe a gradual improvement of sensory abilities, as opposed to an explosive onset of the mature JAR. We further suggest that this may be a rule common in most developing behavioral systems. © 1992 John Wiley & Sons, Inc.     

Phylogenetic and ecological factors influencing the number and distribution of electroreceptors in elasmobranchs

Electroreception is found throughout the animal kingdom from invertebrates to mammals and has been shown to play an important role in prey detection, facilitating social behaviours, the detection of predators and orientation to the earth's magnetic field for navigation. Electroreceptors in elasmobranchs, the ampullae of Lorenzini, detect minute electric fields and independently process these stimuli, thereby providing spatial information to the central nervous system on the location of a source, often potential prey. The ampullae of Lorenzini are individually connected to a single somatic pore on the surface of the skin, with the spatial separation of each pore directly influencing how electrical stimuli are detected and processed. Pore abundance varies across taxonomic groups resulting in unique species-specific differences. The intricate distribution patterns created by the specific positioning of somatic pores on the head are, however, consistent within families, resulting in patterns that are identifiable at higher taxonomic levels. As elasmobranchs evolved, the electrosensory system became more complex and highly specialized, which is evident by a general trend of increasing pore abundance over time. The elasmobranch electrosensory system has evolved to operate efficiently under the environmental conditions of the particular habitat in which a species lives. For example, reduced pore abundance is evident in oceanic pelagic elasmobranchs, for whom visual cues are thought to be of great importance. Pore abundance and spatial distribution may be influenced by multiple factors including head morphology, phylogeny, feeding behaviour and habitat.     

Ecology and biology of paddlefish in North America: historical perspectives,management approaches,and research priorities

Paddlefish (Polyodon spathula, Polyodontidae)are large, mostly-riverine fish that once wereabundant in medium- to large-sized river systemsthroughout much of the central United States. Concernfor paddlefish populations has grown from a regionalfisheries issue to one of national importance for theUnited States. In 1989, the U.S. Fish and WildlifeService (USFWS) was petitioned to list paddlefish asa federally threatened species under the EndangeredSpecies Act. The petition was not granted, primarilybecause of a lack of empirical data on paddlefishpopulation size, age structure, growth, or harvestrates across the present 22-state range. Nonetheless,concern for paddlefish populations prompted the USFWSto recommend that paddlefish be protected through theConvention on International Trade in EndangeredSpecies of Wild Fauna and Flora (CITES). The additionof paddlefish to Appendix II of CITES, which wasapproved in March 1992, provides a mechanism tocurtail illegal trade in paddlefish and their partsand supports a variety of conservation plans. Paddlefish populations have been negatively affectedby overharvest, river modifications, and pollution,but the paddlefish still occupies much of its historicrange and most extant populations seem to be stable. Although many facets of paddlefish biology andecology are well understood, the lack of informationon larval and juvenile ecology, mechanisms thatdetermine recruitment, population size and vitalrates, interjurisdictional movements, and the effectsof anthropogenic activities present significantobstacles for managing paddlefish populations. Questions about the size and structure of localpopulations, and how such populations are affected bynavigation traffic, dams, and pollution are regardedas medium priority areas for future research. Theavailability of suitable spawning habitat and overallreproductive success in impounded rivers are unknownand represent critical areas for future research. Research on reproductive and recruitment success inimpounded rivers have significant implications formanaging paddlefish, as rivers are modified furtherfor human use.     

Use of electroreception during foraging by the Australian lungfish

A diverse range of animals, including elasmobranchs and nonteleost fish, use passive electroreception to locate hidden prey. The Australian lungfish, Neoceratodus forsteri (Krefft 1870), has ampullary organs analogous in form to the electroreceptors of other nonteleost fish. Afferents from these ampullae project to regions in the brain that are known to process electrosensory information in other species, suggesting that N. forsteri possesses an electric sense that may be used during prey location. To explore this hypothesis directly, we first characterized food-locating behaviour in N. forsteri and then conducted an experiment designed to quantify the effects of manipulating electrical and olfactory stimuli from live prey. A small crayfish, Cherax destructor, was housed in a specially constructed chamber hidden beneath the substrate, which prevented emission of chemical, mechanical and visual cues, but allowed transmission of bioelectric fields. Control treatments included presentation of electrically shielded prey, a dead crayfish and an empty chamber. In some treatments, a competing olfactory signal was presented simultaneously at the other end of the test tank to assess the relative salience of this sensory modality. The lungfish responded to the crayfish in the unshielded chamber with accurate and sustained feeding movements, even with a competing olfactory signal. By contrast, the abolition of electrical cues in the three control treatments reduced the accuracy and frequency of feeding movements in the vicinity of the target chamber. These results show that N. forsteri is capable of perceiving the weak electric fields surrounding living animals, and suggest that it uses this information when foraging to locate prey hidden from view. Copyright 1999 The Association for the Study of Animal Behaviour.     

Electrolocation in the platypus--some speculations

In the platypus, electroreceptors are located in rostro-caudal rows in skin of the bill, while mechanoreceptors are uniformly distributed across the bill. The electrosensory area of the cerebral cortex is contained within the tactile somatosensory area, and some cortical cells receive input from both electroreceptors and mechanoreceptors, suggesting a close association between the tactile and electric senses. Platypus can determine the direction of an electric source, perhaps by comparing differences in signal strength across the sheet of electroreceptors as the animal characteristically moves its head from side to side while hunting. The cortical convergence of electrosensory and tactile inputs suggests a mechanism for determining the distance of prey items which, when they move, emit both electrical signals and mechanical pressure pulses. Distance could be computed from the difference in time of arrival of the two signals. Much of the platypus' feeding is done by digging in the bottom of streams with the bill. Perhaps the electroreceptors could also be used to distinguish animate and inanimate objects in this situation where the mechanoreceptors would be continuously stimulated. Much of this is speculation, and there is still much to be learned about electroreception in the platypus and its fellow monotreme, the echidna.     

Central nervous system physiology of electroreception, a review.

There are several reasons why one can expect that the study of electric fish may prove instructive about general mechanisms of sensory processing and neuronal integration. These reasons include the following: the simplicity of the electrical signals which are the normal input and output; the availability of a variety of stereotyped behaviors to characterize the system as a whole; the case with which individual receptors or primary afferents can be activated; the demonstrated presence of corollary discharge and reafference mechanisms for motor control over sensory input; the presence of highly specialized CNS structures which have evolved to meet the unusual demands of the electrosensory system. Work relating to these and other aspects of the electrosensory systems is discussed with an emphasis on the potential which these systems offer.     

Response properties and biological function of the skate electrosensory system during ontogeny

This study examined the response properties of skate electrosensory primary afferent neurons of pre-hatch embryo (8–11 weeks), post-hatch juvenile (1–8 months), and adult (>2 year) clearnose skates (Raja eglanteria) to determine whether encoding of electrosensory information changes with age, and if the electro-sense is adapted to encode natural bioelectric stimuli across life history stages. During ontogeny, electrosensory primary afferents increase resting discharge rate, spike regularity, and sensitivity at best frequency. Best frequency was at 1–2 Hz for embryos, showed an upwards shift to 5 Hz in juveniles, and a downward shift to 2–3 Hz in adults. Encapsulated embryos exhibit ventilatory movements that are interrupted by a “freeze response”” when presented with weak uniform fields at 0.5 and 1 Hz. This phasic electric stimulus contains spectral information found in potentials produced by natural fish predators, and therefore indicates that the embryo electrosense can efficiently mediate predator detection and avoidance. In contrast, reproductively active adult clearnose skates discharge their electric organs at rates near the peak frequency sensitivity of the adult electrosensory system, which; facilitates electric communication during social behavior. We suggest that life-history-dependent functions such as these may shape the evolution of the low-frequency response properties for the elasmobranch electrosensory system. Accepted: 19 February 1998     

Sieving functional morphology of the gill raker feeding apparatus of atlantic menhaden

Menhaden occupy an important position in estuarine food webs, thus the rate processes associated with their feeding are critical to the ecosystem management of fishery and ecological resources. Atlantic menhaden feed on a wide range of plankton, the size and food quality of which change ontogenetically. We analyzed the functional morphology of the menhaden feeding apparatus in a size series of menhaden representative of juveniles and the adult migratory stock. The physical dimensions of gill arches and rakers increased isometrically with fish length; however, branchiospinule spacing, the dimension that forms the sieve apertures of the branchial basket, scaled allometrically with fish length. Juvenile menhaden from North Carolina have branchiospinule spacings that averaged 12 microm, with three arch subsections of average spacing < 10 microm. Spacings did not increase with juvenile growth until the first allometric inflection point at approximately 100 mm fork length (FL). Spacing data for juveniles from other locations suggests spacing increases with latitude. Spacings increase with fish length in adults until a second inflection at 200 mm FL, after which spacing averages 37 microm. These data suggest menhaden juveniles filter smaller plankton with higher filtration efficiency than previously considered and that regional recruitment may affect adult distribution through foraging preferences.     

Plankton‐picking by the goatfish Pseudupeneus maculatus(Mullidae), a specialized bottom forager

Although goatfishes (Mullidae) include c . 50 specialized bottom foraging species, juvenile and adult spotted goatfish Pseudupeneus maculatus were recorded feeding on plankton on rocky reefs off southern and north‐eastern Brazil, respectively.