Swimming at Increasing Speeds in Steady and Unsteady Flows of Atlantic Salmon Salmo salar: Oxygen Consumption, Locomotory Behaviour and Overall Dynamic Body Acceleration.

The swimming performance of cultured finfish species is typically studied under steady flow conditions. However, flow conditions are mostly unsteady, for instance, as experienced in sea pens in exposed sea areas. Using a Loligo swim tunnel, we investigated the effects of swimming in steady and unsteady flows at increasing swimming speeds on post-smolt Atlantic salmon. Oxygen consumption (MO2), locomotory behaviour, and overall dynamic body acceleration (ODBA), as determined with implanted acoustic sensor tags, were compared between both flow conditions. Results were obtained for mean swimming speeds of 0.2 to 0.8 m.s-1 under both flow conditions. Sensor tags that were implanted in the abdominal cavity had no significant effects on MO2 and locomotory parameters. The MO2 of fish swimming in unsteady flows was significantly higher (15-53%) than when swimming in steady flows (p < 0.05). Significant interaction effects of ODBA with flow conditions and swimming speed were found. ODBA was strongly and positively correlated with swimming speed and MO2 in unsteady flow (R2 = 0.94 and R2 = 0.93, respectively) and in steady flow (R2 = 0.91 and R2 = 0.82, respectively). ODBA predicts MO2 well over the investigated range of swimming speeds in both flow conditions. In an unsteady flow condition, ODBA increased twice as fast with MO2 compared with steady flow conditions (p < 0.05). From these results, we can conclude that (1) swimming in unsteady flow is energetically more costly for post-smolt Atlantic salmon than swimming in steady flow, as indicated by higher MO2, and (2) ODBA can be used to estimate the oxygen consumption of post-smolt Atlantic salmon in unsteady flow in swim tunnels.

Heart Rate and Acceleration Dynamics during Swim-Fitness and Stress Challenge Tests in Yellowtail Kingfish (Seriola lalandi).

The yellowtail kingfish is a highly active and fast-growing marine fish with promising potential for aquaculture. In this study, essential insights were gained into the energy economy of this species by heart rate and acceleration logging during a swim-fitness test and a subsequent stress challenge test. Oxygen consumption values of the 600-800 g fish, when swimming in the range of 0.2 up to 1 m·s-1, were high-between 550 and 800 mg·kg-1·h-1-and the heart rate values-up to 228 bpm-were even among the highest ever measured for fishes. When swimming at these increasing speeds, their heart rate increased from 126 up to 162 bpm, and acceleration increased from 11 up to 26 milli-g. When exposed to four sequential steps of increasing stress load, the decreasing peaks of acceleration (baseline values of 12 to peaks of 26, 19 and 15 milli-g) indicated anticipatory behavior, but the heart rate increases (110 up to 138-144 bpm) remained similar. During the fourth step, when fish were also chased, peaking values of 186 bpm and 44 milli-g were measured. Oxygen consumption and heart rate increased with swimming speed and was well reflected by increases in tail beat and head width frequencies. Only when swimming steadily near the optimal swimming speed were these parameters strongly correlated.

Understanding and optimizing fish counting techniques based on electrical impedance measurements.

Sustainable aquatic resources management requires reliable methods for fish detection in various environmental conditions. Herein, we study fundamental mechanisms underlying the application of electrical impedance measurements in this regard. We present results of experimental studies conducted in laboratory conditions using a low-cost impedance measurement circuit, as well as the corresponding numerical models. We also present evaluation results of a newly developed, real-time detection algorithm based on adaptive thresholding. The numerical model was validated by extracting fish tracks in 3D space from the experimental datasets, and then comparing the calculated versus measured impedance values as functions of fish coordinates in time. Numerical predictions closely resemble the experimental data. The detection sensitivity and specificity values determined for various settings exceeded 90%. Electrode width to spacing ratio is demonstrated to be a crucial parameter influencing the system sensitivity distribution. The introduced approach can constitute a framework for designing electrical impedance-based fish counting systems.

Bioinspired flatfish detection using electrical impedance measurements.

Bottom trawling for flatfish by means of tickler chains has a high ecological impact due to the continuous seabed disturbance, low selectivity and high fuel costs. This issue could be significantly mitigated by using localized startle stimuli, triggered by a detection system that selectively targets flatfishes of landable size. Flatfish, however, constitute a significant challenge for remote detection, due to their low optical and acoustical signatures. Some species of predatory fish feeding on flatfish overcome this issue by using electroreception to localize they prey, even if it is buried in bottom sediments. We take this phenomenon as an inspiration in an attempt to develop a biomimetic remote fish detection technique based on electrical impedance measurements. We constructed a detection system including a set of electrodes and a low-cost analog front-end. The electrodes were mounted on a dedicated frame and dragged above a layer of sand inside a tank with sea water and several common sole (Solea solea). An underwater camera was used to acquire video recordings synchronized with impedance data for reference. We demonstrate that fish presence below the electrodes manifests itself by changes in the measured resistance and reactance values. This phenomenon occurs even if the fish is covered with a layer of sand. The results demonstrate the potential of bioinspired remote flatfish detection, which could be highly useful for monitoring or targeted stimulation.

Tracking the flight and landing behaviour of western flower thrips in response to single and two-colour cues.

Real-time 3D tracking and high-speed videography was used to examine the behaviour of a worldwide greenhouse pest, the western flower thrips (WFT), in response to different colours in the context of improving trap design. Measurements were taken of the number of landings on, and flight activity near, a lamp containing two LEDs of either the same colour or a combination of two colours presented side by side. Main findings show that landing patterns of WFT are different between colours, with landings on UV(+ red) as highly attractive stimulus being mostly distributed at the bottom half of the lamp, while for yellow also as very attractive and green as a 'neutral' stimulus, landings were clearly on the upper rim of the lamp. Additionally, a positive interaction with the UV-A(+ red) and yellow combination elicited the highest number of landings and flight time in front of the LED lamp. Conversely, a negative interaction was observed with decreased landings and flight time found for yellow when blue was present as the adjacent colour. Overall, differences between treatments were less obvious for flight times compared to number of landings, with tracking data suggesting that WFT might use different colours to orientate at different distances as they approach a visual stimulus.

Maternal food restriction during pregnancy affects offspring development and swimming performance in a placental live-bearing fish.

How pregnant mothers allocate limited resources to different biological functions such as maintenance, somatic growth, and reproduction can have profound implications for early life development and survival of offspring. Here, we examined the effects of maternal food restriction during pregnancy on offspring in the matrotrophic (i.e. mother-nourishment throughout gestation) live-bearing fish species Phalloptychus januarius (Poeciliidae). We fed pregnant females with either low or high food levels for 6 weeks and quantified the consequences for offspring size and body fat at birth and 1 week after birth. We further measured fast-start escape performance of offspring at birth, as well as swimming kinematics during prey capture at 0, 2 and 7 days after birth. We found that the length of maternal food restriction during pregnancy negatively affected offspring dry mass and lean dry mass at birth, as well as body fat gain during the first week after birth. Moreover, it impacted the locomotor performance of offspring during prey capture at birth and during the first week after birth. We did not observe an effect of food restriction on fast-start escape performance of offspring. Our study suggests that matrotrophic poeciliid fish are maladapted to unpredictably fluctuating resource environments, because sudden reductions in maternal food availability during pregnancy result in smaller offspring with slower postnatal body fat gain and an inhibition of postnatal improving swimming skills during feeding, potentially leading to lower competitive abilities after birth.

Bumblebees land rapidly and robustly using a sophisticated modular flight control strategy.

When approaching a landing surface, many flying animals use visual feedback to control their landing. Here, we studied how foraging bumblebees (Bombus terrestris) use radial optic expansion cues to control in-flight decelerations during landing. By analyzing the flight dynamics of 4,672 landing maneuvers, we showed that landing bumblebees exhibit a series of deceleration bouts, unlike landing honeybees that continuously decelerate. During each bout, the bumblebee keeps its relative rate of optical expansion constant, and from one bout to the next, the bumblebee tends to shift to a higher, constant relative rate of expansion. This modular landing strategy is relatively fast compared to the strategy described for honeybees and results in approach dynamics that is strikingly similar to that of pigeons and hummingbirds. The here discovered modular landing strategy of bumblebees helps explaining why these important pollinators in nature and horticulture can forage effectively in challenging conditions; moreover, it has potential for bio-inspired landing strategies in flying robots.

Varroa destructor infestation impairs the improvement of landing performance in foraging honeybees.

The parasitic mite Varroa destructor is an important contributor to the high losses of western honeybees. Forager bees from Varroa-infested colonies show reduced homing and flight capacity; it is not known whether flight manoeuvrability and related learning capability are also affected. Here, we test how honeybees from Varroa-infested and control colonies fly in an environment that is unfamiliar at the beginning of each experimental day. Using stereoscopic high-speed videography, we analysed 555 landing manoeuvres recorded during 12 days of approximately 5 h in length. From this, we quantified landing success as percentage of successful landings, and assessed how this changed over time. We found that the forager workforce of Varroa-infested colonies did not improve their landing success over time, while for control bees landing success improved with approximately 10% each hour. Analysis of the landing trajectories showed that control bees improved landing success by increasing the ratio between in-flight aerodynamic braking and braking at impact on the landing platform; bees from Varroa-infested colonies did not increase this ratio over time. The Varroa-induced detriment to this landing skill-learning capability might limit forager bees from Varroa-infested colonies to adapt to new or challenging conditions; this might consequently contribute to Varroa-induced mortality of honeybee colonies.

Bumblebees land remarkably well in red-blue greenhouse LED light conditions.

Red-blue emitting LEDs have recently been introduced in greenhouses to optimise plant growth. However, this spectrum may negatively affect the performance of bumblebees used for pollination, because the visual system of bumblebees is more sensitive to green light than to red-blue light. We used high-speed stereoscopic videography to three-dimensionally track and compare landing manoeuvres of Bombus terrestris bumblebees in red-blue light and in regular, broad-spectrum white light. In both conditions, the landing approaches were interspersed by one or several hover phases, followed by leg extension and touchdown. The time between leg extension and touchdown was 25% (0.05 s) longer in red-blue light than in white light, caused by a more tortuous flight path in red-blue light. However, the total landing duration, specified as the time between the first hover phase and touchdown, did not differ between the light conditions. This suggests that the negative effects of red-blue light on the landing manoeuvre are confined to the final phase of the landing.This article has an associated First Person interview with the first author of the paper.

Temporal Limits of Visual Motion Processing: Psychophysics and Neurophysiology.

Under optimal conditions, just 3-6 ms of visual stimulation suffices for humans to see motion. Motion perception on this timescale implies that the visual system under these conditions reliably encodes, transmits, and processes neural signals with near-millisecond precision. Motivated by in vitro evidence for high temporal precision of motion signals in the primate retina, we investigated how neuronal and perceptual limits of motion encoding relate. Specifically, we examined the correspondence between the time scale at which cat retinal ganglion cells in vivo represent motion information and temporal thresholds for human motion discrimination. The timescale for motion encoding by ganglion cells ranged from 4.6 to 91 ms, and depended non-linearly on temporal frequency, but not on contrast. Human psychophysics revealed that minimal stimulus durations required for perceiving motion direction were similarly brief, 5.6-65 ms, and similarly depended on temporal frequency but, above ~10%, not on contrast. Notably, physiological and psychophysical measurements corresponded closely throughout (r = 0.99), despite more than a 20-fold variation in both human thresholds and optimal timescales for motion encoding in the retina. The match in absolute values of the neurophysiological and psychophysical data may be taken to indicate that from the lateral geniculate nucleus (LGN) through to the level of perception little temporal precision is lost. However, we also show that integrating responses from multiple neurons can improve temporal resolution, and this potential trade-off between spatial and temporal resolution would allow for loss of temporal resolution after the LGN. While the extent of neuronal integration cannot be determined from either our human psychophysical or neurophysiological experiments and its contribution to the measured temporal resolution is unknown, our results demonstrate a striking similarity in stimulus dependence between the temporal fidelity established in the retina and the temporal limits of human motion discrimination.

Flight behaviour of malaria mosquitoes around odour-baited traps: capture and escape dynamics.

Host-seeking mosquitoes rely on a range of sensory cues to find and approach blood hosts, as well as to avoid host detection. By using odour blends and visual cues that attract anthropophilic mosquitoes, odour-baited traps have been developed to monitor and control human pathogen-transmitting vectors. Although long-range attraction of such traps has already been studied thoroughly, close-range response of mosquitoes to these traps has been largely ignored. Here, we studied the flight behaviour of female malaria mosquitoes (Anopheles coluzzii) in the immediate vicinity of a commercially available odour-baited trap, positioned in a hanging and standing orientation. By analysing more than 2500 three-dimensional flight tracks, we elucidated how mosquitoes reacted to the trap, and how this led to capture. The measured flight dynamics revealed two distinct stereotypical behaviours: (i) mosquitoes that approached a trap tended to simultaneously fly downward towards the ground; (ii) mosquitoes that came close to a trap changed their flight direction by rapidly accelerating upward. The combination of these behaviours led to strikingly different flight patterns and capture dynamics, resulting in contrasting short-range attractiveness and capture mechanism of the oppositely oriented traps. These new insights may help in improving odour-baited traps, and consequently their contribution in global vector control strategies.

Frequency tuning and directional sensitivity of tympanal vibrations in the field cricket Gryllus bimaculatus.

Female field crickets use phonotaxis to locate males by their calling song. Male song production and female behavioural sensitivity form a pair of matched frequency filters, which in Gryllus bimaculatus are tuned to a frequency of about 4.7 kHz. Directional sensitivity is supported by an elaborate system of acoustic tracheae, which make the ears function as pressure difference receivers. As a result, phase differences between left and right sound inputs are transformed into vibration amplitude differences. Here we critically tested the hypothesis that acoustic properties of internal transmissions play a major role in tuning directional sensitivity to the calling song frequency, by measuring tympanal vibrations as a function of sound direction and frequency. Rather than sharp frequency tuning of directional sensitivity corresponding to the calling song, we found broad frequency tuning, with optima shifted to higher frequencies. These findings agree with predictions from a vector summation model for combining external and internal sounds. We show that the model provides robust directional sensitivity that is, however, broadly tuned with an optimum well above the calling song frequency. We therefore advocate that additional filtering, e.g. at a higher (neuronal) level, significantly contributes to frequency tuning of directional sensitivity.

Acquired versus innate prey capturing skills in super-precocial live-bearing fish.

Live-bearing fish start hunting for mobile prey within hours after birth, an example of extreme precociality. Because prenatal, in utero, development of this behaviour is constrained by the lack of free-swimming sensory-motor interactions, immediate success after birth depends on innate, evolutionarily acquired patterns. Optimal performance however requires flexible adjustment to an unpredictable environment. To distinguish innate from postnatally developing patterns we analysed over 2000 prey capture events for 28 metallic livebearers (Girardinus metallicus; Poeciliidae), during their first 3 days after birth. We show that the use of synchronous pectoral fin beats for final acceleration and ingestion is fixed and presumably innate. It allows for direct, symmetrical control of swimming speed and direction, while avoiding head yaw. Eye movements and body curvatures, however, change considerably in the first few days, showing that eye-tail coordination requires postnatal development. The results show how successful prey captures for newborn, live-bearing fish are based on a combination of fixed motor programmes and rapid, postnatal development.

Speed and direction response profiles of neurons in macaque MT and MST show modest constraint line tuning.

Several models of heading detection during smooth pursuit rely on the assumption of local constraint line tuning to exist in large scale motion detection templates. A motion detector that exhibits pure constraint line tuning responds maximally to any 2D-velocity in the set of vectors that can be decomposed into the central, or classic, preferred velocity (the shortest vector that still yields the maximum response) and any vector orthogonal to that. To test this assumption, we measured the firing rates of isolated middle temporal (MT) and medial superior temporal (MST) neurons to random dot stimuli moving in a range of directions and speeds. We found that as a function of 2D velocity, the pooled responses were best fit with a 2D Gaussian profile with a factor of elongation, orthogonal to the central preferred velocity, of roughly 1.5 for MST and 1.7 for MT. This means that MT and MST cells are more sharply tuned for speed than they are for direction; and that they indeed show some level of constraint line tuning. However, we argue that the observed elongation is insufficient to achieve behavioral heading discrimination accuracy on the order of 1-2 degrees as reported before.

Intermittent stimulus presentation stabilizes neuronal responses in macaque area MT.

Repeated stimulation impacts neuronal responses. Here we show how response characteristics of sensory neurons in macaque visual cortex are influenced by the duration of the interruptions during intermittent stimulus presentation. Besides effects on response magnitude consistent with neuronal adaptation, the response variability was also systematically influenced. Spike rate variability in motion-sensitive area MT decreased when interruption durations were systematically increased from 250 to 2,000 ms. Activity fluctuations between subsequent trials and Fano factors over full response sequences were both lower with longer interruptions, while spike timing patterns became more regular. These variability changes partially depended on the response magnitude, but another significant effect that was uncorrelated with adaptation-induced changes in response magnitude was also present. Reduced response variability was furthermore accompanied by changes in spike-field coherence, pointing to the possibility that reduced spiking variability results from interactions in the local cortical network. While neuronal response stabilization may be a general effect of repeated sensory stimulation, we discuss its potential link with the phenomenon of perceptual stabilization of ambiguous stimuli as a result of interrupted presentation.

Spike-interval triggered averaging reveals a quasi-periodic spiking alternative for stochastic resonance in catfish electroreceptors.

Catfish detect and identify invisible prey by sensing their ultra-weak electric fields with electroreceptors. Any neuron that deals with small-amplitude input has to overcome sensitivity limitations arising from inherent threshold non-linearities in spike-generation mechanisms. Many sensory cells solve this issue with stochastic resonance, in which a moderate amount of intrinsic noise causes irregular spontaneous spiking activity with a probability that is modulated by the input signal. Here we show that catfish electroreceptors have adopted a fundamentally different strategy. Using a reverse correlation technique in which we take spike interval durations into account, we show that the electroreceptors generate a supra-threshold bias current that results in quasi-periodically produced spikes. In this regime stimuli modulate the interval between successive spikes rather than the instantaneous probability for a spike. This alternative for stochastic resonance combines threshold-free sensitivity for weak stimuli with similar sensitivity for excitations and inhibitions based on single interspike intervals.

Spatial summation in macaque parietal area 7a follows a winner-take-all rule.

While neurons in posterior parietal cortex have been found to signal the presence of a salient stimulus among multiple items in a display, spatial summation within their receptive field in the absence of an attentional bias has never been investigated. This information, however, is indispensable when one investigates the mechanisms of spatial attention and competition between multiple visual objects. To examine the spatial summation rule in parietal area 7a neurons, we trained rhesus monkeys to fixate on a central cross while two identical stimuli were briefly displayed in a neuron's receptive field. The response to a pair of dots was compared with the responses to the same dots when they were presented individually. The scaling and power parameters of a generalized summation algorithm varied greatly, both across neurons and across combinations of stimulus locations. However, the averaged response of the recorded population of 7a neurons was consistent with a winner-take-all rule for spatial summation. A control experiment where a monkey covertly attended to both stimuli simultaneously suggests that attention introduces additional competition by facilitating the less optimal stimulus. Thus an averaging stage is introduced between ∼ 200 and 300 ms of the response to a pair of stimuli. In short, the summation algorithm over the population of area 7a neurons carries the signature of a winner-take-all operation, with spatial attention possibly influencing the temporal dynamics of stimulus competition, that is the moment that the "winner" takes "victory" over the "loser" stimulus.

Implied motion activation in cortical area MT can be explained by visual low-level features.

To investigate form-related activity in motion-sensitive cortical areas, we recorded cell responses to animate implied motion in macaque middle temporal (MT) and medial superior temporal (MST) cortex and investigated these areas using fMRI in humans. In the single-cell studies, we compared responses with static images of human or monkey figures walking or running left or right with responses to the same human and monkey figures standing or sitting still. We also investigated whether the view of the animate figure (facing left or right) that elicited the highest response was correlated with the preferred direction for moving random dot patterns. First, figures were presented inside the cell's receptive field. Subsequently, figures were presented at the fovea while a dynamic noise pattern was presented at the cell's receptive field location. The results show that MT neurons did not discriminate between figures on the basis of the implied motion content. Instead, response preferences for implied motion correlated with preferences for low-level visual features such as orientation and size. No correlation was found between the preferred view of figures implying motion and the preferred direction for moving random dot patterns. Similar findings were obtained in a smaller population of MST cortical neurons. Testing human MT+ responses with fMRI further corroborated the notion that low-level stimulus features might explain implied motion activation in human MT+. Together, these results suggest that prior human imaging studies demonstrating animate implied motion processing in area MT+ can be best explained by sensitivity for low-level features rather than sensitivity for the motion implied by animate figures.

Directional anisotropy of motion responses in retinotopic cortex.

Recently, evidence has emerged for a radial orientation bias in early visual cortex. These results predict that in early visual cortex a tangential bias should be present for motion direction. We tested this prediction in a human imaging study, using a translating random dot pattern that slowly rotated its motion direction 360 degrees in cycles of 54 s. In addition, polar angle and eccentricity mapping were performed. This allowed the measurement of the BOLD response across the visual representations of the different retinotopic areas. We found that, in V1, V2, and V3, BOLD responses were consistently enhanced for centrifugal and centripetal motion, relative to tangential motion. The relative magnitude of the centrifugal and centripetal response biases changed with visual eccentricity. We found no motion direction biases in MT+. These results are in line with previously observed anisotropies in motion sensitivity across the visual field. However, the observation of radial motion biases in early visual cortex is surprising considering the evidence for a radial orientation bias. An additional experiment was performed to resolve this apparent conflict in results. The additional experiment revealed that the observed motion direction biases most likely originate from anisotropies in long range horizontal connections within visual cortex.

Sensitivity for reverse-phi motion.

Low-level contrast information in the primary visual pathway is represented in two different channels. ON-center cells signal positive contrasts and OFF-center cells signal negative contrasts. In this study we address the question whether initial motion analysis is performed separately in these two channels, or also through combination of signals from ON and OFF cells. We quantitatively compared motion coherence detection for regular and for reverse-phi motion stimuli. In reverse-phi motion the contrast of a pattern flips during displacements. Sensitivity is therefore based on correlating positive and negative contrasts, whereas for regular motion it is based on correlating similar contrasts. We compared tuning curves for step size and temporal interval for stimuli in which motion information was limited to a single combination of step size and interval. Tuning for step size and temporal interval was highly similar for the two types of motion. Moreover, minimal coherence thresholds for both types of motion matched quantitatively, irrespective of dot density. We also measured sensitivity for so-called no-phi motion stimuli, in which the contrast of displaced dots was set to zero. Sensitivity for no-phi motion was low for stimuli containing only black or only white dots. When both dot polarities were present in the stimulus, sensitivity was absent. Thus, motion information based on separate contrasts was effectively cancelled by a component based on different contrasts. Together these results show equal efficiency in correlating dots of opposite contrast and of similar contrast, which strongly suggests efficient detection of correlations across ON and OFF channels.