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Niven, J. E.

Publications and source records attributed to Niven, J. E..

11 recordsLinked to original sources

Multiple Effects of Artificial Lighting at Night on Male Glow-worms' Mate Searching Behaviour

Artificial lighting at night (ALAN) has been identified as a driver of insect decline, disrupting their ecology, behaviour and physiology. Recent studies have begun to identify the mechanisms by which ALAN affects nocturnal insects but focus primarily on moths. In glow-worms (Lampyris noctiluca), population survival relies on males detecting and reaching the glow emitted by bioluminescent females at night. Despite evidence suggesting many deleterious effects of ALAN on their mating success, little is known about the behavioural mechanisms underlying those effects. Using a translational approach, we assessed males ability to detect and approach females, both in nocturnal conditions and under ALAN showing that males land near a female before walking towards it. Thus, males navigate through dense vegetation to find a mate. Males walking on a trackball were highly reliable in adjusting their course to rapid left to right shifts of a green LEDs mimicking females glow, reorienting in less than 1 second. Under ALAN, males reliability to detect the dummy female was significantly hindered, along with their speed, stamina and orientation. This indicates ALAN has multiple simultaneous impacts on the ability of males to reach females, impairing their mating with potentially severe consequences on glow-worms population survival.

animal behavior and cognition↗

Shifts in honeybee worker metabolism immediately post-eclosion

O_LIThe metabolic rate of an organism is intrinsically linked to key traits such as reproductive output and lifespan. While the drivers of individual differences in metabolic rate are poorly understood, previous research in insects has shown that metabolic rate can change substantially in the initial hours and days post-eclosion as adults. C_LIO_LIHere we repeatedly measured the resting and active metabolic rate of individual adult honeybees (Apis mellifera) for up to 48 hours from the time of eclosion. We combined flow-through respirometry with automated behaviour tracking, permitting us to obtain active (AMR) and true resting metabolic rate (RMR) from freely moving animals. We compared these recordings to the more conventional approach of obtaining resting metabolic rate by restraining animals. C_LIO_LIBoth active and resting metabolic rates and mass-specific metabolic rates increased significantly in the first 48-hours post-eclosion, whereas metabolic scope did not change. Mass-specific water loss was highest in active bees and changed non-linearly with time post-eclosion, increasing in the first 24 hours before decreasing again. A similar quadratic relationship with time was also observed for bees movement speed. Speed- and mass-specific metabolic rate and scope increased with time post-emergence, whereas speed- and mass-specific water loss did not. C_LIO_LIThe metabolic rate of restrained bees was consistently significantly higher than the true RMR at all time points, likely due to the stress associated with being restrained. Therefore, we recommend future studies of insect resting metabolic rates avoid restraining organisms to restrict movement and consider employing behaviour tracking as a means to extract metabolic rate data from periods of true rest. C_LIO_LIThis study provides important insights into the previously overlooked changes in metabolism exhibited by newly emerged honeybee workers. The high mortality rate beyond 48 hours, coupled with significant changes in metabolic rates, body mass, and water loss, underscores the importance of this early post-eclosion period for survival and metabolic stabilization. C_LI

physiology↗

Gustatory sensitivity to amino acids in bumblebees

Bees rely on amino acids from nectar and pollen for essential physiological functions. While nectar typically contains low (<1 mM) amino acid concentrations, while their levels in pollen are higher, but vary widely (10-200 mM). Behavioural studies suggest bumblebees have preferences for specific amino acids but whether such preferences are mediated via gustatory mechanisms remains unclear. This study explores bumblebees (Bombus terrestris) gustatory sensitivity to two essential amino acids (EAAs), valine and lysine, using electrophysiological recordings from gustatory sensilla on their mouthparts. Valine elicited a concentration-dependent response from 0.1 mM, indicating that bumblebees could perceive valine at concentrations found naturally in nectar and pollen. In contrast, lysine failed to evoke a response across tested concentrations (0.1-500 mM). The absence of lysine detection raises questions about the specificity and diversity of amino acid-sensitive receptors in bumblebees. Bees responded to valine at lower concentrations than sucrose, suggesting comparatively higher sensitivity (EC50: 0.7 mM vs. 3.91 mM for sucrose). Our findings indicate that bumblebees can rapidly evaluate the amino acid content of pollen and nectar using pre-ingestive cues, rather than relying on post-ingestive cues or feedback from their nestmates. Such sensory capabilities likely impact foraging strategies, with implications for plant-bee interactions and pollination.

neuroscience↗

Larval nutrition impacts survival to adulthood, body size, and the allometric scaling of metabolic rate in adult honeybees

Resting metabolic rate (RMR) is a fundamental physiological measure linked to numerous aspects of organismal function, including lifespan. Although dietary restriction in insects during larval growth/development affects adult RMR, the impact of larval diet quality on adult RMR has not been studied. Using in vitro rearing to control larval diet quality, we determined the effect of dietary protein and carbohydrate on honeybee survival-to-adulthood, time-to-eclosion, body mass/size and adult RMR. High carbohydrate larval diets increased survival-to-adulthood and time-to-eclosion compared to both low carbohydrate and high protein diets. Upon emergence, bees reared on the high protein diet were smaller and lighter than those reared on other diets, whilst those raised on the high carbohydrate diet varied more in body mass. Newly emerged adult bees reared on the high carbohydrate diet showed a significantly steeper increase in allometric scaling of RMR compared to those reared on other diets. This suggests that diet quality influences survival-to-adulthood, time-to-eclosion, and the allometric scaling of RMR. Given that agricultural intensification and increasing urbanisation have led to a decrease in both forage availability and dietary diversity for bees, our results are critical to improving understanding of the impacts of poor developmental nutrition on bee growth/development and physiology. Summary statementWe show, for the first time, that the nutritional quality of insect larval diets affects the scaling of metabolic rate with body mass in newly emerged adult honeybees.

physiology↗

Impact of central complex lesions on visual orientation in ants: Turning behaviour, but not the overall movement direction, is disrupted

Wood ants are excellent navigators using a combination of innate and learnt navigational strategies to travel between their nest and feeding sites. Visual navigation in ants has been studied extensively, however, we only know little about the underlying neural mechanisms. The central complex (CX) is located at the midline of the insect brain. It receives sensory input that allows an insect to keep track of the direction of sensory cues relative to its own orientation and to control movement. We show here direct evidence for the involvement of the central complex in the innate visual orientation response of freely moving wood ants. Lesions in the CX disrupted the control of turning in a lateralised manner, but had no effect on the overall heading direction, walking speed or path straightness.

animal behavior and cognition↗

A unified mechanism to support innate and learned use of visual landmark guidance in insects

Insects can navigate efficiently in both novel and familiar environments, and this requires flexiblity in how they are guided by sensory cues. A prominent landmark, for example, can ellicit strong innate behaviours (attraction or menotaxis) but can also be used, after learning, as a specific directional cue as part of a navigation memory. However, the mechanisms that allow both pathways to co-exist, interact or override each other are largely unknown. Here we propose a model for the behavioural integration of innate and learned guidance based on the neuroanatomy of the central complex (CX), adapted to control landmark guided behaviours. We consider a reward signal provided either by an innate attraction to landmarks or a long-term visual memory in the mushroom bodies (MB) that modulates the formation of a local vector memory in the CX. Using an operant strategy for a simulated agent exploring a simple world containing a single visual cue, we show how the generated short-term memory can support both innate and learned steering behaviour. In addition, we show how this architecture is consistent with the observed effects of unilateral MB lesions in ants that cause a reversion to innate behaviour. We suggest the formation of a directional memory in the CX can be interpreted as transforming rewarding (positive or negative) sensory signals into a mapping of the environment that describes the geometrical attractiveness (or repulsion). We discuss how this scheme might represent an ideal way to combine multisensory information gathered during the exploration of an environment and support optimized cue integration. 1 Author summaryIn this paper, we modeled the neural pathway allowing insects to perform landmark guided behaviours using their internal compass. First, we observed the intrinsic property of the connectome, extracted from drosophila online database, between the internal compass neurons and the steering neurons to support an oriented behaviour towards a single landmark. Then, we proposed and evaluated an adaptation of the bees path integration neural circuit, to sustain flexible landmark guidance behaviours such as attraction or menotaxis. We showed the model ability to form a memory during the exploration of the local environment to support both innate or learned navigation behaviour using a single landmark in the environment. In addtion, we demonstrated the transformation of a simple goodness/badness signal, from innate or long-term memory pathways, into an oriented steering signal that could be applied to other sensory pathways. Furthermore, by reproducing lesion experiments in the mushroom bodies of wood ants we highlight the consistency of the model with biological observation. We then discuss the different emergent properties and the potential outcome that this local, and operant, memory supports.

animal behavior and cognition↗

Transfer of orientation memories in untethered wood ants (Formica rufa) from walking in an arena to walking on a motion compensation treadmill

The scale of natural insect navigation during foraging makes it challenging to study, in a controlled way, the navigation processes that an insect brain can support. Virtual Reality and trackball setups have offered experimental control over visual environments while studying tethered insects, but potential limitations and confounds introduced by tethering motivates the development of alternative untethered solutions. In this paper we validate the use of a motion compensator (or treadmill) to study visually-driven behaviour of freely moving wood ants (Formica rufa). We show how this setup allows naturalistic walking behaviour and motivation over long timeframes. Furthermore, we show that ants are able to transfer associative and navigational memories from classical maze and arena contexts to our treadmill. Thus, we demonstrate the possibility to study navigational behaviour over ecologically relevant durations (and virtual distances) in precisely controlled environments, bridging the gap between natural and highly controlled laboratory experiments. 1 Summary statementWe have developed and validated a motion compensating treadmill for wood ants which opens new perspectives to study insect navigation behaviour in a fully controlled manner over ecologically relevant durations.

animal behavior and cognition↗

Malpighamoeba infection compromises fluid secretion and P-glycoprotein detoxification in Malpighian tubules

Malpighian tubules, analogous to vertebrate nephrons, play a key role in insect osmoregulation and detoxification. Tubules can become infected with a protozoan, Malpighamoeba, which damages their epithelial cells, potentially compromising their function. Here we used a modified Ramsay assay to quantify the impact of Malpighamoeba infection on fluid secretion and P-glycoprotein-dependent detoxification by desert locust Malpighian tubules. Infected tubules have a greater surface area and a higher fluid secretion rate than uninfected tubules. Infection also impairs P-glycoprotein-dependent detoxification by reducing the net rhodamine extrusion per surface area. However, due to the increased surface area and fluid secretion rate, infected tubules have similar total net extrusion per tubule to uninfected tubules. Increased fluid secretion rate of infected tubules likely exposes locusts to greater water stress and increased energy costs. Coupled with reduced efficiency of P-glycoprotein detoxification per surface area, Malpighamoeba infection is likely to reduce insect survival in natural environments.

physiology↗

P-glycoprotein Detoxification by the Malpighian Tubules of the Desert Locust

Detoxification is essential for allowing animals to remove toxic substances present in their diet or generated as a biproduct of their metabolism. By transporting a wide range of potentially noxious substrates, active transporters of the ABC transporter family play an important role in detoxification. One such class of transporters are the multidrug resistance P-glycoprotein transporters. Here, we investigated P-glycoprotein transport in the Malpighian tubules of the desert locust (Schistocerca gregaria), a species whose diet includes plants that contain toxic secondary metabolites. To this end, we studied transporter physiology using a modified Ramsay assay in which ex vivo Malpighian tubules are incubated in different solutions containing the P-glycoprotein substrate dye rhodamine B in combination with different concentrations of the P-glycoprotein inhibitor verapamil. Our evidence shows that: (i) the Malpighian tubules contain a P-glycoprotein; (ii) tubule surface area is positively correlated with the tubule fluid secretion rate; and (iii) as the fluid secretion rate increases so too does the net extrusion of rhodamine B. We were able to quantify precisely the relationships between the fluid secretion, surface area, and net extrusion. We interpret these results in the context of the life history and foraging ecology of desert locusts. We argue that P-glycoproteins play an important role in the detoxification by contributing to the removal of xenobiotic substances from the haemolymph, thereby enabling gregarious desert locusts to maintain toxicity through the ingestion of toxic plants without suffering the deleterious effects themselves.

physiology↗

Modulation of voltage-dependent K+ conductances in photoreceptors trades off investment in contrast gain for bandwidth

Modulation is essential for adjusting neurons to prevailing conditions and differing demands. Yet understanding how modulators adjust neuronal properties to alter information processing remains unclear, as is the impact of neuromodulation on energy consumption. Here we combine two computational models, one Hodgkin-Huxley type and the other analytic, to investigate the effects of neuromodulation upon Drosophila melanogaster photoreceptors. Voltage-dependent K+ conductances: (i) activate upon depolarisation to reduce membrane resistance and adjust bandwidth to functional requirements; (ii) produce negative feedback to increase bandwidth in an energy efficient way; (iii) produce shunt-peaking thereby increasing the membrane gain bandwidth product; and (iv) inactivate to amplify low frequencies. Through their effects on the voltage-dependent K+ conductances, three modulators, serotonin, calmodulin and PIP2, trade-off contrast gain against membrane bandwidth. Serotonin shifts the photoreceptor performance towards higher contrast gains and lower membrane bandwidths, whereas PIP2 and calmodulin shift performance towards lower contrast gains and higher membrane bandwidths. These neuromodulators have little effect upon the overall energy consumed by photoreceptors, instead they redistribute the energy invested in gain versus bandwidth. This demonstrates how modulators can shift neuronal information processing within the limitations of biophysics and energy consumption.

neuroscience↗

Voltage-dependent K+ Channels Improve the Energy Efficiency of Signalling in Blowfly Photoreceptors

Voltage-dependent conductances in many spiking neurons are tuned to reduce action potential energy consumption, so improving the energy efficiency of spike coding. However, the contribution of voltage-dependent conductances to the energy efficiency of analogue coding, by graded potentials in dendrites and non-spiking neurons, remains unclear. We investigate the contribution of voltage-dependent conductances to the energy efficiency of analogue coding by modelling blowfly R1-6 photoreceptor membrane. Two voltage-dependent delayed rectifier K+ conductances (DRs) shape the membrane's voltage response and contribute to light adaptation. They make two types of energy saving. By reducing membrane resistance upon depolarisation they convert the cheap, low bandwidth membrane needed in dim light to the expensive high bandwidth membrane needed in bright light. This investment of energy in bandwidth according to functional requirements can halve daily energy consumption. Second, DRs produce negative feedback that reduces membrane impedance and increases bandwidth. This negative feedback allows an active membrane with DRs to consume at least 30% less energy than a passive membrane with the same capacitance and bandwidth. Voltage gated conductances in other non-spiking neurons, and in dendrites, might be organized to make similar savings.

biophysics↗