France

Torpor is a state of active metabolic depression associated with a decrease of body temperature that enables individuals to save energy to cope with environmental fluctuations. Heterothermic species can use short, daily bouts of torpor during the active season, e.g., for young individuals to sustain processes of growth, development and pre-hibernation fattening. Hibernators can also employ torpor bouts lasting several days, weeks or months, called hibernation, to survive long winters with no or little food available. Feeding can affect the use of torpor and the seasonal expression of hibernation. For instance, reduced food availability facilitates the use of torpor, which in turn can increase nutrient assimilation during euthermic phases. Also, various proportions of omega fatty acids modulate hibernation onset and impacts hibernation performances, notably the duration and depth of torpor bouts, during the winter. Saturated fatty acids ensure the optimal fuelling of hibernation, while some unsaturated fatty acids regulate oxidative and metabolic functions including the proper functioning of the heart, a key organ to maintain the activity during deep torpor. Further, contrasted torpor and hibernating patterns, resulting from feeding regimes that differ in terms of food quantity and/or quality, can lead to contrasted life-history strategies and impacts on somatic maintenance, survival and longevity. In this talk, I will present evidence for effects of feeding on the seasonal regulations of the expression of torpor and hibernation as strategies affecting the survival and life-history traits of individuals from hibernating species.

SEB Conference 2022

Effects of feeding on the energetics of torpor in hibernating species

technical paper

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2022 found over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years - Montpellier, France.

Migratory flight requires birds to sustain high levels of energy expenditure, fueled almost exclusively by fat, for prolonged periods of time. Beyond fueling flight, the types of dietary fatty acids may influence performance. The natural doping hypothesis proposes that shorebirds feed on diets rich in essential n-3 long chain polyunsaturated fatty acids (LCPUFA), which help prime the flight muscles for endurance flight by enhancing membrane fludity, promoting rapid fatty acid transport, and activating cellular signalling pathways to increase aerobic and fatty acid oxidation capacity. We fed western sandpipers (Calidris mauri) formulated diets low or high in n-3 LCPUFA (EPA and DHA) and flew them for up to 8 hours in a wind tunnel to assess endurance flight performance. We found that a diet high in n-3 LCPUFA decreased flight energy expenditure by 12%. Activities of key oxidative enzymes, citrate synthase and carnitine palmitoyl transferase were significantly greater in the flight muscles of birds fed the n-3 LCPUFA enriched diet, and we are investigating further effects on the regulation of lipid metabolism and oxidative capacity. In addition, we present evidence for limited capacity for endogenous synthesis of n-3 LCPUFA from precursor fatty acids, suggesting an essential dietary requirement for n-3 LCPUFA. These findings support the natural doping hypothesis by demonstrating performance-enhancing effects at the biochemical and whole animal level, and they indicate a critical role of dietary n-3 LCPUFA during migration for shorebirds.

Flight testing natural doping: Influence of dietary n-3 long chain polyunsaturated fatty acids on migratory performance in western sandpipers

Changes in the early-life microbiota of hosts might affect infectious disease risk throughout life, if such disruptions during formative times alter immune system development. For this talk, I present empirical evidence that an early-life disruption of gut microbiota has immediate and long-term consequences on parasite resistance across taxa, including Cuban tree frogs and passerine birds. In these studies, we experimentally manipulated the gut microbiota of hosts, during the immune developmental period, with mild antibiotics then quantified their ability to resist parasitic nematodes (frogs) or nest flies (birds). An early-life microbiota disruption had varying effects on host resistance to parasitism. A microbiota disruption in tapoles led to a decrease in parasite resistance later in life, whereas a disruption in nestling birds lead to either an increase or decrease in resistance to nest flies, depending on the host species. These results support the idea that preventing early-life disruption of host-associated microbiota might confer protection against diseases, but this idea depends on the host taxa.

Early-life disruption of gut microbiota affects resistance to parasites

Many multicellular organisms in streams undergo metamorphosis during their transition from freshwater to terrestrial life-stages. During metamorphosis, chemical concentrations can change drastically in the body tissues, making it difficult to use aquatic contaminant data to predict risk to terrestrial consumers. This talk will summarize research that attempts to resolve this difficulty using stage-structured approaches to ecotoxicology.

Metamorphosis and the impact of contaminants on ecological subsidies

Complex jaw kinematics during chewing are often interpreted as a derived amniote trait, or even a trait unique to mammals. Contrary to these views, this review compiles data from diverse gnathostome jaw systems, including recent biplanar videofluoroscopy analyzes to support the relegation of the origin of rhythmic and cyclic chewing with dimensionally complex jaw kinematics to the base of the gnathostome phylogeny. These data come from taxa often claimed not to chew but instead swallow food whole or relatively unprocessed, including elasmobranch stingrays, teleostean pacus, sirenid salamanders, and anseriform birds. The new examples of dimensionally complex chewing include not only dorsoventral (arcuate) jaw rotations, but also rostrocaudal (propalinal) and transverse jaw movements, which are jaw movements considered diagnostic of mammalian mastication. Like in mammals, propalinal and transverse jaw movements across these groups are facilitated by complex suspensorial and jaw joint anatomies and driven by architecturally diverse jaw adductor muscles. Dimensionally complex chewing kinematics are not limited to mandibular motion but are also seen in hyoid (tongue) kinematics from suction feeding to chewing in terrestrial newts and ambystomatid salamanders, suggesting that the origin of 3D food handling predates mammals. Future studies should include comparative sensorimotor analyses of basal, dimensionally complex chewing systems to determine how metabolic efficiency is maintained and dental wear is minimized to extend individual life-spans across these diverse vertebrate groups.

Dimensionally complex chewing kinematics occur across vertebrates

Rorqual whales are lunge filter-feeders that use baleen plates to process millions of liters of prey-laden water. Baleen is a keratinous oral tissue that hangs down from the roof of the mouth in bi-laterally symmetrical racks, with larger keratin plates positioned labially and smaller plates positioned lingually. The edges of the baleen plate fray into hairs, or fringes, that interlock, creating a dense mat. This mat allows the enormous amount of water engulfed to flow out of the oropharyngeal cavity and retains the prey captured. To define the morphological parameters that dictate water flow and prey capture, we used a multimodal approach to visualize and describe the hierarchical anatomy of baleen across five species of rorqual whales that span an order of magnitude in body length. We hypothesized that baleen morphology would vary by species and prey preference. We used computed tomography (CT) and scanning electron microscopy (SEM) to quantify and understand how variability in baleen morphology may affect filtration. CT showed cylindrical keratin hairs embedded in the baleen plates growing out of the gum tissue. SEM revealed that the keratin plates are worn away at the ventral side, peeling away the exterior layers and exposing the bristles. Although many morphological features of rorquals scale with body size, hair diameter does not. The differences in filter depth, hair diameter, and hair density that we found across the species may not be a proxy for prey size, but instead may reflect changes in resistance throughout the filter that affect fluid flow. 

Comparative morphology of rorqual whale baleen

Despite many decades of research on how fish capture food by generating suction, it remains unclear how food is transported to the oesophagus. Especially relatively small food items are expected to follow the trajectory of the engulfed water, which, in theory, should flow towards and in between the branchial arches. These food items should then end up sieved by the gill rakers. So then how can food be intercepted, for example by the pharyngeal jaws, near the entrance of the oesophagus? What type of water flows are used to deposit food centrally at the back of the pharynx? Using our stereoscopic high-speed x-ray video system (3D2YMOX) in conjunction with a newly developed protocol of constructing small, neutrally buoyant tracers of water flow with X-rays, we managed to visualise intra-oral water flows in tilapia and carp. Tilapia showed a strong jet in the centre of the mouth cavity, often enabling a direct deposit of the food at the pharyngeal jaw region. At the sides of the mouth cavity, flow tends to recirculate, similar to the vena contracta effect behind a narrow nozzle (the mouth aperture in this case). Such flow pattern also appeared in earlier numerical simulations, but was (apparently wrongly) assumed to be an artefact of modelling inaccuracies. This flow pattern could contribute to improving suction feeding performance and efficiency. The central jet pattern was less pronounced in carps, which could be related to their predominantly bottom-detritus feeding habit relying specifically on branchial sieving and tasting before ingestion.

Intraoral waterflows in feeding carp and tilapia

Recent application of biplanar videoradiography and the XROMM workflow to the study of hyolingual kinematics in primates provides new insight into tongue movements during chewing and swallowing. During chewing in macaques, during fast open and fast close the molar region of the tongue rolls to the chewing side simultaneously with sagittal flexion. Twisting and flexion reach their maxima early in the fast close phase of chewing cycles, positioning the food bolus between the approaching teeth prior to the power stroke. Nerve block of tactile sensation from trigeminal innervated oral structures decreased feeding performance, and the fast open phase of the gape cycle became significantly longer, relative to the other phases. The tongue made similar shapes in both the control and nerve block conditions, but the pattern of tongue-jaw coordination became significantly more variable after the block. Disruption of oral somatosensation impacts feeding performance by introducing variability into the typically tight pattern of tongue-jaw coordination. During swallowing, tongue base retraction (TBR) drives the food bolus across the oropharynx towards the esophagus but the mechanics of TBR are poorly understood. XROMM of macaque monkeys falsifies both the hypothesis that extrinsic tongue muscle shortening pulls the tongue base posteriorly, and the muscular hydrostat hypothesis that intrinsic muscle shortening displaces the tongue base posteriorly. Our data suggest a novel hydraulic mechanism of TBR in which shortening and rotation of suprahyoid muscles compresses the tongue between the hard palate, hyoid and mouth floor, squeezing the midline tongue base and food bolus into the oropharynx. 

3D Hyolingual Kinematics Reveal New Insights Into Biomechanical And Neural Control Of Chewing And Swallowing In Primates.

Kestrels exhibit steady flight in gusty conditions, including maintaining a headlock whilst soaring in strong winds; known as “windhovering”. Trying to understand what gives them this remarkable ability, and perhaps how this could be utilised in the growing area of drone flight is not feasible outdoors as it would require simultaneous measurements of the impinging atmospheric wind and wing, body and tail kinematics. We describe a novel wind-tunnel facility which enables such studies; whereby an updraft provides the environment to continuously soar, and upstream turbulence grids can generate a range of smooth and turbulent flows. To provide discrete gusts we have also developed a dedicated gust generator where prior calibration gives us time-accurate knowledge of a range of gust profiles. In a range of smooth and turbulent conditions the kinematics of two Nankeen Kestrels were documented using multiple cameras tracking reflective markers fixed to their wings, tails and bodies. Initial results have demonstrated the feasibility of the facility and techniques and have shown insights into the coupling between wing body and tail kinematics. An unexpected finding is that both birds favoured yawed flight (~30 degrees to the mean wind direction) which is potentially due to localising targets in their visual fovea.

Studying Kestrels Soaring in a Wind Tunnel: The Facility, Techniques and Initial Results

Birds’ wings have a high number of potentially independent degrees of freedom of motion. This enables their wings to morph in shape to suit a range of flight conditions, but potentially increases the complexity of flight control. Here we used motion tracking data from Nankeen kestrels (Falco cenchroides) performing steady wind hovering flights in a wind tunnel to study how different degrees of freedom in wing motion changed as the birds held station. To judge the contribution of a particular degree-of-freedom to flight control, metrics such as variance, correlation and control effectiveness were considered, along with Principal Component Analysis. Wing sweep, which represents the flexion/extension movement of the wing, was the major component of almost all wing motions. This was followed by sectional twist at the root, which although showing lower actuation, would have a strong effect on aerodynamic loads. Together these results highlight the major wing motions which contribute to the wind hovering flight of kestrels and suggest degrees of freedom to concentrate on when considering the design of future agile morphing wing uncrewed air vehicles.

Wing biomechanic couplings of kestrels during wind hovering flight

Animals are frequently faced with the challenge of negotiating unfamiliar structured environments during goal-oriented behaviours. Recent work on visually-guided flight through clutter has conceptualised this as a process of identifying and negotiating gaps that are broadly aligned with the animal’s expected or intended goal. These gaps are thereby conceived as attractors in their own right, rather than as features incidental to obstacles acting as repellers. Here we ask what information birds use to detect and fly through such gaps by tracking pigeons flying through an artificial forest of vertical poles. We find evidence for pigeons combining brightness cues with the sizes of visual gaps available ahead to choose which clearances to fly through. Modelling the free-flight behaviour as a process of sequential gap selection allows us to decompose it into components that can be independently evaluated. We find the observed behaviour is best captured by an autoregressive model including the effect of brightness, the absolute distance between obstacles and apparent visual gaps between a bird’s position and the end of the obstacle field. This can, in turn, be combined with established models of pigeon steering to provide a more complete picture of how birds guide their flight through complex environments

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Flight testing natural doping: Influence of dietary n-3 long chain polyunsaturated fatty acids on migratory performance in western sandpipers

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