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Thermal acclimation is a mechanism that ectotherms use to maintain performance across a range of temperatures. In variable environments, acclimating quickly may be as important as acclimation capacity. The phenotypic changes comprising acclimation require energy and nutrients that ectotherms obtain from their diet. Thus, diet may be a critical factor determining acclimation rate and capacity. Using a temperate omnivorous fish, opaleye (Girella nigricans), we tested the hypotheses that diet can impact thermal acclimation rate and capacity for cardiac performance. We offered juvenile opaleye an ad-lib herbivorous (algae), carnivorous (shrimp), or omnivorous (algae and shrimp) diet for two weeks at 12°C and measured the thermal performance curve (TPC) for maximum heart rate (fHmax) and cardiac thermal limits. Next, we raised the temperature in the holding tanks from 12 to 20ºC, mimicking an abrupt heatwave, and independently sampled fish on days 1, 3, 7, and 14 post-temperature change using the same cardiac test. Acclimation capacity for fHmax was sensitive to diet, with the herbivorous treatment displaying the smallest change in fHmax. However, acclimation rate and all cardiac thermal limits were insensitive to diet, with &amp;gt;60% of acclimation capacity occurring in the first 3 days at 20°C. Our results indicate that for generalist species, like opaleye, variation in diet is an important determinant of thermal performance on environmentally relevant timescales. Our findings also add to growing evidence that it is essential to integrate acclimation time into our predictions of species responses to temperature change.

SEB Conference 2022

Diet effects on acclimation rate and capacity for maximum heart rate in a temperate fish (Girella nigricans)

Thermal acclimation is a mechanism that ectotherms use to maintain performance across a range of temperatures. In variable environments, acclimating quickly may be as important as acclimation capacity. The phenotypic changes comprising acclimation require energy and nutrients that ectotherms obtain from their diet. Thus, diet may be a critical factor determining acclimation rate and capacity. Using a temperate omnivorous fish, opaleye (Girella nigricans), we tested the hypotheses that diet can impact thermal acclimation rate and capacity for cardiac performance. We offered juvenile opaleye an ad-lib herbivorous (algae), carnivorous (shrimp), or omnivorous (algae and shrimp) diet for two weeks at 12°C and measured the thermal performance curve (TPC) for maximum heart rate (fHmax) and cardiac thermal limits. Next, we raised the temperature in the holding tanks from 12 to 20ºC, mimicking an abrupt heatwave, and independently sampled fish on days 1, 3, 7, and 14 post-temperature change using the same cardiac test. Acclimation capacity for fHmax was sensitive to diet, with the herbivorous treatment displaying the smallest change in fHmax. However, acclimation rate and all cardiac thermal limits were insensitive to diet, with &gt;60% of acclimation capacity occurring in the first 3 days at 20°C. Our results indicate that for generalist species, like opaleye, variation in diet is an important determinant of thermal performance on environmentally relevant timescales. Our findings also add to growing evidence that it is essential to integrate acclimation time into our predictions of species responses to temperature change.

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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.

All animals must acquire food for energy, but there is a vast diversity in how different species and even different individuals approach this task. Individuals within a species appear to fall along a bold-shy continuum, whereby some fish acquire food aggressively and with seemingly high risk, while others appear more opportunistic and cautious. Greater food consumption generally results in faster growth, but only if the energy acquired through food is more than enough to compensate for heightened metabolism associated with a more active lifestyle. Fast-growing phenotypes also tend to have elevated baseline metabolism – at least when food is plentiful – which further complicates the link between food consumption and growth. The net energy gained from a meal (as calculated from the specific dynamic action (SDA) coefficient) is optimised with larger meal sizes, but the digestion of large meals can erode the aerobic metabolic scope available for other critical activities such as predator avoidance. Thus, it is expected that fish in predator-rich habitats should regulate meal sizes to maximise growth efficiency without dangerously compromising aerobic capacity, and this balance may differ between individual metabolic phenotypes. This presentation will discuss these complicated interplays with a goal to better understand what drives intraspecific differences in growth performance.

Why some fish grow faster than others: examining the interplay between metabolic phenotype, predator threat and growth performance

In several organisms including fish, lipids are the most efficient source of energy compared to other nutrients. Some fatty acids (e.g. oleic acid, palmitic acid) are known to be preferentially used by organisms to create or to store energy. Here, we aimed to understand the relationship between FA profile, individual growth performance and well-being of European sea bass (Dicentrarchus labrax). For that, we coupled the measurements of growth rate and Fulton’s condition factor (K), both widely used to estimate growth and the well-being of a fish, to an innovative non-lethal sampling method for FA analysis that allows us to measure the evolution of the fatty acid profile individually. Eighteen tagged sea bass juveniles were reared during 130 days in the same food and temperature conditions, in triplicate. White muscle subcutaneous biopsy was carried out on each fish at day 0 and day 130 for FA analysis. Fish were weighted and measured to calculate growth rate (Thermal Growth Coefficient, TGC) and K at d0 and  d130. The fatty acid profiles of the three best and lowest performing fish (TGC related) were compared. The two biopsies performed over the 130 days induced no mortality. All the fish had positive TGC and showed an increase in K (1.01 ±0.15 at d0; 1.20 ±0.12 at d130). The results will be discussed trying to establish a link between FA, TGC and K, on an individual scale.

Relation between fatty acid profile, growth rate and condition factor using a non-lethal sampling method in European sea bass.

The cold of temperate winters slows, and may constrain, ectotherm physiology. Yet many fish species remain active in the winter, with continued performance facilitated by physiological compensation. Conversely, certain species (e.g., cunner, Tautogolabrus adspersus) enter winter dormancy – an energy-savings strategy characterized by inactivity, fasting, and slow metabolism – which allows them to endure frigid, food-poor winters and persist at poleward latitudes. We hypothesized that winter dormancy is a consequence of severe constraints on digestion and growth in the cold, which make it inefficient to remain active and feeding. Cunner become dormant below ~7.5°C, so we predicted negative growth and zero feeding below ~7.5°C even when provided food. In voluntarily feeding fish acclimated to 15, 9, or 3°C, daily food consumption and specific growth rates decreased significantly with declining temperature, and dormant fish at 3°C had near-zero feeding rates with negative growth. We then repeated this experiment with force-feeding 1% body weight every third day of acclimation to determine if fasting and weight loss results from physiological constraints of cold on digestion and growth processes. Contrary to our hypothesis, force-fed cunner showed positive growth at 3°C, indicating that the fasting, inactive, and non-foraging phenotype characteristic of dormancy is a behavioural response rather than a consequence of intrinsic physiological constraints. We are currently analyzing specific dynamic action. Our findings are consistent with an overarching conclusion emerging from our work on cunner: physiological performance is not severely constrained by cold in winter-dormant fishes, and ecological factors are more likely to be driving winter dormancy. 

Fasting in winter-dormant fish is a behavioural response rather than a consequence of constraints of cold on digestion and growth

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.

Effects of feeding on the energetics of torpor in hibernating species

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.

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