Stomatopod crustaceans have among the most complex eyes in the animal kingdom, with up to twelve different color detection channels. The capabilities of these unique eyes include photoreception of ultraviolet (UV) wavelengths (<400 nm). UV vision has been well characterized in adult stomatopods but has not been previously demonstrated in the comparatively simpler larval eye. Larval stomatopod eyes are developmentally distinct from their adult counterpart and have been described as lacking the visual pigment diversity and morphological specializations found in adult eyes. However, recent studies have provided evidence that larval stomatopod eyes are more complex than previously thought and warrant closer investigation. Using electroretinogram recordings in live animals we found physiological evidence of blue and UV sensitive photoreceptors in larvae of the Caribbean stomatopod species Neogonodactylus oerstedii. Transcriptomes of individual larvae were used to identify the expression of three distinct UV opsins transcripts, which may indicate the presence of multiple UV spectral channels. This is the first paper to document UV vision in any larval stomatopod, expanding our understanding of the importance of UV sensitivity in plankton. Similar to adults, larval stomatopod eyes are more complex than expected and contain previously uncharacterized molecular diversity and physiological functions.
Breeding is costly for many animals, including birds that must deliver food to a central place (i.e. nest). Measuring energy expenditure throughout the breeding season can provide valuable insights on physiological limitations by highlighting periods of high demands, and ultimately allows to improve conservation strategies. However, quantifying energy expenditure in wildlife can be challenging, as existing methods do not measure both active (e.g. foraging) and resting energy costs across short and long time scales. Here, we develop a novel method for comparing active and resting costs in 66 pre-breeding and breeding seabirds (black-legged kittiwakes; Rissa tridactyla) by combining accelerometry and triiodothyronine (T3), as proxies for active and resting costs, respectively. Activity energy costs were higher during incubation (p=0.0004) and chick-rearing (p<0.0001) compared to pre-laying, due to an increase in time spent in flight of 11% (p=0.0005) and 15% (p<0.0001), respectively. Levels of T3, reflecting resting costs, peaked marginally during incubation with an average concentration of 4.71±1.97 pg mL−1 in comparison to 2.66±1.30 pg mL−1 in pre-laying (p=0.05), and 3.16±2.85 pg mL−1 in chick-rearing (p=11). Thus, although chick-rearing is often assumed to be the costliest breeding stage by multiple studies, our results suggest that incubation could be more costly due to high resting costs. We highlight the importance of accounting for both active and resting costs when assessing energy expenditure.
Exposure to high PCO2/low pH seawater induces behavioural alterations in fish; a possible explanation for this is a reversal of Cl−/HCO3− currents through GABAA receptors (the GABAA receptor theory). However, the main evidence for this is that gabazine, a GABAA receptor antagonist, reverses these effects when applied to the water, assuming that exposure to systems other than the CNS would be without effect. Here, we show the expression of both metabotropic and ionotropic GABA receptors, and the presence of GABAA receptor protein, in the olfactory epithelium (OE) of gilthead seabream. Furthermore, exposure of the OE to muscimol (a specific GABAA receptor agonist) increases or decreases the apparent olfactory sensitivity to some odorants. Thus, although the exact function of GABAA receptors in the OE is not yet clear, this may complicate the interpretation of studies wherein water-borne gabazine is used to reverse the effects of high CO2 levels on olfactory-driven behaviour in fish.
Small bipedal hoppers, including kangaroo rats, are thought to not benefit from substantial elastic energy storage and return during hopping. However, recent species-specific material properties research suggests that, despite relative thickness, the ankle extensor tendons of these small hoppers are considerably more compliant than had been assumed. With faster locomotor speeds demanding higher forces, a lower tendon stiffness suggests greater tendon deformation and thus a greater potential for elastic energy storage and return with increasing speed. Using the elastic modulus values specific to kangaroo rat tendons, we sought to determine how much elastic energy is stored and returned during hopping across a range of speeds. In vivo techniques were used to record tendon force in the ankle extensors during steady-speed hopping. Our data support the hypothesis that the ankle extensor tendons of kangaroo rats store and return elastic energy in relation to hopping speed, storing more at faster speeds. Despite storing comparatively less elastic energy than larger hoppers, this relationship between speed and energy storage offer novel evidence of a functionally similar energy storage mechanism, operating irrespective of body size or tendon thickness, across the distal muscle-tendon units of both small and large bipedal hoppers.
Many fishes use substantial cranial kinesis to rapidly increase buccal cavity volume, pulling prey into the mouth via suction feeding. Living polypterids are a key lineage for understanding the evolution and biomechanics of suction feeding due to their phylogenetic position and unique morphology. Polypterus bichir have fewer mobile cranial elements compared to teleosts (e.g., immobile [pre]maxillae) but successfully generate suction through dorsal, ventral, and lateral oral cavity expansion. However, the relative contributions of these motions to suction feeding success have not been quantified. Additionally, extensive body musculature and lack of opercular jaw opening linkages make P. bichir of interest for examining the role of cranial vs. axial muscles in driving mandibular depression. Here we analyze the kinematics of buccal expansion during suction feeding in P. bichir using X-Ray Reconstruction of Moving Morphology (XROMM) and quantify the contributions of skeletal elements to oral cavity volume expansion and prey capture. Mouth gape peaks early in the strike, followed by maximum cleithral and ceratohyal rotations, and finally by opercular and suspensorial abductions, maintaining the anterior-to-posterior movement of water. Using a new method of quantifying bones’ relative contributions to volume change (RCVC) we demonstrate that ceratohyal kinematics are the most significant drivers of oral cavity volume change. All measured cranial bone motions, except abduction of the suspensorium, are correlated with prey motion. Lastly, cleithral retraction is largely concurrent with ceratohyal retraction and jaw depression while the sternohyoideus maintains constant length, suggesting a central role of the axial muscles, cleithrum, and ceratohyal in ventral expansion.
Estimates of the energetic costs of locomotion (COL) at different activity levels are necessary to answer fundamental eco-physiological questions and to understand the impacts of anthropogenic disturbance to marine mammals. We combined estimates of energetic costs derived from breath-by-breath respirometry with measurements of overall dynamic body acceleration (ODBA) from biologging tags to validate ODBA as a proxy for COL in trained common bottlenose dolphins (Tursiops truncatus). We measured resting metabolic rate (RMR); mean individual RMR was 0.71-1.42 times that of a similarly sized terrestrial mammal and agreed with past measurements which used breath-by-breath and flow-through respirometry. We also measured energy expenditure during submerged swim trials, at primarily moderate exercise levels. We subtracted RMR to obtain COL, and normalized COL by body size to incorporate individual swimming efficiencies. We found both mass-specific energy expenditure and mass-specific COL were linearly related with ODBA. Measurements of activity level and cost of transport (the energy required to move a given distance) improve understanding of the costs of locomotion in marine mammals. The strength of the correlation between ODBA and COL varied among individuals, but the overall relationship can be used at a broad scale to estimate the energetic costs of disturbance, daily locomotion costs to build energy budgets, and investigate the costs of diving in free-ranging animals where bio-logging data are available. We propose that a similar approach could be applied to other cetacean species.
Cryoprotection is of interest in many fields of research, necessitating a greater understanding of different cryoprotective agents. Antifreeze proteins have been identified that have the ability to confer cryoprotection in certain organisms. Antifreeze proteins are an evolutionary adaptation that contributes to the freeze resistance of certain fish, insects, bacteria, and plants. These proteins adsorb to an ice crystal's surface and restrict its growth within a certain temperature range. We investigated the ability of an antifreeze protein from the desert beetle Anatolica polita, ApAFP752, to confer cryoprotection in the frog Xenopus laevis. X. laevis eggs and embryos microinjected with ApAFP752 exhibited reduced damage and increased survival after a freeze/thaw cycle in a concentration-dependent manner. We also demonstrate that ApAFP752 localizes to the plasma membrane in eggs and embryonic blastomeres and is not toxic for early development. These studies show the potential of an insect antifreeze protein to confer cryoprotection in amphibian eggs and embryos.
Fish in coastal ecosystems can be exposed to acute variations in CO2 of between 0.2-1 kPa CO2 (2,000 - 10,000 µatm). Coping with this environmental challenge will depend on the ability to rapidly compensate the internal acid-base disturbance caused by sudden exposure to high environmental CO2 (blood and tissue acidosis); however, studies about the speed of acid-base regulatory responses in marine fish are scarce. We observed that upon sudden exposure to ∼1 kPa CO2, European sea bass (Dicentrarchus labrax) completely regulate erythrocyte intracellular pH within ∼40 minutes, thus restoring haemoglobin-O2 affinity to pre-exposure levels. Moreover, blood pH returned to normal levels within ∼2 hours, which is one of the fastest acid-base recoveries documented in any fish. This was achieved via a large upregulation of net acid excretion and accumulation of HCO3− in blood, which increased from ∼4 to ∼22 mM. While the abundance and intracellular localisation of gill Na+/K+-ATPase (NKA) and Na+/H+ exchanger 3 (NHE3) remained unchanged, the apical surface area of acid-excreting gill ionocytes doubled. This constitutes a novel mechanism for rapidly increasing acid excretion during sudden blood acidosis. Rapid acid-base regulation was completely prevented when the same high CO2 exposure occurred in seawater with experimentally reduced HCO3− and pH, likely because reduced environmental pH inhibited gill H+ excretion via NHE3. The rapid and robust acid-base regulatory responses identified will enable European sea bass to maintain physiological performance during large and sudden CO2 fluctuations that naturally occur in coastal environments.
Within populations, phenotypic plasticity may allow adaptive phenotypic variation in response to selection generated by environmental heterogeneity. For instance, in multivoltine species, seasonal changes between and within generations may trigger morphological and physiological variation enhancing fitness under different environmental conditions. These seasonal changes may irreversibly affect adult phenotypes when experienced during development. Yet, the irreversible effects of developmental plasticity on adult morphology have rarely been linked to life-history traits even though they may affect different fitness components such as reproduction, mobility and self-maintenance. To address this issue, we raised larvae of Pieris napi butterflies under warm or cool conditions to subsequently compare adult performance in terms of reproduction performance (as assessed through fecundity), displacement capacity (as assessed through flight propensity and endurance) and self-maintenance (as assessed through the measurement of oxidative markers). As expected in ectotherms, individuals developed faster under warm conditions and were smaller than individuals developing under cool conditions. They also had more slender wings and showed a higher wing surface ratio. These morphological differences were associated with changes in the reproductive and flight performances of adults, as individuals developing under warm conditions laid fewer eggs and flew larger distances. Accordingly, the examination of their oxidative status suggested that individuals developing under warm conditions invested more strongly into self-maintenance than individuals developing under cool conditions (possibly at the expense of reproduction). Overall, our results indicate that developmental conditions have long-term consequences on several adult traits in butterflies. This plasticity likely acts on life history strategies for each generation to keep pace with seasonal variations and may facilitate acclimation processes in the context of climate change.
The intramandibular joint (IMJ) is a secondary point of movement between the two major bones of the lower jaw. It has independently evolved in several groups of teleost fishes, each time representing a departure from related species in which the mandible functions as a single structure rotating only at the quadratomandibular joint (QMJ). In this study, we examine kinematic consequences of the IMJ novelty in a freshwater characiform fish, the herbivorous Distichodus sexfasciatus. We combine traditional kinematic approaches with trajectory-based analysis of motion shapes to compare patterns of prey capture movements during substrate biting, the fish's native feeding mode, and suction of prey from the water column. We find that the IMJ enables complex jaw motions and contributes to feeding versatility by allowing the fish to modulate its kinematics in response to different prey and to various scenarios of jaw-substrate interaction. Implications of the IMJ include context-dependent movements of lower versus upper jaws, enhanced lower jaw protrusion, and the ability to maintain contact between the teeth and substrate throughout the jaw closing or biting phase of the motion. The IMJ in D. sexfasciatus appears to be an adaptation for removing attached benthic prey, consistent with its function in other groups that have evolved the joint. This study builds on our understanding of the role of the IMJ during prey capture and provides insights into broader implications of the innovative trait.