Journal of Experimental Biology

Till, Harter,

doi: 10.1242/jeb.214312pmid: N/A

Climate change is bad, we know that much. But we've also learned that life can cope with change. Many fish can tweak their physiology to deal with warmer, less-oxygenated waters, or to combat the adverse effects of a more acidic ocean – but at what cost? A fish that must work harder to extract oxygen from the water, or to remove acid from its tissues, will have less energy available for the more important things in life, such as chasing prey, finding mates and having sex. Perhaps it's surprising then, that we often study the effects of climate change on well-fed fish in the lab, where energy limitations, such as those that occur in the wild, do not exist. With this in mind, Louise Cominassi at the University of Hamburg, Germany, and her international team of collaborators, set out to test whether feeding changes how fish are affected by climate change. For a year, they held European seabass in different combinations of the two most dire outcomes of climate change: high temperatures (20°C) and elevated CO 2 to simulate ocean acidification. Then, they put half of the fish on a strict diet and let the other half feast to their stomach's content, observing the growth of both groups over several weeks. Not surprisingly, the fish that feasted grew faster than those on a restricted diet. So far, so good. Also, seabass like warm water, which accelerated the growth of both groups. But, here's the kicker: when these fast-growing, warm-water - loving seabass were also exposed to ocean acidification, growth of the well-fed fish slowed dramatically and those on a restricted diet barely grew at all. This fits well with the idea that living in acidified water is costly and, when on a budget, energy spent on fighting acidity is not available for growth. In fact, increasing the seabass’ energy budget with plenty of food improved their growth in acidic water over that of fish on a restricted diet, supporting the idea that a shortage of energy was limiting their growth. So why was growth of the well-fed, warm-water seabass affected by ocean acidification? To answer this question, Cominassi had a closer look at how these animals used the food that they were provided with. When the fish in warm water were offered a feast, those in the acidified water chose to eat less, leading to slower growth. What had ruined their appetite? Cominassi found that the fish's digestion was slower in the acidic water and, generally, those with full stomachs are less peckish. The little food that they did eat, however, was also used less efficiently, meaning less growth per bite, perhaps as a result of the slowing of important digestive enzymes. In the end, when dealing with climate change, feeding changed everything. A major effort is underway to get a grasp on how climate change will affect individual fish species and ultimately impact our ocean ecosystems. However, the waters are muddied by the interacting effects of rising temperature, CO 2 and acidity levels, in addition to the falling water oxygen levels due to the increase in temperature. Surely, some animals can cope with these changes, but whether they can afford to do so is a different question. Energy is a limited resource for any organism and future fish will face the challenge of how to spend that budget to cope with climate change and still have enough left in the tank to go on with their lives. Therefore, studying the effects of climate change on well-fed fish in the lab may underestimate the severity of the problem. As with many other problems in life, dealing with climate change is easiest on a full belly. References Cominassi , L. , Moyano , M. , Claireaux , G. , Howald , S. , Mark , F. C. , Zambonino-Infante , J.-L. and Peck , M. A. ( 2020 ). Food availability modulates the combined effects of ocean acidification and warming on fish growth . Sci. Rep. 10 , 1 - 12 . doi:10.1038/s41598-020-58846-2 Google Scholar Crossref Search ADS © 2020. Published by The Company of Biologists Ltd 2020

Nicole, Geberzahn,;Sébastien, Derégnaucourt,

doi: 10.1242/jeb.220087pmid: 32253282

Many species are able to vocally recognize individual conspecifics and this capacity seems widespread in oscine songbirds. The exact acoustic features used for such recognition are often not clear. In the zebra finch ( Taeniopygia guttata ), the song motif is composed of a few syllables repeated in a fixed sequential order and song bouts include several repetitions of the motif. Here, we used an operant discrimination task, the GO/NOGO procedure, to show that zebra finches are capable of individual vocal recognition even if the bird has to distinguish males that all produce an imitation of the same song model. Furthermore, we studied whether such individual vocal recognition was based on spectro-temporal details of song syllables, i.e. the local fine structure of the song, or on the sequential order in which song syllables are arranged in the song bout. To this end, we trained male and female zebra finches to discriminate songs of one male conspecific from those of four others. After learning this baseline discrimination, subjects were exposed to a novel set of stimuli originating from the same individuals, in order to test for their capability to generalise. Subjects correctly classified those novel stimuli, illustrating their ability for individual vocal recognition. Then they were exposed to hybrid stimuli combining the syllable sequences of one individual with the spectro-temporal features of another. Behavioural responses of subjects to hybrid stimuli suggest that they rely on spectro-temporal details of syllables and might pay less attention to syllable sequences for individual vocal recognition.

Jake, Socha,

doi: 10.1242/jeb.225128pmid: N/A

Packed with tall trees and vine-like lianas, the tropical forests of South and Southeast Asia present a maze for vertebrate flyers. In these forests, a wealth of species – frogs, lizards, snakes, squirrels and colugos – flit about on makeshift wings, trading potential energy of height for the benefit of gliding flight. But without the muscle-powered flapping ability of birds and bats, gliders possess far fewer means for control, making navigating a cluttered forest a potentially perilous endeavor. How do gliders avoid arboreal obstacles while gliding and landing safely? Pranav Khandelwal and Ty Hedrick of the University of North Carolina, USA, studied the flying lizard Draco in an Indian rainforest to see how visual information is integrated with mechanics in real-world gliding. Most quantitative studies of gliding have been done in experimental conditions, but natural gliding may be different when an animal chooses to glide for its own reasons. Khandelwal and his field assistant traveled to the Agumbe Rainforest Research Station in the Western Ghats of India, where they arranged a rig of GoPro cameras to record a population of flying lizards going about the business of gliding in the wild. The lizards glided most often in the mornings, motivated by territoriality and mate pursuit, and the highly portable setup enabled the team to move swiftly to record the glides of multiple flying lizards. To maneuver around obstacles in a cluttered natural environment, a flying animal must create directional forces, or it will plod along its forward path, subservient to Newton's third law. Birds, for example, turn by creating asymmetric forces on the wings by altering their flapping kinematics. It is unclear how flying lizards maneuver, but they must create forces with a different set of tools; mainly, a pair of non-flappable wings made of long ribs embedded in patagial skin and a fixed energy budget set by their initial takeoff height. Khandelwal and Hedrick hypothesized that lizards use these tools guided by their visual view of the world. For example, a lizard might plan its path from the start, choosing a route that requires minimal maneuvering when faced with a forest of obstacles. Alternatively, when gliding they could react immediately to an obstacle as it looms into view, although that could be energetically costly. Finally, the lizards might use some form of vision-based planning for braking when landing, lest they barrel headfirst into their landing site, receiving a deathly smack. To test these ideas, the researchers used stereo recordings to extract the 3D paths, velocities and accelerations of the lizards and the exact locations of the trees in their visual environment. By mapping the locations of all trees in the area, they could calculate all possible combinations of takeoff and landing for comparison with the trees that the lizards actually chose. The lizards appeared to use their knowledge of the lay of the land prior to taking off as they navigated each flight. They chose to jump in directions with less surrounding clutter, producing glides with less maneuvering in the air and, in turn, they wasted less energy. Surprisingly, lizards did not take off directly toward their target tree, leaping instead 10–41 deg off the straight-line path. In the air, flying lizards minimized maneuvering with respect to both the obstacle and the target tree, evidence that they employ a vision-based steering model. The data also provide insight into the lizard's flight biomechanics: modeling revealed that they maneuvered around trees by rolling a maximum of 21 deg, a side tilt that provides lateral force but reduces support for body weight by ∼7%. When landing, the lizards used a visual strategy known as ‘tau-dot’, where they gradually decelerate as they approach a target, a way to reduce impact forces as they land while maintaining enough lift to stay aloft. Overall, flying lizards appear to use visual input to guide all aspects of flight, from takeoff to landing, helping to avoid costly aerial collisions and surviving to climb another tree. References Khandelwal , P. C. and Hedrick , T. L. ( 2020 ). How biomechanics, path planning and sensing enable gliding flight in a natural environment . Proc. R. Soc. B 287 , 20192888 . doi:10.1098/rspb.2019.2888 Google Scholar Crossref Search ADS © 2020. Published by The Company of Biologists Ltd 2020

K., McNab, Brian;A., Weston, Kerry

doi: 10.1242/jeb.212126pmid: 32291323

In this study, we examined the thermal physiology of the endangered New Zealand rockwren ( Xenicus gilviventris ), a member of the Acanthisittidae, a family unique to New Zealand. This family, derived from Gondwana, is thought to be the sister taxon to all other passerines. Rockwrens permanently reside above the climatic timberline at altitudes from 1000 to 2900 m in the mountains of South Island. They feed on invertebrates and in winter face ambient temperatures far below freezing and deep deposits of snow. Their body temperature and rate of metabolism are highly variable. The rockwrens in our study regulated their body temperature at ca. 36.4°C, which in one individual decreased to 33.1°C at an ambient temperature of 9.4°C; its rate of metabolism decreased by 30% and its body temperature then spontaneously returned to 36°C. The rate of metabolism in a second individual twice decreased by 35%, nearly to the basal rate expected from its mass without a decrease in body temperature. The New Zealand rockwren's food habits, entrance into torpor and continuous residence in a thermally demanding environment suggest that it may hibernate. However, for that conclusion to be accepted, evidence of its use of torpor for extended periods is required. Acanthisittids are distinguished from other passerines by the combination of their permanent temperate distribution, thermal flexibility and a propensity to evolve a flightless condition. These characteristics may principally reflect their geographical isolation in a temperate environment isolated from Gondwana for 82 million years in the absence of mammalian predators.

Hamed, Rajabi,;Jan-Henning, Dirks,;N., Gorb, Stanislav

doi: 10.1242/jeb.215194pmid: 32366698

The evolution of wings has played a key role in the success of insect species, allowing them to diversify to fill many niches. Insect wings are complex multifunctional structures, which not only have to withstand aerodynamic forces but also need to resist excessive stresses caused by accidental collisions. This Commentary provides a summary of the literature on damage-reducing morphological adaptations in wings, covering natural causes of wing collisions, their impact on the structural integrity of wings and associated consequences for both insect flight performance and life expectancy. Data from the literature and our own observations suggest that insects have evolved strategies that (i) reduce the likelihood of wing damage and (ii) allow them to cope with damage when it occurs: damage-related fractures are minimized because wings evolved to be damage tolerant and, in the case of wing damage, insects compensate for the reduced aerodynamic efficiency with dedicated changes in flight kinematics.

Takao, Sasaki,;Leo, Danczak,;Beth, Thompson,;Trisha, Morshed,;C., Pratt, Stephen

doi: 10.1242/jeb.221408pmid: 32414865

Many animals use information from conspecifics to change their behavior in adaptive ways. When a rock ant, Temnothorax albipennis , finds food, she returns to her colony and uses a method called tandem running to lead nestmates, one at a time, from the nest to the food. In this way, naive ants can learn the location of a food source. Less clear is whether they also learn navigational cues that guide them from nest to food, although this is often assumed. We tested this idea by tracing the routes of individually marked ants as they followed tandem runs to a feeder, returned to the nest, and later traveled independently back to the food. Our results show, for the first time, that tandem run followers learn specific routes from their leaders. Independent journeys back to the food source were significantly more similar to the routes on which the ants had been led, compared with the routes taken by other tandem runs. In contrast, the homeward journey did not resemble the tandem run route. These results are consistent with followers memorizing visual cues during the tandem run that are useful for recapitulating the outward journey, but not as effective when facing in the opposite direction on the homeward journey. We further showed that foraging routes improved through individual experience over multiple trips but not through the social transfer of route information via tandem running. We discuss our findings in relation to social learning and integration of individual and social information in ants.

Krishnamoorthy, Krishnan,;Shahriar, Nafi, Asif;Roi, Gurka,;Roi, Holzman,

doi: 10.1242/jeb.214734pmid: 32253288

Fish larvae are the smallest self-sustaining vertebrates. As such, they face multiple challenges that stem from their minute size, and from the hydrodynamic regime in which they dwell. This regime, of intermediate Reynolds numbers, was shown to affect the swimming of larval fish and impede their ability to capture prey. Prey capture is impeded because smaller larvae produce weaker suction flows, exerting weaker forces on the prey. Previous observations on feeding larvae also showed prey exiting the mouth after initially entering it (hereafter ‘in-and-out’), although the mechanism causing such failures had been unclear. In this study, we used numerical simulations to investigate the hydrodynamic mechanisms responsible for the failure to feed caused by this in-and-out prey movement. Detailed kinematics of the expanding mouth during prey capture by larval Sparus aurata were used to parameterize age-specific numerical models of the flows inside the mouth. These models revealed that for small larvae which expand their mouth slowly, fluid entering the mouth cavity is expelled through the mouth before it is closed, resulting in flow reversal at the orifice. This relative efflux of water through the mouth was >8% of the influx through the mouth for younger ages. However, similar effluxes were found when we simulated slow strikes by larger fish. The simulations can explain the observations of larval fish failing to feed because of the in-and-out movement of the prey. These results further highlight the importance of transporting the prey from the gape deeper into the mouth cavity in determining suction-feeding success.

R., Howard, Scarlett;Jürgen, Schramme,;E., Garcia, Jair;Leslie, Ng,;Aurore, Avarguès-Weber,;D., Greentree, Andrew;G., Dyer, Adrian

doi: 10.1242/jeb.223610pmid: 32409523

Many animals need to process numerical and quantity information in order to survive. Spontaneous quantity discrimination allows differentiation between two or more quantities without reinforcement or prior training on any numerical task. It is useful for assessing food resources, aggressive interactions, predator avoidance and prey choice. Honeybees have previously demonstrated landmark counting, quantity matching, use of numerical rules, quantity discrimination and arithmetic, but have not been tested for spontaneous quantity discrimination. In bees, spontaneous quantity discrimination could be useful when assessing the quantity of flowers available in a patch and thus maximizing foraging efficiency. In the current study, we assessed the spontaneous quantity discrimination behaviour of honeybees. Bees were trained to associate a single yellow artificial flower with sucrose. Bees were then tested for their ability to discriminate between 13 different quantity comparisons of artificial flowers (numeric ratio range: 0.08–0.8). Bees significantly preferred the higher quantity only in comparisons where ‘1’ was the lower quantity and where there was a sufficient magnitudinal distance between quantities (e.g. 1 versus 12, 1 versus 4, and 1 versus 3 but not 1 versus 2). Our results suggest a possible evolutionary benefit to choosing a foraging patch with a higher quantity of flowers when resources are scarce.

Kathryn, Knight,

doi: 10.1242/jeb.225979pmid: N/A

View large Download slide A 19-day-old gilthead seabream ( Sparus aurata ) larva. Photo credit: Roi Holzman. View large Download slide A 19-day-old gilthead seabream ( Sparus aurata ) larva. Photo credit: Roi Holzman. It almost sounds like a punishment worthy of Hades: most morsels slurped up by tiny hungry fish fry are ripped from their lips at the final instant. ‘For example, when 8 day old seabream fry attempt to capture their prey, they need five or six strikes to capture one prey item’, says Roi Holzman from Tel Aviv University, Israel. Yet, no one knew exactly how the unfortunate chain of events that snatches food from the youngsters’ mouths unfolds. Intrigued by the mystery, Holzman and Krishnamoorthy Krishnan, Asif Nafi and Roi Gurka from Costal Carolina University, USA, knew that there was only one way of finding out: by using a computer simulation of the events occurring within the fry's miniscule mouths. But first, the team needed to understand how the tiny fish larvae move their jaws and flare open their gill covers as they slurp in water through their mouths when attempting to gulp down a titbit. Turning to Victor China's movies of gilthead seabream ( Sparus aurata ) larvae – ranging in age from 7 to 37 days post-hatching (dph) – attempting to feed on one of their favourite snacks (0.16 mm long rotifers), Holzman detailed how the fry opened their mouths and gills as they slurped in water and how that changed as they grew. Over a month, the diameter of the fry's mouths doubled to 0.5 mm and their mouths also grew longer (0.7 mm to 2 mm). In addition, the larvae were eventually able to open their gill covers almost 1 mm wide. The team then designed a simulated fish larva mouth based on the measurements of the growing larvae, shaped like an elongated rugby ball, which could open wide at the front as the mouth drew in water. In addition, the team added simulations that took account of how long it took the larva to open its mouth, how the stickiness of the water reduced as each larva grew and the way the water surged forward as the larva's mouth gaped wide, to get a better sense of how water flowed through the minute fry's mouths. After months of patient computer programming, the team was relieved when the first simulations successfully recreated the water flow through the cyberlarva's mouth and out of the gill slits at the back. Also, as the cyberlarva grew, the speed of the simulated water flow through the mouth increased from 28.3 mm s −1 in the youngest larva up to 136.2 mm s −1 in the oldest larva as it swallowed water at a rate of 5.9 mm 3 s −1 . However, when the youngest cyberlarva closed its mouth at the end of a gulp, the team was astonished to see approximately one-tenth of the water gush back out of its mouth. This unexpected turn of events perfectly explained why food fragments that should have been swallowed suddenly popped back out of the frustrated fry's mouth. Fortunately, the inconvenient backwash vanished when the larvae grew older (23 dph); however, if the larger fish only took a leisurely gulp, the problem came back and they too could lose their dinner. Puzzled by the young larvae's misfortune, the team took a closer look at the trajectory of the water surging into the mouths of the tiniest simulated fry and realised the strongest outwash was generated when the mini fish opened their mouths slowly. It seems that opening their mouths fast is essential for famished gilthead seabream larvae to fill their mini bellies. References Krishnan , K. , Nafi , A. S. , Gurka , R. and Holzman , R. ( 2020 ). The hydrodynamic regime drives flow reversals in suction-feeding larval fishes during early ontogeny . J. Exp. Biol. 223 jeb214734 . https://doi.org/10.1242/jeb.214734 Google Scholar Crossref Search ADS © 2020. Published by The Company of Biologists Ltd 2020

Meng-Huan, Bao,;Li-Bing, Chen,;Catherine, Hambly,;R., Speakman, John;Zhi-Jun, Zhao,

doi: 10.1242/jeb.228809pmid: 32414866

There was an error published in the online full-text and PDF versions of Journal of Experimental Biology (2020) 223, jeb223560 ( doi:10.1242/jeb.223560 ). The common name of the study organism was originally given as striped hamsters in the title of the article. The correct name appears in the title above, and both the online full-text and PDF versions of the article have been updated to reflect that the research was carried out with Swiss mice, as stated elsewhere in the article. The authors apologise to readers for this error. View Original Article © 2020. Published by The Company of Biologists Ltd 2020