Journal of Experimental Biology

Po, Theodora; Carrillo, Andres; McKee, Amberle; Pernet, Bruno; McHenry, Matthew J.

doi: 10.1242/jeb.247804pmid: 39104305

Hydrostatic skeletons, such as an elephant trunk or a squid tentacle, permit the transmission of mechanical work through a soft body. Despite the ubiquity of these structures among animals, we generally do not understand how differences in their morphology affect their ability to transmit muscular work. Therefore, the present study used mathematical modeling, morphometrics, and kinematics to understand the transmission of force and displacement in the tube feet of the juvenile six-rayed star (Leptasterias sp.). An inverse-dynamic analysis revealed that the forces generated by the feet during crawling primarily serve to overcome the submerged weight of the body. These forces were disproportionately generated by the feet at more proximal positions along each ray, which were used more frequently for crawling. Owing to a combination of mechanical advantage and muscle mass, these proximal feet exhibited a greater capacity for force generation than the distal feet. However, the higher displacement advantage of the more elongated distal feet offer a superior ability to extend the feet into the environment. Therefore, the morphology of tube feet demonstrates a gradient in gearing along each ray that compliments their role in behavior.

Country, Michael William

doi: 10.1242/jeb.246620pmid: N/A

Why do ants never get sick? Because of their little tiny ant-y bodies, of course. That was my favourite joke, until an insect-loving biologist ruined it. ‘Actually’, he started annoyingly, ‘ants don't produce antibodies like humans do. But they do perform first aid!’. I knew ants were social creatures, but I was surprised to hear they care for their wounded. Florida carpenter ants (Camponotus floridanus) have to defend against rival ant colonies, and their battles sometimes leave them with injured limbs. As Laurent Keller (University of Lausanne, Switzerland) and colleagues noted, other species carry a first-aid kit: they have a gland that produces antimicrobials and wound-healing substances, and they can apply this makeshift medicine to ward off infection. But Florida carpenter ants don't have this gland, or any sort of medicine. Without medicine, how can ants treat each other and prevent fatal infections? Keller and colleagues approached this mystery by making controlled cuts on the ants’ upper legs, and then returned the wounded ants back to their colonies. True to their social nature, nestmates took painstaking care of the wounded insects. Typically, a generous nestmate would approach the injured ant and start to lick its wounds. The uninjured ant would then move its mouthparts methodically up the patient's leg, towards the joint where the femur is attached. The ant would continue the operation by biting at the attachment site repeatedly, tearing through the joint until the injured leg was completely amputated. The whole time, the injured ant would hold up its leg, patiently and obediently. Finally, the insect surgeon would clean the new wound by licking it meticulously for several minutes. So perhaps first aid is the wrong term; these ants perform surgery. But isn't an amputation excessive? Next, Keller and his team tested whether ants really fared better after an amputation. They injured the ants again, but this time they purposefully infected the wounds by smearing them with bacteria. Left alone, most ants died within a day, but they survived if the limb was amputated – no matter whether ants performed the procedure or whether Keller's team performed the amputations themselves. Amputations also reduced bacterial infections. When the researchers did a genetic scan, they found bacterial genes in the injured ants, but these genes were almost completely gone after amputation by either ants or humans. This was the answer – ant appendage amputations were effective, because they limited the spread of bacteria. Interestingly, the story was different for lower leg injuries. Keller's team noted that ants amputated injured upper legs, but they never removed the leg when the lower leg was wounded. Why were lower leg injuries treated differently? To investigate, the researchers injured ants’ lower legs and infected the wound like before. Lower leg injuries were more infectious and fatal, and amputations didn't save the ants. Instead, the best treatment was to just return the ants to their colonies, where nestmates cleaned the wounds with their mouths. The researchers suggested that lower leg anatomy might make infections worse because there's better circulation and more surface area for bacterial growth. This means lower leg injuries likely let infections spread faster, so amputations don't improve survival. So maybe we can save my bad joke after all. How did the army ant recover from his battle wound? He left his arm-y. Without medical knowledge or special equipment, Florida carpenter ants figured out both when and how to amputate a fatal wound. This means that ants can diagnose injuries and perform surgeries, feats which take human doctors years to accomplish. Frank , E. T., Buffat , D., Liberti , J., Aibekova , L., Economo , E. P. and Keller , L. ( 2024 ). Wound-dependent leg amputations to combat infections in an ant society . Curr. Biol . 34 , 3273 - 3278 . https://doi.org/10.1016/j.cub.2024.06.021 Google Scholar Crossref Search ADS PubMed © 2024. Published by The Company of Biologists Ltd 2024

Houchat, Jean-Noël; Castelo, Marcela K.; Crespo, José E.

doi: 10.1242/jeb.247530pmid: 39155696

Barometric pressure is an environmental factor involved in the modulation of a variety of activities in insects. Generally, a drop in barometric pressure precedes the arrival of weather conditions that can affect insect activities and life expectancy. We simulated different scenarios of pressure drop in a modified hermetic chamber and studied their influence on the host-seeking behaviour of the larvae of the robber fly Mallophora ruficauda using air stationary olfactometers. In addition, we studied whether larval density modulates orientation to the host under the same scenarios of pressure drop. We found that motivation to search for hosts is affected by the same slope of pressure drop in both low- and high-density larvae. However, larval density modulates the onset of the responses to pressure decrease, as low-density larvae stop searching for hosts more quickly than high-density larvae. This result reflects an avoidance strategy according to which low-density larvae would have a reduced host range and higher risk of mortality and fewer chances to find a suitable host under adverse pressure conditions. Low-density larvae, known to prefer healthy hosts, do not search for parasitized hosts under normal pressure conditions nor under a range of pressure drops, strongly suggesting that host selectivity is not modulated by barometric pressure. This study paves the way to a better understanding of the changes in crucial insect behaviours induced by weather conditions, and provides more knowledge about the risk factors likely to affect insect survival in the context of foraging ecology.

Tibbetts, Elizabeth A.; Weise, Chloe; Pardo-Sanchez, Juanita; Vi, An Na

doi: 10.1242/jeb.247661pmid: 39119656

Visual recognition of three-dimensional signals, such as faces, is challenging because the signals appear different from different viewpoints. A flexible but cognitively challenging solution is viewpoint-independent recognition, where receivers identify signals from novel viewing angles. Here, we used same/different concept learning to test viewpoint-independent face recognition in Polistes fuscatus, a wasp that uses facial patterns to individually identify conspecifics. We found that wasps use extrapolation to identify novel views of conspecific faces. For example, wasps identify a pair of pictures of the same wasp as the ‘same’, even if the pictures are taken from different views (e.g. one face 0 deg rotation, one face 60 deg rotation). This result is notable because it provides the first evidence of view-invariant recognition via extrapolation in an invertebrate. The results suggest that viewpoint-independent recognition via extrapolation may be a widespread strategy to facilitate individual face recognition.

Tait, Catherine; Chicco, Adam J.; Naug, Dhruba

doi: 10.1242/jeb.247835pmid: 39092671

In the context of slow–fast behavioral variation, fast individuals are hypothesized to be those who prioritize speed over accuracy while slow individuals are those which do the opposite. Since energy metabolism is a critical component of neural and cognitive functioning, this predicts such differences in cognitive style to be reflected at the level of the brain. We tested this idea in honeybees by first classifying individuals into slow and fast cognitive phenotypes based on a learning assay and then measuring their brain respiration with high-resolution respirometry. Our results broadly show that inter-individual differences in cognition are reflected in differences in brain mass and accompanying energy use at the level of the brain and the whole animal. Larger brains had lower mass-specific energy usage and bees with larger brains had a higher metabolic rate. These differences in brain respiration and brain mass were, in turn, associated with cognitive differences, such that bees with larger brains were fast cognitive phenotypes whereas those with smaller brains were slow cognitive phenotypes. We discuss these results in the context of the role of energy in brain functioning and slow–fast decision making and speed accuracy trade-off.

Bergman, Elisabeth A.; Matthews, Philip G. D.

doi: 10.1242/jeb.247966pmid: 39155677

A select group of hemipterans within the suborder Auchenorrhyncha are the only animals that feed exclusively on xylem sap – a nutritionally poor liquid that exists under negative pressure within a plant's xylem vessels. To consume it, xylem-feeding bugs have evolved enlarged cibarial pumps capable of generating enormous negative pressures. A previous study examining the allometry of this feeding model suggested that small xylem feeders pay relatively higher energetic costs while feeding, favouring the evolution of larger-bodied species. However, this interspecific analysis only considered adult xylem-feeding insects and neglected the considerable intraspecific change in size that occurs across the insect's development. Here, we examine the changes in cibarial pump morphology and function that occur during the development of Philaenus spumarius, the common meadow spittlebug. We show that the cibarial pump scales largely as expected from isometry and that the maximum negative pressure is mass independent, indicating that size has no effect on the xylem-feeding capacity of juvenile spittlebugs. We conclude that a first instar nymph with a body mass 2% of the adult can still feed at the >1 MPa tension present in a plant's xylem vessels without a substantial energetic disadvantage.

Best, Carol

doi: 10.1242/jeb.246621pmid: N/A

Imagine you're beside a rocky stream in the mountains and you see a clutch of fish eggs. You think they belong to salmon or trout, but you're not a fish expert and how different could they be, anyway? Turns out, pretty different! If they are chinook salmon eggs, they're probably orphans. Chinook salmon (Oncorhynchus tshawytscha) spawn once in freshwater streams after a substantial migration back from the ocean and then die. If they are rainbow trout eggs, their parents are probably around. Rainbow trout (Oncorhynchus mykiss) spawn in freshwater streams multiple times during their life. Why some salmonids are single-spawners and others are multiple-spawners is not well understood. However, Goro Yoshizaki and colleagues at the Tokyo University of Marine Science and Technology and the University of Tsukuba, Japan, have uncovered a potential reason for this difference and it involves reproductive stem cells: the small but important cells that give rise to eggs and sperm. First, the scientists wondered what happens to these stem cells before and after spawning. When they looked at the immature gonads of rainbow trout (multiple-spawners) and chinook salmon (single-spawners) under the microscope, they saw lots of these stem cells – ready to turn into sperm or eggs. After the fish had spawned once, they checked again and saw stem cells in the ovaries and testes of rainbow trout, but not in those of chinook salmon. This suggested that single-spawning species lose their ability to produce eggs and sperm after one reproductive cycle, while this is retained in multiple-spawners. Next, they wondered whether the loss of these stem cells is a property of the cells themselves, or a result of signals coming from the fish. To tackle this question, the scientists collected the stem cells from chinook salmon and, using a tiny glass needle, transplanted them into rainbow trout. Specifically, larval rainbow trout genetically modified to have no reproductive stem cells of their own. In doing so, the stem cells of the single-spawner were now receiving signals from the body of a multiple-spawner. They then raised these rainbow trout with salmon stem cells to maturity and through several spawning seasons. When the recipient rainbow trout males started to produce sperm, they collected it and analysed the DNA. As they hoped, the trout were producing chinook salmon sperm, confirming that the transplant worked. Similarly, when the female trout started producing eggs, they were chinook salmon eggs. When these recipient rainbow trout mated, they produced fully chinook salmon offspring – as verified by their DNA, development and appearance. After this first spawning, the question remained: would the chinook salmon stem cells disappear after one spawning like they do in their natural host, or would their new rainbow trout host make them stick around for multiple spawning seasons? It turns out these rainbow trout could produce chinook salmon sperm or eggs for multiple spawning seasons! By examining the ovaries and testes under the microscope after spawning, the researchers confirmed that transplanted chinook salmon stem cells stuck around in recipient trout. After this years-long experiment, the scientists concluded that the fate of these reproductive germ cells after the first spawn is not a built-in property, but depends on signals from within the fish. Which signals? That is for future scientists to figure out. Now, imagine you're back at your stream, eyeing these eggs suspiciously. Are they the product of the single monumental spawning of chinook salmon or one of many clutches produced by a rainbow trout? Perhaps they are the chinook salmon offspring of two genetically modified, stem cell recipient rainbow trout created in an attempt to boost an endangered population of chinook salmon. Yoshizaki , G., Fujihara , R., Namura , S., Kanzaka , K., Kamiya , K., Terasawa , M., Shimamori , S., Moriya , N., Miwa , M. and Hayashi , M. ( 2024 ). Gametes of semelparous salmon are repeatedly produced by surrogate rainbow trout . Sci. Adv . 10 , eadm8713 . https://doi.org/10.1126/sciadv.adm8713 Google Scholar Crossref Search ADS PubMed © 2024. Published by The Company of Biologists Ltd 2024

Schwartz, Nicole E.; Garland, Theodore

doi: 10.1242/jeb.249213pmid: 39119628

Selection experiments play an increasingly important role in comparative and evolutionary physiology. However, selection experiments can be limited by relatively low statistical power, in part because replicate line is the experimental unit for analyses of direct or correlated responses (rather than number of individuals measured). One way to increase the ability to detect correlated responses is through a meta-analysis of studies for a given trait across multiple generations. To demonstrate this, we applied meta-analytic techniques to two traits (body mass and heart ventricle mass, with body mass as a covariate) from a long-term artificial selection experiment for high voluntary wheel-running behavior. In this experiment, all four replicate High Runner (HR) lines reached apparent selection limits around generations 17–27, running approximately 2.5- to 3-fold more revolutions per day than the four non-selected Control (C) lines. Although both traits would also be expected to change in HR lines (relative heart size expected to increase, expected direction for body mass is less clear), their statistical significance has varied, despite repeated measurements. We compiled information from 33 unique studies and calculated a measure of effect size (Pearson's R). Our results indicate that, despite a lack of statistical significance in most generations, HR mice have evolved larger hearts and smaller bodies relative to controls. Moreover, plateaus in effect sizes for both traits coincide with the generational range during which the selection limit for wheel-running behavior was reached. Finally, since reaching the selection limit, absolute effect sizes for body mass and heart ventricle mass have become smaller (i.e. closer to 0).

doi: 10.1242/jeb.249456pmid: N/A

ECR Spotlight is a series of interviews with early-career authors from a selection of papers published in Journal of Experimental Biology and aims to promote not only the diversity of early-career researchers (ECRs) working in experimental biology but also the huge variety of animals and physiological systems that are essential for the ‘comparative’ approach. Nicole Schwartz is an author on ‘ A meta-analysis of whole-body and heart mass effect sizes from a long-term artificial selection experiment for high voluntary exercise’, published in JEB. Nicole conducted the research described in this article while a PhD student in Theodore Garland, Jr's lab at University of California, Riverside, USA. She is now a Postdoctoral Fellow in the lab of Patricia C. Lopes at Schmid College of Science and Technology, Chapman University, USA, investigating how early-life effects can alter the development of offspring and modify the expression of complex behaviors (e.g. voluntary exercise) into adulthood.

Braz-Mota, Susana; Luis Val, Adalberto

doi: 10.1242/jeb.247255pmid: 39221648

Higher temperatures exacerbate drought conditions by increasing evaporation rates, reducing soil moisture and altering precipitation patterns. As global temperatures rise as a result of climate change, these effects intensify, leading to more frequent and severe droughts. This link between higher temperatures and drought is particularly evident in sensitive ecosystems like the Amazon rainforest, where reduced rainfall and higher evaporation rates result in significantly lower water levels, threatening biodiversity and human livelihoods. As an example, the serious drought experienced in the Amazon basin in 2023 resulted in a significant decline in fish populations. Elevated water temperatures, reaching up to 38°C, led to mass mortality events, because these temperatures surpass the thermal tolerance of many Amazonian fish species. We know this because our group has collected data on critical thermal maxima (CTmax) for various fish species over multiple years. Additionally, warmer waters can cause hypoxia, further exacerbating fish mortality. Thus, even Amazon fish species, which have relatively high thermal tolerance, are being impacted by climate change. The Amazon drought experienced in 2023 underscores the urgent need for climate action to mitigate the devastating effects on Amazonian biodiversity. The fact that we have been able to link fish mortality events to data on the thermal tolerance of fishes emphasizes the important role of experimental biology in elucidating the mechanisms behind these events, a link that we aim to highlight in this Perspective.