Announcing the 2024 Journal of Experimental Biology Outstanding Paper Prize shortlist and winner

In the first of this year's shortlisted articles, Soonyoung (Kelly) Kim, Jacob Robinson and colleagues from Rice University, USA, investigated how satiety influences the movements of one of the simplest animals – Hydra vulgaris, with just 12 nerve cell types – depending on whether they were well fed or hungry (jeb247503). Impressively, the hungry Hydra somersaulted toward light, tumbling faster by flipping more frequently – without altering their jump length or direction – while the well-fed animals mainly remained in place. Hunger was sufficient to alter how the animals moved toward light. Robinson recalls how, ‘Kelly was incredibly creative in the way she broke down a complex behaviour into an elegant mathematical model’ as she applied her engineering background to explore a biological question. JEB Editor, Sanjay Sane, echoes Robinson's sentiments and says, ‘This was an elegant study that did not require hi-tech equipment, just imagination and careful experimentation’.

The theme of the impact of light on animals is continued in the next shortlisted article, which focuses on animals that harbour symbiotic light-dependent plants within their tissues. But many symbiotic creatures, including corals, are at risk of losing their plant symbionts as temperatures rise. In February 2024, Luella Allen-Waller (University of Pennsylvania, USA), Marcelina Martunek, Kristen Brown and colleagues in Katie Barott's University of Pennsylvania lab, published their investigation of the impact that high temperatures have on the symbiotic pale anemone (Exaiptasia diaphana) (jeb246222). The team revealed that high temperatures directly impair the sea anemone's ability to regulate its internal pH, which is a threat. After overseeing peer review of the article, Katie Gilmour, says, ‘The combination of cool model system, rich dataset and novelty, together with the urgency and relevance of the question made the study very compelling’, and Barott is proud of her young colleagues. ‘Lulu (Luella) led the way as a senior doctoral student working closely with Marcelina and Kristen. The complementary talents of the individual researchers are what really brought this work to fruition’, she exclaims.

Another shortlisted paper investigated the impact of climate change on marine invertebrates, focusing on the solar powered emerald sea slug (Elysia viridis), which kidnaps chloroplasts from their seaweed diet, absorbing them into their body to photosynthesize and provide nutrition for their hosts when food is scarce. Elise Laetz (University of Groningen, The Netherlands) and colleagues from Wilco Verberk's lab (University of Groningen), investigated how much protection the abducted chloroplasts could offer their sea slug hosts as temperatures rise and water oxygen levels decline (jeb246331). Impressively, when the sea slugs experienced a heat wave they could adapt to the hotter conditions, reducing their metabolism, but they coped even better on sunny days as the oxygen in the water dwindled and the photosynthesising chloroplasts in their tissues supplemented their oxygen supply: a seaweed diet could offer emerald sea slugs some protection from climate change. ‘I really liked how the authors investigated the mechanisms of how the slugs gained better thermal tolerance from engulfing algae’, says JEB Editor Pat Wright.

Marine invertebrates are not the only creatures that are likely to experience challenges as global temperatures rise. In their shortlisted paper, Agnès Lewden and Tristan Halna du Fretay (University of Brest, France), with Antoine Stier (University of Strasbourg, France) investigated how gentoo penguins at the Océanopolis aquarium in Brest, France, cope as they grow new feathers, doubling their insulation prior to shedding the previous year's growth (jeb247332). Recording the temperature of the exposed skin around each bird's eyes with a thermal camera, the team revealed that it was difficult for the birds to dissipate the additional heat they generate as their new feathers grow, placing them at risk of overheating. ‘Agnès was impressive at all steps – planning and conducting the study, supervising an MSc student, analysing data, writing and revising the manuscript – demonstrating perfectly her successful transition as a fully-independent scientist’, says Stier. And Franklin, who nominated the paper for the JEB Outstanding paper Prize says, ‘I loved the simplicity of the non-invasive approach of thermal imaging to provide great insight into such a catastrophic annual event in the life of penguins’.

Featuring another aspect of bird physiology, Amalie Hutchinson, Jim Staples and Chris Guglielmo (University of Western Ontario, Canada) focused on the mechanism that allows tiny ruby throated hummingbirds to conserve energy when they are immobile (jeb248027). Knowing that small mammals reduce the metabolic rate of their mitochondria when they become torpid, causing their temperature to fall, Hutchinson and colleagues checked whether torpid hummingbirds use the same strategy. However, the mitochondria of the torpid hummingbirds were every bit as active when the birds were torpid. The team suspects that the birds simply burn less energy when they are inactive, allowing their body temperature to fall, reducing their metabolism. ‘Amalie drove every aspect of this highly integrative study – from animals in the field to organelle function. She produced excellent data and insightful interpretations’, says PI Staples. And nominating Editor, Patricia Schulte, explains that of all of the papers she reviewed in 2024, this one stood out, ‘because the authors were able to assess metabolism across levels of biological organization’.

Switching from the metabolism of hummingbirds to the metabolism of Drosophila larvae metamorphosing into adult insects, Jacob Campbell, Viviane Callier and Jon Harrison from Arizona State University, USA, with colleagues, investigated whether a failure of the larvae's oxygen supply, when they outgrow the network of tubes that supplies oxygen to every cell in their body, might trigger their dramatic transformation (jeb247697). However, the team never saw the larvae suffer from lack of oxygen when their bodies reached the critical size at which they metamorphose. In contrast, the team suspects that low oxygen levels in the prothoracic gland may allow the larvae to grow faster to escape locations where oxygen is dangerously low. JEB Editor John Terblanche explains that the paper impressed him because the team used, ‘neat integration of techniques’ to address the fundamental question of what sets invertebrate size, and Harrison is delighted by the recognition. He describes Callier, who was a postdoc at the time, as ‘dedicated and razor sharp’, and recalls how Campbell was brilliant, insightful and ‘created an atmosphere of fun that kept our dedicated undergraduates smiling as they dug through media for larvae’.

Continuing the metabolic theme, Ashley Potter (Monash University, Australia), working with Craig White and Dustin Marshall, also at Monash University, investigated the impact of concentration on sperm metabolism (jeb246674). Searching the literature – the team identified 198 measurements of sperm metabolism covering 49 species, ranging from mammals and birds to sea urchins, worms and insects. Combining them with Potter's own measurements, they discovered that as sperm become more dilute, their metabolic rate increases significantly. This gives individual sperm a greater chance of success during their final approach to the egg, increasing their energy after leaving the bulk of sperm behind. ‘The power of this study lies in the authors combining a comprehensive systematic review of the literature with empirical observations from experiments’, says Craig Franklin. Marshall remembers the dramatic impact of Melbourne's 2-year Covid lockdown and Potter's dogged determination as she pursued the topic, ‘to turn some preliminary empirical data into a fully-fledged synthesis’, he says.

Successfully attracting mates is also essential for the survival of almost all species and male orchid bees gather pungent and aromatic aromas to concoct scents that attract females. Jonas Henske and Thomas Eltz, Ruhr-Universität Bochum, Germany, wondered whether older male orchid bees, with a lifetime's experience of blending scents, produce the most complex and strongest scents to lure females. However, by investigating the scents produced by more than 400 orchid bees, they found that younger and middle-aged bees blended the scents with the greatest complexity in the largest quantities (jeb246995), making themselves more attractive. Selecting the research as her shortlist nomination, Almut Kelber says, ‘For me it shows how important it can be to question popular hypotheses’, and Eltz recalls that Henske was creative and inquisitive. ‘He ingeniously succeeded in solving all the problems involved with estimating male orchid bee age and measuring change of volatile content in orchid bee perfume’, says Eltz.

Although scent is key for some courtships, many birds depend on their voices to attract a mate and the syringeal muscles that produce these elaborate calls must contract at extraordinarily high frequencies, up to 250 Hz. ‘I tried several ways to get force–length curves of these syringeal muscles over the years’, says Coen Elemans (University of Southern Denmark), but when Nicholas Gladman joined the lab, he seemed to have the golden touch. ‘Nick came in and just did it’ says Elemans, recalling how he cooled the muscles to 30°C, discovering that at natural body temperature the muscles might contract at the extraordinary velocity of 37–42 L_o s⁻¹ (jeb246330). ‘Fully self-motivated, he was always a step ahead’, Elemans adds. Having overseen the paper through peer review, Sheila Patek says, ‘This paper stood out to me because it is remarkable to be able to measure the physiological properties of muscles used for acoustics, especially in extremely high frequency, internal, vertebrate systems’.

From the fastest contracting muscles, the shortlist moves to walking humans and how they adjust their style when they encounter obstacles. Sarah Brinkerhoff, Jamie Roper (Auburn University, USA) and colleagues asked young volunteers to walk on a split treadmill, where the team could suddenly speed up one side of the treadmill to 1.5 m s⁻¹ while slowing the other to 0.5 m s⁻¹. This forced the volunteers to adjust to an uneven walk. Impressively, the volunteers coped well, regaining stability within ∼30 s, but the change required that they used more energy (jeb249217). In addition, Brinkerhoff revealed that the fittest and most unfit volunteers adapted faster than those with average fitness. ‘I thought the paper provided a rigorous analysis’, says Editor Monica Daley and Roper adds that ‘Sarah's exceptional scientific rigor and innovative thinking transformed both research outcomes and her fellow scientists’ development’.

In the final shortlisted article published in 2024, Jarrod Petersen and colleagues from Brown University, USA, and the University of Cincinnati, USA, revealed that the neck skin of boa constrictors that engulf meals in a single mouthful is 25% stretchier than their tail skin, while the neck skin of egg-eating snakes is 90% more stretchable (jeb248142). ‘This project was borne of Jarrod's native curiosity coupled with wisdom, in this case the wisdom of tapping into co-author Bruce Jayne's all-encompassing knowledge of snake biology’, says PI Tom Roberts. Based on their observations, the team suspects that stretchy skin was one of the key factors that allowed snakes to evolve the ability to consume meals in a single mouthful. ‘The manuscript is noteworthy in its use of approaches from materials science to address a question fundamental to the biology of a diversity of snakes’, says nominating Editor Matt McHenry.

Having compiled the shortlist with the JEB Editors, Franklin admits that the task was challenging, but ‘highly rewarding… given the exceptional quality of the articles and science being submitted by ECRs’. He commends all of the finalists. After reviewing the 10 nominated research articles, the Editors are delighted to announce that Elise Laetz, University of Groningen, the Netherlands, has been awarded the 2024 JEB Outstanding Paper prize for her paper, ‘Critical thermal maxima and oxygen uptake in Elysia viridis, a sea slug that steals chloroplasts to photosynthesize’ (jeb246331). Reacting to the news, Laetz says, ‘I was elated!’, explaining that the team had worked on the study for more than a year. ‘Getting it published in JEB was already an incredible reward, but finding out that our work has been honoured with this prize feels even more amazing’, she exclaims.

Like that of many others, Laetz's research was thrown into disarray when the Covid-19 pandemic struck. She could no longer travel to work with international collaborators during her postdoc at University of Groningen, The Netherlands, during which she had begun collaborating with Wilco Verberk at Radboud University, The Netherlands. Laetz had to rethink and quickly. Looking closer to home, she identified the emerald sea-slug (Elysia viridis), which resides in rockpools along the North Sea coast of The Netherlands. ‘Since the beginning of my research career, I've been intrigued by this remarkable association between solar-powered sea-slugs and the chloroplasts they enslave and I've been determined to unravel how it works’, she explains, adding that she wanted to know whether sugar and oxygen produced by kidnapped chloroplasts gave these slugs an advantage when faced with various forms of environmental stress, such as rising water temperatures and low oxygen.

But she soon realised that the 12-hour-long days measuring the metabolic rates of the animals at high temperatures as she monitored the impact for months on end was going to be more than she could manage singlehanded. She invited three Masters’ students, Can Kahyaoglu, Natascha Brogstein and Michiel Merkx, to work with her in the lab over the long, gruelling days. Then followed the extensive analysis to tease out the sea-slugs’ physical responses to the heat as their chloroplasts degraded over time. ‘Luckily, we had Wilco to think with us and guide us through the challenges’, she says, adding ‘the project truly was a team effort’. And Verberk recalls that working with Laetz was a pleasure. ‘She is highly enthusiastic about slugs and solar-powered animals, demonstrating a remarkable ability to integrate knowledge across scales’, he says, adding that he was particularly impressed at how she connected processes in the cell, such as the production of reactive oxygen species, to the broader ecological context.

Since completing this study, Laetz has established her own lab as an Assistant Professor at the University of Groningen, The Netherlands, where she is continuing her work on the impact of environmental stress on solar-powered animals. ‘I have no doubt that her dedication and curiosity will lead to an outstanding career, and I look forward to seeing her contributions shape the field in the years to come’, says Verberk.

Thinking of the future, Franklin is proud of the support that the journal offers early-career researchers through this award and through fellowships as they negotiate the early stages of their careers. ‘The future of comparative physiology, neuroethology and biomechanics rests in the hands of ECRs, so it is essential that JEB recognises and supports their work’, says Franklin acknowledging all of the researchers shortlisted for this year's JEB Outstanding Paper Prize and wishing them every success for the future.