Announcing the 2022 Journal of Experimental Biology Outstanding Paper Prize shortlist and winner

This might sound like a strange question, but what do raccoons, robber flies, Pacific oysters and lumpsuckers have in common? At first glance, not much. Raccoons are notorious thieves, robber flies are noted for their remarkable agility and oysters and lumpsuckers cling on to rocks in shallow water. Any similarities appear tenuous, until we tell you that they are all species that feature in this year's JEB Outstanding Paper Prize shortlist. Since its launch in 2005 in memory of Bob Boutilier, the award has celebrated the achievements of early-career researchers from a diverse range of backgrounds working on a wide array of topics and now the Editors of the journal are delighted to announce the 11 papers that were nominated for the award in 2022. ‘Enabling and empowering early-career researchers is critical as they are the future of our discipline and are integral to how our science evolves and moves forward’, says JEB Editor-in-Chief Craig Franklin.

Kicking off the shortlist, Franklin describes Meredith Johnson, Jordan Glass and Jon Harrison's research article, ‘A desert bee thermoregulates with an abdominal convector during flight’ (jeb244147), as ‘expansive and elegant’, combining experimental measurements with a heat budget model. The researchers, from Arizona State University, USA, measured the body temperatures, water losses and metabolic rates of large male Centris caesalpiniae, to determine how the insects remain cool during flight. ‘What I really loved was that the empirical data were collected in the field, with respirometers set up on a shaded porch, just 20 m from a mating aggregation of desert bees with ambient temperatures approaching 40°C!’, explains Franklin. In contrast, the paper nominated by John Terblanche, published by Bert Foquet and colleagues from Texas A&M University, USA, focuses on the transition made by locusts between the solitary and gregarious lifestyles, which occurs when the previously solitary insects become overcrowded, changing their physiology, appearance and forming large swarms (jeb244621). Comparing the transition of the Central American locust (Schistocerca piceifrons) with that of the well-studied desert locust (Schistocerca gregaria), Fouquet and colleagues discovered that the insects take radically different approaches, suggesting that the underlying mechanisms differ dramatically between the two species. ‘It's clear we cannot rely on our traditional lab models to infer generality of response and time-course of phase change across locust species’, Terblanche says.

The team led by Philip Freda from Kansas State University, USA, and Jantina Toxopeus, University of Colorado Denver, USA, in the third shortlisted article – nominated by former Editor, Julian Dow –revealed that larval and adult Drosophila melanogaster use different strategies to survive cold exposure (jeb244063). ‘Understanding mechanisms underpinning phenotypic plasticity is a bit of a holy grail in environmental physiology research’, says Terblanche, explaining that the mechanisms that allow both life stages to survive in the cold ‘had been poorly disentangled until this paper’. Adding that the paper is very insightful, Terblanche hopes that it will inspire future studies seeking to understand the evolution of stress resistance across insects with diverse life histories.

In the final shortlisted paper, dedicated to understanding insect behaviour and physiology, Samuel Fabian (then at the University of Cambridge, UK) along with, Mary Sumner, Trevor Wardill and Paloma Gonzalez-Bellido from the University of Minnesota, USA, revealed how minute robber flies (Holcocephala fusca) simultaneously combine information about a moving victim and a nearby obstacle to successfully circumnavigate the obstruction by taking an intermediate interception path (jeb243568). Nominating the paper, Sanjay Sane says, ‘it's a really good mix of experiments and modelling’, adding that ‘the insect's minute brain exquisitely disproves the old adage that small is simple’.

A series of seven papers from the aquatic world, covering the fields of biomechanics, neuroethology and comparative physiology, make up the next selection of Outstanding Paper Prize shortlist nominations. Almut Kelber describes, ‘Colour discrimination thresholds vary throughout colour space in a reef fish (Rhinecanthus aculeatus)’ (jeb243533), by Naomi Green and Emily Guevara from University of Brisbane, Australia, and an international team of colleagues, as a landmark paper in the field of animal colour vision. Explaining how the researchers, based in New Zealand, the UK and Australia, used a new method to determine the ability of reef fish to discriminate fine shades of colour, Kelber says, ‘they found that widely used models do not explain the discrimination abilities of fish very well when colour differences get larger’, concluding that ‘the team warns scientists to be cautious when interpreting model results for highly saturated colours’.

Switching from the neuroethology of fish to comparative physiology, Katie Gilmour describes Magnus Aaskov and colleagues’ paper ‘Arapaima gigas maintains gas exchange separation in severe aquatic hypoxia but does not suffer branchial oxygen loss’ (jeb243672) as a ‘technical tour-de-force’. Explaining that the question of whether air-breathing Arapaima gigas from the Amazon lose oxygen through their gills when in hypoxic water has long puzzled scientists, Gilmour describes how the researchers creatively re-purposed a commercial artificial lung to extract CO₂ from water to measure CO₂ excretion in this species. Confirming that the hypoxic fish do not lose oxygen through their gills, the team revealed that the fish still manage to dispose of most of their CO₂ (77%) through the gills, somehow maintaining distinct pathways for oxygen uptake and CO₂ elimination. ‘Their results revealed that we still have much to learn about how species like Arapaima manage respiratory gas exchange’, Gilmour says.

In their shortlisted paper, Haonan Zhouyao from Baylor College of Medicine, USA, and an international team of collaborators including Alex Zimmer (University of New Brunswick, Canada), Sandra Fehsefeld (Université du Quebec à Rimouski, Canada) and Dirk Weihrauch (University of Manitoba, Canada), identified two new ammonia transporter proteins, known as Hiat proteins, in larval zebrafish, which could prove to be essential for ammonia excretion (jeb244279). Nominating the paper, Pat Wright says, ‘I was impressed with how the authors set out to test a clear hypothesis, performed detailed and meticulous experiments, and the results have broad impact on our understanding of epithelial transport across the animal world’. She is excited to see a new protein class added to the lexicon of ammonia transporters ∼20 years on from the discovery of Rhesus glycoproteins.

A pair of papers dedicated to the impact of temperature on the physiology of aquatic organisms feature as the eighth and ninth nominations in the shortlist. Connor Reeve and colleagues from the University of New Brunswick, Canada, investigated whether cold fish actively supress their metabolism in the cold, discovering that they do not; instead, the fish reduce their movement while allowing their metabolism to decline naturally as they cool (jeb243407). Monitoring Editor, Stuart Egginton, says, ‘It's a huge study, very well written-up. It should be highly cited and has the potential to become a classic, if only because it integrates detailed and quantitative behavioural assessments simultaneously with metabolic rate measurements’. Meanwhile, Melissa DellaTorre, Francis Pan, Andrew Griffith, and Ning Li, with Donal Manahan from University of Southern California, USA, used a genetic approach to reveal considerable variation among families of Pacific oysters (Crassostrea gigas) in their response to increased temperature (jeb244518). Referring to the research published in November 2022, Trish Schulte says, ‘What really stands out about this paper is the detailed mechanistic studies of protein synthesis and metabolic rate coupled with an impressively high level of replication’, adding, ‘this work has important implications for responses of animals to global climate change’.

As they have colonised most water masses on the planet, fish have unequivocally proved their versatility, and few are more adaptable than the species that literally cling to life in the turbulent coastal waters of the Pacific. In their shortlisted paper, Jonathan Huie (The George Washington University, USA), Dylan Wainwright (Purdue University) and Karly Cohen (University of Florida, USA), with Adam Summers (University of Washington, USA), compared the adhesive powers of the sucker structures of three inhabitants of the Pacific coast: the Pacific spiny lumpsucker (Eumicrotremus orbis), the marbled snailfish (Liparis dennyi) and the northern clingfish (Gobiesox maeandricus) (jeb244821). ‘Huie and colleagues’ paper used an interesting combination of adhesion performance measures based on foundational principles of biomechanics, combined with visually stunning morphological imaging data to investigate form and function of adhesive organs in fishes’, says Monica Daley, adding that the paper could inspire novel designs for new adhesive devices.

In the final shortlisted article of 2022, Lauren Stanton from the University of Wyoming, USA, revealed that the least bold and most docile raccoons are best suited to urban life, as they seem to be better prepared to learn new tasks than bolder animals that are less capable of learning (jeb243726). Over a four-year period, Stanton tagged more than 200 wild raccoons, monitoring their impulsivity and ability to learn to access food rewards. Nominating Editor, Ken Lukowiak recalls, ‘so many of my non-scientific neighbours knew about the paper through local newspapers and media coverage and asked me about it. This JEB paper reached the general public and made an impact’.

Reflecting on the shortlist, Franklin says, ‘We believe the papers we finally decided upon represent the depth and breadth of JEB's content and, most importantly, highlight the creativity and excellence of our community of early-career researchers’. However, after reviewing the 11 nominated papers published in the journal in 2022, the Editors are delighted to announce that Samuel Fabian and Mary Sumner are the winners of the 2021 JEB Outstanding Paper Prize for their work on ‘Avoiding obstacles while intercepting a moving target: a miniature fly's solution’. Responding to the news, Gonzalez-Bellido, PI on the study, says, ‘This is such an honour’, and Sane, who oversaw peer review of the paper adds, ‘I am delighted that the paper by Fabian and colleagues has won the Outstanding Paper Prize. It is always a joy to read papers that use novel systems to reveal the mysterious ways in which small brains work in their appropriate natural context’.

Considering Fabian's contribution to the paper, Gonzalez-Bellido describes how he planned the experiments, adapted the tools that they used and carried out the analysis. ‘He also came up with the combined law explanation’, she says, while describing Sumner, the Gonzalez-Bellido laboratory assistant, as Fabian's essential side kick. ‘She looked after the fieldwork logistics, controlled the cameras and computers in the field and carried out data digitization’, Gonzalez-Bellido adds. Fabian, who is currently a Research Associate at Imperial College London, UK, recalls that working in the field was a lot of fun and he is still interested in understanding why insects travel on a particular course when intercepting prey. In addition, he admits that the robber flies often play on his mind; ‘When you move through a crowd, play sport or commute to work, your brain is solving many small challenges like those faced by robber flies’, he says. Reacting to the news, Sumner, who is currently working for Roslin Technologies, UK, was gratified to see everyone's hard work getting recognised and says ‘I loved working with Holcocephala, they're so agile and were incredible to watch, dodging around our obstacles’.

Having recognised the contributions of the shortlisted early-career researchers to the discoveries published in 2022, Franklin is excited about the future as the journal embarks on its centenary celebrations in 2023. ‘The quality of the papers in this year's shortlist demonstrates that the future of our discipline is in good hands’, he concludes.