With a century of literature behind Journal of Experimental Biology (JEB) in 2023, I look at some of the extraordinary papers contained within its archive. From publishing Nobel Prize-inspiring discoveries to founding fields and solving long-standing mysteries, the journal has been at the hub of experimental biology for 10 decades, leading the way and shining a light on the physiology of many remarkable animal species. In this Perspective, I highlight some of the key players in the field, summarise their seminal works and consider their long-term impact as JEB embarks on its next 100 years.
With a strong and established reputation for excellence in academic publishing, Journal of Experimental Biology (JEB) is recognised around the world as a champion of exceptional research. Among our authors, we can count Nobel Laureates and titans in the field, including Hermann Muller, who discovered X-ray damage of DNA (Muller and Dippel, 1926); Archibald Hill – of muscle physiology fame – looking at colour changes in mummichogs (Hill et al., 1935); neurobiologist Andrew Huxley, who investigated the physics underpinning structural colours (Huxley, 1968); Alan Hodgkin and Bernard Katz working on nerve structure and conduction (Hodgkin and Katz, 1949); and, of course, August Krogh, who published his first paper with the journal on the permeability of trout eggs to D2O and H2O in 1937 (Krogh and Ussing, 1937). In the accompanying timeline (Fig. 1), I highlight some of the key papers from the journal's past, many of which were featured in our JEB Classics series, where modern experts revisited the research and discussed its long-term impact. Although some of the ground-breaking discoveries featured in the journal's earlier issues are now ensconced in modern textbooks, others, such as Gray and Hancock's 1955 publication on the propulsion of sea urchin spermatozoa (Gray and Hancock, 1955) and Weiss-Fogh's, 1973 paper on lift production mechanisms (Weis-Fogh, 1973), are still being cited today, contributing intellectually more than 50 years later. This Perspective aims to revisit some of the classic papers that have been published in the journal over the past 100 years to provide a snapshot of key journal breakthroughs and a sense of the fields they inspired.
The JEB century in 27 papers
During the early years of JEB, volumes were small and issues tiny. It wasn't until June 1927 that an issue broke into double figures, with a table of contents of 10 papers. But by the 1930s, the journal was beginning to expand. Luminaries, such as Gray – with his series of papers entitled ‘Studies in Animal Locomotion, I-VIII’ (Gray, 1933, 1939) – were establishing the journal as the founding home of comparative biomechanics, while Carl Pantin and J. Z. Young were both early proponents of the fledgling field of neurobiology (Pantin, 1934; Young, 1935). Young published his seminal paper, ‘The function of the giant nerve fibres of the squid’, in the journal in 1938 (Young, 1938). According to Richard Keynes (University of Cambridge, UK), this paper ‘enabled the biophysics and biochemistry of excitable membranes to be properly studied in depth’, adding that in 1973, Alan Hodgkin (University of Cambridge) said that the paper had, ‘done more for axonology than any other single advance in technique during the previous 40 years’ (Keynes, 2005), laying the foundation for two Nobel Prizes. Meanwhile, J. Arthur Ramsay established the journal's credentials in the burgeoning field of insect homeostasis (Ramsay, 1935) while Vincent Wigglesworth cemented the journal at the dawn of insect physiology and developmental patterning (Wigglesworth, 1931, 1940).
By the end of the decade world conflict descended, yet the journal continued to be produced despite the challenges of the Second World War. In 1942, an unlikely quartet of researchers – assembled by J. Z. Young and including a German refugee (Ludwig Guttmann), a Czech prisoner of war (Ernst Gutmann) and Oxford Fellow Peter Medawar – investigated nerve regeneration, publishing their discovery that severed nerves regrew three to five times faster than thought, with functional recovery taking 2–3 weeks (Gutmann et al., 1942). ‘The failure of previous workers to clearly distinguish regeneration from recovery almost certainly led to the general view that axons grew much more slowly’, Jeff Lichtman and Joshua Sanes (Harvard University, USA) say in their JEB Classics review of the study (Lichtman and Sanes, 2006). Ultimately, all of the contributors went on to have successful careers: Ernst Gutmann returned to Czechoslovakia, eventually becoming the Head of the Department of Physiology and Deputy Director of the Czechoslovakian Academy of Sciences; Ludwig Guttmann established the National Spinal Injuries Centre at Stoke Mandeville Hospital, UK, ultimately founding the international Paralympic Movement; Medawar was awarded the Nobel Prize in 1960 for his investigations into transplantation immunity; and Young moved to University College, London, UK, to continue his research into the cellular basis of memory in the octopus (Lichtman and Sanes, 2006).
The 1950s saw a post-war experimental biology renaissance. One of the earlier papers from this era – August Krogh's final contribution to the journal, published with a young Torkel Weis-Fogh – reported the first measurements of metabolic rate and respiratory quotient in a flying desert locust, Schistocerca gregaria (Krogh and Weis-Fogh, 1951), while Rupert Billingham, with Medawar, laid down the basic procedures and principles of skin transplantation in their seminal paper, ‘The technique of free skin grafting in mammals’ (Billingham and Medawar, 1951). Revisiting the article, Jeremy Santa Ono (University of Michigan, USA) said, ‘Both clinicians and scientists still turn to the paper to understand fundamental concepts in dermatology and as a primer to skin grafting in mammals’ (Ono, 2004). By the middle of the decade, Gray switched his intellectual focus from the macroscopic motion of snakes and eels – to the microscopic world of spermatozoa, teaming up with aeronautical engineer G. J. Hancock (Queen Mary College, London, UK), to explain how the beating flagellum propels the miniscule gametes (Gray and Hancock, 1955). Gathering more than 40 Google Scholar citations in 2023, the paper continues to inspire and contribute to the nanotechnology revolution almost 70 years after Hancock derived the basic mathematics of flagellar propulsion. Three years later, University of Cambridge scientists Hans Lissmann and Ken Machin revealed a previously unidentified sense when they discovered that weakly electric fish can locate objects through the distortions in the electric fields they produce (Lissmann and Machin, 1958). ‘The story told in Cambridge was that the first clue to the electric sense had come when a student combed her hair near [the fish's] tank, and the Gymnarchus went wild’, McNeill Alexander reminisced (Alexander, 2006). Regardless of whether the tale is truth or myth, together the pair revealed and explained a novel sense ‘unlike anything we humans can experience’ (Alexander, 2006).
As the decades rolled on and the journal matured, JEB Editorial Board member George Hughes applied engineering principles to investigate gill resistance to water flow in fish ranging from small (12 g) mackerel to more sizeable angler fish (1.5 kg), revealing that, ‘more active fish not only have larger gill areas but that the conditions for gaseous exchange are better than for more sluggish forms and that the area is increased in such a way as to keep the resistance to flow to a low value’ (Hughes, 1966). With this research, Hughes inspired modern investigations into the function of the gill that continue to this day. Twelve months later, Henry Bennet-Clark and Eric Lucey solved the age-old mystery of how fleas perform their extraordinary jumps, achieving accelerations of 1020–1330 m s−2 within 1 ms of push off, by filming the insects at 1000 frames s−1 (Bennet-Clark and Lucey, 1967); an exceptional feat in the era of celluloid film. Calculating the power required to produce such explosive take-offs, it was clear that the manoeuvre could not be powered directly by muscular contraction, leading Bennet-Clark and Lucey to conclude that the ballistic leaps must be powered by the explosive release of energy stored in the insect's exoskeleton, like a catapult. One of the journal's most influential papers of the last century, Weis-Fogh's ‘Quick estimates of flight fitness in hovering animals, including novel mechanisms for lift production’ (Weis-Fogh, 1973), derived a series of equations to calculate the average lift coefficient, Reynolds number and aerodynamic power of flying animals ranging from tiny insects to hummingbirds. Weis-Fogh also identified the iconic ‘clap-and-fling’ mechanism of lift production, sowing the seed for Charles Ellington to found the microflight engineering revolution a decade later (Knight, 2010).
Transitioning into the 1980s, two of the most highly cited papers from that time focused on the physiology of flight. George Bartholomew, David Vleck and Carol Vleck (University of California, Los Angeles, USA) made the first instantaneous oxygen consumption measurements in moths (Bartholomew et al., 1981), showing that insect oxygen consumption can rocket to 70 times their resting oxygen consumption during preflight warmup. Six years later, James Marden (University of Vermont, USA) measured the maximum lift forces that could be generated by 49 insect species (including moths and butterflies), nine species of bird (from hummingbirds to pigeons) and three bat species (Marden, 1987). By attaching weights to the animals until they could no longer take off, Marden discovered that many of the animals, including members of all three groups, generate similar maximum lifts per flight muscle mass (54–63 N kg−1); however, he revealed that animals that benefited from Weis-Fogh's clap-and-fling for lift production are able to produce 25% more force.
Expanding the range of metabolic measurements to encapsulate large wild animals lay at the heart of C. Richard Taylor, Norman Heglund and Geoffrey Maloiy's extraordinary 1982 publication, ‘Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals’ (Taylor et al., 1982). The trio conducted the majority of the work in Kenya, cajoling and training animals ranging from dwarf mongooses (∼0.6 kg) up to 254 kg zebu cattle to move on a treadmill at various speeds while recording their oxygen consumption, before combining the new observations with the oxygen consumptions of 42 additional species – including birds – to determine how the mass-specific cost of transport scales with body mass. Based on their observations, the team defined a single equation that accurately predicts the cost of transport in animals ranging in size from ants to elephants (Kram, 2012). And in the final ground-breaking paper from the 1980s, Robert Josephson (University of California, Irvine, USA) revolutionised the measurement of synchronous muscle mechanical power output by adding phasic stimulation (Josephson, 1985) to a method previously used by Machin and John Pringle (Machin and Pringle, 1959), to develop his now legendary ‘work loop technique’ for the in vitro study of muscle mechanical work and power output across all muscle types.
The journal's influence in comparative biomechanics continued into the next decade, with Claire Farley, James Glasheen and Thomas McMahon (all at Harvard University) measuring the reaction forces of animals ranging from a tiny kangaroo rat (∼100 g) to a horse (135 kg) to find out how the stiffness of muscle–tendon spring units varies with the animal's speed. Although speed had very little effect on the stiffness of energy-storing muscle–tendon springs, the size of the animal did, with the largest animal's elastic units being 100 times stiffer than those of the smallest creatures (Farley et al., 1993). However, a new trend emerged during the 1990s: studies investigating the physiological responses of animals to climate change began to appear. In 1992, R. S. Batty and J. H. S. Blaxter (Dunstaffnage Marine Laboratory, UK) used the phrase ‘climate change’ in the journal for the first time (Batty and Blaxter, 1992) and in 1996, Jonathan Stillman and George Somero (Stanford University, USA) first mentioned ‘global warming’ (Stillman and Somero, 1996). Three years later, Lars Tomanek (Stanford University) and Somero investigated the impact of high temperatures on three Tegula sea snail species, residing at different heights on the rocky seashore at the Hopkins Marine Station. Although they discovered that all of the snails had some ability to acclimate to higher temperatures, it was clear even in the late 1990s that some were already living close to the highest temperatures that they could endure and were potentially at risk as environmental temperatures continued to climb (Tomanek and Somero, 1999).
While it is difficult to say at this close range which papers from the 2000s, 2010s and early 2020s will go on to become classics, there are already studies that have made defining contributions to the literature, including Sane and Dickinson's ‘The aerodynamic effects of wing rotation and a revised quasi-steady model of flapping flight’ (Sane and Dickinson, 2002), ‘Frictional adhesion: a new angle on gecko attachment’ by Keller Autumn and colleagues (Autumn et al., 2006) and ‘Biomimetic shark skin: design, fabrication and hydrodynamic function’ by Li Wen, James Weaver and George Lauder (Wen et al., 2014). Only time will tell which other studies will shift paradigms and reveal the mysteries of the extraordinary creatures that inspire our community; new and unexpected gems will continue to emerge.
Looking to the future
As the journal embarks on the next century of discovery, the subjects it covers remain as diverse as ever. From jet propulsion in cuttlefish (Gladman and Askew, 2023) and jellyfish (Strock et al., 2023), to hearing in sharks (Nieder et al., 2023a,b), echolocation in bats (de Framond et al., 2023) and how tardigrades distinguish males from females using their sense of smell (Chartrain et al., 2023), the journal never fails to intrigue and inform. We hope that you have enjoyed this snapshot of the astonishing world encased within the journal's archive of the past 100 years and we look forward to continuing to share your discoveries with the extraordinary community of researchers that is the lifeblood of Journal of Experimental Biology.
The author declares no competing or financial interests.