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RICHARD W. EPPLEY (1931–2023): Generous Giant in the Field of Biological Oceanography

2024; Wiley; Volume: 33; Issue: 1 Linguagem: Inglês

10.1002/lob.10621

1539-6088

John J. Cullen, Zoe A. Eppley,

Marine and coastal ecosystems

Richard W. "Dick" Eppley died peacefully on 7 October 2023, just 5 days shy of his 92nd birthday. When the news spread among oceanographers now regarded as elders, one word in particular emerged: giant. Dick Eppley was indeed a giant in the field of biological oceanography, not only because of his fundamental contributions to its conceptual structure, but also through the lasting impacts of his mentorship, quiet support, and inspiration on a generation of scientists who have been guided by his vision of how to study processes that structure food webs and biogeochemical cycles in the sea (Fig. 1). Son of a fifth-generation metalworker, Dick Eppley broke the mold. He was born and raised in Washington State, where he attended college (B.A. in Botany, Washington State College, Pullman) and met Jean, his life-long sweetheart. Dick played jazz in big bands and quartets to make ends meet and won a National Science Foundation (NSF) scholarship for graduate study. After quickly proposing to and marrying Jean, he enrolled in Stanford University's graduate program in marine biology. He completed his Ph.D. in plant physiology under the direction of Lawrence W. Blinks, studying ion transport in seaweeds at the Hopkins Marine Station. Seeking better opportunities for his growing family after teaching at the University of Southern California (1957–1960), he took a research position with the Northrop Corporation (1960–1963) where he worked on culturing algae for life support in space vehicles. Dick's pivot to oceanography began in 1963 when he was recruited by the innovative and immensely influential John D. H. Strickland to join the new Food Chain Research Group (FCRG) at the Scripps Institution of Oceanography. Eppley remained with the FCRG throughout its existence, 1963–1989, as a Research Biologist, Lecturer, and de facto group leader after Strickland's death in 1970. When accepting ASLO's John Martin Award for his classic paper on new production (Table 1, Eppley and Peterson 1979), Dick showed a group photo of the FCRG, describing them as a "fun group to be with … kind of a who's who of biological oceanography at the time." He took the time to identify contributions of individual FCRG students and each of the support staff, always the appreciative and proud leader. Dick Eppley's publications (full list in Supporting Information) serve as a robust tutorial in how to describe and explain the distributions and activities of marine phytoplankton and their influence on marine food webs and biogeochemical cycles. Cumulatively, their influence on biological oceanography is inestimable. A select few illustrate the brilliance and long-term impact of Dick's research. Eppley, R. W., and B. J. Peterson. 1979. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282: 677–680. doi:10.1038/282677a0 (ASLO's 2008 John Martin Award for a high-impact paper.*) Dick's boss, John D. Isaacs, did not like it and Science rejected it.† Yet this study, along with Dugdale and Goering's (1967) landmark paper on new and regenerated production, was transformational in linking the sinking flux of particulate organic carbon to N-based new production, which, along with total primary production, is driven by the physical process of mixing and upwelling. "Ocean physics and biology were formally wed by this landmark achievement" (Barber and Hilting 2000). Frequently cited to this day and a perennial on classroom reading lists, it is a foundational publication in ocean science. Rather than relying on summaries of this paper's key contributions, read it again to see exactly what Eppley and Peterson wrote. Eppley, R. W. 1972. Temperature and phytoplankton growth in the sea. Fish. Bull. 70: 1063–1085 (https://fisherybulletin.nmfs.noaa.gov/sites/default/files/pdf-content/1972/704/eppley.pdf).‡ This paper is frequently cited to this day for its Q10 (increase in growth rate per 10°C rise) equal to 1.88—a centrally important parameter in many models of primary production and food-web dynamics that are increasingly relevant to a warming ocean. But it is so much more. In this scholarly review, Dick describes interrelationships among growth rate, photosynthetic rate per weight of chlorophyll, and the carbon : chlorophyll ratio in phytoplankton as influenced by temperature. Now called photoacclimation, this remains a cutting-edge topic for research and modeling 50 yr after Eppley helped to set the stage. Eppley, R. W., J. N. Rogers, and J. J. McCarthy. 1969. Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnol. Oceanogr. 14: 912–920. doi:10.4319/lo.1969.14.6.0912 In Eppley's words: "This work came about in order to find out if the kinetic parameters of nitrate and ammonium uptake by marine phytoplankton could help explain why some species live in the nutrient-impoverished central oceans while others live in richer coastal regions; why there is often a succession of species over the seasons in coastal waters; and why some species live in rock pools at the ocean's edge but not in the ocean itself."§ Acknowledging that Jim McCarthy was instrumental in the ecological interpretation, Eppley succeeded admirably and their insights have stood the test of time. Trait-based modeling of phytoplankton dynamics has its roots in ground-breaking studies like this. Eppley, R. W., and E. H. Renger. 1974. Nitrogen assimilation of an oceanic diatom in nitrogen-limited continuous culture. J. Phycol. 10: 15–23. doi:10.1111/j.1529-8817.1974.tb02671.x Exploiting the power of experiments on continuous cultures to describe relationships between nutrient-limited growth rate and the chemical composition and physiological characteristics of phytoplankton, Eppley built upon foundational research by Jack Myers to lay the groundwork for diagnosing nutrient limitation in natural phytoplankton, including the realization that phytoplankton could grow rapidly at concentrations of limiting nutrients that were bordering on or below the limit of detection by methods then available. This set the stage for Joel Goldman's transformative concept of relative growth rate that provided a robust framework for describing nutrient limitation of growth. Eppley's carefully targeted experimental design, comprehensive analysis of the data, and perspicacious interpretations of results in historical context stand as models for today's molecular studies, for which the number of potential diagnostics is nearly unlimited, but the challenges of relating culture work to nature are the same. Eppley, R. W., O. Holm-Hansen, and J. D. H. Strickland. 1968. Some observations on the vertical migration of dinoflagellates. J. Phycol. 4: 333–340. doi:10.1111/j.1529-8817.1968.tb04704.x Pioneers in the use of a pump-and-hose to profile in vivo chlorophyll fluorescence and in using the 3-m diameter by 10-m "deep tank" at Scripps for experimental work, Eppley and FCRG colleagues used these tools to demonstrate that dinoflagellates can migrate vertically each day and exploit deep nitrate at night if it is depleted at the surface. Behavior patterns differed with nutrient supply and between species. It has since been shown that these adaptions are essential to understanding competition between species, harmful algal bloom dynamics, and stoichiometric variability of C, N, and O in vertical profiles. Dick Eppley took a special joy in educating young scientists. Even though he never had a tenure-track faculty position, he managed to support a steady stream of students and postdocs through research grants, often involving them in the proposal writing. He also provided students with a travel stipend when they were presenting results, even if it meant that he had no funds left for himself. Most importantly, Dick Eppley was an unwavering source of support and guidance in the learning process for all who were fortunate enough to be supervised by him. As a bonus, Dick's long- time research associate, Ed Renger, expertly—and with legendary humor—trained us all in laboratory and shipboard procedures. Ph.D. students (year of Ph.D.) of Richard W. Eppley, with current or last position: James J. McCarthy (1971) Alexander Agassiz Professor of Biological Oceanography, Harvard University (died 2019). Mary Jane Perry (1974) Emerita Professor, University of Maine, Orono Michael M. Sinclair (1977) Director of the Bedford Institute of Oceanography, Canada (retired) C. Susan Weiler (1978) Senior Research Scientist, Whitman College John J. Cullen (1980) Professor Emeritus of Oceanography, Dalhousie University William M. (Barney) Balch (1985) Senior Research Scientist Emeritus, Bigelow Laboratory for Ocean Sciences James R. Nelson (1986) Retired Emeritus, University of Georgia, Skidaway Institute Patricia A. Matrai (1988) Senior Research Scientist Emerita, Bigelow Laboratory for Ocean Sciences Postdoctoral supervisor (years) to the following: Jonathan H. Sharp (1971–1973) Professor Emeritus of Oceanography, School of Marine Science and Policy, University of Delaware W. Glenn Harrison (1974–1976) Manager, Ocean and Ecosystem Sciences Division and Senior Research Scientist, Bedford Institute of Oceanography, Canada (retired) Sallie W. (Penny) Chisholm (1974–1976) Institute Professor, Massachusetts Institute of Technology Don G. Redalje (1980–1982) Retired Professor, The University of Southern Mississippi Department of Marine Science The 1990 article describing Eppley's research provides a roadmap to a trove of information on his publications and their impacts at that time. Readily available with open access, it stands as a great resource for students. Because Dick always strove to place his work in historical context—he considered it "an obligation"—his papers also guide the reader to the ground-breaking work by others. Recognizing the breadth, depth, and insight of his research, Dick's students and postdocs concluded that "Richard W. Eppley has established himself as one of the most influential biological oceanographers of this century through his contributions to the field of phytoplankton physiological ecology and his interdisciplinary approach to oceanographic processes" (Weiler et al. 1990). As illustrated with a few examples of key papers in Table 1, Dick's work has continued to influence the direction of oceanographic research well into the 21st century and it is clearly foundational for studies of phytoplankton dynamics and biogeochemical cycles. For example, Eppley and Bruce Peterson's 1979 paper, "Particulate organic matter flux and planktonic new production in the deep ocean" was recognized in 2008 with ASLO's John Martin Award for high-impact papers (Table 1; Eppley and Peterson 1979). Richard Barber—another giant in biological oceanography—described it, along with Dugdale and Goering's (1967) landmark paper on new and regenerated production, as the "link forged between physical and biological oceanography. The new concept required that physical processes of mixing and upwelling be an integral part of ecosystem models dealing with new production, fish production, or export of organic material from the surface layer" (Barber and Hilting 2000). His 1972 paper on temperature and phytoplankton growth in the sea (Table 1, Eppley 1972) is still highly cited today, no surprise given its relevance to the warming world ocean. With almost a fifth of the total citations of this paper since 2020, its equation for the dependence of phytoplankton growth on temperature can be found in the roots of most plankton- and, hence, Earth-system models. Dick also brought people together to solve thorny global issues: such as with the Plankton Rate Processes in Oligotrophic Oceans (PRPOOS, aka "purpose") program when many then-new techniques to measure primary productivity (dilution, 18O, and dark–light bottle oxygen methods) were first tested, and then tested together with the 14C method, under newly understood contaminant-free conditions; this approach, designed to address active controversies, provided the still-accepted value for primary production for the open ocean (Marra 2015). The success of PRPOOS, and the new knowledge gained, helped to formulate a much larger project that was eventually dubbed the Global Ocean Flux Study (GOFS), and later Joint Global Ocean Flux Study (JGOFS) when the U.S. project became an international program. Dick was a leading member of the planning committee for the first workshop on GOFS and later became a valued member of the Executive Committee, helping to create the research framework that would support oceanographic fieldwork for more than one decade, including plans to build an ocean observatory for time-series studies in the North Pacific Subtropical Gyre, where Dick and others in the FCRG had conducted the truly pioneering work during the 1970s. The Hawaii Ocean Time-series project (HOT) was founded in 1988 and has been funded continually ever since. Looking back, it is fair to say that Dick's influence both as a respected scientist and as an advocate for the GOFS project was instrumental in establishing the time-series station, providing inestimable value to oceanography and microbial ecology. Service to the oceanographic community was always important to Dick. Besides being President of ASLO (1981–1982), he was a member of Executive/Steering Committees for the NSF Ocean Sciences Division (1981–1985), GOFS (1985–1989), and the international Scientific Committee for Oceanic Research (SCOR) committee for JGOFS. Highlights of his many contributions to institutions, societies, and agencies include: Rotator, U.S. Atomic Energy Commission, Biomedical and Environmental Research Division (1972–1973); and participation in 26 working groups and workshops, including the NASA SeaWiFS Working Group for what was then the next ocean color scanner. Despite his many commitments, he set aside the time to review an average of 40 manuscripts per year in addition to proposals to NSF, the Department of Energy, and Sea Grant. He also served as Biology Editor for Journal of Geophysical Research Oceans. Not one for self-promotion, Dick was nonetheless recognized with major honors, including membership in Phi Beta Kappa, the Darbaker Prize in Phycology by the Botanical Society of America (1971), and the G. Evelyn Hutchinson Medal from ASLO in 1984. In 1990, he was the first biological oceanographer elected Fellow of the American Geophysical Union, sparking a near-riot among exuberant biologists at the awards ceremony in San Francisco. As a celebration of his inspirational contributions, the 1991 Brookhaven Symposium on Primary Productivity and Biogeochemical Cycles in the Sea was dedicated to Eppley. The proceedings are a testament to his legacy; they include Dick's own remembrances, illustrating the breadth of his research and his generosity in describing who influenced his journey of discovery (Eppley 1992). These examples only scratch the surface. Dick Eppley's impact and legacy will continue to be felt for decades to come, establishing him as one of the most influential biological oceanographers of all time. Readers of Eppley's publications (Table 1; Supporting Information) will be rewarded with examples of the best in scientific research and writing: well-chosen questions explored with innovative and rigorous experimental approaches, data interpreted critically with special attention to uncertainties, and discussions of results leading to fundamental insights, always placed in historical context. Times have changed and no one can cite the relevant literature as Dick did, but today's researchers can see that building upon the work of others, rather than emphasizing self-citation, can serve as the most effective scientific strategy for advancing the field. Dick, with his long-time research associate, Ed Renger, exemplified how to run a research laboratory as they masterfully mentored students in this basic knowledge. In the days long before formal courses on such, lucky students received informal mentoring on how to write proposals, review proposals, develop a conceptual model, critically read scientific papers, and even how to be a chief scientist, complete final cruise reports, and submit data for archiving. Students in the Eppley lab also received informal instruction on practical skills like how to pack, mobilize, and demobilize from a cruise. Dick also offered an intensive, though informal, one-on-one reading course in "Phytoplankton Lore"—going back to the early 20th century—that provided the perfect foundation for a properly grounded career studying the physiological ecology of phytoplankton. The bottom line was that mentoring from Dick was all about the duty to do the most careful science possible. Those of us who benefited from his tutelage during stays in his laboratory or through other associations are a particularly fortunate lot. There was also mentoring about life balance. Through example, Dick showed students that it was possible to balance one's science life with a home life. He always headed home at 5PM to be with the family (plus maybe do some manuscript reviewing). He maintained a life-long passion for music. Dick and Jean's hospitality was epic, with regular parties at their mountain-side home that frequently included jam sessions with Dick on piano, sax, or clarinet, with other scientists (and closet musicians!) joining in until the wee hours of the morning. Indeed, Dick's jam sessions provided a metaphor of how he approached his science, always with collaboration of people, ideas, and a healthy dose of improvisation. And as in both music and science, when mistakes happened (which they inevitably did), one picks up the pieces and moves on without missing a beat! Dick embraced early retirement at the age of 58, savoring the leisure as much as he did his professional pursuits (Fig. 3). He laughed that he left at the top of his game to become an apprentice handyman for Jean. Their summers were spent at Jean's family homestead cabin in the Cascade Mountains of Washington State. In San Diego, Dick relished softball, golf, and weekly strolls with the "Old Guys." The couple, avid dancers, were members of two ballroom dance clubs, forging friendships that extended to global explorations. Dick's colleagues, students, and postdocs from near and far gathered in San Diego to celebrate his 80th birthday, and shared many fond memories. As age took its toll, Dick and Jean moved to Eskaton Village in Grass Valley, California, where they celebrated their 70th wedding anniversary in their final year together. Dick died peacefully, after a long and rich life. He succumbed to the ravages of age, but left a glow in many hearts. A full record of Richard W. Eppley's publications can be found in the Supporting Information. The following people supplied material or comments for this tribute and also shared many appreciative stories that could not be accommodated in this format: Barney Balch, Penny Chisholm, Paul Falkowski, Glenn Harrison, Dave Karl, Ed Laws, Paty Matrai, Mary Jane Perry, Don Redalje, Jon Sharp, Mike Sinclair, and Sue Weiler. Data S1. Supporting Information. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.