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Larval Ecology of Marine Invertebrates: a Sesquicentennial History

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Larval Ecology of Marine Invertebrates: a Sesquicentennial History FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1990 Taylor & Francis Group. This is an electronic published version of an article which may be cited as: Young, C. M. (1990). Larval ecology of marine invertebrates: a sesquicentennial history. Ophelia, 32(1-2), 1-48. doi: 10.1080/00785236.1990.10422023 Ophelia is available online at: http://www.tandfonline.com/openurl?genre=article&issn=0078- 5326&date=1990&volume=32&issue=1-2&spage=1 -- OPHELIA 32 (1-2): 1-48 (October 1990) LARVAL ECOLOGY OF MARINE INVERTEBRATES: A SESQUICENTENNIAL HISTORY Craig M. .Young Division of Marine Science, Harbor Branch Oceanographic Institution, 5600 Old Dixie Hwy., Ft. Pierce, Florida 34946, USA ABSTRACT Although larval ecology has roots as far back as Aristotle, the earliest accurate ideas about larval recruitment, dispersal, and behavior arose about 150 years ago, during the time of J. Vaughn Thompson and Edward Forbes. In this review, the history oflarval ecology is traced from the initial discovery of larvae and the early formulation of ideas in the nineteenth century through the de­ velopment of methodology for addressing hard-to-study field processes in the 1980's. A survey of the literature in major marine biologyjournals reveals the overall trends in larval research and the temporal changes in the proportion of effort devoted to various kinds of studies. Many recent studies of larval processes resemble seldom-cited studies that were done more than a halfcentury earlier. INTRODUCTION Marine invertebrate larval ecology is a youngdiscipline. Unlike many areas ofbi­ ology which legitimately trace their roots to the ideas and observations ofAristo­ tle, larval ecology did not (indeed could not) begin until larvae were first recog­ nized as such. Thus, although Aristotle [1965] did report experiments on larval recruitment in the sea he attributed the phenomenon to spontaneous generation. Brooded larvae of oysters and polychaetes were recognized before 1800 (Brach 1689, Leeuwenhoek 1722, Slabber 1778), but the first speculations on the ecologi­ cal significance of larvae appear not to have occurred until Thompson (1828, 1830) recognized the true affinities offree-living zoeae and cyprids about one and one-halfcenturies ago. With only a few exceptions, the remaininglarval forms we know today were recognized and described between 1845 and 1890. Many impor­ tant ecological ideas about larvae arose during the nineteenth century, but the term "Larval Ecology" was coined and popularized less than a halfcentury ago (Thorson 1946). Ecology may be defined as "the study of factors influencing the distribution and abundance of species" (Andrewartha 1961, Krebs 1972). Larval ecology is defined in similar terms, but with a two-fold twist: 1)the study offactors influenc­ ing the distribution and abundance oflarvae, and 2) the study ofprocesses occur- 2 CRAIG M. YOUNG ring in the embryonic and larval stages that influence the distributions and abun­ dances ofadults. By these definitions, the field integrates those aspects ofbehavior, physiology, and embryology that help us understand field processes. Studies of larval adaptation and evolution have traditionally been part ofthe field. For our purposes, however, neither purely morphological studies nor the use oflarvae as models of suborganismal phenomena constitutes larval ecology. Ecology, by its very nature, attempts to infer processes occurring under natural conditions in the field. In this review, I will trace the historical progress of such efforts from 1828 to the present day. Many aspects ofinvertebrate larval biology, notably morphology and behavior, have been reviewed adequately in recent years (Meadows & Campbell 1972b, Chia & Rice, 1978, Scheltema 1974, Crisp 1974,1976, Giese & Pearse 1974 and subsequent volumes) and a few historical ac­ counts have appeared (Crisp 1984, Winsor 1969, 1976, Meadows & Campbell 1972a). My motivation for adding yet another history stems from a sense that the current generation ofmarine ecologists (I include myselfhere), in its frenzied ex­ ploration ofrecruitment, juvenile processes, and "supply-side ecology", has often failed to acknowledge its academic roots (Underwood & Fairweather 1989, Young 1988). As is common in the history ofscience, major ideas are subject to rediscov­ ery by each generation, and really new ideas are hard to come by. I hope that a review ofthe older ideas and methods will help researchers identify the areas in which our understanding is inadequate, thereby stimulating original research in those areas. As evidenced by the recent surge ofinterest in "supply-side ecology" (Rough­ garden et al. 1988, Underwood & Fairweather 1989), recruitment studies have now become quite fashionable. However, relatively few classic papers on larvae tend to be cited in the recent recruitment literature (Young 1988). This is a sign that the logical and expected marriage between mainstream marine ecology and larval biology has been difficult to consummate. Larval ecology lies at the inter­ face oftwo disciplines, ecology and embryology, so practitioners may be trained in eithercamp. Larval ecologists trained as ecologists tend to be field oriented and interested in mechanisms that influence populations and communities, whereas those trained in the laboratory as embryologists or traditional zoologists often emphasize studies of functional morphology, physiology or behavior at the or­ ganismal and suborganismal levels. Where ecologists have neglected early life history stages it is generally because these stages are difficult to study in the field. It is easier to remove predators, cage prey, enhance densities ofcompetitors, or to manipulate the physical environment of adults than to design and run field studies that would help us sort out the contribution ofplanktonic larvae to popu­ lation variability. Thus, the plankton has sometimes been regarded as a "mystery stage" ora "black box" that holds many keys to the understandingofmarine ecol­ ogy, yet has been difficult to crack. Ifthe new field ofsupply-side ecology is reallyjust a repackagingofthe old field ... ------ ~~-~ --------------- LARVAL ECOLOGY OF MARINE INVERTEBRATES 3 oflarval ecology, as has been suggested (Young 1988, Underwood & Fairweather 1989), why has a 150 year tradition of larval ecology seldom been incorporated into population models? Have the methods oflarval ecology yielded weak infer­ ences? Have the questions addressed been inappropriate? If work with microscopic larvae is to be relevant in interpreting the ecology ofpopulations or communities, it must be either conducted under field conditions or be designed for extrapolation to field conditions with minimal and reasonable assumptions. In this paper, I will review the approaches that have dominated the field oflarval ecology from its inception, highlighting efforts to extrapolate conclusions to the field. Before discussing specific historical periods, I shall provide a broad over­ view of the historical trends by presenting a survey of larval ecology papers in major marine biologyjournals. The remaining papers in this volume discuss ap­ proaches and techniques that are likely to yield strong inferences in the study of larval ecology. This paper would not have been possible without the help of many individuals, particularly those with long memories and old photographs. I thank the librarians at the Marine Biological Laborato­ ry (Woods Hole), the Museum of Comparative Zoology, (Harvard), and Scripps Institute of Oceanography, LaJolla. Jane Fessenden at Woods Hole was especially helpful in granting me ac­ cess to rare books and photographs in the MBL archives. Ruth Turner, Rudolf Scheltema, James Hanks, Joel Hedgpeth, Mary Rice,John Ryland,John Ryther, Paul Tyler, Hal Haskin, Bob Ingle, Kathryn Manahan, Dennis Crisp and Pamela B1ades-Eckelbarger provided photos and/or reminiscences about larval ecologists they have known. Mary Rice and Kevin Eckelbarger com­ mented on the manuscript. Brian Bingham checked my French translations and xeroxed many hundreds of pages of old manuscripts at the M.C.Z. and M.B.L. libraries. Birger Neuhaus assisted with German references. Kristen Metzger, HBOI librarian, ran numerous computer literature searches and Lane Cameron helped plot the data. Joel Elliot kindly mailed me tables of contents from journals I could not find in Ft. Pierce. The project was supported by grant no. OCE-8717922 from the National Science Foundation and is Harbor Branch Contribution No. 776. PUBLICATION TRENDS IN LARVAL BIOLOGY Papers on larvae are found in many kinds ofjournals, including those devoted primarily to developmental processes, systematics and ultrastructure. A compre­ hensive survey of the entire larval literature therefore goes beyond the scope of this review. Instead, we sampled the larval literature by undertaking a compre­ hensive search of six journals that have traditionally accepted papers on ecologi­ cal aspects of larval biology: Marine Biology, Journal of the Marine Biological Association of the United Kingdom, Biological Bulletin, Journal ofExperimen­ tal Marine Biology and Ecology, Marine Ecology Progress Series, and Ophelia. Because the relative proportion of larval papers in the more general ecological journals (e.g. Ecology) is low and few larval papers appeared in thesejournals un­ til the past decade, they were not included in this historical analysis. Special sym­ posium volumes and reviewjournals
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