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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

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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 were excluded because they cannot be inter- 4 CRAIG M. YOUNG

Table 1. Scheme for classifying papers in larval biology on the basis of approaches and methods used. Major categories are the same as those plotted in Figs 1 and 3-5. Subcategories are ordered on the basis of applicability to field inferences in larval ecology. Major Category Subcategory I. Field Observations & Experiments 1. Direct field observations oflarvae. 2. Field manipulations of settlement surfaces. 3. Field experiments in enclosures. II. Sampling of Field Patterns. 4. Field sampling of spatial patterns, temporal patterns, or diets. 5. Field studies of settlement rates or patterns. 6. Larval processes inferred from field patterns of adults or from adult shell morphology. III. Laboratory Studies 7. Behavioral studies in lab correlated with field data on adult distribution patterns. 8. Behavioral studies with no supporting field data. 9. Lab. studies on physiology, feeding, growth, etc. with no supporting field observations. IV. Morphology 10. Structural and ultrastructural studies of larvae. 11. Studies oflarval systematics. preted as part of a continuous time series. The searches were done not by com­ puter, but by scanning tables of contents of each individual issue from the first volume until the end of 1988. No volumes or numbers were missed. Each paper was listed in the major category of information, or classified according to the major approaches used in the study. Although 10 different categories were used in the initial survey (Table 1), the data were ultimately collapsed into 4 major categories for presentation: 1) morphological studies, 2) laboratory studies of physiology, behavior, nutrition, etc., 3) field studies in which spatial or temporal patterns oflarvae or settlers were sampled, and 4) field studies involving direct in situ observations or field manipulations. These represent a continuum of ap­ proaches from those least applicable to field ecology to those most likely to produce strong inferences. The total number ofpapers published by eachjournal duringeach year(for use in the denominators ofproportions) were obtained from tables ofcontents. Obituaries, letters, financial reports, editorials, etc. were not included in the analysis. -

LARVAL ECOLOGY OF MARINE INVERTEBRATES 5

180 -~~~-~----~~--~----~------,

160 • Field Observations & Exper-iments 140 o Sompf.oq of Field Patterns l" Q) gg Laboratory Studies Q 120 0 ~ Morphology Q. Fig. 1. The number of papers on a 100 various aspects of larval biology ~ 80 0 appearing in 6 marine biology E 60 :J journals from 1893 through 1988. Z The four major categories are 40 taken from the classification 20 scheme in Table 1. Data from each o~~" 5-year interval are pooled for each 1893 1903 19L3 192.3 1933 1943 1953 1963 1973 1983 point. 5~Year Interval

Like many field of science, the number of papers on larvae has seen an ex­ ponential increase over the past century, with the curve becoming particularly steep over the past 20 years (Fig. 1). Although there has been a slight increase in the number of morphological studies since electron microscopy became a com­ mon tool in the early sixties, most ofthe 2-decade growth can be attributed to an explosion of studies carried out in the laboratory. In such studies, culture methods developed for embryology are used to explore the responses oflarvae to various substances, environmental factors, or stimuli, either behaviorally or physiologically. Field sampling oflarvae has received minor, sporadic emphasis since the 1920's and has increased in proportion to earlier efforts only in the present decade. Field experimentation shows two peaks: one in the decades sur­ rounding the second world war, when fouling studies were important for reasons ofeconomy and national security, and one in the last decade when in situ studies using direct methods commenced in earnest. Part ofthe increase in larval papers in recent years can be attributed to the larg­ er sizes ofvolumes and more issues per year ofmost major marine biology jour­ nals. However, the proportion ofthe total literature made up oflarval papers has always fluctuated within relatively narrow limits. Larval studies increased from less than 1% ofpapers in the years preceding 1908 to nearly 7% ofall marine biol­ ogy papers in the early 1950's (Fig. 2). Since 1958, larval biology has grown at about the same rate as the rest ofmarine science, producing for that entire period between 4% and 6% of all papers published in marine biology journals. The waxing and waning of interest in larvae is most apparent in the two jour­ nals that have been publishinglarval papers for the longest period oftime, Biolog­ ical Bulletin and Journal of the Marine Biological Association of the United Kingdom. The latter, which is also the older, contains many of the landmark papers in larval ecology, some ofwhich have been largely forgotten. In The Bio­ logical Bulletin, fluctuating interest in larval biology is roughly correlated with major historical and economic events in the United States (Fig. 3). Thus, for ex- 6 CRAIG M. YOUNG

4000 ------0.10 ...... Totol Papers 3600 • -. Papers on Larvae ·0 3200 0 0.08 -0 (" 00 QJ 2800 :J;:1- Q r-. , ' ,0 ei: 2400 , ' 0.06 0 :J , ' , ' ·--k :< 0 '0 2000 , ' 0_ , ' --j L , ' rno 1i 1600 It- -. 0.04 ~·o )! .. E , " 0 :J 1200 ~/ \ ~ .. -.., .o U Z , , '< 0 , -0 800 0.02 (1) , ;;; 400 '.

o ~·I--r--r-----, Iii 0,00 1893 1903 1913 1923 1933 1943 1953 1963 1973 1983 5-Year Interval Fig. 2. Fluctuations in total number oflarval papers (dotted line) in 6 marine biology journals over the past 100 years, and proportion of all papers in the same journals that deal with aspects of larval biology (solid line) over the past 100 years.

24,--·~---- J. Mar. Bio[. Assn. U.K.

20

(" QJ Q 16 o o '0 12 , QJ .o E 8 :J Z

1903 1913 1923 1933 1943 1953 1963 1973 1983

35 "iOO~logicol B~-----_·---·_­

30

(" ~ 25 r CL 20 '0

:J 1 10 z Fig. 3. Publication trends in larval bi­

5 ology: Journal of the Marine Biologi­ cal Association of the United King­ dom and Biological Bulletin. See Fig. 1 1913 1923 1933 1943 1953 1963 1973 1983 for a key to the shading patterns in this 5-Year Interval and subsequent curves. p

LARVAL ECOLOGY OF MARINE INVERTEBRATES 7

10 ------, Mar. Ecal. Prag. Ser.

8

L Q) .o E ::J Z o~~ 1979 1981 1983 1985 1987

Ophelia

~ Q) 5 o, o Q.. 4 o ~ 3 .o E ::J 2 Z

Fig.4. Publication trends in larval biol­ ogy: Marine Ecology Progress Series 1969 1974 1979 1984 and Ophelia. Year

ample, larval biology experienced significant declines during World War I, dur­ ing the great depression, and the height ofthe Vietnam war. An increase in larval papers during World War II was indicative ofan explosion ofresearch on applied aspects offouling, which produced the largest number offield studies in the histo­ ry ofthe journal. In the North Americanjournal, many ofthe laboratory papers that contributed to a major increase in the late 60's and 70's dealt with responses of larvae to pollutants, a trend that mirrored the upswing in public concern for the environment during that era. The peak in larval studies that occurred in Great Britain in the 1950's was followed by a peak in the United States with a lag of about 10 years. Throughout its history, Journal of the Marine Biological As­ sociation of the United Kingdom has supported a sustained interest in morpho­ logical descriptions oflarvae (Fig. 3), though papers on aspects oflarval ecology were present even in the first volumes (Weldon 1889, Montagu 1890). The Bio­ logical Bulletin, by contrast, always placed greater emphasis on laboratory ex­ perimentation than morphology until ultrastructural studies began to appear in the early 1970's (Fig. 3). Most of the newer journals have been dominated by laboratory studies. The 8 CRAIG M. YOUNG

major emphasis in Ophelia has always been morphology until the last four years, when the few larval studies published have involved both field and laboratory ex­ perimentation (Fig. 4). Marine Ecology Progress Series, in accordance with its mandate, accepts no papers on morphology. Ever since its founding, field studies have been published in most years, but these were still overshadowed by laborato­ ry experiments until the past two years, when all larval studies published in Ma­ rine Ecology Progress Series involved either field sampling or field experimenta­ tion (Fig. 4). The number oflarval papers published In Marine Biology has al­ ways fluctuated within relatively stable limits (Fig. 5), whereas the overall num­ ber oflarval papers published by Journal of Experimental Marine Biology and Ecology, a journal ofapproximately the same age, has increased steadily (Fig. 5). In bothjournals, direct field studies have become prominent only in the last few years.

LARVAL ECOLOGY IN THE NINETEENTH CENTURY AND EARLIER

The discovery and recognition oflarval jorms John Vaughn Thompson, an amateur naturalist whose profession as surgeon in the Irish army provided him with opportunities to explore the coastal waters of Gibraltar, Madagascar, Guiana, the West Indies, and Mauritius, made his most famous observations in the Irish harbor of Cork (Winsor 1969, Wheeler 1968). He first discovered the nature of crustacean larvae between 1823 and 1826 (Thompson 1828, 1830). By observing the transformation of a zoea into a lO-legged megalopa and the metamorphosis of swimming cyprids into benthic barnacles, Thompson not only clarified the taxonomic affinities of barnacles (originally considered baby geese, then molluscs) and zoeae (previously a distinct genus of uncertain affinity), but also paved the way for further work on inver­ tebrate larvae. Although some of his studies were disputed by contemporaries (Westwood 1835), Thompson's observations stood the test oftime; indeed, many ideas and techniques often attributed to later workers actually originated with Thompson. His 1828 paper, for example, contains the following advice on collect­ ing larvae: ... [the naturalist] must use the greatest diligence, seizing every opportunity when the way of the ship does not exceed three or four miles per hour, to throw out a-stern a small towing net of gauze, bunting, or other tolerably close material, occasionally drawing it up, and turning it inside out into a glass vessel of seawater, to ascertain what captures have been made; when a ship goes at a greater rate, and in stormy weather, a net ofthis kind might be appended to the spout of one of the sea-water pumps, and examined three or four times a day, or oftener, according to the circumstances. ?

LARVAL ECOLOGY OF MARINE INVERTEBRATES 9

20 J Exp. Mar. Bioi Ecol

~ 15 QJ CL 0 G- o 10 L QJ D t ::J Z 5

0 1967 1972 1977 1982 1987

Marine Biology

"I15 ~ QJ CL 0 G- o 10 Q; 0 E ::J Z

Fig. 5. Publication trends in larval biology: Journal of Experimental O· Marine Biology and Ecology and 1967 1972 1977 1982 1987 Marine Biology. Year

Thus, the discoverer ofcrustacean larvae also invented the plankton net and the plankton pump, which remain the major tools for sampling larvae even today. Thompson was sent to New South Wales, Australia, in 1835, to work as a medi­ al officer in the convict settlement there (Wheeler 1968). The same year, he pub­ lished a breakthrough in echinoderm embryology: the discovery that sessile, stalked pentacrinoids were actually young comatulids (Thompson 1835, see review by Winsor 1976). Thomson died in Australia in 1847 without making fur­ ther published contributions to larval biology. In 1845, about 20 years after Thompson's seminal discoveries, Johannes Muller of Berlin (Fig. 6-A), who had already gained prominence as Germany's foremost physiologist, apparently reinvented the plankton net for use with sum­ mer courses taught at Heligoland (Muller 1846a, Winsor 1976). His findings in the plankton included echinoplutei, ophioplutei, tornaria larvae, and ac­ tinotrochs, all of which he described in a series of beautifully illustrated papers. Just one year before Muller's first plankton-collecting trip, the Norwegian biolo­ gist Michael Sars (1844) had published the first description ofdevelopment in an asteroid with lecithotrophic development. However, this description was of an 10 CRAIG M. YOUNG unusual species and did not shed much light on the problem of echinoderm de­ velopment in general. It was not until Muller and his students found an ophiopluteus with the rudiment of a young ophiuroid (which Muller named Pluteus paradoxus) that the nature of the echinoderm life cycle was understood. Muller published his classic paper describing echinoderm metamorphosis in 1850. One yearlater, Edward Desor (1851), a Swiss seismologist who had come to America to work with Louis Agassiz at Harvard, published observations on de­ velopment ofa planktotrophic starfish larva. These exciting discoveries generat­ ed much discussion among systematists interested in the relationships ofvarious phyla. Such phylogenetic debates, which have been reviewed in detail by Winsor (1976), completely overshadowed any interest in larval ecology of echinoderms. The initial recognition of larval polychaetes was published by the Dutch microscopist Martinus Slabber (1778), who described larvae of syllids emerging from their brood sac (Schroeder & Hermans 1975). By the end ofthe nineteenth century, numerous classic studies ofpolychaete embryology and larval develop­ ment had already been completed (see Schroeder & Hermans 1975 for a compre­ hensive review). Johannes Muller first described the unusual mitraria larva of Owenia from the south of France in 1851 (Wilson 1932). Although he recognized it as a polychaete larva at that time, its specific taxonomic affinity was not under­ stood until Kowalevsky observed metamorphosis around 1867 (Metchnikoff 1871, see Wilson 1932 for complete account). Bivalved veliger larvae brooded in the gills of Ostrea edulis were described by some of the earliest microscopists (Brach 1689, Leeuwenhoek 1722), but I have not been able to discover the earliest references to gastropod veligers. We do know that opisthobranch development had already been described in some detail as early as the 1840's (Nordmann 1846, Schultze 1849), and Forbes (1844b) refers (without giving specific citations) to earlier papers by Sars, Dalyell, Alder and Hancock and Allman to support his contention that molluscs disperse in the plankton. Lacaze-Duthiers (1856-57) reared scaphopod embryos through 35 days oflarvallife and described the trochophore and veliger larvae; the Russian embryologist Kowalevsky (1883) later provided a more detailed description. The double-shelled echinospira larvae were first described by Krohn in 1853. Entoproct larvae were discovered independently in England and France the same year (Reid 1845, Van Beneden 1845). The Muller's larva ofpolyclad turbel­ larians was discovered by Johannes Muller (1850), who also observed its metamorphosis into thejuvenileworm. Gotte (1882) later described a second type of flatworm larva, which was in turn named for him. The first embryological study offlatworms was by Dalyell (1853), who published under the creative title: "The powers of the Creator displayed in the creation, or, observations on life, amidst the various forms of the humbler tribes of animated nature." Phoronids were described as larvae before they were known as adults. Muller (1846, 1847) found large numbers ofactinotrochs at Heligoland, to which he as- LARVAL ECOLOGY OF MARINE INVERTEBRATES 11 signed genus and species names: Actinotrocha branchiata. Adult phoronids were dis­ covered one decade later (Wright 1856), but once again, correct interpretation re­ quired the careful observations ofthe Russian embryologist Kowalevsky (1867b). A comprehensive description of phoronid metamorphosis was presented by Metchnikoff in 1871. The cyphonautes larvae of bryozoans were classified as rotifers (Ehrenberg 1834) until metamorphosis of Electra was observed 35 years after the original description (Schneider 1869). Additional descriptions of cyphonautes were presented by Prouho (1892). Coronate larvae ofascophoran bryozoans apparent­ ly were described first by Barrois (1877) and Vigelius (1886). The larvae ofinarticulate brachiopods were first identified from plankton col" lections twice in the same year, once by McCrady (1860) in North America and once by Fritz Muller (1860), who collected his samples offthe coast ofBrazil. The systematic position of these larvae was inferred correctly from the very begin­ ning. Muller (1861) described the swimming behavior ofthese larvae, noting that they swim vertically because ofthe shell weight. He also observed that larvae clap their shells together and sink when disturbed and that they feed on diatoms. The first larva of an articulate brachiopod was observed and describ,ed at about the same time in France (Lacaze-Duthiers 1861). Rice (1966) has reviewed the events surrounding the discovery of sipunculan larvae. Although larval stages ofSipunculus nudus were described in the middle of the nineteenth century (Mueller 1850, Krohn 1851) by German planktologists, oceanic pelagosphaera larvae remained an enigma for more than another half century. In 1883, Hatchek described much ofthe organogenesis ofS. nudus using material collected from the plankton at Messina. Hacker (1898), while sorting material collected on the great German plankton expedition, first recognized that oceanic pelagosphaeras were in fact larval sipunculans. This did not, however, stop the confusion. A pelagosphaera collected by the Italian research vessel "Liguria" in the South Pacific, was described as a holoplanktonic adult as late as 1905 (Mingazzini 1905), a mistake rectified one year later by Senna (1906) while examining additional material from the same expedition. . Milne-Edwards (1842) and Van Beneden (1847) first observed ascidian tad­ poles. Because they had reared them from eggs, both workers recognized that they were larval ascidians. However, the higher taxonomic status ofascidians was still not understood. At the time, most workers classified ascidians as molluscs. The state ofthis confusion is illustrated well by Forbes in his address to the British Royal Institution made just 2 years after the initial description of tadpoles:

It is not improbable that the form of the larva of a Pteropod, when it shall be known, will be found to be that ofan Ascidian polype, even as the larva of the Tunicata presents us with the representation of a hydroid polyp. (Forbes, 1844, p. 326) 12 CRAIG M. YOUNG

Kowalevsky, who ultimately solved numerous problems of metamorphosis and taxonomic affinity in the animal kingdom, determined on the basis of larval structure that ascidians were chordates in 1867 (Kowalevsky 1867a).

Early ideas in larval ecology Aristotle made the earliest recorded observations ofrecruitment in marine inver­ tebrates when he reported the appearance ofbarnacles on ships and ofoysters on clay amphorae (the fore-runners of ceramic settlement tilesl). Aristotle's in­ terpretations were incorrect, but forgiveable consideringthat larvae would not be discovered for another two millennia. As support for his contention that spon­ taneous generation occurs amongst marine invertebrates and other "bloodless" animals, Aristotle lined up all of the existing observations on recruitment:

That all testacea are formed spontaneously is clear from such facts as these. They come into being on the side ofboats when the frothy mud putrefies. In many places where previously nothing of the kind existed, the so-called limnostrea, a kind of oyster, have come into being when the spot turned muddy through want ofwater; thus when a naval armament cast anchor at Rhodes a number of clay vessels were thrown out into the sea, and after some time, when mud had collected round them, oysters used to be found in them. Here is another proofthat such animals do not emit any generative substance from themselves; when certain Chians carried some live oysters over from Pyrrha in Lesbos and placed them in narrow straits of the sea where tides clash, they became no more numerous as time passed, but in­ creased greatly in size. (De Generatione Animalium, 763a, lines 24 ff. in Aristotle, [1965])

In modern times, the patternAristotle observed (site-specific differences in settle­ ment rates correlated with wave energy) would probably be interpreted in terms oflarval abundances. Aristotle also noted seasonal changes in gonads of oysters (De Generatione Animalium 763a, 763b) and lunar cycles of sea urchin reproduction:

For no testacea can abide extremes oftemperature, and they are therefore in evil plight in seasons ofgreat cold and heat. This is clearly shown by what occurs in the case of sea urchins. For although the ova are to be found in these animals even directly they are born, yet they acquire a greater size than usual at the time ofthe full moon; not, as some think, because sea ur­ chins eat more at that season, but because the nights are then warmer, ow­ ingto the moonlight. (De Partibus Animalium 660a, lines 25 ff. in Aristotle, [1965]) LARVAL ECOLOGY OF MARINE INVERTEBRATES 13

Even though he referred to the gonads as ova, Aristotle stated emphatically that they were only fat-like indicators of condition, not reproductive organs; to his mind, even gametogenic and spawning cycles pointed to spontaneous genera­ tion. Duringthe nineteenth century, when systematists were interpretingphylogeny on the basis ofembryogenesis, early oceanographers were beginning to consider aspects of animal distribution and abundance in the sea. Foremost among these was Edward Forbes, who began sampling the bottom communities by dredge be­ fore 1839 (Murray & Hjort 1912). In one study, reported in 1840, he monitored the animals on a shell bank near the Isle of Man for 7 years, during which time he noted the unexpected arrival of molluscs that had not previously been there (Forbes 1844b). The same year he published his oft-cited erroneous hypothesis that the deep sea is azoic (Forbes 1844a, see Hedgpeth 1957), Forbes concluded that the unexpected immigration of molluscs could only be explained by larval recruitment (Forbes 1844b). In the same lecture, he cites the earlier discovery of veliger larvae by Dalyell, Sars, Alder and Hancock and Allman to support his idea that subtidal zonation is maintained by larval migration followed by differential post-settlement mortality:

Ifthey [i.e., the larvae] reach the region and ground, of which the perfect animal is a member, then they develope and flourish; but if the period of their development arrives before they have reached their destination, they perish, and their fragile shells sink into the depths ofthe sea. Were it not for the law which permits ofthe development ofthese larvae only in the region of which the adult is a true native, the zones ofdepth would long ago have been confounded with each other, and the very existence of the zones of depth is the strongest proof of the existence of the law. (Forbes 1844b, pp. 326-327)

Ignoring the tautological argument in the final sentence, we find here the germs ofthree important ecological concepts: 1) that larvae are wasted if they fail to lo­ cate the adult habitat (see Thorson 1950 for a restatement of the same idea), 2) that animal distribution may be limited by the physiological tolerances of their larvae and 3) that larval development proceeds according to a fixed timetable. The third assumption (determinate larval development) prevailed in the litera­ ture until delay of metamorphosis was discovered in the 1920's. A few of J. Vaughn Thompson's writings on problems of systematics and descriptive morphology contain ecological ideas about larvae. For example, he entertained (then rejected) the hypothesis that distributional differences between goose barnacles and acorn barnacles might result from differences in egg buoyan­ cy. Upon discovering that barnacle larvae possess an eye, he adopted the alterna­ tive hypothesis, namely that larvae select settlement sites actively: 14 CRAIG M. YOUNG

...in the first state of these animals they not only possess perfect freedom and power ofmotion, but organs of sight which furnish them with the me­ ans ofmaking that election which is best suited to their respective habits as impressed upon them by Omnipotence, and members calculated to anchor them securely to the chosen spot! how otherwise shouldwe find the Coronu­ la and Tubicinella exclusively on the backs ofthe Whale tribe, the Chenolo­ bia on the shells of Turtle, and Acasta as invariably imbedded in Sponge? (Thompson 1830, p. 71)

The idea that behavior ofmarine animals can influence their distribution should therefore be attributed to Thompson, not to microbiologists near the end ofthe nineteenth century, as has been suggested in a recent review (Meadows & Camp­ bell 1972a). AlthoughThompson's ideas abouthabitat selection have never, to my knowledge, been attributed to him in the recentliterature, such ideas form the ba­ sis for a great body ofbehavioral work on barnacle larvae beginning with the dis­ covery of gregarious settlement 40 years ago (Knight-Jones & Stevenson 1950, Knight-jones 1953a) and continuing to the present day (reviewed by Crisp 1974, 1976, 1984, Lewis 1978). Recent authors (e.g., Knight-jones & Stevenson 1950, Crisp 1976) have hypothesized that aggregation is necessary in barnacles in order to facilitate copulation. Thompson (1830, p. 80) also appears to have noted that the penis ("...the tubular organ which terminates the body above...") was long enough to reach among individuals in a typical cluster ofbarnacles. Some of the rare ecological observations that crept into nineteenth century papers on embryology appear to have been quite incorrect. One interesting ex­ ample is part of the elegant description of starfish development published by Alexander Agassiz in 1877. In the only field observation included in his mono­ graph, Agassiz infers something about larval feeding:

These larvae are found floating in large numbers at night near the surface, among cast-offskins ofbarnacles, which furnish them with food during the time when they swim freely about, in company with multitudes of small Crustacea, Annelids, and H ydroids. They seem to be nocturnal, as I have only found here and there single specimens when fishing for them under ex­ actly the same circumstances oftide and wind during the daytime. (Agassiz 1877, pp. 28-29)

To his credit, Agassiz described accurately the movements, ciliary fields, and orientation of larvae in vitro. He also noted that echinoderm larvae generally orient with the anterior end up, an observation that has been rediscovered many times (Runnstrorn 1918, Lyon 1906, Pennington & Emlet 1986, reviewed by Young & Chia 1987) and which may have important implications for the distribu­ tion of larvae. •

LARVAL ECOLOGY OF MARINE INVERTEBRATES 15

From the earliest days, aquaculturists have recognized the importance oflarval stages in determining seed set, standing stock, and yield ofadult shellfish. Conse­ quently, the larvae ofoysters and crabs have always received much attention. In Germany, Karl Mobius (1877), in a treatise on oyster propagation, estimated fecundity ofoysters by weighing gonads and counting subsamples ofegg suspen­ sions. Extrapolating these figures to the entire population ("during the breeding season there are upon our oyster-beds at least 2,200,000,000,000 young oysters") he became convinced that larval supply could not limit distribution ofadults and proposed as an alternative that larvae settling passively on areas of shifting sand or heavy sedimentation are eliminated in the early benthic stage. Several important ideas often attributed to Gunnar Thorson's (1946, 1950, 1964, 1966) major review articles were suggested in a letter dated 1890 from a gen­ tleman oyster farmer, Lord Montagu ofBeaulieu (Montagu 1890). With respect to larval mortality, he wrote: There is no doubt that an oyster must have innumerable enemies. When it is an established fact that one oyster will emit a million little eggs or spat, it is clear that if it were not for the wholesale destruction the stock of oysters would be always abundant, but it is not so. After maturing... the oysters are devoured wholesale by crabs, & c.; but what destroys them almost at their birth? This is the most important question. Montagu's premise that larval mortality ("wastage" in the terminology ofThor­ son) is critical in understanding high invertebrate fecundity was also the founda­ tion for Thorson's (1950) treatment of developmental patterns, fecundity and mortality more than a halfcentury later. Likewise, Montagu (1890) made in vitro observations under natural light conditions that foreshadowed generations of work on photoresponses and vertical migration of bivalve and other larvae (reviewed by Thorson 1964, Young & Chia 1987). In this regard, Montagu made the following empirical observations: I believe it is true that spat rises to the surface in the day and falls to the bot­ tom at night. I have tried this by experiments in large bottles, and there is no doubt that it did fall to the bottom in the dark, and rose to the surface with great activity on being brought out in the light. However, Montagu's concept ofrandom settlement ("When spat is really mature it will adhere to anything") had to be discarded with the later discovery ofgregari­ ous settlement (Cole & Knight-jones 1939) and delay of metamorphosis (Maz­ zarelli 1922) in oysters. Quantitative sampling of plankton was pioneered by Victor Hensen, a col­ league of Mobius at Kiel. In 1889, Hensen obtained major funding from the government ofGermany for a 93-day plankton expedition that sampled much of the Atlantic Ocean along a large circular track (Haeckel1883). Hensen's quan- 16 CRAIG M. YOUNG titative approach to plankton sampling and his conclusion that plankton are ui­ formly distributed were strongly criticized by Haeckel (1883, debate summarized by Harbison 1983). Nevertheless, the resulting series ofmonographs (e.g., Hack­ er 1898, Mortensen 1898), published over the following 20 years, include descrip­ tions of numerous larvae from the open ocean. Oceanic larvae were problematic for some of the early biologists, partly be­ cause they were found so far from shore. Although the potential role of such lar­ vae in transatlantic dispersal was suggested early on, it was only demonstrated convincingly about 20 years ago by RudolfScheltema (Fig. 9-D) ofWoods Hole (Scheltema 1966, 1968, 1971). In his 1876 book on biogeography, Alfred Russel Wallace commented on the dispersal potential of molluscan larvae: The univalve and bivalve mollusca, ofwhich the whelk and the cockle may be taken as types, move so slowly in their adult state, that we should expect them to have an exceedingly limited distribution; but the young ofall these are free-swimming embryos, and they thus have a powerful means of dis­ persal, and are carried by tides and currents so as ultimately to spread over every shore and shoal that offers conditions favourable for their develop­ ment. (Wallace 1876, p. 30) Some ofthe large teleplanic veligers found in theopen sea were initially assumed to be pteropod-like adult gastropods. John Denis MacDonald first refuted this idea in 1858. While serving as assistant surgeon on a surveying ship in the South­ western Pacific, he noted that many oceanic gastropods had similar features, in­ cluding large velar lobes and lipid globules in the digestive gland. Such features were interpreted much later by Scheltema (1971) as common adaptations for a long pelagic existence. MacDonald correctly stated that most of the open ocean gastropods were in fact larval forms. Some long-lived planktonic veligers have a double notch in the lip margin to accommodate large velar lobes. We now know that this character is common to the veligers ofmany gastropod families. In the nineteenth century, however, such sinusigerous larvae were initially placed in a single genus, Sinusigera, and regarded as holoplanktonic adult mol­ luscs. Craven (1883) recognized this error when he came into possession ofsome metamorphosed snails that still had intact protoconchs. Craven (1883) also ap­ pears to have been the first to hint that larvae could prolong their existence in the absence ofa suitable settlement site, but he had no empirical data to support the idea. In 1885, W. J. Sollas, professor ofgeology and mineralogy at the University of Dublin, pointed out that the presence of a pelagic larval stage was one of the major differences between freshwater and marine invertebrates and proposed that freshwater diversity is relatively low because larvae cannot be retained in flowing streams. He also speculated on the advantages of lecithotrophy and parental protection of embryos: LARVAL ECOLOGY OF MARINE INVERTEBRATES 17

...it [the larva] is spared the drudgery ofworking for its own existence, and is supplied with nutriment in a form that makes the least demands on its digestive powers, a larger balance remains available for metamorphic changes. (Sollas 1885) The end of the nineteenth century saw two advances in plankton sampling methods which were to have an important impact on larval ecology. The first was invention of a closing net, which Haeckel (1883) credits to two officers of the Italian navy, G. Palumbo and Gaetano Chierchia. The use ofcontinuously open nets on the Challenger expedition had been subject to criticism (Haeckel 1883). The secondwas an increased use ofpumps for sampling plankton. Pumps ofvari­ ous kinds were used by Herdman, Murray, and Garstang (Wheeler 1968). Gar­ stang's ingenious sampling method consisted offastening a net to the ship's bath faucets (Wheeler 1968). Ernst Haeckel's (Fig. 6-B) interest in plankton began under the tutelage ofJo­ hannes Muller in 1854. After making important contributions to the biology of radiolarians and other plankton organisms, he was appointed Professor ofZoolo­ gy at Jena in 1862 (Gross 1985). Although most of Haeckel's contributions in plankton research dealt with gelatinous zooplankton (medusae and siphono­ phores) and radiolarians, his biogenetic law ("ontogeny recapitulates phyloge­ ny"), which he expounded in a series of papers and books (e.g., Haeckel 1866), stimulated larval studies ofall kinds. Although Haeckel was primarily a morphol­ ogist, he coined and defined the word "ecology" as well as numerous other terms that remain part of modern marine biological jargon (Hedgpeth 1957).

1900-1930: EMBRYOS AND OYSTERS By the turn of the century, recapitulationism was hailed by many as a major unifying theory for biology. MacBride (1914), a prominent embryologist and out­ spoken proponent of the doctrine expressed the optimistic view that this "law" would ultimately allow us to "sketch the main history oflife on the earth". Gould (1977) and Moore (1987) have elaborated on the history and controversies as­ sociated with recapitulation theories; Gould's (1977) arguments on various kinds ofdevelopmental heterochrony extend far beyond this briefhistory. From an eco­ logical standpoint, perhaps the most significant contribution that arose from the recapitulation debate was a recognition that larval forms are subject to natural selection in their own right and are not just transient stages that mirror the phylogenetic history of a species. Walter Garstang (Fig. 8-F; see obituary by Hardy 1951) made this point eloquently in his much-cited presidential address to the British Association for the Advancement of Science (Garstang 1929) and in his famous book ofpoems (Garstang 1985), published two years after his death. Garstang's molluscan examples of larval adaptation remain for the most part convincing, even though one recent study challenges his torsion hypothesis with 18 CRAIG M. YOUNG good data on vulnerability to predators (Pennington & Chia 1985). However, many of Garstang's ideas had been bantered about by both anti-recapitula­ tionists and recapitulationists (who recognized "secondary" larval adaptations that tended to obscure the historical patterns) for decades prior to Garstang's (1922, 1929) renouncements of Haeckel's law. As early as 1894, McBride's men­ tor, Adam Sedgwick, argued that larval features, whether or not they recapitulate phylogeny, represent adaptations to either present or past larval environments and to the larval mode oflife. Moreover, both Weldon (1889) and Gurney (1902) investigated experimentally the adaptive functions oflarval structures (carapace spines in crustacean zoeae) around the turn of the century. Duringthe 30-year period from 1923 to 1953, about 60 larval papers, including nearly one-third (19/61) ofall larval papers published inJMBAUK were authored by one ofWalter Garstang's early protegees, Marie Lebour (Fig. 8-E; see obitu­ ary by Russell 1972, for complete listing of Lebour's papers). Working at Plymouth first as a research associate then as a full-fledged researcher, Lebour produced baseline data which provide important insights into larval taxonomy, feeding, predator-prey interactions, morphology, and behavior. Although most of her larval contributions were made with larval crabs and snails, she also showed that larvae can be important foods for herringlarvae and other fishes. Le­ bour perfected the use ofthe "plungerjar" as an effective means ofrearinglarvae to metamorphosis (Lebour 1933, Hardy 1972). From a practical standpoint, larvae could not be studied by ecologists until they had been described and until methods had been developed for rearing them in the laboratory. Consequently, many important contributions were made by embryologists and systematists. Comparative embryology reached its zenith at Marine Biological Laboratories, Woods Hole in the first two decades ofthe twen­ tieth century (see historical reviews by Lillie 1944, Monroy & Groeben 1985, Gross 1985). With their classic studies ofcelllineage, E. B. Wilson, E. G. Conklin (Fig. 6-E), C. M. Child, C. 0. Whitman and numerous others established a tradi­ tion that persists at MBL to the present day. Historical aspects ofthe cell lineage period at MBL have been covered exhaustively in recent reviews (Lillie 1944, Gross 1985). After several generations of embryologists had developed larval rearing techniques, these methods were compiled in a handbook (Costello & Henley 1971) which has been of great value to larval ecologists. Mass culture techniques developed in fisheries and aquaculture laboratories also madelarvae available for ecological studies. More importantly, however, oys­ ter aquaculturists did some of the best field studies of larval ecology during the

-Fig. 6. Larval biologists in the nineteenth and early twentieth century. A: Johannes Muller. B: Ernst Haeckel. C: S.o. Mast at Marine Biological Laboratories (Woods Hole) in 1924 (photo: MBL archives). D:Jacques Loeb. E: E. G. Conklin at M.B.L. in 1935 (photo by Ruth Turner, Har­ vard University). F: Caswell Grave at M.B.L. in 1926 (photo: MBL archives). -

LARVAL ECOLOGY OF MARINE INVERTEBRATES 19 20 CRAIG M. YOUNG

first half of the century. The early oyster studies by Mobius and Montagu have already been mentioned. In North America, oyster culture was pioneered by Julius Nelson (Fig. 7-A, B) working at the NewJersey Agricultural Experiment Station (now Rutgers University Shellfish Laboratory) between 1888 and his death in 1916. Beginning in 1909, much of this work was done on a houseboat laboratory that could be moved among estuarine study sites (Fig. 7-D; Hal Haskin, pers. comm.). Carriker (1988) has given an interesting account of these early efforts. According to Carriker (1988), plankton netting was not available in NewJersey at the time these studies began. Initially, therefore, samples oflarvae were taken by dipping water from the estuary in glass vessels and filtering them through paper funnels. An early photograph (Fig. 7-B) showsJulius Nelson seek­ ing larvae in the field with a microscope. His efforts resulted in the first studies of larval migrations and abundance patterns. Thurlow Nelson (Fig. 7-C), son of Julius, continued the work started by his father by considering factors that limit recruitment of oysters and mussels. During Thurlow's lifetime, technology progressed from the filter paper technique mentioned above through plankton nets to plankton pumps. The latter were used for studies oflarval distribution as early as the 1920's (Nelson 1928). One ofThurlow Nelson's classic studies implicated the ctenophore Mnemiopsis as a predator on oyster larvae (Nelson 1925). After documenting the presence of large numbers of oysterlarvae in ctenophore guts, Nelson compared larval abun­ dances and recruitment levels in adjacent bays differing naturally in density of ctenophores. This clever approach, which produced interesting results, may be regarded as an early "natural experiment". If Nelson were alive to submit this paper today, he would probably encounter trouble with reviewers over issues of confounding covariates and pseudoreplication. However, it is undeniable that Nelson was well ahead ofhis time (see Thorson 1950, Roughgarden et al. 1988, Olson & McPherson 1987 for recent papers with similar conclusions) by recog­ nizing the importance ofpelagic mortality as a determinant of recruitment densi­ ty. Thurlow Nelson (1924) also made careful observations on settlement and pre­ settlement behavior of bivalve larvae which will be discussed later. The tradition of research on bivalve larvae continued in North America at several locations besides New Jersey, notably the U. S. Bureau of Fisheries Laboratory at Milford, Connecticut. Beginning in the 1920's, Paul Galtsoff(Fig.

---+ Fig. 7. Biology of shellfish larvae in North America. A: Julius Nelson in his New Jersey oyster laboratory near Tuckerton, NewJersey, about 1906 (photos A-D courtesy of Hal Haskin, Rutgers University). B:Julius Nelson examining bivalve larvae in the field about 1906. C: Thurlow Nelson with plankton pump in the 1930's. D: The houseboat laboratory "Cynthia" constructed in 1909 and used by the Nelsons and subsequent oyster larval biologists until about 20 years ago. E: Paul GaItsoff at M.B.L. in the 1920's (M.B.L. archives). F: Victor Loosanoff spawning oysters at Mil­ ford, probably in the 1950's (photo courtesy ofJames E. Hanks, Milford Laboratory, National Ma- rine Fisheries Service). LARVAL ECOLOGY OF MARINE INVERTEBRATES 21

A

D 22 CRAIG M. YOUNG

7-E) and Herbert Prytherch initiated extensive studies on the distribution and ecology ofoysterlarvae in Long Island Sound. These studies included the deploy­ ment ofhundreds of drift tubes to predict where larvae might travel (Prytherch 1929). This and similar Lagrangian techniques have gained renewed interest with the current widespread interest in the interactions between physical oceanography and recruitment (reviewed by Levin 1990). Duringthe same periodwhen the Nelsons were studyingoysterlarvae in North America, the Italian zoologist Giuseppe Mazzarelli was observing in vitro larval behavior of Ostrea edulis and other molluscs near Naples (Mazzarelli 1922). He was one of the first to note that convection currents may cause mass migrations of larvae under laboratory conditions, an artifact that has plagued numerous such studies. He contrasted the behavior of photopositive and geonegative opisthobranch larvae ("...si tengono abitualmente verso la superficie e verso la luce...") with completely random swimming of oyster larvae: Regardless ofwhether the vessel is held in darkness or in full light, or with only one side being hit by light rays, the rest being in darkness, the oyster larvae always continue to wander throughout the entire water mass, in which they continue to distribute themselves in an entirely uniform man­ ner. (Translated from Mazzarelli 1922, p. 155) In a recent review, D. J. Crisp (1984, p. 104) stated, "By far the most important influence on the progress of larval biology since pre-war days was the discovery of delayed metamorphosis". This important discovery has often been attributed jointly to Theodor Mortensen (1921) ofthe Copenhagen Zoological Museum and Douglas P. Wilson (1932) of Plymouth (Wilson 1952, Crisp 1984). However, as Wilson (Fig. 8-A) himself recognized (Wilson 1952), his discovery was fore­ shadowed not only by that of Mortensen (Fig. 8-C), but also by earlier observa­ tions by Thurlow Nelson (1924). Indeed, Nelson (Fig. 7-C) presented clear evi­ dence for larval searching behavior and cited circumstantial evidence from even earlier papers (e.g., Sigerfoos 1908) to support his contention that selection oc­ curs. He dismissed the notion that larvae settle passively when their shells be­ come too heavy with his observation ofa pediveliger search pattern that involves alternate swimming and crawling (Nelson 1928). He also documented territorial behavior ("spacing out"), rediscovered by Crisp (1961) for barnacles and Knight­ Jones (1951) for serpulids. Nelson interpreted spacing behavior as a mechanism for reducing intraspecific competition amongst juveniles.

-4 Fig. 8. Some pioneeringlarval biologists in Europe. A: Douglas P. Wilson at his home in Plymouth in 1988 (photo by Pamela Blades-Eckelbarger, Harbor Branch Oceanographic Institution). B: E. W. Knight-]ones at Swansea in 1988 (photo by C. M. Young). C: Theodor Mortensen (by permis­ sion, Zool. Mus. Copenhagen). D: Dennis]. Crisp (photo courtesy of Mary Crisp). E: Marie Le­ bour (by permission,]. Mar. BioI. Assoc. u.K.). F: Walter Garstang (by permission,]. Mar. BioI. Assoc. u.x.j, •

LARVAL ECOLOGY OF MARINE INVERTEBRATES 23 24 CRAIG M. YOUNG

Mortensen's (1921) discovery that several kinds of sea urchin larvae delayed metamorphosis until natural sediments were provided was a minor peripheral observation made during his distinguished work on adult taxonomy and larval morphology, but Wilson's discovery that polychaetes (specifically Ophelia bicornis) choose optimal substrata paved the way for another halfcentury ofmore detailed studies by Wilson himselfand provided impetus for a large school ofBritish wor­ kers to work on the physiology, behavior, and ecology ofsubstratum selection for many decades. The impact ofWilson's work is undeniable; nevertheless, his credit for discov­ ery of delayed metamorphosis is rightly shared with not only Mortensen (1921) but also with the Italian biologist Guiseppe Mazzarelli (1922). The latter clearly described the phenomenon from experiments similar to those of Mortensen (1921), though he published the results one year later. Because his contribution has often been overlooked by reviewers, I include an excerpt from the Italian text (Mazarelli 1922, p. 157):

Al fondo di vetro del vaso le larve si mantengono in vita, con vivaci movimenti, due 0 tre giorni; rna poi muoiono tutte. Se pero sul fondo del vaso stesso si e avuto precedentemente cura di collocare dei corpi solidi a su­ perficie scabra (negli esperimenti sono stati collocati frammenti di tegole e piccoli pezzi di tufo) allora le larve cadute su di essi vi si fissano, e continu­ ano illoro sviluppo, del quale il primo segno e la scomparsa del velo.U

According to Mazzarelli, however, oyster larvae are incapable of a long delay, since they do not approach the bottom until just before the larval shell becomes too heavy to carry. Several biologists working on behavioral ecology oflarvae in the early years of the twentieth century were influenced by the approach ofJacques Loeb (Fig. 6-D), a German physiologist who migrated to the United States at the invitation of Charles Otis Whitman, first director of the Marine Biological Laboratories (Gross 1985). One ofLoeb's major interests was the study ofanimal "tropisms", which he explained in strict mechanistic terms by showinghow behavior could be modified by simple chemical and physical changes in the environment (Loeb 1906). Besides doing behavioral experiments with both adult and larval stages of various marine animals, he also made many important contributions in develop­ mental biology (Gross 1985). The work of Groom & Loeb (1890a, b) on the be­ havior of barnacle nauplii was the first detailed study of larval swimming be-

1) At the bottom of the glass ofthe vase, the larvae remain alive, moving actively for two orthree days; but then all of them die. If, on the other hand, on the bottom of the same dish one has previously arranged solid objects with rough surfaces (in the experiments there were arranged fragments oftile and small pieces oftufa), then larvae falling to the bottom attach themselves to these objects and continue their development, ofwhich the first sign is disappearance ofthe velum. LARVAL ECOLOGY OF MARINE INVERTEBRATES 25 havior. In these papers, it was demonstrated that the sign ofnaupliar phototaxis could be reversed by modifying light intensity and that light in the ultraviolet region of the spectrum is especially effective in causing photopositive nauplii to become photonegative. Using the same species of barnacle larvae at Naples, Wolfgang Ewald (1912) followed Loeb's research with more detailed analyses in which light intensity, temperature, pH, and various chemical treatments were related to phototaxis and the speed oflocomotion. By comparing the survival of larvae in direct sunlight to that oflarvae under clear filters, Ewald (1912) demon­ strated that ultraviolet irradiation causes mortality, thus providing an adaptive explanation for the negative phototaxis observed by Groom & Loeb (1890a, b). In the final paragraph of his results section, Ewald makes the remarkable prediction that larvae should undergo vertical migrations. Such migrations were not documented in the field for many more years. An American scientist ofthe same era, S. O. Mast (Fig. 6-C) of Goucher Col­ lege, Maryland, applied behavioral methods to numerous kinds oflarvae includ­ ing hydrozoan planulae, polychaete setigers (Mast 1911), and ascidian tadpoles (Mast 1921). Mast's work with ascidians remains the only viable explanation of ascidian orientation mechanisms to this day (reveiwed by Svane & Young 1989). While working at Woods Hole, Mast interacted with another summer visitor, Caswell Grave, professor of biology at Washington University in St. Louis. Grave's work, which spanned a 25-year period beginning in 1920, addressed numerous problems of ascidian larval ecology including phototaxis, geotaxis, and induction of metamorphosis (e.g. Grave & Nicoll 1939, see Svane & Young 1989 for a complete review). Grave was a biologist in the broadest sense of the word; his papers are remarkable for their coverage of all aspects of each organ­ ism's biology, from cellular descriptions of sensory organs to experiments on the adaptive and distributional consequences ofbehavior (e.g., Grave & Woodbridge 1924). He was particularly interested in determining how variations in receptor morphology translate into specific behaviors.

1930-1950: LARVAL ECOLOGY EMERGES AS A DISCIPLINE The tradition ofoyster larval biology continued at the Milford Laboratory under direction of Victor Loosanoff (Fig. 7-F) beginning in 1931. Like Galtsoff, Loosanoffhad his academic origins in the Soviet Union (Hanks 1987, R. Turner, pers. comm.). After serving as an officer in the White Army during the Russian Revolution, Loosanoff escaped into China (Hanks 1988). Loosanoff worked on oyster biology for more than 30 years at Milford. It was during this period that he began to accumulate one ofthe most extensive long-term data sets on fluctua­ tions of marine populations: his classic study of oysters and starfish in Long Is­ land Sound (Loosanoff et al. 1955, Loosanoff 1964). These data, together with 26 CRAIG M. YOUNG those for pismo clams in California (Coe & Fitch 1950) and soft-bottom species in the 0resund (Thorson 1950) showed that populations of animals with plank­ tonic larvae can vary chaotically over time, thus providing an importantjustifica­ tion for studies of recruitment biology even now. Mariculturists acknowledge Loosanoff and his group for numerous breakthroughs in bivalve rearing tech­ niques, especially aspects oflarval nutrition and induction ofspawning (reviewed by Loosanoff & Davis 1963). Loosanoff & Davis (1947) recognized early on the importance oftracing larvae in the field (Levin 1990) and recommended the use of vital stains for this purpose. On the Pacific Coast of North America, another major study of oyster larvae was done by Hopkins (1937). Like Loosanoff, Hopkins considered many aspects ofoysterbiology, includingspawning and settlement. Perhaps his most important ecological insights come from an impressive effort to measure correlations be­ tween settlement and various physical factors including tides, current velocity, temperature, salinity and pH. Sampling of spatfall and physical correlates was done on an hourly basis for 48-hour periods. While Loosanoff and others were pushing forward our knowledge of larval ecology with bivalve studies in North America, Pieter Korringa (Fig. 9-E) led the way with similar studies in Europe. His 249 page monograph (which was the pub­ lished version ofhis PhD dissertation), published in 1949, provided an incredibly complete picture ofoyster reproduction and larval biology in the Oosterschelde. Korringa (1949) considered the role ofnumerous physical factors, includinglight, temperature, wind, waves, salinity, and current velocity on both larval distribu­ tion and settlement intensity and conducted field manipulations of settlement surfaces to investigate the role of bottom characteristics on spatfall. Forty years later, we may still look to Korringa's study as one ofa small handful in which lar­ val density was related quantitatively to planktonic mortality and advection. Several important forerunners of modern intertidal ecology published their work in Europe during the decades surrounding 1930 (Moore 1934, Hatton 1938, Coleman 1933, Fischer-Piette 1932, Orton 1929 and others). Several ofthese wor­ kers either expressed opinions about the role oflarvae or provided data on recruit­ ment processes. Coleman's paperhas often been used as a "straw man" by propo­ nents oflarval behavior because he inferred random settlement from the patterns he observed on the shore:

...spores ofalgae and larvae ofbarnacles are free in the sea, and are appar­ ently away from any influence that could affect their subsequent zonation when settled between tide marks. The assumption is made, then, that larvae and spores, given suitable sub­ stratum, settle in a manner entirely at random in respect to tide levels. The further assumption is made, that a barnacle, or an alga, once settled, never moves agam. •

LARVAL ECOLOGY OF MARINE INVERTEBRATES 27

That the settling ofa barnacle larva must in some cases be practically in­ stantaneous, and final, and not a matter of 'deliberation' or 'choice,' is shown by those individuals of Chthamalusstellatus which are found above a predicted level of Extreme High Water Springs. These barnacles can only have settled in rough weather, when the seas were raising the splash zone. Zonation in the algae and barnacles, then, is the result of a hit-or-miss method. Ifa spore or larva settles within the environment which will suit it as an adult, it may survive. Ifit settles outside this range, it will sooner or later die without maturing. (Coleman 1933, p. 472)

Ironically, this carefully worded passage, often cited because ofits apparent dis­ regard for habitat selection, deals only with the issue of zonation, not other aspects of animal distribution (e.g., small-scale aggregation) known to be in­ fluenced by behavior. Indeed, later work by Hatton (1938) and Connell (1961) with the same species ofbarnacles bore out Coleman's accurate fielel observation that larvae settle both inside and outside the zone occupied by the adults and that the latter zone is established largely by differential post-settlement mortality. Hatton's (1938) paper on the distribution ofintertidal plants and animals at Saint Malo must be regarded as the most important forerunner of intertidal "supply­ side" ecology. In this work, which deals with two species ofbarnacles, a limpet, and three species of algae, Hatton addressed not only the problem of zonation, but also physical and biological factors (e.g., waves, water currents, exposure, substratum type, substratum orientation) that determined horizonal patterns of recruitment and mortality. Recognizing that early mortality could confound in­ terpretations of settlement pattern, he was careful to begin his cohort survivor­ ship curves with newly settled cyprids rather than metamorphosed juveniles. He demonstrated that 5 sites maintained approximately the same rank order of set­ tlement densities for three years and correlated this pattern with water move­ ments. He also discovered major settlement differences among various kinds of rocks. Similar studies have been done recently, also with barnacles, by Caffey (1982) in Australia and Raimondi (1988) in Mexico. With the exception of Wilson's ongoing work with polychaetes and Grave's papers on ascidian larvae, laboratory studies on larval behavior were relatively scarce during the 1930's and early 1940's. The two papers most often cited are by Jagersten (1940) on settlement of Protodrilus larvae and by Cole & Knight:Jones (1939) on settlement ofoysters. An interesting paper that is often overlooked was by Pierre Garbarini (1936), who worked at Roscoffon the settlement behavior of spirorbid polychaetes. He contrasted the substratum choices ofSpirorbis borealis, a species that lives primarily on fucoid algae with that ofS. pagenstecheri, a species that occupies ascidians and other substrata. Besides demonstrating that the be­ haviors oflarvae correspond to the distributions of adults, Garbarini (1936) also made observations on photoresponses. His observations were verified and quan- f

28 CRAIG M. YOUNG tified years later by Gross & Knight:Jones (1957), DeSilva (1962), Stebbings (1972) and Williams (1964). Grosberg's (1981) recent discovery that larvae of several species of solitary organisms, including Spirorbis borealis, avoid settling near the colonial ascidian Botryllus schlosseri was actually a rediscovery of the phenomenon first described by Garbarini (1936)nearly a half century earlier:

Si un Botrylle est fixe sur une fronde de Fucus, les larves de Spirorbis borealis ne se fixent ni sur le Botrylle, ni a son voisinage imrnediat; mais aquelque distance, et partout ailleurs, le Fucus se couvre de jeunes Spirorbes, comme a l'ordinaire. (Garbarini, 1936, p. 160)1)

Investigations of the recruitment of fouling organisms began early in North America with the deployment of "test panels" by William F. Clapp (Clench 1953), but true experimental studies peaked both in the United States and Great Britain around the time ofWorld War II. During the very period that non-ran­ dom settlement behavior was first being discovered in the laboratory (Mortensen 1921, Wilson 1932, Nelson 1924, Mazzarelli 1922), controlled experiments documented patterns consistent with the idea of larval behavior in the field. These early field experiments, which are seldom cited in the modern ecological literature, involved carefully thought-out manipulations of settlement surfaces. One ofthe largest ofthese studies was by Paul Visscher (1928a), who maintained that light was a major factor determining the extent offouling. Besides deploying panels of various colors for recruitment comparisons, Visscher studied the be­ havior ofcyprid larvae in the laboratory (Visscher 1928b, Visscher & Luce 1928). One ofhis many contributions was a careful description ofsearching behavior in barnacle larvae:

When the internal physiological conditions necessary for attachment are present, apparently correlated with the 'lipoid' content ofthe organism, the larvae have been observed, on many occasions, to 'walk' on the substratum, apparently hunting for a place for attachment. This remarkable perfor­ mance is accomplished by alternate attachment and release ofthe adhesive tips of the antennae... In this manner these organisms have been observed to 'walk' for considerable distances, and to 'test' various areas for a period of more than an hour before finally attaching. (Visscher 1928a)

Recognizing that many ofthe early fouling studies (including his own) had been plagued with confounded variables (e.g., paint toxicity confounded with color; color confounded with surface reflectance), Visscher was careful to design field

1) Ifa Botryllus is attached to the blade of Fucus, the larvae ofSpirorbisborealis attach themselves neither to the Botryllus nor its immediate vicinity; but at some distance, and everywhere else, the Fucus is covered with young Spirorbids, as usual. o <

LARVAL ECOLOGY OF MARINE INVERTEBRATES 29

experiments without artifacts. Although Visscher concentrated his work on the effects oflight, other workers during the same era explored interactive effects of numerous factors influencing settlement. A case in point is the study ofPomerat & Reiner (1942). These workers examined the settlement ofvarious bryozoan and barnacle species on opaque, translucent and transparent plates held at various angles in relation to the horizontal. They recognized that short-term experiments were necessary in order to document settlement processes because of the effects of post-settlement mortality. Modern ecologists have emphasized this point repeatedly; surprisingly, however, they generally attribute the idea to Keough & Downes (1982) rather than Hatton (1938), Pomerat & Reiner (1942) and several others who discussed it decades earlier. The clever method of comparing settle­ ment on opaque and transparent plates has been used by numerous workers (e.g., Hopkins 1937, Cole & Knight-]ones (1939). Weiss (1947) studied patterns ofset­ tlement by counting newly-settled cyprids at ll-h or 2-h intervals. These data were used for analyzing day/night differences and vertical distribution ofsettlers (see Grosberg 1982 for a similar experiment in the recent literature). One ofthe most interesting results was that normal diel patterns of settlement could be eliminated by illuminating the plates at night. The experimental approaches used initially in fouling studies have played a major, but often unacknowledged role in marine recruitment ecology. Although the initial work had mostly eco­ nomic goals, use offouling panels has proliferated in recent years as a method of exploring the recruitment processes on natural substrata. Good examples ofsuch studies are those of Dybern (1965) who deployed enormous panels at various orientations to study ascidian settlement in a Swedish fjord and the subtidal recruitment work of Osman (1977) and Keough (1983). Gunnar Thorson (Fig. 9-A) is best known for his thoughtful review articles, which touched upon virtually all questions that have been addressed by larval ecologists since and have provided guidance and inspiration for several genera­ tions of graduate students seeking thesis topics. Although Thorson was able to bring an amazing command of the literature to bear on the problems he ad­ dressed, his works are insightful largely because Thorson began as an empiricist; he understood larvae because he spent so many years sampling them from the plankton. As a graduate student, Thorson had the opportunity of participating in a 3-year(1931-34) expedition that investigated the hydrography and marine bi­ ology of a large fjord system in East Greenland (Thorson 1934, 1935, 1936). Recognizing the importance ofobtaining samples throughout the year, he over­ wintered in 1931-32, and with only the help of an Eskimo assistant (K. Ockel­ mann, pers. comm.), sampled plankton and benthos through the ice. Thorson (1936) described the logistics ofwhat must have been a very difficult thesis project:

During the winter these samples were taken in a shed built on the ice for this purpose. Through a hole in the ice floor, and by a special heating of the 30 CRAIG M. YOUNG

shed the plankton samples were placed in glass tubes without freezing, so that a countingofthe contents could take place on livingmaterial. (Thorson 1936, p. 17) Thorson also took horizontal tows and collected bottom samples by stringing a sy­ stem ofunderwater wires before the water froze (K. Ockelmann, pers. comm.). These data provided the basis for his well known rule that relates mode of de­ velopment to latitude and depth (Thorson 1946, 1950). Upon returning to Den­ mark, Thorson initiated a long-term study on the larval development of all spe­ cies in the 0resund (Thorson 1946). Much of this work was done in a small laboratory near his summer home on Ven Island, which lies in the middle ofthe 0resund, south of Helsingor (Fig. 9-B). Thorson pioneered the use of several in situ methods that only came into widespread use after his death. For example, he introduced "larval traps", which were essentially moored midwater sedimenttraps into whichlarvae settled, either actively or passively. Similar techniques have recently been used to quantify the passive component ofthe settlement process (Hannan 1984, Butman 1987), and containers of defaunated sediment are often deployed to study habitat selection or recruitment rates in soft sediment systems ranging from the intertidal zone to the deep sea. Thorson also attempted to rear larvae in the field for studies ofgrowth and de­ velopment. His apparatus, which was constructed of medicine bottles and silk bolting cloth, failed to produce any interesting data in the stratified waters ofthe 0resund, but Thorson expressed the strong opinion that it would work in isoha­ line waters where the larvae would not have to be lowered through a low salinity layer en route to their incubation depth. As Thorson predicted, larval rearing chambers have now been used in the field for studies of substratum selection (Young & Chia 1982), photoresponse (Young 1982, Olson & McPherson 1987), vertical migration (Pennington & Emlet 1986), juvenile population dynamics (Sebens 1982), feeding and growth (Olson 1985b, 1987, Olson et al. 1987), and developmental rates (Young & Cameron 1989). In situ rearing techniques, con­ ceived by Thorson but unworkable in his hands, hold much promise as methods from which good field inferences can be made.

--+ Fig. 9. Larval ecologists. A: Gunnar Thorson during a visit to Harvard in 1953 (photo by Ruth Turner, Harvard University). B: Thorson's laboratory near his summer home on Ven Island in 1969. This is where he wrote most of his 1946 monograph (photo by Ruth Turner, Harvard Univer­ sity). C: MartinJohnson sampling larvae aboard the R/V Scripps, August 1, 1935 (photo by Eu­ gene LaFond, courtesy of Deborah Day, Scripps Institution of Oceanography archives, University ofCalifornia, San Diego). D: Simeone Mileikovsky (left) and RudolfScheltema in Moscow in the 1960's (photo courtesy ofRudy Scheltema). E: Pieter Korringa at the F.AD. aquaculture meeting in KyotoJapan, 1976 (photo by permission, Marine Ecology Progress Series). F: Robert L. Fernald at Friday Harbor in 1982 (Photo by Ruth Illg). LARVAL ECOLOGY OF MARINE INVERTEBRATES 31 32 CRAIG M. YOUNG

In 1937,]. H. Orton published a small but important paper in which he pro­ posed that high densities of bivalves and other organisms occur where eddies and other hydrographic features concentrate larvae. In North America, oceanographers at Scripps Institution ofOceanography in California also consi­ dered how currents and other offshore physical phenomena might affect the dy­ namics ofpopulations on the shore. In the late 1930's MartinJohnson (Fig. 9-C) began studying the larvae in plankton samples, ostensibly as a means to trace water currents Gohnson 1939). He reasoned that by samplinglarvae ofan animal with a restricted, known distribution, one could learn much about the circulation patterns and mixing of coastal water masses. His first works on crustacean larvae (johnson 1939) were followed by several general papers on problems ofplankton ecology (e.g., Johnson 1949, 1954). In his later years, Johnson turned his atten­ tion once again to the distribution oflarvallobsters (johnson 1960, 1971)through­ out the Pacific Ocean. Johnson's early papers were among the first to highlight the importance oflarge oceanographic features in larval loss and return oflarvae to the shore, which are themes that have dominated thinking by marine ecologists in recent years (Shanks 1983, Roughgarden et al. 1985, Gaines & Roughgarden 1985, Ebert & Russell 1988). Likewise, Johnson's extensive sampling of lobster larvae provided a pattern for more recent studies ofthe ecology oflarvallobsters in Australia and elsewhere (reviewed by Phillips & Sastry 1980). Wesley R. Coe, also at Scripps, monitored populations of various bivalves up and down the California coast for many years. He noted that such populations often fluctuate wildly and that "resurgent populations" sometimes appear where only low numbers were found previously (Coe 1953). Although he did not pro­ vide data on currents or larvae, Coe (1953, 1956) used "supply-side" arguments and invoked mesoscale oceanographic processes to explain the population phenomena he observed. At about the same time, Bousfield (1955) published his classic paper that explains estuarine populations of barnacles in terms of reten­ tion processes and water circulation. A more detailed study ofbarnacle larval dis­ tribution as it relates to settlement was later conducted by De Wolf (1973) in the Dutch Wadden Sea.

1950-1970: THE GOLDEN AGE OF SETTLEMENT BEHAVIOR The British school oflarvalbiology peaked during the 1950's and 1960's underthe influence ofD. P. Wilson (Fig. 8-A), D.]. Crisp (Fig. 8-C), E. W. Knight-jones (Fig. 8-B), B. Bayne,]. Ryland and others. The majority ofpapers written during this era commented on the role ofbehavior in controlling distribution and abun­ dance patterns, though very few ofthe papers used quantitative methods to docu­ ment the field patterns they attempted to explain (see Crisp, 1961 for a notable ex­ ception). Behavioral phenomena to which patterns were attributed included gregarious settlement (Knight-Jones 1951, 1953a, Knight-Jones & Stevenson •

LARVAL ECOLOGY OF MARINE INVERTEBRATES 33

1950, Bayne 1969, and others), delay of settlement (Wilson 1952), selection of microbial films (e.g., Crisp & Ryland 1960, DeSilva 1962), selection of specific sediments or other substrata (e.g., Wilson 1954, Thompson 1958, Ryland 1959, Crisp & Williams 1960), decreased discrimination with larval age (Knight-jones 1953b), rugophilia (Ryland 1959), photoresponses (reviewed by Thorson 1964), and territorial behavior (Knight:Jones 1951, Wisely 1960, Crisp 1961). Although most of these studies involved laboratory experiments with lab-reared or field­ collected larvae, experimental manipulation of settlement surfaces deployed at Menai Bridge (where barnacle larvae are very abundant seasonally) and else­ where figured importantly in some of the research (Knight:Jones & Stevenson 1950, Crisp & Meadows 1963). The major ideapromulgated in all of this research was that an animal's distribution was under behavioral control. This was challenged vociferously by Moore (1975), who pointed out that an animal's distri­ bution must depend not only on what the larvae are capable of doing, but also upon the "ecological opportunities" that a larva encounters. More recently, But­ man (1987) has attempted to resolve this controversy by suggesting that the rela­ tive importance of behavior and the other processes (e.g., currents) depends in part upon the scale of investigation. It was also during this period that work accelerated on the suborganismal phenomena by which ecologically relevant processes are mediated. Thus, for ex­ ample, the field saw a proliferation of structural and ultrastructural studies of sensory and attachment organs (e.g., Nott 1969, Lane 1973), as well as numerous attempts to isolate and identify substratum-bound substances to which larvae respond at settlement (e.g., Crisp 1967, Crisp & Meadows 1962, Williams 1964). This productive era of larval research has been reviewed extensively and ap­ propriately by some ofits leading players (Crisp 1984, Wilson 1952, Meadows & Campbell 1972b, Scheltema 1974), making a thorough coverage of the British contributions here both unneccessary and redundant. The 1967 Torrey Canyon oil disaster in the English Channel and the 1969 San­ ta Barbara drilling platform blowout in California occurred at about the same time as popular works like "The Population Bomb" (Ehrlich 1968) were stirring up environmental concern in the general public. Larval ecologists followed this trend by producing numerous papers on physiological tolerances oflarvae to var­ ious natural and artificial insults. Using the reasoning that larvae should be more susceptible than adults to lethal and sublethal effects ofpollution, many workers proclaimed the usefulness of larvae as bioassay organisms in environmental monitoring. Such work has continued to the present day (reviewed by Pechenik 1987). Simeone Mileikovsky (Fig. 9-F), a Soviet oceanographer at the Academy of Sciences in Moscow made numerous contributions to both theoretical and em­ pirical aspects oflarval ecology. His short but productive scientific life has been summarized by Costlow (1982). Most ofMileikovsky's early writings (beginning 34 CRAIG M. YOUNG in 1958) were based on plankton samples taken in the White Sea; laterwork incor­ porated data taken on cruises in the Barents and Norwegian seas. In addition to studies oflarval systematics and morphology, he worked on invertebrate spawn­ ing cycles (Mileikovsky 1958), daily fluctuations in larval populations (e.g., Mileikovsky 1960, 1970) and recruitment of deep-water benthic populations (Mileikovsky 1961), but, like Gunnar Thorson, he is best known for his important review articles (Mileikovsky 1971, 1973, 1974). The influence of excellent teaching in larval biology is exemplified by the life of Robert L. Fernald (Fig. 9-F). Beginning in the 1940's, he taught his famous embryology class each spring at Friday Harbor for more than 30 years, thereby stimulating not only several generations ofyoung embryologists, but also many ecologists and systematists who went on to investigate the natural history and ecology oflarvae. Dr. Fernald kept a card file on observations ofreproductive bi­ ology which has now been expanded into a valuable reference book that outlines available information and rearing methods for numerous species in the Friday Harbor region (Strathmann 1987). His students produced a Festschrift volume on the general topics of settlement and metamorphosis in 1978 (Chia & Rice 1978). Richard Vance's (1973) model, which has stimulated major discussions in larval ecology, was conceived during one ofDr. Fernald's embryology classes (F. S. Chia, pers. comm.). At Stanford, Arthur Giese's pioneering interests in reproductive cycles had a similar influence on ecologists working on problems of invertebrate reproduction.

1970-1989: A DIVERSITY OF APPROACHES Interest in larvae has increased dramatically over the past 20 years. Using the BI­ OSIS computer data base, I searched titles and abstracts since 1968 for papers that used several key words indicative ofinterest in larval biology. Because fresh­ water and terrestrial studies were not eliminated from this particular search, the data represent an overestimate ofusage by marine ecologists. Nevertheless, usage trends ofthe words "recruitment" and "settlement" (Fig. 10) indicate a striking increase ofinterest in early life-history ecology during the past two decades. The words "larva", "larval", and "larvae" were used 2153 times in 1969-1970 and 8798 times in 1987-1988. This growth is due partly to a widespread recognition that lar­ val processes are important in understanding benthic ecology and partly to the availability of exciting new approaches, methods, and technology. So many im­ portant papers have appeared in the past 20 years that complete coverage is im­ possible. Fortunately, a proliferation of recent reviews provides ready access to the current literature. During the decades when field experimentation with adult marine organisms was first coming into vogue among marine ecologists, (reviewed by Connell 1972, Paine 1977, Underwood 1985, Kitching & Ebling 1967), the planktonic portion LARVAL ECOLOGY OF MARINE INVERTEBRATES 35

1500

1200

>, u c; 900 QJ :J 0- "Recruitment" ....QJ 600 u, ..... - -1 Fig. 10. Citation frequency of the 300 -. - - ..... words "recruitment" and "settle­ ~--- ment" in titles and abstracts dur­ "Settlement" ing the past 20 years. Data are from 0, , I I 1968 1980 1984 1988 the BIOSIS data base and are pooled over two-year intervals. Year ofcomplex invertebrate life cycles, while recognized, was generallyassumed to be more-or-less irrelevant to the understanding of adult population dynamics. Caffey (1985) has summarized the traditional viewpoint ofmany marine ecolo­ gists as follows: Implicit in this approach has been the assumption that the settlement and subsequent early survival ofjuveniles from the plankton are either (1) near­ ly uniform in horizontal space and occur during well- defined seasons year after year, or (2) if they vary on different spatial and temporal scales, this variability has only immediate, transient effects on community structure. These largely untested assumptions have simplified the analysis and in­ terpretation of observational and experimental data. This attitude was finally challenged only a few years ago by pivotal papers (Un­ derwod & Denley 1984, Dayton & Oliver 1980, Woodin 1976, Connell 1985) that focused attention on the larval stage. Happily, the trend set in motion by these papers has stimulated an upswing in larval recruitment research throughout the world. Major initiatives in larval recruitment research have recently been an­ nounced by government funding agencies in the U.S. and France and Australia. The U.S. programon "GlobalOcean Ecosystems Dymamics" promises to stimu­ late research on the causes ofpopulation fluctuations by focusing on the relation­ ships between physical oceanographic processes and recruitment (Cullen 1988). Evolutionary approaches to larval biology have also become popular during the past few years. One major springboard for evolutionary arguments was Vance's model (Vance 1973) which relates larval mortality and fecundity to egg size. The model has been criticised and defended repeatedly (Underwood 1974, Strathmann 1977, Vance 1974, Christiansen & Fenchel 1979 and others). Richard Strathmann, Professor ofZoology at the University ofWashington's Fri­ day Harbor Laboratories, and his students have taken the lead in addressing evolutionary aspects of form and function in larvae (e.g., Strathmann 1974, 36 CRAIG M. YOUNG

Jackson & Strathmann 1981, Palmer & Strathmann 1981, Strathmann & Strath­ mann 1982, McEdward 1985, Emlet 1983, and others). Many ofthe evolutionary questions that could only be addressed hypothetically in the past are now receiv­ ing attention by population geneticists and immunologists with access to the latest technology (e.g., Grosberg & Quinn 1986, Hedgecock 1986). The work on chemical stimulation of settlement that was begun in Great Bri­ tain during the 1950's has grown into a major field ofinvestigation. Several meta­ morphic inducers have been isolated and characterized, with much ofthe current work being done in the laboratories of Daniel Morse in Santa Barbara and Michael Hadfield in Hawaii (reviewed by Morse 1984). Investigations of larval sensory organs used during and before settlement as well as other aspects oflarval morphology and ecology have continued in the laboratory of F. S. Chia at the University of Alberta (e.g., Chia et al. 1981, Chia & Koss 1979) and elsewhere. Thorson's (1950) recognition that developmental modes of gastropods can be in­ ferred from the veliger protoconch has stimulated much recent interest in larval ecology among paleontologists (reviewed by Jablonski & Lutz 1983, Jablonski 1986). The 1980's saw a tremendous increase in attempts to study larvae in their natural habitat. Some ofthe earliest and most successful studies ofthis kind have been done with the large, short-lived larvae of colonial ascidians. While still a graduate student, Randy Olson, now ofthe University of New Hampshire, suc­ cessfully tracked numerous larval didemnids from release to settlement on the Great Barrier Reef(Olson 1985a). His pioneering efforts were followed by other studies in which predator-prey relationships (Olson & McPherson 1987), settle­ ment behavior (Davis 1987), and larval swimming behavior (Young 1986) were studied by direct, in situ observations (see review by Levin 1990). Novel methods of in situ incubation were also introduced (Olson 1985b, 1987). Field studies of larval ecology are currently underway in the Antarctic (Olson et al. 1987) and the deep sea (e.g., Young & Cameron 1989) as well as various intertidal and subtidal habitats at both temperate and tropical latitudes. Laboratory investigations oflarval behavior increased greatly in sophistication duringthe past two decades. For example, natural light fields can now be imitated quite closely in the laboratory (Forward et al. 1984). Sulkin (1984) and Forward (1976) have reviewed some ofthe methods by which responses to isolated and in­ teracting stimuli are studied in the laboratory and Sulkin (1990) has published a rationale and defense of the reductionist approach in behavioral studies. Com­ puterized image analysis equipment has greatly expanded the kinds oflaboratory studies that are feasible. Several new methods of sampling larval populations have become available during the past few years. Willis & Oliver (1990) describe the tracking of coral eggs and larvae by aerial photography. David Wethey (unpublished) has in­ troduced the use ofvideo cameras to monitor settlement oflarvae in the field, and -

LARVAL ECOLOGY OF MARINE INVERTEBRATES 37

Steven Gaines (unpublished) has devised larval collectors that may be deployed inexpensively and in large numbers to monitor spatial variation in larval supply. New methods of tracking larvae are reviewed by Levin (1990).

CONCLUSION E. W. MacBride (1914)ended his classic Textbook ofEmbryology onthe following note: ...we have striven to represent the science ofComparative Embryology, not as a well-ordered and complete system ofphilosophy, but rather as a gold­ mine from which rich rewards have already been reaped, but ofwhich only a small part has as yet been developed, and which promises abundance of gratifying surprises and rewarding returns to the worker of the future. The same platitudes could be expressed in 1990 for Larval Ecology, a discipline that unites the traditionally distinct fields ofembryology and ecology and whose findings continue to promise broad application in fisheries, fouling, mariculture, and biotechnology. Important advances will be made most quickly if ecologists interact with zoologists and physical oceanographers to use existing knowledge as a springboard for efficient progres.s toward new discoveries.

REFERENCES

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