Volume 34, Number 3, Fall 1991 Reproductive Adaptations in Marine Organisms Mark V CTD P. Dunn K McCarthy THE HIGHEST STANDARD IN ACCURACY At sea in direct comparisons with other conductivity sensors, the Mark V external volume conductivity sensor has proven its superior dynamic response. The Mark V CTD has unmatched capability to calibrate to the accuracy limits of laboratory standards. Its superior stability carries this accuracy into the field where new levels of dynamic accuracy and spacial resolution are achieved. n Marine Instruments P.O. Box 498 11 40 Route 28 A Cataumet MA 02534 U.S.A. Telephone: (508) 563-93 17 FAX: (508) 564-4496 TELEX: 24-0096 EGG MCI MAIL: 322-6809 The World's Most Accurate CTD We go to sea with our instruments, get involved in the science, and continuously apply what we learn toward refinement. As a result, the Sea-Bird 9/11 CTD offers unmatched precision, superior static and dynamic accuracy, and exceptional reliability. We're serious about CTD performance. Call us. QBE? SEA-BIRD ELECTRONICS, INC. Telephone (206) 643-9866 %^^ ^ 1808 - 136th Place Northeast Bellevue, Washington, 98005 USA Telex: 292915SBEIUR Fax (206) 643-9954 PRODUCTIVE ADAPTATIONS 6 An Introduction to Reproductive Adaptations in Marine Organisms Lisa Clark Whether they acquire adaptations or employ strategies, marine organisms display a rich diversity of reproduc- tive behavior, function, and form. 11 Caribbean Reef Corals Alina M. Szmant and Nancy }. Gassman Though threats to their well-being abound, reef- building corals remain strong contenders in the fight against extinction. Pacific reef scene 19 Mating Strategies of Coastal Marine Fishes Phillip S. Lobel Sex switching, hermaphroditism, group spawning... since the 1960s we've learned much about fish reproduction, but our own sensory capabilities may still be limiting us. ^\ ^7 Sex (and Asex) in the Jellies J / Katherine A.C. Madin and Laurence P. Madin 4*m / Although of different phyla, these otherwise disparate groups share some seemingly bizarre yet intriguing adaptations to their common habitat. Snip (Cyclosalpa pinnata) whorl The Story of the Coelacanth Keith S. Thomson Many questions surfaced about this fish when it "reappeared" in 1938, but it seems the puzzle of its reproduction, at least, has been solved. A A Box lujL^l^L Coelacanths...The Fate of a Famous Fish JL JL Hans Fricke and Karen Hissmann Conservation is of the essence if this "living fossil" is to survive. numb-sized octopus (fish larvae predator) Copyright 1991 by the Woods Hole Oceanographic Institution. Oceatius (ISSN 0029-8182) is published in March, June, September, and December by the Woods Hole Oceanographic Institution, 9 Maury Lane, Woods Hole, Massachusetts 02543. Second-class postage paid at Falmouth, Massachusetts and additional mailing points. POSTMASTER: Send address change to Oceanus Subscriber Service Center, P.O. Box 6419, Syracuse, NY 13217-6419. Oceamts Headings and Readings y| ^^ Elasmobranch Fish: Oviparous, Viviparous, ^\ / and Ovoviviparous JL / Carl A. Luer and Perry W. Gilbert Elasmobranchs, including sharks, skates, and rays, employ a host of reproductive adaptations that compare more to birds and mammals than other, bony, fishes. Challenging the Challenger Craig M. Young Today, two long-standing ideas about reproduction in the deep sea are being challenged: Do deep-sea larvae feed? Does seasonal reproduction exist? Deep-sea urchin (Stylocidaris lineata) larva Hydrothermal Vent Plumes: Larval Highways? Lauren S. Miillineaux, Peter H. Wiebe, and Edward T. Baker Like unwitting passengers in a hydrothermal hot-air balloon, deep-sea larvae are swept into plumes of warm vent water and carried. . .where? F^ f\ Photoessay / I I A World of Art Beneath the Waves i vy Kathy Sharp Frisbee Award-winning photo artists Maurine Shimlock and Burt Jones capture the vivid, evanescent images of undersea life. Mushroom coral (family Fiingiidfte) See inside back cover Books On the Cover FEATURES Larval Forms with Zoological Verses by Walter Garstang; illustrated by Rudolf Scheltema Some well-known life histories take a whimsical turn with poetry and illustrations by two scientists who have studied them. 89 Creature Feature Ugly, dangerous, and fascinating: What IS it? Oceanus has won two Ozzie Awards .. .again! See page 53. Fall 1991 Vicky Cullen Editor Lisa Clark Assistant Editor Kathy Sharp Frisbee Editorial Assistant Robert W. Bragdon Advertising & Business Coordinator Lisa Poole Publishing Intern The views expressed in Oceamis are those of the authors and do not necessarily reflect those of Oceanus magazine or its publisher, the Woods Hole Oceanographic Institution. Editorial responses are welcome. Please write: Oceanus Magazine Woods Hole Oceanographic Institution Woods Hole, Massachusetts 02543, or telephone: (508) 457-2000, extension 2386. Subscribers within the US, please write: Oceanus Subscriber Service Center, P.O. Box 6419, Syracuse, NY 13217-6419. Individual subscription rate, $25 per year; Students, $20; Libraries and Institutions, $50. Current issue price, $6.25; 25% discount on current issue orders for five or more. Please make checks payable to the Woods Hole Oceanographic Institution. Subscribers outside the US, please write: Oceanus, Cambridge University Press, The Edinburgh Building, Shaftesbury Road, Cambridge CB2 2RU, England. Individual subscription rate: 24 per year; Students, 15; Libraries and Institutions, 43. Single- copy price, 7. Please make checks payable to Cambridge University Press. Canadian subscriptions available through Faxon at P.O. Box 2382, London, Ontario N6A 5A7, Canada. Add $5 to basic rates. When sending change of address, please include mailing label. Claims for missing numbers from the US will be honored within three months of publication; overseas, five months. Oceanus and its logo are Registered Trademarks of the Woods Hole Oceano- graphic Institution. All Rights Reserved. Oceanus International Perspectives on Our Ocean Environment Volume 34, Number 3, Fall 1991 ISSN 0029-8182 T93O Published Quarterly by the Woods Hole Oceanographic Institution Guy W. Nichols, Chairman of the Board of Trustees James M. Clark, President of the Corporation Charles A. Dana, III, President of the Associates Craig E. Dorman, Director of the Institution Charles D. Hollister, Associate Director, External Affairs Sallie K. Riggs, Director of Communications Editorial Advisory Board Robert D. Ballard, Director of the Center for Marine Exploration, WHOI James M. Broadus, Director of the Marine Policy Center, WHOI Henry Charnock, Professor of Physical Oceanography, University of Southampton, England Gotthilf Hempel, Director of the Alfred Wegener Institute for Polar Research, Germany John Imbrie, Henry L. Doherty Professor of Oceanography, Brown University John A. Knauss, US Undersecretary for the Oceans and Atmosphere, NOAA Arthur E. Maxwell, Director of the Institute for Geophysics, University of Texas Timothy R. Parsons, Professor, Institute of Oceanography, University of British Columbia, Canada Allan R. Robinson, Gordon McKay Professor of Geophysical Fluid Dynamics, Harvard University David A. 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Tel: 504-455-9988 Faxtel: 504-455-9795 ivftooerfson *^^^^^5* A Bird Group Cofr^pofiy N-4371 Egersuntl Norway Tel: *47 4 49 17 77 Faxlel 47 4 49 31 00 Telex 33139 Robertson Gyrocompass Robertson Manual and Automatic Steering Robertson Dynamic Positioning An Introduction to Reproductive Adaptations in Marine Organisms Lisa Clark The fact that so many organisms have done so well without sex for so long proves it is not necessary for survival. rhe ocean is Earth's oldest habitat, so it comes as no surprise that it is also the most diverse. This diversity extends into all realms of marine life, as organisms have evolved to exploit every imaginable advantage. It follows that marine animals would employ a wider variety of reproductive means than their land-based counterparts, and this is the case. In this issue, we highlight the reproductive modes of various animals, from the perspectives of the researchers studying them. Sex? Asex? Both? At the most general, we divide reproduction into two categories: asexual and sexual. Asexual reproduction is the oldest and simplest form of reproduction, by which one parent's body divides or breaks apart in some way to produce offspring that are genetically identical to the parent. Asexual reproduction methods include fission, where a parent's body splits into two more-or-less equal parts; budding, where a small part of a parent's body becomes differentiated and separates from the rest; and fragmentation, where a parent's body breaks into many pieces and each piece develops into an offspring (starfish can regrow an entire body from a single broken-off arm this way). In contrast, sexual reproduction occurred later in the evolutionary scene, and requires two parents. Offspring result from the fusion of cells from each parent (called gauietes or sperm and eggs). Many marine organisms, such as jellyfish, actually alternate between asexual and sexual reproduction. Some, such as pygmy angelfish and some corals, alternate between being male and female, a practice called hermaphrodit- ism. Some do both, alternating reproductive style and sexual orientation. Larry and Kate Madin describe how salps and doliolids accomplish this intriguing feat. Many organisms employ a simple method of sexual reproduction termed broadcasting: males and females cast their gametes into the water, where mixing occurs, and if all goes well, fertilization follows. After that, the parents ignore them. This risky method requires both males and females to produce enormous numbers of gametes to beat the odds and actually have offspring that develop and mature. Ways of bettering these odds are numerous and often extraordinary, involving both behavioral and anatomical adaptations. Some described here include elaborate courtship rituals, or releasing gametes only at particular times or in certain places that may be safer, as Phil Lobel describes; synchronized gamete release, as reviewed by Craig Young; and Oceanus holding gametes together with egg sacs, cases, or mucus as Carl Luer and Perry Gilbert discuss. Alina Szmant and Nancy Gassman provide an excellent overview of the theoretical basis for many of these adaptations, delving into r- and K- selection and the benefits and liabilities of broadcasting as it pertains to coral reef communities. Moving fertilization from outside the parents' bodies to inside the mother creates a safer place for development to occur, but again imposes size and quantity restrictions on the parents as to how many offspring they can produce. Carl Luer and Perry Gilbert investigate how these restrictions can explain how sharks, skates, and rays reproduce. Why Does Sexual Reproduction Even Exist? Sex is so widespread that it must be significant, but the fact that so many organisms have done so well without it for so long proves it is not necessary for survival. Sexual reproduction contains inherent costs; for example, the number of young is limited by the fecundity of the females, and females and males contribute half of their genes to each offspring. Males could have more young if they weren't limited by females, and females could pass on all of their genes to their young if they reproduced asexually. But sexual reproduction has benefits, too: It generates genetic variability, so that mutations can occur faster and more often, allowing populations to respond to environmental change more easily. Further, within a brood or a set of siblings, each individual will be different, making survival of at least some more likely if the environment is a changing one. The subject is complex and becomes even more so when genetics, behavior, predation, and specific environments are considered. One thing we can all agree on: Whether sexual or asexual, reproduction is the only way a species can assure its survival. But What IS a Species? Over one million animal species have been described, and there may be more than five million species of animals and one million species of plants in the world today. These numbers vary tremendously, depend- ing on how one defines species. Classically speaking, a species is some- thing that is seen or intuited as distinctive, usually morphologically so. Plato referred to an organism's eidos, or essence, as that which made it distinctive; organisms with similar distinctions constituted species. Modern definitions abound. The definition that seems to be most ac- cepted by biologists requires reproductive isolation: Basically, if two organisms can interbreed, they are usually of the same species usually, because there are exceptions. When individuals from different species Jclh/fish reproduce in a variety of ways, as Katherine and Laurence Mad in reveal. Aegina citrea illustrates an interesting, if complex, arrangement: The tiny little jellyfish growing inside Aegina 's bell are not its own, but belong to an individual from an entirely different species. Fall 1991 interbreed (a rare event), the resulting offspring is a hybrid. If the hybrid is sterile, it cannot reproduce. If fertile, the hybrid may provide a mecha- nism for producing another species. Many other definitions for species exist, and the debate most likely will continue, because a working definition for species that is appropriate for all branches of science, from population biology through philosophy, does not yet exist. Actually, some think one definition will never work because there is, in fact, more than one type of species. Phylogeny refers to the evolutionary relationship between organisms, and provides a good theoretical basis for classifying these millions of animals into some framework, so that we might study them more easily. The framework itself is called taxonomy, and the most specific level of the classification scheme is the species. All animals are part of Kingdom Animalia, the most general level of the taxonomic system. Animals are grouped according to how closely related they are: related species are grouped into a genus, related genera into a family, related families into an order, and so on. Often subcategories are introduced as well. For example, within this system, human beings are classified as shown. Kingdom Phylum subphylum Class Order suborder superfamily Family Genus Species Animalia Chordata Vertebrata Mammalia Primate Anthropoidea Hominoidea Hominidae Homo sapiens Human Proportions, from Accademia. by Leonardo da Vinci, Venice. From The Notebooks of Leonardo da Vinci by Edward MacCurdy An animal's evolutionary history can be charted in a phylogenetic tree that reveals its origin (as we know it) as a base, and diverging categories as different branches. Animals that diverged close to the base, or relatively early in the animal kingdom's history, are often referred to as "lower" or "primitive," while those that diverged later may be called "higher" or "advanced" animals. These designations do not imply any level of complexity, as is frequently (and erroneously) believed. For example, sponges and cnidarians are believed to have originated close to the base of the animal kingdom phylogenetic tree, and although "primi- tive," these animals display some specialized and unique features. A topographical map presents a good analogy for the phylogenetic tree: the terms "higher" and "lower" represent position only, and carry no further connotation. Although he used them, Darwin detested these adjectives, and was constantly reminding himself not to use them. The Coelacanth Lives In this issue we have also included an article on an animal about which very little is known: the coelacanth. Long thought to be extinct, this huge, iridescent blue fish resurfaced in 1938 when it was trawled off of South Africa. A local museum curator, Marjorie Courtenay-Latimer, often perused the fishermen's catches for interesting specimens, and on the deck of the trawler Nerine one cold December afternoon she certainly found one. She couldn't identify it, so she wrote her friend Leonard Oceanus Smith, an ichthyologist. Upon consideration of her description, Smith commented to his wife, "Don't think me mad, but I believe there is a good chance that it is a type of fish generally thought to have been extinct for many millions of years." He wasn't mad, but the fish wasn't extinct, either. Until this finding, the only coelacanths seen were fossils; the last ones were believed to have died out with the dinosaurs at least 70 million years ago. Keith Thomson's article about this illustrious fish is from his recent book Living Fossil: The Story of the Coelacanth, a riveting tome that relays what is known and isn't about coelacanths, in a manner that combines well the excitement and romance of scientific discovery. We recommend it. Following Thomson's article, Hans Fricke and Karen Hissmann elucidate their perspective on coelacanth conserva- tion, based on their extensive filming of the coelacanth in its natural environment and their ongoing research. Sex in the Seas An early choice for this issue's title was "Sex in the Seas," a rather catchy theme, we thought. Soon, though, we realized that although it's an alluring and interesting title, the problem is it gives a back seat to asexual reproduction. We then settled on "Reproductive Strategies of Marine Organisms" and unwittingly paved our entrance into a debate that has AH animals are believed to have evolved from the same source: flagellated, single-celled animals. This simplified pln/logenetic tree shows some basic interrelationships between large animal groups. (After Villee, Walker, and Barnes, General Zoology, 2978.) Amphibians Sharks & Rays Coelacanths Eels Bony Fishes Reptiles Birds Mammals Arthropods (spiders, crustaceans, centipedes, insects) Vertebrates Cephalochordates , j Urochordates 1 (tunicates, salps) Chordates Annelids (tubeworms, earthworms, leeches) Echinoderms (starfish, sea urchins, sand dollars, sea cucumbers) Bryozoans (moss animals). Molluscs (snails, squids, clams, octopods) Psuedocoelomates (rotifers, nematodes) Acoelomates (flatworms) Sponges *-- Cnidarians (jellyfish) Ctenophor es Multiple-Celled Animals Flagellated Single-Celled Animals Fall 1991 THE FAR SIDE By GARY LARSON The committee to decide whether spawning should be taught in school. Lisa Clark is the Assistant Editor of Oceanus and an avid follower of evolutionary history debates. been raging for years (Ernst Mayr, an eminent biologist and philosopher, maintains it goes back at least as far as Aristotle): Should the scientific community tolerate teleological language? According to Webster's Third Neiv International Dictionary (1986), teleolog}/ is "The philosophical study of evidences of design in nature compare mechanism; the use of design, purpose, or utility as an explanation of any natural phenomenon." Strictly speaking, to suggest that organisms have strategies for what they do implies their actions are shaped by purpose. So we gave it more thought and came up with "Reproductive Adaptations in Marine Organisms," and relaxed in the knowledge that we had satisfied the purists, not offended anyone, and still gotten our intended meaning across. Objections to teleological language in the discussion of scientific research or theory may seem obvious. Delving into evolutionary theory, natural selection does not possess tenets for surmising future activities. Past events are rewarded; future plans are nonexistent. But what effect would complete eradication of teleological language have? For example, consider the statement, "Within the intricate cardiovascular system, the heart functions as a blood pump," versus "Within the intricate cardio- vascular system, the heart pumps blood." While the former implicates function, the latter describes action. But, the former also has a stronger emphasis on the heart as one element of an extensive system than has the latter. If this emphasis is the author's intended point, is the reader mis- guided by the terminology selected? Doubtless the sentence could be rewritten any sentence can. Is there a line, that, when crossed, immedi- ately identifies the user as syntactically untidy or, worse yet, philosophically in error? The views on this topic are as varied as the individuals doing the speaking. As with so many other issues, a continuum exists, and there are, seemingly, proponents for every point along the line. George Williams (author of Adaptation and Natural Selection, 1966) maintains that "Reproduction is sexual if it produces offspring with new combinations of the parental genes, and does so by means of machinery designed to produce that result." He concedes that to include the anticipa- tory element of increased fitness in any definition relating to evolution or its forces is teleological, and warns that "Sex may act to increase population size, and it may act to confer evolutionary plasticity, but these are effects, not functions." However they reproduce, whether by acquiring adaptations or employing strategies, marine organisms display a diversity of reproduc- tive behavior, function, and form that comprises a rich field for study and reading. Selecting just a few articles for inclusion in Oceanus was no easy task; it did however, give us renewed appreciation for the incredible variation the ocean environment supports. 10 Oceanus Caribbean Reef Corals The Evolution of Reproductive Strategies Alina M. Szmant and Nancy J. Gassman o paraphrase Benjamin Franklin, for humans. ..life comes with only two certainties: death and taxes. For all other species, death remains the only sure thing. While most individual life-spans are relatively short (months to a century or so), the longevity of the species they belong to is generally much longer (thousands to millions of years). Reproduction is the process through which individuals contribute to the persistence of their species. Within each species, those members with the most repro- ductive success have the greatest role in shaping their species' future. A minimal definition of reproductive success for a species is that the overall recruitment rate (the rate at which new individuals survive to reproductive maturity) must equal or exceed the death rate. Different habitats are characterized by levels of disturbance that influence the death rate of the indigenous population. A species living within a given habitat must adapt as the environment changes, or face extinction. How a species approaches the problem of survival its life-history strategy- On the Belize Barrier Reef in Carrie Bow Cay, a diverse coral community supports many species and colony sizes. At lower left is the brain coral Diploria strigosa; the one that looks like a head of lettuce is Agaricia tenuifolia, or lettuce coral; and the branching one in the foreground is the staghorn coral Acropora cervicornis. Many species of feather- and fan-type corals fill the background, including Gorgonia sp. and Pseudoplexaura sp. Fall 1991 11 Reproduce as early as possible, as often as possible" or "Live long, and produce a few good offspring/' depends on how past environmental change has influenced the evolu- tionary forces of natural selection. The theory behind life-history strategy is the subject of the first part of this article. In the latter part we will explore how corals, subjected to the reef's variable environment, use a wide variety of life-history and reproductive strategies to keep their species going. Variations on Life-History Themes The time interval between birth and death varies from individual to individual and species to species, and depends on a number of factors. Prime among these are aging patterns, called senescence sequences, that are preprogrammed and genetically determined characteristics of each species. Individual mortality is also affected by the level of environmen- tal danger, in terms of predation and physical disturbances such as storms. Another factor influencing survival is the availability of suffi- cient resources to support life (the extent of competition for food and shelter) as well as an individual's susceptibility to disease. For each species, the sum of these evolutionary and environmentally determined factors results in a "probability versus time" relationship predicting the individual's life-span. Species whose members have a good chance of being killed at an early age or are genetically programmed for early senescence (a short life-span) must begin reproduction when young and must produce offspring at a high rate to avoid extinction. These so-called r-selected species have populations characterized by a high turnover of individuals, large fluctuations in population size, and a large investment in sexual reproduction beginning at a young age or a small size. This life-history pattern is characteristic of opportunistic and weedy organisms such as mice and dandelions. Their motto might be "Reproduce as early as possible, as often as possible." Conversely, species with individuals that can avoid sources of mortality and live to a ripe old age can afford to wait before beginning to reproduce. They can produce fewer but better-equipped offspring. Populations of these K-selected species are dominated by fewer, larger, older individuals, and are characterized by reproduction later in life and a large energy investment into a small number of offspring, each with a good chance for survival. Prolonged parental care is common among these species, which include elephants and humans. They live under the banner "Live long, and produce a few good offspring." How do individuals of long-lived species avoid the environmental sources of mortality? One way is to reach a refuge in size, that is, to become so large that few things can kill you. Another way is to subdi- vide at periodic intervals (via vegetative or asexual reproduction), which results in clones of genetically identical individuals, and thereby reach a refuge in space. Dispersing clone-mates, like giving away clippings from a favorite houseplant, decreases the probability that any single event will kill off the entire clone, and thus increases the longevity of the individual genetic makeup or genotype. In avoiding mortality, an individual spends a considerable amount of energy on growth. This explains why sexual reproduction, always an energy-intensive process, may be delayed for many years. Ultimately, limits on available energy resources (food), or an organism's ability to 12 Ocennus process resources (eat or digest), forces what can be viewed from an evolutionary perspective as a choice between emphasizing growth versus emphasizing sexual reproduction as a life-history strategy. The r- and K-patterns represent the extremes in a continuum of evolutionary options concerning the allocation of resources between growth and reproduction. No single combination is best under all circumstances, and many different choices are equally good under the same circumstances, leading to the variety of reproductive and life-history patterns we observe in nature. As Ursula says to Ariel in Walt Disney's movie The Little Mermaid, "Life is full of tough choices, ain't it?" In the case of evolution, responses to this combination of choices determines the difference between a species' survival or extinction. The Significance of Asexual Reproduction in Coral Communities Reef-building corals are a group of species that come in an amazing variety of shapes and sizes. Thriving Caribbean coral reef communities can support more than fifty species of coral; Indo-Pacific reefs are many times more diverse. Consequently, corals live close to each other, com- peting for space and light on the structure they communally produce. Most reef corals are colonial, and their growth form (branching, plate- like, or mounding) depends on how polyps derived from asexual budding remain connected to each other. The individual polyps are the reproductive units of the colony. Each polyp develops a set of gonads that may be male, female, or hermaphrodite, depending on the species. The more polyps a colony has, the greater its reproductive potential. Many species appear able to continue to bud and grow in an indeter- minate way. In other words, these species are potentially immortal, as they lack aging sequences and will grow until some external factor kills them. Some of these long-lived species form massive colonies that are meters in diameter and hundreds of years old. Others form branching colonies, with branches that can break off, roll away, and survive to form new colonies. Some large reef areas are dominated by just a few clones of branching species that have propagated asexually. For example, in the Caribbean, two branching species of Acropora (elkhorn and staghorn The fragile branching coral Acropora cervicornis (left) can dominate large areas of reef through asexual propagation after fragmentation, but only when physical distur- bance is relatively low. Massive Montastrea annularis colonies (right) average 3 to 4 meters in height and have a maximum growth rate of 1 centimeter per year. They can survive for centuries. Fall 1991 13 Back Ffeef Lagoon L 2!one /-Ffeef Ff&t J-Z'ont Milleporz This Caribbean reef profile reveals how various habitat-determining environmental factors change with (and ore responsible for) reef zonation. Coral response to these changes is also included, slwwn by coral diversity. As light decreases on the fore-reef slope , coral growth slows and eventually stops. Corals grow better where there is more light (in the shallow breaker and buttress zones), but higli turbulence and high rates of sediment accumulation (sedimentation) prevent many species from successfully inhabiting these well-lit, shallow areas. Corals can gain better attachment to the substrate when it is hard and stable; attachment to loose rubble can mean death when a storm comes through. For these reasons, coral cover and diversity is highest at intermediate depths, where light is sufficient yet unfavorable physical factors are minimized. coral), two massive species of Montastrea (mountainous star coral and large star coral), and several brain coral species grow indeterminately and are responsible for producing most of the reef framework. Some species are always found as small colonies, suggesting they either stop growing at some genetically limited size, and /or they have high mortality rates and die before reaching their growth potential. Although many of these species are numerous, because of their small size they do not contribute significantly to the reef framework. The remaining species provide a continuum between the larger- and smaller- sized species. Many of these species are most common in the small- to medium-size colony range, but some of them also form large colonies. Answering the Need for High Recruitment Rates Reef coral structure is unique, combining a skeleton-building animal with photosynthesizing algae that live within the coral's tissues. As a sessile animal that attaches itself to one spot for life, a coral larva's choice of a settlement site becomes the future colony's permanent home. Optimally, this home includes plenty of light for the coral's symbiotic algae, substantial water movement to bring in nutrients and remove wastes, and enough space for growth. Reproductive strategies evolved by different coral species allow the adult colonies to influence the fates of their larvae and recruits. The shallow depths of the back reef and reef flat are frequently dis- turbed by storms, resulting in high mortality rates for organisms attached to the loose rubble that characterizes these areas. While occasional medium- sized corals may be found, small, short-lived colonies are more common to 14 Ocean us - Zone fit Acropora Zone fV- Buttress- 7 V-Fore Slope these rubble zones. These colonies begin reproduction within the first few years of growth; for example, Favin fragum, the golf-ball coral, begins producing gametes when the colony diameter is less than 3 centimeters. Thousands of colonies of this species are found all over back reefs, but they seldom get bigger than (as their common name implies) a golf ball! The golf- ball coral's strategy seems to be a simple one: Reproduce often, thirteen cycles a year to be exact, and begin doing it as soon as you can. However, the mode of reproduction of this and similar coral species contrasts with what we expect based on the traits usually associated with r-selected organisms (i.e., very large numbers of offspring that can recruit every- where). F. fragum exhibits a mode of reproduction that is the closest thing to parental care found in corals: After internal fertilization, the maternal polyp broods the eggs, then holds the developing embryos in her stomach cavity for about three weeks, until mature planula larvae develop. Why? Brooding can be seen as an adaptive trait for living in frequently dis- turbed habitats. Maintaining a population that suffers from high adult- mortality rates requires high recruitment rates; in other words, birth rates and death rates must balance. Brooded planulae are mature and can settle within hours after release from the maternal polyp. This decreases the time the larvae spend drifting in the plankton, a phase of marine life characterized by high mortality and wide dispersal rates, and insures a large number of offspring to support high local-recruitment rates. Environmental disturbance and brooding, however, is not confined to shallow-water species, as exem- plified by the congeners (closely related species) Agaricia huinilus and Agaricia agaricites, two types of platy lettuce-leaf coral. A. cigaricites forms plates attached (by one edge) to substrates from the reef flat, to Off Puerto Rico, in the LaPargnera area, small colonies of the brooding golf-ball coral Favia fragum are abundant but inconspicuous in buck-reef waters. This species has a high mortality rate, likely due to their habit of settling and growing on loose reef rubble. Fall 1991 15 Life cycles of corals include a "choice" between broadcasting, with embryonic development in the water column, or brooding embryos to the planula stage. Differences in other life-history characteristics are also included. depths up to 35 meters. This coral reaches a maximum diameter of 60 centimeters, but seldom reaches this size on the reef flat. A. humilus is mainly found at depths less than 10 meters, and reaches a maximum diameter of 12 centimeters. Both species brood their larvae. A. humilus reproduces at one-third the size of A. agaricites (when, on average, the colony diameter is 2.8 centimeters for A. humilus and 10.8 centimeters for A. agaricites). Both species have peak planulae production in spring and summer, but the smaller A. humilus releases planulae year-round while its cousin's reproductive season is limited to a narrow spring window. Overall, on an annual basis A. humilus probably produces more planulae, but A. agaricites produces larger planulae. The differences between the reproductive strategies of these two species can be attributed to the predictability of their preferred habitats. A. humilus occupies some of the same shallow zone that F. fragum does. Frequent physical and biological disturbances cause a high turnover of the substratum and attached corals. As with F. fragum, postponing reproduction to a later time is a risk that could mean never reproducing at all. Adult colonies of A. agaricites, on the other hand, inhabit parts of the reef that appear to be more predictable: Storm waves don't usually exert a major force at moderate and deeper depths, and the substrate they attach to is not loose rubble, but reef framework. However, bioerosion, the dissolution and chipping away of the reef framework by boring plants and animals, is hard at work at these depths. Boring sponges can severely weaken the rather limited attachment of A. agaricites colonies to their substrates. Substrate slumping causes high rates of mortality of A. agaricites, especially on the steeper parts of the reef. Thus, most colonies are almost assured of death after only one or two decades of growth, and high recruitment rates are necessary to sustain population densities. The larger planulae of this congener, produced at the expense of a shortened reproductive season, may provide some advantage in survival after settlement in this reef zone where competition for space is great. The buttress and fore-reef zones are dominated by moderate to large 16 Oceanus coral species that reproduce by broadcasting. During a few nights each year, within a specific lunar phase that is characteristic of each species, massive coral colonies spawn eggs and sperm into the water column. Gametes are fertilized externally, and larval development occurs in the plankton. These planulae cannot settle for many days to weeks. All of the large indeterminate-growing, framework-building species mentioned earlier use this strategy, as do most Indo-Pacific corals. Broadcasting results in currents transporting the larvae away from the parental reef to unknown habitats, with a very high larval mortality rate. While disadvantageous in terms of contributing to local recruit- ment, such dispersal is essential for corals to establish themselves in new environments where competition for space may be lower. Early settlers to new environments may have an advantage in reaching the coveted refuge in size without being overtopped or out-competed for space. Furthermore, as the colony grows larger, its reproductive potential will increase (there will be more polyps to produce gametes), as will its relative contribution to population reproduction and its chances of producing a successful recruit. For massive colonies that live for literally hundreds of years, survival of only a few of the billions of eggs that one colony may produce in its lifetime is considered successful reproduction. Once established, these large colonies will survive all but the most severe disturbances, so successful recruitment on the decade-to-century time scale alone can balance mortality. No Eternal Life for Reef Corals What kinds of severe disturbances can kill large corals? Three come immediately to mind: direct hits by major hurricanes, epidemics of diseases or predators, and (if corals had emotions, probably the most dreaded) sea-level changes. Hurricane Hattie hit the Belize area in 1962, and totally denuded about 20 linear miles of reef of its corals. Surround- ing areas received lower levels of damage, thus coral recruits would have to come from a fair distance to repopulate these reefs. Diseases such as white-band disease, which infects the Acroporas, and black-band disease, which infects several of the large star- and brain-coral species, have reduced coral population sizes on reefs throughout the Caribbean. As mentioned, within a population, fewer individuals translates to lowered reproductive potential, so again, recovery depends on recruits arriving from unaffected reefs. Plagues of predators such as the coral- eating crown-of-thorns starfish, Acanthaster planci that devastated Compare these two corals with the photos of heal tin/ colonies on page 13. High-energy environments can result in death for Acropora cervicornis (left). Similarly, Montastrea annularis (right) can survive for centuries, only to be ravaged by black-band disease, as shown, or toppled by hurricanes. Fall 1991 17 Broadcast spawners can have much of their annual reproductive effort quickly decimated by predators. These marauding brittle stars are feeding on a Diploria strigosa colony. Indo-Pacific coral communities), so far have not been noted in the Caribbean. The worst threat to coral reefs over geological time, however, is sea-level change. Dozens of major and minor sea-level fluctuations have occurred over the past 1.6 million years. Every time sea level gradually drops, entire coral reef communities are left high and dry: For example, the Florida Keys are the remains of coral reefs that flourished 120,000 years ago when sea level was several meters higher than it is now. When sea level rises again, established corals will be left behind in the dark. For coral species to survive these repeated long- term disturbances, they must be able to colonize new substrates brought into the light (as sea level recedes) or reflooded (as sea level rises). This is true for both short-lived brooding species and long-lived broadcasting ones, and probably occurs by a combination of long-distance and local recruitment. The planulae of Pocillopora damicomis, a typical Indo-Pacific r-selected brooder with high rates of local recruitment, can remain in the plankton for up to two months. Thus brooding, with its potential for high local- recruitment rates, does not preclude long-distance dispersal as well. Since brooding seems to be so effective for both short-term and long- term recruitment needs, why aren't more, or all, coral species brooders? One possibility is that brooding is energetically expensive, which may explain why there is a paucity of examples of large-sized brooding species. Unfortunately, no study to date has compared the costs of brooding versus broadcasting. We may never know the answer to this question, but it must be related to the reason why plant communities have both weeds and trees. Luckily, Mother Nature likes diversity, or else we might not have forests or coral reefs! Coral communities have been part of the geological record for hundreds of millions of years, surviving major extinction events that decimated entire groups of species, such as dinosaurs. Each day brings a new challenge in the fight against extinction, and corals employ a variety of life-history strategies to remain competitive contenders in the ever- changing game of survival. Alina M. Szmant is an Assistant Professor of Marine Biology and Fisheries at the Rosenstiel School of Marine and Atmospheric Science (RSMAS), University of Miami, Florida. Her attraction to coral reefs began while growing up in Cuba and Puerto Rico, and her research interests in the physiological ecology of reef corals were developed during undergraduate and graduate studies at the University of Puerto Rico, the Scripps Institution of Oceanography (University of California, San Diego), the University of Hawaii, and the University of Rhode Island. She was a member of the first team of female scientists to live and conduct underwa- ter research during the Tektite II project in the US Virgin Islands. Nancy J. Gassman is a senior graduate student at RSMAS. She is presently finishing her Ph.D. on the biochemical aspects of coral reproduction, and has participated in studies of coral reproduction in the Eastern Pacific. 18 Ocean us Mating Strategies of Coastal Marine Fishes Phillip S. Lobel ourtship displays and mating rituals are among the most fascinating behaviors of fishes. They exhibit an array of reproductive styles that includes sex switching, simulta- neous hermaphroditism (individual fish are functionally both male and female at the same time), and spawning in pairs, trios, or groups. The reproductive habits and life-history ecology of only a few species is known from observations of fishes in aquariums, on tropical coral reefs, and in clear freshwater habitats such as the African Rift Lakes and in North American and European waters. One of the better-studied locations is the Hawaiian Islands, whose waters harbor at least 461 species of coastal marine fishes. So far, we know the breeding habits of fewer than 30 of these fishes. Knowledge of where and when fishes spawn allows effective planning of species conservation protocols. Traditionally, openings and closings of fishing seasons have been planned to protect fish spawning All photos for this article are by Phillip S. Lobel. The sexes of this mated pair of longnose butterflyfish (Forcipiger flavissimus) can onh/ be distinguished because the female's abdomen is swollen with In/drated eggs, as she is ready to spawn (lower left). At other times, males and females look alike. This pJwto was taken off Kona, Hawaii. Fall 1991 19 A Caribbean male damselfish Abudefduf sexatilis (right) protects a nest of zi/gotes (shown as a purple mass) that are attached to coral substrate. The male jawfish Opisgnathus aurifrons (below) incubates zi/gotes in his mouth for several dai/s until the fry are free-swimming. > ' periods. Studies of fish reproductive habits over the past 20 years revealed that many species migrate to specific breeding grounds and that specific habitats serve as nursery grounds for juveniles. As a result, permanent nature reserves have been established to protect fish spawning areas, a good example of the practical application of scientific knowledge. Studies of reproductive behavior provide insight into the ecological and evolutionary processes that ultimately govern a species' existence. The evolutionary process operates via natural selection upon individual organ- isms. Therefore, knowledge of individual behaviors, such as mate selection, mating rituals, parental care of offspring, larval orientation behavior, and feeding strategies, is fundamental to construction of realistic models for understanding and predicting population changes, community structure, and population dynamics. The history of scientific observation of fishes' reproductive behavior began with the aquarium hobby. Freshwater fishes were first kept in glass containers during the 1850s, but observations of marine fishes spaw r ning in their natural habitats followed the invention of scuba equipment a century later. John E. Randall (Bishop Museum, Honolulu, Hawaii), foremost among the first generation of diving ichthyologists, first described the spawning behavior of several coral reef fishes in the early 1960s. Very few coastal marine fishes were actually seen mating in the wild during the 1960s. Those most commonly observed were damselfishes (fam- ily Pomacentridae) which have nests of eggs protected by the male; jawfishes (Opisgnath- idae), with males incu- bating zygotes in their mouth; and the wrasses and parrotfishes (Labroidei, Labridae, and Scaridae), which spawn conspicuously by rushing upward to release free-floating gametes a few meters above the bottom. These fishes are reproductively active during the peak daylight hours when the '60s scuba divers were also most active. Despite numerous field studies, the reproductive activity of most other marine fishes including many common and conspicuous reef fishes, remained a mystery. A partial explanation for why we have seen so little activity is due to our habits and not that of the fishes! Most human activities, including scientific investigation and sport diving, peak during the brightest times of day. By dusk we settle into the comforts of home, and while most of us are eating dinner, many reef fishes are spawning. A similar situation existed with observations of the predatory activities of reef 20 Oceanus fishes until 1970, when Edmund S. Hobson (National Oceanic and Atmo- spheric Administration, Tiburon, California) conducted studies during the crepusular periods (dawn and dusk). In my junior year (1974) at the University of Hawaii, I discovered that several Hawaiian reef fishes spawned during a restricted time period around twilight and sunset. Until then, sunset diving was not a popular activity. Since then, scientists have learned that many fishes, both temperate and tropical, spawn during this evening crepuscular period, especially species that broadcast their gametes. We know more about the behavior of tropical marine species than temperate marine fishes simply because of the favorable diving and observ- ing conditions in the tropics. Spending a lot of time in the sea is the key to understanding the many-faceted behavior and mating strategies of marine animals. However, direct observation can instill a certain bias in the ob- server. Historically, descriptions of spawning behavior emphasize visual aspects such as color patterns, movements, and body postures. Technical difficulties have prevented exploration of the behavioral roles of other sensory cues, such as chemical and acoustic signals. There is still no easy way to study the role of chemical signals in sexual communication among wild fishes; however, recent advances in acoustic instrumentation and video cameras provide new, and relatively easy, ways to study marine animal sounds. Three years ago I built a synchronized video and acoustic recording system that allows a scuba diver to record wild fishes in their natural environment. The results have been fantastic! I found that some fishes hitherto unknown as sound producers in fact use acoustic signals as an integral part of their courtship and spawning behaviors. In addition, 1 have associated a variety of sounds with specific behaviors other than those already known in sound-producing fishes. The results were startling because humans cannot directly hear many of these sounds underwater; for us, it is mostly a silent sea. Some of the first fishes examined are among the most thoroughly studied in terms of the number of scientific papers written about their reproductive behavior: Caribbean hamlets (Hypoplectrus unicolor, family Serranidae), Caribbean striped parrotfish (Scarus iserti, family Scaridae), African Rift-Lake cichlids (particularly Copadichromis cucinostomus, family Cichlidae), and a Pacific damselfish (Dnsci/llus nlbisclla, family Pomacentridae). My current research focuses on the behavioral context of purposeful sounds. One goal is to develop passive acoustic methods that will allow us to quantify mating frequency by counting specific spawning sounds, providing the means to determine the relationships between fish spawn- ing activities and fluctuations in environmental variables such as tem- perature, currents, light, etc. Previous approaches to fish reproduction studies required some sort of disturbance to the fishes. These included collecting specimens for gonad analysis, plankton-net collections for egg and larval counts, and direct observation of fishes in their natural habitats, all labor-intensive and intrusive. Most importantly, it has been difficult to obtain time-series data from a variety of sites simultaneously. If a fish produces a distinct sound pattern explicitly associated with courtship behavior and /or with the mating act, then passive acoustic methods can be developed to document the frequency of these activities Recent advances in acoustic instrumentation and video cameras provide new, and relatively easy, ways to study marine animal sounds. Fall 1991 21 i at specific locations. Synchronous measurement of environmental variables will then provide the scientific database required to elucidate how fish spawning fluctuates with physical changes in the ocean. Life History of Coastal Marine Fish Coastal fishes exhibit tremendous diversity of breeding behaviors but there is one general fate of the zygotes and hatchlings. Because new spawn float to the near surface and drift in the ocean currents, the survival of the next generation of fishes is greatly influenced by the mating site the breeding adults select. The majority of coral reef fishes broadcast their eggs and sperm, which are mixed in the water before they float away from the natal habitat. The spawn drifts out to sea where it remains for various periods of time, typically ranging from three weeks to three months for tropical marine fishes. Once these pelagic larvae have completed their planktonic phases, the little fishes somehow find their way back to appropriate nursery habitats that include coral reefs, sea-grass beds, mangroves, sand flats, estuaries, and tide pools. Here the larvae undergo metamorphosis and transform into their juvenile stages. In general, very little is known about the lives of pelagic larval fish and the process of metamorpho- sis from larvae to juveniles. The fact is that scientists are work- ing hard just on species identification of larvae, because larval forms look dramatically different than juvenile and adult forms. The timing of reproduction among near-shore fishes reflects adaptation to a variety of ecological factors. Their daily cycles appear to be influenced by balancing two threats: daytime planktivores that feed on eggs and newly hatched larvae and crepusular predators that attack spawning adults. While spawning at dusk reduces the risk to eggs and larvae, it is also the time of peak predation upon adult fishes. Lunar reproductive synchrony may further reduce chances of preda- tion on individuals through a swamping effect: Essentially, an individual fish is safer among a group of other individuals doing the same thing at the same time. The full moon can act as a signal to the general population and thus synchronize their behavior to elicit this "safety in numbers." Daytime planktivores are adapted to plucking small prey from midwater, while nocturnal planktivores possess large mouths and feed mainly on larger plankton and settlement- stage larvae. By dusk, most daytime planktivores have de- scended to the reef for the night. Spawning at dusk appears to reduce chances of eggs being eaten in two ways: There are few active planktivores, and any planktivores still active may be quickly satiated by the bounty from the simultaneous spawn- ing of many fishes. The blue tang (Acanthuraus coeruleus) is silver when in its larval form (top), yellow when recently transformed into a juvenile (second), blue during the process of maturing from late juvenile into adult (third), and vibrant blue at full adulthood (bottom). 22 Oceanus Twilight is a visually difficult time for most shallow- water, near-shore fishes. It may be possible that the low light levels just before sunset and the onset of moonlight twilight are sufficient for fishes to recognize mates, spawn, and avoid potential predators, but not enough for small planktivorous fishes, requiring high visual acuity, to continue foraging. Twilight is also the time when predation by big fishes peaks. The threat from predation may partially explain why a towering reef structure is important in the mating arenas of some fishes. While spawning above the bottom, they remain close to a reef, where they can dart to shelter be- tween encounters, after spawning, and when disturbed by bigger fishes. Not all fishes, however, spawn at dusk. A number of fishes that typically build nests or produce many hun- dreds of eggs spawn during the daytime. For example, damselfishes and triggerfishes adhere eggs to the reef substrate in the daytime and vigor- ously protect their nests from all potential egg-eating fishes. The eggs hatch predominantly after sunset, the free-swimming larvae ascend in the water, and are gone from the nest before morning. Wrasses and parrotfishes also spawn during daylight but do not build nests. Instead, they broadcast many hundreds of eggs, possibly satiating any nearby planktivores. Eggs may also have less chance of being eaten if they are poisonous, such as those of some puffers, or if they float at the water's surface where few fishes feed. Mating Behavior of Pygmy Angelfish The Hawaiian pygmy angelfish, Cent ropy ge potteri, family Pomacanthidae, also known as Potter's angelfish, is endemic to the Hawaiian islands and found abundantly on coral reefs. Other Centropyge spp. are found on tropical reefs throughout the world. This fish's habitat includes two basic coral reef types. One is an extensive reef, a vast expanse of coral and rubble that fits the "usual" concept of a coral reef. The other, a patch reef, is usually smaller than 24 meters square and is isolated from other reefs by stretches of sand that resident fishes will not cross. The pygmy angelfish inhabits both types of coral reefs within the 3- to 50-meter depth range and is one of the ten fishes most commonly seen in this zone. The nature of the coral reef has an important effect on the mating organization of C. potteri. On patch reefs, males can control a well- defined territory, and the dominant male aggressively excludes other males. Consequently, there are two to four more females per male on patch reefs than on extensive reefs, where many territories are available and each male pairs with a single female. Males on patch reefs can, therefore, spawn more frequently than males on extensive reefs. Pygmy angelfishes are protogynous hermaphrodites: All individuals begin as females, and then the largest and behaviorally dominant female in a social group switches her sex to male. Males and females display some- what different color patterns in most angelfish species. Courtship is initiated by the male, who ceases feeding and begins courting about one hour before sunset. The male swims toward a female Off Hawaii, a pair of pygmy angelfish (Centropyge potteri) rise above the reef in the mating posture. The male is nuzzling the female's abdomen. Fall 1991 23 At the time of spawning, a pair of copper-banded butterflyfish CChaetodon multicinctus) is rushed In/ three sneaker males who release sperm and tJiereln/ steal fertilizations. in a vertical undulating manner unlike his normal swimming motion. He stops above her and erects all median fins while fluttering the pectoral fins. This display continues as the male drifts slowly upward with his head diagonally up or with his side parallel to the substrate. If the female fails to follow, the male halts immediately and darts back to her. The male continues courtship by swimming forward toward the female, while rising and falling in a swooping, fluttering motion. Courtship continues until the female is enticed to a prominent coral or rock tower and rises above the tower with the male. This usually requires only a few courting passes. Spawning occurs only over the tallest coral or rock in the immediate area. During courtship and spawning, the overall blue color of both fish pales as the red color intensifies. During the first few encounters, the female rises up with the male and then darts back to cover when the male attempts to move to the spawning position. The male pursues her while continuing his courtship display. During courtship, these fish make various clicking and grunting sounds whose precise role during reproduction is not yet known. Spawning climaxes when the female remains in midwater, about a meter above the coral /rock tower. The male approaches from underneath and appears to press his snout against her abdomen, perhaps to signal or facilitate egg release. A single burst of eggs and sperm is broadcast and floats away. Immediately after the release of eggs and sperm, the pair darts to cover with the female chasing the male, apparently nipping at his caudal fin. Chasing by the female occurs only after spawning and not during earlier episodes of courtship. Soon after sunset the fish retire for the night into a reef cavity. Mating Behavior of Butterflyfish Butterflyfish are renown for their beautiful coloration and long-term pair bonding. There are about 115 butterflyfish species distributed worldwide on tropical coral reefs. These fish mate with a single partner and main- tain a monogamous relationship for mating and feeding-area defense. I discovered an interesting twist to their sex lives when I observed ma- rauding single males intruding upon a mating pair and steal fertiliza- tions from the pair-bonded male. Most male and female butterflyfish species do not exhibit any immediately obvious sexually dimorphic color patterns. Females can only be distinguished with some certainty by a swollen abdomen filled with hyd rated eggs, which is most pronounced during the several hours before spawning. I made the first observations of mating butterfly fishes in Hawaii during 1975 and since then have studied one species in particular, the copper- banded butterflyfish, Chaetodon multicinctus, which is endemic to the Hawaiian islands and Johnston Atoll. At first look, the mating behavior of the banded butterflyfish conformed to the conventional model of pair-bonded species. A female, obviously swollen with roe, led the pair as they swam along the reef. As they swam, the female tilted her head slightly down- ward as she continued in front of the male. The male 24 Oceanus swam from behind and up alongside the female. As the male reached the female and placed his snout to her abdomen, both fish quivered and eggs and sperm were released. In one case, a male C. multicinctus ap- proached a female three times in this fashion before spawning. The butterflyfish spawning posture was strikingly similar to that described for Centropyge potteri. Again, the nuzzling by the male may signal the female to release eggs. During the first observation in 1975 of mating banded-butterflyfish pairs, I noticed other solitary fish following the breeding pair. Then after several years of field studies, I was utterly surprised during 1981 and 1982 observations to see solitary, intruder males rushing upon a mating pair and lining up behind the original male of a pair. The number of intruding (or sneaker) males lined up behind a breeding pair ranged from one to eight! It seems that the social structure of butterflyfishes is more complex than previously suspected! Mating Behavior of Hamletfish The hamlet is a particularly interesting fish because of a controversy concerning whether the genus Hypoplectrus consists of a single multicolored species or several different-colored, distinct species. The genus was consid- ered at one time to consist of nine species and three additional unnamed color variants whose only systematic difference was color pattern. Hypoplectrus is found throughout the tropical western Atlantic Ocean, and on any single reef several color variants commonly exist simultaneously. Mating usually occurs between individuals with the same color pattern; hybrid crossings are rare. One hypothesis suggests that these fish were aggressive mimics of common, nonpredatory reef fishes and that a stable population of polymorphs could have evolved without complete speciation, though some degree of reproductive isolation was necessary. Examination of the genetic relationships (by scientists at Scripps Institution of Oceanogra- phy) of the color morphs/ species indicated that all Hypoplectrus color rnorphs form a single species now known as H. unicolor. The reproductive behavior of Hypoplectrus is complex, involving particular courtship and spawning behaviors and a specific spawning Hamletfish arc simultaneous hermaphrodites. At left, the "two-spot" Butter hamlet (Hypoplectrus unicolor) /s in the female spawn ing position; at right, it has changed to the male position. Fall 1991 25 The sound is likely a signal to the spawning partner for coordinating simultaneous gamete release. site. The hamletfish, a simultaneous hermaphrodite, usually pair bonds with a single same-color-pattern partner. A pair typically spawns from several to a few dozen times an evening. Individuals spawn alternatively as male and female. The daily spawning period is restricted to the evening crepuscular period, about 45 minutes before and during sunset- twilight. Though other related serranids are well-known sonic species, I recorded the first H. unicolor sounds in 1988 while observing their spawning behavior. A few to several seconds before spawning the fish ready to assume the male role sounds a courtship call consisting of a series of sound pulses lasting 0.2 to 1.5 seconds. The fish taking the female role also produces a spawning sound that is acoustically distinct from all other fish sounds reported so far in the literature. It consists of two discrete parts: an FM downward tonal sweep followed by a broadband sound that occurs upon egg release. This sound may have originated partly as a byproduct of the mechanics of egg extrusion abdominal muscle con- traction that forces the eggs out may also cause the swim bladder to vibrate. During the broadband sound production, the female vigorously flutters her pectoral fins while rapidly and repeatedly contracting her abdominal muscles. This behavior and sound production are synchro- nous and last about 1.5 seconds, after which the pair abruptly breaks apart and each dashes downward to the reef substrate. The mechanism of sound production by Hypoplectrus probably involves the movement of the head and pectoral girdle muscles as well as the sonic swim bladder muscles. Movement of the pectoral girdle muscles was clearly evident from the rapid fluttering of the fish's pectoral fins. The biological func- tion of the spawning sound is likely a signal to the spawning partner for coordinating simultaneous gamete release, possibly maximizing external fertilization of eggs by sperm mixing in the water. Turbulence created by the fluttering fins may also enhance mixing. Interestingly, the spawning embrace of the hamletfish is such that the partners face in opposite directions. Hamletfish spawn when large, predatory fishes are particularly active. This position may provide the greatest sphere of visual awareness for the pair, but it also places the fish in a posture that separates their genital vents. If they were positioned so that their genital vents were closely aligned, it would result in both fish looking one way and leaving their backs vulnerable. These few examples provide only a glimpse into the many variations of reproductive style in coastal marine fishes. The state of the art is still largely descriptive, with the major effort focused on the discovery of where, when, and how fishes breed. Recent technical advances in underwater acoustic-video instrumentation have proved to be enlighten- ing and demonstrate how our knowledge can be hampered by the limits of our own sensory capabilities. Phillip S. Label is an Associate Scientist in the Biology Department at the Woods Hole Oceanographic Institution. His current research focuses on the spawning behavior and sounds of fishes. His field research is conducted mostly at Johnston Atoll in the central Pacific Ocean, with occasional forays to the Caribbean and Africa. 26 Ocean us Sex (and Asex) in the Jellies Katherine A.C. Madin and Laurence P. Madin ife on earth began in the ocean, and its greatest diversity is still found there. Plankton, organisms that swim weakly or drift with the currents, live in the largest ocean habitat, the water column. Zooplankton, the animal portion of the plank ton, includes everything from single-celled protozoans to fishes, all adapted to living in vast three-dimensional spaces. Some of them are gelatinous their jellylike tissues are about 95 percent water, and they have no hard skeletal elements. Their lucid transparency endows them with other worldly beauty to the eyes of human behold- ers and invisibility to the eyes of many predators. Though from many different phyla, these animals have a constella- tion of characteristics in common. Their similarities in locomotion, buoyancy, feeding behavior, and reproduction represent like adaptation to their oceanic habitat. Here we will describe a remarkable reproductive strategy that contributes to the ecological and evolutionary success of two seemingly disparate groups of gelatinous zooplankton, the cnidarians and the tunicates. Much of the basic zoology of gelatinous organisms was revealed by patient naturalists of the 19th century. More recently, the use of scuba diving and research submersibles to study this fragile fauna alive in the ocean has brought exciting new discoveries about their distribution, behavior, and physiology, and led to a renewed appreciation of their ecological importance. Doliolids are colonial tunicates with a complex and fascinating system of reproduction. This "old nurse" oozoid is pulling a long tail of gastrozooids and phorozooids. Although they are from different phi/la, planktonic cnidarians and tunicates share many common adaptations. Fall 1991 27 Most hydrozoan cnidarians, such as Leuckartiara octona, alternate between a sexually reproducing form, the uiedtisn sliouui, and an asexualh/ reproducing form, which is a polyp (see tJie diagram at right, top). Jellyfish, often seen stranded on the beach or drifting past a boat, are probably the most familiar planktonic cnidarians. Large popula- tions of jellyfish often appear suddenly in bays or harbors in the spring or summer and can be a nuisance to boats and beachcombers, a difficulty to net fishermen, and a hazard to swimmers because of their stings. In Chesapeake Bay, large summer populations of the sea nettle Chn/saora make swimming nearly impossible. On Austra- lian beaches, the sting of the sea wasp Chironex can be fatal. These sudden population explosions are due in part to the jellyfish's mode of reproduction: they alternate between sexual and asexual generations. The familiar umbrella-shaped jellyfish, called a medusa, is the sexually repro- ducing form. It alternates with the smaller and less conspicuous polyp, a cylindrical, bottom- dwelling animal that looks like a tiny sea anemone. The medusoid generation produces eggs and sperm that will develop into polyps. The polyp generation reproduces by asexual means to form more medusae, and it is usually then that great population increases occur. As singular as this reproductive methodol- ogy may seem, there is another group of gelati- nous zooplankton that does essentially the same thing: the pelagic tunicates. These are transpar- ent, barrel-shaped members of the class Thaliacea, a subdivision of the phylum Chordata (to which we verte- brates also belong). Although far from jellyfish on the evolutionary spectrum, they have evolved a strikingly parallel adaptation to plank- tonic life. Alternation of Generations Many animals (such as some starfishes, flatworms, and segmented worms) that usually reproduce sexually are also capable of asexual reproduction. In these cases, the type of reproductive method an animal uses depends on its maturity, health or nutritional state, the proximity of others of its species, or environmental factors such as season, tempera- ture, or length of day. The same individual is usually capable of both sexual and asexual reproduction, under different conditions, or perhaps at different times of life. By contrast, in these two types of gelatinous zooplankton, sexual and asexual reproduction follow one another in a regular pattern of alternating morphologies (medusa and polyp) and, sometimes, habitats. The basic alternation cycle has been varied by different species of cnidarians and tunicates into life histories so different from the vertebrate norm that they sometimes seem more like creatures of outer space than of inner space. 28 Occnnus fertilized egg adult medusa Jellyfish and Their Kin Jellyfish are the planktonic medusoid generation of the phylum Cnidaria (named for their stinging cells, called cnidae or nematocysts). The Cnidaria comprises three classes, the Hydrozoa, Scyphozoa, and Cubozoa, and each class employs different ways of alternating between sexual and asexual generations. It is simplest to begin with the general- ized life cycle of a hydrozoan as a "typical jellyfish." A hydrozoan medusa is small, delicate, and transparent; drifting with the currents and water masses, it acts as the dispersal stage of the species. A planktonic predator, the medusa uses its tentacles and cnidae to capture smaller zooplankton prey. Male and female medusae grow to produce sperm and eggs that are usually shed into the water, often synchronously (simultaneously with other hydro- zoan medusae) within a local population. Fertilization is usually external, and a fertilized egg grows into a ciliated larval form called a planula. This planktonic larva eventually settles on a firm surface such as a rock or wharf, and develops into a polyp. The polyp feeds and grows, often budding off other, connected polyps to form a colony that may eventually include hundreds or thousands of individual polyps. At maturity, the polyps bud off small individual medusae, releasing them into the water to drift off and grow up. Scyphozoan jellyfish are generally firmer, more opaque, and much larger than hydrozoan medusae; for example, Cyanea, the Lion's Mane, can reach 2 meters in diameter. Scyphozoans also produce eggs and sperm, resulting in planula larvae. A planula settles on a suitable surface, develops into a polyp called a sci/phistoma, feeds, grows, and may bud off other polyps asexually. When it is mature and conditions are right, the polyp undergoes a process called strobila- tiou, a tissue reorganization that transforms part of its body into a stack of tiny medusoid forms called ephyrae. The ephyrae then break small medusa medusa bud -*' fertilized egg adult jellyfish liberated ephyra ephyrae "Typical" life cycles for two classes of cnidarians, the Hydrozoa (top) and Scyphozoa (bottom) illustrate some of their many similarities in alternating between sexual and asexual reproduction. planula hydroid colony scyphistoma Fall 1991 29 Variations on the "typical" patterns abound. Medusae usually reproduce sexually, however, they may also reproduce asexually. Aequorea (left) is in the process of fissioning into three daughter medusae, while Arctapodema broods small medusae that were likely budded from its gonads. Arctapodema has no known polyp stage. away one at a time and grow into adult jellyfish. As in the Hydrozoa, seasonal synchronous reproduction, in this case by strobilation, produces the sudden production of massive jellyfish swarms. Reproduction in the cubozoan medusae (sea wasps or box jellyfish) is not well understood. These large (up to about 20 centimeters) and very toxic medusae also alternate between medusa and polyp, but the solitary polyp is thought to metamorphose directly into a single medusa to complete the cycle. In this case, population increase must occur in the sexual medusa stage. This may be why cubozoans are the only jellyfish known to ensure fertilization by copulating. Complications and Simplifications Of course, not all planktonic cnidarians follow this "typical pattern." Life histories have been written for only a handful of some 1,000 known species of medusae, but even these show a number of variations on the alternating pattern. Most fall into three categories. Budding or Fission. Some medusae reproduce asexually by budding or fission, in addition to producing gametes. Some bud polyps that remain attached to the medusa and then produce new medusae, bypass- ing the planula and benthic hydroid stages. Others simply bud medusae directly from various parts of their bodies; sometimes the newly budded jellyfish develop even tinier buds of their own while still attached. There are even more direct modes of asexual reproduction; for instance, the hydrozoan Aequorea , while it can reproduce sexually, can also reproduce by asexual fission of the entire adult medusa: It simply splits itself into two or more parts. The unusual Mediterranean hydrozoan Euclieilota paradoxica displays most of these variations. Its temperature-dependent life cycle has only recently been described. In warm water, it buds small daughter medusae along its radial canals. When temperatures fall below 18C, the medusa produces dormant frustules that will develop into polyps when the water warms again. But if temperatures reach 15C, a most amazing metamor- phosis occurs: A polyp buds off from the medusa's gonadal tissue and grows as the medusa regresses, until the one is almost entirely trans- formed into the other. Asexual reproduction is less common in scyphozoan medusae, but the 30 Oceanus Hydromedusa gonads radial canal manubrium mouth velum tentacles oral arms Scyphomedusa Hydrozoan and Scyphozoan Anatomy deep-sea medusa Stygiomedusa fabulosa, which attains a diameter of 1.5 meters, is both asexual and viviparous (live-bearing). It buds small medusae from germinal tissue near its stomach, and then broods them in its gastric pouches until they are developed enough to live on their own. This strategy may be particularly important in the deep sea, where prey organisms are scarce and larger size is an advantage. Complete Absence of a Polyp Stage. Some groups have "lost" one entire generation. The scyphozoan Pelagia, whose populations can reach enormous numbers in the Mediterranean Sea, has no polyp stage; its gametes develop directly into planulae, then ephyrae, then adult jelly- fish. This is also true for the entire hydrozoan order Trachylina, com- monly found in open ocean and deep-sea habitats. They reproduce only sexually, and the planulae metamorphose directly into medusae. In some species the developing medusae are brooded within the bell of the parent until they are large enough to swim and feed independently. A bizarre twist on brooding is found in some species whose larvae are brooded in the gastrovascular cavity of another species. Once inside their hosts, the young may bud off additional larvae, all of which develop into small medusae. How they locate their foster parents remains a mystery. Connected Polyp and Medusa Stages. Even when both medusa and polyp stages occur, the two may not separate, but remain connected, with one stage subordinate to the other. In some hydrozoans, a colonial polyp stage is predominant and the small medusae that are produced remain attached to the colony as elaborate gonads. A more impressive example is the hydrozoan order of siphonophores. These aren't single medusae, but complex assemblages of several types of both medusae and polyps, con- nected and coordinated into single functional units that can take varied, fantastic, and beautiful shapes. The Portuguese Man-O'-War Physalia is the FaU1991 31 Siphonophores arc intricate assemblages of different ti/pes of medusae and pol\/ps coordinated into single functional units. As Physophora hydrostatica reveals, these col 01 lies can assume fantastic shapes. Compare this to the doliolid coloni/ on page 27. best-known example, but all are predators with long fishing tentacles that are well equipped with nematocysts. In siphonophores, several types of zooids (individual ani- mals that are part of the colony) have taken specialization very seriously. Arising by metamorphosis and budding of the original planula larva, the colony soon includes a gas-filled float, or pnciimatophore, and two kinds of modified polyps: gastrozooids, whose sole function is prey capture, and dactylozooids, whose batteries of nematocysts defend the colony. Attached modified medusae include nectophores, swimming bells that don't feed but exist only to propel the colony through the water, and gonophores, sexually reproduc- ing individuals that correspond to the free-living medusae of other hydrozoans. The gastrozooids, dactylozooids, and gonophores, together with protective structures called bracts, form quasi-independent clusters or cormidia, arranged along a central stem and all pulled along by the nectophores. Cormidia sometimes break off as free-swimming eudoxids, ap- parently to further disperse the sexual gonophores. Eggs and sperm liberated from gonophores unite to form planulae. Each planula develops into a siphonula larva bearing a rudi- mentary float, a tentacle, and a gastrozooid. This is the pre- cursor to the siphonophore colony, budding off all the other zooid types as it grows. Some of this type of colonial form and organization is eerily echoed in the doliolid tunicates. Reproduction in Thaliacea Common benthic tunicates known as sea squirts are often seen on rocks or piers. Their open-ocean relatives, the thaliaceans, are much less familiar, but ecologically important members of the offshore gelatinous plankton. The two orders of pelagic tunicates considered here are transparent, barrel-shaped animals that occur either singly or fastened together in long chains. The individuals are called zooids, as in the Cnidaria, and range in size from less than 1 to 30 centimeters. The chains may be a few centimeters to many meters long. Snips exhibit a more clear-cut alternation of generations, so we use them to illustrate a generalized life cycle for pelagic tunicates, and then compare the more elaborate reproduction of their relatives the doliolids. Salps. Salps show a strict pattern of alternating sexual and asexual reproduction. This remarkable life history, when first reported in 1819 by the poet /naturalist Aclelbertus von Chamisso, was discounted as too fanciful to be believed! One form of adult salp is called the solitary generation. These swim about individually, filtering food through a mesh of mucus suspended within their bodies. As they mature, a strand of tissue called a stolon grows from the salp, subdividing into small daugh- ter salps that are connected like paper dolls. These zooids, the aggregate generation, break off from the parent, but are still connected to each other in whorls, clusters, or chains. Aggregate salps are protogynous hermaph- rodites (first female, then male) and are viviparous. When budded from the stolon, each daughter salp contains an egg enclosed in an ovary. Very soon after the aggregate chain breaks off from its parent salp, these eggs 32 Oceanus are fertilized by sperm from older aggregate salps that have become males. Fertilization is internal and the zygote develops directly into a small embryo of the solitary generation, nourished through a placental connection to its mother. After the embryos are born, they continue to grow into the asexual solitary generation, and their former mothers become future fathers. Doliolids. If the description of the salp life cycle is too fantastic to be believed, then that of their cousins the doliolids must seem to be pure invention. Doliolids are similar to but smaller than salps. Highly trans- parent and delicate, these rapid swimmers are sometimes found in dense swarms in coastal waters. Reproduction in these organisms is like a set of complicated variations on the salp's theme, with multiple, specialized zooids arranged in a cycle of sexual and asexual, colonial and solitary forms. The generalized life cycle that follows is based on descriptions of several Mediterranean species. Sexual, hermaphroditic adults called gonozooids produce eggs and sperm, and fertilization results in a free-living, motile larva enclosed in a jelly capsule. A simple notochord (believed to be a primitive spinal column) in the temporary tail of these larvae is the structure that fleet- ingly links the thaliaceans to the chordate phylum. The larvae lose their tails and capsules and develop into oozooids, asexually reproducing stages analogous to the solitary generation in salps. Like the larval siphono- phore, the oozooid then begins a budding process that leads to a polymorphic colony containing thousands of zooids and sometimes attaining a meter in length. From this point on, doliolid re- production gets complicated. A sto- lon (like that of salps) near the heart divides transversely into prebuds in a process called strobilation (recall- ing scyphozoan polyps). Motile cells near the stolon carry the prebuds over the surface of the parent's body and onto a tail-like appendage at the rear of the oozooid. There, as their number increases and the tail elon- gates, the prebuds arrange them- selves into two lateral and one cen- tral double column. The buds on the two sides of the tail will become gastrozooids, and collect food for the colony by filter feeding. Along the axis of the tail the buds will become phorozooids, a generation of nonreproducing individuals that eventually break away and disperse the sexual stages, and probuds, which migrate onto the phoro- zooids, elongate, and bud off the next generation of gonozooids. As the salp Pegea socia matures, a stolon grows (top) that will later subdivide into a chain of connected, small, daughter salps, called the aggregate generation. Each daughter has an egg enclosed in an ovary that is later internally fertilized. If all goes well, it will develop into an embryo of the solitary generation (bottom). Fall 1991 33 SIPHONOPHORE nectophore cnidae batteries gastrozooids cormidium Schematic illustrations of the polymorphic colonies ofsiphono- phores and doliolids reveal their many similarities. The swimming bell is at the top of the siphonophore Muggiaea atlantica, and zooid clusters along the stem are maturing in proportion to the distance from the bell. The cormidium will event ualh/ be released as a eudoxid, as shown at the bottom. (After Chun, 1882.) As they develop, the colony members become as specialized as the zooids of siphonophores. Hav- ing produced the "tail" of budded zooids, the original oozooid loses its feeding apparatus, resorbs its inter- nal organs, and becomes an old nurse, pulling the colony through the water by jet propulsion. The gastrozooids' only job is to feed themselves, the nurse, and the de- veloping buds in the middle row of the colony. Once grown, the phorozooids break off from the mother colony and swim away to feed and nourish the little clusters of gonozooid buds. When these are large enough, they too break away, and, as individuals, feed, grow, and eventually produce eggs and sperm to complete the cycle. Why All the Complexity? There is only a remote phyloge- netic kinship between the cnidarians and the tunicates. Medusae and polyps are among the simplest of animals, character- ized by radial symmetry, few tis- sue types, and carnivorous feed- ing. Thaliaceans are far more advanced, with bilateral symme- try, well-developed muscular and nervous systems, and a complex mechanism for filter feeding on phytoplankton. Yet with few exceptions elsewhere in the animal kingdom (various internal parasites such as trematodes and cestodes and a very few insects), reproduction by alter- nating sexual and asexual generations, and the development of polymor- phic colonies, is found only in these two otherwise disparate groups. Though the cnidarians are far more plastic and varied in their approach to alternation, and while all thaliacean groups follow a fixed, alternating pattern, and though alternating generations and coloniality are adaptive for different reasons in the internal parasites, these striking similarities in the physical forms and life histories of cnidarians and thaliaceans clearly relate to their common habitat, the water column. Successful reproductive adaptations for planktonic life vary accord- ing to the specific habitat. For hydrozoans and scyphozoans with benthic polyp stages, alternating generations provides the capacity for enlarging the population by budding (from polyps), and for dispersal and genetic recombination (by medusae). This works well for near-shore species where benthic and planktonic habitats are physically close together; polyps can produce a flood of medusae to take advantage of seasonal gonophore t eudoxid 34 Oceanus nurse gastrozooids DOLIOLID food resources and to disperse the species throughout its range. But for open ocean species that live far from benthic habitats, alternatives to an obligate return to the bottom are preferable, and here we see the benthic stage bypassed by di- rect sexual or asexual production of new medu- sae from old ones. The wholly planktonic salps and doliolids have left their benthic stages be- hind in evolutionary history, but still keep both generations in the plankton. Adaptations such as budding, brooding, and viviparity yield the further advantage of providing parental protection and nourishment to developing offspring. It's not sur- prising, then, that we see these strategies in the pe- lagic tunicates and in jellyfish like the deep-sea Stygiomedusa that live in food-poor environments of the open ocean and deep sea. Supporting offspring is also the point of the elaborate colonies produced by siphonophores and doliolids. Asexual budding produces assem- blages that are huge compared to individual zoo- ids (some siphonophores reach 100 feet long), all apparently to provide nutrition to the tiny but es- sential sexual gonophores or gonozooids that are sometimes (siphonophores) or always (doliolids) liberated from the colony. The parallels in organi- zation of the two types of superorganisms are in- deed remarkable. The divisions of labor within the colonies include nectophores or old nurses for locomotion, gastrozooids (meat-eating or veg- etarian) for nutrition, eudoxids or phorozooids for secondary support and dispersal, and, even- tually, gonophores or gonozooids for producing gametes. Each type of zooid has evolved to fulfill a specific role, and the sculpting hand of natural selection can also be seen in the coordination and shape of the entire colony. In ecological and evolutionary terms, reproduction of the species is the reason for existence of plants and animals. What seem to us to be bi- zarre ways of going about it have evidently served these animals well for a very long time, and may continue to do so long after human zoologists have passed from the scene. phorozooids sonozooid buds K.A.C Madin Katherine A.C. Madin, an invertebrate physiologist, is a Guest Investigator of the Department of Biology at the Woods Hole Oceanographic Institution (WHOI). Her interests are planktonic and intertidal organisms. Laurence P. Madin is an Associate Scientist in the Department of Biology at WHOI, where he pursues in-situ studies on the distribution, ecology, and behavior of open-ocean and deep-sea zooplankton. The "old nurse" oozoid is at the top, and gastrozooids and immature phorozooids form a long tail (shown much shorter here) of this doliolid colony. The maturing phorozooids, with their cargo of developing gonozooid buds, break off and develop into the gonozooid at the bottom. Fall 1991 35 orms. . . id's Fan Dance leaves ishine most prevails ianced wings and tails Floating to Itywer levels, So may one see these larval mites Press upwards towards the brighter lights And, for the counterpart, Flick out, like fans, their tufts extended And, as on parachutes suspended, Fall slowly to the start. Is it, as there, just playtime zest? More probably, be it confessed, Their mode of food collection: For diatoms crowd up aloft, And movements that are soft and smooth Can best escape detection. Now equatorial water warm Present against a sinking form A much reduced resistance: A North Sea creature falling there, Without some compensating care, Would drop through twice the distance. So tropic Mitraria drifting down There spread not bristles but a crown Of broad and gleaming blades, Which some say give protection martial, But we to seem not over-partial Will call fanfaronades! The Nauplius and Protaspis The Nauplius is a wobbly thing, a head without a body: He flops about with foolish jerks, a regular Tom-noddy. Some said he was an ancestor, but others said: "What HIM? He's just a Nectochaeta with Crustacean skin and limb!" These poems are excerpted from Larval Forms with Other Zoological Verses, by Walter Garstang 1951 Basil Blackwell, Oxford, UK and 1985 University of Chicago Press, Chicago IL and London UK. Reprinted with permission of Blackwell Publishers. 36 Ocean us The Ballad of the Veliger, or How the Gastropod Got its Twist The Veliger's a lively tar, the liveliest afloat, A whirling wheel on either side propels his little boat; But when the danger signal warns his bustling submarine, He stops the engine, shuts the port, and drops below unseen. with Zoological Verses by Walter Garstang Illustrations by Rudolf Scheltema The Trochophores The Trochophores are larval tops the Polychaetes set spinning With just a ciliated ring at least in the beginning They feed, and feel an urgent need to grow more like their mothers So sprout some segments on behind, first one, and then the others. And since more weight demands more power, each segment has to bring Its contribution in an extra locomotive ring: With these the larva swims with ease, and, adding segments more, Becomes a Polytrochula instead ofTrochophore. Then setose bundles sprout and grow, and the sequel can't be hid: The larva fails to pull its weight and sinks an Annelid. Fall 1991 Tornaria's Water-Works Of all the sea-jellies that dazzle the eyes, Whose motions delight and whose forms surprise, Two are outstanding, the gay Ctenophore And the modest Tornaria: these hold the floor. For symmetry, fitness, and manifold graces Their eminence shines in the watery spaces: Whether waltzing or gliding or poised quite still, No others display such perfect skill. But if I must for one the other relinquish, And the premier star of the pair distinguish, From a standpoint of sheer architectural beauty A naturalist must, I think, feel it a duty Of all the sea-jellies that dazzle the eyes To give to Tornaria the highest prize. 37 Although we know quite a lot about the species, until recently we had no idea how it reproduced. This article is excerpted from Living Fossil: The Story of the Coelacanth, 1991 Keith Stewart Thomson, and is reprinted with permission of the publisher, W.W. Norton & Company, Inc./Liverright Publishing Corporation. The Story of the Coelacanth Reproductive Biology Keith Stewart Thomson omewhere below the surface of the Indian Ocean, along the steep sides of Grande Comore and Anjouan islands, lives at least one population of coelacanths. They swim, breathe, and feed in the currents that sweep along the island bases. We do not know how many fish there are. And although we know quite a lot about the species, until recently we had no idea how it reproduced. Latimeria's survival can hardly be considered secure. We are not sure of where it lives, how many there are, or what the rate of addition to the population(s) is through reproduction, or the loss through predation. We certainly do not know, although we should be concerned, what the effect of human predation (fishing) upon this species is. These facts of life make it critically important that we learn about the reproductive biology of Latimeria. Amphibians usually lay eggs into the water, although they are often attached to plants and protected by a "jelly" coat. But many species pro- tect them in other ways, the midwife toad carrying the developing eggs around on its back rather like the sea horse. Reptiles and birds lay only a few eggs, each protected with a special shell and endowed with lots of yolk. In live-bearing fishes one usually sees a particular strategy called ovoviviparity (egg-live-bearing), in which the female retains the eggs in her reproductive tract and protects them so that they grow up inside her body, being released at the "hatchling" stage. Ovoviviparity, like any form of live bearing, obviously requires in- ternal fertilization by the male and an egg with a good yolk supply. The essential respiratory gases, oxygen and carbon dioxide, pass through the egg membranes. Certain food materials may in fact be available inside the mother through simple transfer front the uterine environment (ab- sorption or swallowing of uterine secretions, for example), but basically the egg is self-supporting while it remains inside the mother. The extreme in live bearing is the development of a special set of tis- sues that connects the developing embryo with the tissues of the mother, for nutrition and removal of waste materials. This is the adaptation that makes advanced mammals the placental mammals so successful. The placenta is a special set of tissues developed for embryonic support and nutrition, and it is shed as the afterbirth when it is no longer needed. There is one last and very curious variation on this set of themes of 38 Ocean us *w "viviparous" embryonic development in fishes. In a few sharks (for ex- ample, the mackerel shark Lamna cornubica ) the embryos may feed cannibalistically on immature eggs or even on one another while within the uterus. What do the lungfishes, the closest living cousins of the Latiuicria, do? Lungfishes make nests. All three genera scoop out depressions in the bottom where the water is shallow and lay large, yolky eggs. The male fertilizes the eggs in the nest by shedding its sperm onto the eggs as the female releases them. This requires a special courtship behavior to en- sure perfect timing, for the sperm will not live for long independently in the water. In the African genus Protoptents the male guards the nest and may beat the water with his tail to scare away predators and perhaps to aerate it. Like amphibians, lungfish larvae have external gills, and in their reproductive behavior lungfishes generally act much like primitive amphibians, the cousins of both lungfishes and coelacanths. As for the coelacanths, up to 1975 the evidence was confused. As we have seen, there was quite good evidence that at least one fossil genus was a live-bearer. In these Jurassic fossils there is a smallish number of obviously highly immature individuals within the abdominal cavity, and they are positioned too far back to have been stomach contents. When Professor Watson described the specimens, there was general agreement that this coelacanth at least was a live-bearer, a not particularly suprising view considering that live bearing is reasonably common in all groups of fishes. The fossil evidence could never be conclusive, of course, but Watson's interpretation lasted for 50 years. The ninth coelacanth to be caught (February 12, 1955) was a female with a swollen ovary containing "about ten ovocytes" (unshed eggs) of one to two centimeters in diameter. Number 18 (January 1, 1960) was a very badly preserved specimen, but on dissection it had rather more fully developed eggs in the ovaries, one egg being seven centimeters in diameter, and was thought to be ripe "vraisemblement en cours de ponte." These were the first coelacanth eggs to be seen. And for the first time the suggestion was raised that perhaps Latimeria was simply an egg-laying fish. Although there is no sign of a shellforming gland in the female reproductive J.L.B. Smith' s formal photograph of Latimeria has an arrow indicating the position of a structure called the spiracular organ, and the torn rear margin of the first dorsal fin has been shaded in. This photo was probabh/ taken in 1939. (Courtesy Department of Library Services, American Museum of Natural History; negative number 124485.) Fall 1991 39 But how could such a large egg, the largest egg of any known fish, be shed into the water with so little protection? tract, eggs as big as seven centimeters should need protection. The detailed dissections of the French group showed nothing in any of the female speci- mens to suggest that they were live-bearing. Indeed, as there is also no obvi- ous intromittent organ in the male, the possibility of live bearing seemed ruled out. Latimeria was therefore thought to be oviparous: "nous avons pus nous assurer. ..que las reproduction est ovipare." The question then lay largely unaddressed until 1972. Members of the 1972 expedition by the Royal Society, National Geographic Society, National Academy of Sciences, and Musee National d'Histoire Naturelle were lucky enough to be present when a large female specimen of Latimeria was brought in. This specimen proved to be gravid, containing 19 huge eggs that had already been released from the ovaries. There was no evidence that de- velopment had been initiated. Further, the eggs had only the very thinnest of membranous coatings, and they were fluid to the touch. There was no sign of their being attached to the oviduct. The more scientists involved thought about this, the stranger it all seemed. The French had already shown that there were no shell glands as- sociated with the oviduct and, therefore, no way for the female to protect the egg with a tough case. But how could such a large egg, the largest egg of any known fish, be shed into the water with so little protection? How could it survive? Perhaps the eggs were normally laid into a nest, as is the case in lungfishes. Fertilization would occur by the male coming to shed its sperm on them. Then the delicate eggs must have been very closely guarded by one or both parents. In any case, the discovery of this heavily gravid female seemed to be evidence that the fossil specimens might have been mistakenly interpreted by Watson. Probably it was a case of can- nibalism after all. Latimeria at least did not seem to be ovoviviparous. Al- most immediately thereafter Hans-Peter Schultze described some tiny fossil specimens of the Carboniferous coelacanth Khabdoderma that were actually very immature young with yolk sacs attached. These specimens occurred in a significant size range and seemed to represent young hatchlings at the yolk-sac stage. This seemed to be further evidence that the eggs were laid into a nest or the open water and that the young fry, with the yolk sacs at- tached, developed out in the open. Schultze stated: "This proves that the coelacanth is oviparous." But Robert Griffith, who had been a member of the 1972 expedition and was present at the dissection of that first gravid specimen and who was a student of Professor Pickford and myself, continued to worry about those eggs. He is a tall man, slow-speaking and quick-witted. Bob's idea of torture is having to wear a coat and tie. Periodically he would sit down in my office and say, "I don't believe it." Gradually he built up an argument that Latim- eria must be ovoviviparous after all. He and I published this theory together in 1973, although I wish to emphasize that credit largely goes to Bob Griffith. It seemed crazy to many people, but it was an argument based on established comparative data, so we decided to stick our necks out. The argument is as follows. Large eggs of the size found in Latimeria are found elsewhere only in fishes like sharks that are ovoviviparous. An egg that size is never laid without a shell. Latimeria is a ureotelic fish, meaning that it osmoregulates by a mechanism of urea synthesis and retention, as, again, do sharks. There is a special connection between ureotely and 40 Oceanus ovoviviparity in sharks, for the following reason. The specialized adaptation of urea retention may come fully into operation only rather late in develop- ment. Before it does, the young are constantly at risk of lethal osmotic imbal- ance because the outside seawater is more concentrated than the embryo blood. The only way to prevent this is to surround the egg in a closed, con- trollable environment. Sharks do this either by means of laying their eggs with the protection of tough egg cases (creating a closed mini-environment) or by means of ovoviviparity (in which case they grow up within the mater- nal environment). For example, the large six-gilled shark Hexanchus, which is found at the same depth as Latimeria, is ovoviviparous. Therefore, if Latimeria is so much like a large shark in all other respects, especially ureotely, and does not produce a tough egg case, the fish should be ovoviviparous. In that case, how could fertilization occur? One possibility is that the structure of curious folds and tubercles around the external genitalia of the male actually constitutes some kind of erectile intromittent organ. But it also has to be pointed out that many vertebrates have internal fertilization with- out intromission. Many amphibians fit this category. In the common Euro- pean newt Tritums, for example, the male courts the female with elaborate wriggling movements and pheromone secretions, and she positions herself next to him. He deposits his sperm in a gelatinous package, and she slides alongside, places her cloaca over the package, and picks it up. The gelati- nous material dissolves, and the sperm swim up into the oviduct. There seems no obvious reason why Latimeria could not do the same. But the trouble is the usual one: no direct evidence. Quite inadvertently the puzzle was solved. Ichthyologists at the Ameri- can Museum of Natural History in New York decided to dissect their big fe- male specimen. This was specimen number 26, acquired by the museum in 1962. The fish had a checkered history. It was caught off Anjouan on Janu- ary 8, 1962, but the name of the fisherman was not recorded. Dr. Garrouste, the physician on Anjouan who was so instrumental in preserving the first French specimens caught in 1953, obtained the fish (presumably direct from the fisherman), bypassing the governmental channels. He first offered to sell the fish to J.L.B. Smith in South Africa. Smith decided that he did not want it but knew that the American Museum of Natural History would. Bobb j Schaeffer was then head of the Department of Vertebrate Paleontology at the museum and very much wanted the specimen. At first it was difficult to arrange the transfer because the French authorities did not want Garrouste to sell it. Finally they released the fish in exchange for a thousand dollars of medical supplies for Garrouste, donated by a patron of the museum. In 1975 Charles Rand, a hematologist on the faculty of Long Island University, wanted to get tissue samples from the spleen of a coelacanth for comparative purposes. Since so many other coelacanth specimens had by that time been dissected and used for research and, indeed, other superficial dissections of this specimen had already been made at the museum, the old injunction that it could be used only for display was obviously inoperative. When C.L. Smith from the department of ichthyology at the museum and Rand opened up number 26, to their amazement, they found five al- most fully developed young Latimeria inside the swollen oviduct, each with the remnants of a large yolk sac still attached. Each was nearly 30 centimeters long, and the yolk sac still measured 6 centimeters. Quite inadvertently the puzzle was solved. Fall 1991 41 The swollen uterus of specimen number 62 contained five 35- centimeter embryos like Hits. (Courtesy Department of Library Services, American Museum of Natural History; negative number 66637.) Latimeria is indeed a live-bearer, so Professor Watson must have been right about the fossils after all. We do not know at what size the young are born and whether they are born with any remnant of the yolk sac still attached or whether it has all been resorbed by that point. A 43-cen- timeter specimen, presumably free-swimming since it was caught by a hook and line in 1973, showed no sign of a yolk sac, so all we know is that they are borne at a size somewhere between 30 and 43 centimeters. The Carboniferous fossils that Schultze had described as free-living yolk sac larvae were from a genus (Rhabdoderma) that may have lived in brackish waters rather than the sea. In this case (if the water was less sa- line than the body tissues) it is possible that ovoviviparity was not needed, but economy of hypothesis suggests the strong likelihood that this genus was ovoviviparous also. When our 1969 expedition caught the shark Hexanchus in the western Indian Ocean, we would occasionally take a gravid female. The highly stressed fish would shed its embryos onto the deck when it was heaved on board. Perhaps these fossil em- bryos of Rhabdoderma were also shed by stressed females, dying in the swamps of ancient coal deposits. Of the five coelacanth babies discovered at the American Museum of Natural History, one was given to the British Museum (Natural History), and one was given to the Musee National d'Histoire Naturelle in Paris in exchange for an adult specimen (number 25, a male). One specimen was sent to the Children's Hospital of San Francisco to be specially serial-sec- tioned, which means that it would exist in the form of a complete series of microscope slides, each representing a slice a few thousandths of a millimeter thick. This series of slides would enable students to see the finest details of anatomy at any point in the body and to reconstruct, for example, the finest details of nerves and blood vessels passing through the organs. (This project has unfortunately stalled and is incomplete.) One of the specimens remaining at the American Museum has been pre- pared by a special method that renders the soft tissues transparent and reveals minutiae of the internal skeleton. The last specimen has been pre- served intact. At last the puzzle of reproduction in Latimeria has been solved and another hypothesis based on reasoning from indirect data has come out right. Recently James Atz of the American Museum and John Wourms of Clemson University have added a final new wrinkle to the story by sug- gesting that Latimeria might in fact show the odd "cannibalistic" feeding 42 Ocean us of the young on unfertilized eggs, as in sharks like Lamna. For all our euphoria at confirming what seemed at the time to be a daring hypothesis, in one very important respect all this new informa- tion about the mode of reproduction in Latimeria is alarming. Because the gestation period for Latimeria must be quite long, perhaps as long as a year, the rate of renewal of the small population would necessarily be slow. And because the female is single-handedly responsible for the well-being of a small number of live young, rather than huge numbers of eggs, any time a female is caught there is potential for significant reduc- tion of the capacity of the population for renewal. We may have discov- ered an important vulnerability of the living coelacanth. Keith Stewart Thomson, a biologist, is the Chief Executive Officer of the Acad- emy of Natural Sciences of Philadelphia, a corporate member and trustee of the Woods Hole Oceanographic Institution, and a past dean of the Graduate School of Arts and Sciences at Yale University. His research interests include vertebrate biology and evolutionary theory, especially the Devonian transition between fishes and tetrapods, and the history of Darwinism. Living Fossil: The Story of the Coelncnntli is available at bookstores or it can be ordered directly from the publisher by sending a check or money order for $19.95 US per copy, post paid, to: W.W. Norton & Company, Inc. 500 Fifth Ave New York, NY 10110 (NY and CA residents, please add sales tax) We may have discovered an important vulnerability of the living coelacanth. Oceanus Oceanus Oceanus Oceanus Oceanus Oceanus Oceanus Attention Students & Teacher s\ Interested in an internship? Oceanus offers special rates to you! Oceanus would like to hear A student subscription is only from anyone interested in $20 a year, a savings of $5 off being an intern with us in 1992. the cover price. For teachers, Excellent English skills and we offer a 25 percent discount on an interest in magazine bulk orders of five or more copies. publishing are the requirements. A discount also applies to a For futher information, one-year subscription for class contact Lisa Clark adoption ($20 each). at (508) 457-2000, ext. 2393. Fall 1991 43 COELACANTHS. iving fossils" are not unusual in the animal kingdom, and occur in almost all animal groups. Among vertebrates, how- ever, coelacanths are indeed something spe- cial. Known since the Devonian period, but thought to be extinct for millions of years, the coelacanth's "reappearance" on Earth can be compared to meeting a dinosaur. Today, more than 50 years later, South Africans celebrate their 1938 discovery with un- changed enthusiasm. Since coelacanths "be- came alive again" they have made world press: In 1987 a portrait of the fish appeared on the front page of The New York Times. Scientists have found many outstanding characteristics that coelacanths share with land-living tetrapods, and academic debates on their origin will undoubtedly continue. Their evolutionary importance is certain. Fishermen of the Comoro Islands catch two to four coelacanths annually, as an acciden- tal byproduct of oilfish fishing with deep- water baited lines. Probably 200 have been caught in the last five decades, all along the west coast of Grande Comore and off Anjouan at depths greater than 100 meters. Since coelacanths are equally interesting for scientific and public institutions, a market exists for the few caught specimens. Offi- cially this trade is controlled by the Comorian Government, which pays 150 US dollars for each caught specimen about five times the annual income of a local fisherman, and enor- mous incentive for coelacanth fishing. How- ever, coelacanths are too rare to support this. The Cormorian Government sells dead coelacanths worldwide. Although caught individuals are registered, it is not known how reliable the catch and sale records are. A black market is blooming, supported by the high rewards paid privately. Coelacanths are not only rare, they are sold out. Is there a future for the coelacanth? This question was raised very early by concerned scientists. In 1986 we left Europe with our submersible GEO to search for coelacanths, to film and study them in their natural environment (with permission from the Comorian Government). We surveyed the Grande Comore coastline between 80- and 200-meter depths to study the living coela- canths' habitat. The result was depressing: Especially off the fishing villages, the steep and barren lava slopes were almost empty. After traveling many miles under water on more than 22 dives, we found only six coela- canths between 117- and 198-meter depths. Our intensive survey confirmed that coela- canths are, indeed, very rare. We immedi- ately dropped our plan to bring them home to Germany. Wilbert Neugebauer, director of the Stuttgart Aquarium, supported our decision, although he would have loved to be the first showing coelacanths in a zoo. Having a coelacanth in a public aquarium is similar to having a Blue Mauritius (the most expensive stamp in a stamp collection), and an unforgettable dream for an animal collector. Bernard Fritzsch, a neuroanatomist at the University of Bielefeld (Germany) has investigated the inner-ear structure of coela- canths. All fish analyzed suffered inner-ear damage, probably as a result of the pressure changes that occurred when they were raised from 250 meters deep to the surface. Interfer- ence of inner-ear fluids with the brain causes balance problems, and, invariably, death. At the University of Bristol (England), George Hughes has found that the temperature dif- ference the fish experience when raised causes respiratory distress; in short, the fish slowly suffocate. These sad discoveries could reveal a serious threat to the survival of captured coelacanths: Even if immediately released, HANS FRICKE AND KAREN HISSMANN 44 Oceanus .The Fate of a Famous Fish hooked specimens will probably die. Comorian Republic officials are in favor of any attempts to save their coelacanth, gombessa, which is also their national symbol. The habitat of the living coelacanth is almost unknown. In 1986 we gathered the first field data with our submersible; cur- rently, these are insufficient to understand the fish's ecological requirements. How can we transport entire breeding populations if our knowledge of their habitat is so poor? Do safe, suitable locations for coelacanths, out- side the Comores, exist? Detailed knowl- edge on population density, reproductive biology, social behavior, and ecology are urgently needed before any attempts can be made to transport coelacanths to other areas or public zoos. In 1989, with our new 400-meter sub- mersible JAGO, we studied the coelacanth population off Grande Comore. The results were astonishing. During the day, coela- canths are cave dwellers and aggregate in small, peaceful groups, with the number of members changing daily. Individual coela- canths appear to produce few offspring and have a high longevity. Although the popula- tion size is small, it seems to be stable. In September 1989, a team from the TOB A Aquarium, one of the largest in Japan, arrived at the Comores to catch two coela- canths. The project director claimed that the fish is not endangered by extinction. We opposed this new capture project. The expe- dition was unsuccessful, as no coelacanth was caught. But the run for coelacanths will probably continue, and the umbrellas of sci- ence and conservation will be used to hide commercial interests. Of course scientists would love to watch coelacanths in an aquarium. But what could be gained? From watching fish behavior for many years in the wild, ethologists know that aquarium observations of social behav- ior are not representative of real life. Main- taining a delicate species such as the coela- canth alive in an aquarium is problematic enough. Breeding them is too farfetched. Since October of 1989, coelacanths are on schedule 1 of the conservation charter for the Convention on International Trade in Endangered Species, and the World Wildlife Fund has also been notified of their situation. Internationally there should be a ban onany further attempts to capture live specimens. Coelacanths are rare, and commercializa- tion will speed up their extinction. Scientists should concentrate on studying them in their natural environment, and specimens acci- dently caught by native fishermen should be fixed and conserved with the best methods and techniques available. Is the enormous effort and money spent to catch live coelacanths for public display worth it? With our present poor knowledge of their natural history and reproductive biology, we think the answer is no. The best protection for the coelacanth's survival is to stop all deep-water fishing; however, we must likewise be concerned with the sur- vival of the impoverished local fishermen who require deep-water fish as a food source. We hope that future generations of scientists can share the intellectual excitement and enthusiasm for this extraordinary creature that is so important to understanding our own evolution as vertebrates. Although we cannot prevent coelacanths from being acci- dentally hooked and dying slowly on the surface, we can discourage any attempts to go for the Blue Mauritius. Max Planck Institute for Animal Behaviour & Physiology, Seewiesen, Germany Fall 1991 45 It's TIU; simply good In business-in fact, in just about any endeavor-there 's a fine line between keeping up and staying one step ahead. And often, the people who stay ahead are the people who are best informed. That's where The Wall Street Journal comes in. It gives you a broad perspective on business, and valuable information on your competi- tion. . .on marketing. . .on technology. . . on politics. . .on corporate and financial events throughout the U.S. and the world. And only The Journal gives you this essential information with such insight and clarity. The Guide to Understanding Money and Markets sells for $13.95. But With This CTffer, It's Yours Free. This invaluable 120-page, easy-to-read reference book defines and explains a variety of investment terms, so you can make full use of your money-making opportuni- ties. It's a $13.95 value, yours FREE when you get 13 weeks of The Journal for just $37. So here's the dotted line. You know what to do. business to cut right The Wall Street Journal- every business day. The Guide to Understanding Money and Markets- FREE. What more do you need to know? to the dotted line* Cut out this coupon now for The Journal and your FREE Guide. ] Yes. Send me 1 3 weeks of The Journal tor just $37. D I prefer six months (26 weeks) for just $71. With either choice, send my FREE Guide as soon as you receive payment. H Payment enclosed (payable to The Watt Street Journal) D Bill me. D Charge my: D American Express D MasterCard D VISA THE WALL STREET JOURNAL. Oceanus/WHOI Woods Hole, MA 02543 Name (please print) Address Suite/Apt. Card No. Signature City Expires State Zip Limited time offer-good in the continental 17 5 only. 10CMA/39KL Elasmobranch Fish: Oviparous, Viviparous, and Ovoviviparous Carl A. Luer and Perry W. Gilbert daptation to its environment is one measure of an animal group's evolutionary success, and part of this adaptation involves development of efficient means of reproduction. As characterized by their relative positions on the phyloge- netic scale, birds and mammals are generally considered the most "advanced" or "higher" vertebrate animals. The evolutionary trend in reproduction among vertebrates, as epitomized by birds and mam- mals, is toward production of a smaller number of larger offspring, each representing a great investment of energy in terms of both nutritive supply and parental care. One group of "lower" animals, the subclass of fish known as elasmo- branchs (sharks, skates, rays, sawfish, and guitarfish), owes a large measure of its success to its modes of reproduction, which range from oviparity (egg laying) to viviparity (live bearing). Having branched from the main line of vertebrate evolution some 400 million years ago, the pathway leading to today's elasmobranchs has, in fact, evolved amazingly parallel reproductive adaptations to those of avian and mammalian species. While the basic processes and trends are similar, the adaptations contain obvious differ- ences, many of which are unique to the elasmobranchs and result from pressures brought by their vastly different environment. Elasmobranch Fertilization Without exception, as in birds and mammals, fertilization among elas- mobranch species is internal. This is in distinct contrast to broadcast spawning (where vast quantities of eggs and sperm are simultaneously released into the water column) practiced by most of the bony fish. To achieve internal fertilization, elasmobranchs engage in courtship and copulatory activities that last from a few minutes to several hours. Sperm pass from the male into the female through one of two modified portions of the male pelvic fins known as claspers. Associated with each clasper is a muscular bladder, called a siphon sac, that lies just beneath the belly The unique reproductive adaptations of elasmobranchs result from pressures brought by their vastly different environment. Fall 1991 47 Locations and relative sizes of siphon sacs of (A) the spim/ dogfish Squalus acanthias, ami (B) the smooth dogfish Mustelus canis are shown. The siphon sacs are situated between the belli/ skin and bod\/ musculature, end blind h/ at their forward end, and open into the clasper groove distalli/. A pair of clenrnosc skates (Raja eglanteria) ;';; their breeding positions. The male bites onto the trailing edge of one of the female's pectoral fins, swings his bodi/ beneatli her pelvic region, flexes one of his claspers medialh/ (in this picture his right clasper is flexed and not visible), and inserts it into the female's reproductive tract. skin of all sharks and fills with seawater just prior to mating. During copulation, the male flexes one of his claspers medially and inserts it into the reproductive tract of the female. Following insertion of the clasper, seawater is discharged from one of the siphon sacs, washing sperm along a groove in the clasper and into the female. Unlike their shark relatives, skates possess a clasper gland rather than a siphon sac, which results in a more passive flow of sperm from male to female. In these animals, copulation has been observed to continue for several hours. Once inside the female, sperm make their way up either or both sides of a Y-shaped uterus, not unlike that of most mammals. Between the uterine horns and the paired oviducts, however, lies a gland unique to elasmo- branchs. Referred to as the nidamental or shell gland, this tissue serves several functions, including the secretion of an albuminlike substance as well as the tough collagenous membrane that forms a protective case around the fertilized egg. The nidamental gland also functions in the storage of sperm, which can remain viable in the female for many months, or possibly even years, depending upon the species. In a process similar to mammalian ovulation, mature eggs are released from the ovary or ovaries (in most sharks, only a single ovary is functional) and enter the paired oviducts through a common ostium. Sperm and fertilized eggs have been recorded in the oviducts, although in most elasmobranchs the eggs are fertilized in the nidamental gland. In species whose mating activity and ovulation last only a few days, there is little need, and little evidence, for sperm storage. In most elasmo- branchs, especially oviparous species or those relying on extended periods of ovulation, sperm storage is a distinct adaptive advantage. These species, then, do not require freshly deposited sperm to coincide with each ovulatory event, but rather can continue to produce fertilized eggs without having to find a mate every few days or weeks. Perry W Gilbert and Gordon W Heath 48 Oceanns Feeding Developing Elasmobranchs Following successful fertilization of an egg, elasmobranch species employ several different methods of embryonic nourishment and prenatal develop- ment. Reasons for elasmobranch oviparity or viviparity certainly are the result of millions of years of evolutionary pressures, and the adaptive significance in each situation is still a popular topic of discussion. Oviparity is generally considered the most primitive of elasmobranch reproductive modes. All skate and some shark species are oviparous. While there are exceptions, the oviparous sharks tend to be small in size. The retention of a developing embryo or fetus within a small animal greatly restricts the possible number of progeny and size of offspring at birth. It is a distinct adaptive advantage for a small shark to ovulate and fertilize eggs in pairs (oviparous sharks tend to have two functional ovaries), encapsulate each in a protective egg case (comparable to the shell of a bird egg), and lay eggs at regular intervals for extended periods of time after the copulatory event. Researchers have observed one oviparous shark, the chain dogfish Scyliorliinus retifer, depositing 40 to 70 pairs of eggs at approximately 15-day intervals over a period of two to three years. Another oviparous elasmo- branch, the clearnose skate Raja eglanteria, lays pairs of fertile eggs every four to five days during an approximately six-month egg-laying season. Oviparous elasmobranchs tend to be demersal (bottom-dwelling), which facilitates the egg-deposition process. Unlike birds, however, oviparous elasmobranchs display no parental care for their eggs once they are laid, although adaptive pressures have resulted in a variety of egg-case designs that protect the developing embryo from the elements as well as from predators. Elasmobranch egg cases typically are tough and leathery rather than brittle, and are camouflaged by a dark or mottled appearance. Stringlike tendrils attached to many egg cases allow for entanglement on rocky hard bottoms or coral, as a means of preventing their being washed ashore. Large entangled masses of egg cases have also been observed, fueling speculation that some oviparous sharks return to the same location for repeated egg depositions. Other adaptations include skates providing sticky mucus material with their egg cases as a means of attachment to sandy substrate, and the horn shark Heterodontus sp. evolving a screw- shaped egg case that wedges into crevices along rocky shorelines through the force of repeated wave action. If oviparity is considered primitive, the obvious evolutionary advance consistent with the trend of producing a smaller number of larger offspring is to retain the fertilized eggs in the maternal uterus until hatching. This type of reproduction, where embryos develop on The chain dogfish Scyliorhinus retifer, an oviparous elasmobranch, lias a "ti/pical" egg case (left). Here it is shown with a newly hatched offspring and a size reference. Screw-shaped egg cases (right) laid by the hornshark Heterodontus francisci wedge into rock crevices that provide safe locations for incubation. Fall 1991 49 Captive breeding and egg ln\/ing In/ Hie clearnose skate Raja eglanteria allows observation of the development of embn/os of known age. Embn/os tit two weeks (a), four weeks (b), seven weeks (c), and ten weeks (d) into the approximately 12-week incubation period reveal growth and development as a result of nutrients absorbed from the i/olk sac. yolk reserves within the uterus, but without a direct maternal connec- tion, resulting in the birth of live young, is called ovoviviparity, also known as aplacental viviparity. This basic strategy occurs in most shark species and all rays, sawfish, and guitarfish, although there are many variations on the theme. In ovoviviparous elasmobranchs, the tough leathery egg case is replaced by a thin, smooth membrane or envelope. The animals range in size from the meter-long dogfish shark Sqiialus sp., to the 10-meter-long whale shark Rhineodon t\/pus, the largest fish in the oceans. The size of the adult fish tends to be reflected in the size and /or the number of developing embryos retained in the uterus. Mature female spiny dogfish (Squalus acanthias) at 70 to 100 centimeters in length, for example, tend to sustain two to six embryos in each of their two uteri, giving birth to fully formed offspring of 20 to 30 centimeters after a gestation period lasting up to two full years. At the other size extreme, tiger sharks (Galeocerdo euvieri), at 550-centimeter maximum, typically produce litters of 35 to 55 "pups" ranging in size from 68 to 85 centimeters follow-ing a Embryos of some rays absorb their yolk reserves in addition to "uterine milk" before completing development. After two- to four-months gestatioti, these rays are born as fully developed offspring. 50 Ocean us gestation period lasting slightly longer than one year. Until time of parturition, the yolk sac is generally sufficient to nourish the develop- ing young of ovoviviparous elasmo- branchs, but this is not always the case. Among the lamnoid sharks, which include the makos (Isurus sp.), porbeagles (Lmnna sp.), threshers (Alopias sp.), crocodile sharks (Pseudocarcharias sp.), false catsharks (Pseudotriakis sp.), great white (Carcharodon carcharias), and sand tiger (Carcharias taurus), the yolk sac is totally absorbed and the embryos "hatch" in the uterus within the first few months of development. To nourish her few developing offspring (usually two to eight in these species), the female continues to ovulate throughout much of gestation. The steady supply of nutritious eggs are devoured by the rapidly growing young (a practice known as oophagy, or egg eating) to the point where their guts become tremendously distended with consumed eggs. When ovulation ceases, the offspring complete their development by absorbing the yolk reserves in their stomachs, and they are born at a very large size, often exceeding 100 centimeters in length. In at least one of these species, the sand tiger, the first embryo in each horn of the uterus to hatch will consume the other developing embryos as they hatch (a form of embryonic nourishment termed embryophagy). Once its siblings are gone, the remaining embryo in each uterine horn continues to nourish itself through oophagy. In this species, then, two very large offspring are born per female. Another variation among ovoviviparous elasmo- branchs occurs in several of the rays (stingrays Dasuatis sp. and Urolophus sp., butterfly rays Gymnura sp., electric rays Torpedo sp. and Narcine sp., and devil rays Mobula sp.). As in the lamnoid sharks, the yolk sac is absorbed before development is complete. In these rays, however, the inner surface of the maternal uterus is lined with stringlike "trophonemata" that nourish the embryos until birth by secreting a nutritious fluid often termed uterine milk. Gestation in these rays tends to be shorter (two to four months) than in the ovoviviparous sharks (10 to 12 months). Litter size in rays can be as little as one offspring per female, but generally averages four to six. The mode of elasmobranch reproduction considered the most advanced is probably rated as such because of its Following an approximately 12-week incubation period, fully formed miniature clearnose skates (Raja eglanteria) hatch by poking their noses through seams in the ends of their egg cases (top), unfolding their pectoral fins (center), and swimming away (bottom). 8 CD [ o In tJie sand tiger shark (Carcharias taurus), one large embryo develops in each of the two material uterine horns. i-. *' ^-~- - these deep-sea species appear very similar to those of shallow-water species and they feed readily on the same phytoplankton cells that we routinely feed to other invertebrate larvae. Thorson's expectations are also at odds with recent work on deep- sea snail larvae done by Michael Rex (University of Massachusetts) and Phillipe Bouchet (National Museum of Natural History, Paris) and their colleagues. These workers convincingly demonstrated by a variety of methods that larvae of some deep-sea snails come all the way to the surface, where they feed upon phytoplankton. It is not known whether these larvae feed during the migration. We have reared embryos and larvae of several deep-sea echinoderm species at various temperatures in the laboratory, and in vials incubated at different depths in the field. Our results show that most species are unable to tolerate the temperatures in or near the euphotic zone. If these planktotrophic species pass their larval lives in deeper water, what do they eat? The most abundant living organisms at these depths are bacteria, which typically occur at rela- tively high concentrations throughout the water column even in clear tropical waters. To see if echinoderm larvae can use these very tiny particles, we (Sid Bosch, Lane Cameron, and I) trapped natural bacteria in chambers attached to the front of a submers- ible, labeled them with radioactive thymi- dine, and incubated them in situ with larvae that had been reared in the laboratory. Counts of radioactivity in the larvae demon- strated that larvae consumed substantial numbers of bacteria. Further experiments by Will Jaeckle at our institution also demon- strate that deep-sea larvae can absorb organic materials dissolved in seawater. At present, we suspect that bacteria, dead plankton from the surface, and dissolved organic matter provide the major food for planktotrophic larvae that develop in the deep sea. Thorson was probably correct in his assumption that planktotrophic species cannot migrate to the euphotic zone without feeding. This does not, however, eliminate 60 Ocean us planktotrophy as a viable strategy for deep-sea animals. It now appears that alternative foods available in deep water are sufficient to support develop- ment, either near the bottom or during long ascents to the surface. A final note of irony. Lecithotrophic eggs of deep-sea echinothuriids and many starfish are so packed with buoyant yolk that they actually float. Thus, the species that do not require food in the larval stages are probably the first to arrive at the surface! Reproductive Adaptations: An Interesting Case Study One of the most common bathyal sea urchins in the Bahamas is Aspidodiadema jacoln/i, a tiny animal about 2 centimeters in diameter that has long, flexible spines. Despite years of working with this species, we have observed spawning on only one occasion but this single experi- ence provided us with a wealth of interesting observations. Aspidodia- dema shows unusual features in spawning, sperm morphology, embryol- ogy, and larval feeding. As such, it exemplifies an extreme of reproduc- tive adaptation to the deep-sea environment. As mentioned before, the sperm of this diminutive species have the longest heads of any known echinoderm sperm. The 26- micrometer nucleus is thin and sickle shaped. The eggs are about the same size (90 micrometers) as those of planktotrophic species from shallow water, and are spawned in tangled threads of mucus that become attached, at least temporarily, to the female's spines. When the flexible, curved spines are examined with a microscope, one can see tiny barbs The author (left) and research associate Lane Cameron measure the flotation rates of echinothuriid sea urchin eggs. The unusual sperm of the deep-water sea urchin Aspidodiadema jacobyi has a sickle- slmped nucleus tJint is the longest known among echinoderms. Midpiece Head Craig M Young Fall 1991 61 Stalked crinoids, also known as sea //7/cs, are just one of many groups of common deep-sen annuals whose embryology is completely unknown. that point down toward the spine's base. These barbs may help in retaining eggs and mucus. The reason for having an enormous, pointed sperm head is not known; perhaps it aids the sperm in swimming through the highly viscous material that the eggs are embedded in. The tiny eggs are densely packed with opaque yolk. In this way, they resemble the much larger eggs of typical lecithotrophic species. During the blastula stage, when a typical urchin embryo would consist of a hollow ball of cells surrounding a central cavity, Aspidodiadema embryos pack the cavity completely full of yolk-laden cells. These remain in the region of the devel- oping gut for several weeks. A typical echinoid larva begins feeding only a few days after fertilization. Aspidodiadema larvae resemble those of more typical species in every respect except one: The mouth does not open for the first three weeks of development. Larvae are capable of living with no particulate food for up to 44 days after fertilization, at which time they require food for further development. During this extended prefeeding period, the larvae presumably survive on the yolk material packed around the gut. We interpret this unusual mode of larval development as an adaptation to patchy or rare food supplies in the deep-sea environment. What's Left To Do? A Lot In recent years, the media's attention has been focused on hydrothermal vents, mid-oceanic spreading centers, hydrocarbon seeps, and other unique deep-sea environments. The larvae of a few hydrothermal vent species have been collected in the water column. Ever since vent faunas were discovered, deep-sea biologists have wondered how the larvae produced in these relatively rare and ephemeral habitats manage to locate and colonize other vent habitats some distance away. (See 62 Ocean us Hydrothermal Vent Plumes: Larval Highways in the Deep Sea?, page 64.) One intriguing possibility suggested by Craig Smith (University of Hawaii) involves the use of whale carcasses as stepping stones for dispersal. Novel methods are needed to determine where microscopic larvae from vent habitats actually go. Despite some important advances, the reproduction of the vast majority of deep-sea animals remains completely unstudied. Embryos of several major groups such as stalked crinoids and glass sponges have never even been described. If information gained in the past two decades has been sufficient to overthrow the two major paradigms of deep-sea reproduction, it is exciting to contemplate the phenomena still hidden in the depths. Craig M. Young is an Associate Scientist at Harbor Branch Oceanographic Institution in Fort Pierce, Florida, where he heads the Department of Larval Ecology. When he is not working on deep-sea reproductive ecology, he studies the larvae of subtidal ascidians and other sessile animals. J oods Jiole Oceanoijraphic Associates.. . Join the growing number of people who care about our ocean environment as it is today. . .and could be tomorrow. For almost tofty years, WHOI Associ- ates have helped make possible the Woods Hole Oceanographic Institution's cutting edge research. Research which helps us understand the critical issues facing our ocean environ- ment. Hpu can share the excitement of our research through our magazine Oceanus, newsletters, tours, and special visits to the Institution. Please join us. For more information, please contact: Ms. DorseyMilot, Director of the Associates Woods Hole Oceanographic Institution Woods Hole, MA 02543 or call (508) 457-2000, ext. 2392 1930 . . . woutdn *t you like to fieip< ? 3 Fall 1991 63 Hydrothermal Vent Plumes: Larval Highways in the Deep Sea? Lauren S. Mullineaux, Peter H. Wiebe, and Edward T. Baker Traces of plumes and their larval passengers can be found many kilometers away from their original vent source. long the crest of the globe-encircling mid-ocean ridge, cold and dark seawater is transformed into a warm, nutrient- laden broth that supports a chemosynthetic ecosystem unique to the planet. Deep-seated lava beneath the ridge heats seawater seeping through the fissured rocks, trans- forming it into 350C hydrothermal fluids that gush from the seafloor through chimneys of precipitated metal sulh'des and other minerals. The pure hydrothermal fluids are diluted instantly by the surrounding seawater. Larvae of benthic invertebrates and other zooplankton living at the vents are swept into this buoyant mixture of warm fluids and carried away from the seafloor, like unwitting passengers in a hydrothermal hot-air balloon. A few hundred meters above the seafloor the now very dilute plume reaches neutral buoyancy and begins to spread laterally, mixed and transported by deep-sea currents. Traces of plumes and their larval passengers can be found many kilometers away from their original vent source. Transport of larvae in these plumes may be critical for the maintenance of communities living at hydrothermal vents and the colonization of new vents. Most of the organisms in these communities cannot live in the absence of vents and their associated resident chemosynthetic microorgan- isms. In many Pacific locales, vent activity appears to be ephemeral on time scales of decades, with the hydrothermal flow at individual vent sites slowing or ceasing altogether. Once the hydrothermal fluids at a vent field stop flowing, most of the organisms living there perish because the chemo- synthetic microbes at the base of their food chain can no longer survive. The only way for these sessile (stationary), benthic species to survive (on evolutionary time scales) is to colonize other active vent habitats, using dispersive larvae or juveniles. Life in Vent Plumes We are using hydrodynamic models and measurements of hydrothermal vent plumes to determine if larvae or juveniles can disperse from one vent 64 Ocean us habitat to another by drifting in the plume. The buoyant plume rises until the diluted plume water has the same density as ambient seawater, usually approximately 200 meters above the bottom. At this level, the plume spreads out, often in the direction of existing horizontal water currents. Vertical velocities averaging 5 to 10 centimeters per second and greater are not uncommon in hydrothermal plumes, so particles are transported into the lateral portion of the plume in a matter of hours. Once in the lateral plume, however, the amount of time that particles and organisms stay in the vicinity of the vent field depends on their settling velocities and how much advection they experience from horizontal currents. Reduced chemicals (those in their electron-rich state) and organic particles transported in the plume may also affect (adversely or construc- tively) the growth and reproduction of deep-sea zooplankton entrained in the plume. If injecting chemosynthetically fixed carbon into the water column at the lateral plume level enhances the food resources compared to nearby nonplume sites, one might also expect to find more and /or different kinds of zooplankton in the plume. Plumes that are enriched in reduced compounds and bacterial populations are a potentially significant nutrient- enriched environment in the otherwise nutrient-poor but oxygen- rich deep sea. Alternatively, hydro- gen sulfide and other chemicals that are toxic to marine invertebrates may occur in the lateral plume in concentrations high enough to reduce the populations of these sensitive zooplankton species. Sampling with Nets Towed Near the Seafloor Researchers began to wonder about how vent larvae disperse as soon as they realized that vent organisms could live only at vents, and that vent habitats were ephemeral. Only recently, however, have we been able to sample larvae in the deep ocean with techniques that allow us to answer these questions. To sample large volumes of seawater in the plumes, it is necessary to tow nets very near the bottom (within tens of meters of the seafloor). Towing a net from a long cable behind a ship is a little like flying a kite near high-tension wires on a very long string from a moving car you are never quite sure where it will end up. Because of this, biologists have traditionally towed nets well above the bottom. MOCNESS was towed in the plume above a vent field at Juan de Fuca. Water characteristics such as temperature, salinity, particle concentration, and fluorescence are gathered by sensors mounted on the net frame, and transmitted in real time to the surface through the cable. A new altimeter measures height off seafloor, which is crucial for avoiding collisions. / / Fall 1991 65 Many types ofbenthic invertebrate larvae caught in MOCNESS tows have been identified and photographed, includ- ing the starfish juvenile (left), a cephalopod (octopus and squid) larva (center), and a bivalve larva (right). (Photos by Lisa Garland, who also sorted and identified larvae from plankton samples.) On a July 1990 cruise to the vents on the Cleft Segment of the Juan de Fuca Ridge (200 miles southwest of Seattle in 2,200-meter-deep water), we towed a MOCNESS through a plume and within 30 meters of the bottom. A MOCNESS is a Multiple Opening/Closing Net and Environ- mental Sensing System that is equipped with a newly developed altim- eter. Real-time readings from the altimeter and a CTD (conductivity/ temperature/depth) sensor attached to the MOCNESS showed the distance of the nets from the bottom. This information was coupled with detailed seafloor topography maps to help the net controller avoid collisions between the nets and any underwater cliffs or spires. National Oceanographic and Atmospheric Administration (NOAA) physical oceanographers generated maps of the plume during the same cruise from CTD tow data. We navigated the MOCNESS through the plume by comparing water temperature and particle density measured by net- mounted sensors with their maps. Nine nets made of very fine mesh (64- micrometer openings) could be opened and closed on each tow, so we accomplished fine-scale sampling both within and outside the plumes. Plumes Harbor Abundant Larvae Preliminary examinations of the MOCNESS net samples revealed larvae of a wide variety of benthic taxa, including gastropods, bivalves, polychaete worms, cephalopods, coelenterates, and bryozoans. Abun- dances ranged from 60 to 600 larvae per 1,000 cubic meters, numbers that are unusually high for the deep sea. Part of our success in catching larvae was due to our using fine-mesh nets that can catch small larvae missed by most standard plankton nets. Surprisingly, juvenile starfish (aster- oids) and brittle stars (opiuroids) were also caught in nets towed hun- dreds of meters off the seafloor, indicating that the plume is capable of transporting even fairly large, post-metamorphic organisms. The number of larvae moving in the plume can be estimated by taking into account the larval abundances, the plume's width, and the ambient currents. Using maps of the plume size and shape compiled from five years of annual surveys by NOAA researchers, a conservative estimate of the plume's volume at this site is 42 square kilometers. If larval abundances throughout the plume are, on average, similar to those we measured, then at least 11 billion larvae reside in the plume over the north end of the Cleft Segment. Given a plume cross section of approxi- mately 1.4 square kilometers, and ambient currents between 1 and 2 66 Oceanus kilometers per day, these calculations suggest that perhaps 350 to 700 million larvae are trans- ported away from the vents each day. This discovery that substantial numbers of benthic larvae exist in the Cleft Segment plume supports our hypothesis that larvae are dispersing in the plume. We still must demonstrate that the larvae of vent organisms are able to colonize new vent habitats after they arrive by drifting in the plume. One important remaining task is to distinguish larvae in the plume belonging to vent species from larvae released by nonvent benthic organisms. This taxonomic work is currently under way in the laborato- ries of Ruth Turner (Harvard University), James Blake (Science Applications Inc.), and Rudolf Scheltema (Woods Hole Oceano- graphic Institution). Zooplankton not Enhanced in Plumes We estimated the zooplankton biomass in the plume by imaging the silhouettes of individuals in each net sample. For this proce- dure, we placed an 8- by 10-inch photographic film in the bottom of a transparent Plexiglas box, then poured the plankton sample over the film, distributing the animals as evenly as possible. We exposed the film with a strobe light ap- proximately 30 centimeters above the box, washed the animals off the film, and then developed the film. From this process, we ob- tained silhouette negatives that we placed on a translucent electronic digitizer and examined with a dissecting microscope. We identi- fied silhouettes of zooplankton according to general taxonomic group and electronically measured the total lengths. Using equations -1800 ~ -2000 a 0) Q -2200 CO o o o it m E o o o Net Tow MOC-Q-014 7200 10800 14400 18000 Time (seconds) 21600 Time (Hours) 1 20000 20 , 3 ; 4 ; 5.0 6.0 7. 80000 - b Total Numbers of Zooplankton 1 40000 - | :| 200 - 400 - c T ZooplanTt I on > 5 mm (ESD) 100 - Total Plankton Biomass 50 - o - Ui 1 i- ^^JB i ' 2.0 3.0 4.0 5.0 6.0 7 Time (Hours) This contour plot (top) shows the particle density along the MOCNESS fore path (the white line), across the plume axis above the ]uan de Fuca Ridge. These measurements were used to map the position and intensity of the lateral plume. The net passed over the ridge-a\is center and hydrothermal vent field about four hours into the tow. Numbers of zooplankton (per 1,000 cubic meters) in eight MOCNESS nets (as counted from silhouettes), were collected at discrete intervals across the plume (b). Numbers of large zooplankton (those greater than 5 millimeters in diameter) in eight MOCNESS nets is illustrated in (c). Animals in this size class scatter 100- kilohertz acoustic beams, and may comprise the scattering layer found above plumes. The plankton biomass (in cubic centimeters, per 1,000 cubic meters) from eight MOCNESS nets, as calculated from silhouette images is revealed in (d). Upper plot by Sharon Walker, lower plot by Peter Wiebe. Fall 1991 67 These zooplankton were captured in MOCNESS tows. The silhouette-image analysis procedure was used to determine numbers of individuals present, their sizes, and their taxonornic compositions. (Photos by Nancy Copley, who also identified zooplankton and analyzed their distributions.) or subgroup, the lengths of indi- viduals were then converted into wet weights. Zooplankton biomass collected in a net tow traversing the axis of the plume was not larger in the core of the plume than in ambient deep-sea waters away from the plume. In fact, large zooplankton (those with linear dimensions greater than 5 millimeters) appeared to be depleted in the plume core. These preliminary results suggest that not only do zooplankton not benefit from organic particles in the plume, but that large zooplankton are ad- versely affected by it. This latter finding is consistent with previous work by Richard Thomson and coworkers involving the use of a 100-kilohertz acoustic doppler current profiler that revealed a significant decrease in the number of acoustical targets (particles greater than 5 millimeters in diameter) present in the core of a plume above the Endeavor Segment of the Juan de Fuca Ridge. Our zooplankton biomass data provide some support for the idea that the occurrence of fewer acoustical targets in the plume's core is due to lower numbers of living acoustical targets (zoo- plankton) there. The Next Step Our future work will include more detailed taxonomic identifications, and additional plankton samples taken very near the vent communities. These samples, scheduled to be collected with the submersible Alvin in fall 1991, are critical for determining which larvae in the lateral plume came from vent communities. Work is also continuing on the zooplank- ton from the net samples. Since some of the larger zooplankton species appear to be depleted in the plume core, we plan to examine distribu- tions of individual taxa to determine how specific animals respond to different aspects of the vent plume. ""\ Lauren S. Mullineaux is an Assistant Scientist in the Biology Department at Woods Hole Oceanographic Institution (WHOI). Her interests are larval dispersal and its effects on community structure in the deep sea. Peter H. Wiebe is a Senior Scientist and the Biology Department Chair at WHOI. His research interests include quantitative population ecology and acoustical studies of zooplankton. Edward T. Baker is a Scientist with the Pacific Marine Environmental Lab of the National Oceanic and Atmospheric Administration (NOAA). He has been working on water-column processes above vents at Juan de Fuca as part of the NOAA Vents program. 68 Oceanus - . B ; .Let's face it, you either get results that pay off. . . H cind or resu ts does your advertising get or you? ...or you don't. Oceonus can provide a stable platform from which to launch your advertising program. With qualified readers who are eager to read what the worlcPs leading scientists and experts have to say about our ocean environment, there is no better way to reach the marine science field. Don't let your advertising die on the page. Have your marketing or advertising department contact the Oceonus Advertising Office at (508) 457-2000, extension 3391 for rates and information. Oceanus International Perspectives on Our Ocean Environment FA World of Art Beneath the Waves Kathy Sharp Frisbee ' n the snap of an instant when all the elements of strength, beauty, and inspiration come together in momentary suspense is when Maurine Shimlock and Burt Jones capture their art. Like other fine artists, they strive to depict the fleeting effects of nature, personalities, and creation as a never-ending process. Unlike traditional artists, they cannot return to their canvas day after day to add dabs of color here, lighten lilting brushstrokes there, or accentuate graceful curves. Their work is accomplished not on land, but under water at 25- to 150-foot depths. Their medium employs cameras, lenses, film, strobes, and diving equipment, along with artistic sensitiv- ity and physical stamina sufficient to contend with the oceans' nether-worldly conditions. They record water fantasia moments in the ever-moving world of marine life from various perspec- tives: hovering in swift currents 2 inches above the seafloor; gripping a fingerhold on a coral reef's jagged and jutting wall; sitting statue-still on a reef's sandy patch; or in a split-second after turning somersaults in the sea. Out of hundreds of photos taken, one or two will emerge to forever frame a colorful and captivating moment when art and artist merged. (Continued on page 78) Shimmering pink and pearl-colored soft-coral polyps (Dendronephthya) sway with the sea's surges in West Pacific waters off the Solomon Islands, extending their tentacles to filter and feed on the passing plankton-rich buffet. Low in zooxanthellae, symbiotic algae found within the tissues of various animals including corals, these coral polyps are nearly transparent, permitting the maximum amount of sunlight to reach the zooxanthellae. This coral colony was in a bleached condition when this photo was taken. One week later, Shimlock and Jones returned to photograph it again and found that it had returned to its normal, deep-fleshy color. '.': f , Almost too picturesque to be true, this lionfish family (Pterois volitans) appears to be out for a swim along the ever-blooming West Pacific coral reef gardens just beyond the Solomon Islands. Lionfish are members of a large family known as the scorpionfish (Scorpaenidae). Captivating in their peacocklike appearance, the lionfish is a formidable smart weapon in disguise with anal, pelvic, dorsal, and pectoral fins, sharply pointed and venomous, capable of inflicting severe pain and even killing humans. As Georgia O'Keeffe focused on the fine details of flowers, here the photo artist has focused on one of the many fine details in a coral reef's brilliant tapestry, the delicately fanlike shape and brushstroke texture of a sea anemone's green and peach-colored mouth. Sea anemones (phylum Cnidaria) are of two forms, sedentary polyps and free-swimming medusae. Each has specialized tissues, such as an epidermis for protec- tion, a nerve net for motor coordination, and a gastrodermis for digestion. Their gastrovascular cavity has a single opening that is used for both taking in food and extruding wastes. i Pachycheles pubescens, informally known as the porcelain crab, peeks from beneath its gray/green anemone carpet lair in the West Pacific off the Solomon Islands, in search, it appears, of its errant juvenile frolicking above. F rt * T > Looking every bit like a rose-pink ribbon adornment for an evening gown, this egg case of a Doridacea nudibranch, also known as a Spanish dancer sea slug, sways in Red Sea currents. Millions of tiny, bright pink eggs have been woven into a gelatinous coil, slimy to the touch, during a Spanish Dancer's night spawn. To weave its offspring ribbon, the shell-less marine snail worked through the night, rotating its spawning eggs slowly on its foot, adding row after row. A few hours later, the eggs hatch and the swimming larvae disperse. The brilliant colors of the nudibranch and its eggs are the result of concentrated noxious toxins, and serve as warning colors to passing fish. The playful and attentive spotted dolphins (Stenella attenuata) that Shimlock and Jones encountered in the North Atlantic off Grand Bahama Island are nomadic in nature, swimming in ranges of 1,000 miles and more in Atlantic and Pacific waters, traveling 30 to 50 miles a day, at speeds of 15 knots. Their social behavior is noted for bouts of abundant activity, such as leaps and tailspins, alternating with periods of quiet. Typical greetings include unison breathing, unison swimming exchanging body rubs, or pectoral pats. F 41 -15 > I r~ ' > Small star coral (genus Montastrea) are shown here in West Pacific ocean waters just off the Solomon Islands. With cups nearly one centimeter in diameter, here in shades of moss green with lilac centers, the star coral grows on average 6 millimeters a year. Assuming normal, healthy growth, unencumbered by pollution, extreme sea-level or water-temperature changes, it could reach a height of 45 meters within 7,500 years. A World Of Art... continued Twenty years ago the technology didn't exist to do this work, and 20 years from now the environment may not exist. "I may take ten pictures of the same swirling school of jacks," said Shimlock, "but one is going to be my favorite because it is exactly what the moment was like to me when I actually saw that scene the move- ment, the depth, the color, all the things that made my heart skip a beat." Where Claude Monet painted the impressionistic character of the French landscape and seascape with oils on canvas, and Ansel Adams photographed the realistic majesty of the American Southwest, Shimlock and Jones capture on film realistic to surrealistic images from the world of art beneath the waves, from the Solomon Islands to Malaysia, from the Grand Bahamas to the South Pacific. The artistry of marine life inspires their work and offers them an opportunity to entertain viewers by revealing undersea wonders that most people have never seen and may never have a chance to see firsthand, and to educate them by revealing interrelationships in undersea life. It is important to them to preserve in picture what may not be here in time. This added mission was prompted by someone's comment to them, that they are in a good place in time because 20 years ago the technology didn't exist to do this work, and 20 years from now the environment may not exist. When under water, Shimlock and Jones feel they are truly in their element. Indicative of this devotion, they spent their summer "vacation" this year diving and photographing marine life, this time a pod of 15 sleek Atlantic-spotted dolphins frolicking in the crystalline blue waters west of Grand Bahama Island (see page 76). Following their host's advice, they used snorkels during the photo shoot, rather than their usual scuba equipment, a method their host had found on previous trips to be more agreeable with the dolphins. Plunging for 30 seconds at a time to 25 foot depths, Shimlock and Jones snapped enthralling portraits of the dolphins at play. What excited and engaged the dolphins most, they discovered, were their humble human efforts to turn flips and mimic their aquatic audience's playful antics in the water. More than anything, the dolphins liked and continually sought eye contact, preferring not to have the camera come between them and their human entertainers. For this shoot, the team used Nikon S-3 cameras in Aquatica and Ikelite underwater housings, with Nikon 15- and 20-millimeter lenses, Fujichrome 125 and 250 Velvia film at 1 /60th shutter speed, and natural light. Shimlock and Jones soon found one key to success: Performing for the dolphins, then quickly turning, focusing, and snapping their images. Evidently, the dolphins didn't like having a photographer just tread water and try to take their picture, because at those times they wouldn't come around. Nor did they want people reaching out and touching them, a response that prompted the dolphins to dart away. "Sometimes they would stop swimming, come right up to you, and look you in the eye," said Shimlock. "At times you wouldn't know when they were coming, you would just turn around and find one staring right at you." The dolphins suddenly appeared around Shimlock and Jones while they swam in search of subjects on the perfect-weather day of July llth (which was also the day of a solar eclipse); then, two hours later, they disappeared just as suddenly, much to the team's bewilderment. Ex- hausted from the experience, Shimlock and Jones were nevertheless 78 Ocean us eager to rejoin their dolphin friends. They cruised the area by boat for three hours, and repeated the search during the next two days, all to no avail. It was yet another exhilirating if fleeting moment with nature. In August, the vacation was over and Shimlock and Jones resumed their professional agenda as owners and operators of Secret Sea Visions by escorting a group of nine diving and photography enthusiasts to Sipadan Island for two weeks. A sanctuary for the past 30 years, Sipadan is under the jurisdiction of Malaysia, and located 15 miles off the north- east coast of Borneo. Sipadan is not attached to the continental shelf, but comes straight up from the ocean floor with a 2,000-foot drop-off on all sides. Today it is a popular diving spot, known for its abundant schools of marine life and green turtles. In addition to escorting photo /diving adventures worldwide, Shimlock and Jones also offer presentations nationwide on Secret Sea Visions' excursions, and seminars on underwater photography techniques at places such as the New England Aquarium in Boston, Massachusetts, and Sea Space in Houston, Texas. Through their semi- nars and excursions, Shimlock and Jones have discovered that underwa- ter photographers' main weaknesses are understanding the importance of learning how to read light in the water, balancing the use of natural and artificial light with strobes, and preventing artificial light from overwhelming natural light. According to Shimlock, most people will rely on their camera's light meter alone, when it is really better if they use an external light meter. Once a light reading is made, the artificial light from the strobes needs to be brought into balance with available natural light, first by pre-equipping the stobes with white plastic diffus- ers, and second by setting the amperes at quarter power. Situations and settings vary depending upon the amount of particles afloat in the water, shafts of sunlight underwater that tend to scatter and absorb artificial light, the photographer's distance from the subject and, if the subject is white, such as some coral, how much of the strobe light will reflect back. To get started in underwater photography today would cost, Shimlock estimates, between $700 and $1,000 for special camera, lens, and strobes, and not including diving equipment. In the past few years, Shimlock and Jones's photo work has been featured in numerous publications. In the next six months, their photo artistry will also appear in a book being published by the Osaka Aquarium in Japan. They are the first underwater photo artists to have their work appear in Helmut Gernsheim's Contemporary Collection in Lugano, Switzerland. A noted photography collector, Gernsheim has written 14 books on photography, including a three-volume Histon/ of Photography. Gernsheim said he was attracted to Shimlock and Jones's photography because "their work goes beyond nature photography to presenting true art." For both Shimlock and Jones, the fascination with marine life developed in their youth. Though a landlocked child growing up in Texas with "chilis in my blood," Jones said as far back as he could remember, he was "a little fish," who would religiously sit before the television watching "Sea Hunt," while wearing his toy mask, fins, and snorkel. Shimlock, who grew up along the western mountain fringes of South Carolina, said she has always felt she "would literally rather be "Their work goes beyond nature photography to presenting true art." Fall 1991 79 There's a world of difference between underwater and landside photography. underwater than anyplace else." For a time their photographic interest was focused on the Mayan ruins, before their enthusiasm for underwater photography took seed and blossomed between 1976 and 1987. During that 11-year period, they owned and operated a resort and managed dive operations for two hotels in Puerto Morelos along the Caribbean coast of Mexico. In 1987, they sold their business and for the next two years managed live-aboard dive boats on the Solomon Islands in the western Pacific, east of New Guinea. "We're self-taught," said Shimlock. "Because we had this place on a beach in Mexico, we could go diving everyday and take pictures. Both of us had a strong, natural curiosity about marine creatures, and we really got to know life cycles and habitats. So when we decided to pursue underwater photography, we were several steps ahead in the process because we already knew where everything lived, how to find it, and by that time we had become accomplished divers." There's a world of difference between underwater and landside photography. Shimlock and Jones haul about 300 pounds of equipment to a photo site, including special, housed underwater cameras weighing 20 to 35 pounds each, air tanks, regulators, and backpacks, all of which becomes neutrally buoyant, but still somewhat cumbersome underwater. "Once you're on site, you're totally limited on time, depth, marine-life interactions, and managing your nitrogen," said Jones. "You're dealing with mobility in your environment, you're moving, your subject's moving, you've got one film choice and one camera choice per dive, and you can only take four to five rolls of film a day, whereas a land photographer on safari can take 50 rolls of film a day. It can be like hauling all your equipment into a tropical storm with winds blowing and rains falling, all the elements seem to conspire against capturing a few pictures while the photographer is expending a great deal of physi- cal energy." A key to successful underwater photo work, Jones explained, is forgetting that you are underwater and striving for neutral buoyancy, that light-as-a-feather feeling, allowing you to flow with the ocean's currents and surges, and actually hover like a helicopter inches off the seafloor. "It's a real trick that takes time," Jones said. Though their dives will take them to 150-foot depths, most of their photo shoots are made between 40 and 80 feet, where they typically find the best growth, light, and menagerie of rainbow-hued sea life. They have found their best success for color, clarity, and processing with Fujichrome's new technology film, Velvia. Their equipment selection also includes 15- and 20-millimeter lenses for wide angle shots, and a 55- millimeter micro lens or a 90-millimeter lens for macro shots. For any artificial lighting, they use Oceanic strobes. According to Shimlock, the camera equipment rig is "a stainless steel bar with two three-foot long arms on either side, with elbow bends, and what looks like a bread box on the end with strobes that can extend to eight feet. So there you are," she mused, "swimming along, trying to look natural and not scare anything." They have numerous favorite subjects. Said Jones, "The crinoids are always good sources of art because they have brilliant color combina- tions and they're everywhere. You're always looking for the bottom- 80 Occam is dweller-type fish too scorpion fish, crocodile fish, flounder varieties, stargazers, and angler fish, those captivating critters that are camouflage artists." Finding an intriguing sea-creature subject with bold, shimmer- ing colors and striking, reticulated patterns is only half the challenge. The other half is capturing it against a background that will heighten the picture's overall composition, such as tomato-red clownfish nestled in a jade-green anemone meadow, or tangerine-orange starfish atop a royal- purple starfish hugging a large, algae-green covered rock. Finding a good location is important too. "There's always a sandy or dead spot, even on a healthy reef," said Shimlock, "and if you just settle in there, in a few minutes sea creatures will come to you. Also, a lot of reef residents are scared by your bubbles, so if you're real quiet, you'll have a much better success rate." Ocean pollution is a factor Shimlock and Jones have been increas- ingly encountering, especially in the South Pacific. "There's intense logging of tropical hardwoods," said Shimlock," and that is causing critical erosion from the barren mountains, making the surrounding waters dirtier and covering the reefs with siltation that kills them. Dynamite fishing is another concern," she said. "Someone will throw a stick of dynamite in the water, kill everything, and only harvest one- tenth of the kill. At the same time, the dynamiting is killing the reefs and ruining underwater habitats, so there are fewer and fewer fish." In November, the team will escort another photo /diving excursion group to Vanuatu, a string of islands in the South Pacific. This trip will be their second on behalf of Oceanica, an international nonprofit membership organization that promotes "environmentally stable stewardship of ocean resources." For Shimlock and Jones, such opportunities lend further dimen- sion to their photo work and the water world they so admire. For further information or consultation about photography and travel with Shimlock and Jones, write to Burt Jones and Maurine Shimlock; Secret Sea Visions; P.O. Box 162931; Austin, Texas 78716; or call (512) 328-1201. Kathy Sharp Frisbee is the Editorial Assistant for Oceanus. Finding an intriguing sea-creature subject with bold, shimmering colors and striking, reticulated patterns is only half the challenge. ON THE COVER Looking like a jeweled setting, two deep-golden skunk clownfish (Amphiprion perideraion) nestle in their host anemone in the West Pacific Ocean, a safe shelter from which they never retreat into the wild. When predators approach, clownfish huddle within the protective shelter of their sea anemones. Deadly cells called nematocysts on the anemone's tentacles paralyze and ensnare prey, but do not harm the clownfish because they have a mucus coat that protects them from the anemone's stinging-cell shocks. When danger subsides, the clownfish rise and hover just above the anemone to dine on algae and zooplankton. Likewise the fish protect their anemones from the butterflyfish and parrotfish that typically feed on anemones: If an anemone's nematocyst barrages provide little deterence to an avenger, a clownfish will also mount a counterattack, with fins splayed, head high, and teeth nipping. (Photo by Burt Jones and Maurine Shimlock.) Fall 1991 81 BOOK & VIDEO REVIEWS Deep-Sea Biology: A Natural History of Organisms at the Deep-Sea Floor by J.D. Gage and P.A. Tyler. 1991. Cambridge University Press, Port Chester, NY. 504 pp. - $135.00. The 1960s were a time unparalleled for new discoveries of life on the deep-sea floor. Surpisingly, this sudden, rapid increase in knowledge of deep-ocean bottom fauna was not the result of technological advances, but rather a consequence of using nets with finer screens than had ever before been used (less than 0.4 millimeters), and by an elutriation process that employed nothing newer or more sophisticated than a gimbaled dustbin with an overflow (or, in American parlance, a trash can with a spout). The discovery of such an ex- traordinarily rich fauna, equalled on land only by tropical rain forests, was made early in the 1960s by H.L. Sanders and R.R. Hessler on a transect between the New England coast and the Bermuda islands, from the 43-meter ketch R/V Atlantis from Woods Hole, Massachusetts. Their findings and the advances that followed during the past 30 years are described and summarized by John D. Gage and Paul A. Tyler in their new book Deep-Sen Biology: A Natural History of Organisms at the Deep-Sea Floor. The authors are eminently competent to write such a volume. Indeed, Gage, as a post- doctoral fellow at the Woods Hole Oceano- graphic Institution in 1964, was an early participant in the exciting new discoveries. Subsequently, Gage and Tyler together have done extensive work in the Rockall Trough in the Northeast Atlantic studying such processes as reproduction and the demography of deep- sea populations. The book is divided into five parts. After a five-page historical summary, Part I deals with changing theories about the deep-sea's physi- cal environment and the means of study used during the last 30 years. The conception that the deep-sea environment has "large-scale homogeneity in salinity, temperature, and oxygen" has been replaced, with a current emphasis on the environment's dynamic aspects, in particular, studies on the bottom boundary layer and the measurement of organic-material flux from the sea surface. As the questions have changed, methods for obtaining deep-sea-bottom samples have also evolved, from the predominant use of dredges and epibenthic sleds to the box corer, which obtains undisturbed, quantitative samples. The use of deep-sea submersibles has allowed direct observation heretofore impossible, and has made it possible to study the metabolism of abyssal-organism communities at great depths. Part II compiles an extensive "natural history of organisms at the sea floor," and includes chapters on the megafauna and other smaller animals. Part III considers "patterns in space," and includes chapters on small-scale spatial patterns, abundance and size structure of the deep-sea benthos, diversity gradients, depth-related patterns in community composi- tion, and the zoogeography, speciation, and origin of deep-sea fauna. Not all of these subjects are or can be treated in equal depth simply because more has been done on some than others. For example, as a consequence of studies in the early 1960s, much consideration is given to species diversity. On the other hand, owing to the lack of data, the zoogeography of the deep-sea benthos must remain largely an area of speculation. Part IV takes up ecological aspects of the deep-sea fauna including food resources, energetics, and adaptations for feeding; metabolic processes; reproduction, recruit- ment, and growth; and animal sediment relationships. Studies of the ecology of deep- sea organisms, completely unexplored until two decades ago, has now begun to transcend 82 Oceanus BOOK & VIDEO REVIEWS mere speculation about processes that lead to patterns of spatial distribution observed in the deep sea. Here the authors have synthesized and effectively conveyed their special interest in ecological proceses of the deep-sea benthos. Part V considers those aspects of deep-sea life that have recently become interesting to the general public. The deep-sea hydrothermal vents, which appear at junctures between tectonic plates, have a unique and spectacular fauna dependent upon chemoautotrophic bacteria that obtain their energy from the oxidation of reduced sulphur and other compounds. Man's effect on the deep-sea environment, particularly through living- and nonliving-resource exploitation, and waste disposal such as dredge spoil, sewage sludge, Pharmaceuticals, industrial wastes, and radioactive materials, is still imperfectly known. The authors conclude that "exploita- tion of [the deep-sea] resources should not be attempted until we understand the natural history and ecology of this complex system." Finally, the volume has an extensive bibliography of 82 pages with 1,286 entries. Not all of these references pertain to the deep sea; some deal with shoal-water processes to which deep-sea phenomena are referred or compared. Nonetheless, the bibliography alone is a useful compendium for anyone who wishes to enter the deep-sea literature that has been published over the past 30 years. One possible shortcoming is the underrepresentation of Soviet literature, with only 42 bibliographic entries included. How- ever, representative works of important Soviet deep-sea biologists, for example, those of Zenkevitch, N.G. Vinogradova, Filatova, Belyaev, and others, are included. The book, in general, is well produced. Only occasional uncorrected editorial errors and a few misspelled names in the bibliogra- phy (for example, Weibe for Wiebe; M.E. Vinoradova for M.E. Vinogradov) appear. Illustrations throughout the book are effective and well chosen. The authors of Deep-Sea Biology transmit to the reader a keen enthusiasm and deep in- volvement in their subject. For those engaged in research on any one of the many aspects of deep-sea biology, this is a stimulating and useful summary to keep on one's shelf. For the student aspiring to the study of deep-sea life, this is without a doubt the single most useful volume presently available. Rudolf S. Scheltema Senior Scientist Department of Biology Woods Hole Oceanographic Institution WE'D LIKE TO HEAR FROM YOU. Oceanus welcomes and occasionally publishes letters from readers regarding editorial content or other ocean- science issues. Please write to the address on page 4. 1992 CALENDAR of BEAUTIFUL LIGHTHOUSES Full Color Spiral Bound, 8 7/2 .v 7 7.3 Send$8.00ea. + $l.50S&H to: HORIZON IMAGES 6841 PcrshingSt. Hollywood FL. 33024 Dcpt. C 4 FREE Postcards Included 3 Calandarsfor $23.00 + $3.00 for 1st Class Po -Satisfaction Guaranteed- Fall 1991 83 BOOK & VIDEO REVIEWS Chesapeake: The Twilight Estuary VHS video by Maryland Sea Grant. College Park, MD. 1991. 39 minutes - $50.00. The University of Maryland Sea Grant Pro- gram weaves an environmental mystery story in Chesapeake: The Twilight Estuary. As the place where rivers meet the sea, estuaries have long been recognized as highly productive areas that form the underpinning of diverse habitats supporting economically valuable fisheries, migratory waterfowl feeding grounds, and even an entire way of life for the human inhabitants of this rich coastal zone. Chesapeake sets the scene for lay viewers with artistic photography, and establishes the case that a nearly limitless bounty is produced by these waters a bounty that enriches man as well as the multitude of nonhuman species residing in and adjacent to this bay. The mystery begins with the observed loss of sea grasses. Submerged grass beds form the basis of an extensive and essential habitat in Chesapeake Bay. Species vary with growing conditions, but together they create a "huge prairie" of underwater grasses. These grass beds supply food and shelter for crab and finfish and are critical feeding grounds for migratory water- fowl. Grass beds are the necessary base on which the historic crab fishery is built. The casually observed loss of sea-grass beds becomes a scientific mystery when public concern raises the issue of deteriorating environmental quality, resulting in lost jobs and reduced economic value of the traditional fishery. Can the loss of sea grass be docu- mented, and from this documentation process, can any pattern of loss be detected? If scientists can read the patterns, they can begin to determine the causes. The national estuarine system appears as a tangled web of interacting processes that the ecosystem scientist must attempt to unravel. From a collection of aerial photographs reaching back more than 60 years, investigators could detect a comeback of the sea-grass beds following devastation by disease in the 1930s. A regular increase in grass habitat area is revealed through the 1960s, and then a dra- matic die-off is shown through the 1970s. The die-off pattern shows a loss first in the upriver grass beds, followed by loss of downriver and river-mouth beds, leading to die-off in the main stem of the Bay. Now the scientists have documented a Bay-wide problem and have detected a pattern in the progression of dying grass beds. What causes can be ascribed to this observed pattern? The standard coastal pollution issues such as oil spills, urban runoff, shipping, pipe outfall effluents (containing excess heat, biocides, heavy metals, etc.) were all examined by Chesapeake scientists and rejected as the cause for this problem. After eliminating many of the possible causes, investigators began to focus on non-point-source loading of agricul- tural chemicals from farmland in the water- shed. Herbicide use has tripled in the water- shed since 1960; using the hypothesis that chemicals that kill land plants will also kill aquatic plants, two of the most commonly used chemicals were investigated. With very good use of graphics to display complex scientific data, the video clearly demonstrates that although toxic agricultural chemicals could be the cause for some of the die-off, these chemi- cals alone could not be responsible for the patterns detected. To some extent, the lack of an obvious solution to this mystery drove the scientists back to basics and they asked if the lack of light could be related to the sea-grass problem. Bingo. Results from in-situ experiments under Plexiglas chambers in various parts of the Bay show that the pattern of die-off could be related to reduced light. With a course to 84 Oceanus BOOK & VIDEO REVIEWS follow, scientists now began to investigate several factors that darken the estuary. Sus- pended sediment from land-based erosion is one obvious factor. In pursuing this, we are presented with dramatic evidence of the immense size of the drainage basin and the effect on the coastal zone of human activities alongside "a thousand creeks and a hundred rivers." That the light is failing and that the suspended sediment in the Bay is contributing to the diminished light becomes apparent but, as with the herbicides, suspended sediment does not appear to be the sole cause of such a dramatic sea grass die-off. The human population around Chesa- peake Bay has exploded in the past two decades. Nitrogen and phosphorous concentra- tions in the rivers have more than doubled in the same time. Nutrients from sewage treat- ment plants and agricultural runoff have enriched the estuary beyond its normal capac- ity to assimilate these chemicals. Just as too much fertilizer in a home garden can injure vegetables and flowers, so too are excess nutrients damaging to a complex natural system. Our scientific detectives found that the excess nutrients in the estuary resulted in a population explosion of epiphytes (single-cell algae, primarily diatoms) glowing on the leaves of grass, and that this grass-epiphyte relationship caused shading of the leaves to the point of killing the plant. The mystery, made more complex because there were multiple villains, has been solved but this is only the first step in resolving the problem. It's easy now to see that if we save the light we will save the grasses which will, in turn, preserve the bounty of the Bay for us and our heirs. To save the light, we must closely examine our current practices of waste dis- posal, and consider new ways to use the land that take into consideration the health of the estuary. Although the video ignores this critical issue, new waste-disposal and land-use practices will have to be paid for, and into the cost-benefit equation we must insert the real cost, over the long term, of impaired environ- mental quality, of the lost habitat, of damaged fisheries, of closed shellfish beds, and of a destroyed way of life. Only then will we pre- serve these precious resources for those who live and work by these waters and only then will we begin to pay the full cost of our actions and stop transferring those costs to our heirs. Bruce Tripp Research Associate Coastal Research Laboratories Woods Hole Oceanographic Institution The Soviet . Maritime Arctic THE SOVIET MARITIME ARCTIC edited by Lawson W. Brigham This volume contains a collection of seventeen essays that examine the historical record and current developments surrounding the activi- ties and policies of the Soviets in their vast maritime arctic region. ^4 95 J -M. UST LIST PRICE 336 pages. 16 photos. 19 maps. 10 line drawings. Appendix. Index. #1-7538. NAVAL INSTITUTE PRESS Customer Service (7911) 2062 Generals Highway, Annapolis, MD 21401 800-233-8764 Monday - Friday: 8:00 am - 9:30 pm, EST Pall 1991 85 BOOKS & VIDEOS RECEIVED OCEANOGRAPHY Methods For Fish Biology edited by C.B. Schreck and P.B. Moyle; 1990; American Fisheries Society, Bethesda, MD; 704 pp. - $50.00. Advances in Research on the Beluga Whale edited by T.G. Smith, D.J. St. Aubin, and J.R. Geraci; 1991; Department of Fisheries and Oceans, Quebec Region, Cap-Diamant, Quebec; 206 pp. - $39.00. Pathology in Marine Science edited by Frank O. Perkins and Thomas C. Cheng; 1990; Academic Press, Inc., Chicago, IL; 256 pp.- $59.95. From Gaia to Selfish Genes: Selected Writings in the Life Sciences edited by Connie Barlow; 1991; MIT Press, London, England; 255 pp. - 15.75. MARINE POLICY The Legal Determination of International Maritime Boundaries: The Progressive Development of Continental Shelf, FEZ, and FEZ Law edited by Gerard J. Tanja; 1990; Kluwer Law and Taxa- tion Publishers, Boston, MA; 360 pp. - $73.00. Environmental Policy in the 1990s edited by Norman J. Vig and Michael E. Kraft; 1990; Congressional Quarterly Press, Washington, DC; 418 pp. - $18.95. Oceanic Processes in Marine Pollution (six-volume set) by Iver W. Duedall, Dana R. Kester, and P. Kilho Park; 1990; Krieger Publishing Company, Melbourne, FL; 1,758pp. -$367.00. Oceanography of a Large- Scale Estuarine System: The St. Lawrence edited by j Mohammed El-Sabh and Norman Silverberg; 1990; Springer- Verlag, New York, NY; 442 pp. - $79.00. Pacific Rift by Michael Lewis; 1991; Whittle Direct Books, Knoxville, TN; 85 pp. - $11.95. olphin Societies Discoveries and Puzzles Edited by KAREN PRYOR & KENNETH S. NORRIS In this unusual book, two of the best-known scientists in the marine mammal field have assembled an astonishing variety of discoveries about dolphins. $34.95 at bookstores or order toll-free 1-800-822-6657. Visa/MasterCard onl\. UNIVERSITY OF CALIFORNIA PRESS BERKELEY 94720 ENVIRONMENT Environmental Consequences of Deep Seabed Mining: Problem Areas and Regula- tions by Stig Berge, Jan Magne Markussen, and Gudmund Vigerust; 1991; Fridtjoff Nansen Institute, Lysaker, Norway; 135 pp. - $30.00. Antarctica: Private Property or Public Heritage? by Keith Suter; 1991; Zed Books, Lon- don, England; 209 pp. - $49.95. Our Common Seas: Coasts in Crisis by Don Hinrichsen; 1990; Earthscan Publications, Lon- don, England; 192 pp. - $14.95. The Uses of Ecology: Lake Washington and Beyond by W.T. Edmondson; 1991; University of Washington Press, Seattle, WA; 352 pp. - $19.95. Wetlands: Market and Inter- vention Failures; Four Case Studies edited by Tom Jones and Kerry Turner; 1991; Earthscan Publications, London, England; 180 pp. - $29.95. The Fragile South Pacific: An Ecological Odyssey by Andrew Mitchell; 1991; University of Texas Press, Austin, TX; 256 pp. - $24.95. Turning the Tide: Saving the Chesapeake Bay by Tom Horton and William M. Eichbaum; 1991; Island Press, Washington, DC; 324 pp. - $14.95. Water: The International Crisis by Robin Clarke; 1991; Earthscan Publications, London, England; 224 pp. - 8.95. 86 Oceanus BOOKS & VIDEOS RECEIVED REFERENCE YOUNG PEOPLE FISHERIES Atlas of Sponge Morphology by Louis DeVos, Klaus Rutzler, Nicole Boury-Esnault, Claude Donadey, and Jean Vacelet; 1991; Smithsonian Institution Press, Washington, DC; 117 pp. -$135.00. One Long Argument: Charles Darwin and the Genesis of Modern Evolutionary Thought by Ernst Mayr; 1991; Harvard University Press, Cambridge, MA; 195 pp. - $19.95. Tidal Hydrodynamics edited by Bruce B. Parker; 1991; John Wiley & Sons, Inc.; Somerset, NJ; 883 pp. - $98.00. ORIGINAL ANTIQUE MAPS & SEA CHARTS U.S. & WORLDWIDE GRACE GALLERIES, INC. Box 2488, RR5 Brunswick, ME 040 11 (207)729-1329 Call or Write for Listings ANTIQUE MAPS PRINTS CARTOGRAPHIC BOOKS Call to Adventure Deep Sea Divers to Mountain Climbers by Hillary Hauser; 1991; Best Publishing Company, Flag- staff, AZ; 60 pp. - $14.95. Look Inside a Ship by Denise Patrick (ages 4 to 8); 1989; Putnam Publishing Group, New York, NY; 20 pp. - $10.95. The Whale's Song by Dyan Sheldon (all ages); 1991; Penguin Books, Inc., New York, NY; 24 pp. - $14.95. Discover My World Ocean by Ron Hirschi (ages 4 to 8); 1991; Bantam Books, New York, NY; 29 pp. - $4.99. VIDEOS Ecology of the Coral Reef produced by Films for the Humanities, Princeton, NJ; 28 minutes - purchase $149.00; rental $75.00. Seas Under Siege produced by Films for the Humanities, Princeton, NJ; 56 minutes - purchase $149.00; rental $75.00. Texas Shores Saving What's Left by Texas A&M University Sea Grant College Program, Galveston, TX; 26 minutes - $20.00. Ocean Ranching by Universtiy of Alaska Sea Grant Marine Advisory Program; 1990; Anchorage, AK; 29 minutes -$15.00. Common and Scientific Names of Fishes from the United States and Canada, 5th edition by C.R. Robins; 1990; American Fisheries Society, Bethesda, MD; 190 pp. - $32.00. European Inland Water Fish (a multilingual catalogue); 1990; Fishing News Books, Osney Mead, Oxford, En- gland; 196 pp. - 18.95. Fisheries Oceanography and Ecology by Taivo Laevastu and Maurray L. Hayes; 1990; Fishing News Books, Osney Mead, Oxford, England; 216 pp. - 27.50. THE NOW GENERATION of CONTINENTAL SHELF INSTRUMENTS and HOUSINGS. IHOSTAFORMC"' PLASTIC) . BATTERIES ELECTRONICS ACOUSTIC RELEASE Programmable TRANSPONDER SELF-RECORDING TIDE GAUGE with or without an ACOUSTIC RELEASE Other MORS oceanographic packages O.E.M. housings & internal frame- work for your specific needs Low cost. No external metal parts. 600 m operational depth. No corrosion or biofouling. MORS MORS ENVIRONNEMENT- MASSY, France (1) 64 47 19 19 MORS ENVIORNNEMENT- BREST, France 98458510 OCEANO INSTRUMENTS UK-EDINBURGH 031- 552 6619 OCEANO INSTRUMENTS-SEATTLE, WA (206) 363-0500 Fall 1991 87 COMING UP NEXT. . . Mid-Ocean Ridges Volume 34, Number 4, Winter 1991/92 Earth's crust resembles a gigantic jigsaw puzzle whose pieces are great plates that move slowly about the face of the globe. The plates meet at the Mid-Ocean Ridge, a 70,000- kilometer belt of mountains that is the site of earthquakes, volcanos, submarine hot springs, and major lava flows. Our authors reveal the latest information on the mechan- ics of the dynamic ridge system, how scien- tists model features they can't easily see or measure, and what we know of ridge earth- quakes. They'll describe the far-reaching in- fluence of water rising from hydrothermal seafloor vents and tell us of the unusual animals thriving in darkness around the vents. Please join us for this update on a fascinating feature of Planet Earth. Mineral-laden fluid rises from a hydrothermal vent on the East Pacific Rise section of the Mid-Ocean Ridge. ORDER BACK ISSUES! What's Still Available? Ocean Engineering & Technology Vol. 34/1, Spring 1991 Naval Oceanography Vol. 33/4, Winter 1990/91 Waste Disposal Reconsidered Vol. 33/2, Summer 1990 The Mediterranean Vol. 33/1, Spring 1990 Pacific Century, Dead Ahead! Vol. 32/4, Winter 1989/90 The Bismarck Saga and Ports & Harbors Vol. 32/3, Fall 1989 ' The Oceans and Global Warming Vol. 32/2, Summer 1989 1 DSV Alvin: 25 Years of Discovery Vol. 31/4, Winter 1988/89 1 Sea Grant Vol. 31/3, Fall 1988 1 and many, many, more... To place your order, send a check or money order (payable to WHOI) to: Oceanus Back Issues WHOI Woods Hole, MA 02543 Please enclose $6.00 plus $1.00 shipping and han- dling for each magazine ordered, and include a street address and daytime telephone number with your order. Allow 3 to 4 weeks for delivery. All payments must be made in US dollars drawn on a US bank. For orders outside the US, please add an additional $1 .00 per item for shipping. Sorry, we cannot deliver to Canadian addresses. For information on other available back issues, con- sult the Oceanus editorial offices at the address listed above. Back issues of Oceanus are also available on microfilm through University Microfilm International, 300 N. Zeeb Road, Ann Arbor, MI 48106. 88 Oceanus Save on OceORUS Holiday Gift Subscriptions The perfect seasonal gift for your friends and relatives. Give Oceanus for the Holidays First subscription is $21.95, each additional subscription is only $19.95. What a great way to send Season's Greetings! 1st Gift Recipient Your Name Address Address City/State/ZIP H New ] Renewal City/State/ZIP 2nd Gift Recipient Address City/State/ZIP 114BRC D New D RelKAV.ll ] Begin a subscription for me also for $19.95 with my gift order! Q D Payment Enclosed D Please Bill Me OCEANUS is published quarterly bv ilie Woods Hole Oceanographic Institution. Cover rate is $25.00 annu.illv For subscriptions outside ot tin- 1 S ple.i-e see the inside front cover ot this issue or consult our editorial ottu.es. OCEANUS will send a card to the recipient acknowledging your yift. G i ve Oceanus to Yourself This year, give yourself a subscription to OCEANUS. With our special holiday rate, a full year costs only $21.95. 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Box 6419 Syracuse, NY 13217-6419 NO POSTAGE NECESSARY IF MAILED IN THE UNITED STATES MBL/WHOI LIBRARY CREATURE FEATURE The face of a West Pacific scorpionfish (Scorpaena), with beady eyes, ragged beard, and persistent frown, is unquestionably ugly, but that's his style, a form of camouflage used for his protective and dietary benefit. Adept at finding a matching background whether dwelling on the ocean bottom, in shallow water, in bays, coral reefs, or along rocky coastlines, the clever scorpionfish makes it nearly impossible at times to distinguish its shape against its setting. Capable of inflicting a venomous sting, the scorpionfish will sometimes allow itself to be handled and even stroked... then erect its venomous spines in defense. At other times, it will splay its pectoral fins, revealing vivid pink, purple, orange, and black stripes as a flaglike warning to its intruder, (Photo by Burt Jones and Maurine Shimlock.) Florida Institute of Technol- ogy's department of ocean- ography, ocean engineering, and environmental science offers a wide variety of programs at the bachelor's, master's, and doctoral levels. The department's blend of basic science and applied engineering, truly unique among American universities, fosters multidisciplinary education and research. F.I.T. is a distinctive indepen- dent university, located on the Atlantic Ocean, 25 miles south of Cape Canaveral. Program Interests Ocean Engineering Beach Processes and Coastal Engineering Corrosion, Biofouling, and Marine Materials Fisheries Engineering Marine Vehicles and Systems, Naval Architecture Oceanography Biological Oceanography, Ecology of Aquatic Systems Coastal Processes and Marine Meteorology Coastal Zone Management Marine Chemistry Marine Geology /Geochemistry Environmental Science Environmental Chemistry Lagoonal and Wetlands Systems Marine, Atmospheric, and Terrestrial Pollution Waste Management and Utilization Water Supply and Groundwater Dynamics Ocean Engineering Oceanography Environmental Science ABOVE: Human- powered submarine "Sea Panther" an Ocean Engineering student project. LEFT: Beach processes class after retrieving an electromag- netic current meter from the surf. FLORIDA ^INSTITUTE OFJECHNQLOGY A Distinctive Independent University For more information, contact Dr. N. Thomas Stephens, Head, Department of Oceanography, Ocean Engineering, and Environmental Science, 150 West University Boulevard, Melbourne, FL 32901-6988 (407) 768-8000, ext. 8096 FAX (407) 984-8461