Endogenous and Exogenous Control of Gametogenesis and Spawning in Echinoderms

Advances in MARINE BIOLOGY Series Editor DAVID W. SIMS Marine Biological Association of the United Kingdom, The Laborat...

Author: Annie Mercier | Jean-Francois Hamel

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Advances in MARINE BIOLOGY Series Editor

DAVID W. SIMS Marine Biological Association of the United Kingdom, The Laboratory Citadel Hill, Plymouth, United Kingdom Editors Emeritus

LEE A. FUIMAN University of Texas at Austin

CRAIG M. YOUNG Oregon Institute of Marine Biology Advisory Editorial Board

ANDREW J. GOODAY Southampton Oceanography Centre

GRAEME C. HAYS University of Wales Swansea

SANDRA E. SHUMWAY University of Connecticut

ROBERT B. WHITLATCH University of Connecticut

Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands Linacre House, Jordan Hill, Oxford OX2 8DP, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1900, San Diego, CA 92101-4495, USA First edition 2009 Copyright # 2009 Elsevier Ltd. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher. Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865 843830; fax (+44) (0) 1865 853333; email: [email protected]. Alternatively you can submit your request online by visiting the Elsevier web site at http://www.elsevier.com/locate/permissions, and selecting Obtaining permission to use Elsevier material Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made. ISBN: 978-0-12-374959-8 ISSN: 0065-2881 For information on all Academic Press publications visit our website at elsevierdirect.com Printed and bound in UK 09 10 11 12

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Volume 54, 2008. Bridget S. Green. Maternal Effects in Fish Populations. pp. 1–105. Victoria J. Wearmouth and David W. Sims. Sexual Segregation in Marine Fish, Reptiles, Birds and Mammals: Behaviour Patterns, Mechanisms and Conservation Implications. pp. 107–170. David W. Sims. Sieving a Living: A Review of the Biology, Ecology and Conservation Status of the Plankton-Feeding Basking Shark Cetorhinus Maximus. pp. 171–220. Charles H. Peterson, Kenneth W. Able, Christin Frieswyk DeJong, Michael F. Piehler, Charles A. Simenstad, and Joy B. Zedler. Practical Proxies for Tidal Marsh Ecosystem Services: Application to Injury and Restoration. pp. 221–226.

PREFACE

Echinoderms are fascinating creatures that display a rich array of reproductive modes and strategies. As members of the invertebrate deuterostomes, the closest extant relatives of vertebrates, they also occupy a very significant phylogenetic position. For this reason, echinoderms have received considerable attention over the past decades from researchers in various fields. This has allowed particularly significant advances to be made in the areas of gamete biology, developmental processes, and genomics. With the advent of new biochemical and molecular tools, the recent discovery of species dwelling in deep-sea habitats (presumably far removed from the direct influence of familiar environmental fluctuations) and the growing number of aquaculture initiatives, studies on the reproduction of echinoderms have entered a new era. Nevertheless, fundamental questions such as the respective, and possibly, synergistic contributions of biological, chemical, and physical factors to successful breeding events and the recruitment of new generations remain incompletely understood. To draw a comprehensive portrait of our current understanding of the endogenous and exogenous mediation of gamete synthesis and spawning in echinoderms, we have endeavored in this review to compile and assimilate a large body of literature, including work dating back over a century. Early and recent studies provide a wide blend of approaches and exhibit various degrees of reliability and completeness. We have tried to present the data as objectively as possible, outlining the proposed hypotheses and leaving the reader to weigh opposing arguments. In the concluding chapter, we provide a personal analysis, contrasting, and sometimes questioning both the traditional paradigms and novel theories, and identifying the main gaps in our knowledge. It goes without saying that this contribution relies entirely on the collective effort of innumerable colleagues, which form a vast and rich research community dedicated to the study of echinoderm ecology and reproduction. They are too numerous to acknowledge fully here; however, we would like to highlight in this context the pioneering work of Arthur C. Giese, Haruo Kanatani, Fu-Shiang Chia, John M. Lawrence, and John S. Pearse who have paved the way for generations of enthusiastic echinodermologists around the world. We would also like to extend our warmest and most sincere thanks to John S. Pearse (University of California, Santa Cruz) and Raymond J. Thompson (Memorial University) for their valuable input and comments. xi

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Preface

Owing to the apparent complexity and diversity of reproductive strategies displayed by echinoderms of all shapes and origins, and the likely absence of universal patterns, we wholeheartedly admit that this work is by no means definitive. It is our sincere hope that it will, however, provide solid framework for those wishing to push our understanding yet further, and fuel our never-ending fascination with this exceptional Phylum. ANNIE MERCIER JEAN-FRANÇOIS HAMEL

C H A P T E R

O N E

Introduction Abstract Most echinoderms display seasonal or other temporal cycles of reproduction that presumably result from the complex interplay of endogenous and exogenous signals. Various environmental, chemical and hormonal factors, acting directly or indirectly, individually or in combination, have been proposed to cue, favour or modulate a suite of reproductive functions from the onset of gametogenesis to gamete release. From as early as the nineteenth century, an astonishing array of studies has been published on topics related to the control of reproduction in echinoderms, ranging from fortuitous behavioural observations to complex experimental demonstrations and molecular analyses. Although the exact pathways involved in the perception of external signals and their transduction into coordinated spawning events remain obscure for most species, significant advances have been made that shed new light on the information gathered over decades of research. By compiling the existing literature (over 1000 references), interpreting the main results, critically assessing the methodologies used and reviewing the emerging hypotheses, we endeavour to draw a clearer picture of the existing knowledge and to provide a framework for future investigation of the mechanisms that underlie reproductive strategies in echinoderms and, by extension, in other marine invertebrates.

Contents 3 5

1. Terminology 2. Brief Overview of Reproductive Features

The regulation of reproductive processes in marine invertebrates has been discussed in the literature since the end of the nineteenth century. Echinoderms were initially studied in this context because they were abundant and fairly easy to collect and maintain in captivity. More recently, they have become models for the study of gamete biology and some species of echinoids and holothuroids have been reared in captivity as part of aquaculture or restocking programmes, yielding a larger body of knowledge on their reproductive processes. Except for a small number of mammals, including humans, most animals show distinct reproductive seasons or cycles (Cloudsley-Thompson, 1961; Rusak and Zucker, 1975). Both timing and duration of breeding periods are crucial elements of the overall life history strategy of an organism Advances in Marine Biology, Volume 55 ISSN 0065-2881, DOI: 10.1016/S0065-2881(09)55001-8

#

2009 Elsevier Ltd. All rights reserved.

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Annie Mercier and Jean-François Hamel

(Boolootian, 1966; Giese et al., 1991). Reproductive activity is usually timed to coincide with optimal environmental conditions for offspring survival, including food availability. Breeding success in echinoderms, as in other marine invertebrates, depends on highly synchronized processes between individuals of a population at the level of gamete synthesis and spawning. This synchronization is generally believed to be mediated by external cues (i.e., environmental factors) which may act either directly or indirectly, alone or in synergy, to reset or maintain biological clocks. Increasing evidence is pointing to the transduction of environmental signals via the endocrine system, but we are only beginning to understand the depth and complexity of the pathways and mechanisms involved and the possible role of chemical communication in this scheme. Indeed, different species may exhibit markedly different breeding strategies and periodicities, based largely on their specific life history, social arrangement, type of gonad and gamete development, endocrine system, and response to environmental fluctuations/stimuli. Furthermore, different populations of the same species often breed at different, locally suitable times while using the same suite of synchronizing cues. Reviews of echinoderm biology which either focused on or included various aspects of their reproduction were published between 1955 and 1991 (e.g., Binyon, 1972; Boolootian, 1966; Giese and Pearse, 1974; Giese et al., 1991; Hyman, 1955; Kanatani and Nagahama, 1983; Shirai and Walker, 1988). These publications considered what was known at the time about gametogenesis, spawning, gonad morphology and environmental cues related to the reproductive cycle. Interest in these concepts has flourished over the past two decades following the study of species from new locations (e.g., Antarctica, deep-sea habitats) or within aquaculture programmes and the use of novel techniques to probe the neurological and hormonal reactions involved in the synthesis and release of gametes. Apart from reproductive aspects discussed within reviews of specific groups [e.g., edible sea urchins (Lawrence, 2007)], there has been no comprehensive synthesis of the abundant data published on the control of reproduction in echinoderms since the early 1990s. The objective of this review is to update this wealth of information and discuss the control of reproduction in echinoderms in light of a more complete understanding of the interactions and processes involved. In so doing, we present a comprehensive account that integrates the early ground-breaking work on the influence of external factors (e.g., temperature, photoperiod, lunar cycle, phytoplankton) with recent results on chemical ecology, endocrine systems, entrained biological clocks and social behaviours. Evidence has been compiled for coastal and deep-sea species within the five conventional classes of extant echinoderms (Crinoidea, Ophiuroidea, Holothuroidea, Asteroidea and Echinoidea). The enigmatic class Concentricyloidea is not included as it currently contains only three

Control of Reproduction in Echinoderms

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little known species of Xyloplax and is the subject of taxonomic controversy ( Janies and Mooi, 1998; Mah, 2006; Pearse and Pearse, 1994; Rowe, 1988). We hope that the concepts emerging from the analysis of this large body of literature will provide a framework for further investigation of the mechanisms underlying reproductive behaviour, and be used as a guide for manipulating reproductive processes to gain insights into the proximate and ultimate triggers of the observed breeding strategies and periodicities. Understanding how exogenous and endogenous factors interact to ensure gamete competence at the proper time of year is important not only from an ecological standpoint but also for developing sustainable fisheries and aquaculture programmes, and for assessing how echinoderm populations may be affected by, and respond to, natural and man-made disturbances (e.g., fisheries, climate change, endocrine-disrupting chemicals). Through its appraisal and discussion of the presumed and confirmed paradigms, we trust that this review will provide a clearer picture of the existing knowledge and identify the areas in need of further investigation.

1. Terminology Regulation of the reproductive cycle is not only concerned with the timing of spawn-out, for this is merely the climax of considerable preparatory activity, but encompasses all aspects of the organism’s physiology and behaviour. The overall length of the breeding cycle can be looked upon as a function of the rate of growth, development, and maturation of gonadal tissues, ending in a spawning or a series of spawning events, followed by a period of germinal redevelopment (Giese, 1959a). Boolootian (1966) indicated that the reproductive cycle refers to the total course of events, regardless of the time period over which gamete production occurs (daily, weekly, monthly, annually, etc.) and Holland (1991) rightly pointed out that defining a beginning and an end in the annual reproductive cycle is arbitrary. The breeding season of a species, usually delineated in terms of months, is generally defined as the period of the year when most individuals in a population have numerous ripe gametes available for release (Giese and Pearse, 1974). In some species there is only one gametogenic cycle in each individual during each breeding season. The gametes may be released simultaneously or intermittently during the season (Giese and Pearse, 1974). In this review the breeding season will be discussed as a part of the gametogenic cycle, whereas spawning events will be addressed in a separate chapter, as years of research on the specific stimuli resulting in gamete release have identified it as a clearly distinct step in the reproductive process. There exists an important distinction between proximate factors, which serve as cues to maintain synchronous breeding within a population, and

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ultimate factors, which serve as selective forces that give survival value to the adaptation. In other words, the adaptive significance of spawning under certain conditions at a certain time can be distinguished from the mechanism by which this is achieved. The initial definitions of ultimate and proximate factors in the control of reproduction were first outlined by Baker (1938); however, Clark (1979) later suggested a further distinction between necessary environmental conditions (i.e., those allowing the completion of some cellular process essential for gamete maturation and breeding) and specific environmental signals that control the timing of reproductive events (Olive, 1995). According to Baker (1938), ultimate factors select individuals that produce young at the optimum time for survival; these factors do not, however, regulate the precise timing of breeding each year, which is controlled by proximate factors acting on gonad development well in advance of spawning. Proximate factors have been subdivided by Wingfield (1980) into two different types of information. The primary sources of initial predictive information for many animals are the large annual cycles such as photoperiod and temperature. Complete gonad development, mating (if any), and spawning are stimulated by supplementary information, for instance social cues and availability of particular foods. These factors vary from year to year and between locations, and they determine the exact timing of breeding each year. In echinoderms and other marine invertebrates, reproductive cycles are usually cyclic with annual, seasonal or monthly periodicities involving most individuals within a given population. This cyclic pattern is generally associated with habitats where environmental factors (e.g., photoperiod, temperature) fluctuate according to a predictable regime. However, a ‘‘continuous’’ reproductive pattern has been proposed for a growing number of species, mainly those found along the equator (e.g., Muthiga, 2005; Ramofafia et al., 2003) and in deep-water habitats (reviewed by Young, 2003). Like many of our colleagues, we recommend the use of the term ‘‘aperiodic’’, which refers to the absence of any detectable pattern. It is still unclear whether these species synthesize gametes and spawn opportunistically (or continuously) or whether part of the population follows a cyclic pattern (e.g., monthly) that is not detectable by conventional sampling techniques and analyses. Traditional gonad analysis of the equatorial sea cucumber Isostichopus fuscus from Ecuador suggested an aperiodic pattern of reproduction (Mercier et al., 2007), but direct observations over several years revealed a clear and predictable monthly periodicity, with 12 h) (Fig. 2.2). However, the out-of-phase oogenic cycle was not sustained for more than a few months in specimens exposed to long day lengths, indicating that short day lengths may be required as well to maintain later phases of oogenesis. On the other hand, a fixed photoperiod (either short, neutral or long) had no effect on gametogenesis, implying that the gametogenic cycle is under the control of an endogenous annual rhythm (Pearse et al., 1986a). Pearse and Beauchamp (1986) found that individuals of Leptasterias sp. maintained for almost 3 years under two different photoperiod regimes under controlled laboratory settings shifted out-of-phase with respect to in-phase animals. Pearse and Walker (1986) demonstrated a major role for photoperiod on the reproduction of another species of sea star, Asterias rubens (¼vulgaris), in this case on the north-eastern coast of the USA. They mentioned that it was tempting to conclude that control of reproduction by photoperiod is a general phenomenon, at least for shallow-water species.

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Laboratory photoperiod

Field

6 Mo out of phase

Ambient Hours

16

Daylength

12

Gonad index

20

Body wet wt (kg)

15

Pyloric cecum index

8 +++ ∗∗∗

∗

Gonads

∗∗∗

∗∗

++

10 5 0

Pyloric ceca

15 10 5 0

1.0

Body weight

0.5 0 1979

1980

1979

1980

1979

1980

Figure 2.2 Pisaster ochraceus (Asteroidea). Changes in day length, gonad index, pyloric caecum index, and total wet body weight in field and laboratory populations held under ambient (in-phase) and 6-month out-of-phase photoperiod (mean SE). There were no differences between values for males and females in any of the samples. Continuous lines: individuals collected in and maintained from December 1978. Dashed lines: individuals collected in and maintained from June 1979. Asterisks and crosses: laboratory observations of spawning in individuals collected in December 1978 and June 1979, respectively. Reprinted with permission from Pearse and Eernisse (1982).

Regulation of oogenesis in Sclerasterias mollis was studied by Xu and Barker (1990a) in New Zealand using an experimental design similar to that of Pearse and Eernisse (1982). Well-fed individuals maintained 6 months out-of-phase of the ambient photoperiod underwent a gradual shift in the breeding periodicity that was apparent in the gonad index, the size of oocytes and the steroid levels after a few months. Interestingly, individuals maintained in-phase did not entirely follow the field population, exhibiting differences in gonad index and oocyte size, possibly because of the different


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light, temperature and feeding regimes (Xu and Barker, 1990a). Nevertheless, the two experimental groups displayed clear out-of-phase reproductive rhythms in response to the photoperiod regime, while their feeding, body size and pyloric caecum index remained unaffected. Pearse and Bosch (2002) worked with the sea star Odontaster validus in McMurdo Sound (Antarctica) and demonstrated the photoperiodic control of gametogenesis in this species with a well-defined gametogenic cycle throughout its circumantarctic distribution (Grange et al., 2007; Pearse, 1965, 1966). Gametogenesis in specimens kept on a photoperiod 6 months out-of-phase with ambient (constant light in winter, constant dark in summer) switched within a year to the out-of-phase regime, unlike sea stars kept on an ambient photoperiod or collected from the field. Gametogenesis in sea stars kept in constant light or on a 12L:12D photoperiod appeared to be maintained more or less continuously, whereas day lengths >12 h apparently stimulated gametogenesis. In contrast, gametogenesis in sea stars kept in constant darkness was comparable to that in sea stars kept under ambient photoperiod or collected from the field, suggesting an underlying circannual rhythm (Pearse and Bosch, 2002). Bouland and Jangoux (1988) used a comparative investigation of gonad cycles in Asterias rubens under laboratory controlled conditions and in the field in the Netherlands to show that the sensitivity of gonad synthesis to environmental factors differs according to whether the gonads are initiating their gametogenesis or are at the pre-spawning stage. Gametogenesis initiation and spawning were either suppressed or delayed when individuals were held in static seawater for at least 2 months. Bouland and Jangoux (1988) suggested that the effect of these manipulations was more marked when asteroids were initiating gametogenesis. In contrast, individuals in which gametogenesis had begun showed no difference between natural field conditions and laboratory conditions. Byrne et al. (1997) have shown that the reproductive cycle of Asterias amurensis introduced in Tasmania, Australia (Byrne et al., 1997) is analogous to that of this species in Japan (Hatanaka and Kosaka, 1959; Ino et al., 1955), populations occurring at similar latitudes on either side of the equator (42–43 S and 35–41 N, respectively). Patterns of gametogenesis and spawning exhibited correlations with temperature and photoperiod cycles in both regions, though reproductive timings were 6 months out-of-phase. In Japan, gonads were mature in winter ( January) and spawning occurred between late winter and early spring (February–May) when temperatures ranged from 5 to 12 C (Hatanaka and Kosaka, 1959; Ino et al., 1955; Kim, 1968). In Tasmania, gonads were fully developed in the austral winter ( June–July) and spawning occurred between late winter and spring ( July– October) at seawater temperatures of 10–13 C (Byrne et al., 1997). It has been suggested that although temperature would be expected to have an influence given the correspondence of northern and southern seawater

24


temperature regimes, gametogenic events would be most reliably entrained by the seasonally varying photoperiod, since recovery and spawning coincided with the longest and shortest days of the year, respectively (Byrne et al., 1997). A study of Coscinasterias muricata at Governor’s Reef (Australia) revealed that significant events in the gametogenic cycle of females were associated with changes in photoperiod (Georgiades et al., 2006). A peak in pyloric caecum index coincided with the March equinox, while the gonad index was low, whereas a nearly opposite pattern occurred at the September equinox. The pyloric caecum and gonad indices were almost equal around the solstices. The summer solstice was proposed as an environmental cue for the onset of spawning as specimens appeared to spawn or be ready to spawn around this period both in 1999 and 2000 (Georgiades et al., 2006). Noticeable peaks in progesterone concentration in the pyloric caeca of the females were observed in the months immediately following the March and September equinoxes, suggesting a possible relationship (Georgiades et al., 2006). The authors also stated that gametogenesis appeared to start with the highest seawater temperatures (March), and that the spawning event coincided with the coldest seawater temperatures (September). 2.1.5. Echinoidea Pearse and Cameron (1991) suggested that temperature and photoperiod greatly influence gonad development in sea urchins. Photoperiod is the most frequent factor correlated with initiation of gametogenesis and nutritive phagocyte utilization in echinoid species (Pearse et al., 1986b; Walker and Lesser, 1998), though the specific action of the photoperiodic cue remains unclear (Walker et al., 2007). Nevertheless, evidence for the role of temperature is rapidly accumulating (Agatsuma, 2007; Agatsuma and Nakata, 2004; Cochran and Engelmann, 1975; Ito et al., 1989; Sakairi et al., 1989; Viktorovskaya and Matveev, 2000; Yamamoto et al., 1988; Yatsuya and Nakahara, 2004). Given the abundance and possibly confusing nature of the data on the photoperiodic and/or temperature control of gametogenic cycles in sea urchins, for the sake of clarity this section has been further subdivided into three sub-sections (‘‘Temperature’’, ‘‘Photoperiod’’, ‘‘Uncertain influence of temperature vs photoperiod’’). (a) Temperature Populations of Strongylocentrotus purpuratus along a latitudinal gradient exhibited very low correlation coefficients between seawater temperature and gonad development at 18 stations sampled along the west coast of the USA (Boolootian, 1966). In Oregon, gonad growth of S. purpuratus began in July, when temperature was high but variable due


25

to upwelling, and continued as temperature declined in autumn; spawning occurred at the time of lowest temperature, but did not coincide with either a particular temperature or an abrupt change (Gonor, 1973a). Similarly, Pearse (1981) found that the reproductive cycle of S. purpuratus and S. franciscanus from areas with contrasting temperature regimes did not diverge. Experimental trials conducted by Garrido and Barber (2001) with S. droebachiensis from Maine (USA) revealed that well-fed sea urchins attained similar gonad index values within 12 weeks at both 3 and 12 C, indicating that gonad growth in this species may be independent of temperature. In S. franciscanus, holding temperatures did not have any effect on the gametogenic development of captive specimens, which was similar to that of specimens from the field in California (USA) (McBride et al., 1997). Nevertheless, latitudinal gradients in gonad maturation have been noted in many species and are often perceived as evidence of the effect of temperature. For instance, populations of Diadema setosum near the equator seem to breed year long, whereas those living in subtropical areas where seasonal temperature patterns occur, have restricted summer spawning periods (Hori et al., 1987; Pearse, 1968a; Tuason and Gomez, 1979). Yonge (1940) proposed that species of tropical marine invertebrates could be categorized according to lower and/or upper sea temperatures that might limit their reproductive activity. He included D. setosum of the Indo-Pacific among the species that reproduce whenever sea temperatures are above ca. 25 C, and this inclusion has been supported by later work (Pearse, 1974; Tuason and Gomez, 1979). Iliffe and Pearse (1982) found that gonads of D. antillarum from Bermuda increased in size in spring in 1979 and 1980 as temperature rose above 20 C; gonad size then fluctuated erratically until the final drop in late fall or early winter after sea temperatures fell below 20 C. Although the latter study indicates that reproduction of D. antillarum may be restricted to periods when sea temperatures rise above ca. 20 C in Bermuda, the relatively low gonad indices found when sea temperatures exceeded ca. 25 C in August and September suggests that higher temperatures may also inhibit gonadal growth. In Curaçao and the Virgin Islands, D. antillarum is apparently ripe all year long, with a peak gonad index in winter and early spring (Randall et al., 1964). Lessios (1981) also reported that D. antillarum did not display any evident seasonality in Panama, where mean sea temperatures range between 26 and 28 C (Hendler, 1979). Reproduction of this species appears more restricted in Barbados, where spawning coincides mainly with minimum seawater temperatures (ca. 26 C) in winter and spring (Lewis, 1966). Gonadal growth and spawnings occurred mainly in late fall and winter on the Florida Keys (Bauer, 1976), when seawater temperature was below ca. 25 C. According to Pearse (1968a), D. setosum and Echinometra mathaei from the Indo-Pacific respond to sea temperature since

26


reproduction occurred when temperatures were above 25 C for D. setosum and 18–20 C for E. mathaei. Yatsuya and Nakahara (2004) found that the reproductive cycles of Anthocidaris crassispina from Wakasa Bay ( Japan) were almost synchronous between two different habitats they studied, and suggested that the reproductive cycles may be controlled by seawater temperature. Seawater temperature was also suggested to play an important role in gonad maturation of Pseudocentrotus depressus, Hemicentrotus pulcherrimus and A. crassispina whereas photic conditions (continuous light, continuous darkness, out-of-phase photoperiod) was not (Ito et al., 1989; Sakairi et al., 1989; Yamamoto et al., 1988). Furthermore, there are several reports of experimentally induced gametogenesis out-of-season in echinoids that experience marked seasonal changes in sea temperature (Khotimchenko, 1982; Sakairi et al., 1989; Townsend, 1940; Yamamoto et al., 1988). Conflicting evidence exists for triggering and inhibiting gametogenesis using both colder and warmer temperatures. Viktorovskaya and Matveev (2000) found that when the seawater temperature fell to 0 C in December, the development of gametes in populations of Strongylocentrotus intermedius on the Primor’e Coast (Russia) slowed down. In spring, when the temperature increased to 1.5–4 C, gametes at different stages of development were observed. Finally, in June, the rate of gametogenic development increased as the seawater temperature reached 10 C. Vaschenko et al. (2001) showed that lower temperatures in summer months could slightly retard gametogenesis in S. intermedius. A recent study in the south-western North Sea revealed a high level of gametogenic synchronization among individuals of Echinocardium cordatum and a nearly perfect recurrence of the same reproductive cycle over 3 consecutive years (Nunes and Jangoux, 2004). This investigation suggests that a marked drop in seawater temperature followed by a regular temperature increase would initiate gametogenesis in this species. Gametogenesis in Pseudocentrotus depressus was induced several months early by holding animals in the laboratory at 20 C, a temperature coinciding with the onset of gametogenesis in the field after a decrease from summer highs of ca. 30 C (Yamamoto et al., 1988). According to Masaki and Kawahara (1995), a decrease in temperature can advance gonad maturation of P. depressus by a month. Other investigations have determined that gonad maturation in P. depressus is promoted when individuals are kept at a constant seawater temperature of 19–20 C, but not at 13 C (Noguchi et al., 1995; Yamamoto et al., 1988). Noguchi et al. (1995) further reported that gonad maturation in the adult sea urchins was enhanced by a rise in temperature to 25 C from February to June, and then a constant seawater temperature of 20 C after July. As in Strongylocentrotus purpuratus (see below), gametogenesis in P. depressus thus appears to be inhibited by higher temperatures. In contrast, gametogenesis in Anthocidaris crassispina occurred


27

in mid-summer and could be inhibited by holding specimens continuously at low temperatures of 15 C, and triggered several months earlier by maintaining them at 20 or 25 C (Sakairi et al., 1989). In Hemicentrotus pulcherrimus, gametogenesis normally occurs in fall and early winter when the sea temperature is below 20 C; gamete growth was suppressed when the animals were held at 20 C (Yamamoto et al., 1988) or 15 C (Sakairi et al., 1989). Gonad maturation could only be initiated by a change from high (ca. 25 C) to low (ca. 15 C) seawater temperature and was inhibited at constant seawater temperatures (Ito et al., 1989; Sakairi et al., 1989). According to Ito et al. (1989), adult H. pulcherrimus that had experienced a period of rising seawater temperature to 26 C could mature and spawn ca. 45 days after the temperature was again lowered to 15 C. Seasonal changes in gonad index and gonad developmental stage indicated that spawning in H. pulcherrimus in Oshoro Bay (Hokkaido, Japan) peaked in April (Agatsuma and Nakata, 2004), later than in southern Honshu (November–April) and roughly at the same time than at Matsumae (April–June) (Agatsuma, 2007). Agatsuma (2007) concluded that seawater temperature played a major role in gonad maturation of H. pulcherrimus, whereas light did not. Gonad maturation was initiated by a decrease in seawater temperature to ca. 15 C (Agatsuma and Nakata, 2004) as observed in the southern regions (Agatsuma, 2007). Gametogenesis of the sea urchin Strongylocentrotus purpuratus was inhibited in the laboratory at temperatures above 17 C, and no gravid specimens were found when the summer sea temperature exceeded 17 C in southern California, USA (Cochran and Engelmann, 1975). Sea urchins held at normal winter temperature in the laboratory delayed spawning by nearly 2 months compared with populations in the field. Moreover, Pearse (1981) kept animals at three experimental temperatures (7, 14, 21 C), and found that gametogenesis was completely inhibited at 21 C. Nonetheless, when Pearse (1981) reviewed synchronization of gametogenesis, he found that while gametogenesis and spawning of S. purpuratus were inhibited at temperatures above 17 C, temperature changes had not been shown to play any role in synchronizing reproductive activities. Another example of suppressed gametogenesis at high temperatures was observed in individuals of Eucidaris tribuloides lacking mature spermatozoa when held at 30 C for 2 months (Lares and McClintock, 1991). (b) Photoperiod Evidence for photoperiodic control of gametogenesis in echinoids was first presented half a century ago. Giese (1959a) mentioned the possibility in an early review and a few years later Boolootian (1963) reported that the testes of Strongylocentrotus purpuratus developed mature gametes only when the sea urchins were held under long day lengths and subsequently exposed to short day lengths. While subsequent

28


short-term experiments with adults of S. purpuratus did not reveal any influence of photoperiod (Cochran and Engelmann, 1975; Holland, 1964), Leahy et al. (1978, 1981) found that gametogenesis in this species was nearly continuous when the animals were maintained in the dark at relatively low temperatures and provided with excess food. Although experiments to separate the role of light, food, and temperature were not carried out, trials and observations under variable food and temperature conditions suggested that these factors had little influence on the timing of gametogenesis in this species (Pearse, 1981). In some species gametogenesis appears to be controlled by short day lengths, e.g., Strongylocentrotus purpuratus (Bay-Schmith and Pearse, 1987; Pearse et al., 1986b), Eucidaris tribuloides (McClintock and Watts, 1990), Strongylocentrotus droebachiensis (Walker and Lesser, 1998), Paracentrotus lividus (Shpigel et al., 2004), whereas others are considered long-day species, for example, Psammechinus miliaris (Kelly, 2001). Pearse et al. (1986b) eventually confirmed the photoperiodic control of gametogenesis in Strongylocentrotus purpuratus during an 18-month study. Using field collected juveniles from Baja California (Mexico), they measured both oocyte size frequency and incorporation of 3H-labeled thymidine by the testes, showing that animals held 6 months out-of-phase with ambient photoperiod shifted their gametogenic cycle accordingly, in contrast to field and captive animals held under ambient photoperiods (Pearse et al., 1986b). Other experiments showed that individuals of S. purpuratus that were submitted to two successive 6-month periods of fall–winter photoperiods (12 h of light daily) failed to undergo substantial gametogenesis for over a year (Pearse et al., 1986b). Bay-Schmith and Pearse (1987) compared the gametogenic response of Strongylocentrotus purpuratus (California, USA) under different photoperiod regimes of fixed and seasonally changing day length. Quantification of gametogenic activity in enzymatically disaggregated ovaries and in histological sections of testes revealed that sea urchins were sensitive to both fixed and variable day lengths. After 1 year at fixed short day (8L:16D) or fixed neutral day (12L:12D), the gonads were ripe and undergoing gametogenesis, as were gonads of animals reared with varying photoperiod and sampled during the short-day phase of the cycle (Bay-Schmith and Pearse, 1987). Under fixed long day (16L:8D), the gonads did not contain significant numbers of gametes and had the constitution of gonads found in animals reared at varying photoperiod and sampled during the long-day phase of the cycle (Bay-Schmith and Pearse, 1987). Such findings suggest that gametogenesis in this species is sensitive to the absolute number of hours of light or dark. Photoperiods of 12 h or shorter promote growth of oocytes to full size and their maturation into ova in females, and the production of


29

spermatocytes and spermatozoa in males. In contrast, a regime of 15–16 h of light inhibits vitellogenesis and spermatogenesis. In S. purpuratus, gametogenesis is therefore likely under control of a critical day length of less than ca. 12 h (Bay-Schmith and Pearse, 1987). In the Gulf of Maine, the initiation of gametogenesis in Strongylocentrotus droebachiensis appears to be triggered by the onset of shortening day length in the fall (Walker and Lesser, 1998). The authors suggested that the changing photoperiod in autumn might lead to activation of oogonial or spermatogonial mitosis directly through a mitogen-induced mechanism or, alternatively, might result in mobilization of nutrients from nutritive phagocytes which would then stimulate gonial cell mitosis (Walker and Lesser, 1998). In the field, gonial cell mitosis occurs as seawater temperature drops from 17 to 13 C in autumn; in the experimental study of Walker and Lesser (1998), it occurred as temperature rose from 11 to 14 C. Low temperatures are probably required to complete vitellogenesis in this species. Bo¨ttger et al. (2006) have studied the effects of invariant summer versus progressing ambient (fall/winter) photoperiod regimes on the gonads of Strongylocentrotus droebachiensis from north-eastern USA. They observed that males and females maintained on commercial feed under invariant photoperiod did not initiate annual gametogenesis (Fig. 2.3), although some production of new spermatozoa was noted (Walker et al., 2005). Male and female gonads reached large sizes due to proliferation of nutritive phagocytes. In the ovaries, a few residual primary oocytes remaining from the previous year also grew (Walker et al., 2005). Dumont et al. (2006) showed that once gametogenesis was initiated in Strongylocentrotus droebachiensis spawning could not be halted by photoperiod regulation (Fig. 2.4). In other species, individuals collected from the wild and held under experimental conditions retained their internal reproductive calendars for long periods of time (Leahy et al., 1981). Dumont et al. (2006), however, suggested that the rate at which echinoids progress through the various developmental stages of gamete synthesis can be affected by the photoperiod regime. By the end of the 12-week experiment, sea urchins in all fed photoperiod treatments had completely spawned out, but the proportion of individuals in the recovering and growing stages were markedly different, the 16-h daylight treatment group having by far the greatest percentage of individuals in the growing stage (Dumont et al., 2006). A more direct influence of light was observed in Strongylocentrotus nudus from eastern Russia by Evdokimov et al. (2001) who found that light of wavelength 720 nm activated gonad development, while at 520 nm it had a suppressive effect by decreasing the oogonial and spermatogonial content without disturbing the cellular structure. In Stylocidaris affinis from the Gulf of Naples (Italy), the discrete reproductive cycle and the lack of seasonal fluctuations in temperature, salinity and other factors support photoperiod as the major factor affecting the

30


Figure 2.3 Strongylocentrotus droebachiensis (Echinoidea). Representative ovary (A) and testis (B) of individuals maintained for 5 months at constant photoperiod showing predominance of nutritive phagocytes and few gametes. A few residual primary oocytes (RO) are present (but no new ones) near the ovarian wall and limited numbers of new spermatozoa (arrows) are evident between the expanded nutritive phagocytes, as are spermatogonial mitoses among the spermatogenic cells (SC). Representative ovary (C) and testis (D) of individuals maintained for 5 months at ambient photoperiod showing growing residual (RO) and new (NO) primary oocytes in nutritive phagocyte incubation chambers. The testicular lumen is filled with new spermatozoa and the nutritive phagocytes (dark granules containing cells) are reduced in size with only a slender strand of cytoplasm connecting them to the testicular wall. Circle denotes spermatogonial mitosis (SC); C, coelom. Scale bars ¼ 50 mm. Reprinted with permission from Bo¨ttger et al. (2006).

31


0 week 100

4 weeks

(30)

(15)

(14)

(13)

(15)

0D

(9)

(13)

(14)

(14)

(15)

(10)

8D

16D

24D

Recovering Growing Premature Mature Partly spawned Spent

80 60 40

Frequency (%)

20 0

8 weeks 100

12 weeks

(15)

(15)

(15)

(13)

Ambient

0D

8D

16D

(15)

80 60 40 20 0

24D Ambient Photoperiod

Figure 2.4 Strongylocentrotus droebachiensis (Echinoidea). Mean frequency (%) of fed sea urchins at various gametogenic stages at each sampling date for the five photoperiod treatments: 0D, 0 h darkness per day; 8D, 8 h darkness per day; 16D, 16 h darkness per day, 24D, 24 h darkness per day, Ambient, ambient photoperiod with natural light. Numbers in parenthesis indicate the sample size. Reprinted with permission from Dumont et al. (2006).

reproductive cycle (Holland, 1967). The marked annual fluctuations in photoperiod probably influence reproduction in the sea urchins from Bocca Piccola, where the water is clear and receives sufficient light at 70 m to support growth of macro-algae. However, Holland (1967) estimated that the long periods of oocyte growth and spermatocyte accumulation did not closely follow photoperiod, nor did the short periods of spawning, initiation of oocyte growth, and initiation of spermatocyte accumulation. Even when photoperiod does not exert a direct influence on sea urchin reproduction, it may serve as a periodic reference point to synchronize an endogenous reproductive rhythm (Holland, 1967). Photoperiod could also have an important indirect effect on reproduction by influencing the quantity and quality of the algal food available to the sea urchins (Holland, 1967). McClintock and Watts (1990) studied Eucidaris tribuloides from Florida (USA) under two variable and two fixed photoperiod regimes at a constant

32


temperature for a year to demonstrate the role of photoperiod in the regulation of gametogenesis. Individuals maintained 6 months out-ofphase with the ambient photoperiod did not become reproductively mature until March, indicating that gametogenesis was delayed until the day length decreased during the artificial winter photoperiod. Sea urchins held under fixed long days (15L:9D) delayed gametogenesis for the entire year; and only ca. 20% of them developed mature gonads. Sea urchins held under fixed short days (9L:15D) produced mature gametes throughout the year, and mature gonads were found in ca. 60% of these individuals. These observations suggest that short days or long nights enhance and entrain gametogenic development in E. tribuloides (McClintock and Watts, 1990). On the other hand, gametogenesis in Japanese echinoid species is apparently not under photoperiodic control (Sakairi et al., 1989; Yamamoto et al., 1988). Groups of laboratory-reared Pseudocentrotus depressus all developed ripe gonads at about the same time when held under ambient, out-of-phase, constant dark, and constant light conditions. Similarly, laboratory-reared Hemicentrotus pulcherrimus developed ripe gonads in early winter, and laboratory-reared Anthocidaris crassispina developed mature gonads in midsummer, whether they were held in constant dark, constant light, or ambient conditions. These authors suggest that the timing of gametogenesis is regulated by an endogenous temporal program and critical changes in sea temperature (Sakairi et al., 1989; Yamamoto et al., 1988). For details, see sub-section Temperature above.

(c) Uncertain influence of temperature versus photoperiod In some species, the respective roles played by temperature and photoperiod are somewhat unclear, either because of the incomplete or inaccurate environmental data available, or because experimental results are ambiguous. The influence of temperature and light on the reproductive cycle of Echinometra mathaei is not well understood. Based on the prediction of Pearse and Phillips (1968) that a minimum temperature (18 C) is required for the onset of gametogenesis, spawning in Kenya would be expected to occur year round (Muthiga, 2005) as it does in Rottnest Island, Western Australia (Pearse and Phillips, 1968), where seawater temperatures range from 18 to 22 C (Hodgkin et al., 1959). However, along the Kenyan coast, which is characterized by temperatures of 24–31 C, E. mathaei exhibits a restricted reproductive cycle (Muthiga, 2005), as in areas with a wider range of temperatures, such as Seto and Okinawa, Japan (Arakaki and Uehara, 1991; Onoda, 1936), Wadi el Dom, Gulf of Suez (Pearse, 1969b), and the eastern coast of South Africa (Drummond, 1995). Paradoxically, populations of E. mathaei from the northern Red Sea, closer to the equator, spawn throughout the year (Pearse, 1969b). Thus, seawater temperature is


33

apparently not the main factor controlling gametogenic development of this species along the coast of Kenya (Muthiga, 2005). In Centrostephanus rodgersii from New South Wales (Australia), an increase in the rate of gametogenesis in May and the onset of breeding in June–July occurred at all locations studied over 9 of latitude (Byrne et al., 1998). This reproductive synchrony suggests that reproductive processes are controlled by exogenous factors operating at all locations, the most probable one being photoperiod according to the authors. They state that gametogenesis is probably initiated in April as days become shorter than nights and argue that while gamete production and spawning occur as sea temperature is decreasing, this factor would not provide a uniform cue at all the locations studied (Byrne et al., 1998). Furthermore, given the contrasting winter temperatures to which northern and southern populations are exposed, C. rodgersii likely does not require a temperature threshold to initiate reproductive processes, though temperature may still act on gamete storage and length of the spawning period (Byrne et al., 1998). Experimental trials conducted in Scotland have shown that the reproductive cycle can be altered by the manipulation of photoperiod or temperature regimes in Psammechinus miliaris (Kelly, 2001). The author wished to investigate the effect on gametogenesis of removing a specific environmental cue (either increasing spring days or increasing seawater temperatures). In the absence of increasing spring day lengths, the proportion of males and females producing mature gametes decreased significantly, indicating that reproduction in this species is influenced by photoperiod (Kelly, 2001). However, short days did not prevent the onset of gametogenesis, and no demonstrable difference in the developmental stages was found until late spring (Kelly, 2001). Cold water (in winter) was apparently important for the completion of oogenesis and less critical for spermatogenesis. Significantly fewer females in the temperature-controlled treatment produced mature oocytes, whereas there was no significant difference in the numbers of mature males found among the temperature treatments (Kelly, 2001). The investigator further determined that the temperature cue required by P. miliaris was between 6.2 and 9.8 C. The European echinoid Paracentrotus lividus has been studied in several regions, as well as under laboratory conditions, generating abundant yet occasionally conflicting results. On the west coast of Ireland, the species exhibits maximal periods of gonadal growth coinciding with decreasing sea temperatures and a day length of 13 C, and proceeded until temperature reached a maximum of ca. 18 C in August. Important differences, or the occurrence of one or two annual peaks, can be observed within a given region, as well as between localities and habitats. For instance, Byrne (1990) recorded inter-annual variations in spawning of P. lividus in Ireland, with the onset of gamete release differing by as much as 4 weeks between years. One hypothesis is that the zoogeographic differences in spawning may reflect the existence of different ‘‘physiological races’’ of P. lividus that spawn at different temperatures at the different latitudes (Byrne, 1990). The spawning season of Strongylocentrotus nudus (September and October) corresponded to a drop in seawater temperature from 25 to 20 C in Wakasa Bay, Japan (Tsuji et al., 1989), and from 20 to 15 C in Tohoku and Hokkaido (Agatsuma et al., 1988; Odagiri et al., 1984; Sugimoto et al., 1982). The reproductive period of Hemicentrotus pulcherrimus in Japan appears to vary among locations, depending on the temperature regime. In eastern Fukui, spawning took place from December to April, at a time when the temperature fell from 13 to 10 C and rose again to 13 C, maximum gamete release occurring in January–March when seawater temperature was ca. 10 C (Kawana, 1938). In northern Kyushu, sea urchins spawned from December to May as seawater temperature fell to 3 days (Fig. 3.3). Although it is now apparent that Strongylocentrotus droebachiensis responds to phytoplankton by releasing gametes under laboratory conditions, the relationship established from field observations is not always as clear according to compilations by Starr et al. (1993) and Seward (2002) (Table 3.2). For example, Munk (1992) found that the onset of spawning in S. droebachiensis from Kodiak (Alaska, USA) coincided with the spring phytoplankton bloom (late March–April) in two of the 3 years investigated. In the third year, however, spawning started 6–8 weeks after the bloom. Likewise, a study by Seward (2002) demonstrated that most populations of S. droebachiensis in Maine (eastern USA) spawned when chlorophyll a concentrations were low (ca. 2 mg m3), only one group spawning at concentrations

Tidal amplitude (m)

5 4 3 2 1

Temperature (⬚C)

12

Urchin spawning

Urchin spawning

8 4

Seasonal trend

Minimum point of the seasonal trend

30 20 Daily mean

Chlorophyll a (mg • m−3)

8 6 4 2 0

Gonadal Index (%)

10

20 16 12 8 4

Daily mean

Minimum point of the seasonal trend

Strongylocentrotus droebachiensis

Gonadal index Gonadal index Mature oocytes

April

May

Mature oocytes

June 1983

July

April

May

June

July

100 80 60 40 20 0

Mature oocytes (%)

Salinity (ppt)

Seasonal trend

Daily mean

Daily mean

0

1984

Figure 3.3 Strongylocentrotus droebachiensis (Echinoidea). Temporal variations in the mean gonad index and the percentage of mature oocytes (n ¼ 30) in relation to tidal amplitude, daily mean temperature and salinity, and chlorophyll a concentration in the St. Lawrence Estuary (eastern Canada), during the spring and summer of 1983 and 1984. Vertical lines represent 95% confidence intervals. Reprinted with permission from Starr et al. (1993).

Table 3.2 Spawning periods of the green sea urchin Strongylocentrotus droebachiensis with respect to temperature and phytoplankton blooms. Adapted from Seward (2002) and Starr et al. (1993) Location

Spawning period

Seawater temperature

Phytoplankton bloom

Pointe-au-Pe`re (QC, Canada) St. Lawrence Estuary (QC, Canada) Gulf of St. Lawrence (eastern Canada) Gulf of St. Lawrence (eastern Canada) Portugal Cove (NL, Canada) St. Margaret’s Bay (NS, Canada)

June (Starr et al., 1993)

4–10 C (Starr et al., 1993)

June (Starr et al., 1993)

4–10 C (Starr et al., 1993)

Ends in May (Starr et al., 1993) Early July

90% were usually obtained. However, ‘‘nirina’’ was ineffective on the gonadal tubules or via injection into the coelomic cavity (Rasolofonirina et al., 2009). Kato et al. (2009) purified a gonadotropic neural peptide (NGIWYamide) from the buccal ring nerve of Apostichopus japonicus which induced gamete release after injection into mature males and females. A synthetic derivative (NGLWYamide) was 10 times more potent than the natural NGIWYamide. The gametes obtained through this induced spawning were successfully fertilized, developed normally and metamorphosed into young holothuroids. Unlike ‘‘nirina’’, the peptides were ineffective in directly inducing maturation and germinal vesicle breakdown in follicle-enclosed or follicle-free oocytes, requiring the ovarian wall to induce oocyte maturation (Kato et al., 2009), much like the radial nerve factor (RNF) in the asteroid Pisaster ochraceus (Schuetz, 2000). The data suggest that ‘‘nirina’’ and the neural peptide act at different levels of the spawning cascade. Stevens (1970) reported that 1-MA (which induces oocyte maturation in asteroids) failed to induce spawning of Parastichopus (¼Stichopus) californicus. In the sea cucumber Leptosynapta inhaerens, immature oocytes connected by a thick follicular envelope inside the ovotesticular fragments neither spawned nor were induced to mature by 1-MA, whereas the ovotestis shed sperm immediately upon treatment (Ikegami et al., 1976). Thus, during gamete shedding in Leptosynapta, 1-MA seems to act on the gonadal nerve cells or at the neuromuscular junctions. Using extracted oocytes, Smiley (1984, 1988a) and Maruyama (1985, 1986) determined that an RNF acted through the follicle cells to produce a maturation-inducing substance (MIS) leading to germinal vesicle breakdown (GVBD) in several holothuroids: Parastichopus (¼Stichopus) californicus, Holothuria leucospilota, H. moebi, H. pardalis, H. pervicax and Apostichopus (=Stichopus) japonicus. Maruyama (1985) noted that follicle-free oocytes in H. leucospilota did not undergo GVBD when exposed to tissue extracts containing RNF. Oocytes of P. californicus exhibited higher levels of GVBD when isolated ovarian tubules were incubated in an aqueous extract containing RNF from asteroids (Maruyama, 1986; Strathmann and Sato, 1969) or conspecific holothuroids (Smiley, 1988a). Furthermore, according to Maruyama (1985), the maturation-inducing properties of RNF were neither species-specific nor sex-specific, and were only effective on oocytes with intact follicle cells, suggesting that a secondary factor (MIS) produced by the follicle cells was necessary for oocyte maturation to proceed. This MIS would be the equivalent of 1-MA in sea stars. Hufty and Schroeder (1974) demonstrated that the ovaries of Parastichopus (¼Stichopus) californicus produced a substance similar to 1-MA when incubated in vitro with an extract containing RNF from the sea star Patiria miniata. This holothuroid MIS induced GVBD in oocytes of both the sea star and the sea cucumber, although the reaction of the latter was less


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marked and less consistent. The investigators stated that the endocrine significance of the holothuroid MIS remained unclear. Indeed, it has been shown that sea star RNF can induce maturation of follicle cell-free oocytes of sea cucumbers (Maruyama, 1986), although this response may be due to the contamination of RNF extracts by a true MIS or other stimulating agent(s) (Smiley et al., 1991). Similarities between 1-MA and the holothuroid MIS were supported by preliminary characterization (Hufty and Schroeder, 1974) and only one report of spawning induction by 1-MA in the sea cucumber Leptosynapta inhaerens (Ikegami, 1976). Most investigators failed to induce maturation in holothuroid oocytes with 1-MA (Hufty and Schroeder, 1974; Kishimoto et al., 1982; Maruyama, 1980, 1986; Smiley, 1988a). Smiley (1988a) further purified the MIS in P. californicus, found it to be clearly different from 1-MA, and suggested that it might be a 2,8disubstituted adenine. The pathway through which RNF acts on the gonad is unclear, although the anatomy of holothuroids and asteroids suggests that the radial haemal sinus is a possible mode of transport (Smiley et al., 1991). While the discovery of RNF in the radial haemal sinus of a sea star by Caine and Burke (1985) lent some credibility to the hypothesis, some reservations have been expressed concerning the ability of these minute passages to translocate RNF efficiently (Smiley et al., 1991). Alternatively, transport through the peritoneal nerve cells has been proposed (Smiley and Cloney, 1985; Smiley et al., 1991), but the issue of RNF action has yet to be resolved in echinoderms. Because GVBD induction by RNF reportedly takes 2–4 h in holothuroids (Maruyama, 1985, 1986; Smiley, 1988a), Smiley et al. (1991) suggested that a proximal signal would have to be perceived several hours before gamete release. However, shorter delays have been reported for hormonally activated ovulation, GVBD and maturation to occur in holothuroids. For instance, the oocytes of Holothuria leucospilota consistently required ca. 85 min to achieve competency, from the natural onset of ovulation to the final broadcast (Hamel and Mercier, 2007). Similarly, a recently purified neural peptide induced spawning within 70–90 min in females of Apostichopus japonicus (Kato et al., 2009). Furthermore, stress of capture and the induction methods used in aquaculture resulted in the release of fully fertilizable oocytes in ca. 60 min by individuals that had not previously shown any signs of spawning activity (Hamel and Mercier, 2004; Hamel et al., 2001; Mercier and Hamel, 2002; Reichenbach, 1999). Smiley et al. (1991) proposed that a concerted contraction of actin microfilaments promotes extrusion of oocytes from the follicle, but it is unclear how this can be triggered within the ovaries. Furthermore, spontaneous ovulation occurs in Parastichopus californicus but not in most other sea cucumbers. This species also possesses a very distinctive ovarian tubule recruitment mechanism (Smiley, 1988b) which is shared only by a small

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number of anatomically similar species (Sewell et al., 1997). Hence, although holothuroid oocytes are normally ovulated before spawning, the factors involved remain poorly understood. Experiments with RNF usually involve extracted gametes and/or a number of manipulations, which can influence oocyte maturation and the time needed for it to be completed. Smiley (1984, 1988a) and Maruyama (1985, 1986) used such methods to predict that an RNF acted on the follicle cells to produce the MIS leading to GVBD in holothuroids. However, a recent in vivo study (Hamel and Mercier, 2007) suggests a different mechanism as (1) GVBD was completed well after extrusion of oocytes from the follicle cells and (2) GVBD was never observed in oocytes collected in the lumen of the ovarian tubules or in the gonad basis after ovulation but before passage through the proximal constricted section of the oviduct, no matter how long they were left to soak in seawater (Fig. 3.7). Two hypotheses can be offered: (1) the action of RNF via follicle cells must be combined with mechanical activation (i.e., passage through the constricted duct, or pipetting in the case of in vitro studies) and (2) RNF acts through another pathway inside the gonoduct (Hamel and Mercier, 2007). Oocytes of several sea cucumbers, including Holothuria leucospilota respond to sea star RNF by undergoing GVBD even when denuded of their follicle cells (Maruyama, 1986), suggesting that other ovarian components may indeed produce the MIS. Such inconsistencies stress that in vitro studies of oocytes, which can involve manipulations such as squeezing, pipetting, rinsing, soaking in seawater and other media, centrifugation, and injection provide valuable data for elucidating cellular processes but do not necessarily reflect the actual in situ sequence. Further in vivo investigations may shed new light on the fine control of oocyte maturation in the hours or minutes before spawning and on the sequential involvement of RNF, MIF and other factors, but it is becoming clear that we must not expect to find a uniform pattern among holothuroids. The perivisceral coelomic fluid of several tropical holothuroids becomes bioactive immediately prior to and during spawning, eliciting gamete release in non-spawning individuals when injected or spread in the surrounding water (Mercier and Hamel, 2002). See Section 4.2 for details.

5.4. Asteroidea Mechanisms of final oocyte maturation and spawning have been mainly investigated in asteroids (Kanatani and Nagahama, 1983). As a result, the gonad-stimulating hormone of sea stars is among the better studied endogenous factors in echinoderms. Chaet and McConnaughy (1959) were the first to report that the injection of a hot-water extract of the radial nerve of Asterias forbesi induced gamete release in ripe females and males. The presence in the radial nerve of a substance responsible for inducing gamete

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A

(1)

(2)

(3)

o GP OT

FC GV

L

B o L GV

C o L

D o

JC L

Figure 3.7 Holothuria leucospilota (Holothruoidea). Schematic representation of oocyte maturation and passage through the gonoduct during spawning (not to scale). Sections of the reproductive tract are divided into: (1) gonad basis (and attached ovary), (2) proximal section, and (3) distal section of the gonoduct. Transient deformations are illustrated by dashed lines, and insets show an enlarged view of the oocytes. T0 marks

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shedding was suspected, and later confirmed. Similar data have since been obtained for several sea star species (Kanatani, 1979). Cross-assays among different species have shown that the radial nerve factor acts, with some exceptions, in a non-species-specific manner (Kanatani, 1973). Positive responses were noted in whole animals receiving the nerve extract (Chaet, 1964; Kanatani and Noumura, 1962; Noumura and Kanatani, 1962) as well as in isolated ovary, testis or gonad fragments to the RNF (Chaet, 1966; Kanatani, 1964). The substance was thus believed to act directly on the gonad, an assumption that was confirmed by partial application of RNF to the whole ovary, in which case the treated portion alone released the oocytes (Kanatani, 1964). The substance was called the ‘‘gamete-shedding substance’’ (GSS), and is apparently present in the radial nerve throughout the year in nearly equal amounts, irrespective of the breeding season (Chaet, 1967). A number of manipulations have been conducted to localize the GSS. An extract prepared from male nerves induced gamete release in both sexes (Chaet, 1964). Furthermore, the GSS level in the radial nerve when assayed with isolated ovarian fragments in vitro in the presence of isolated ovarian fragments was equal in both sexes and also constant along the radial nerve and circumoral nerve ring (Kanatani and Ohguri, 1966). Other body components that are rich in nervous tissue such as the epidermis, tube feet, and cardiac stomach, have also been found to contain GSS, although its activity in these tissues is much lower than in the radial nerve (Kanatani and Ohguri, 1966). The fact that GSS is present in the coelomic fluid only when sea stars are undergoing natural spawning suggests that GSS is a hormone (Kanatani and Ohguri, 1966; Kanatani and Shirai, 1970). According to data from granules isolated from homogenates of the radial nerves of Asterina pectinifera by differential centrifugation and sucrose density gradient ultracentrifugation, and to histological studies using neuro-secretory staining in several asteroid species, granules containing GSS have been determined to occur in the supporting cells located just beneath the outer sheath of the radial nerve (Atwood and Simon, 1971; Imlay and Chaet, 1967; Unger, 1962). Similar structures were also found in the subepithelial plexus the onset of side-to-side sweeping movements in spawning females. (A) T0 15 min: mature oocytes in the ovarian tubules (OT), just before ovulation. FC, follicle cells; GV, germinal vesicles; GP, gonopore; L, lumen. (B) T0 þ 20 min: following ovulation, oocytes are transferred from the ovarian tubules to the gonad basis, where they are still not fertilizable. (C) T0 þ 30 min: oocytes are moving from the gonad basis through the proximal section of the gonoduct into the distal section, where they complete germinal vesicle breakdown, although most are still not fertilizable unless presoaked in seawater. (D) T0 þ 55 min: oocytes are lying in the distal section of the gonoduct, which begins to form a bulge under the gonopore. Seawater begins to enter, hydration of the jelly coat ( JC) occurs, and the majority of the oocytes become fertilizable. Broadcast will occur within ca. 15 min. Reprinted with permission from Hamel and Mercier (2007).


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of the tube feet, body wall, and cardiac stomach where GSS activity had been detected. In contrast, no GSS granules or GSS activity were found in the pyloric caecum, presumably because its extensive nerve plexus has no supporting cells (Atwood and Simon, 1971; Kanatani and Ohguri, 1966). Unger (1962) studied the transport of the fuschinophilic granules present in supporting cells along the fibres and suggested that GSS could be conveyed in a similar fashion to the radial and transverse haemal canals and through the water vascular system to the coelomic cavity, where the gonads are suspended. During the early investigations, GSS was believed to be a direct inducer of spawning in sea stars (Chaet, 1967), but later experiments have revealed that the action of this hormone is indirect, and that it acts on the ovary to produce a second active substance which induces oocyte maturation and spawning (Kanatani and Shirai, 1968; Kanatani et al., 1969; Schuetz and Biggers, 1968). GSS was shown to enter the ovary and act on the follicle cells around the oocytes to produce this second hormone (Cloud and Schuetz, 1973a,b; Hirai and Kanatani, 1971; Hirai et al., 1973), which has been isolated from ovarian fragments of Asterias amurensis and identified as 1-methyladenine (1-MA) (Kanatani et al., 1969). The gamete-shedding substance was later renamed the gonad-stimulating substance (GSS), retaining the same acronym (Kanatani, 1967). Isolated ovarian fragments undergo spawning in seawater containing 1-MA and ripe sea stars are induced to spawn when 1-MA is injected into the coelomic cavity (Kanatani, 1969). This author found that oocyte release in Marthasterias glacialis and A. forbesi occurred within ca. 30 min of injection of 30 mg 1-MA, whereas sperm release began after a slightly shorter latent period. The short interval preceding discharge of gametes after injection of GSS indicates that 1-MA production, presumably in the follicle cells, begins immediately after GSS is detected (Kanatani, 1969; Kanatani and Shirai, 1970). Mita (1993) confirmed that the amount of 1-MA produced by the follicle cells of Asterina pectinifera was sufficient for meiosis initiation and release of oocytes, and Mita and Nakamura (1994) concluded that the 1-MA content of sea star ovaries was sufficient to induce GVBD and ovulation. On the other hand, Schuetz (2000) provided evidence of extra-follicular mediation of oocyte maturation by RNF in Pisaster ochraceus, suggesting that other ovarian components could be a source of 1-MA. The effectiveness of 1-MA in inducing ovulation and spawning, either through intra-coelomic injection or soaking of the extracted ovaries, appears to be universal in asteroids, and has been shown in many species, for example, Patiria miniata, Pisaster brevispinus, Pisaster giganteus, Pisaster ochraceus, Pycnopodia helianthoides, Mediaster aequalis (Stevens, 1970), Pteraster militaris (McClary and Mladenov, 1989), Patiriella regularis (Byrne and Barker, 1991), Acanthaster planci (Babcock et al., 1994), Leptasterias polaris (Hamel and Mercier, 1995b), Coscinasterias muricata (Babcock et al., 2000),

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Smilasterias multipara (Komatsu et al., 2006) and several Antarctic species (Bosch and Pearse, 1990; Stanwell-Smith and Peck, 1998). The role of 1-MA in spawning induction is reportedly due to its capacity to dissolve the cementing substance that lies between the follicle cells and between the follicles and the oocytes (Kanatani and Nagahama, 1983). Ripe oocytes isolated from Asterina pectinifera and treated with 1-MA begin follicular envelope breakdown within half and hour; shrinkage of the envelope into a small clump may be due to contraction of the individual follicle cells which seem to be in an extended state (Kanatani and Shirai, 1969, 1970). Cytochalasin B, which is an inhibitor of certain contractile processes, immobilizes the follicle cells on the surfaces of oocytes treated with 1-MA (Schroeder, 1981), suggesting that cell contraction is the cause of the breakdown of the follicular envelope. Whether the action of 1-MA on the cementing substance is direct or indirect (i.e., activating an enzyme responsible for dissolving the cement) is not yet known (Kanatani and Nagahama, 1983). Once the follicular envelopes around the oocytes are removed by the action of 1-MA, the denuded oocytes become free within the lumen of ovary and are expelled by contraction of the ovarian wall (Kanatani and Shirai, 1969). When ovarian fragments of sea stars Asterias amnurensis were placed in seawater devoid of Mg2þ, they began to release oocytes after ca. 30 min (Kanatani and Shirai, 1969). Furthermore, ovarian fragments kept in Ca2þfree seawater for more than 30–45 min shed oocytes when Ca2þ was added, implying that lack of Ca2þ causes dissolution of the cementing substance and breakdown of the follicular envelope and that contraction of the ovarian wall, caused by the addition of Ca2þ, then forces out the loosened oocytes. Since bivalent cations such as Ca2þ and Mg2þ are known to stabilize intercellular cementing substances, spawning induced by the absence of these ions is attributable to the breakdown of the follicular envelope due to dissolution of the cementing substance. Isolated ovaries do not release oocytes when placed in seawater devoid of Ca2þ even in the presence of GSS (Mecklenburg and Chaet, 1964; Schuetz and Biggers, 1968), indicating that while contraction of the ovarian wall appears to be essential for carrying out the discharge of oocytes, dissolution of the cementing substance leading to follicular disintegration is a prerequisite for such contraction (Kanatani and Shirai, 1969). Tension has been detected in the ovarian wall of Asterina pectinifera after treatment with 1-MA (Shirai et al., 1981), suggesting that a jelly-like substance presumed to come in contact with the ovarian wall as a result of breakdown of the follicular envelopes may act as a direct inducer of tension in the ovarian wall. Since isolated ovarian walls that are stretched do not generate tension immediately when the jelly substance from mature oocytes is applied, 1-MA possibly induces ovarian contraction indirectly by allowing contact between the jelly and the ovarian wall (Shirai et al., 1981).


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Ever since the natural mitogen that converts the vitellogenic oocytes of asteroids into fertilizable oocytes was identified as 1-MA, extensive investigations have failed to isolate its receptor and early transduction pathway. Nevertheless, several elements of the signalling pathway that link the 1-MA receptor to MPF activation and maturation have been reported (e.g., Sadler and Ruderman, 1998; Tadenuma et al., 1992).

5.5. Echinoidea Unlike the oocytes of other echinoderms, those of sea urchins attain full maturity within the ovaries. Gamete release can be easily induced through injection of contraction-inducing substances like potassium chloride (KCl) and acetylcholine, or by applying an electric stimulus. Gonads readily respond to these stimuli by contraction of the gonadal wall and discharge of gametes (Appendix A10). A substance similar to sea star GSS has been detected in sea urchin radial nerves. Cochran and Engelmann (1972) reported that an extract of the radial nerves of Strongylocentrotus purpuratus induced spawning within 1 min in this and other species of sea urchins. The same extract also triggered spawning in sea stars after an average delay of 45 min. The GSS of Strongylocentrotus, a heat-stable polypeptide, presumably stimulated sea urchin gonads to produce a non-protein gonad factor which, like 1-MA, caused testis fragments to spawn (Cochran and Engelmann, 1975). This gonad factor co-migrated with 1-MA in thin layer chromatography (Cochran and Engelmann, 1972) but was not identified definitively. Since oocyte maturation is continuous and asynchronous throughout the breeding season in S. purpuratus (Chatlynne, 1969), Cochran and Engelmann (1972) suggested that significant levels of this gonad factor must be constantly maintained to induce spontaneous oocyte maturation, but no seasonal values of this gonad factor have been reported. Currently, the mode of action and transfer of this radial nerve factor (RNF) is unknown. Wasson and Watts (2007) speculated that nutritive phagocytes synthesize and store this gonad factor and discharge it upon stimulation by the RNF. The gonad factor subsequently triggers the release of neighbouring gametes or stimulates the contraction of the muscular epithelium, forcibly releasing gametes from the gonad lumen. The authors further presumed that the gonad factor is synthesized and stored in the neurons or epithelial cells of the peritoneum and released to stimulate contraction of the muscular epithelium in the presence of the RNF. Stevens (1970) reported that 1-MA failed to induce spawning of the echinoid Dendraster excentricus. In contrast, Kanatani (1974) found that high concentrations of 1-MA increased the proportion of oocytes maturing into ova in isolated ovarian fragments of Anthocidaris crassispina. Furthermore, gonadal extracts of several echinoids (Aeudocentrotus depressus, Anthocidaris

crassispina, Hemicentrotus pulcherrimus, Clypeaster japonicus and Peronella japonica) that induced maturation of oocytes in the asteroids Asterina pectinifera and Asterias amurensis contained 1-MA. According to Kanatani (1974), the presence of 1-MA in the ovaries of echinoids, particularly at the peak of the breeding season, could explain how oocytes can undergo maturation long before the onset of spawning.

C H A P T E R

F O U R

Discussion Contents 170 170 172 174 175 176

1. Methodological Considerations 1.1. Gonad index 1.2. Histology 1.3. Laboratory observation and experimentation 1.4. Field observations 1.5. Sampling interval and replication 1.6. Possible impact of climate change and anthropogenic disturbances 2. Insights from the Deep Sea 3. Emerging Trends and Future Research 3.1. Perception of cues 3.2. Understanding the role of food supply, temperature and photoperiod 3.3. Latitudinal effects 3.4. Heterospecific simultaneous spawnings 3.5. Final remarks

179 181 182 183 184 188 190 191

In common with earlier reviews (Giese and Pearse, 1974; Giese et al., 1991), we are obliged to recognise that the timing of reproductive events is undeniably variable. In some species, reproduction is aperiodical and apparently ‘‘continuous’’ (at least at the population level, though not necessarily at the individual level), whereas in others it is periodical, ranging from biennial/annual to semi-monthly. Breeding seasons at the population level tend to be variable, sometimes according to latitude. Nevertheless, it is becoming increasingly evident that a number of exogenous factors synchronize reproduction in echinoderm species. While considerable progress has been made over the past decades, our understanding is far from complete and only more research into this field will allow us to paint a comprehensive picture of the forces that drive reproductive processes and strategies in echinoderms. The current state of knowledge may simply reflect our inability to evaluate the reproductive cycles properly, most studies being of insufficient duration and/or detail to measure reproductive variability in space and time. We will consider a few of the most important methodological limitations in

Advances in Marine Biology, Volume 55 ISSN 0065-2881, DOI: 10.1016/S0065-2881(09)55004-3

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this field of research before outlining the common trends and hypotheses emerging from this review and the questions that merit more attention in the future.

1. Methodological Considerations The types of data deemed useful in determining reproductive periodicity (Giese and Pearse, 1974) have not changed much over the past decades. They can still be summarized as (1) rough estimates of the amount of material expended during the reproduction, estimated from changes in the gonad index; (2) transformation of gonadal cells during the gametogenic cycle as revealed by light and electron microscopy; (3) time course of gametogenesis, measured in successive samples taken from a population of animals or, when feasible, from the same animal; and (4) time and conditions under which spawning occurs, from laboratory and/or field observations. Major flaws and inaccuracies emerge when only one of these elements is studied, independent of the others.

1.1. Gonad index The oldest and most widely used quantitative method for estimating reproductive activity is the gonad index (GI) (Giese and Pearse, 1974), also termed gonadosomatic index (GSI). Although not precise, the technique is particularly suitable for routinely handling large numbers of samples. The GI is calculated in several ways, but is usually defined as the ratio of the gonad wet weight (or volume) to the wet weight (or volume) of the body wall, test or whole animal, expressed as a percentage. Because the body cavity can hold variable amounts of water and the digestive tract may or may not contain food, variations of GI can occur that are unrelated to reproduction. Therefore, determining ratios for eviscerated body wet weight or dry weight is more meaningful. One assumption of the method is that GI is independent of body size. Correlation between GI and body size should always be checked by regression analysis and individuals of similar size selected for the determination of the index. In particular, the relationship between gonad size and body size varies between juveniles and adults (Giese and Pearse, 1974; Gonor, 1972). Another important limitation of the GI method is that unless it is combined with microscopic examination of the gonadal tissues, it provides little indication as to what is occurring within the gonads. Many investigators have cautioned against relying on the GI alone, because it gives little indication of the development of the gametes themselves, and consider that it should always be used in combination with


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histological techniques (Nichols and Barker, 1984b,d; Nichols et al., 1985). For instance, when nutritive tissue within the gonads is utilized to synthesize the gametes, the index may remain unchanged despite an increase in actual gametogenesis (Nichols and Barker, 1984a). In contrast, when cellular changes are also followed (i.e., oocyte size frequency distributions), a more accurate picture of gamete development at each phase of the cycle can be obtained. Nichols (1994) noted that the use of the GI technique is generally precluded in crinoids, since the gonad is subdivided into many hundreds of small units, one to each genital pinnule, and, furthermore, the arms are seldom intact after collection. Thus, it is impractical to obtain measurements of both gonad and body size over an acceptable time scale and with an adequate sample size. Crinoid reproductive cycles are therefore generally determined from oocyte size frequency data or, for males, from the identification of spermatocyte development stages or measurement of the thickness of formative layers within the testis. Byrne et al. (1998) stated that although the GI of sea urchins is often used in studies of reproduction, it is inappropriate in cases where it does not provide a clear indication of the reproductive cycle (King et al., 1994) and where a wide size range of individuals is used (Gonor, 1972; Grant and Tyler, 1983). Instead, Byrne et al. (1998) used the gonad retrieval rate, calculated as the slope of a regression of gonad weight against total weight. Seward (2002) also extensively discussed the limitations of GI for the study of spawning periodicities in sea urchins, and concluded that few studies on reproductive cycles have provided a quantitative definition of spawning (i.e., based on changes in GI), or have been corroborated by histological analysis. Studies that did meet these criteria showed that a sharp decline in GI could be indicative of spawning in some species [e.g., Strongylocentrotus droebachiensis (Meidel and Scheibling, 1998)], but not in all [e.g., Centrostephanus rodgersii (King et al., 1994)]. In many echinoids, such as Sphaerechinus granularis, some GI peaks may have no clear relationship with the gametogenic cycle (Byrne, 1990; Guillou and Michel, 1993; King et al., 1994). For instance, such peaks appeared in S. granularis off South Brittany (France) when the seawater temperature was abnormally low, indicating the possible use of nutrient resources from the gonad (Guillou and Michel, 1993). Byrne (1990) also suggested that decreases in GI can be due not only to spawning but also to utilization of nutrient resources stored in the gonad. Other problems with the GI technique include asynchrony in gonad development among individuals, partial spawnings in some species, and variations in spawning patterns at the population level. The GI method proved to be much better suited to that species display a pronounced and synchronous annual spawning, involving most of the population, than to species in which few individuals of a population spawn at intervals (biannualy, monthly, etc.). For instance, declining GI values can accurately

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identify spawning periods in populations where individuals release all their gametes synchronously during one spawning event, such as in some coldtemperate species of holothuroids (Hamel and Mercier, 1996a; Hamel et al., 1993). However, in the case of reproductively asynchronous individuals or individuals that emit a portion of their gametes during multiple spawning events, such a quantitative definition of spawning becomes more difficult (Seward, 2002). Specific spawning behaviour is often poorly known since spawning is rarely observed in nature (Giese et al., 1991), so the relevance of GI cannot generally be predicted and inferences about population-level spawning based on changes in GI may be weak or erroneous. The few accounts of natural spawning show that sea urchins can spawn in aggregations or as scattered individuals (Pennington, 1985), that males typically spawn first, that once spawning is initiated conspecifics are stimulated to spawn (Giese and Pearse, 1974), and that spawning is highly variable, both temporally and spatially (Levitan, 2002a; Pennington, 1985). A final drawback of the GI is that it is not equally precise in all species, depending on their morphology. For example, McClary and Barker (1998) found that three species of echinoids exhibited GI values of unequal magnitude due to the test thickness, the GI cycle being more pronounced in the species with a thinner test.

1.2. Histology Gonadal smears and/or histological sections of the gonads are widely used to estimate reproductive status. Such data are not quantitative when the developmental cycle is merely divided into a series of maturity stages in a manner which may differ from that used by other investigators. Furthermore, the intervals between stages are not equal or fixed (or even known), so that they cannot be treated as a continuous variable and compared statistically. However, more robust quantitative data can be extracted from the sections by measuring the diameter, surface or volume of germ cells and oocytes, and estimating their size frequency distributions over time. This method allows the assessment of the progressive development of successive oocyte cohorts, and of the associated reproductive cycle. Obviously, the reliability of both GI and histological analysis is largely dependent on the number of samples taken throughout the year and the sampling intervals, and this aspect will be more extensively examined below in Section 1.5. According to a review by Hendler (1991), histological determinations of GI and gonad maturity have proved more reliable in establishing breeding periods in ophiuroids than have gonad smears, records of spawning in the laboratory and larval counts in plankton samples. In contrast, Singh et al. (2001) were critical of GI and histological methods in their study of the holothuroid Cucumaria frondosa, since collection of similar-sized individuals did not allow the authors to meet the requirement of size independence of


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GI, indicating that GI was not a reliable indicator of reproductive condition in this species. Discrepancies can also arise from other factors such as the spatial scale of sampling individual animals and sub-sampling within an individual gonad (see Section 1.5 for a discussion of these potential biases). Singh et al. (2001) tested several other techniques and suggested that gonad volume fraction, gonad dry weight and cross-sectional tubule area provided more accurate determination of the spawning period. Furthermore, the proportion of the tubule respectively occupied by haemal fluid and spermatids or spermatozoa was another good indicator of spawning in males (Singh et al., 2001). Histological analysis of the gonads of the asteroid Asterina stellifera in Brazil showed that spawning started earlier than suggested by the GI, further highlighting the importance of using histological analysis in addition to GI in the investigation of reproductive cycles (Carvalho and Ventura, 2002). Similarly, a field study of pre- and post-spawning indices and biochemical composition in Asterias rubens (¼vulgaris) from eastern Canada, demonstrated the limitations of tissue indices, especially that of the pyloric caecum, since an increase in mass sometimes corresponded with a decrease in biochemical components (Raymond et al., 2007). According to Lozano et al. (1995), the maturity index, the thickness of the gonad wall and cellular composition of the gonad provide the most reliable indicators of the reproductive cycle of sea urchins, whereas the GI is less reliable, as it is significantly affected by the nutritive tissue of the gonad (Gonor, 1973c; Pearse, 1969b). Lozano et al. (1995) also emphasized that the GI method is often flawed because some inherent assumptions, especially the absence of a relationship between body size and GI, are not necessarily valid. Indeed, many studies do not specify whether analyses have been restricted to a particular range of sizes. Lozano et al. (1995) observed fluctuations in the temporal pattern of the GI and the presence of peaks that had little to do with the gametogenic cycle, according to all other indices measured. The authors suggested that successive storm events could have depleted nutrient stores in a manner similar to the decreases in GI recorded by King et al. (1994) that were related not to spawning but to changes in nutrients stored in the gonad. Bennett and Giese (1955) suggested that gametogenesis may be the last process to be interrupted in sea urchins. Similarly, Vaschenko et al. (2001) reported that the common assumption that GI values in sea urchins reflect the level of gonad maturity was not supported by a study of Strongylocentrotus intermedius at four stations in the Sea of Japan. Some individuals exhibited a fairly high gonad maturity yet very low GI value, while in others had the highest GI value coincided with the lowest gonad maturity index. This emphasizes the benefits of using other methods to complement GI measurements in studies of gametogenesis, since gonad growth is not always due to gamete synthesis and a decrease in gonad size is not necessarily the result of spawning.

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1.3. Laboratory observation and experimentation Although infrequently used, the long-term rearing and monitoring of animals in the laboratory provides another way of assessing reproductive processes and spawning periodicities. However, compiling data on gamete release in the laboratory constitutes a powerful tool only when the holding conditions simulate those of the natural environment (i.e., exposure to unfiltered running seawater under natural conditions of light, temperature and food supply). Spontaneous spawning under such conditions is especially reliable when occurrences are repeated and/or corroborated by observations in the field (through serial gonad samples or in situ sightings). For instance, excellent correlations between laboratory and field spawning events have been reported for the sea star Leptasterias polaris (Hamel and Mercier, 1995b), and the bathyal asteroid Henricia lisa repeatedly spawned in the laboratory at the time predicted from the examination of serial gonad sections (Mercier and Hamel, 2008). These two studies allowed the investigators to identify the most probable spawning cues. On the other hand, field and laboratory data on spawning are not always in agreement. For instance, in the Bristol Channel the asteroid Astropecten irregularis was fully ripe in June and spawned in July (Grant and Tyler, 1986), whereas a laboratory population of A. irregularis spawned earlier, in May–June (Christensen, 1970). Furthermore, Pearse and collaborators repeatedly witnessed gamete shedding in Pisaster ochraceus (Pearse and Eernisse, 1982) and Strongylocentrotus droebachiensis (Pearse et al., 1986b) in the laboratory well after spawning in the field, determined by regular sampling. Captive animals may be disconnected from the spawning cue and retain their mature gametes until the individuals become ultrasensitive to an unknown stimulus, in a process similar to stress-induced gamete release during collection and handling ( J. S. Pearse, personal communication). However, this hypothesis does not fully explain why spawning, when it eventually occurred, was synchonized between several unconnected tanks. Precocious or delayed spawning in laboratory-held echinoderms may thus be due to spatial, temporal or sub-population effects, or to the influence of laboratory conditions on potential cues (e.g., light intensity, temperature). With respect to the onset and progression of gametogenesis, periodic biopsies or in vivo investigation of the gonads of the same individual would provide valuable information. One of the disadvantages of this procedure is that results may be difficult to interpret due to possible effects of an invasive technique on the animal. Nevertheless, biopsies and in vivo observations are useful for some species (Hamel and Mercier, 1996b; Hamel et al., 2007; Pearse et al., 1986a), and radiographic methods may also merit consideration. There have been few comprehensive experimental investigations of the effects of biological or environmental factors on the reproduction of echinoderms. While very useful, experimental manipulation of reproductive


175

activity may be misleading by emphasizing only one of many interacting time cues, and perhaps not those that are usually important in nature (Giese and Pearse, 1974). Nevertheless, as stated above for laboratory monitoring, experimental trials become powerful tools when properly designed, especially when they are supported by field data or in situ observations. Examples include the suite of studies conducted by Pearse and collaborators on the effect of photoperiod on gametogenesis in asteroids and echinoids (Pearse and Beauchamp, 1986; Pearse and Bosch, 2002; Pearse and Eernisse, 1982; Pearse and Walker, 1986; Pearse et al., 1986a,b) and the determination of phytoplankton as a spawning inducer in the sea urchin Strongylocentrotus droebachiensis (Starr et al., 1990, 1992). Furthermore, one of the first demonstrations of chemical communication between individuals during gametogenesis in echinoderms was achieved with experimental trials (Hamel and Mercier, 1996b, 1999). In echinoids, the determination of spawning periodicity (both in the laboratory and in the field) has commonly been achieved by evaluating the response of individuals to KCl injections (Appendix A1.). Although concern has been expressed about the possible side effects of this technique (e.g., McCarthy and Young, 2004), it has also been shown that peak induction of gamete release in Antarctic echinoids coincided with the presence of pluteus larvae in the wild (Stanwell-Smith and Peck, 1998). We believe that the response to KCl might be a suitable means of determining readiness to spawn in those species that exhibit annual spawning events involving a major portion of the population, but may not be appropriate for species in which partial spawning occurs on a biannual or monthly cycle, since ripe gametes may be released by some individuals at almost any time, thus masking the underlying trend.

1.4. Field observations The collection of eggs, embryos, larvae, or juveniles in the field during or following the breeding period is another approach in the study of reproductive periodicity, although the identification of offspring is sometimes difficult. Furthermore, such measures can only indicate the spawning time and periodicity when the embryonic development and duration of the larval phase under various environmental conditions are well known. In situ observations of spawning in the field provide the most reliable data, but correlations with environmental triggers are not easy to make unless the observations are repeated several times or the spawning event is massive. However, even the most fortuitous field observation can confirm or falsify data for breeding cycles obtained from laboratory observations and/or GI and histological analysis. For instance, according to gonad, histology spawning of the holothuroid Cucumaria frondosa occurs in February–May in Newfoundland (eastern Canada) (Coady, 1973), yet gamete shedding has

176


been observed only in March–April of 2 consecutive years in the Avalon Peninsula, Newfoundland (personal observation). The same species spawns later in the spring in other areas of eastern Canada; direct observations in the Gulf of St. Lawrence consistently point to mid-June (Hamel and Mercier, 1995a, 1996a,c,d), whereas gonad indices indicate April–June in the Bay of Fundy (Singh et al., 1999, 2001). However, the data may be biased owing to heterogeneity in the gonad morphology of C. frondosa along the north-east American coast (Hamel and Mercier, 1996a). The gonad is divided into two distinct classes of gonadal tubules in northern latitudes, where gamete maturation requires 2 years (Fig. 4.1), while on the Grand Banks and south of mid-New Brunswick (Canada) tubule structure is homogenous and an annual cycle is evident. Different local environmental conditions may regulate this morphological disparity, including temperature and length of the vegetative season. Sea cucumbers in southernmost locations presumably benefit from a longer feeding period and higher mean annual temperature, which may favour an annual gametogenic cycle and also increase fecundity (Hamel and Mercier, 1996a).

1.5. Sampling interval and replication When using serial sampling to assess GI, gonad maturity or oocyte size frequency distribution, a major difficulty lies in the temporal resolution used to examine changes at the population level. Most studies of reproductive cycles sample populations at monthly intervals, sometimes less frequently, and may not capture spawning or other events that take place on a shorter time scale. Furthermore, a complete annual cycle is sometimes determined by assembling monthly samples from different years, especially when opportunities for collection are severely limited, such as for deep-sea species. Spatial variability is rarely considered in sampling protocols but can be important. For example, Kelly (2000) found significant variation in the GI of the echinoid Psammechinus miliaris among samples collected only ca. 200 m apart. The author emphasized that the conclusions of the study could therefore be very different depending on which sub-sites of the two distinct habitats investigated (intertidal and subtidal) were contrasted. Thus, comparisons among locations without adequate replication may not accurately reflect habitat effects (Kelly, 2000). However, single site comparisons remain the most widely used method of comparing reproductive variability between populations (e.g., Guillou and Lumingas, 1999; Konar, 2001; Lamare et al., 2002; Lozano et al., 1995). Another example of the importance of spatial sampling scales on the study of reproductive processes is provided by Seward (2002), who observed high variability in changes in GI in sea urchins (Strongylocentrotus droebachiensis) sampled without regard for spatial distribution. Local effects may have been involved, whereby individuals close to one another may

177


Constant conditions 100

Female (small tubules)

Female (large tubules)

75 50 25 0 Natural conditions

100 75 50

Frequency (%)

25 0 Constant conditions 100

Male (small tubules)

Male (large tubules)

75 50 25 0 Natural conditions

100 75 50 25 0

J J A S O N D J F M A M J J 1992 1993 Postspawning

Recovery

Growth

J J A S O N D J F M A M J J 1992 1993 Advanced-growth

Maturity

Figure 4.1 Cucumaria frondosa (Holothuroidea). Relative frequencies of different gametogenic stages in the small and large gonadal tubules of males and females kept under constant environmental conditions and naturally varying conditions from May 1992 to November 1993. Reprinted with permission from Hamel and Mercier (1996b).

178


have been spawning synchronously, while distant individuals may not yet have spawned. The author concluded that the lack of information regarding the spatial distribution of the sampled individuals, combined with temporal variability of natural spawning, made it difficult to define spawning from measurements of GI alone (Seward, 2002). Local or intra-site variability such as that reported by Kelly (2000) may bias the results of studies of reproductive cycles in most echinoderms, limiting the conclusions that can be drawn from comparisons of populations from dissimilar temperature or food regimes (see Section 3 in Chapter 3). Another source of sampling bias arises when gamete development is not uniform within the gonadal tissue and histological sections do not adequately take this into account. Homogeneity within the gonad was observed in several individuals of the echinoid Heterocentrotus mammillatus (Dotan, 1990), and although the author argued that such homogeneity is common in echinoids worldwide, he did not provide any supporting argument, referencing only the work of Pearse and Phillips (1968) on Echinometra mathaei. However, in some holothuroid species, the gonadal tubules are not homogenous (Hamel and Mercier, 1996a; Hamel et al., 1993; Smiley et al., 1991) and sub-sampling of the gonad can easily introduce a bias in the histological analysis (see discussion on Cucumaria frondosa in Section 1.4). The study of reproductive cycles in deep-sea echinoderms is complicated by additional problems that may compromise the data obtained. Because opportunities for sampling are scarce, data are often pooled from samples collected from stations distant from one another and/or from different depths (Tyler and Gage, 1984b; Tyler et al., 1990). For instance, after pooling data from sporadic collections made between 1973 and 1984 at stations up to hundreds of kilometers apart, Tyler et al. (1985) concluded that the deep-sea holothuroids Peniagone azorica and P. diaphana possessed a ‘‘continuous’’ reproductive cycle. A study on the asteroid Henricia abyssicola in the NE Atlantic was based on six samples collected between 1979 and 1984 from areas that were sometimes distant from one another, data from different months every year being combined to construct the annual cycle (Benitez-Villalobos et al., 2007). The impact of such constraints is not yet fully known. As noted earlier, sampling in shallow water over relatively large areas (and even within perimeters 16 C and long days (>15 h); also strong current and induction by release of gametes from congeners (generally males) A mix of temperature increase (>16 C) and conspecific spawning (synergistic effects) induces and propagates spawning

Rumrill (1984) Selvakumaraswamy and Byrne (2000) Mladenov (1979)

Davoult et al. (1990); Lefebvre and Davoult (2000)

Morgan and Jangoux (2002)

Morgan and Jangoux (2002)

203

(continued)

204

Appendix A4

(continued)

Species

Location

Methods

Control

Source

Ophiothrix fragilis

Pas-de-Calais (France)

H, MI

Ophiothrix schayeri

Australia

Laboratory observations

Gounin and Richard (1992) Selvakumaraswamy and Byrne (2000)

Ophiothrix spiculata

California (USA)

F, gonad size/ripeness, reproductive effort

Ophiothrix spongicola

Australia

Ophiura albida

Bristol Channel (UK)

Laboratory observations H, MI, OSFD

Ophiura albida Ophiura albida Ophiura gracilis

Oresund (Denmark) North Sea NE Atlantic (deep sea)

– Larvae in the field Larvae in the field

Ophiura robusta

Gulf of St. Lawrence (QC, Canada) Bristol Channel (UK)

Field observations, GI

In summer when maximum temperature is reached Various times of the year, spontaneously and after temperature change and stimulation by light In spring, correlated with increasing temperature and late phytoplankton blooms From March to June, spontaneously and after stimulation by light In May and early June, when temperature >12.5 C When temperature >12.5 C When temperature >12.5 C Correlation between presence of phytodetritus from surface primary production and larvae Massive events coincided with major increase in temperature in summer From June to November when temperature reaches 12.5 C, but also in coldest month (7.25 C)

Ophiura texturata

H, MI, OSFD

Rumrill (1984)

Selvakumaraswamy and Byrne (2000) Tyler (1977) Thorson (1946) Rees (1954) Sumida et al. (2000)

Himmelman et al. (2008) Tyler (1977)

Appendix A5 Summary of correlations suggested for the exogenous control of gametogenesis in holothuroids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species

Location

Gametogenesis

Control

Source

Actinopyga echinites

New Caledonia

GI, MI, OSFD, gonad morphology

Conand (1982)


New Caledonia

GI


New Caledonia

GI, gonad morphology

Actinopyga mauritiana

New Caledonia



Guam



Solomon Islands

GI, H, tubule length and diameter

Amperima rosea

Porcupine Abyssal Plain (NE Atlantic, deep sea) Galway Bay (Ireland)

GI, H, OSFD

Temperature increase corresponds to growing and maturing phases Temperature decrease corresponds to post-spawning or regression Onset of gametogenesis linked to increase in temperature Temperature seems to modulate gametogenesis with resting period during coolest period of the year and maturation stage when water is warming up Temperature seems to modulate gametogenesis with the resting period during coolest period of the year and maturation stage when water is warming up Variation of reproductive peak between years dependent on La Ninã event Annual cycle with early phase of gametogenesis when day length decreasing Flux of phytodetritus from surface productivity High oxygen concentrations and low temperature coincide with active gametogenesis. Feeding in warmer months build-up nutrients in winter months

Costelloe (1985)

Aslia lefevrei

GI, H, OSFD

Conand (1989) Conand (1993b)

Conand (1993b)

Hopper et al. (1998) Ramofafia et al. (2001) Wigham et al. (2003a)

205

(continued)

Appendix A5

(continued)

206

Species

Location

Gametogenesis

Control

Source

Cucumaria frondosa

St. Lawrence Estuary (QC, Canada)

Initiation of gametogenesis correlated with increased photoperiod; acceleration of synthesis in spring coincides with increase in temperature and food availability

Hamel and Mercier (1996a)

Cucumaria frondosa


Body wall thickness, energy contents of various organs, GI, gonad morphology, H, intestinal-muscle band-respiratory tree indices, intestinal contents, tubule diameter Laboratory experiments

Hamel and Mercier (1996b, 1999)

Cucumaria frondosa

Passamaquoddy Bay (NB, Canada)

Chemical communication among congener to fine-tune progression of gametogenesis toward spawning; body wall mucus is the apparent carrier of the active molecule Feeding has little influence on reproductive cycle

Gamete dry weight, GI, gonadal tubule surface area, H, haemal fluid space, OSFD Comparison of different methods

Ekmocucumis steineni

Weddell Sea (Antarctica)

F, relative gonad weight

Holothuria atra

Fiji

GI, gonad morphology, OSFD, sperm activity

Haemal space increases greatly after spawning in May–June and decreases rapidly by September No correlation found, but data suggest a potential role for environmental factors in control of reproductive biology Gametogenesis correlated with temperature fluctuation (onset in August; ripe gametes around September)

Singh et al. (2001)

Gutt et al. (1992)

Seeto (1994)

Holothuria (¼Microthele) fuscogilva Holothuria fuscogilva

New Caledonia

Holothuria fuscogilva, Holothuria fuscopunctata Holothuria fuscopunctata

New Caledonia

Gamete feature, GI, gonad morphology GI, H, gonad morphology, tubule length and diameter GI

New Caledonia


Holothuria leucospilota

Hong Kong (China)

Calorimetry, GI, H

Holothuria (¼Microthele) nobilis

New Caledonia

Gamete feature, GI, gonad morphology

Holothuria scabra

Stradbroke Island (Australia) Southwest Sulawesi (Indonesia)

GI, H, OSFD

Holothuria scabra

Holothuria scabra

Solomon Islands

Calatagan (Philippines)

GI, H MI

GI, H, OSFD

Annual reproductive cycle correlated with seasonal temperature change Onset of gametogenesis possibly as photoperiod decreases

Conand (1981)

Onset of gametogenesis linked with increase in temperature

Conand (1989)

Temperature seems to modulate gametogenesis, the resting period occurring during the coolest period of the year and the maturation stage when water is warming up Initiation of gametogenesis when temperature increasing Maturing individuals between January and May correlated with annual temperature cycle Combination of photoperiod, temperature and food availability Post-spawning accentuated in two phases: one during dry season (temperature increase) and second at beginning of rainy season (temperature decrease) Reproductive pulse in May–June as temperature falls to annual minimum and salinity decreases due to rainy season. Increase in temperature and salinity (November–January) corresponds to another pulse

Conand (1993b)

Ramofafia et al. (2000)

Ong Che (1990) Conand (1981)

Morgan (2000b) Tuwo (1999)

Ong Che and Gomez (1985)

207

(continued)

Appendix A5

(continued)

208

Species

Location

Gametogenesis

Control

Source

Holothuria scabra

India

GI

Holothuria scabra

Solomon Islands

Krishnaswamy and Krishnan (1967) Battaglene (1999a)

Holothuria scabra

Madagascar

Sapwning induction (laboratory) GI, H, MI, OSFD

Holothuria scabra

New Caledonia


Holothuria scabra

Solomon Islands

Laboratory observations (outdoor tanks)

Holothuria scabra Holothuria scabra versicolor Holothuria scabra versicolor

New Caledonia

GI

Salinity variation may be modulating reproductive cycle Both salinity and temperature may regulate reproductive cycle Gametogenesis not synchronous in entire population. Maturity reached in November–April. Temperature may regulate gametogenesis, mainly in females (other factors like rainy period could also have an effect) Temperature weakly modulating gametogenesis with resting period during coolest period of year and maturation stage as water is warming up Lunar phase plays a role in pre-spawning pairing behaviour and gametogenic synchronicity Onset of gametogenesis when temperature increases

New Caledonia


Wrightsville (NC, USA)

H, OSFD

Leptosynapta tenuis

Temperature weakly modulating gametogenesis with resting period during coolest period of year and maturation stage as water is warming up Oocyte diameter peaked in May–June and August–October. In July and August there is no gametogenesis. Could be temperature fluctuation (very poor, no correlation). Absence of reproductive individuals in midsummer during highest temperature

Rasolofonirina et al. (2005)

Conand (1993b)

Mercier et al. (2000a) Conand (1989)

Conand (1993b)

Green (1978)

Parastichopus (¼Stichopus) californicus

Woodlands Bay (BC, Canada

GI, gonad volume displacement, H

Peniagone vignoni

West Antarctic Peninsula (deep)

F, GI, H, OSFD

Protelpidia murrayi

West Antarctic Peninsula (deep) St. Lawrence Estuary (QC, Canada)

F, GI, H, OSFD

Stichopus chloronotus

Straits of Malacca (Malaysia)

GI, H, OSFD

Stichopus herrmanni

Kish Island (Iran)

GI, H

Stichopus japonicus

Southern Hokkaido ( Japan)

GI, H

Stichopus mollis

NE New Zealand

GI, H, MI, OSFD

Psolus fabricii

GI, H, OSFD, tubule diameter

209

Largest gonad in June–July and smallest in November–December. Temperature fluctuation and stratification? Vitellogenetic oocytes present year round but more intense production during greater food input from phytodetritus pulses Onset of vitellogenesis coincides with phytodetritus pulse Initiation of gametogenesis possibly related to increasing photoperiod. Acceleration of gamete synthesis later in spring as temperature and food availability increase Rapid development of gametogenesis with increase in salinity and chlorophyll a Active stage of gametogenesis coincides with increasing photoperiod In November, gametogenesis resumes and continues to increase until next spawning. Could be regulated by temperature Environmental factors may explain the difference observed between two latitudes/populations studied. Temperature and photoperiod may regulate gametogenesis

Cameron and Fankboner (1986) Galley et al. (2008)

Galley et al. (2008) Hamel et al. (1993)

Tan and Zulfigar (2001) Tehranifard et al. (2006) Tanaka (1958)

Sewell (1992)

(continued)

210

Appendix A5

(continued)

Species

Location

Gametogenesis

Control

Source

Stichopus mollis

NE New Zealand

GI, H

Sewell and Bergquist (1990)

Stichopus variegatus

New Caledonia



New Caledonia



New Caledonia

GI

Thelenota ananas

New Caledonia

Gamete feature, GI, gonad morphology

Thelenota ananas

New Caledonia

GI

Thelenota ananas

New Caledonia


Lower temperature in second year of the study prolonged reproductive cycle. Extended reproductive season could be due to El Ninõ Maturing seems to occur during temperature increase, post-spawning during cooling period and a long resting stage during cool season Temperature seems to modulate gametogenesis with resting period during coolest period of year and maturation stage when water is warming up Onset of gametogenesis linked to increase in temperature Maturing individuals noted in October–December. GI declines from January–June followed by low values in July–October (correlated with annual temperature cycle) Onset of gametogenesis with increase in temperature Temperature seems to modulate gametogenesis with resting period during coolest period of year and maturation stage when water is warming up

Conand (1993a)

Conand (1993b)

Conand (1989) Conand (1981)

Conand (1989) Conand (1993b)

Appendix A6 Summary of correlations suggested for the exogenous control of spawning in holothuroids. This table completes the field observations (Table 3.1) for which supplementary data are available. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species

Location

Methods

Control

Source

Actinopyga echinites Actinopyga echinites

Taiwan New Caledonia New Caledonia

Phytoplankton production In January–February with warm-water temperature (peak) In January–February during warm season

Chao et al. (1995) Conand (1982)

Actinaupyga echinites Actinopyga mauritiana

New Caledonia


Solomon Islands

GI, H GI, MI, morphology of tubules, OSFD GI, morphology of gonad GI, morphology of gonad GI, H, tubule length and diameter

Afrocucumis africana

Taiwan

GI, H

Apostichopus (=Stichopus) japonicus Apostichopus (=Stichopus) japonicus Aslia lefevrei

Southern Hokkaido ( Japan) Japan

GI, H

Galway Bay (Ireland)

Artificial induction (laboratory) GI, H, OSFD

Bohdschia argus, Bohadschia marmorata

Solomon Islands

Laboratory experiments

Caudina chilensis

Japan


In December–January during warm season In October–December. Correlation during increasing temperature and day length Gametes released at beginning of warm months (March–April), during spring plankton production and temperature increase From middle June for 2 months. May be related to temperature Thermal shock (5–6 C increase) and addition of sperm Between end of February and beginning of April (correlated with temperature and light cycles) Perivisceral coelomic fluid involved in inducing and spreading spawning among congeners During high tide in the evening

Conand (1993b) Conand (1993b) Ramofafia et al. (2001) Chao et al. (1995)

Tanaka (1958) Yanagisawa (1995) Costelloe (1985)

Mercier and Hamel (2002) Inaba (1930)

211

(continued)

Appendix A6 (continued) 212

Species

Location

Methods

Control

Source

Cucumaria frondosa Cucumaria frondosa

Newfoundland (Canada) Maine (USA)

Related to phytoplankton bloom Related to phytoplankton bloom in spring

Coady (1973) Jordan (1972)

Cucumaria frondosa


GI, gonad volume, H GI, gonad volume, H, larvae in the field, MI Field observations and experiments

Hamel and Mercier (1995a)

Cucumaria miniata

San Juan Archipelago (WA, USA) San Juan Archipelago (WA, USA) Intertidal zone (CA, USA) Intertidal Aoshima Island ( Japan)

Field and laboratory observations Field and laboratory observations GI

Holothuria atra

New Caledonia

Holothuria atra

Solomon Islands

GI, morphology of gonad Laboratory experiments

Massive event in mid-June. Phytoplankton bloom seems to induce male; but female seems to react to presence of sperm; rapid temperature change also seems to play a role In March–May with phytoplankton bloom. Males spawn first In February after 2 days of sun. Males spawn first In January, could be linked to aggregative behaviour Low light intensity and possibly temperature may be inducers. Spawned in December (laboratory observation) from midnight to 04:00 h In correlation with warm season

Holothuria cinerascens

Taiwan

GI, H

Cucumaria populifera Cucumaria pseudocurata Eupentacta chronhjelmi

GI, H, laboratory observations, OSFD

Perivisceral coelomic fluid involved in inducing and spreading spawning among congeners In April–June with phytoplankton production

McEuen (1986) McEuen (1986) Rutherford (1973) Catalan and Yamamoto (1994)

Conand (1993b) Mercier and Hamel (2002) Chao et al. (1995)

Holothuria difficilis

Taiwan

GI, H

Holothuria forskali

Glenan Archipelago (France) Solomon Islands

GI, H, OSFD, tubule classes GI, H, tubule morphology-lengthdiameter

New Caledonia

Gamete feature, GI, gonad morphology GI, gonad morphology

Holothuria fuscogilva

213

Holothuria (¼Microthele) fuscogilva Holothuria fuscopunctata

New Caledonia


Cook Islands

GI, gonad morphology, H


Taiwan

GI, H


Solomon Islands


Holothuria (¼Microthele) nobilis Holothuria nobilis

New Caledonia New Caledonia


Holothuria scabra

Solomon Islands

Laboratory and field observations

Holothuria scabra

India


Holothuria scabra

Solomon Islands

GI, H, tubule length and diameter

In August–September with phytoplankton production In April with increase in temperature Successful induction in the laboratory: thermal shock could be similar to short-term heat stress in situ: some results with dried alga Schizochytrium sp. In March–April during warmest months Between December and February during warm season Gametogenesis correlated with increasing temperature and longer days In June–September with phytoplankton production Perivisceral coelomic fluid involved in inducing and spreading spawning among congeners In May–July during coldest months Between June and August during cool season Pre-spawning aggregation and spawning seem to be linked to moon phases (full moon) Change of water and thermal shock (water temperature increase by 5 C) Peak of activity weakly linked to dry season, increased day length and temperature

Chao et al. (1995) Tuwo and Conand (1992) Ramofafia et al. (2000)

Conand (1981) Conand (1993b) Drumm and Loneragan (2005) Chao et al. (1995) Mercier and Hamel (2002) Conand (1981) Conand (1993b) Mercier et al. (1999, 2000a) James (1996) Ramofafia et al. (2003) (continued)


Species

Location

Methods

Control

Source

Holothuria scabra

South Sulawesi (Indonesia)

GI, H, MI

Tuwo (1999)

Holothuria scabra

Heron Island (Australia)

GI, H

Holothuria scabra

Anjuna (India)

Gonad morphology

Two main spawning periods; one during dry season and increase in temperature, the other during rainy season and decrease in temperature Gonad maturity peak twice a year in early winter and summer. Loosely linked to temperature Weak correlation with temperature and salinity

Holothuria scabra

India

GI

Holothuria scabra

India

Holothuria scabra

New Caledonia

Artificial spawning induction (laboratory) GI, gonad morphology

Holothuria scabra versicolor

New Caledonia


Holothuria tubulosa

Adriatic Sea

H, OSFD

Isostichopus fuscus

Coast of Ecuador


Leptosynapta tenuis

Wrighsville (NC, USA)

H, OSFD

Opheodesoma grisea

Taiwan

GI, H

Salinity may be responsible for onset of breeding Thermal shock (increasing temperature by 5 C) From December to February and in August–September. During warm season except for August–September episode which occurs when water starts to warm up after the cool season From November to February during warm season When temperature increases and reaches 22–26 C Cycle of lunar luminance determines periodicity In spring and fall. Absence of reproductive individuals at highest temperatures in summer In June–July during phytoplankton production

Harriott (1982)

Jayasree and Bhavanarayana (1994) Krishnaswamy and Krishnan (1967) James (1994a); James et al. (1994a) Conand (1993b)

Conand (1993b) Despalatovic et al. (2004) Mercier et al. (2004, 2007) Green (1978)

Chao et al. (1995)

Parastichopus (¼Stichopus) californicus

San Juan Archipelago (WA, USA)


Patinapta ooplax

Southern Japan

GI, H, OSFD

Patinapta taiwaniensis

Taiwan

GI, H

Polycheira rufescens

Taiwan

GI, H

Pseudocnus lubricus (¼Cucumaria lubrica)


Field and laboratory observations

P. lubricus

Puget Sound (USA)


Psolus chitonoides



Psolus fabricii


GI, H, OSFD, tubule diameter

215

In April–May and July after successive sunny days and increase in air temperature. Males spawn first From mid-July to end of August once a year; gamete released in evening; occurs only some individuals of population every new and full moon In June–July with phytoplankton production In April and June. Gametes released at beginning of warm months, correlated with spring plankton production and temperature increase Males spawn first. In December–January after several days of sun and phytoplankton bloom From mid-day to early evening during periods of low or zero tidal current. Males spawn first. Temperature and day length may set months each year. Tides and time of day may be proximate factors In March–June after a sunny day or a series of sunny days (individuals maintained in darkness delay spawning for several weeks; when placed in sun, spawning occurs in 30 min). Males spawn first In early summer ( July). Possible role of phytoplankton bloom and decrease in freshwater runoff

McEuen (1986)

Kubota (2000)

Chao et al. (1995) Chao et al. (1995)

McEuen (1986)

Engstrom (1982)

McEuen (1986)

Hamel et al. (1993)

(continued)


Species

Location

Methods

Control

Source

Stichopus chloronotus

GI, H

Stichopus herrmanni

Straits of Malacca (Malaysia) Kish Island (Iran)

GI, H

Stichopus variegatus Stichopus variegatus Synapta maculate

New Caledonia New Caledonia Taiwan

GI, gonad morphology GI, tubule diameter GI, H

Tan and Zulfigar (2001) Tehranifard et al. (2006) Conand (1993b) Conand (1993a) Chao et al. (1995)

Thelenota ananas

New Caledonia

Thelenota ananas

New Caledonia


Thyone briareus

Woods Hole (MA, USA)


With slight increase in temperature and chlorophyll a In summer. Temperature may be the trigger In December and January (warm season) In December–January (warm season) In June and July with phytoplankton production From December to April with a peak during three warmest months From January to March during warm season In June for several days, between 08:00 and 10:00 h. Temperature manipulation induces spawning

Conand (1981) Conand (1993b) Colwin (1948)

Appendix A7 Summary of correlations suggested for the exogenous control of gametogenesis in asteroids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species

Location

Methods

Control

Source

Asterias amurensis

Derwent River estuary (Australia)

GI, H

Byrne et al. (1997)

Asterias rubens

Zeeland (Netherlands)

Field observations, laboratory experiments

Asterias rubens

North and Baltic Seas

OSFD

Asterias rubens (¼vulgaris) Astrobrachion constrictum

New Hampshire (USA)

H, laboratory experiments, OSFD GI, H, MI, OSFD

Reproductive cycle apparently under photoperiodic control; temperature could play a role Photoperiod induces gametogenesis, however, once gametogenesis has begun, static environment and lack of food will not prevent gonad from reaching maturity Influence of salinity on rate of gonad development (brackish conditions inhibit process) Controlled by photoperiod

Coscinasterias muricata

Coscinasterias tenuispina

Doubtful Sound (New Zealand) Port Phillip Bay (Australia)

Brazil

GI, OSFD, progesterone levels, pyloric caecum index

GI

217

Correlated with increasing temperature Reproductive cycle of female influenced by progesterone, which in turn appears to be coordinated by changes in photoperiod. Months with maximum and minimum temperature mark onset of gametogenesis and spring spawning event. Temperature and photoperiod may influence key periods of reproductive cycle Gonad development weakly correlated with temperature

Bouland and Jangoux (1988)

Schlieper (1957)

Pearse and Walker (1986) Stewart and Mladenov (1995) Georgiades et al. (2006)

Alves et al. (2002) (continued)

Appendix A7

(continued)

218

Species

Location

Methods

Control

Source

Cosmasterias lurida

Argentina

GI, H, OSFD

Ctenodiscus crispatus

Maine (USA)

GI, H, OSFD

Pastor-de-Ward et al. (2007) Shick et al. (1981)

Dytaster grandis

Porcupine Abyssal Plain (deep sea NE Atlantic) Procupine Seabight (deep sea NE Atlantic) Continental slope (deep sea NL, Canada)

OSFD

Possible correlation of gametogenesis with photoperiod Continuous reproduction with peaks possibly explained by pulses of phytodetritus to sea floor Availability of labile organic matter may fuel vitellogenesis Role of phytodetritus on gonadal growth

Benitez-Villalobos et al. (2007)

Populations at 600 m have seasonal cycles possibly related to temperature (and light?). Population at 1300 m shows continuous presence of maturity stage and no correlation with environmental factors Very rapid gametogenesis toward maturity in late fall within a single lunar cycle (probably barometric pressure change) Reproductive cycle influenced by food quantity and quality

Mercier and Hamel (2008)

Normal feeding in summer is a prerequisite for subsequent gametogenesis

Smith (1971)

Henricia abyssicola

Henricia lisa

F, GI, gonad morphology, H, OSFD GI, H, laboratory observations, OFSD

Hippasteria phrygiana

Continental slope (deep sea NL, Canada)

GI, H, OSFD

Hyphalaster inermis

Porcupine Abyssal Plain, Madeira Abyssal Plain and NW African Slope Monterey Bay (CA, USA)

GI, H, OSFD

Leptasterias pusilla

Laboratory work

Tyler et al. (1990)

(Baillon, Hamel and Mercier, unpublished data) Ramirez-Llodra et al. (2002)

Leptasterias sp.

Gonad morphology, H

Luidia clathrata

Pacific Grove (CA, USA) Block Island Sound (RI, USA) Tampa Bay (FL, USA)

Luidia clathrata

Tampa Bay (FL, USA)

GI

Odontaster validus

McMurdo Sound (Antarctica)

GI, H, oocyte abundance and volume, OSFD

Odontaster validus

Balleny Islands (deep, Antarctica)

H OSFD

Odontaster validus

McMurdo Sound (Antarctica) Monterey Bay (CA, USA) Barkley Sound (BC, Canada) Santa Cruz (CA, USA)

GI, H, laboratory experiments, OSFD GI, pyloric caecum index GI

Leptasterias tenera

Patiria miniata Patiria (as Asterina) miniata Pisaster ochraceus

Pisaster ochraceus

Intertidal (West coast USA)


GI

H, laboratory experiments

Role of photoperiod in gametogenesis and brooding Greatest activity correlated with period of active feeding Correlation between decrease in temperature and onset of gametogenesis Peak digestive gland development corresponds to onset of gametogenesis Food abundance and quality may play a role in quantity of gametes synthesized, but temperature and salinity could be regulating factors Possible role of phytodetritus abundance from seasonal production in surface waters Demonstrated role of photoperiod on gametogenesis Availability of food may promote gamete production Seasonal fluctuation in temperature and food items Long day length (or short nightlength) apparently synchronizes or entrains initiation of gametogenesis and gonad growth Gonad development correlated with decreasing temperature

Pearse and Beauchamp (1986) Worley et al. (1977) Dehn (1980a)

Dehn (1980b)

Pearse (1965)

Pearse (1966)

Pearse and Bosch (2002) Gerard (1976) Rumrill (1989) Pearse and Eernisse (1982)

Feder (1956)

219

(continued)

Appendix A7

(continued)

220

Species

Location

Methods

Control

Source

Pisaster ochraceus

West coast (USA)


Pearse et al. (1986a)

Protoreaster nodosus

Philippines

GI

Plutonaster bifrons

Rockall Trough (NE Atlantic) Passamaquoddy Bay (NB, Canada)

GI

Demonstrated role of photoperiod on gametogenesis (underlying endogenous rhythm) Increase in gonad development coincides with increased temperature and decreased salinity Seasonal input of food may result in seasonal reproduction Possible role of day length and temperature increase

Photoperiod control

Xu and Barker (1990a)

Reproductive cycle influenced by food quantity and quality

Ramirez-Llodra et al. (2002)

Pteraster militaris

Sclerasterias mollis

New Zealand

Styracaster chuni, Styracaster horridus

Porcupine Abyssal Plain, Madeira Abyssal Plain and NW African Slope

Effectiveness of 1-methyladenine injection, GI, H, Laboratory work, MI, OSFD GI, H, laboratory experiments, steroid levels GI, H, OSFD

Bos et al. (2008)

Tyler et al. (1993) McClary and Mladenov (1988, 1989)

Appendix A8 Summary of correlations suggested for the exogenous control of spawning in asteroids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species

Location

Methods

Control

Source

Acanthaster planci

Davies Reef (Australia)

Field observations

At low tide during third moon quarter

Archaster typicus

Japan

Field observations

During receding tide

Archaster typicus Asterias amurensis Asterias amurensis

Philippines Tokyo Bay ( Japan) Derwent River estuary (Australia) Sendai Bay ( Japan)

H Field survey GI, H

Asterias forbesi

Long Island (eastern USA)

Asterias forbesi Asterias forbesi, Asterias rubens (¼vulgaris) Asterias rubens

Long Island Sound (eastern USA) Woods Hole (MA, USA) Millport (UK)

GI, Perivisceral coelomic fluid volume, pyloric caecum index Field work

Mating may coincide with new moon Correlated with temperature Seems to correlate with longest and shortest days of year From January–March when temperature between 9.8 and 12.3 C but varying slightly in other locations In late June to early July when bottom temperature 16–18 C

Babcock and Mundy (1992) Ohshima and Ikeda (1934) Janssen (1991) Ino et al. (1955) Byrne et al. (1997)

Asterias rubens

Essex (UK)

Asterias rubens

Oresund (Denmark)

Asterias rubens

Balsfjorden (Northern Norway)

Asterias amurensis

Gonad morphology, OSFD

Laboratory experiments Laboratory experiments

Abundance of recently settled juveniles Larvae in the field

221

Examination of gametes, GI, H, larvae in the field

Hatanaka and Kosaka (1959) Franz (1986)

Starts when temperature rises to 15 C

Loosanoff (1964)

When exposed to direct sun and increase in temperature From April to June–July. Addition of sperm induces mature individuals to spawn Starts when temperature reaches ca. 15 C Seems to coincide with slight increase in temperature (spring) Correlates with last part of phytoplankton bloom and higher temperature

Costello and Henley (1971) Gemmill (1914)

Hancock (1958) Thorson (1946) Falk-Petersen (1982)

(continued)

Appendix A8

(continued)

222

Species

Location

Methods

Control

Source

Asterias rubens (¼vulgaris) Astrobrachion constrictum

Gulf of St. Lawrence (QC, Canada) Doubtful Sound (New Zealand) Rockall Trough (deep sea NE Atlantic) Port Phillip Bay (Australia)

Field observations, GI

Massive events coincide with major increase of temperature in summer Weak correlation with decrease in temperature Role of food availability in seasonality of reproductive cycle Months with the maximum and minimum temperature coincide with onset of gametogenesis and spring spawning event During period of maximum temperature, early decrease in photoperiod and increasing larval food supply High tide, 1 day after full moon

Himmelman et al (2008) Stewart and Mladenov (1995) Tyler et al. (1993)

Correlated with temperature threshold of ca. 3–4 C; heterosexual aggregations during spawning Presence of gametes from congeners

Mercier and Hamel (2008)

Males induced to spawn by decrease in temperature and female by presence of sperm Decrease in temperature to ca. 2 C induces males to spawn; presence of sperm possibly induces females to spawn Potential role of temperature

O’Brien (1976)

Bathybiaster vexillifer, Plutonaster bifrons Coscinasterias muricata

GI, H, MI, OSFD GI, Gonad ash-free dry weight GI, OSFD, progesterone levels, pyloric caecum index GI, H, OSFD

Cosmasterias lurida

Argentina

Dermasterias imbricate

Vancouver Island (BC, Canada) Continental slope (deep sea NL, Canada)

Dive in August 1987

Friday Harbor (WA, USA) Casco Bay (ME, USA)

Laboratory observations Field observations

Leptasterias polaris



Leptasterias polaris


Field observations, H

Henricia lisa

Leptasterias hexactis Leptasterias littoralis

GI, H, laboratory observations, OSFD

Georgiades et al. (2006)

Pastor-de-Ward et al. (2007)

Pearse et al. (1988)

Chia (1968)

Hamel and Mercier (1995b)

Boivin et al. (1986)

Leptasterias pusilla

Monterey Bay (CA, USA) Ireland


Odontaster validus

Signy Island (Antarctica)

Ophidiaster granifer

Guam

Orthasterias koehleri Patiriella calcar

Vancouver Island (BC, Canada) SE Australia

Effectiveness of inducing spawning artificially, GI, Larval density H, OSFD, laboratory observations Drive in August 1987 GI, H

Patiriella gunnii

SE Australia

GI, H

Patiriella parvivipara

Eyre Peninsula (South Australia) Otago Harbour (New Zealand) Vancouver Island (BC, Canada) Palau


Marthasterias glacialis

Patiriella regularis Pisaster brevispinus Protoreaster nodosus

223

Pteraster militaris

Passamaquoddy Bay (NB, Canada)

Stylasterias forreri

Vancouver Island (BC, Canada)

Field observations

Field observations Drive in August 1987 Laboratory observations Effectiveness of 1-MA injection, GI, H, laboratory experiments, MI, OSFD Drive in August 1987

Weak demonstration of role of increased photoperiod In July–August during afternoon or early evening. Could be induced by local increase in temperature May correlate with decrease in phytoplankton abundance

Smith (1971)

At night during full moon

Yamaguchi and Lucas (1984) Pearse et al. (1988)

High tide, 1 day after full moon Temperature increase may cue gamete release Temperature increase may cue gamete release Release of juveniles when temperature reaches ca. 20–23 C During the day at slack tide High tide, 1 day after full moon At full moon in May May be induced in females by release of sperm or a chemical released with it

High tide, 1 day after full moon

Minchin (1987, 1992)

Stanwell-Smith and Clarke (1998)

Byrne (1992) Byrne (1992) Keough and Dartnall (1978) Byrne and Barker (1991) Pearse et al. (1988) Scheibling and Metaxas (2008) McClary and Mladenov (1988, 1989)

Pearse et al. (1988)

224

Appendix A9 Summary of correlations suggested for the exogenous control of gametogenesis in echinoids. F, fecundity; GI, gonad index; H, histology; MI, maturity index; OSFD, oocyte size frequency distribution Species

Location

Methods

Control

Source

Anthocidaris crassispina Anthocidaris crassispina

Hong Kong (China) Wakasa Bay ( Japan)

GI, H GI, H

Anthocidaris crassispina

Mera Bay ( Japan)

GI, H

Chiu (1988) Yatsuya and Nakahara (2004) Horii (1997)

Anthocidaris crassispina

Japan


Centrostephanus coronatus Centrostephanus coronatus

California (USA)

Centrostephanus rodgersii

Diadema antillarum Diadema antillarum Diadema savignyi

Barbados Florida Keys (USA) Kenya

Diadema savignyi

Fiji

Increased tempo in gametogenesis during decreasing day length Onset of gametogenesis correlated with increasing day length and temperature Temperature and lunar rhythms synchronize reproduction Peak at low temperature (April–May) Peak at low temperature Peak at high temperature and solar radiation. Monthly reproductive rhythms attuned to lunar cycle Monthly reproductive rhythms attuned to lunar cycle

Byrne et al. (1998)

Diadema antillarum

New South Wales (Australia) New South Wales (Australia) Bermuda

H, laboratory experiments H, OSFD, thickness of layer of spermatogenic cells Gonad retrieval rate, H

Food availability Maturation may be inhibited at 15 C but not at 20 and 25 C Gametogenesis may be linked to change in temperature Gametogenesis in mid-summer can be inhibited by holding individuals at 15 C, and triggered several months earlier by maintaining them at 20 or 25 C Reproductive rhythm may be related to monthly lunar (tidal) cycle Possible role of monthly moonlight cycle on reproductive rhythms

Centrostephanus rodgersii

Santa Catalina Island (CA, USA)

Effectiveness of KCl injections, GI, H GI, H, OSFD GI GI Effectiveness of KCl injections, GI, H, oocyte diameter GI, gonad smears, H

Sakairi et al. (1989)

Pearse (1972) Kennedy and Pearse (1975)

King et al. (1994) Iliffe and Pearse (1982) Lewis (1966) Bauer (1976) Muthiga (2003)

Coppard and Campbell (2005)

Diadema setosum

Fiji

GI, gonad smears, H

Diadema (¼Centrechinus) setosum Diadema setosum

Alexandria (Mediterranean Sea)


Gulf of Suez

GI, H, OSFD

Diadema setosum

Indo-Pacific (various locations)

H, OSFD

Diadema setosum

Philippines

GI

Diadema setosum

Kenya

Effectiveness of KCl injections, GI, H, oocyte diameter

Echinocardium cordatum

Northern France

GI, H, MI

Echinocardium cordatum

UK

Echinometra mathaei

Gulf of Suez

Echinometra mathaei

Coast of Kenya

Morphometric and gonad phenotype GI, H, OSFD, thickness of nutritive phagocyte layer GI, H

Monthly reproductive rhythms attuned to lunar cycle More mature individuals found during full moon in summer

Coppard and Campbell (2005) Fox (1924a)

A critical temperature of 25 C required to stimulate gametogenesis; however, high temperature in summer may limit gametogenesis Observed latitudinal variations, and sexual activity when temperature >25 C Possible role of lunar cycle with peak maturation at full moon Annual breeding season negatively correlated with temperature and light. Monthly reproductive rhythms attuned to lunar cycle Marked drop in water temperature followed by a regular temperature increase initiates gametogenesis When feeding is impaired individuals never reach reproductive maturity Minimum temperature and nutrient reserves may regulate reproductive periodicity Gametogenesis commences when temperature and light are at their minima

Pearse (1970)

Pearse (1968a, 1974)

Tuason and Gomez (1979) Muthiga (2003)

Nunes and Jangoux (2004) Buchanan (1966) Pearse (1969b)

Muthiga and Jaccarini (2005)

225

(continued)

Appendix A9

(continued)

226

Species

Location

Methods

Control

Source

Echinometra mathaei

H, OSFD

Echinothrix calamaris

Rottnest Island (Western Australia) Fiji

Echinothrix diadema

Fiji

GI, gonad smears, H

Echinus affinis

Deep sea from NE Atlantic

Pearse and Phillips (1968) Coppard and Campbell (2005) Coppard and Campbell (2005) Campos-Creasey et al. (1994)

Eucidaris tribuloides

Florida (USA)

Analysis of digestive tract contents, OSFD GI, H, laboratory experiments

Eucidaris tribuloides

Plantation and Tavernier Keys (FL, USA) Marlborough Sounds (New Zealand)

GI, H, laboratory experiments

Gamete synthesis possibly under the influence of temperature Monthly reproductive rhythms attuned to lunar cycle Monthly reproductive rhythms attuned to lunar cycle Possible correlation between phytodetritus pulses and gonad growth Demonstrated role of photoperiod in control of gametogenesis; short days entrain gametogenic development High temperature inhibits spermatogenesis, but not oogenesis

Brewin et al. (2000)

Evechinus chloroticus

Doubtful Sound (New Zealand)

GI, H, OSFD

Hemicentrotus pulcherrimus

Oshoro Bay ( Japan)

GI, whole gonad maturation stage

Hemicentrotus pulcherrimus

Japan


Gametogenesis possibly cued by increasing day length and nutrient availability Differentiation and proliferation of gametes coincide with increase in temperature and day length Gonad maturation initiated by decrease in temperature to ca. 15 C Continuation of maturation occurs when temperature is

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The Spawning

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Endogenous Development: Networking, Innovation, Institutions and Cities

Endogenous Market Structures and the Macroeconomy

Enslaved 2 Spawning

Endogenous Growth Theory

Fundamental Limitations in Filtering and Control (Communications and Control Engineering)

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Fundamental Limitations in Filtering and Control (Communications and Control Engineering)

Sliding Modes in Control and Optimization (Communications and Control Engineering)

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Advances in Dynamics and Control

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Recent Advances in Control and Optimization of Manufacturing Systems (Lecture Notes in Control and Information Sciences)

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Modeling and Control of Antennas and Telescopes

Handbook of Biological Control: Principles and Applications of Biological Control

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Control and Estimation of Systems with Input Output Delays (Lecture Notes in Control and Information Sciences)

Assessment and Future Directions of Nonlinear Model Predictive Control (Lecture Notes in Control and Information Sciences)

Endogenous and Exogenous Control of Gametogenesis and Spawning in Echinoderms

Meiosis and Gametogenesis

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The Spawning

The Spawning

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Endogenous Development: Networking, Innovation, Institutions and Cities

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Enslaved 2 Spawning

Endogenous Growth Theory

Fundamental Limitations in Filtering and Control (Communications and Control Engineering)

Stochastic Processes, Estimation, and Control (Advances in Design and Control)

Sliding Modes in Control and Optimization (Communications and Control Engineering)

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Sliding Modes in Control and Optimization (Communications and Control Engineering)

Negation and Control in Prolog

Advances in Dynamics and Control

Advances in Control and Communication

Modeling and Control of Complex Systems (Automation and Control Engineering)

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Recent Advances in Control and Optimization of Manufacturing Systems (Lecture Notes in Control and Information Sciences)

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Handbook of Biological Control: Principles and Applications of Biological Control

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