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From competent larva to exotrophic juvenile: A morphofunctional study of the perimetamorphic period of Paracentrotus lividus (Echinodermata, Echinoida)
Abstract
The perimetamorphic period in Paracentrotus lividus lasts for 8-12 days. It starts from the acquisition of larval competence, includes the change in form (metamorphosis) and the endotrophic postlarval life, and stops with the appearance of the exotrophic juvenile. All major postlarval appendages already occur in competent larvae being either grouped into the echinoid rudiment (terminal plates, early spines and primary podia) or scattered within the larval integument (genital plates and sessile pedicellariae). Competent larvae show particular behaviour which brings them close to the substratum. The latter is tested by primary podia protruding through the vestibular aperture of the larva. Primary podia are sensory-secretory appendages that are deprived ampullae. They are able to adhere to the substratum in order to allow evagination of the echinoid rudiment (i.e. metamorphosis) and substatum adhesion of the postlarva. Particular spines are borne by the postlarva; these are multifid non-mobile appendages forming a kind of protective armour. Like those of the larva, all characteristic structures of the postlarva (primary podia, multified spines and sessile pedicellariae) are transitory and regress either at the end of postlarval life (primary podia) or during early juvenile life (multifid spines and sessile pedicellariae). Other appendages that develop during postlarval life (i.e. podia with ampulla, point-tipped spines and sphaeridiae) are similar to those borne by the adults and become functional when the individual enters its juvenile life. Thus, the perimetamorphic period appears to be a fully fledged period in the life-cycle of P. lividus, and presumably in the life-cycle of any other sea-urchin species.
... Elucidating late-larval morphology and factors influencing D. antillarum development prior to settlement is equally difficult to examine in the field due to larval scarcity (Feehan et al. 2016), the cryptic nature and small size of juveniles (Levitan et al. 2014), and other confounding factors. Larval competence, or the developmental point at which larvae can successfully undergo metamorphosis (Gosselin and Jangoux 1998), is presumed to occur sometime after the formation of the rudiment, or imaginal disc, off of which various juvenile structures such as the mouth, spines, ring nerve, and podia grow (Okazaki 1975). Echinoderms display marked phenotypic variation at competence (Emlet 2010) and limited descriptions of this stage exist for diadematids with echinopluteus transversus larval forms. ...
... At 40 DPF, proportions of larva began to display differentiated rudiments with podia positioned either internal or external to the vestibular pore (Fig. 1b, c). The vestibular pore is an orifice which typically remains closed during planktonic development and widens prior to metamorphosis to allow sensory podia to protrude and assess the quality of a substratum (Okazaki 1975;Gosselin and Jangoux 1998). An initial experiment compared settlement rates between separate groups of larvae with internal and external podia to attempt understanding of how this attribute determines D. antillarum competence. ...
... Competence is assumed to be the developmental point at which planktonic larvae can successfully undergo metamorphosis and transition into a benthic juvenile life-stage (Gosselin and Jangoux 1998). For D. antillarum, this point was not determined by podia position relative to the vestibular pore. ...
Understanding early life histories of keystone marine herbivores can broaden insight into population dynamics and ecosystem functioning. Settlement, defined as the transitional process from planktonic larva to benthic juvenile, is not well understood for the long-spined sea urchin Diadema antillarum despite outsized herbivory effects on Caribbean coral reefs. Recent advances in aquaculture methods have enabled experimental investigation of larval ontogeny and cue-mediated settlement dynamics otherwise difficult to understand through field observations. In this study, the morphological attributes preceding metamorphosis of feeding larvae were characterized and factors influencing development of these attributes were examined. Simple access to the nutritious microalgae Rhodomonas lens led to metamorphic competence, defined here by presence of a large rudiment, or imaginal disc, and either internal or external podia with suction rings at the terminal tips. Subsequent exposure to a suite of individual cues revealed highest settlement to two calcareous algae, Halimeda sp. and crustose coralline algae, at 58.0% (± 3.7 SE) and 46.0% (± 5.1 SE), respectively, and zero settlement to a sterile seawater negative control. Significantly higher settlement to a ceramic tile overgrown with biofilm compared to separate sterile tile and isolated biofilm treatments revealed a synergistic relationship between a structural and biochemical cue. Microalgae exposure further enhanced settlement, but only when a strongly inductive primary cue was present. Together, these results provide insight into active habitat selection and factors likely influencing D. antillarum recruitment potential. Findings can be applied to improve both population dynamics models and aquaculture production methods.
... Spawning takes place in the water column during coordinated events, and fertilization is external, hence making this species easily amenable for in vitro fertilization in the laboratory (Tenuzzo et al., 2012;Ortiz et al., 2019). Following fertilization, like many other echinoids, P. lividus exhibits an indirect mode of development (Cellario and Fenaux, 1990;Gosselin and Jangoux, 1998). Thus, the animal undergoes a bi-phasic lifecycle with the initial formation, following embryogenesis, of a pelagic, planktotrophic larva called the echinopluteus (or pluteus) larva that exhibits a classical bilateral symmetry. ...
... For instance, classical developmental descriptions of embryos and larvae have been published by Boveri (1901), von Ubisch (1913, and Hörstadius (1973). Likewise, the transition from the larval to the adult stage of P. lividus, i.e., from competent larva to early juvenile, has been reported by Gosselin and Jangoux (1998). A staging scheme for early juvenile stages of P. lividus, i.e., during the first 4 weeks of its post-metamorphic life, has also recently been provided by Thompson et al. (2021). ...
... Each of the defined developmental periods was then subdivided into several distinct developmental stages, which cover various time spans (Figure 3). The stages during the embryonic and larval periods as well as for rudiment and juvenile development were defined based on previous descriptions made for P. lividus and other sea urchin species (Hörstadius, 1973;Okazaki, 1975;Gosselin and Jangoux, 1998;Smith, 2008;Heyland and Hodin, 2014). ...
The sea urchin Paracentrotus lividus has been used as a model system in biology for more than a century. Over the past decades, it has been at the center of a number of studies in cell, developmental, ecological, toxicological, evolutionary, and aquaculture research. Due to this previous work, a significant amount of information is already available on the development of this species. However, this information is fragmented and rather incomplete. Here, we propose a comprehensive developmental atlas for this sea urchin species, describing its ontogeny from fertilization to juvenile stages. Our staging scheme includes three periods divided into 33 stages, plus 15 independent stages focused on the development of the coeloms and the adult rudiment. For each stage, we provide a thorough description based on observations made on live specimens using light microscopy, and when needed on fixed specimens using confocal microscopy. Our descriptions include, for each stage, the main anatomical characteristics related, for instance, to cell division, tissue morphogenesis, and/or organogenesis. Altogether, this work is the first of its kind providing, in a single study, a comprehensive description of the development of P. lividus embryos, larvae, and juveniles, including details on skeletogenesis, ciliogenesis, myogenesis, coelomogenesis, and formation of the adult rudiment as well as on the process of metamorphosis in live specimens. Given the renewed interest for the use of sea urchins in ecotoxicological, developmental, and evolutionary studies as well as in using marine invertebrates as alternative model systems for biomedical investigations, this study will greatly benefit the scientific community and will serve as a reference for specialists and non-specialists interested in studying sea urchins.
... It will be the only part of the larval skeleton left in the juvenile. The second series of events (beginning of perimetamorphic period, Gosselin and Jangoux, 1998) comprises the development of the rudiment up to the competent larva (ready to metamorphose). The rudiment develops inside the vestibule, ending by deforming the body of the competent larvae (swollen left side, bulging of the circumoral area, displacement of anus and hydropore to the right). ...
... Epibenthic biofilms, detritus, cleaned sediment (same origin than the natural one), macroalgae (Enteromorpha sp.) are only slightly or not effective. Metamorphosis is rapid (<1 h) and differs from that of regular echinoids by the lack of rudiment eversion (Gosselin and Jangoux, 1998). Here indeed, the rudiment spines and tube feet rupture the larval epidermis while the growing vestibular epidermis becomes the epidermis of the postlarva. ...
... Primary tube feet are permanent in E. cordatum and become functional digitate tube feet of the phyllodes. This contrasts with the Echinoidea where primary tube feet are transitory (Gosselin and Jangoux, 1998). Early juveniles harbor conspicuously developed clavulae and sphaeridia presumably related to a burrowing behavior (Nichols, 1962;Buchanan, 1966). ...
... Most echinoids, like many marine invertebrates, have a biphasic life style. Following a protracted larval stage, the adult or juvenile body plan emerges from the larvae during metamorphosis [9]. The post-metamorphic sea urchin body plan is pentaradially symmetrical, globe shaped, and comprised multiple CaCO 3 tessellate plates which make up the test (Fig. 1). ...
... Despite the long history of work characterizing changes in echinoid morphology through ontogeny [9,11,12,[17][18][19][20][21], there has been relatively little work tying these morphological changes to their molecular and cellular underpinning. To fill this gap, we performed detailed analyses of morphological changes during growth, immunohistochemistry, and fluorescent assays of skeletal growth and cell proliferation in post-metamorphic juveniles of the sea urchin Paracentrotus lividus. ...
... During growth of the late larvae, the adult body plan develops (Additional file 1: Fig. S1) and the pentaradial juvenile emerges during metamorphosis [9]. After metamorphosis, juveniles are approximately 200-400 μm in diameter and have distinct ambulacral and interambulacral areas with spines and primary podia. ...
Background
Understanding the molecular and cellular processes that underpin animal development are crucial for understanding the diversity of body plans found on the planet today. Because of their abundance in the fossil record, and tractability as a model system in the lab, skeletons provide an ideal experimental model to understand the origins of animal diversity. We herein use molecular and cellular markers to understand the growth and development of the juvenile sea urchin (echinoid) skeleton.
Results
We developed a detailed staging scheme based off of the first ~ 4 weeks of post-metamorphic life of the regular echinoid Paracentrotus lividus. We paired this scheme with immunohistochemical staining for neuronal, muscular, and skeletal tissues, and fluorescent assays of skeletal growth and cell proliferation to understand the molecular and cellular mechanisms underlying skeletal growth and development of the sea urchin body plan.
Conclusions
Our experiments highlight the role of skeletogenic proteins in accretionary skeletal growth and cell proliferation in the addition of new metameric tissues. Furthermore, this work provides a framework for understanding the developmental evolution of sea urchin body plans on macroevolutionary timescales.
... Early juveniles resemble miniature versions of the adults, already possessing all adult echinoderm synapomorphies. However, immediately following metamorphosis, they sometimes lack a functional digestive tract, such as in echinoids and asteroids, in which the adult mouth and anus perforate only at later stages (Gosselin & Jangoux, 1998;Haesaerts, Jangoux, & Flammang, 2003). The endoskeleton of early juveniles is moreover rather transparent and their anatomy is relatively simple, since they ...
... The background was removed using a particle size threshold, and the obtained images were processed using Blender version 2.79 (Blender Foundation, RRID:SCR_008606). Figure S1a). Along the oral-aboral axis, the body of an early juvenile can be subdivided into three distinct regions (Gosselin & Jangoux, 1998): (i) the supracoronal region, which constitutes the aboral surface (directed away from the substrate), (ii) the coronal region, located at the midline, and (iii) the infracoronal region, which corresponds to the oral surface ( Figure 1a). On the supracoronal region, two types of appendages were commonly observed: the juvenile spines and the pedicellariae (Figure 1a,b). ...
... While primary podia are transient organs that develop in the rudiment and are lost as development proceeds, secondary podia are permanent podia that emerge upon metamorphosis and are subsequently maintained in the adult. By definition, all podia developing after metamorphosis are thus secondary podia (David et al., 1995;Gosselin & Jangoux, 1998;Morris, 2009). In 4-dayold early juveniles, primary and secondary podia were anatomically similar, with primary podia being slightly larger, since they developed earlier (Supporting Information Figure S1f). ...
The echinoderms are a phylum of marine deuterostomes characterized by the pentaradial (five fold) symmetry of their adult bodies. Due to this unusual body plan, adult echinoderms have long been excluded from comparative analyses aimed at understanding the origin and evolution of deuterostome nervous systems. Here, we investigated the neural anatomy of early juveniles of members of three of the five echinoderm classes: the echinoid Paracentrotus lividus, the asteroid Patiria miniata, and the holothuroid Parastichopus parvimensis. Using whole mount immunohistochemistry and confocal microscopy, we found that the nervous system of echinoid early juveniles is composed of three main structures: a basiepidermal nerve plexus, five radial nerve cords connected by a circumoral nerve ring, and peripheral nerves innervating the appendages. Our whole mount preparations further allowed us to obtain thorough descriptions of these structures and of several innervation patterns, in particular at the level of the appendages. Detailed comparisons of the echinoid juvenile nervous system with those of asteroid and holothuroid juveniles moreover supported a general conservation of the main neural structures in all three species. Our results sustain the hypotheses of previous work for the existence of two neural units in echinoderms: one consisting of the basiepidermal nerve plexus to process sensory stimuli locally, and one composed of the radial nerve cords and the peripheral nerves constituting a centralized control system. This study provides the basis of more in‐depth comparisons of the echinoderm adult nervous system with those of other animals, in particular hemichordates and chordates, to address the long‐standing controversies about deuterostome nervous system evolution.
... It will be the only part of the larval skeleton left in the juvenile. The second series of events (beginning of perimetamorphic period, Gosselin and Jangoux, 1998) comprises the development of the rudiment up to the competent larva (ready to metamorphose). The rudiment develops inside the vestibule, ending by deforming the body of the competent larvae (swollen left side, bulging of the circumoral area, displacement of anus and hydropore to the right). ...
... Epibenthic biofilms, detritus, cleaned sediment (same origin than the natural one), macroalgae (Enteromorpha sp.) are only slightly or not effective. Metamorphosis is rapid (<1 h) and differs from that of regular echinoids by the lack of rudiment eversion (Gosselin and Jangoux, 1998). Here indeed, the rudiment spines and tube feet rupture the larval epidermis while the growing vestibular epidermis becomes the epidermis of the postlarva. ...
... Primary tube feet are permanent in E. cordatum and become functional digitate tube feet of the phyllodes. This contrasts with the Echinoidea where primary tube feet are transitory (Gosselin and Jangoux, 1998). Early juveniles harbor conspicuously developed clavulae and sphaeridia presumably related to a burrowing behavior (Nichols, 1962;Buchanan, 1966). ...
... Such type of discrepancy may be related to the species differences (Thet et al., 2004). Following the induction of complete metamorphosis, S.sphaeroides juveniles had 4 primary spines per interambulacrum (20 totals), similar to those documented in P. lividus (Gosselin and Jangoux, 1998) and Strongylocentrotuspurpuratus (Miller and Emlet, 1999). The irregular echinoid Echinocardiumcordatum has a greater number of primary spines per interqambulacrum after metamorphosis and also differs from S. sphaeroides by the presence of secondary spines and a subanalfacsciole and 4 primaryspines (Nunes and Jangoux, 2007). ...
... The irregular echinoid Echinocardiumcordatum has a greater number of primary spines per interqambulacrum after metamorphosis and also differs from S. sphaeroides by the presence of secondary spines and a subanalfacsciole and 4 primaryspines (Nunes and Jangoux, 2007). Similar to the events in S. fanciscanus and S. Purpuratus (Miller and Emlet, 1999), P. lividus (Gosselin and Jangoux, 1998), and E. cordatum (Nunes and Jangoux, 2007), the newly metamorphosed juveniles of S. spheroidshad one tube foot per ambulacra. In contrast, C. subdepressusuniquely displayed three podia after metamorphosis (Vellutini and Migotto, 2010). ...
... The dorsal organs appear to develop out of this tissue. For the first 2days, the larval tissue can easily be picked off the urchin.The digestive system and probably other internal organsappeared at about 4-5 days after settlement and then theurchin began to feed, as similar to those documented in Colobocentrotusmertensii (Thet et al., 2004), P. lividus (Gosselin and Jangoux, 1998), and L. pictus (Hinegardner, 1969). In contrast, the juveniles of C. subdepressus and C.rosaceus start feeding 7 and 10 days, respectively, when theAristotle's lantern and mouth become functional (Emlet, 1986,Vellutini andMigotto, 2010). ...
Adults of August (2014) along the northern estruarine of gametes has been carried out by potassium chloride injection using a one ml tuberculin syringe equipped with a 26 or 30 gauge needle. Gentle shaking of the animal anticlockwise 90 minutes of injection aided in gamete shedding. Gently sperm and eggs were mixed with a clean stirring rod. time schedule for different stages has been tabulated. and were placed on glass slides with embedding mixture of PBS / glycerol / DABCO. Immediate viewing and photographing were very small and extremely motile Zygote (3 min. after fertilization) has undergone radial holoblastic cleavage till the blastul (3.50-4.15 hrs. after fertilization).The early blastula had a blastoderm enclosing a central blastocoel (6 hr 20 min. after fertilization). Cilia were developed on the exterior of the blastoderm and gradually this embryonic stage hatc At the animal pole an apical plate was formed in the form of a thickened region of epithelium with a tuft of long cilia while the epithelium at the vegetal pole flattened and thick plate (16hr 45min.. after fertilization). Ingression of primary mesenchyme cells into the blastocoel took place and a new cavity was formed referred to enteron. (19hr 15min. after During the prism stage the embryo took the shape of a rounded pyramid (21 hr 20 min. after fertilization). Pluteus larva with two arms was developed (24hr 30 min. afte larva developed into into eight continued larval developme swimming blastulae were subjected to certain bioactive inducers which had been claimed to induce metamorphosis, involved in signaling systems, serve in neuronal control, control morphogen behavioral reactions or interact with members of several signal transduction proteins pathways under normal physiological conditions. Results of these trails were introduced to One variance (ANOVA) with P < 0.05 and Dunnett's Multi It has been concluded that Acetyl choline 0.5 mM, Serotonine NH4ClNH4Cl and cGMP 1 pluteus larval stage with and NH4Cl 300 µM exereted no role in metamorphosis and antibiotic sea water had negligible effect.
... At this stage the mouth of the juvenile sea urchin (Aristotle lantern) is incompletely developed, and hence newly settled juveniles are unable to feed in the benthos for the first few days (Gosselin and Joangoux 1998;Miller and Emlet 1999;Byrne et al. 2008, Emlet 2010Fadl et al. 2017). Therefore, they likely feed on endogenous (larval) resources, carried over to the juvenile stage during this perimetamorphic period (sensu Gosselin and Jangoux 1998). Work by Miller and Emlet (1999) also suggests that the time period to mouth opening and juvenile feeding depends on temperature, and our previously published data show that the presettlement feeding regime of the larva affects juvenile survival, further emphasizing the importance of carryover effects during the metamorphic transition of sea urchins (Fadl et al. 2017). ...
... While FoxO is an important and well-established mediator of the stress response in animals (Bridge et al. 2010), it remains unclear how and where the stress response is established in early juvenile sea urchins. Based on previously published data Miller and Emlet 1999;Byrne et al. 2008;Fadl et al. 2017), we hypothesize that the stress response is, in part, activated by the fact that juveniles have an incomplete feeding and digestive system and therefore heavily rely on larval reserves (Emlet and Hoegh-Guldberg 1997; Gosselin and Jangoux 1998;Miller and Emlet 1999). Here we present a detailed description of feeding structures post settlement and before the onset of feeding, using phalloidin stain to visualize muscle development as well as SEM for the external morphology of early juvenile stages. ...
... Our results of growing juvenile sea urchins match similar studies previously presented by Gosselin and Jangoux (1998) and Miller and Emlet (1999). These studies emphasize two important aspects: First, several juvenile structures begin forming in the juvenile rudiment within the larva and mature as the larva reaches metamorphic competence. ...
The purple sea urchin, Strongylocentrotus purpuratus, has been the focus of extensive ecological and developmental research over the years. S. purpuratus larvae transition into the juvenile stage after an extensive planktonic period. The metamorphic transition is characterized by dramatic changes in morphology and physiology of the juvenile compared to the larval form and mechanisms underlying this process, especially the early days post-settlement, remain poorly understood. We SEM and phalloidin stain analysis as well as whole mount in situ hybridization to gain a detailed understanding of juvenile development in relation to nutrient signalling [insulin-like growth factor (IIS), FoxO (forkhead box, sub-group ‘O’) and TOR (target of rampamycin), also known as IIS/TOR/FoxO signalling]. Our results show that the majority of juvenile feeding features are fully developed only after 8-days of juvenile development, leaving an extensive period of nutritional stress. We found that FoxO gene expression increases during that time period and is localized in juvenile tube feet, potentially associated with sensory structures involved in nutrient signalling. Our data complement existing work on sea urchin juvenile development and shed new light on the perimetamorphic period of S. purpuratus, with respect to nutrient signalling and the potential stressful pre-feeding period of juvenile sea urchins.
... Se utilizó una lupa binocular, modelo LEYCA.ZOOM-2000, y el microscopio electrónico de barrido, modelo JEOL.JSM-6300, del servicio de microscopía de La Universidad de La Laguna. Se tomaron fotografías digitales de todas las fases de crecimiento encontradas (postlarvas y juveniles recientes), salvo de las post-larvas con el microscopio electrónico, debido a la baja consistencia que presentan y a la imposibilidad de aplicar el método "punto crítico" para endurecerlas y secarlas de forma correcta (Gosselin & Jangoux, 1998). ...
... A la hora de estudiar el asentamiento se suelen utilizar los sustratos artificiales (ver revisión en Balch & Scheibling, 2001), por ello muchos autores (e.g. Kessing et al., 1993;Gosselin & Jangoux, 1998;Lamare & Baker, 2001;Tomas et al., 2004) han definido el asentamiento de equinoideos, de forma práctica, como la llegada de nuevos individuos a los colectores artificiales, donde aprecerían post-larvas y juveniles recientes. En estos trabajos la temporalidad de muestreo varió desde unas semanas a varios meses (ver revisión en Balch & Scheibling, 2001). ...
... Las postlarvas encontradas (Figura 23-1) tienen un tamaño medio de 718 ± 54 µm, superior al encontrado por Eckert (1998) para postlarvas en cultivo de la forma del Atlántico occidental, que fue de 515 ± 17 µm. Poseen cinco podios primarios o pies cuya función principal es sensitiva y de adhesión al sustrato, como se ha comprobado en Paracentrotus lividus (Gosselin & Jangoux, 1998). No presentan pedicelarios ni púas rígidas, aunque aparecen unos filamentos rudimentarios que posiblemente darán origen a las mismas. ...
... In the competent larval stage, T. gratilla has been observed to demonstrate substrate test behavior, which are similar to those documented in other echinoids [19,32,[34][35][36][37]. The early post larval juveniles look like a regular urchin, having a spherical body shape, bilateral symmetry could be identified soon after the resorption of larval tissues and was possibly determined during the formation of rudiment as those observed recently in sea urchins [19,20] and sea biscuits [32]. ...
... Larval arms were found to be completely absorbed together with the skeletons and epidermis in the newly metamorphosed juvenile of T. gratilla (Fig. 3I). In contrast, tissue resorption in Eucidaris thouarsi and Paracentrotus lividus was achieved by the retraction of only epidermis resulting in the naked skeleton [27,36]. However, the naked skeletal rods will eventually be broken down and such kinds of discrepancy may be related to the species differences [31]. ...
... After the induction of complete metamorphosis, T. gratilla juveniles had 4 primary spines per interambulacrum (20 totals), similar to those documented in P. lividus [36], Strongylocentrotus purpuratus (Miller and Emlet, 1999), S. sphaeroides [19] and E. mathaei [20]. However, a greater number of key spines per interqanbulacrum was documented after metamorphosis in the asymmetrical echinoid E. cordatum. ...
A detailed ontogenic development of the tropical sea urchin, Tripneustes gratilla was studied in a captive laboratory condition. Matured gametes were collected by injecting 0.5M KCl into the coelomic cavity of the adult sea urchin. Insemination was done using 10-5 "dry" sperm dilution and the mean fertilization success was estimated to be 96.6±1.4%. The resulted embryos were incubated in glass beakers containing sterilized filtered seawater (SFSW) at 26-28ºC. The 2-cell (first cleavage), 4-cell, 8-cell, 16-cell, 32-cell, and multi-cell, (morula) stages were reached at 01.22, 02.18, 2.48, 3.48 and 04.01 h post fertilization respectively. Ciliated blastulae and gastrulae were formed after 09.26 and 16.41 h of fertilization. Pluteus larvae started feeding unicellular algae (Chaetoceros calcitrans) within 2 d, grew continuously and attained metamorphic competence in 35 d after fertilization. Metamorphosis took place nearly 1.5 h from the attachment to complete resorption of larval tissues and the formation of a complete juvenile structure with adult spines and prolonged tube feet, the whole event of which usually took place within 1 d post settlement. This study represents the first successful documentation of the complete embryonic, larval and early juvenile development of T. gratilla in tropical Malaysia, the findings of which would greatly be helpful to understand the ontogeny and life-history strategies that will facilitate the development of breeding, seed production and culture techniques of this high-valued sea urchin for commercial aquaculture.
... Competent larvae of Salmacissphaeroidescontain pedicellariae during the late larval phase and after metamorphosis, as in Paracentrotus lividus (Gosselin and Jangoux, 1998), and Strongylocentrotus franciscanus (Miller and Emlet,1999), but pedicellariae of Strongylocentrotus sometime after metamorphosis. On the other hand, competent larvae of Echinocardium cordatum lack spines and pedicellariae (De Amaral P. Nunes and Jangoux, 2007), whilst those of Clypeastersub depressus have spines but no pedicellariae (Vellutini and Migotto, 2010). ...
... On the other hand, competent larvae of Echinocardium cordatum lack spines and pedicellariae (De Amaral P. Nunes and Jangoux, 2007), whilst those of Clypeastersub depressus have spines but no pedicellariae (Vellutini and Migotto, 2010). Similar to Colobocentrotus mertensii (Thet et al., 2004), Paracentrotus lividus (Gosselin and Jangoux, 1998), and Lytechinus pictus (Hinegardner, 1969), the digestive system and maybe other internal organs developed approximately 4-5 days after settling, and the urchin began to eat, while in the present study the newly settled young sea urchins, E. mathaei are nearly competent after the third day of observation. E. mathaei, newly settled juvenile sea urchins, are almost 630μm wide, have grown mouth parts, and have begun eating on benthic diatoms. ...
The sea urchins (Echinoidea) are keystone species in an ecosystem with the simplest form of development. The mature specimens of Echinometra mathaei (Blainville, 1825) were collected from Cape Monze on 17th March and kept in the laboratory. Spawning occurred after same day, at room temperature 28°C in filtered seawater with a salinity of 37 ppt and a pH of 8. After fertilization the developmental stages of embryos and the timing of each stage including cleavage, morula, blastula, gastrula, prism and pluteus larvae were studied under the microscope. This study represents the first successful analysis on embryonic, larval, and pre-juvenile development of E. mathaei. Understanding of ontogeny and life-history strategies will make it easier to develop techniques for breeding, seed production, and culture of sea urchins in captivity conditions also the findings would greatly be helpful for future biologist.
... Furthermore, the developmental origin of the hydropore, which has been classified as part of the perforate extraxial skeleton, varies across extant taxa. During the development of the echinoid Paracentrotus lividus, the calcified madreporite found in the adult body plan forms around the larval hydropore as a result of further biomineral deposition in continuity with the larval skeleton (Gosselin and Jangoux, 1998). In this echinoid, the adult hydropore is thus the same structure as the larval hydropore. ...
... In juvenile echinoids, each podium protrudes through a single ambulacral pore in each plate, which, at early postmetamorphic stages of growth, lacks the interporal partition that characterizes echinoid pore pairs. In at least some taxa, the pore through which the podia protrude is at the border between two sequentially added plates (Gosselin and Jangoux, 1998;Gao et al., 2015). This is also similar to the podia that span across multiple ambulacral plates seen in some bothriocidaroid echinozoans , and is also reminiscent of the pores in Kailidiscus and the shared podial basins of asterozoans (Zhao et al., 2010). ...
The extraxial-axial theory (EAT) and universal elemental homology (UEH) are often portrayed as mutually exclusive hypotheses of homology within pentaradiate Echinodermata. EAT describes homology upon the echinoderm bauplan, interpreted through early post-metamorphic growth and growth zones, dividing it into axial regions generally associated with elements of the ambulacral system and extraxial regions that are not. UEH describes the detailed construction of the axial skeleton, dividing it into homologous plates and plate series based on symmetry, early growth, and function. These hypotheses are not in conflict; the latter is rooted in refinement of the former. Some interpretive differences arise because many of the morphologies described from eleutherozoan development are difficult to reconcile with Paleozoic forms. Conversely, many elements described for Paleozoic taxa by UEH, such as the peristomial border plates, are absent in eleutherozoans. This Element recommends these two hypotheses be used together to generate a better understanding of homology across Echinodermata.
... Larval bodies are supported by four to eight calcareous skeletal rods. After roughly three weeks, the larvae build a juvenile rudiment inside an epidermic invagination (Gosselin and Jangoux 1998). Once they reach this stage, the larvae become "competent" and show behavior, which brings them close to the substratum. ...
... Post-larvae were found to have significantly larger diameters when treated at pH 7.7 compared to control conditions at pH 8.1. As juveniles become exotrophic around 8 days after metamorphosis (Gosselin and Jangoux 1998), the increased scope for growth could be caused by increased metabolism under non-energy limiting conditions (Pörtner and Farrell 2008). The larger juveniles could be less susceptible to predation as they possess larger defensive structures. ...
... Larval bodies are supported by four to eight calcareous skeletal rods. After roughly three weeks, the larvae build a juvenile rudiment inside an epidermic invagination (Gosselin and Jangoux 1998). Once they reach this stage, the larvae become "competent" and show behavior, which brings them close to the substratum. ...
... Post-larvae were found to have significantly larger diameters when treated at pH 7.7 compared to control conditions at pH 8.1. As juveniles become exotrophic around 8 days after metamorphosis (Gosselin and Jangoux 1998), the increased scope for growth could be caused by increased metabolism under non-energy limiting conditions (Pörtner and Farrell 2008). The larger juveniles could be less susceptible to predation as they possess larger defensive structures. ...
Ocean acidification is causing changes to the chemistry and biology of the marine environment, in ways that we are only just beginning to understand. Growing evidences demonstrate that ocean acidification can influence the survival, growth, development, and physiology of marine invertebrates. Here, we assessed the impact of ocean acidification on the sea urchin Paracentrotus lividus larval development (from embryos exposed to experimental conditions from the 24 h gastrula stage to 35 days) and settlement. Samples were collected from the Canary Islands (28°24′N, 16°18′W) in March 2012. Three pH treatments were tested: (1) pH 8.1, the present average pH; (2) pH 7.7, the average predicted for the year 2100, but already experienced in the natural environment during extremes of variability; and (3) pH 7.4, predicted extremes of natural variability by 2100. The mortality rate was significantly increased by 40 % at the lowest pH. Time required by larvae to achieve each developmental stage (from gastrula to competent stage) was decreased at pH 7.7 (larval development speed increased by 18 %), but larval morphology at a given size did not differ from the other pH treatments. Settlement was delayed by 8 days at pH 7.7 compared to pH 8.1, and no settlement was observed at pH 7.4. Overall, only sublethal effects were observed in larvae exposed to pH 7.7, while pH 7.4 induced both lethal and sublethal effects. Our results support the hypothesis that P. lividus is robust to survive in an environment with the present natural variation. However, the species is sensitive to extreme levels of pH that are predicted within the next 90 years.
... One impediment to using echinoderms as subjects for detailed metamorphic studies is the lack of an agreed upon, simple, yet appropriately detailed scheme for describing the stages of juvenile morphogenesis leading up to settlement (except for brittle stars; [31,32]). This information gap exists despite many careful studies over more than a hundred years into the ontogeny of the structures in echinoderm larvae that are fated to form the juvenile (i.e., juvenile structures in contrast to larval onessee e.g., [33][34][35][36]). ...
... To encourage the use of echinoids in these ways, we envision our staging scheme as a template for the development of similar schemes across echinoids. Over 120 years of research effort has been directed at descriptions of late larval and juvenile development across a wide range of echinoid species [12,[34][35][36][37][38][39][40]42,[56][57][58][59][60] and from these studies it is clear that there is substantial variation across echinoids in what and when juvenile skeletal elements form during late larval development. For example, pedicellariae form before settlement in a widely divergent assemblage of species (reviewed in [89]), whereas they form only after settlement in most taxa, including S. purpuratus. ...
Background
The purple sea urchin, Strongylocentrotus purpuratus, has long been the focus of developmental and ecological studies, and its recently-sequenced genome has spawned a diversity of functional genomics approaches. S. purpuratus has an indirect developmental mode with a pluteus larva that transforms after 1–3 months in the plankton into a juvenile urchin. Compared to insects and frogs, mechanisms underlying the correspondingly dramatic metamorphosis in sea urchins remain poorly understood. In order to take advantage of modern techniques to further our understanding of juvenile morphogenesis, organ formation, metamorphosis and the evolution of the pentameral sea urchin body plan, it is critical to assess developmental progression and rate during the late larval phase. This requires a staging scheme that describes developmental landmarks that can quickly and consistently be used to identify the stage of individual living larvae, and can be tracked during the final two weeks of larval development, as the juvenile is forming.
Results
Notable structures that are easily observable in developing urchin larvae are the developing spines, test and tube feet within the juvenile rudiment that constitute much of the oral portion of the adult body plan. Here we present a detailed staging scheme of rudiment development in the purple urchin using soft structures of the rudiment and the primordia of these juvenile skeletal elements. We provide evidence that this scheme is robust and applicable across a range of temperature and feeding regimes.
Conclusions
Our proposed staging scheme provides both a useful method to study late larval development in the purple urchin, and a framework for developing similar staging schemes across echinoderms. Such efforts will have a high impact on evolutionary developmental studies and larval ecology, and facilitate research on this important deuterostome group.
... In the present study, we analysed P. lividus larval mortality and growth in response to OA conditions, together with the presence of carry-over effects due to acclimation of parents to different pH during gametogenesis. The mortality observed at control condition was consistent with data reported in the literature for P. lividus larvae reared for 18-20 days (Gosselin and Jangoux, 1998;Liu et al., 2007). In previous studies, the survival of P. lividus larvae was not affected by pH 7.7 during both endotrophic (Martin et al., 2011;Garcia et al., 2018) and exotrophic phase (Garcia et al., 2015a;). ...
In marine organisms, differing degree of sensitivity to ocean acidification (OA) is expected for each life stage, and disturbance at one stage can carry over into the following stage or following generation. In this study we investigated phenotypic changes of sperm and larvae of the sea urchin Paracentrotus lividus in response to different pH conditions (8.0, 7.7, 7.4) experienced by the parents during gametogenesis. In sperm from two-months exposed males, sperm motility, velocity, ATP content, ATP consumption and respiration rate were evaluated at three pH values of the activating medium (8.0, 7.7 and 7.4). Moreover, larvae from each parental group were reared at pH 8.0 and 7.7 for 20 days and larval mortality and growth were then assessed. Sperm motility and respiration rate were not affected either by exposure of males to low pH or by the post-activation pH. Sperm velocity did not differ among post-activation pH values in all sperm groups, but it decreased slower in sperm developed under acidified conditions, suggesting the presence of positive carryover effect on sperm longevity. This positive carryover effect of exposure of males to low pH values was highlighted also for the sperm ATP content, which was higher in these groups of sperm. ATP consumption rate was affected by post-activation pH with higher values at pH 8.0 in sperm from males maintained at control condition and pH 7.7 while the energy consumption appeared to be differently modulated at different experimental conditions. A negative carry over effect of OA was observed on survival of larvae from parents acclimated at pH 7.4 and additive negative effects of both parental and larval exposure to low pH can be suggested. In all groups of larvae, decreased somatic growth was observed at low rearing pH, thus larvae from parents maintained at low pH did not show an increased capability to cope with OA.
... The mechanisms to avoid oxidative damage cost energy which is not available to growth and might explain the effect observed in our work in the first 48 h of exposure. Approximately 48 h post-hatching the energy reserves of the egg start to decrease, the digestive system of P. lividus larvae is fully developed and larvae start the digestion of phytoplankton (Gosselin and Jangoux, 1998). Additional energy uptake through feeding might temporarily counter the cost of growing in an adverse media. ...
One of the major consequences of increasing atmospheric CO2 is a phenomenon known as ocean acidification. This alteration of water chemistry can modulate the impact on marine organisms of other stressors also present in the environment, such as microplastics (MP). The objective of this work was to determine the combined impact of microplastic pollution and ocean acidification on the early development of Paracentrotus lividus. To study these multi-stressor impacts on development P. lividus the sea urchin embryo test (SET) was used. Newly fertilised embryos of P. lividus were exposed to a control treatment (filtered natural seawater), MP (3000 particles/mL), acidified sea water (pH = 7.6), and a combination of MP and acidification (3000 particles/mL + pH = 7.6). After 48, 72, and 96 h measurements of growth and morphometric parameters were taken. Results showed that ocean acidification and MP cause alterations in growth and larval morphology both before and after the larvae start to feed exogenously. The exposure to MP under conditions of ocean acidification did not produce any additional effect on growth, but differences were observed at the morphological level related to a decrease in the width of larvae at 24 h. Overall, changes in larvae shape observed at three key points of their development could modify their buoyancy affecting their ability to obtain and ingest food. Therefore, ocean acidification and MP pollution might compromise the chances of P. lividus to survive in the environment under future scenarios of global climate change.
... After finding OPEN www.nature.com/scientificreports/ suitable settlement substrate and attaching to it, full metamorphosis into a benthic juvenile can be achieved [19][20][21] . While these transitions are likely to be susceptible to OA, most studies have been restricted to a single stage. ...
Ongoing ocean acidification is expected to affect marine organisms and ecosystems. While sea urchins can tolerate a wide range of pH, this comes at a high energetic cost, and early life stages are particularly vulnerable. Information on how ocean acidification affects transitions between life-history stages is scarce. We evaluated the direct and indirect effects of pH (pHT 8.0, 7.6 and 7.2) on the development and transition between life-history stages of the sea urchin Strongylocentrotusdroebachiensis, from fertilization to early juvenile. Continuous exposure to low pH negatively affected larval mortality and growth. At pH 7.2, formation of the rudiment (the primordial juvenile) was delayed by two days. Larvae raised at pH 8.0 and transferred to 7.2 after competency had mortality rates five to six times lower than those kept at 8.0, indicating that pH also has a direct effect on older, competent larvae. Latent effects were visible on the larvae raised at pH 7.6: they were more successful in settling (45% at day 40 post-fertilization) and metamorphosing (30%) than larvae raised at 8.0 (17 and 1% respectively). These direct and indirect effects of ocean acidification on settlement and metamorphosis have important implications for population survival.
... A competent larva develops a large embryonic urchin inside its body, the rudiment. After finding suitable settlement substrate and attaching to it, full metamorphosis into a benthic juvenile can be achieved [18][19][20] . While these transitions are likely to be susceptible to OA, most studies have been restricted to a single stage. ...
A bstract
Ongoing ocean acidification (OA) is expected to affect marine organisms and ecosystems. While sea urchins can survive a wide range of pH, this comes at a high energetic cost, and early life stages are particularly vulnerable. Information on how OA affects transitions between life-history stages is scarce. We evaluated the direct and indirect effects of pH (pH T 8.0, 7.6 and 7.2) on the development and transition between life-history stages of the sea urchin Strongylocentrotus droebachiensis , from fertilization to early juvenile. Continuous exposure to low pH negatively affected larval mortality and growth. At pH 7.2, formation of the rudiment (the primordial juvenile) was delayed by two days. Larvae raised at pH 8.0 and transferred to 7.2 after competency had mortality rates five to six times lower than those kept at 8.0, indicating that pH also has a direct effect on older, competent larvae. Latent effects were visible on the larvae raised at pH 7.6: they were more successful in settling (45%) and metamorphosing (30%) than larvae raised at 8.0 (17 and 1% respectively). These direct and indirect effects of OA on settlement and metamorphosis have important implications for population survival.
... Stages during embryogenesis have been defined based on previous descriptions (Hörstadius, 1973) and the same applies for the larval stages (e.g. Gosselin and Jangoux, 1998). Importantly, larval growth and development following embryogenesis rely on food uptake. ...
Nervous systems in metazoans range from simple nerve nets to complex centralized organs. Because of such diversity, the evolutionary history of nervous system in metazoans has been heavily debated. Echinoderms are a large group of metazoans that constitute with the hemichordates the clade of the ambulacrarians, within the deuterostomes. So far, adult echinoderms have been largely ignored in comparative biology because they exhibit a large set of anatomical oddities. However, a careful examination of neural patterning and organization in adult echinoderms is needed to decipher nervous system evolution in deuterostomes. To achieve this goal, we first improved the husbandry protocol for the sea urchin species Paracentrotus lividus to obtain suitable quantities of post-metamorphic individuals for experimentations. Then, we facilitated the study of post-metamorphic echinoids by staging the development of P. lividus from fertilization to post-metamorphic juvenile stages. Finally, we yielded an exhaustive body-wide description of the neuromuscular anatomy of post-metamorphic P. lividus juveniles which indicated that the nervous system of adult echinoids is not strictly centralized as it also includes elements that are typical of nerve nets. Similar investigation in post-metamorphic specimens of the sea star Patiria miniata and the sea cucumber Parastichopus parvimensis revealed a similar organization. Finally, we started a molecular screening of neural patterning genes in post-metamorphic P. lividus and P. miniata juveniles, suggesting that a genetic program similar to the one found in hemichordates is also used to pattern the ectoderm of adult echinoderms.
... This type of interaction between stressors was described by Darling et al. (2010) as a non-additive antagonism, present when one of the stressors has a dominant or greater impact than the others. These effects occur in the first 48 h after hatching, the beginning of the so-called planktonic stage in which the larvae start to feed independently (Gosselin and Jangoux, 1998). Although after 30 days the larvae structures are reabsorbed leading to the adult form of the sea urchin, during the planktonic stage the size and morphology of P. lividus larvae are crucial to ensure their buoyancy and therefore their survival. ...
The aim of this work was to estimate the potential risk of the combined effect of global change factors (acidification, temperature increase) and microplastic (MP) pollution on the growth and development of the sea urchin P. lividus. Embryo-larval bioassays were conducted to determine growth and morphology after 48 h of incubation with MP (1000 and 3000 particles/mL); with filtered sea water at pH = 7.6; and with their combinations. A second experiment was conducted to study the effect of pH and MP in combination with a temperature increase of 4 °C compared to control (20 °C). We found that the inhibition of growth in embryos reared at pH = 7.6 was around 75%. Larvae incubated at 3000 MP particles/mL showed a 20% decrease in growth compared to controls. The exposure to MP also induced an increase in the postoral arm separation or rounded vertices. The combined exposure to a pH 7.6 and MP caused a significant decrease of larval growth compared to control, to MP and to pH 7.6 treatments. Morphological alterations were observed in these treatments, including the development of only two arms. Increasing the temperature resulted in an increased growth in control, in pH 7.6 and pH 7.6 + MP3000 treatments, but the relative stomach volume decreased. However, when growth parameters were expressed per Degree-Days the lower growth provoked by the thermal stress was evidenced in all treatments. In this work we demonstrated that MP could aggravate the effect of a decreased pH and that an increase in water temperature generated an additional stress on P. lividus larvae, manifested in a lower growth and an altered development. Therefore, the combined stress caused by ocean warming, ocean acidification, and microplastic pollution, could threaten sea urchin populations leading to a potential impact on coastal ecosystems.
... The metamorphic transition is a critical one for animals with complex life cycles, with 30% mortality reported within the first day of benthic life (reviewed by Gosselin and Qian 1997). At the same time, the feeding structures of juvenile echinoderms are often not yet functional following metamorphosis and metabolism during the first week or more of juvenile life is fueled entirely by endogenous reserves accumulated during the larval period (e.g., Gosselin and Jangoux 1998). Given these aspects of juvenile biology, and despite prior reports of adult cannibalism in at least a dozen asteroid species (Lawrence et al. 2013), we were surprised to find frequent juvenile cannibalism among laboratory cultures of the New England sea star Asterias forbesi as soon as 4 d postmetamorphosis. ...
Cannibalism is widespread across the animal kingdom, occurring in more than 1300 species of invertebrates and vertebrates across terrestrial and aquatic habitats (Fox, 1975; Polis, 1981; Elgar and Crespi, 1992). Cannibalism, defined as the consumption of all or part of a conspecific individual, can occur during multiple stages in the life cycle of an organism (Elgar and Crespi, 1992). As such, cannibalism potentially affects animal behavior, life history strategies, population size and reproductive success (Cushing et al., 2015).
... Cobbles with at least one juvenile attached to them were used for experiments. A total of six cobbles were placed into each experimental tank and left there for a total of 4 days (5 days after introduction to the cue), given that sea urchin juveniles undergo a perimetamorphic period that generally lasts at least 4 day, where they are unable to feed because they have yet to develop a digestive system and other internal structures (Gosselin and Jangoux, 1998;Rahman et al., 2012). Newly settled P. huttoni juveniles were grown under six experimental treatment conditions, comprised of three bulk seawater pH levels (pH T 7.5, 7.7, and 8.1) and two irradiance levels (light and dark), with each treatment replicated three times. ...
Chemical changes in the diffusive boundary layer (DBL) generated by photosynthesising macroalgae are expected to play an important role in modulating the effects of ocean acidification (OA), but little is known about the effects on early life stages of marine invertebrates in modified DBLs. Larvae that settle to macroalgal surfaces and remain within the DBL will experience pH conditions markedly different from the bulk seawater. We investigated the interactive effects of seawater pH and DBL thickness on settlement and early post-settlement growth of the sea urchin Pseudechinus huttoni, testing whether coralline-algal DBLs act as an environmental buffer to OA. DBL thickness and pH levels (estimated from well-established relationships with oxygen concentration) above the crustose coralline algal surfaces varied with light availability (with photosynthesis increasing pH to as high as pH 9.0 and respiration reducing pH to as low as pH 7.4 under light and dark conditions, respectively), independent of bulk seawater pH (7.5, 7.7, and 8.1). Settlement success of P. huttoni increased over time for all treatments, irrespective of estimated pH in the DBL. Juvenile test growth was similar in all DBL manipulations, showing resilience to variable and low seawater pH. Spine development, however, displayed greater variance with spine growth being negatively affected by reduced seawater pH in the DBL only in the dark treatments. Scanning electron microscopy revealed no observable differences in structural integrity or morphology of the sea urchin spines among pH treatments. Our results suggest that early juvenile stages of P. huttoni are well adapted to variable pH regimes in the DBL of macroalgae across a range of bulk seawater pH treatments.
... Substantial long-distance gene flow is also reported outward the NEA, for the sea cucumber Cucumaria frondosa over 5000 km from Norway to the East coasts of North America (N e m = 80) [56]. The PLD of 4-8 weeks in M. neritoides is comparable to that of Paracentrotus lividus (PLD = 3 weeks) [57], Scrobicularia plana (PLD = 2-4 weeks) [58] and Cucumaria frondosa (PLD = 6 weeks) [59] (the PLD of Tectarius striatus is unknown). This suggests that, as expected, planktonic-dispersing species with a long-lived larval dispersal stage may achieve high levels of gene flow in the NEA basin. ...
Background
Hyperdiverse mtDNA with more than 5% of variable synonymous nucleotide sites can lead to erroneous interpretations of population genetic differentiation patterns and parameters (φST, DEST). We illustrate this by using hyperdiverse mtDNA markers to infer population genetic differentiation and connectivity in Melarhaphe neritoides, a NE Atlantic (NEA) gastropod with a high dispersal potential. We also provide a recent literature example of how mtDNA hyperdiversity may have misguided the interpretation of genetic connectivity in the crab Opecarcinus hypostegus.
Results
mtDNA variation surveyed throughout the NEA showed that nearly all M. neritoides specimens had haplotypes private to populations, suggesting at first glance a lack of gene flow and thus a strong population genetic differentiation. Yet, the bush-like haplotype network, though visually misleading, showed no signs of phylogeographic or other haplotype structuring. Coalescent-based gene flow estimates were high throughout the NEA, irrespective of whether or not mtDNA hyperdiversity was reduced by removing hypervariable sites.
Conclusions
Melarhaphe neritoides seems to be panmictic over the entire NEA, which is consistent with its long-lived pelagic larval stage. With hyperdiverse mtDNA, the apparent lack of shared haplotypes among populations does not necessarily reflect a lack of gene flow and/or population genetic differentiation by fixation of alternative haplotypes (DEST ≈ 1 does not a fortiori imply φST ≈ 1), but may be due to (1) a too low sampling effort to detect shared haplotypes and/or (2) a very high mutation rate that may conceal the signal of gene flow. Hyperdiverse mtDNA can be used to assess connectivity by coalescent-based methods. Yet, the combined use of φST and DEST can provide a reasonable inference of connectivity patterns from hyperdiverse mtDNA, too.
... Most echinoids settle a few days to a week or so before their juvenile mouths open, during which time they use up endogenous reserves from the larva. Once their mouths are open, they are more or less ready to begin feeding (Fadl, Mahfouz, El-Gamal, & Heyland, 2017;Gosselin & Jangoux, 1998;Miller & Emlet, 1999). At that point, in particular with juveniles deriving from planktotrophic larvae, juveniles (2006) Note that these concentrations are the excess potassium added to SW (which already contains potassium at approximately 90 mM). ...
Echinoderms are favored study organisms not only in cell and developmental biology, but also physiology, larval biology, benthic ecology, population biology and paleontology, among other fields. However, many echinoderm embryology labs are not well-equipped to continue to rear the post-embryonic stages that result. This is unfortunate, as such labs are thus unable to address many intriguing biological phenomena, related to their own cell and developmental biology studies, that emerge during larval and juvenile stages. To facilitate broader studies of post-embryonic echinoderms, we provide here our collective experience rearing these organisms, with suggestions to try and pitfalls to avoid. Furthermore, we present information on rearing larvae from small laboratory to large aquaculture scales. Finally, we review taxon-specific approaches to larval rearing through metamorphosis in each of the four most commonly-studied echinoderm classes—asteroids, echinoids, holothuroids and ophiuroids.
... We described two developmental stages in the present study: in June we sampled an early post-larva, in July a late-stage larva with maximum arm length of 3 mm (arms can growth >4.5 mm long) (Williams et al. 2011), and in August another early post-larva that was ready to settle. It was unusual to find post-larvae in the plankton tows since this developmental stage precedes the juvenile stage in most sea urchin species (Gosselin and Jangoux 1998). A settling larva experiences numerous hydrodynamic forces (lift, drag, friction, fluid acceleration, and turbulent shear stresses, among others). ...
The reduction in the Diadema antillarum Philippi, 1845 population across the Caribbean region in the 1980s had adverse ecological consequences, including coralalgal phase-shifts. Reduced larval supply, and subsequent low recruitment success, has hampered population recovery. To examine larval density and the influence of hydrodynamics on settlement of D. antillarum, monthly plankton tows were conducted from May 2014 to April 2015 in the lagoon and fore reef zones of a western Caribbean coral reef (Xcalak, Mexico). A moored Nortek acoustic waves and currents (AWAC-Nortek) oceanographic instrument recorded wave height, wave velocity, and suspended particles in the water column. To assess settlement of D. antillarum, collectors were placed along the lagoon and fore reef, and inspected monthly. Monthly samples had a mean density of 0.06 larvae per 15 m3 from June to August corresponding to two developmental stages. Five settlers with test diameter approximately 1 mm were collected from August to December. During August, Doppler profiles recorded via the AWAC-Nortek instrument showed the lowest wave height values (<0.3 m) and a low bottom shear stress of <0.15 N m ⁻¹ . Acoustic signals indicated that the particle displacement was driven primarily by wave action and that currents played a secondary role. During settlement of D. antillarum, wave orbital velocity (U w ) was below the threshold of motion (U wr ), allowing deposition of particles at the seabed. These hydrodynamic conditions suggest a window of opportunity for larval transport and benthic settlement. Ours is the first field study documenting the mechanisms that link hydrodynamics to the settlement of D. antillarum to a Caribbean reef. © 2019 Rosenstiel School of Marine & Atmospheric Science of the University of Miami.
... During this process, most larval structures (including most larval skeletal elements) are lost. During the late feeding stage, some future adult skeletal elements (e.g., certain genital and terminal plates that will be incorporated into the test on the aboral side of the animal) grow from the proximal tips of larval rods (Emlet, 1985;Gosselin & Jangoux, 1998). Most adult skeletal structures, however, arise de novo within the echinus rudiment and are produced by fusogenic, mesenchymal cells of unknown lineage (Kniprath, 1974;Märkel, Roeser, Mackenstedt, & Klostermann, 1986 Ettensohn et al., 1997). ...
... These larvae, at the end of the experimental period, had similar survival rates and rudiment lengths to those reared at low density (1 mL −1 ) despite a smaller size. This indicates that a density change approach to larval rearing may be a viable option in large scale cultivation of P. miliaris as rudiment development is key to metamorphosis into a competent juvenile (Gosselin and Jangoux, 1998). ...
Increased pressure on wild stocks of sea urchins had led to a requirement for aquaculture based production. However, effective and efficient methodologies still remain under development. The effects of stocking density on Psammechinus miliaris and Paracentrotus lividus were investigated in order to evaluate optimum stocking densities for large scale production. Larvae were reared at stocking densities of 1, 2, 3 and 4 larvae mL⁻¹ and the effects on survival, development, abnormality and morphology were recorded. Additional cultures were maintained at a high density of 3 larvae mL⁻¹ and then displaced to a lower density of 1 larvae mL⁻¹ part way through the larval life cycle (‘displacement treatment’; day 13), to evaluate whether negative effects of high stocking densities could be mitigated. Responses from each species differed. P. miliaris demonstrated the highest growth at 1 larvae mL⁻¹, resulting in larger larval and rudiment sizes by the end of the experiment (day 16). Rearing at 2 larvae mL⁻¹ also demonstrated good growth performance, but only up to day 12. Higher densities of 3 and 4 larvae mL⁻¹ did not affect survival or development, but significantly negatively impacted growth. There was no significant impact on survival, development, and morphology at any of the tested stocking densities for P. lividus. However, of note is that P. lividus reared at a high density of 4 larvae mL⁻¹ had 25% lower survival than controls by the end of the experimental period (day 16). Displacement (larvae transferred from 3 to 1 larvae mL⁻¹ on day 13) was effective for both P. miliaris and P. lividus with survival and rudiment sizes similar to larvae stocked continuously at low densities of 1 larvae mL⁻¹. Although, P. lividus generally performed well at high densities, this demonstrates that displacement approaches could be possible for this species if required. However, of note is that displaced P. lividus had 30% lower survival than controls by the end of the experimental period (day 16). Therefore, this cultivation approach may be a generally viable option for large scale cultivation of these species. This study highlights that species responses can be different when reared at differing stocking densities highlighting a need to expand this approach to a wider range of marketable species. It also demonstrates that more efficient means of production (e.g. displacing larval densities part way through the production process) might be possible for some species (e.g. P. miliaris).
... The perimetamorphic period is an essential period in the life-history of P. lividus and assembles all the events for the transformation of a pelagic organism into a benthic one. This period, as defined by Gosselin and Jangoux (1998), starts from the acquisition of larval competence, includes the metamorphosis and the endotrophic post-larval life, and stops with the appearance of the exotrophic juvenile. This period is a non-feeding stage where metamorphosed larva uses stored reserves during the larval life (Byrne et al., 2008). ...
In this study, the morphological plasticity and larval and post-larval survival from eggs obtained
from a single population of Paracentrotus lividus (Lamarck, 1816) during a reproductive
cycle was compared. For this purpose, four seasonal larval cultures were conducted and
maintained in the same feeding conditions. Morphological parameters were recorded during
larval development and survival and metamorphosis rate at the end of the cultures. The duration
of larval life ranged from 16-18 days, except for the culture of autumn that ended the
day 26. On day 11, 100% of larvae sampled had the rudiment in spring, summer and winter;
no differences in size. No significant differences between larval survival (>80%), however,
metamorphosis rates were significantly different between seasons. Spring larvae reached the
best results (94%), while autumn equinopluteus, with the worst rates recorded, only got 31%.
The observations obtained on the morphometry of equinopluteus and larval and post-larval
reached at different times of the year contribute to the knowledge of larval behavior and the
establishment of optimal and profitable aquaculture production periods yields.
... We tested the effects of biofilm and larval food on juvenile development postsettlement, before the onset of feeding, (i.e., the peri-metamorphic period sensu Gosselin and Jangoux, 1998). While biofilm grown from artificial seawater appears to change the ratio of arm length to test diameter, it does not affect juvenile test size. ...
Some sea urchins, including the purple sea urchin Strongylocentrotus purpuratus, have been successfully used in aquaculture, but their slow growth and late reproduction are challenging to overcome when developing efficient aquaculture production techniques. S. purpuratus develops via an indirect life history that is characterized by a drastic settlement process at the end of a larval period that lasts for several weeks. During this transition, the bilateral larva is transformed into a pentaradial juvenile, which will start feeding and growing in the benthic habitat. Due to predation and other ecological factors, settlement is typically associated with high mortality rates in juvenile populations. Additionally, juveniles require several days to develop a functional mouth and digestive system. During this perimetamorphic period, juveniles use up larval resources until they are capable to digest adult food. Mechanisms underlying the onset of juvenile feeding and metabolism have implications for the recruitment of natural populations as well as aquaculture and are relatively poorly understood in S. purpuratus. The insulin/insulin-like growth factor signalling (IIS)/Target of Rapamycin (TOR) pathway (IIS/TOR) is well conserved among animal phyla and regulates physiological and developmental functions, such as growth, reproduction, aging and nutritional status. We analyzed the expression of FoxO, TOR, and ILPs in post-settlement juveniles in conjunction with their early growth trajectories. We also tested how pre-settlement starvation affected post-settlement expression of IIS. We found that FoxO provides a useful molecular marker in early juveniles as its expression is strongly correlated with juvenile growth. We also found that pre-settlement starvation affects juvenile growth trajectories as well as IIS. Our findings provide preliminary insights into the mechanisms underlying post-settlement growth and metabolism in S. purpuratus. They also have important implications for sea urchin aquaculture, as they show that pre-settlement nutrient environment significantly affects both early growth trajectories and gene expression. This information can be used to develop new biomarkers for juvenile health in sea urchin population ecology and aquaculture aquaculture.
... −1 of energetic lipid (~representing 10% of total lipid) that is presumably used to fuel subsequent growth and development. These energetic reserves may be particularly important during the peri metamorphic period, before the juveniles are capable of independent feeding (Gosselin & Jangoux 1998). ...
The eggs of marine species with planktotrophic development must contain, at a minimum, sufficient material for production of a larva that can then sequester additional materials to grow and metamorphose successfully. In echinoderms, lipids perform crucial energy storage and structural functions during larval construction, but their roles during later development and metamorphosis are poorly understood. We investigated lipid-class depletion in early development and accumulation in late development and a lipid nutritional condition index (energetic lipid:sterol ratio) from the egg to the juvenile in the sea star Patiriella regularis and the sea urchin Heliocidaris tuberculata. Three phases were identified: (1) rapid depletion of energetic lipids during embryogenesis and the facultative feeding period (between feeding competence and exhaustion of energetic lipid reserves), (2) larval growth with no improvement in lipid nutritional condition, and (3) rapid lipid accumulation in advanced larvae prior to metamorphosis. Maternally derived energetic lipids were depleted more slowly in fed than unfed larvae but were still exhausted quickly. Patiriella regularis improved their lipid condition index during Phase 3 by accumulating energetic lipid (triacylglycerol [TAG], diacylglycerol ether [DAGE]) reserves that were then partially used to fuel settlement and metamorphosis. In contrast, Heliocidaris tuberculata did not accumulate TAG or DAGE during this phase, suggesting that metamorphosis is fuelled by other reserves, which we hypothesize may be phospholipids.
... Previous studies have shown that PAHs and trace metals sorbed on suspended particles were bioavailable for Crassostrea gigas larvae (Geffard et al., 2002;Geffard et al., 2003). However, this uptake pathway is unlikely for Paracentrotus lividus 48 h pluteus larvae since the endotrophic period lasts for 3 days after fertilization (Fenaux et al., 1985;Gosselin and Jangoux, 1998). ...
Sediments from the Rias of A Coruña, Ferrol, Betanzos and Ares (n = 26) and the Bay of Santander (n = 11) were sampled in July 2012. The concentration of organic contaminants in sediment elutriates (CBs, PAHs, pesticides and personal care products) and sea urchin (Paracentrotus lividus) embryotoxicity were assessed. Relevant concentrations of organic pollutants were detected in the elutriates (ΣContaminants < 400 ng/L) but their interpretation in terms of the observed toxicity was not straightforward. A clear gradient of toxicity from the inner to the outer areas of the Bay of Santander was observed. Sediment elutriates from three stations situated close to the city of A Coruña showed moderate toxicity values, whereas sediment elutriates from the Rias of Ares and Betanzos showed no marked toxicity. Stations located close to the city of Ferrol showed moderate to high toxicity, which is indicative of a nearby source of contamination. On the contrary, the outer area of the Ria of Ferrol was classified as “Good” according to the calculated toxic units. These results allowed for an integrative assessment of the environmental quality of the studied areas.
... For most echinoderms, metamorphosis transforms a bilaterally symmetrical and pelagic larva into a radially symmetrical and benthic postmetamorphic individual. Settlement always takes place during the so-called perimetamorphic period (Gosselin and Jangoux 1998;Haesaerts et al. 2003), but either before or after the metamorphic stage according to the class considered (Strathmann 1978). In both cases, adhesive organs attach either the competent larva or the postlarva to the substratum during settlement. ...
... Differences in post-settlement survival in this study could be because energy reserves can increase with larval development (Byrne et al. 2008). The amount of energy stored by sea urchins as larvae is a key determinate of survival following metamorphosis, as they do not feed for the first 7 to 20 d (Chia & Burke 1978, Gosselin & Jangoux 1998, Vaitilingon et al. 2001, Byrne et al. 2008. The time required to complete metamorphosis and post-settlement size is also linked to larval energy reserves (Downie et al. 2004, Emlet & Sadro 2006. ...
Dispersing organisms often cannot assess habitat quality directly, so they employ
proxies (cues) to choose habitats that maximise fitness. Theory suggests organisms should settle
as soon as they find appropriate cues in order to reduce physiological costs and mortality risk
incurred whilst searching. We propose that for planktotrophic marine larvae, when resources are
plentiful, development of adult structures during an extended larval phase provide post-metamorphosis
benefits that offset the costs of remaining in the plankton. To test this, we measured fitness
consequences of metamorphosis in response to habitat cues at a range of developmental maturities
in 2 sea urchin larvae, Tripneustes gratilla and Centrostephanus rodgersii. We found larvae
that were capable of responding to cues and settling accrued significant benefits if they extended
their pelagic development. Compared to more developed larvae, larvae without adult structures
took longer to metamorphose, and after metamorphosis were 11 to 25% smaller, 0.1 to 6 times
more likely to lack defensive structures and 3 to 13 times more likely to have abnormal morphology.
Most early settlers died within 1 wk compared to >40% survival for more developed larvae.
We found larvae avoid the costs of early metamorphosis by only responding to low concentrations
of cues in the water column once they have adult structures. Our results contrast with models of
habitat selection that suggest organisms should settle in habitat quickly to minimise search costs.
Incorporating the trade-off between the benefits of larval development and search costs into current
models of habitat selection may provide new insights into how fitness consequences affect
habitat selection.
... The perimetamorphic period in sea urchin development starts with the acquisition of larval competence and goes to endotrophic postlarva (prejuvenile stage) (Gosselin and Jangoux, 1998). This period has been progressively seen as particularly sensitive to nanosilver toxicity (Suwa et al., 2014;Chan and Chiu, 2015). ...
... Postlarvae were significantly larger in test diameter at pH 7.7 and 7.4 compared to control conditions (8.1) at 20.5 C. Hence more acidic conditions seem to have a positive impact on postlarvae at 20.5 C. Juveniles become exotrophic around eight days after metamorphosis (Gosselin and Jangoux, 1998), thus, this increased scope for growth could be a consequence of an increased metabolism under non-limiting energy conditions (P€ ortner and Farrel, 2008). Larger juveniles have larger defensive structures (e.g. ...
... The postmetamorphic period begins with a short endotrophic stage. During this period, the postmetamorphic individuals, also called postlarvae, reorganize their digestive tract (Gosselin and Jangoux 1998). The mouth and anus of the future juvenile are not yet pierced. ...
Today, most sea urchins fisheries worldwide must deal with overexploitation. Better management of exploited field populations and/or aquaculture is increasingly considered necessary to sustain sea urchin production in the future. In this context, we evaluate the potential of land-based, closed-cycle echiniculture. A long-term experiment with the edible sea urchin Paracentrotus lividus has been done on a pilot scale. The process allows total independence from natural resources, because the entire biological cycle of the echinoids is under control (closed-cycle echiniculture), and all activities are performed on land. Furthermore, a method has been set up to control the reproductive cycle with the aim to produce marketable individuals all year long. Performances obtained on each stage of the rearing process are quantified and analyzed. Overall, the results of this experiment are promising; however, some problems remain to be solved before we can claim profitability. The most important finding is that land-based, closed-cycle echiniculture is a potential viable supplement to fisheries to sustain worldwide sea urchin roe production.
... All plates bear spines that are attached to tubercles (Smith, 1984). A single large primary tubercle is attached on each interambulacral plate, and several small tubercles and granules grow along the outer margins of interambulacral plates and on the suture between ambulacral columns (David and Néraudeau, 1989;Gosselin and Jangoux, 1998). The corona of sea urchins comprises five growth zones that originate from each ocular plate (Fig. 3, David et al., 1995;Mooi and David, 2008;Mooi et al., 1994Mooi et al., , 2005Morris and Byrne, 2005) and numbered according to a specific morphogenetic sequence (Lovén, 1874). ...
Tropical western Atlantic reefs have gradually shifted from being dominated by corals to being mainly covered by macroalgae. The mass-mortality of the sea urchin Diadema antillarum in the 80s and the slow to non-existent recovery exacerbated this shift. Chemical cues associated with these reefs are expected to have shifted too with potential negative effects on larval recruitment, possibly limiting recovery of important species like D. antillarum. In this study, we tested the effects of naturally derived biofilm and macroalgae species native to Caribbean coral reefs on the settlement rate of cultured D. antillarum larvae in two separate experiments. Crustose coralline algae (CCA) were included in both experiments, making it possible to compare settlement rates from both experiments. A biofilm of one week old yielded significantly lower settlement rates compared to two, four, and six weeks old biofilm and the highest settlement rate was found for CCA with over 62% of total larvae. All six tested macroalgae species resulted in settled larvae, with little significant difference between algal species, partly due to a high variation in settlement rates within treatments. Sargassum fluitans induced the highest settlement rate with 33%, which was not significantly different from CCA with 29%. We conclude that dominant macroalgae species likely to be encountered by D. antillarum on shifted reefs are no major constraint to settlement. Our findings increase the understanding of alternative stable state settlement dynamics for a keystone coral reef herbivore.
Marine invertebrates with biphasic life cycles feature life history transitions that coincide with habitat changes from benthic adults to planktonic embryos and larvae, then a return to the benthos as a juvenile at metamorphosis. The metamorphic transition exposes animals to a new suite of benthic predators, and high mortality often occurs in the hours and days following settlement. Juvenile invertebrates may produce phenotypically plastic morphological defenses when predator cues are detected. However, time lags inherent to phenotypic plasticity may delay the production of defenses until after the period of highest vulnerability. It should, therefore, be beneficial for planktonic larvae approaching settlement to detect waterborne cues from benthic predators and produce juvenile phenotypes appropriate for postmetamorphic survival. Echinoderms are useful models for testing transhabitat and trans-life history stage phenotypic plasticity because many species have larvae that construct their juvenile phenotype while still in the water column. In this study, we tested whether planktonic echinoderm larvae exposed to cues from benthic predators modified their juvenile phenotypes at settlement. Green urchin (Strongylocentrotus droebachiensis) and Pacific sand dollar (Dendraster excentricus) larvae were exposed to predatory green crab (Carcinus maenus) or red rock crab (Cancer productus) cues, respectively, from their early-stage juvenile rudiment formation through settlement. Green urchin larvae exposed to predator cues settled with significantly more juvenile spines compared to unexposed controls. Sand dollars exhibited earlier settlement, larger disk area, fewer spines, and shorter spines when exposed to benthic predator cues. Sand dollar larvae were also exposed to cues from planktonic crab larvae and in response settled sooner and larger, with even fewer and shorter spines than those exposed to benthic predator cues. These results suggest that echinoderm larvae alter their juvenile phenotype in response to predator cues, but the response varies between species, and responses to planktonic threats may be prioritized over benthic ones.
Echinoderms are a common component of benthic marine ecosystems, with many being ecologically and/or economically important. Like many marine organisms, most echinoderms have a bipartite life history with a planktonic larval phase and a benthic adult phase. The transition between these phases (i.e. settlement) is complex and comprises a cascade of events including the location, exploration and selection of suitable benthic habitat, and metamorphosis to adapt from a pelagic to a benthic lifestyle. This review provides a comprehensive synthesis of the various processes involved in the settlement phase across all five extant classes of echinoderms. Central to the review is a detailed assessment of settlement behaviour and the diverse mechanisms of settlement induction. Most echinoderms, including keystone sea urchins, starfishes and sea cucumbers, do not settle indiscriminately; specific environmental conditions or cues are often necessary for settlement to occur, resulting in marked spatial and temporal variability in settlement rates. Fluctuations in settlement, in turn, lead to major changes in the local abundance of echinoderms and often have profound ecological consequences, due to the pivotal role that many echinoderms play in ecosystem functioning. Given important knowledge gaps persist, this review also explores opportunities for future research to advance our understanding of this critical early life-history phase.
The development of sustainable methods for sea urchin juvenile production is currently constrained by high mortality rates during larval growth and the high costs of larval rearing systems management. With the aim of developing a method for the production of juveniles of the purple sea urchin Paracentrotus lividus in a medium‐scale recirculating system, the present study focused on the effects of high stocking densities on larval growth. Plutei larvae were reared at three different densities (up to 7 ind/ml) in a semi‐static culture system. Larval survival and metamorphosis success were evaluated in order to identify the most effective density range. The highest metamorphosis rates (80%–95%) were obtained at 4 and 7 larvae/ml. These results are comparable with (and in some cases higher than) those reported for the same species at much lower larval densities. In conclusion, the rearing conditions tested here show for the first time that a significantly higher (4 ind/ml) stocking density than those of traditional P. lividus rearing methods (based on large volumes and low densities) can be adopted, thus supporting the feasibility of an increase in the final output of competent larvae with no increase in rearing volumes.
Sea urchin larvae have developed metamorphosis and settlement stages as an adaptation serving to increase their distribution and find more suitable habitats; for aquaculture farmers, these stages represent a bottleneck, as the cost-effective production of large numbers of metamorphosed larvae in confined conditions remains a major constraint. The aim of this study was the development of a reliable metamorphosis cue for Paracentrotus lividus larvae that is widely available and easy to prepare and use even at the hatchery scale. For this purpose, substrates of environmental origin (GUS - ground Ulva spp. solution) and chemical origin (histamine) were tested for their effectiveness, evaluating the metamorphosis rates of competent P. lividus larvae after 24-h exposure. In addition, differences in metamorphosis rates following exposure to scaled concentrations of both fresh and frozen-thawed GUS were evaluated, with a view to the latter's routine adoption as a metamorphic cue. The metamorphosis rates obtained in the presence of GUS were always around 80%, using both fresh and thawed solutions. Decreasing GUS concentrations resulted in significantly lower percentages of metamorphosed larvae. No metamorphosis occurred after exposure to histamine solutions. GUS proved to be an effective metamorphic cue and to have several other strengths. Indeed, Ulva spp. are widely available and easy to collect in the field as well as being currently cultivated, in some cases in integrated multi-trophic systems. Ulva spp. represent a common food source for natural populations of juvenile and adult P. lividus, and GUS can therefore be used in the formulation of a settlement substrate that also serves as food in the initial post-metamorphosis period. Finally, GUS is prepared by grinding fragments of Ulva spp. with FSW in a mortar and then filtering the solution, with no need for time-consuming or expensive methods. It can thus be easily produced on a commercial scale and then stored or delivered after being frozen. In conclusion, the formulation of GUS represents a promising advance in the development of protocols for echiniculture, meeting the need for tailored metamorphosis and settlement methods that support successful and cost-effective production of sea urchin juveniles. Moreover, it could represent an additional valuable method for obtaining marketable products from harvested Ulva grown in integrated multi-trophic aquaculture systems.
The effect of different treatments on the settlement success, survival and growth of sea urchin juveniles has been evaluated. Two experiments were performed for assessing the ability of substrates or seawater to induce settlement. In the first test 500 competent larvae were inoculated in transparent plastic containers conditioned for ten days with: Tetraselmis marina, Cyilindrotheca closterium, Nitzschia sp., Maërl beds, 100 μm filtered natural seawater and 1 μm filtered and UV disinfected seawater. Maximum settlement values were obtained with C. closterium, Nitzschia sp. films and UV treated seawater; and significant differences were only detected between T. marina films and the other treatments. In the second test the following treatments were performed in order to investigate the effects of filtered seawater on settlement: 0.22 μm filtered and autoclaved seawater (negative control), 1 μm filtered and UV treated seawater and C. closterium (positive control). Settlement success was significantly higher for C. closterium than for autoclaved seawater. Survival and growth of juveniles were monitored for 32 days on these treatments: T. marina, C. closterium, Nitzschia sp., Maërl beds and 100 μm filtered natural seawater. Growth of juveniles could be adequately described by linear fitting and maximum growth rate was found for C. closterium film. There were no significant differences between treatments in terms of mortality at days 21 or 32. In general, the results showed that C. closterium biofilms provide good settlement, growth and survival of sea urchin juveniles which would allow improving general performance of these phases of culture compared to the other diets tested.
A new system of skeletal homologies for echinoderms is presented. The EAT (extraxial-axial theory) recognizes two major components of the body wall: axial elements are arranged in accordance with specific ontogenetic rules operating in association with the water vascular system; and extraxial elements. Embryological evidence demonstrates that axial and extraxial elements are of different origins. The explanatory power of the EAT is tested by deciphering the architecture of extreme morphologies and teratological phenomena. Several implications of the EAT for our interpretation of the phylum and its evolution are analyzed. (1) The interambulacra of echinoids are not homologous with those of other echinoderms, and echinoids are without doubt among the most atypical of echinoderms. (2) The marginal rings of asteroids and edrioasteroids are not homologous. (3) There are different types of < >; those of crinoids and asteroids are homologous, and consequently the pelmatozoan grouping is undetermined. (4) The stylophorans are not early echinoderms, but appear to be closely related to the crinoids. (5) Pentameral symmetry is superimposed on a fundamentally linear arrangement which is comparable to that of most other groups of organisms.
Diadema setosum (Leske, 1778), is one of the common echinoids widely distributed in the Indo-West Pacific Ocean, where it occurs from the Red Sea, Persian Gulf and the east coast of Africa to Japan, Australia and Malaysia. To investigate the developmental basis of morphological changes in embryos and larvae, we documented the ontogeny of D. setosum in a controlled laboratory condition at the Institute of Bioscience, Universiti Putra Malaysia, during July-September, 2012. Matured gametes were obtained from the adult individuals and the eggs fertilized at limited sperm concentration (10-5 dilution). The obtained embryos were then reared at 24-25°C. First cleavage (2-cell), 4-cell, 8-cell, 16-cell, 32-cell and multi-cell (Morulla) stages were attained at 01.20, 02.14, 02.44, 03.09, 03.32 and 03.54 h after fertilization, respectively. Blastulae with a mean length of 111.47±1.88 μm (mean±SD) hatched 08.45 h after sperm entry. Gastrula formed 16.36 h post-fertilization and the archenteron extended constantly, while the ectodermal red-pigmented cells migrated synchronously to the apical plate. The pluteus larva started to feed unicellular algae (Chaetoceros calcitrans) in 2 d, grew continuously, and finally attained metamorphic competence within 35 d after fertilization. Induction of metamorphosis took approximately 1 h 30 min from attachment on the substratum to the complete resorption of larval tissues and the development of complete juvenile structure with adult spines, extended tubefeet and well-developed pedicellaria, the whole event usually took place within 1 d post-settlement. The newly formed juvenile (473.16 ± 6.96 μm, n=30) with a complete adult structure then grew on coralline algae to 3-month old juvenile, which represents the "sea urchin seed" for stocking in grow-out culture. This study represents the first successful investigation on embryonic, larval and early juvenile development of D. setosum. The findings would greatly be helpful towards the development of breeding and seed production techniques for aquaculture of sea urchins. © 2015, Iranian Fisheries Research Organization. All rights reserved.
Echinoderms are a phylum of invertebrate deuterostomes that are morphologically characterized by a fivefold (pentameric) symmetric adult body plan. There are five extant subtaxa, Crinoidea (e.g., sea lilies and feather stars), Asteroidea (e.g., sea stars), Ophiuroidea (e.g., brittle stars), Echinoidea (e.g., sea urchins), and Holothuroidea (e.g., sea cucumbers) (Fig. 1.1). Studies of morphology and molecules demonstrate the existence of two higher-order subphylum clades: Pelmatozoa (Crinoidea) and Eleutherozoa (the remaining classes). Echinodermata together with Hemichordata form the clade Ambulacraria (to which some authors add the enigmatic Xenacoelomorpha group). This grouping is the sister to the Chordata.
The coralline red algae, Lithothumnion gla- ciale, Phymatolithon luevigat urn, P. rugulosum, and Cor- allinu ollicinulis, induced >85% of laboratory-reared lar- vae of Strongyloccntrotus droehachiensis to metamor- phose. Larvae must contact live L. glaciale or its spores for metamorphosis to occur: the inducer is not sensed in the water column. However, aqueous extracts of L. gfu- ciule can induce metamorphosis, suggesting that the in- ducing factor is chemical. Neither ashed nor boiled L. gluciule induces metamorphosis, indicating that the factor is heat-labile and that thigmotaxis, per se, is not important in the response. The amino-acid, y-aminobutyric acid (GABA), which induces settlement of other marine in- vertebrate larvae, also induces significant rates of meta- morphosis of S. droebachiensis at concentrations 2 10e4 M. A reduction (with antibiotics) in the number of live bacteria on the surface of L. glaciale does not affect the rate of metamorphosis of larvae.
Balanus balanoides (L.) has seven planktonic larval stages. The first six are nauplius larvae while the seventh is the cypris larva. The cypris larva is specially adapted to locate a suitable place for settlement. The structure of the nauplius larva is basically similar to that of the nauplii of other crustacean groups. During successive nauplius stages, however, the simplicity of its anatomy is progressively obscured by the development of the cypris organ systems. All the organ systems do not differentiate simultaneously, but development is closely related to the time at which the organ must start to function. The three pairs of nauplius appendages, antennules, antennae and mandibles, are used in locomotion and the latter two pairs are also used in feeding. The six pairs of cypris thoracic swimming appendages, and the first and second maxillae with their associated ganglia and muscles, develop from groups of ectoteloblasts and mesoteloblasts in the ventral thoracic region of the nauplius. The compound eyes develop as outgrowths of the lateral lobes of the brain. The paired cement glands develop pre-orally. The end sacs of the adult maxillary glands develop as cavities in the somites of the second maxillary segment. The cypris antennules develop within the nauplius antennules but differentiation of their intrinsic musculature is delayed until after the nauplius-cypris moult. The various muscles of the cypris carapace are fully formed by the time of the nauplius-cypris moult. During, and after, the moult, a number of morphological and histological changes occur. The antennae and mandibles regress, the intrinsic musculature and cement ducts of the antennules complete their development. At the same time all the nauplius muscles and the antennal glands histolyse. Until these changes are completed the cypris larva is probably unable to settle, and thus to initiate the changes leading to the completion of metamorphosis. Rudimentary adult mandibles, and first and second maxillae are incorporated into the oral cone. After the moult the digestive region of the nauplius mid-gut epithelium and other epithelial cells are sloughed off into the gut lumen and digested together with the remains of the food ingested by the nauplius. The oesophagus and hind gut are now closed and the cypris larva does not feed. The adult digestive glands develop at the junction of the oesophagus and mid-gut. In the cypris the nauplius frontal filaments are associated with the compound eyes and connected to the brain via the optic ganglia. The median eye is apparently unchanged. Paired antennular ganglia are present. Those neurons, which innervated nauplius structures which have histolysed, also degenerate. The nauplius antennal glands degenerate at the nauplius-cypris moult; the maxillary glands are probably the functional organs of ionic regulation in the cypris as well as in the adult. The conspicuous multinucleate oil cells of the cypris are probably a food reserve. The paired masses of yellow cells in the carapace, originate in the antennae of the nauplius and migrate into the carapace after the moult. During the 24 h between settlement and the moult to the young adult, all the cypris muscles histolyse. The muscles break up spontaneously into short fragments which are then ingested by phagocytic haemocytes. There is widespread histolysis of neurons in the nervous system and further cells are sloughed from the gut epithelium. The adult mantle muscles, which are recognizable in the free swimming cypris larva, complete their differentiation, and in the few hours preceding the cypris-adult moult the adult thoracic muscles develop. The nervous system assumes its adult form and adult neurons differentiate from cells which had previously lain dormant in the nervous system. The compound eyes, frontal filaments and optic ganglia degenerate, but the median eye persists apparently unchanged. The yellow cells disperse, but their function is unknown. The cement glands persist in the adult, but the adult gland cells differentiate from cells aroung the collecting duct of the larval gland while the larval cement gland cells histolyse. The median eye persists, but in the newly moulted adult the three components separate giving rise to the three adult photoreceptors: a pair of pigmented ocelli and a median unpigmented photoreceptor. Shortly after the moult the young adult resumes feeding. This study has shown that metamorphosis in Balanus balanoides must be thought of in terms of the change from the nauplius through the cypris to the young adult and not just as the changes taking place between settlement and ecdysis to the young adult.
Larvae of Strongylocentrotus droebachiensis (Müller), Lytechinus pictus (Verrill), and Lytechinus variegatus (Leske) which are competent to metamorphose display what appears to be substratum-testing behavior prior to metamorphosis. Larvae cease swimming, partially evert the adult rudiment, and walk about examining the substratum with their five primary podia. Larvae eithe r metamorphose or withdraw their podia and resume swimming to settle again elsewhere. Scanning and transmission electron microscopic examinations of the primary podia revealed sensory receptor cells on the rim and on a conical projection at the center of the podial sucker. Each sensory cell has a single short cilium on its apical surface a axonal process at its base which contributes to the basiepithelial nerve plexus. Mature adults of the same species also have comparable sensory structures on their tube feet suckers. It is suggested that the sensory receptors on the primary podia of setting larvae, although they are not specialized larval structures, may be involved in the perception of tactil e stimuli which have been previously demonstrated to be involved in the induction of metamorphosis.
The structure of the brachiolar arms and adhesive disk of the brachiolaria larvae of Stichaster australis (Verrill) and Coscinasterias calamaria (Gray) was determined from light microscopy and from scanning and transmission electron microscopy. The structure of these organs was very similar in both species.The brachiolar arms are comprised of a stem region terminating in a crown of adhesive papillae which are made up of a variety of secretory cell types. Principal among these are elongated cells producing very electron-dense secretory particles, which are released at the free cell surface attached to cilia. Secretory particles appear to be important in temporary attachment of the brachiolar arms to the substratum. Ciliary sense cells, possibly used in the recognition of specific substrata are located at the tip of adhesive papillae.The adhesive disk is comprised of large cells packed with secretory droplets and elongated intracellular fibres. In the attached adhesive disk, secretory droplets are lost, having formed the cement that attaches the disk to the substratum. It appears that adhesive papillae lateral to the adhesive disk hold the disk in position close to the substratum during secretion and hardening of the cement. The intracellular fibres are the principal anchoring structures running from microvilli (locked into the attachment cement) on the surface of the disk to the underlying connective tissue of the attachment stalk.
The sea urcimimi enmbryo has played a key role iii embryological studhies for almost a century. Derbès first described time devebopnmental process (thiougim not with complete accuracy) in 1847. In 1876 the eggs were used in Hertwig's experi ments demonstrating the role of sperni in fertilization, and in 1891, Driesch used sea urchin eggs in his experimmmemmts simowing imideternminate cleavage. Iii recent years time sea urchin egg has becomimepartictmiarly promimimmemit in time study of both the niorpimology amid biocimemimistryof eari@' deveiopmmmeimt. ( See reviews by Gustafson and Wolpert, 1963 ; Gross, 1967 ; Davidsomi, 1968.) Probably nmore is now knowmmabout the early devehopnmemmtof time sea urchin than about ammyother organisnm. The reasons for this, other than time fact that early eciminodermmm and vertebrate developmmmentare simmmilar, are primimarihy technical. The animals are easy to obtaimi on ainmost any sea coast, they spawn readily and yield large nummmbers of eggs. Time eggs conmplete meiosis imm time ovaries and therefore can be fertilized inmnmediateiy after spawning. Fertilization is easily accomplished sinmply by addimig sperm to an egg suspension. Development usually follows with good synchrony and with nmininmum care. These eggs readily take up a large miummmber of cimemmmicahs of biological immterest,amid they have time further advammtageof being small amid comitaimming nmuchm less yolk thammeither frog or chicken eggs. One nmajor disadvammtage in the use of sea urchimis has beemi time extreme difficulty in raisimmgthe larvae beyond plutei to adults and thus obtaiimimmg a second generation. This has seldoni been domme,amid never as a useable laboratory procedure. (See Harvey, 1956 for the relevant references.) If the larvae could confidemitly be raised, it would then be possible to apply genetic techniques to the study of sea urchin development. This, along with time otimer advantages these eggs offer, would nmakethem ahimmost ideal nmaterial to use in unravehimmg the developmental process. This paper reports time first steps in that direction. It is aim outhimme of the techniques for raisiimg sea urchins in the laboratory, amid a descriptiomi of the general features of the devehopmmmemmtai stages. Time techiumidlues have mmowbeemi de veloped to the poimmt where large mmummmmbers of umrchmimms can be takemm fronmegg to egg. Though the procedure is not yet as simpie as raising Drosophila, it is l)ractical@