Reproduction
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  Larval life & brooding
  The topic of larval life & brooding is considered in this section, while GONAD GROWTH, SPAWNING & FERTILISATION, and METAMORPHOSIS & SYMMETRY, are considered in other sections.
black dotResearch study 1

photograph of a sea cucumber Psolus chitonoidesA single female Psolus chitonoides may release 35,000 eggs (each 400 x 600µm in size) in a single spawning.  Development is to a gastrula and then to a non-feeding swimming larva called a doliolaria.  Tube feet and tentacles begin to develop in the doliolaria. Within 2wk a pentacula develops that has five primary tentacles and 2 early-stage tube feet.  The pentacula preferentially settles on a conspecific adult or, lacking that, in a shady spot.  Metamorphosis begins after about 4wk and involves secretion of ossicles to form the body plates, branching of the primary tentacles, flattening of the body, and proliferation of the tube feet.  The juvenile then seeks out a shady habitat and shortly begins to feed.  As an adult, Psolus chitonoides rarely moves, and is termed “functionally sessile” by the authors.  Young & Chia 1982 Mar Biol 69: 195; McEuen & Chia 1991 Mar Biol 109: 267.

NOTE  non-feeding invertebrate larvae are rich in yolk and are termed lecithotrophic (lit. "yolk food" G.). Another larval type known as an auricularia is perhaps more common in holothuroids. It is a feeding larva and is termed planktotrophic (see Research Study 6 below)

NOTE  lit. “five” L., referring to the presence of 5 primary tentacles

Sea cucumber Psolus chitonoides amongst yellow cup corals Balanophyllia elegans 1X

scanning e-microscopical photograph of the gastrula stage of development of the sea cucumber Psolus chitonoides
Series showing developmental stages of sea cucumber Psolus chitonoides
scanning e-microscopical photograph of the ealy doiolaria stage of development of the sea cucumber Psolus chitonoides
Tentacles will emerge from the vestibule and tube feet from the podial pit
scanning e-microscopical photograph of the 7-d doliolaria stage of development of the sea cucumber Psolus chitonoides
The aboral surface of the doliolaria larva bears the hydropore, or madreporite
scanning e-microscopical photograph of the 7-d doliolaria stage of development of the sea cucumber Psolus chitonoides
On the oral surface the 5 primary tentacles and primary tube feet are emerging
scanning e-microscopical photograph of the settled pentacula stage of development of the sea cucumber Psolus chitonoides
The settled pentacula stage crawls about for a day or 2, then begins to metamorphose
  black dotResearch study 2
 

graph showing sizes of larvae of various classes of echinoderms and whether they have transverse ciliated bands or are uniformly ciliated
The early early doliolaria larva of Psolus chitonoides is 1100µm in length and has whole-body ciliation for locomotion. The later doliolaria larva is 900µm in length and has three transverse bands of cilia for locomotion.  This is unremarkable in itself, but the author points out an interesting tendency in echinoderm larvae, including those of holothuroids, that small non-feeding larvae tend to have transverse cilitated bands, while larger non-feeding larvae tend to be ciliated all over.  Note in the graph graph showing relationship of buoyancy forces to larval length in doliolaria larvae of the sea cucumber Psolus chitonoideson the Left that this pattern holds for crinoid and ophiuroid larvae, which tend to be small in size. Echinoid and holothuroid larvae are mixed sizes, but note that the larger larvae in these groups tend to have whole-body ciliation.  The largest larvae in Echinodermata are possessed by asteroids and also tend to have whole-body ciliation. 

But what is the significance of transverse-banded or whole-body ciliation?  The author suggests that bands of cilia, while providing enough propulsion for small larvae, are insufficient for larger larvae that have greater buoyancy forces to overcome.  The author calculates these theoretical forces and shows in a model for a theoretical larva a cross-over point at about 650-800µm in length, where drag and buoyancy forces exceed the propulsive forces theoretically generated by 3 or more bands of cilia.  Note that this cross-over size is close to that of the transition size of 900-1100µm noted above for Psolus larvae. 

If whole-body ciliation is so good for propulsion, why are 3- and 4-band patterns retained in smaller-sized larvae?  This, of course, can’t be answered without knowing a lot more about the kinematics of cilia and the water movements caused by them.  The author suggests that for the opposite situation, that is, for ciliary bands to generate sufficient propulsion in larger larvae, they would have to be disproportionately wide, and close-packing of the cilia in this way could create inter-ciliary interference and related water-movement problems.  The author also notes that the theory assumes that the cilia are for propulsion.  If they were to be involved in some not yet known energy-obtaining process, then these ideas would have to be reconsidered.  The theory is an interesting one and is deserving of further research.  Emlet 1994 Am Zool 34: 570.

NOTE  the author also includes frictional drag as a force that the larvae have to overcome when swimming.  This is true.  However, as drag is directly related to surface area, it could be argued that small-sized larvae, having relatively greater surface area than large-sized larvae, would correspondingly have relatively greater frictional resistance to overcome; hence, perhaps should be the ones that possess whole-body ciliation

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photograph of two sea cucumbers Pseudocnus curatus
Several west-coast holothuroids are lecithotrophic, that is, their larvae, while free-living, subsist on yolk and do not feed from the plankton.  Some examples are Cucumaria miniata, C. piperata, Eupentacta quinquesemita, and Psolus chitonoides.  At least 2 other west-coast species, C. pseudocurata and C. curata, brood their eggs under their bodies until the juveniles can crawl out and take up life on their own.  Rutherford 1973 Mar Biol 22: 167.

 

Two well-camouflaged Cucumaria piperata have burrowed into
the sand so that just their mouths and tentacles are visible 1X

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An early description of reproduction in one of these brooding species, Pseudocnus curatus (Cucumaria curata) collected near Dillon Beach, California includes simultaneous production of sperm and eggs in the same individual, suggesting hermaphroditism.  The eggs are sticky on release and this, combined with secretion of mucus over the entire body by the adult, aids in attachment of the eggs to the ventral side of the body among the tube feet.  A gastrula stage is reached about 3d after fertilisation and, after 5d, this transforms to a stage that the author calls a “pentacula”.  This tiny juvenile has 5 primary tentacles and may use these to crawl onto the upper surface of the adult.  By 2wk of age the juvenile (no size given by the author) leaves the parent and takes up independent life. Smith 1962 Pac Nat 3: 233.

NOTE  a pentacula stage is usually considered part of a pelagic developmental pattern in holothuroids, not a brooding one, but the stage shown here does bear close resemblance to that shown in Research Study 1 above

  Research study 4.1
 

photograph of sea cucumber Pseudocnus lubricus courtesy Keoki Stender, Hawai'iField and laboratory observations of sea cucumbers Pseudocnus lubricus at the Friday Harbor Laboratories, Washington reveal that females spawn eggs from anterior gonopores, but capture them immediately in their tube feet before they drift away.   The eggs are retained as a mass between the female’s body and the substratum, hemmed in on either side by tube feet.  Although no sticky mucus is involved, a female is able to move around without losing her eggs.  Males spawn from a genital papilla extended several millimeters from the body and the sperm strands break up as they drift downwards, catching up on females on their way.  Spawning by females occurs during Nov-Jan in late afternoon, while that by males takes place in the same period at mid-day.  Females appear not to feed during the brooding period of autumn-late winter. The eggs are large (almost 1mm diameter) and  are full of yolk.  Egg numbers range between 120-150 depending upon habitat.  Eggs hatch after 6wk, but the young are non-feeding for another 4-8wk until they crawl free of the brood area.  Brooding commences when an adult reaches 1.5-2.4cm in length, at 3-4yr of age.  The author notes that brooding provides protection for the developing embryo and ensures that large numbers of young are recruited to a favourable habitat.  Engstrom 1982 p. 447 In, Echinoderms: Proc Intern Conf, Tampa Bay (ed. JM Lawrence), AA Balkema, Rotterdam. Photograph courtesy Keoki & Yuko Stender, Hawai'i.

NOTE  formerly known as Cucumaria lubrica

NOTE  the author describes an incident in which a brooding adult is reflected back to show its brood, at which time amphipods Parapleustes pugettensis immediately swarm in for the kill

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Research study 5
 

photograph of an auricularia larva of the sea cucumber Parastichopus californicus
photomicrograph of an auricular larva of a sea cucumberMost west-coast holothuroids, including Parastichopus californicus, have an auricularia larva that feeds in the plankton for about 3-5wk.  During this time the larvae propel themselves about and feed using a single, sinuate, ciliary band.  A second, smaller ciliary band is located around the mouth. The bands are thickened regions of the epidermis densely packed with a row of ciliated cells.  The bands are arranged so that a large proportion of the ciliary beat is directed posteriorly and the larva moves with its anterior end foremost.  As food and other particles pass over the ciliated bands, the beating direction reverses in those areas and the particles are deflected towards the oral region.  Inedible particles are sensed and ignored by the bands, or rejected wholesale by complete reversal of beating.  This causes the larva to move backwards and clears the particles from the oral area.  Burke et al. 1986 Biol Bull 170: 450.


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Research study 6
 

scanning e-microscopical photograph of an auricularia larva of the sea cucumber Parastichopus californicusscanning e-microscopical photograph of an doliolaria larva of the sea cucumber Parastichopus californicusThese scanning e-microscopical views show the considerable morphogenetic transformation required in the change from auricularia to doliolaria stages in Parastichopus californicus. Note that the mouth shifts from mid-way along the body to the front of the animal. Lacalli 1993 Acta Zoologica 74: 127.

AURICULARIA stage of development in
Parastichopus californicus
. Note the apparent
difference in size between this larva and the
auricularia shown in Research Study 5 above

DOLIOLARIA stage of development
in Parastichopus californicus

 

 

 

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Research study 7
 
Feeding in the auricularia larva stage is the same as in other echinoderm larvae, as shown in this generalised representation (on the Left). Phytoplankton cells are swept up in micro-currents generated by beating of cilia in the main ciliary band (which also provides for propulsion of the larva). Strathmann 1971 J Exp Mar Biol Ecol 6: 109.





In this simplified diagrammatic representation of the auricularia, ,
water currents generated by the ciliary band are shown on the Right, while
movements of food particles are shown on the Left (thin black arrows)

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Research study 8
 

graph showing seasonal changes in gonadal indices in male and female sea cucumbers Leptosynapta clarkidiagram of an ovary in the viviarous sea cucumber Leptosynapta clarki showing development of pentacula stageThe viviparous sea cucumber Leptosynapta clarki inhabits burrows in intertidal mudflats along the west coast from Haida Gwaii, British Columbia to central California.  In Barkely Sound, British Columbia gonadal growth of L. clarki occurs during the summer, with spawning of males in Nov-Dec (see graph on Right). The female ovary consists of 2 bilaterally symmetrical sacs within which the eggs are packed.  Fertilisation of the oocytes occurs in the ovary, although it is not known how the sperm gain entry, and development to a pentacula stage takes about 2wk (see diagram on Left).  The pentaculae have functional guts and move about in the ovarian fluid feeding on droplets and organic matter. The organic material is derived, in part, from resorption of unfertilised eggs and dead embryos by the parent.  After about 30wk in the ovary, the juveniles are released via rupture of the body wall and crawl out into the immediate habitat of the adult.  Leptosynapta clarki is protandrous, and most or all of these juveniles will function as males for the next reproductive season, after which many will transform to females. Some males remain so through their lifetime. However, at a size of about 500g the sex ratio reaches 1:1.  Sewell & Chia 1994 Mar Biol 121: 285.

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Research study 9
 

Studies at the Bamfield Marine Sciences Centre, British Columbia provide further information on the reproductive cycle of the sea cucumber Leptosynapta clarki. Juveniles of 1-2mm length are released from the ovary in early spring and are reproductively active as males by November graph showing relationship between number of eggs and pentaculae produced by sea cucumbers Leptosynapta clarki in relation to size of femaleof the same year.  By the following year, some individuals continue to reproduce as males, while others transform to females.  Transformation to female occurs at about 200mg live mass or 20mm body length.  Not all individuals change sex.  In fact, the population appears to be divided into ones that change sex at a specific time, ones that change under the influence of some genetic or environmental factor, and ones that remain as males for their entire lifetimes.  There is no allometric constraint on brood size in L. clarki because the brooding is done within the distensible ovary.  Thus, number of eggs or pentaculae scale linearly with mass of female (see graph). The author suggests that sequential hermaphroditism or protandry, which is not common in holothurians, may function to reduce inbreeding in a species with limited dispersal by reducing the chances of sibling crosses.  Sewell 1994 Biol Bull 187: 112.

NOTE  the so-called allometric hypothesis, proposed initially for an external brooder, the sea star Leptasterias hexactis, predicts that brooding will not occur in large species because of spatial limitations on brood size with increasing individual size.  While applicable to external brooders where brooding space scales allometrically with animal mass, it does not apply to internal brooders where internal brooding volume scales isometrically with animal mass.  More on this subject can be found at: LEARN ABOUT CLAMS & RELATIVES/REPRODUCTION & DEVELOPMENT

NOTE  for some reason the author uses drained mass of female, that is, with the coelomic fluid removed, as the abscissa axis of the graph.  This would not change the slope of the relationship, but would affect the intercept

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Research study 10
 

graph showing annual brood mortality in the viviparous sea cucumber Leptosynapta clarki in Barkely Sound, British ColumbiaA follow-up study at the Bamfield Marine Sciences Centre, British Columbia by the same author of Research Study 9 above assesses mortality of the pentaculae (early-stage embryos) over the 30-wk brooding period in the viviparous sea cucumber Leptosynapta clarki. Apparently, such a study has not been done before owing to the difficulty in determining the number of embryos at the start of brooding and not having a way to estimate how many embryos are resorbed after death.  The project is made possible by the discovery that a calcareous ring is present in the embryo at the base of the tentacles that remains after death and is not resorbed by the parental ovary.  Counts of rings and live embryos indicate that mortality, even up to 100% or total brood loss, is not uncommon in Leptosynapta (see graph). The dead larvae are not wasted, however, as  their resorption in the ovary may provide nutrients and energy for general metabolic maintenance of the female, for the later production of eggs and, as the pentaculae feed on organic matter in the ovarian fluid, for nutrition of the brood. Sewell 1996 Biol Bull 190: 188.

NOTE  this is a general problem encountered when estimating brood mortality in other marine invertebrates

NOTE  the ring appears in the embryo about 14d after fertilisation; hence, pre-ring estimates of mortality are not possible.  The author notes, however, that the ring is present for about 93% of the long brooding period, and this minimises underestimation of mortality

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Research study 10.1
 

A research consortium from British Columbia and Mexico establish a molecular phylogeny of 16 species of west-coast holothuroidea based on mitochondrial DNA sequences.  With a few exceptions, results support the existing taxonomy, based largely on the morphology of calcareous skin ossicles.  In addition to confirming that Cucumaria pseudocurata and C. curata are separate species, the researchers note that C. lubrica may actually represent 2 species, a subtidal one and an intertidal one (see differences in ossicle morphology in specimens from the Victoria, British Columbia area) and, finally, that brooding has arisen in at least 2 separate lineages within the Family Cucumariidae.  Arndt et al. 1996 Mol Phylogenetics Evol 6 (3): 425.

NOTE  of 5 families represented in the study, F. Cucumariidae is the largest with 9 species.  Of these, 7 (Cucumaria curata, C. lubrica [possibly represented by 2 species], C. pseudocurata, C. vegae, Pseudocnus astigmatus, and P. californicus) exhibit direct development

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Research study 11
 

graph showing change in organic content of embryos of sea cucumbers Leptosynapta clarki during developmentViviparity, where eggs are fertilized internally and develop for a time within the female reproductive system, is quite rare in marine invertebrates.  In the brooding sea cucumber Leptosynapta clarki, recent findings from work at the Bamfield Marine Sciences Centre shows that the parent provides significant additional nutrients for development of the embryo during viviparous development.  The authors describe histological changes in the structure of the ovarian wall, primarily an increase in size of the connective tissue/genital hemal sinus, suggestive of transfer of nutrients.  Embryos during development end up with significantly greater carbon content than they had in the egg stage, up to a factor of 10-fold, providing clear evidence for matrotrophy (see graph). Sewell et al. 2006 Invert Reprod Dev 49: 225.

NOTE  only 14 species are known, all echinoderms

NOTE  this is termed matrotrophy, where the young first depend upon yolk and then on additional nutrients provided by the female, distinct from lecithotrophy, where the young depend solely upon the yolk for nutritional requirements during development

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