title for sandworms & relatives section of A SNAIL'S ODYSSEY
  Reproduction & development

Sandworm species generally have separate sexes and their reproductive cycles are highly varied.  Some nereid species swarm from their burrows at spawning time and do nuptial dances round-and-round before releasing their gametes.  These species produce planktonic larvae that disperse widely.  Other species stay in their burrows while they release their gametes.  These species generally produce benthic larvae whose dispersal is much less.  Still other species are eptokous, that is, their back ends become modified into large storage sacs of gametes.  When ready to release their gametes the worms of both sexes swim to the sea surface.

The Research Studies below are separated for convenience into epitokous & other free-spawning forms, scaleworms, and oviparous forms.

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Epitokous & other free-spawing forms

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Research study 1

drawing of early juvenile stage of sandworm Nereis vexillosadrawing of female sandworm Nereis vexillosa with egg massThe nereid Nereis vexillosa spawns its eggs (0.2mm diameter) in gelatinoid masses of blue-green, greenish, or brownish tints.  Up to the time of this study in the area around the Friday Harbor Laboratories, Washington the identity of the organism laying such egg masses was not known, and the primary aim of the study was to identify the species involved. During culture of such a mass the newly hatched worms are fed on minced flesh of other polychaetes and diatoms, indicating an omnivorous type of diet (see drawing on Left). In the culture dishes the worms build flimsy tubes of sand and debris cemented together with mucus.  At about 1yr of age the worms become sexually mature, transform to a heteronereid form (= epitoke) with extra-large parapodia and paddle-like setae, and swim in masses at the surface of the sea at night where they spawn.  A female is likely stimulated to spawn by the presence of sperm in the water.  The eggs are extruded in large masses from the gonopores, at which time they instantly agglutinate (see drawing on Right).  The female sinks to the sea bottom together with the mass, breaks free from it, and presumably swims away to die.  The egg mass swells to 3 or 4 times its original size through absorption of water, but remains demersal on the sea bottom.  Johnson 1943 Biol Bull 84: 106.

NOTE  the author starts the culture at the Friday Harbor Laboratories, Washington, then later moves the developing worms to the Scripps Institution of Oceanography and rears them there to a 60-setiger stage (4.5mo)

NOTE lit. “different nereid” G., referring to the modified shape of the posterior part of the body.  The transformation, or “metamorphosis” (also known as “chaetogenesis”) is described in more detail in Research Study 3 to follow

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Research study 2

photograph of pileworm Neanthes succinea courtesy Hans HillewaertAn investigation by researchers at the University of California Los Angeles of reproduction of pileworms Neanthes succinea in the Salton Sea describes production of heteronereids (epitoke)s from Nov-Mar.  The worms spawn year-round, but with seasonal maxima in spring and autumn/winter.  The heteronereids of both sexes appear at the sea surface shortly after sunset, but do not seem to have a lunar cycle.  Fertilisation occurs immediately after eggs are released through ruptures in the body wall and trochophores appear after 24h (at 20-25oC).   After 2d the larva has 3 seta-bearing segments and swim actively.  Settlement takes place after 2wk at a size of 6-9 segments. Carpelan & Linsley 1961 Ecology 42 (1): 189. Photograph courtesy Hans Hillewaert and Smithsonian Marine Station at Fort Pierce, Florida.

NOTE  the species (= Alitta succinea = Nereis succinea), now one of the most common invertebrates in the Salton Sea, was apparently introduced from the Pacific coast along with about 2 dozen other marine macroinvertebrate species by the California Department of Fish & Game in a programme of food enhancement for sports fisheries active from the 1930s-1960s.  Of these species, apparently the only surviver is N. succinea.  Detwiler et al. 2002 Hydrobiologia 473: 139.

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Research study 3

At the end of life of the nereid Nereis grubei, usually at about 1yr of age, gonads mature, and the setae at the posterior half of the body transform (= metamorphose = undergo chaetogenesis) into a larger size for more effective swimming to the sea surface for spawning (see drawing below). After the transformation is complete the individual is known as an heteronereid.  A study on N. grubei at Hopkins Marine Station, Pacific Grove, California provides information on changes in setal morphology to their paddle-like shape, including histological changes of the chaetogenetic tissues, and gives details of decapitation experiments that accelerate the process. The changes in morphology occur simultaneously with accelerated growth of oocytes, suggesting that the two phenomena are controlled by the same inhibitory hormone produced in the supra-esophageal ganglia in the head.  Decapitation of an immature female worm or decapitation of a female in early stage of oogenesis (i.e., removing the source of the hormone), will therefore initiate the transformation process.  However, decapitation of a female with oocytes greater than 140µ in diameter, and already in the process of chaetogenesis, does not affect the speed of the process.   On the basis of observations on N. grubei, the author infers that the level of the inhibitory hormone must begin to wane about 2mo before metamorphosis is completed, and before swarming takes place. Chaetogenesis in N. grubei requires about 70d at 15-16oC.  Schroeder 1967 Biol Bull 133: 426; Schroeder 1968 Pac Sci 22: 476.

drawing of developing paddle-like setae in the epitokous nereid Nereis grubeiNOTE  as noted elsewhere in the ODYSSEY, the terms “seta” (L.) and “chaeta” (G.) are considered to be synonymous.  Preference in this paper is for “seta” to be used on its own as a noun and “chaeta” to be used in combination, such as in “chaetogenesis”

NOTE  the production of such a hormone is described in earlier work on European nereid species

The new paddle-like setae develop within the parapodia
during the latter stages of egg maturation, and erupt through
the epidermis when the eggs are abou 180um in diameter

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Research study 4

A study on polychaete development in Tomales Bay, California provides information on several species, of which one is presented here as being representative of an errant life cycle. Platynereis bicanaliculata is one the most common nereids on the west coast.  In rocky areas it is found among algae and mussels, and on mudflats within beds of green algae Ulva and EnteromorphaPlatynereis is epitokous, as are many nereids.  When sexually mature it becomes a swimming heteronereid or epitoke.  The cue for transformation is a full moon in spring and the change is completed by the next full moon.  At that time the worms swarm to the surface and the males, stimulated by the presence of eggs and associated chemical stimuli in the water, spiral around the females releasing plumes of sperm.  The eggs are 160µm in diameter and contain large oil globules.  A gastrula develops after 18h at 16oC, followed by a trochophore larva (see second set of drawings below). Primordial setigers or segments with setae appear at about 2d of age. The author notes that this is the first description of the larval stages of Platynereis bicanaliculata. Blake 1975 Ophelia 14: 23.

NOTE  “setae” is Latin for “bristles”, while the term polychaeta means “many bristles” in Greek 

  Developmental stages of sandworm Platynereis bicanaliculata:
drawing of trochophore larva of polychaete Platynereis bicanaliculata showing eyespots and oil globules
40h trochophore larva of polychaete Platynereis bicanaliculata showing eyes and 4 oil globules. 160um dia
drawing of early metatrochophore larva of polychaete Platynereis bicanaliculata
2d early metatrochophore larva with 3pr eyes and 3 setigerss with setae. Gut rudiments visible. 180um length
drawing of late metatrochophore larva 3d old
3d late metatrochophore larva with 2pr eyes and 3 setigers with developed setae. 210um length
drawing of 3-setiger nectochaete stage of polychaete Platynereis bicanaliculata
6d-old, 3-setiger nectochaete stage of development with one pair of large eyes and 2 pr small eyes. Oil globules still prominant. 330um length
drawing of 5-setiger nectochaete stage of development of polychaete Platynereis bicanaliculata
1-3wk 5-setiger, large pair ofcup-shaped eyes , palps developing, pharynx with jaws, parapodia well-developed. 500um length
drawing of 6-setiger nectochaete developmental stage of polychaete Platynereis bicanaliculata
6-setiger crawling juvenile stage of Platynereis bicanaliculata, large eyes lost, 2pr small eyes, oil globules gone, jaws are large and functional. 600um length
drawing of 10-setiger juvenile of polychaete Platynereis bicanaliculata
10-setiger juvenile with prostomial antennae and 4pr tentacular cirri developing (2pr large, 2pr small). The juvenile is constructing tubes. 1.5mm length
drawing of 21-setiger developmental stage in polychaete Platynereis bicanaliculata
21-setiger juvenile with adult-looking head, all 4pr tentacular cirri adult length, prostomial palps fully developed, parapodia with adult morphology. 3.7mm length
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Research study 5

In the San Juan Islands, Washington epitokal stages of Platynereis bicanaliculata spawn synchronously in early August.  The juvenile stages are planktonic for about a week.  By 3wk of age in the laboratory at 10oC the worms are 4mm in length and building tubes.  By the following summer they are 20-23mm in length and are sexually mature.  Females bear 6000-7000 eggs.  Life span is 1yr and the adults die after spawning.  In comparison, Nereis vexillosa in the same area have a 2-yr life span and are mature in their second year at a length of 10-13cm.  The author describes epitokous spawning but also notes the presence of benthic egg masses.  Within a week in the laboratory the hatched juveniles are building tubes.  Interestingly, both of these nereid species are territorial and defend their tube-spaces vigorously.  Intraspecific interactions are “no-holds-barred”, with use of jaws and often leading to a smaller protagonist being eaten.  The aggression continues through life in both species.  Roe 1975 Pac Sci 29: 341.

NOTE for either type of reproductive strategy, it is important that the two sexes synchronise spawning to ensure maximum fertilisation of the eggs, and pheromones are known to be involved.  Studies on a species of Nereis in China have identified 32 different organic compounds in the coelomic fluid of female worms, some of which appear to function as pheromones.  Why potentially so many?  Some may be for long-distance attraction, some for stimulating and synchronising gonadal growth, some for signaling a mate’s readiness to engage in nuptial dance, and others for stimulating actual release of gametes. This would seem to represent good research opportunities on our local species. Bartels-Hardege et al. 1996 J Exp Mar Biol Ecol 201: 275. One of these pheromones has been identified in Neanthes succinea as cysteine-glutathione disulfide. It is released by females along with eggs and coelomic fluid during spawning, and induces spawning by males. Zeeck et al. 1998 Chemoecology 8: 33.

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Research study 5.1

The orbiniid worm Scoloplos acmeceps is a small burrowing species that lives in intertidal mud/sand areas associated with algal holdfasts and eelgrass roots.  Its early development is described by a researcher at the Tomales Bay Marine Laboratory, California.  It spawns its gametes into the sea and has lecithotrophic development.  After a swimming pelagic phase of about 3wk, it settles/metamorphoses (in laboratory culture at 14oC).   Selected developmental phases are illustrated below.  Blake 1980 Ophelia 19 (1): 1.

NOTE  the author includes some material on another orbiniid, Leitoscoloplos pugettensis, also common in California and Oregon, but not included here

drawing of trochophore stage in development of orbiniid polychaete Scoloplos acmeceps drawing of 6-segment metatrochophore stage in development of orbiniid polychaete Scoloplos acmeceps drawing of 7-setiger nectochaet stage in development of orbiniid polychaete Scoloplos acmeceps
Ventral view of trochophore stage, 48h of age, length 240um Dorsal view of 6-segment metatrochophore, about 4d of age, length 430um Dorsal view of 7-setiger nectochaete stage, length 500ul, swimming in the plankton
drawing of 25-setiger juvenile stage in development of orbiniid polychaete Scoloplos acmeceps
Dorsal view of 11-setiger juvenile in laboratory culture, length 1.8mm Later view of 25-setiger juvenile collected from the plankton, length 1.8mm
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Research study 6

photograph of Neanthes succinea courtesy Blaise BarretteAlthough common on the west coast of North America, the epitokous pileworm Neanthes succinea is actually indigenous to the east coast.  It was introduced1 into San Francisco Bay, California in the late 1860s, coincidental with imports of Virginia oysters.  It reproduces by epitoky, which occurs in phase with a full moon in late summer.  Spawning in synchrony with moon phases2 is common in epitokous nereids, but are there other contributing environmental factors?  This is investigated at Long Marine Laboratory, California using physical parameters of salinity, temperature, and photoperiod as treatments on worms collected from San Francisco Bay.  Results show that neither temperature (ambient air vs. ambient seawater) nor photoperiod (in-phase and 6mo out-of-phase) alone significantly affects the frequency of epitokal metamorphosis (treatments are up to 12-mo in duration).  Worms maintained in salinities3 of 20‰, however, metamorphose significantly more often and sooner than ones in 5‰ (see histogram). A significant interaction between salinity and temperature is also detected.  Fong 1991 J Exp Mar Biol Ecol 149: 177.  Photograph courtesy Blaise Barrette.

NOTE1  for a review of the role of pheromones in reproduction in N. succinea (Europe) see Hardege et al. 2004 Peptides 25: 1517

NOTE2  observations at Woods Hole, Massachusetts reveal epitokous swarming by N. succinea after full moons and before new moons.  Other observations on the west coast indicate swarming at onset of new moon. Blake 1975 Ophelia 14: 23

NOTE3 in this area seawater in the muddy areas of the Bay commonly range seasonally from 8-21oC and 0-33‰

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Research study 7

histogram showing relationship of spawning in the sandworm Platynereis bicanaliculata with the phases of the moonOther research by the same author at the Long Marine Laboratory, Santa Cruz, California on the epitokal-spawing Platynereis bicanaliculata suggests that spawning is synchronized to the phase of the moon.  A variety of experiments involving holding worms in the laboratory under different combinations of daylength and cycles of artificial moonlight show that swarming is entrained by moonlight, specifically, its decline in intensity from full moon to last-quarter moon.  A sampling of data for worms in the laboratory shows an entrainment with natural moon conditions in the field during November/December, with most laboratory spawnings occurring after the time of the ambient full moon.  The author notes that these data provide the first experimental evidence of lunar-synchronised reproductive cycle in a west-coast marine invertebrate.  Fong 1993 Bull Mar Sci 52 (3): 911.

NOTE  one guesses that the emphasis in this claim is on the word experimental, as the phenomenon is well known in various marine taxa including sandworms in many parts of the world, and in various research studies above, including the author's own (see RS 4 & 6 above)

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Research study 1

photograph of scaleworm Halosydna brevisetosa courtesy Lovell & Libby Langstroth, Pacific Grove, CaliforniaHalosydna brevisetosa is one of the most common free-living scaleworms on the west coast. Spawning in Tomales Bay, California occurs in spring/summer and fertilisation is external.  The larvae spend days or weeks in the plankton before settling as a juvenile (see first row of drawings below).  Blake 1975 Ophelia 14: 23. Photograph courtesy Lovell & Libby Langstroth, Pacific Grove, California

NOTE  the author obtained larvae from plankton tows, from egg masses hatched in the lab, and from adults collected and spawned in the lab



  Three developmental stages of the scaleworm Halosydna brevisetosa:
drawing of early metatrochophore larva of scaleworm Halosydna brevisetosa
Early metatrochophore larva of Halosydna brevisetosa, lateral view. 400um width. The larva shows primordia of elytra = scales
drawing of late metatrochophore larva of polychaete Halosydna brevisetosa
Late metatrochophore stage. 550 um length. 8-setiger =segment stage with scales, half illustrated
drawing of juvenile scaleworm Halosydna brevisetosa showing 6 pairs of elytra (scales)
Benthic juvenile stage of scaleworm Halosydna brevisetosa showing a medial antenna, a pair of palps, a pair of lateral antennae, a pair of tentacular cirri (not labeled), and 2 pairs of eyes. Six pairs of elytra are present, only half of which are illustrated here. 900um length
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Research study 2

histrogram showing fertilisation potentials among 3 species of Arctonoe scalewormsphotograph of scaleworm Arctonoe fragilis courtesy Dave Cowles, Walla Walla University, Washingtonphotograph of a scaleworm Arctonoe pulchra courtesy Dave Cowles, Walla Walla University, Washingtonphotograph of scaleworm Arctonoe fragilis on the arm of a sea star Orthasterias koehleriWhat explains gamete incompatibility, one of the reasons for reproductive isolation, in free-spawning marine invertebrate species, such as polychaetes? Three hypotheses have been proposed: independent divergence at gamete-recognition loci, selection against hybrids, and sexual selection involving polymorphic gamete-recognition loci.  Which, or whether any, of these may have operated during speciation in the genus Arctonoe is the subject of a study at Friday Harbor Laboratories, Washington.  Suprisingly, gametes of the 3 species A. pulchra, A. vittata, and A. fragilis are compatible in all crosses over a broad range of gamete concentrations and contact times (see blue bars of histograms).

Note that for 2 of the species, A. fragilis and A. pulchra, eggs are fertilised slightly but significantly more by heterospecific sperm than by conspecific sperm.  Although some fertile hybrids are produced, the author’s data on allozyme and mitochondrial DNA sequences indicate that the 3 species do not regularly exchange genes.  In fact, gametes of the 3 species are compatible despite estimated divergence times of 1-3 MYBP.  In other marine invertebrates, for example, tropical sea urchins, such divergence times are associated with complete gamete incompatibility.  The results support the first 2 hypotheses. Moreover, because speciation has occurred in the genus Arctonoe without the evolution of gamete incompatibility, the third hypothesis concerning gamete incompatibility and speciation must be rejected. The author suggests that spatial segregation of the worms on their respective host species, with consequent gamete dilution effects, may sufficiently restrict fertilisation opportunities and, thus, gene flow among these Arctonoe species.  Pernet 1999 Evolution 53: 435. Photographs of A. vittata and A. pulchra courtesy Dave Cowles, Walla Walla University, Washington. wallawalla.edu.

NOTE  the author remarks that there is no evidence that these scaleworm species mate in pairs on their respective host species.  For Arctonoe pulchra and A. vittata, at least, only one individual is usually found per host

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Research study 3

photograph of 45h trochophore larva of a scaleworm Arctonoe sp.drawings showing metamorphic and juveniles stages of scaleworms Arctonoe spp. in culture in the laboratoryA later study by the same author at Friday Harbor Laboratories, Washington shows that the 3 species of sympatric polynoid polychaetes Arctonoe have similar patterns of reproduction and development.  Eggs of 80µm diameter are spawned freely during Mar-Aug and develop into feeding planktonic larvae.  The photo shows a 45h trochophore larva of one of the species. The gut is complete at this time but feeding does not commence until about 50h post-fertilisation.  In the laboratory, in the absence of their hosts, the larvae metamorphose within 6-12wk (at 9-11oC).  Within a few days after metamorphosis the juveniles begin to feed and sexual maturity is reached 4-6mo later.  The long planktonic larval period of these polynoids potentially leads to high dispersal. The author suggests that the ability to raise naive scaleworms in laboratory culture may permit the role of genetically based host preferences in determining host-use patterns to be assessed.  Host choice by juveniles has not been studied previously in these polynoids because prior to this study it has not been possible to obtain naive juveniles for experimentation.  Pernet 2000 Invert Biol 119: 45.

NOTE  the scaleworms are collected from their hosts as follows: Arctonoe vittata from keyhole limpets Diodora aspera; A. fragilis from sea stars Evasterias troschelii; and A. pulchra from sea cucumbers Parastichopus californicus

NOTE  the larvae are fed on a variety of phytoplankter species and invertebrate larvae such as gastropod veligers.  After metamorphosis the juveniles are able to eat newly hatched Artemia salina nauplii, but only if the prey is rendered immotile by the researcher.  As they grow larger the juveniles are able to capture the swimming nauplii themselves

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Viviparous forms

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Research study 1

Embryonic and larval development of the viviparous hermaphroditic nereid Neanthes limnicola is described by a researcher at the University of California, Berkeley for mature specimens collected in the Salinas River estuary near Monterey, California.  The eggs mature in the coelom and are apparently fertilised there by sperm from the same individual.  Birth occurs at about 4mm length (28d of age at 17-20oC) via ruptures in the body wall.  At this time the juveniles are able to construct their own tubes.  Smith 1950 J Morphol 87 (3): 417.

NOTE the author uses an older name Neanthes lighti in the publication

NOTE Neanthes limnicola can tolerate salinities ranging from near zero to 115% seawater

Development proceeds as shown in the drawings:

drawing of egg of sandworm Nereis limnicola gastrula stage of nereid Nereis limnicola early trochophore stage of nereid Nereis limnicola 2-setiger stage of development of nereid Nereis limnicola
Eggs are held in the coelom Gastrula stage is motile Trochophore with yolky endodermal cells Free-swimming larval stage in coelom of parent
3-setiger larva of nereid Nereis limnicola 6-setiger larval stage of nereid Nereis limnicola juveniles emerging from adult Nereis limnicola via body-wall ruptures
Gut is well defined and eyespots are visible Pre-birth larva has 2pr tentacular cirri and anterior palps Juveniles emerge at 4mm length via body-wall ruptures
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Research study 2

graph showing development of Neanthes limnicola over a 2yr study period histogram showing fecundity of Neanthes limnicola in different salinitiesReproductive maturation in nereid polychaetes culminates in spawning (or birthing), often synchronised with phase of the moon.  But what regulates the timing of development leading up to that event?  Research at the Institute of Marine Sciences, Santa Cruz, California on Neanthes limnicola suggests that the life cycle is dependent upon increasing day lengths.  Neanthes is an hermaphroditic ovoviviparous species that has been reported to be self-fertilising. In fav992oured brackish-creek habitats in Monterey Bay it histograms showing effect of daylengths on fecundity and life span of worms Neanthes limnicolagives birth to young in late winter/spring (late Feb-May).  Eggs develop in the coelomic spaces of the adult (see graph on Left), and the juveniles later emerge through fissures in the body wall of the degenerating parent. 

Laboratory experiments show that hiighest fecundities are realised in brackish salinities (15-20‰), while worms maintained in full-strength seawater (33‰) show abnormal development and produce comparatively few young (see histogram upper Right).  In other experiments, juveniles are exposed in the laboratory to fixed daylengths of either 8h light:16h dark (“short”), 16h light:8h dark (“long”), or 12h light:12h dark (“neutral”) and maintained through their complete life cycle.  Some worms are switched between different fixed daylengths or switched from fixed to increasing or decreasing daylengths.  Results show that worms on a “neutral” pattern exhibit highest fecundities and shortest life spans ("days in culture" in histogram on lower Right).  Note in the histogram that worms on “long” daylength have lowest fecundities, but longest life spans.  All worms switched from a fixed pattern to a pattern of decreasing daylength become asynchronous with respect to time of birthing in the treatment group.  In contrast, worms switched from any fixed pattern to an increasing-daylength pattern exhibit synchronised times of birthing, and significantly higher fecundities and shorter life spans (mean of 230d vs 340d for ones on fixed patterns).  This last resembles the natural pattern most closely, where birthing occurs in springtime when daylight periods are lengthening.  The authors conclude that N. limnicola has an endogenous, circ-annual rhythm responsive to increasing daylengths.  Fong & Pearse 1992 Biol Bull 182: 289; Fong & Pearse 1992 Mar Biol 112: 81.

NOTE  later allozyme electrophoretic analyses of N. limnicola and 2 other closely related neanthids suggest, in fact, that some cross-fertilisation must occur in the field in this species.  Fong & Garthwaite 1994 Mar Biol 118: 463

NOTE  worms used in the experiments are ones reared from eggs in the laboratory

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