title for a learn-about section in A SNAIL'S ODYSSEY
  Reproduction & development
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  Studies on reproduction & development of flatworms is considered in this sub-section, while those on ribbon worms are presented in the following sub-section.
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Research study 1

drawing of a larva of a marine flatworm Pseudoceros canadensisdrawings of larval types of marine polyclad flatwormsMarine polyclad flatworms are hermaphroditic, but sperm exchange between individuals is usual.  Eggs hatch to a motile larva known as a Müller’s larva or Götte’s larva (see drawings on Left). The larva of Pseudoceros canadensis from San Juan Islands, Washington, is heavily ciliated, swims rapidly, and has a complex brain and nervous system.  Little is known of its biology.  Lacalli 1983 Can J Zool 61: 39.

NOTE  drawings of Müller’s and Götte’s larvae are taken from a review by Ruppert 1978 p. 65 In, Settlement and metamorphosis of marine invertebrate larvae (Chia & Rice, eds.)  Elsevier/North Holland, NY


Larva of marine flatworm Pseudoceros canadensis
showing nervous system and sensory elements

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  Ribbon worm

Sexes are separate in nemerteans but cannot be distinguished visually. Most species appararently produce a free-living pilidium larva that swims for a few days, then settles and metamorphoses. However, in a few species, eggs are laid that hatch to a crawl-away juvenile.

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Research study 1

Studies at Friday Harbor Laboratories, Washington reveal that nemerteans Paranemertes peregrina spawn mainly in spring and summer over a period of about a month (Mar-Apr).  Smaller spawnings may additionally occur in autumn.  Gonads ripen for 3-4mo before spawning, and gametes are released through temporary gonopores that appear on the dorso-lateral surfaces.  Although gelatinous egg masses are described in the literature, in San Juan Islands eggs and photograph of nemertean worm Paranemertes peregrina courtesy Dave Cowles, Walla Walla University, Washingtonsperm are released into the sea.  In the laboratory at 10oC the eggs hatch after 3d.  Metamorphosis occurs gradually over about 8wk, transforming the ciliated, teardrop-shaped, and weakly swimming larva into an elongated, muscular benthic form.  The little worm gradually spends more time on the bottom until finally it seems not able to swim anymore.  Worms in culture feed almost immediately on small polychaetes offered as food.  Interestingly, nereid worms such as Nereis vexillosa of all ages exhibit strong swimming escape responses to P. peregrina.  Based on evidence from laboratory culture and field collections, the life span of P. peregrina is about 1.6yr.  Roe 1976 Biol Bull 150: 80. Photograph courtesy Dave Cowles, Walla Walla University, Washington wallawalla.edu.

NOTE  eggs are yolky and measure 235µm in diameter, or 650µm if the fertilisation membrane and jelly coat are included

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Research study 2

Studies in Bodega Marine Laboratory, California on the crab parasite Carcinonemertes epialti show that eggs masses are laid in small batches of about 80 eggs every 2-3d over a 12-d period.  A gastrula stage is reached within 1-2d from laying, and the pilidium larval stage hatches within 6-10d, at 15o.  Despite experimentally arranged contact of the pilidia larvae at different times during the development of crabs Hemigrapsus oregonensis and Pachygrapsus crassipes from zoea to adult stages, none of the pilidia is observed to metamorphose.  Roe 1979 Biol Bull 156: 130; Roe 1984 Biol Bull 167: 426.

NOTE  male crabs harbour only juvenile Carcinonemertes.  When they become old enough to mate, the juvenile worms leave the male crabs and inhabit the females.  When the female crab releases eggs into her pleopodal region for incubation, the nemerteans move there and begin to feed on the eggs.  At this time the worm is often described as an “egg predator”, but an equally fitting descriptor is parasite

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Research study 3

scanning e-micrograph photo of a newly hatched pilidium larva of the nemertean Carcinonemertes epialtidrawing of a pilidium larva of a nemertean Carcinonemertes epialti showing morphologyA newly hatched pilidium larva of Carcinonemertes epialti is 110µm in length, heavily ciliated, and has a prominant cirrus at either end of the body (see photo on Left). The anterior cirrus has associated gland cells, while the posterior one has two prominent “knob” cells that protrude visibly from the epithelial surface.  Both cirri have associated nerve cells originating from the “brain” (see drawing above). In culture dishes in the laboratory the larvae are observed to adhere by the posterior end and, for this reason, the authors suggest that the posterior cirrus, in particular, may be involved in settlement.  Although metamorphosis is not observed in these cultures, because the larva at about 13d of age contains well-developed juvenile/adult rudiments, such as gut, proboscis rudiments, “brain”, and ocellus, metamorphosis is thought to be a gradual one.  In fact, the authors note that small juveniles, presumably recently post-metamorphic ones, differ from the larvae mainly in the absence of knob cells and cirri.  Stricker & Reed 1981 J Morphol 169: 61.

NOTE the reproductively mature adult worms are from crabs Cancer gracilis collected at Orcas Island, Washington

NOTE name given to a slender appendage, such as as the cirri or feeding appendages of a barnacle or, as in this case, a prominent cilium

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Research study 4

By placing potential crab hosts Pachygrapsus crassipes in cages both on the sea bottom and suspended in the water column in Carmel Pond in Monterey Bay, California, researchers confirm that larvae of Carcinonemertes epialti are free-swimming and settle onto their hosts from the plankton.  Settlement is highest in August and occurs on both sexes of crabs.  A higher infestation of crabs in the cages resting on the bottom than in suspended cages suggests that the larvae swim epi-benthically over the bottom seeking out their crab hosts.  Bauman 1984 The Wasmann J Biol 42: 27.

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Research study 5

If juvenile nemerteans Carcinonemertes spp. are removed from their crab hosts and maintained together for 3-4wk in laboratory culture (13oC), they later deposit egg masses that hatch into normal diploid larvae.  However, if female juveniles are kept isolated from males they also produce egg masses, but parthenogenetically and, thus, the eggs are haploid.  In laboratory culture at the Bodega Marine Laboratory, California only a few of these haploid eggs develop to a swimming pilidium larva stage, and none survives long enough in laboratory culture to know whether it would metamorphose. The author notes that this is the first report of parthenogenesis in Carcinonemertes and suggests, if it is found to occur also in field populations, that it may be a useful strategy in circumstances of low population density on a given host.  Roe 1986 Biol Bull 171: 640.

NOTE C. epialti live on several species of crabs, including Hemigrapsus oregonensis, Pachygrapsus crassipes, and Cancer gracilis.  Carcinonemertes errans lives on Dungeness crabs Cancer magister

NOTE however, even normal diploid larvae apparently do not survive under the particular culture conditions imposed

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Research study 6

Studies of laboratory spawning of the high intertidal-inhabiting Pantinonemertes californiensis reveal that females release hundreds or even thousands of eggs.  The eggs are initially held together in mucous strings or clumps, but these readily disperse in seawater.  Average egg diameter is 96µm, or 247µm if the jelly coat is included.  Eggs cultured at 22oC hatch to swimming larvae in 12-16h.  Although larvae can be maintained for several weeks in laboratory culture, it is not clear that they are planktotrophic, or how long they spend as larvae.  Roe 1993 Hydrobiologia 266: 29.

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Research study 7

drawing of pilidium larva of nemertean Cerebratulus sp.photographs of pilidium larva of nemertean worm Cerebratulus sp. showing different developmental eventsA researcher at the University of Victoria describes characteristic pilidia larvae collected from the plankton around the Bamfield Marine Sciences Centre in Barkley Sound, British Columbia.  Two of the larval types are assigned to Cerebratulus and Lineus, respectively, with the former at 1.45mm in height being among the largest pilidium larval types known.  The juvenile develops within the larva (see drawing above) and, when mature, consumes the larval body then takes up the adult mode of life (see photographs).  Metamorphosis is mentioned by the author, but not explained; it is oviously gradual and perhaps represents the moment the juvenile rudiment frees itself and consumes the larval tissues.  Lacalli 2005 Acta Zoologica 86:267.

NOTE  the author also includes descriptions of pilidia from Florida and Australia, not included here.  Previous collecting records of adults in the Barkley Sound area suggest that there are 6 species of Cerebratulus and 4 of Lineus

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Research study 8

drawing of 4-d larva of hoplonemertean Paranemertes peregrina showing adult features presentdrawing of hoplonemertean Paranemertes peregrinaDevelopment of the hoplonemertean Paranemertes peregrina is described by researchers working at Friday Harbor Laboratories, Washington.  A feature of interest appears to be that the larva of this species has a transitory epidermis that is replaced by the definitive epidermis during planktonic development.  This is the only obvious metamorphic transformation that takes place, as all major adult structures, including gut, digestive system, proboscis, and nervous system, are already present in the larva, and these simply elaborate during development (see drawing on Right). The larva appears about 4d after fertilisation and the juvenile form is realized in about 10d (at 7-10oC). The unusual planuliform larva described here for this hoplonemertean is noted by the authors to be fundamentally different from other larvae described for nemerteans (e.g., pilidium and “hidden trochophore”).  The authors provide much detail on the development of P. peregrina, including some lovely confocal micrographs of stained specimens.   Maslakova & Dohren 2009 Biol Bull 216: 273; see also Maslakova 2010 Integr Comp Biol 50: 734 for other aspects of development of the pilidium larva.

NOTE  another west-coast hoplonemertean species Antarctonemertes phyllospadicola is also studied by the researchers, as well as an east-coast species, but these are not included here

Other developmental stages are shown in these photographs: photograph of egg of hoplonemertean Paranemertes peregrina
Egg of P. peregrina
photograph of blastula of hoplonemertean Paranemertes peregrina
photograph of 4-d larva of hoplonemertean Paranemertes peregrina
4-d larva
Other developmental stages are shown in these photographs
10-d larva
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Research study 9

Early development of Pantinonemertes californiensis is described by researchers at the Oregon Institute of Marine Biology, Charleston.  The larva is non-feeding and can readily be cultured in the laboratory at temperatures of 12-16oC.  Unusual features in development are the appearance of 2 pairs of invaginations just at the time of hatching, the anterior pair of which may give rise to the adult cerebral organs.  The fate of the posterior pair of invaginations is not known.  A 5th invagination, coming later in development, forms the proboscis.  Finally, P. californiensis has a transitory larval epidermis comprised of 80 cells, that is shed at about 3-4d of development (see photograph on Right below).  The authors provide considerable details of the development of this species. Hiebert 2010 J Nat Hist 44: 2331.

Some developmental stages of P. californiensis:: photograph of fertilised egg of nemertean Pantinonemertes californiensis
Fertilised egg showing release of 1st polar body
photograph of 32-cell stage of nemertean Pantinonemertes californiensis
32-cell developmental stage in egg envelope
photograph of 3-d larval stage of nemertean Pantinonemertes californiensis
3-d larva showing a distinct proboscis rudiment, an apical tuft of cilia, and 2 eyespots
photograph of 3-d larval stage of nemertean Pantinonemertes californiensis"
A chaiin of ciliated epidermal cells cast off and left behind by larva

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