Reproduction
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  Hatching & larval life
  Hatching & larval life are dealt with in this section, while topics of MATE SELECTION & COPULATION, EGG-LAYING, EMBRYONIC DEVELOPMENT, SETTLEMENT & METAMORPHOSIS, SETTLEMENT CUES, and ONTOGENETIC DEVELOPMENT OF BEHAVIOUR are considered in other sections. After some general introductory material in Research Studies 1-5, the following genera are considered specifically in their own subsections: Alderia, Berthella, Cadlina, Coryphella, Dendrodoris, Dendronotus, Doridella, Doris, Haminoea, Hermissenda, Onchidoris, and Phyllaplysia.
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Research study 1
 

histogram showing number of west-coast opisthobranch species that have planktotrophic, lecithotrophic, or direct types of development along with associated egg diameterA common pattern in marine invertebrate development is that a planktotrophic pelagic existence is associated with small-sized eggs, and this same pattern is exhibited for 126 species of west-coast opisthobranchs (indigenous species for which data are known; see graph on Left).  91% of the species are planktotrophic with a mean egg size of 86µm, 5% are lecithotrophic (and pelagic) with a mean graph showing shell size at hatching for opisthobranch eggs of different diametersegg size of 134µm, and 5% have direct development with a mean egg size of 161µm. Not surprisingly, larger eggs produce larger shell sizes in the veligers at hatching for most of the species (see graph on Right). 


Five of 12 species with non-feeding (lecithotrophic) larvae or direct development occur largely or entirely south of Point Conception, California where the seawater is warmer, has less nutrients, and thus is less productive than further north.  Another 4 of the 12 occur mainly in estuaries that are small and sparsely distributed along the coast, and one occurs in the Arctic.  The remaining 2 have distributions that are fairly extensive along the west coast. The author notes that direct development in the 126 species is correlated with small adult size.  Goddard 2004 Can J Zool 82: 1954.

NOTE  these eggs hatch to a crawl-away juvenile

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Research study 2
 

The gelatinous mass around the eggs of opisthobranchs acts to protect the eggs, but at the same time it does represent an “unstirred” barrier between the egg capsules and the external environment.  Respiratory gases and other diffusible substances (e.g., ammonium) must diffuse sometimes several millimeters across the gelatinous material. Like all other opisthobranchs, late in development the embryos of Haminoea sp. begin to spin rapidly (50-100rpm) within their capsules.  The authors calculate that spinning enhances gas diffusion by about 8% over what there would be if they were non-spinning.  Hunter & Vogel 1986 J Exp Mar Biol Ecol 96: 303.

NOTE  the authors do not describe the species used. A photo of H. virescens can be seen below in Research Study 1 of subsection "Haminoea"

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Research study 3
 

photograph of dorid nudibranch Rostanga pulchradrawing of veliger larva showing location of balance receptors, the statocystsNudibranch veligers (and all other veligers) swim in a constant orientation, with velum uppermost and leading.  Part of this may owe to the location of the velum and to the body’s centre of gravity, but the veliger larva does have well-developed paired statocysts located in the base of the foot.  Studies at Friday Harbor Laboratories, Washington on the nudibranch Rostanga pulchra show that the statocysts, each spherical and about 20µm in diameter, develop from ectodermal invaginations, and are situated between the cerebral and pedal ganglia. 

representation of statocyst of a nudibranch Rostanga pulchra showing morphologyThe statocyst is a fluid-filled capsule containing one large spherical calcareous statolith (5µm in diameter) and several smaller concretions (each about 1µm in diameter).  Interestingly, there are only 10 ciliated sensory hair cells and 11 accessory cells surrounding the statolith.  The cilia (hairs) project inwards and communicate with nerves via the hair cells.  Four hair cells at the bottom of the capsule may be the “operational” ones during swimming, as the cilia on these are the ones the statolith would mostly rest on during swimming.  In other veligers, the statolith rotates erratically within the capsule, but this is not confirmed for Rostanga.  The authors note that the statocysts function for gravity perception, with the possibility that they may also perceive angular acceleration (not yet demonstrated in any mollusc but cephalopods).  Chia et al. 1981 Cell Tissue Res 214: 67; drawing from Bonar 1978 p.177 In Settlement and metamorphosis of marine invertebrate larvae (Chia & Rice, eds.) Elsevier, N.Y.

NOTE  nudibranchs and perhaps opisthobranchs, in general, seem to be unique in having so few sensory hair cells.  Other marine gastropods possess hundreds or even thousands of sensory cells

 
Research study 4
 

drawing of veliger larva of a nudibranchphotograph of mouth area of veliger larva of Rostanga pulchra to show the location of the cephalic sensory organAnother sensory device in a competent veliger larva of Rostanga pulchra, termed the cephalic sensory organ, is located between the rhinophores just above the mouth (see drawing on Left and photo on Right). The organ is comprised of 3 types of sensory cells, their cell bodies extending as axons into the cerebral commissure. 

A tuft of cilia extends from the surfaces of the sensory cells.  The entire complex consists of about 14 cells (see drawing below Left).  Morphological evidence, but not neurophysiological at this stage of investigation, suggests chemoreceptive and/or mechanoreceptive function. The authors provide a list of possible functions for the cephalic sensory organ: orientating during settlement, initiating drawing of cephalic sensory organ of the nudibranch Rostanga pulchrametamorposis, monitoring orientation during swimming, controlling water quality in the mantle cavity, coordinating velar and cephalopedal retractions and protractions, discriminating edible from inedible food items. None of these possible functions has been tested.  Chia & Koss 1984 Zoomorph 104: 131.

NOTE  the nerve connecting the paired cerebral ganglia

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Research study 5
 

drawing of the eye of a nudibranch Rostanga pulchra in cross-section
Eyes in the veliger larva are located immediately behind the velar lobes (see drawing above Research Study 2).  In Rostanga pulchra they develop approximately 20d after hatching (at summer seawater temperatures in Friday Harbor, Washington).  Each is a miniature version of the adult eye, 15µm in its longest dimension, and consists of a pigmented cup with lens (5µm), a single corneal cell, and 7 sensory cells (shown in blue in the drawing).  Eight pigment cells comprise the pigment cup.  The sensory cells communicate with the optic ganglion via a nerve composed of 7 neurones.  The optic ganglion, in turn, joins the lateral region of the cerebral ganglion.  The authors note the few sensory cells and simple cup-shape of the eyes and express doubt about an image-forming capability. Rather, they suggest, the eyes may be restricted to detecting different light intensities and the movement of light stimuli as suggested for adult eyes of other nudibranchs.  Such capabilities in the larva may be useful in regulating vertical position in the water column and perhaps in migration to the substratum during settlement.  Chia & Koss 1983 Zoomorph 102: 1.

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  Accounts now proceed alphabetically for selected genera:
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Alderia

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Research study 1
 

photograph of the eggs of the sacoglossan Alderia modesta courtesy Patrick Krug, CSU Los Angeles, California An example of poecilogony has been identified in a population of the sacoglossan Alderia modesta in Mission Bay near San Diego, California.  In this instance, one-half of the adults release egg masses each photograph of a sacoglossan Alderia modesta courtesy A. Chernyshev, Russiacontaining about 300 eggs of mean diameter 68µm.  After 3d these hatch as planktotrophic veligers with maximum shell dimension of 116µm (top 2 photos on Right).

photographs of the eggs and veliger larva of a sacoglossan Alderia modesta courtesy Patrick Krug, CSU Los Angeles, California. The remaining adults spawn masses each containing about 30 eggs with mean diameter 105µm.  These hatch after 5-6d to lecithotrophic veligers of 186µm size (bottom 2 photos on Right). Note that the photographs are presented at the same scale to show the remarkable difference in sizes of both eggs and resulting larvae.

Interestingly, when starved over several days, adults that previously produced only lecithotrophic larvae switch after a few days to producing planktotrophic larvae or mixed clutches of planktotrophic and lecithotrophic larvae. The author suggests that poecilogony in Alderia is an adaptive mechanism to increase larval dispersion following starvation. Virgin adults are used in laboratory breeding crosses to ensure known egg and sperm history. The author notes that A. histograms showing the relationship between number of egg masses deposited daily vs. days of starvation in the sacoglossan Alderia modestamodesta is the only species known at the time to have both planktotrophic and pelagic lecithotrophic development within a single population.  It is advantageous as a bet-hedging dispersal strategy, in that some offspring from each clutch are retained in the parental habitat, while the remainder can potentially locate to a new algal patch. Krug 1998 Mar Biol 132: 483; see also Krug 2001 Mar Ecol Progr Ser 213: 177; for a good review of poecilogony in Alderia see Krug 2007 Amer Malac Bull 23: 99;  for a good general review of poecilogony see Gibson & Gibson 2004 Evolution 58: 2704. Photo of Alderia courtesy A. Chernyshev, Russia and seaslugforum; other photos courtesy Patrick Krug, California State University, Los Angeles.

NOTE  the presence of 2 or more developmental modes within a species is poecilogony (lit. “varied offspring” G.).  In opisthobranchs poecilogony occurs in only a few species and seems to be related to geography, feeding conditions, and other factors (for another example, see Research Study 1 in the subsection "Haminoea" below

NOTE  a cosmopolitan species found in Europe and both coasts of North America.  It is a specialist sucking-type herbivore, feeding exclusively on algae Vaucheria spp. Recently, however, the author has determined that the subject of this and other studies by his research group is actually a new species Alderia willowi.  It is this new species A. willowi, indigenous to California south of Bodega Harbor, that is poecilogonous, while Alderia modesta produces strictly planktotrophic larvae.  Krug 2007 Amer Malac Bull 23: 99. For more information on mate selection and copulation in Alderia spp. see the section ALDERIA

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Research study 2
 

histogram comparing metamorphic inducer algae on larvae of the ascoglossan Alderia modestaThe developmental dimorphism described above for the ascoglossan Alderia modestahas important consequences for dispersal.  One of the larval types is planktotrophic and long-lived. It becomes competent, that is, physiologically capable of metamorphosing, about 32d after hatching.  The other form is lecithotrophic and and short-lived. It is competent to metamorphose immediately upon hatching and generally does so within about 3d.  Observation of swimming behaviour of both forms by researchers at California State University, Los Angeles shows that newly hatched planktotrophic larvae swim in meandering paths with equal extent of upward and downward movements.  Later, as settlement time approaches, their swimming becomes straighter, faster, and increasingly directed towards the sea bottom.  In comparison, although swimming behaviour is qualitatively similar in lecithotrophic larvae, their swimming speed is 2-fold greater than in the planktotrophic type, and the bottom is reached much quicker.  Interestingly, while both larval types actually sink faster than they are able to swim downwards, the authors think that swimming may allow a larva to keep its velum extended, the better to sense chemical settlement cues from their host alga, Vaucheria spp.  That Vaucheria is the preferred substratum for both larval types is confirmed in cafeteria-style settlement tests.  The histogram shows preferential settlement to V. longicaulis over 4 other green-algal species, with no significant difference between planktotrophic and lecithotrophic larval forms in their settling fidelity to this alga.  None of the other algal species triggers significantly more metamorphosis in the larvae than the FSW (filtered seawater) controls.  Krug & Zimmer 2004 Biol Bull 207: 233.

NOTE information provided here is for a new species A. willowi (see Research Study 3 below)

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Research study 3
 

photographs of ascoglossans Alderia modesta and A. willowi along with their spawn courtesy Patrick Krug, CSU Los Angeles, Californiain more recent papers the author and his colleagues have determined through molecular evidence that the subject of this and other earlier studies is actually a new species Alderia willowi.  It is this new species A. willowi, indigenous to California south of Bodega Harbor, that is poecilogonous, while Alderia modesta produces strictly planktotrophic larvae as it does everywhere else in its northern Pacific and Atlantic distributions.  Krug 2007 Amer Malac Bull 23: 99; Krug et al. 2007 J Moll Stud 73: 29. Photographs courtesy Patrick Krug, CSU Los Angeles, California KrugLab.

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Research study 4
 

map showing types of development, whether planktotrophic or lecithotrophic, in the ascoglossan Alderia willowi along the west coastInterestingly, poecilogony in the cosmopolitan ascoglossan Alderia modesta only occurs in southern California.  In all other areas of its distribution, including the Atlantic basin and Russia, and the west coast from Monterey, California north to Alaska, it exhibits planktotrophic development, and this prompts the question as to its evolutionary origin.  This is addressed in a study at Calfornia State University, Los Angeles using collections of A. modesta from 17 sites spanning the eastern and western Pacific and North Atlantic oceans and analysed for mitochondrial DNA haplotypes.  Results for west-coast populations show that poecilogonous (producing both lecithotrophic and planktotrophic larvae) and planktotrophic Alderia overlap at Tomales Bay, California, but show no evidence of hybridisation in laboratory breeding experiments. Note that production of lecithotrophic larvae by Alderia in southern locations in California is a summer phenomenon; reproduction in winter also includes the release of planktotrophic larvae.  Poecilogony seems therefore to be seasonally influenced, with lecithotrophy being expressed primarily in the summer, possibly as a “bet-hedging” strategy.  Data suggest that separation in California may have occurred about 4.1mya through geographical isolation.  Results further show that Atlantic and Pacific populations may have diverged about 1.7mya through interruption of trans-Arctic gene flow by Pleistocene glaciation.  The authors discuss developmental features that may have favoured seasonal lecithotrophy, that is, poecilogony in southern estuaries in California. Ellingson & Krug 2006 Evolution 60: 2293.

NOTE  the poecilogonous population in southern California is referred to by the authors as Alderia sp. to separate it from the recognised cosmopolitan species Alderia modesta.   However, recently the author has determined that the subject of this and other studies by his research group is actually a new species Alderia willowi.  It is this new species A. willowi, indigenous to California south of Bodega Harbor,  that is poecilogonous, that is, producing both lecithotrophic and planktotrophic larvae, while Alderia modesta produces strictly planktotrophic larvae.  Krug 2007 Amer Malac Bull 23: 99.

NOTE  live mass of Alderia modesta north of San Francisco (to Coos Bay, Oregon) is 3-4fold greater than that of Alderia sp. in southern California

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Research study 5
 

In a later publication the same research group at California State University, Los Angeles reviews poecilogony in Alderia willowi and presents field and laboratory evidence showing that its dimorphic larval development is, indeed, a seasonal expression.  Note in the histogram that over a 3yr period, field histogram showing proportions of broods of opisthobranchs Alderia willowi that are lecithotrophic and planktotrophic during different times of the yearindividuals in Mission Bay, California exclusively produce lecithotrophic larvae (direct development) during summer (May-Sept), whereas a variable proportion of individuals produce planktotrophic larvae during winter/spring (Nov-Apr).  In laboratory experiments, individuals reared under summer conditions of high temperature and high salinity (24oC, 32‰) produce the highest proportion of lecithotrophic offspring (about 60%), while ones reared under winter conditions of low temperature and low salinity (16oC, 16‰) produce the lowest proportion (25%).  These results seem contrary to a common pattern in opisthobranchs of production of planktotrophic larval forms in spring and summer when foods are available.  However, the authors suggest that in the high-intertidal coastal wetlands of southern California inhabited by these Alderia, seasonal drying of habitat in summer may have precluded selection for a dispersive stage.  In A. willowi, then, seasonal cues experienced by the adult stage influence the phenotype of the offspring, and thus their dispersal potential.  Krug et al. 2012 Integr Comp Biol 52 (1): 161.

NOTE  data are actually collected for 2 full years and 2 half years; for visual clarity only the 2 full years are shown here

NOTE  the authors comment that “no other marine animal is known to toggle between larval morphs”, but in saying this they may not be familiar with the poecilogonous development of spionid tubeworms Boccardia proboscidea, where latitude plays a strong role in determining mode of larval development:  LEARNABOUT TUBEWORMS: REPRODUCTION: SPECIES THAT ARE POECILOGONOUS: BOCCARDIA

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Aplysia

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Research study 1
 

For a number of years sea hares Aplysia californica have been reared from egg through metamorphosis at the Rosenstiel School of Marine and Atmospheric Sciences, University of Miami (the National Resource for Aplysia) to supply research animals for use by scientists in the fields of neuroscience, behaviour, and learning.  During those years the  researchers involved have learned much about optimal conditions needed for culture of large numbers of high quality larval Aplysia. Results of several experiments show that highest growth and survival are achieved on a mixed algal diet of 1:1 Isochrysis sp. and Chaetoceros muelleri at a concentration of 250 x 103 cells . ml-1 and at a density of 0.5-1.0 veligers .  ml-1.  Under these conditions and at 22oC the larvae are metamorphically competent by 3wk after hatching (see graphs below). The authors include several practical suggestions for culture protocol, most notably the use of roller bottles as culture containers.  Use of these same culture techniques has allowed the authors to culture several other planktotrophic larval types with similar levels of success. Capo et al. 2008 Comp Biochem Physiol Part C 149: 215.

NOTE  broodstock animals are obtained from Santa Barbara Marine Biologicals

 
graph showing effects of food types and concentrations on growth of sea-hare Aplysia veligers graph showing effects of reearing density on growth of sea-hare Aplysia veligers
   
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Research study 2
 

drawing of statocyst of a sea hare Aplysia californicagraph showing number of statoconia in a statocyst with body size in sea hares Aplysia californicaGravity perception is important for marine invertebrates, both for larvae and for adults.  Researchers at the University of Texas, San Antonio follow development of the gravity receptors or statocysts from larva through adult stages in sea hares Aplysia californica (see drawing on Left).  Larval statocysts are paired sacs located on either side of the foot and each contains just a single statolith. They are the earliest neural structure to appear in development (2d post-fertilisation at the 300-cell stage), perhaps attesting to their importance.  At hatching each statocyst consists of 13 sensory cells and a single statolith. Stimulation of the sensory cells occurs when the statolith falls under the influence of gravity.  After metamorphosis the statocysts relocate to the circumesophageal ring of ganglia just posterior to the buccal mass. After about 75d post-hatching, at a statocyst size of 45um diameter and a body length of about 10mm, the number of statoliths, now known as statoconia, increase and they continue to do so through an individual’s life (see graph).  Note that maximum number in A. californica is about 900 at a  statocyst diameter of about 250um.  In the larva the statolith has an amorphous structure and is produced in the lumen of the sac, while in the adult the multiple statoconia consist of calcified layers around internal kernels of protein and are produced by supporting cells located between the receptor cells in the sac.  Wiederhold et al. 1990 Hearing Res 49: 63

NOTE the authors fit a line to their data with a 4th-order polynomial, which may be statistically correct but is not biologically meaningful

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Berthella

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Research study 1
 

photograph of notaspid Berthella californica courtesy Dave Cowles, Walla Walla University, Washingtonnewly hatched larva of notaspid Berthella californica courtesy Louise Page, University of Victoria, British Columbia Early development of the notaspid Berthella californica is studied at the University of Victoria from eggs collected at the southern end of Vancouver Island, British Columbia. Eggs hatch to a swimming veliger larva after 19d at 11-12oC and development is similar to that of other opisthobranchs (see photograph above Right).  However, an unusual occurrence at a later larval stage, around 80d of age on a diet of 1:1 mixture of Pavlova lutheri and Isochrysis sp., is that the larval shell becomes bilaterally symmetrical, an event apparently not seen in manyphotograph of larval shell of the notaspid Berthella californica showing asymmetrical growth courtesy Louise Page, University of Victoria, British Columbia other opisthobranchs (see photograph below Right).

Metamorphosis occurs in larval culture after about 80d, but only if a small piece of bivalve shell bearing encrusting invertebrates is placed in the culture vessel for the larvae to crawl on.  In the words of the authors the most spectacular metamorphic event is the rapid expansion of mantle-fold epithelium over the shell surface, resulting in  the shell becoming internalised.  This is a distinctive feature of development of notaspids, but apparently has similarities with some nudibranchs that lead to significant phylogenetic considerations.   Rhinophores appear about 5d after metamorphosis. The juveniles do not survive in culture beyond about 2wk.  The authors discuss their results in the context of the overall phylogeny of opisthobranch molluscs.  LaForge & Page 2007 Invert Biol 126: 318.

NOTE  the authors are interested in comparing features of development in notaspids with those in nudibranchs for phylogenetic purposes

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Cadlina

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Research study 1
 

photograph of Cadlina luteomarginata courtesy Paul Young
Hatching of Cadlina luteomarginata (and probably all nudibranch species) in Howe Sound, British Columbia is temperature dependent.  Thus, time to hatching at 5oC is 86d, at 10oC is 35d, and at 15oC is 25d.  The embryos die at 20oCDehnel & Kong 1979 Can J Zool 57: 1835.

 

 


Cadlina luteomarginata
1X. Photo courtesy
Paul Young and seaslugforum

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Dendrodoris

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Research study 1
 

photograph of dorid nudibranch Dendrodoris behrensi courtesy Jeff Goddard, UC Santa Barbara, CaliforniaPlanktonic larval development is almost universal in nudibranchs and only 4 examples of direct development have been described, all of them occurring in the F. Dendrodorididae.  One is Dendrodoris behrensi, which in the egg capsule passes through a vestigial veliger larval stage lacking a shell and other larval features. After 38d of embryonic development (16-19oC), Dendrodoris hatches to a juvenile of about 500µm in length. Four days after this, at a size of 570µm, the juveniles develop rhinophores.  Adults range from 12-22mm in size.  Goddard 2005 Proc Cal Acad Sci 56: 201. Photographs courtesy Jeff Goddard, UC Santa Barbara, California.

NOTE specimens for study are collected in Baja California

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Dendronotus

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Research study 1
 


drawing os shells of pre- and post-hatching veliger larvae of the nudibranch Dendronotus frondosusStudies on early development of Dendrontus frondosus collected in Tomales Bay, California show the following events (14oC): gastrula (30h from laying), trochophore (48h), early veliger (62h: shell is cap-shaped), pre-hatching veliger shell (6d: shell is cup-shaped) and, after hatching, the shell is dome-shaped (see illustration above Right).

photograph of eolid nudibranch Dendronotus frondosus courtesy Peter  van Bragt, Netherlands In the free-swimming veliger the mantle fold appears to be separate from the shell. Later, the shell is discarded, although based on what we now know of larval development in opisthobranchs this is likely an artifact from lab culture.  The author did not witness metamorphosis.  Williams 1971 Veliger 14: 166.


Dendrontus frondosus has a cosmopolitan distribution
and is found throughout Europe. Photo courtesy Peter
van Bragt, Netherlands and seaslugforum



 

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Doridella

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Research study 1
 

graph of shell growth of larvae of Corambe steinbergae over several weeksAuthors of a detailed study on early development of Corambe (Doridella) steinbergae at Friday Harbor Laboratories, Washington divide the 4-5wk planktonic larval period into 4 arbitrary stages. Stage I photograph of nudibranch Corambe steinbergae feeding on the bryozoan Membranipora sp. courtesy Clinton Bauder, Montereycommences with hatching (7-8d from egg-laying), Stage II with the appearance of eyespots and beginning of heartbeat (18-20d), Stage III with appearance of radula sac and adult-kidney rudiments (28-30d), and Stage IV with appearance of radular cusps and other adult features (33-34d).  Stage IV veligers are competent to metamorphose.  During this stage the larval shell grows from 142 to 168µm in greatest diameter.   Bickell & Chia 1979 Mar Biol 52: 291. Photo courtesy Clinton Bauder, Monterey and seaslugforum.

NOTE  in laboratory culture at 12-15oC

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Research study 2
 

drawing of veliger larva of nudibranch Corambe (Doridella) steinbergae illustrating digestive systemdrawing of post-metamorphic stage of nudibranch Corambe (Doridella) steinbergae showing digestive systemDuring larval life Corambe (Doridella) steinbergae feeds on unicellular algae and its stomach and associated digestive organs are specialised for this task.  At this time the larval stomach consists of a ciliated vestibule (the openings of the esophagus and digestive gland open into this), gastric shield, style sac, and intestinal groove (drawing on Left).  Algal cells captured by the velar cilia are conveyed to the stomach by ciliary beating and accumulate as a food bolus.  The bolus is vigorously rotated against the gastric shield by cilia of the style-sac cells, which breaks apart the algal cells.
All of these structures, save for the stomach vestibule, are lost during metamorphosis. The vestibule becomes the ventral stomach in the juvenile, and the proximal end of the intestine becomes enlarged and muscularised to form the dorsal part of the stomach (see drawing on Right).  During metamorphosis this new stomach is shifted to its dorsal postition by contraction of special muscles.  Also present in the competent larva is a radular rudiment containing 6-8 cusps. This is retained during metamorphosis and develops into the radula of the juvenile.  Within 3d after the onset of metamorphosis and at a size of only 0.2mm in length, the juvenile begins to feed on its adult food, zooids of the bryozoan Membranipora.  The study provides the first description of  metamorphic change in gut structure from planktivorous veliger larva to carnivorous juvenile in a dorid-nudibranch species.  Bickell et al. 1981 Mar Biol 62: 1.

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Doris

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Research study 1
  photograph of copulating dorid nudibranchs Doris montereyensis with egg massA schedule of development at 17oC of Doris montereyensis collected from Cape Arago/Yaquina Head, Oregon is as follows: early trochophore (6d from laying), early veliger (14d), late veliger (20d), and hatching (20-24d). The authors describe settlement as occurring 1-2h after hatching, but no metamorphosis is reported, nor is it clear that a crawling juvenile stage is reached.  These observations likely represent a laboratory artifact or result from poor health of the hatchlings, as a period of planktotrophic life followed by metamorphosis would be anticipated for Doris based on information from studies on other dorids.  McGowan & Pratt 1953 Bull Mus Comp Zool Harvard Coll 111: 261.

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  based on other studies of nudibranch development, hatching would be expected in 6-10d at this rearing temperature - not 20-24d as reported
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Research study 2
 

photograph of dorid nudibranch Doris sp. with egg massWhen adult Doris montereyensis deposit their egg masses, do they select spots providing optimal survival of the embryos?  Factors that may be important in this regard are intensity of solar radiation, degree of microalgal/diatom fouling, and current velocities.  Field studies done at Friday Harbor Laboratories, San Juan Islands, Washington show that D. montereyensis preferentially deposit their egg ribbons in the shade of macroalgae, such as green algae Ulva spp., more often than by chance alone, and this leads to greater survival of embryos.  In 16 test quadrats, for example, the proportion of egg masses shaded by algae is 0.5, while the proportion of general substratum shaded by algae is 0.2, indicating a significant preference by Doris for shady substrata. These algal-protected egg masses are less fouled by microalgae and remain whiteish and cream-coloured through to the veliger stage.  In comparison, egg ribbons in full sunlight invariably become brown with a coating of diatoms. Laboratory experiments show that the embryos within these fouled masses suffer retardation in development and greater mortality. Biermann et al. 1992 Mar Ecol Progr Ser 86: 205.

Doris sp. with fouled egg mass. Compare this
mass with the one in Research Study 1 above

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Doto

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Research study 1
 

photograph of nudibranch Doto amyra Gary McDonaldThe tiny nudibranch Doto amyra feeds almost exclusively on  hydroids Abietinaria spp., uses it as a place to deposit its eggs, and preferentially settles on it as a competent larva.  Research on Doto’s development at the Oregon Institute of Marine Biology, Charleston shows that its eggs (150µm diameter) are lecithotrophic and that hatching occurs after 3wk at 16C.  The newly hatched larvae alternate swimming and crawling and, if they alight upon an Abietinaria colony, will settle on it within 1-2d and metamorphose.  The larval shell is lost after about 4d and within 7d from hatching the juveniles are feeding.  They feed by drilling a hole in the hydroid’s perisarc and then sucking out the contents of the coenosarc.  The author notes that the youngsters are not skilled at this, as often the contents are sucked back out of Doto’s alimentary tract by negative pressure in the hydroid’s coenosarc.  This may be just an adolescent problem that will be overcome with age, but the author speculates that the negative pressure might also be a defensive strategy on the part of the hydroid to interfere with predators attempting to feed on it, or even perhaps a way for the predator to introduce digestive enzymes into the hydroid.  Goddard 1996 The Veliger 39 (1): 43. Photograph courtesy Gary McDonald, Long Marine Laboratory Santa Cruz, California.

Some stages in development are shown below:

 
number 1 in a series of 5 developmental stages of the nudibranch Doto amyra number 2 in a series of 5 developmental stages of the nudibranch Doto amyra number 3 in a series of 5 developmental stages of the nudibranch Doto amyra number 4 in a series of 5 developmental stages of the nudibranch Doto amyra number 5 in a series of 5 developmental stages of the nudibranch Doto amyra
Pre-hatching veliger 125X Newly hatched veliger Post-larva after exit from shell 7d juvenile with functional radula 38d juvenile with rhinophore buds
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Flabellina (Coryphella)

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Research study 1
 

photograph of an aeolid nudibranch Flabellina trilineataDevelopment of Flabellina (Coryphella) trilineata in the Dillon Beach area of California takes 5-6d at 15oCBridges & Blake 1972 Veliger 14: 293.

 

 

Figures below from Left to Right: egg mass, development to trochophore stage,
hatched veliger larva with digestive-tract elements highlighted (5d of age)

 
drawing of egg strings of the aeolid nudibranch Flabellina trilineata courtesy Bridges & Blake 1972 Veliger 14: 293 drawings of capsuls of the aeolid nudibranch Flabellina trilineata showing different developmental stages courtesy Bridges & Blake 1972 Veliger 14: 293 drawing of veliger larva of the aeolid nudibranch Flabellina trilineata courtesy Bridges & Blake 1972 Veliger 14: 293
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Haminoea

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Research study 1
 

photographs of a cephalaspidean opisthobranch Haminoe (Haminaea) callidegenita with egg mass Photo courtesy Jan Kocianphotograph of veliger larva of cephalaspidean opisthobranch Haminoea (Haminaea) callidegenita Gibson & Chia 1989 Biol Bull 176: 103The cephalaspidean Haminoea (Haminaea) callidegenita1 (shown in the photo on the Left is the related H. virescens) has an unusual pattern2 of development, with some embryos hatching as lecithotrophic veligers and others hatching as juveniles from a single egg mass.  Studies at Friday Harbor Laboratories, Washington and Bamfield Marine Sciences Centre, British Columbia indicate that about 40%3 of the eggs hatch to veligers (photograph upper Right), while 60% metamorphose within the egg capsule and emerge as crawling juveniles (photograph lower Right), both taking about 5wk at 15oC.

photograph of a 30d-juvenile of cephalaspidean opisthobranch Haminoea (Haminaea) callidegenita Gibson & Chia 1989 Biol Bull 176: 103Development of the 2 morphs within the gelatinous egg mass is synchronous until about 30d after egg deposition, but there then ensues a prolonged hatching of both types over 3-11d. If embryos are cultured separately from the egg mass, then about 80% hatch as veligers; if cultured in the presence of pieces of egg-mass jelly, then this value drops to 40% as noted above.  Since the egg-mass jelly also induces metamorphosis in veligers, the authors photographs of cephalaspidean Haminoea japonica courtesy Terry Gosliner and Yukari Satosuggest that some diffusible compound may be present in the jelly that induces intracapsular metamorphosis.  The authors suggest that the split developmental pattern in Haminaea is a bet-hedging strategy, allowing immediate recruitment in a site guaranteed to be “adult-favourable”, while at the same time providing the benefits of larval dispersal.  Gibson & Chia 1989 Biol Bull 176: 103. Photo of H virescens courtesy Jan Kocian and seaslugforum, of H. japonica (California) Terry Gosliner, and of H. japonica (Japan) Yukari Sato.

NOTE1  the species is now known as Haminoea japonica (see photos on lower Left) after investigation by researchers at the California Academy of Sciences.  Gosliner & Behrens 2006 Proc Calif Acad Sciences 57 (37): 1003

NOTE2  the term used for the presence of 2 or more developmental modes within a species is poecilogonous (lit. “varied offspring” G.).  In opisthobranchs poecilogony occurs in only a few species and seems to be related to geography, feeding conditions, and other factors (another example of poecilogony is presented in Research Study 1 in subsection "Alderia" above)

NOTE3  there is, however, considerable variability with respect to % veligers (10-70% among 9 egg masses) 

 

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Research study 2

 

A few days before hatching in the cephalaspidean  Haminoea (Haminaea) japonica, the jelly mass begins to deteriorate and become colonised by microorganisms and nematodes.  A softening of the egg capsule allows egress of veligers and juveniles, and they make their way, by swimming and crawling, respectively, out of the jelly mass. Veligers then swim for several days (up to 20d for some individuals) and then metamorphose.  Veligers do not grow during the few days of pelagic life, and the only visible change is a diminution of yolk reserves.  Juveniles also have a reserve of yolk to stay them over for a few days if their algal food is not immediately available. Gibson & Chia 1989 Biol Bull 176: 103.

NOTE  epiphytes growing on the green alga Chaetomorpha linum is a favoured food for both adults and juveniles, and the alga itself is a metamorphosis-inducer

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Research study 3
  A later study by the same authors using Haminoea callidegenita collected at San Juan Islands and nearby mainland bays in Washington shows that the proportion of juveniles released per egg mass is not influenced by time of year, female fecundity or body size, egg size, type of metamorphosis inducer, different culture conditions, or other factors.  However, variability does occur among clutches of a given female, different populations, and different years.  In fact, the only effect identified by the authors is food deprivation.  Food-deprived females initially produce more pelagic veligers than do control females (62 vs. 48%).  After about 10d of food deprivation, however, the difference becomes non-significant.  Gibson & Chia 1995 Mar Ecol Prog Ser 121: 139.
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Research study 4
 

In comparison with the unusual developmental pattern of the cephalaspidean Haminoea japonica described above, the related Haminoea vesicula exhibits a pattern “typical of other planktonic opisthobranchs”.  Developmental stages at 12-15oC are: gastrula (26-35h after eggs are laid), veligers hatch (9-12d). By 40-45d the larvae are competent to metamorphose. They begin to swim near the bottom of the culture dishes with velar lobes extended. By 5d post-metamorphosis the juveniles are feeding. The authors investigated, but could not identify, a metamorphosis-inducing substratum.  Gibson & Chia 1989 Veliger 32: 409.

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Research study 5
 

To what extent might scarcity of suitable sites for attaching eggs be a cost to an opisthobranch?  This is tested with the bubble-shell snail Haminoea vesicula, which inhabits sand/mud substrata and requires solid objects to which to attach its egg masses.  On beaches around Friday Harbor Laboratories, Washington such solid objects as eelgrass blades, membranous algae, and bivalve shells comprise less than 1% of the available area.  To test the hypothesis that substratum availability limits deposition of eggs, bubble shells in tidepools in the field are presented with artificial eelgrass made photograph with highlights showing bubble shells Haminoea vesicula on a sand/mud flatof strips of duct tape.  Results show that significantly more egg ribbons are deposited in the experimental area than in nearby control areas, in some cases up to 360-fold more.  Moreover, the artificial eelgrass areas actually attract more snails than nearby natural eelgrass patches.  The implication of this is that Haminaea will preferentially incur extra costs in time, energy, and risk in traveling to scarce substrata for egg deposition.  The authors note, then, that scarcity of deposition sites may represent a significant, and hidden, cost of benthic development.  Von Dassow & Strathmann 2005 Mar Ecol Progr Ser 294: 23.

 

Sand/mudflat with numerous Haminoea and a single,
aggregated egg mass. Available algal and shell-bit egg-
deposition sites have been visually enhanced 0.1X

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Hermissenda

 
Research study 1
 

histograms comparins sizes of veliger larvae of 2 aeolid nudibranchs Hermissenda crassicornia and Aeolidia papillosaLaboratory culture of Hermissenda crassicornis and Aeolidia papillosa from Tomales Bay, California show that hatching occurs 7 and 8d after fertilisation, respectively (at 14oC).  The early-hatching Hermissenda larvae are histograms showing proportions of yolk-free and yolk-laden larvae of the aeolid nudibranch Aeolidia papillosasmaller than those of Aeolidia (see figure on Left).

Interestingly, within the range of size of Aeolidia hatchlings, larger individuals have utilised their yolk reserves fully, while smaller ones have residual yolk in their stomachs and digestive glands (see histograms on Right). Those larvae without yolk begin feeding almost immediately after hatching, while those with yolk commence feeding some time later.  The author suggests that the yolk reserves at hatching allows a portion of the larval population temporary independence from the need to feed, perhaps leading to greater dispersal.  Williams 1980 Malacologia 20: 99.

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Research study 2
 

graph showing effect of crowding on growth of larvae of the aeolid nudibranch Hermissenda crassicornis
A single egg mass of Hermissenda crassicornis yields 7000 to one million veliger larvae.  The larvae swim and feed on phytoplankton for 30-40d before metamorphosing.  Laboratory experiments on larval H. crassicornis in Woods Hole, Massachusetts provide information on the best conditions for growth and metamorphosis.  Growth is best at larval densities of 1-4 larvae . ml-1 on a diet of Isochrysis galbana  and Rhodomonas salina (1:1) at densities of 10-25 x 103 cells . ml-1 (12oC).   Avila et al. 1997 J Exp Mar Biol Ecol 218: 243.

NOTE  growth at densities of 1-4 . ml-1 do not differ significantly; however, growth at a density of 15. ml-1 is significantly depressed

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Onchidoris

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Research study 1
 

photograph of dorid nudibranch Onchidoris belamellata courtesy Paul Young
Eggs of the barnacle-eating Onchidoris bilamellata are laid in late winter when the adults are of maximum size and reproductive output is greatest.  The larvae remain planktonic for several months and settle in springtime coincidental with the appearance of barnacle spat which are the food of the juvenile nudibranchs.  The duration of the larval lifetime of Onchidoris, then, is a balance between 2 factors: optimal time to spawn (when the adults are biggest) and optimal time to settle (when suitable food is available).  Todd & Doyle 1981 Mar Ecol Progr Ser 4: 75. Photo courtesy Paul Young and the Seaslug Forum at seaslugforum.

NOTE  a term for recently settled juveniles of sessile shellfish, such as oysters and barnacles.  In past times, as evidenced by the following quote from a French document in 1376, the word was used more generally: “…le spat des oistres, musklys, & d’autres pessons.”

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Phyllaplysia

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Research study 1
 

photograph of the anaspidean opisthobranch Phyllaplysia tayloridrawing of egg mass of the anaspidean Phyllaplysia taylori showing disposition of nutritional bodies courtesy Bridges 1975 Ophelia 14: 161
Studies on development of the anaspidean Phyllaplysia taylori at Dillon Beach, California reveal a unique pattern, one in which a planktonic larval stage is lacking.  Eggs are laid on eelgrass blades Zostera in jelly masses.  Each capsule contains a single egg (about 150µm in diameter) and each egg is accompanied by a “nutritional body”, to be later eaten by the newly metamorphosed juvenile. Development takes 27d (at 17oC) and proceeds through veliger larval stages and a metamorphosed juvenile, at which time hatching takes place (see drawings below).

The juveniles soon grow an enlarged shell and are known as veliconchs. Juveniles consume an adult diet of diatoms which are grazed from the surface of the eel-grass blades.  Adults are short-lived and there are 2 generations per year.  Bridges 1975 Ophelia 14: 161.

NOTE  this is the remnant of the polar-body and is about 50µm in diameter

drawing of early veliger larva of the anaspidean Phyllaplysia taylori showing disposition of nutritional bodies courtesy Bridges 1975 Ophelia 14: 161

During larval development the veligers feed on yolk. The mouth becomes functional only after hatching
drawing of late veliger larva of the anaspidean Phyllaplysia taylori showing disposition of nutritional bodies courtesy Bridges 1975 Ophelia 14: 161
Prior to metamorphosis the velum is resorbed and a radula develops. Metamorphosis takes place within the capsule
drawing of post-metamorphic juvenile of the anaspidean Phyllaplysia taylori showing disposition of nutritional bodies courtesy Bridges 1975 Ophelia 14: 161

The hatchling crawls and eats. Its first food is the nutritional body, which seems here to be within the shell
drawing of the juvenile velichonch stage of the anaspidean Phyllaplysia taylori showing disposition of nutritional bodies courtesy Bridges 1975 Ophelia 14: 161

Soon after hatching the shell expands into a veliconch. In some localities the velichonch does not persist into the adult
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Research study 2
 

drawing of micrograph section of egg strand of anaspid Phyllaplysia tayloriphotograph of eggs of the anaspid Phyllaplysia taylori courtesy Ken-ichi Ueda, CaliforniaIn a comparative study of fine structure of egg masses of 19 world species of opisthobranchs, researchers at Ruhr-Universität, Germany confirm that Phyllaplysia taylori has just a single egg within each capsule.  In this way the species differs from 2 other anaspid species examined, Aplysia punctata and Bursatella leachii, that have multiple eggs per capsule.  Klussmann-Kolb & Wägele 2001 Zoologischer Anzeiger 240: 101. Photograph courtesy Ken-ichi Ueda, California.

 

The eggs appear to be doubly protected,
in an enclosing membrane and embedded
in a mucous matrix

Eggs deposited in a flat layer on
a blade of eelgrass zostera

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