Biol. Bull.
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Web of Science (2)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Strathmann, M. F.
Right arrow Articles by Strathmann, R. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Strathmann, M. F.
Right arrow Articles by Strathmann, R. R.
Related Collections
Right arrow Development
Right arrow Ecology
Right arrow Evolution
Right arrow Larval Biology
Right arrow Molluscs
Biol. Bull. 213: 152-159. (October 2007)
© 2007 Marine Biological Laboratory

An Extraordinarily Long Larval Duration of 4.5 Years from Hatching to Metamorphosis for Teleplanic Veligers of Fusitriton oregonensis

Megumi F. Strathmann and Richard R. Strathmann*

Friday Harbor Laboratories, University of Washington, 620 University Road, Friday Harbor, Washington 98250

* To whom correspondence should be addressed. E-mail: rrstrath{at}u.washington.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Literature Cited
 
Veliger larvae of the NE Pacific snail Fusitriton oregonensis were reared in culture for 4.5 to 4.6 years from hatching to metamorphosis and through postlarval growth to reproduction. Larval shells grew in length from 0.20 to 3.9 mm. Late veligers grew slowly, but shell sizes increased even in the 4th and 5th years. Widths of larval shells at late stages equaled or exceeded those of the protoconchs of two juveniles from the field. Cultured larvae did not metamorphose until presented with subtidal rocks and associated biota. There was no indication of larval senescence: the first 2 years of postmetamorphic shell growth were slightly faster, and time from metamorphosis to first reproduction (3.3 years) was slightly less than for an individual that had developed to metamorphic competence in the plankton. A 4.5-year larval phase exceeds previous estimates for teleplanic larval durations and greatly exceeds estimates of the time for transport across oceans. This extraordinarily long larval period may exceed the usual duration in nature but shows that larval periods can be much longer than previously suspected without complete stasis in growth and with little if any loss of viability.


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Literature Cited
 
Teleplanic (long-lived) larvae are transported by currents across ocean basins (Häcker, 1898; Mortensen, 1898; Scheltema, 1968, 1988; Laursen, 1981) and have been reported in diverse taxa, including ranellid and architectonicid gastropods (Scheltema, 1966, 1971a, b, 1988; Laursen, 1981; Bieler, 1983; Scheltema and Williams, 1983), bivalves (Gofas, 2000; Scheltema and Williams, 1983), polychaetes (Scheltema, 1974; Murina, 1997), sipunculans (Scheltema and Rice, 1990; Staton and Rice, 1999), and spiny lobsters (Phillips et al., 1979; Pollock, 1990). Such transoceanic transport suggests capacities to prolong greatly the pelagic larval stage (Pechenik et al., 1984). Larval duration is extended by the period of larval metamorphic competence, which often exceeds the period preceding competence (Jackson and Strathmann, 1981). Larvae extend their competent period either by feeding (Kempf and Hadfield, 1985) or, as in Heliocidaris erythrogramma and Mediaster aequalis, at the expense of reserves otherwise used by the postmetamorphic juvenile (Birkeland et al., 1971; Emlet and Hoegh-Guldberg, 1997; Bryan, 2004). Non-feeding larvae eventually run out of metabolic fuel (Lucas et al., 1979; Pechenik et al., 1998), and some feeding larvae eventually metamorphose without the usual stimulus (Fenaux and Pedrotti, 1988).

Thorson (1961) estimated the minimum larval longevities required for transport in several ocean currents and compared these times to observed larval durations. More recent observations of larval longevity from cultures or presumed cohorts in plankton samples exceed the maximum estimates available to Thorson (e.g., Birkeland et al., 1971; Hadfield, 1978; Phillips et al., 1979; Kempf, 1981; Sekine et al., 2000). Pelagic durations of a year or more have been observed or inferred for teleplanic larvae, but establishment of known extremes for larval duration appears to be limited by capacity to maintain cultures or recognize members of a pelagic cohort.

Here we report a longevity record for marine invertebrate larvae. The larvae were veligers of Fusitriton oregonensis (Redfield, 1846) of the gastropod family Ranellidae (formerly Cymatiidae, see Beu and Cernohorsky, 1986). Larvae of other ranellid species have been found in plankton samples from surface waters across both the Atlantic and Pacific oceans (Scheltema, 1966, 1971a, b, 1988; Laursen, 1981; Scheltema and Williams, 1983), and it was in discussion of ranellid distributions that the adjective "teleplanic" was coined for long-lived larvae dispersing great distances in ocean currents (Scheltema, 1971b). Sirenko (1993) noted the large protoconch (larval shell) and pelagic larva of Fusitriton oregonensis, which has a reported range from California to northern Japan (Beu, 1978) that includes the isolated seamounts Cobb and Patton (Birkeland, 1971; Somerton, 1981).

This study was not planned as one of larval longevity and replication is low, but the observations are surprising and noteworthy. Although the long larval phase in culture may not reflect the usual duration in nature, the results demonstrate that larval durations can be far longer than previously suspected. Also, to our knowledge, this is the first successful rearing of ranellid veligers from hatching through metamorphosis and of their juveniles from metamorphosis to maturity.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Literature Cited
 
Cultures
Egg capsules of Fusitriton oregonensis were collected by scuba from rocky, shallow subtidal areas near San Juan Island, Washington, and maintained in flow-through seawater aquaria at the Friday Harbor Laboratories. Kawabe et al. (2000) and Brante (2006) have described form and function of the egg capsules. An array of capsules (clutch) that was brought into the laboratory on 22 July 1992 began hatching on 24–27 July of that year. Sizes and ages reported here are for larvae from this one clutch, and because each female lays a clutch and guards it (Eaton, 1971), these larvae are inferred to have the same mother. On 29 July, veligers from six capsules were cultured at an initial density of 2000 larvae per liter in each of four 2-liter cultures in 4-liter jars, open at the top and stirred with paddles swinging at 8 cycles per min (Strathmann, 1987). Densities were reduced after one week, again after 2.5 weeks, and later by attrition from sampling and mortality (see below).

We initially changed the water three times per week, in later years at least twice weekly, and then at least once each week. We changed water by reverse filtration through a 70-µm nylon mesh when the veligers were small and later by decanting. Seawater was initially filtered through a 0.45-µm membrane filter; later through a bag filter of about 10-µm mesh. Larvae were transferred to clean jars with removal of dead larvae and debris about weekly. Veligers were fed the alga Rhodomonas sp. initially at about 4000 cells ml–1, after 3 weeks at 5000 cells ml–1, and after 10 weeks at approximately 5000 to 10,000 cells ml–1. The cultures supplied with seawater from 10-µm filters contained other organisms as additional food.

Partial immersion of the jars in aquaria kept cultures within ± 2 °C of the temperature in a natural habitat, the San Juan Channel. Recorded winter (January–February) temperatures during 4 years of larval culture were 9 °C median, 7 to 11.5 °C range (n = 72); and summer (July–August) temperatures were 13 °C median and range 12 to 15 °C (n = 72). Over all months, the temperatures were 11.3 ± 1.8 °C (mean ± SD, n = 388).

Sampling and treatments varied over the unexpectedly long study. For the first 2 months, 25 actively swimming veligers were removed and preserved for measurement about weekly. At day 79, sampling was reduced to 10 veligers every 2 weeks. After day 110, sampling was nondestructive. From day 206, we measured shells of live veligers under a dissecting microscope, and the remaining 133 veligers were divided into two jars. After the first year we attempted several times to stimulate metamorphosis of subsamples of veligers. All but the final attempt was unsuccessful, and after each test survivors were maintained in a separate culture jar. Fouling of veligers' shells in their later years was reduced by hand-cleaning individual shells with a small short-bristled paintbrush. Larger veligers were manipulated for cleaning and measurements with small plastic dental picks.

Newly metamorphosed juveniles were placed in cages with 1-mm-mesh sides. The cages were weighted with rocks and submerged in a flow-through aquarium. Metamorphosed juveniles were fed small pieces of oysters (Crassostrea gigas, from Westcott Bay Sea Farms, San Juan Island) and occasionally other bivalves, once or twice weekly. Two and one-half years after metamorphosis, the five surviving juveniles were released into a flow-through seawater aquarium with a variety of other marine invertebrates, including two larger males of F. oregonensis. These seven snails were fed fresh oyster on the half shell, initially weekly and after 3 years less frequently. A juvenile reared from a field-collected veliger was added later.

Measurements and counts
Sizes of veligers near hatching were measured from five capsules from the field-collected clutch that was the source of larvae reared in culture. Throughout rearing, veliger shells (not including periostracal spines) were measured with an ocular micrometer for shell length (maximum dimension parallel to the coiling axis) and shell width (maximum dimension perpendicular to the coiling axis). Accuracy was limited by difficulty in orienting shells and also by fouling, though fouling could be partially removed. Juvenile and adult shells were measured with calipers or a ruler.

Fecundity was estimated from counts of capsules per clutch and counts of prehatching veligers per capsule. Veligers were counted in a Bogaroff tray.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Literature Cited
 
Veliger growth and duration of larval life
Near hatching, veliger shell lengths were 0.197 ± 0.0056 mm and shell widths were 0.237 ± 0.0082 mm (mean ± SD, n = 50, 10 each from five egg capsules). Four and a half years later, near metamorphosis, survivors' shells were 3.90 ± 0.55 mm in length and 3.21 ± 0.35 mm in width (mean ± SD, n = 11). The initial two simple velar lobes elaborated to form two long lobes on each side (Fig. 1), so that for most of their development the larvae had four velar lobes, each with red to dark red pigment at their distal ends. Velar lobes reached a total transverse spread as great as 2 cm.


Figure 1
View larger version (82K):
[in this window]
[in a new window]

  		Figure 1. Veliger of Fusitriton oregonensis at 1 year from hatching, 1.1 cm across the velar lobes.

 
The shells had periostracal spines in rows along the shell's spiral. The shells were initially almost planispiral but elongated during development (Fig. 2). Mean shell sizes indicated slower growth with increased age (Fig. 2). Because size-dependent mortality can bias estimates of growth, for estimates of later growth we measured sizes of all larvae in a culture jar during two intervals that had no mortality. (These were larvae from an unsuccessful attempt to induce metamorphosis.) These measurements showed that growth in shell size still occurred from age 2 to 4.5 years (Fig. 3).


Figure 2
View larger version (18K):
[in this window]
[in a new window]

  		Figure 2. Shell sizes at age of veligers of Fusitriton oregonensis from 5 days before hatching to 15 days before metamorphosis (mean, maximum, and minimum). Top: shell length (greatest dimension parallel to the axis of coiling). Bottom: shell width (greatest dimension perpendicular to axis of coiling). Measures were from subsamples of sibling veligers reared together in culture and did not include veligers removed in attempts to induce metamorphosis.

 

Figure 3
View larger version (22K):
[in this window]
[in a new window]

  		Figure 3. Growth in shell length (greatest dimension parallel to the axis of coiling) of veligers of Fusitriton oregonensis. Top: growth in their 2nd and 3rd year measured from sampling and replacement of all 10 sibling veligers reared together in a culture. Bottom: growth between 3 and 4.5 years of age measured from sampling and replacement of all four sibling veligers reared together (survivors from the same culture as above). Overlapping points are displaced on the x-axis to show measurements for all individuals. These veligers, reared separately after an unsuccessful attempt to induce metamorphosis, grew larger than those in the source culture (Fig. 2).

 
At 1647 days, the shell width of 11 surviving veligers was 3.21 ± 0.35 mm (mean ± SD). Most were greater than the 2.8 mm widths of protoconchs of two field-collected juvenile snails, indicating that veligers in culture had equaled or exceeded size at metamorphosis in nature.

Pelagic larval duration in nature was indicated by hatching times in the field and time of metamorphosis of a field-collected veliger. Eaton (1971) reported that egg deposition usually started in June or July, although one case occurred in late August. B. Pernet collected a veliger at the Laboratories' dock in early December. This veliger metamorphosed shortly after collection. With about 50 days from deposition to hatching, pelagic duration may therefore be as short as 2 to 4 months (60 to 120 days), but the larval duration of the competent larva observed in December could have been 2 to 4 months plus n years and was most likely 14 to 16 months, based on larval growth in culture (Fig. 2).

Veliger shell calcification
The veligers' shells were calcified from before hatching through late stages. Veliger shells fractured under compression. When shells were acidified with HCl in seawater, bubbles (presumably CO2) were generated, brightness with crossed polarizing filters was lost, and the shells wrinkled instead of fracturing when compressed.

Metamorphosis
Several attempts to induce metamorphosis failed. After 371 days in culture, five veligers were exposed for 24 h to a 20 mmol l–1 elevation of K+ (Yool et al., 1986; Pechenik and Heyman, 1987). After 688 days, six other veligers were exposed to rocks from the intertidal zone. After 1107 days, four veligers previously exposed to elevated K+ as 1-year-olds were exposed to 20 mmol l–1 elevation of Cs+ ions (Hadfield et al., 2000) for 2–3 h, then rinsed in seawater. In each case an equal number with similar history were controls. None metamorphosed in any of these tests.

After 4 years and 7 months in culture, 11 surviving larvae were tested again for competence in three batches between mid-February and early March at 1663, 1669, and 1683 days posthatching. The first three veligers had previously been tested for metamorphic competence by CsCl and the second four by intertidal rocks. The last four had not been previously tested. The veligers were placed in mesh-sided cages and presented with rocks with attached shells and some live barnacles, bivalves, bryozoans, brachiopods, coralline algae, and other organisms. These rocks had been collected subtidally. At least 8 of the 11 veligers settled. Some veligers began crawling within the first day. Juveniles were crawling within 6 to 8 days. Some had initiated a teleoconch (postmetamorphic shell) within 19 days. Time from hatching to settlement was thus 4.5 to 4.6 years for these larvae.

Five of the 11 animals had died within one to several days after transfer to the cages with subtidal rocks: one by accidental crushing during a transfer, one by drying on the cage mesh above the water line, three from unknown causes. The remaining six grew. One died 4 months after metamorphosis, with two teleoconch whorls. The remaining five were labeled with bee tags glued to the protoconch and transferred to a large aquarium at about 2.5 years after metamorphosis.

In contrast, the field-collected veliger metamorphosed within 3 days of collection with no more stimulus than a clean glass bowl. It cast off its four velar lobes.

Postlarval growth and first egg deposition
Five metamorphosed juveniles survived and grew rapidly for 2 years (Fig. 4). Then growth slowed until all remained nearly constant in shell length from 900 to 1400 days after metamorphosis. The three males, but not the two females, resumed growth later in life (Fig. 4). The two females deposited their first clutches within 3.3 years after metamorphosis. One female has survived and deposited eggs annually for 7 years. The females did not grow as large as females of 95- to 110-mm length that were seen guarding eggs in the field. The shell of the surviving laboratory-reared female was still only 80 mm in March 2007, while those of the three laboratory-reared males had reached 94, 98, and 98 mm.


Figure 4
View larger version (23K):
[in this window]
[in a new window]

  		Figure 4. Growth in shell length after metamorphosis. Postlarval snails from veligers reared in the laboratory grew faster and deposited eggs sooner after metamorphosis than the one that had developed to metamorphic competence in the field. Each symbol is for a different individual.

 
The field-collected veliger metamorphosed in a different year (December 2002) from the laboratory-reared veligers (February–March 1997), but its growth is also plotted in Figure 4. Its postmetamorphic growth was no faster and its age at maturation was no earlier than for the individuals with the prolonged larval period in the laboratory, but this female continued to grow after first reproduction and was 94 mm long in March 2007.

Because growth of females in the aquarium ceased at a small size, we tested for an effect of the 5:2 male-to-female ratio in the aquarium by isolating the surviving female from the other snails from January 2004 to October 2005, initially for 4 months in another aquarium, then within a cage in the same aquarium as the males. She did not resume growth during isolation.

In summer of 2004 the isolated female deposited eggs that developed into veligers, but in 2005 none of her deposited eggs developed. The non-developing eggs were 166 µm in diameter (n = 20), similar in size to developing eggs from a field-collected female that deposited in the aquarium (165 µm, n = 20). In 2006, with access again to males, her deposited eggs developed. These observations imply storage of viable sperm for at least 7 months but not for another egg deposition after 19 months.

Fecundity
Because Fusitriton oregonensis does not provide nurse eggs in its capsules and mortality is low for their guarded capsules (Eaton, 1971), the counts of capsules and of veligers per capsule provide an estimate of both fecundity and numbers of hatching veligers per clutch. Numbers of capsules in three clutches from the two laboratory-reared mothers were 328, 314, and 299. Two capsules, each from a different clutch and mother, contained 2200 and 2662 veligers. Capsule sizes from four clutches averaged 9.0 x 6.2 x 2.4 mm. Mothers in the field were larger, deposited larger capsules with more veligers, and therefore had greater fecundity. One deposited 332 capsules in an aquarium. Capsules in two field-collected egg masses contained 4557 ± 894 and 5441 ± 672 veligers (mean ± SD, n = 5 capsules from each clutch). Capsules from these three clutches averaged 10.3 x 6.9 x 3.0 mm. At about 300 capsules per clutch and 2200 to 2700 veligers per capsule, laboratory-reared females of F. oregonensis produced an estimated 7 to 8 x 105 veligers per clutch. With about 5000 veligers per capsule, larger mothers in the field might commonly release 1.5 x 106 veligers per mother per year.

Peculiar effects of laboratory rearing
Diatoms, vorticellid ciliates, and other organisms fouled the veligers' shells, with some fouling observed as early as the 4th month in culture. Fouling may be less in nature; the pelagic veliger collected near the Laboratories' floating breakwater by B. Pernet was metamorphically competent but had an unfouled shell. Folliculinid ciliates occurred on the shells of veligers of Cymatium parthenopeum and other gastropods collected in the North Atlantic by Scheltema (1973), but fouling is generally less in the field than in our cultures, where the usual deterrents of shell fouling may have been overwhelmed. There were times when the larvae seemed slow to retract and withdrew only when handled. At these times, the mantle was extended over the aperture edge, like the fluted edge of a piecrust, perhaps in the process of secreting new periostracal bristles. This area was usually clean and unfouled. Sometimes a small triangular appendage at the mantle edge (near the shell suture at the upper edge of the largest whorl) was expanded over part of the preceding whorl. The shell surface underneath was bare of periostracum and clean, perhaps for attachment of new shell to the preceding whorl. This appendage is presumably homologous to the mantle appendage in related genera (Bandel et al., 1994).

The larvae in culture spent their last 2 years mostly on the bottom of the gently stirred glass jars, often with not all their velar lobes extended. In contrast, a metamorphically competent veliger of F. oregonensis was swimming near the surface in the field when collected by B. Pernet.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Literature Cited
 
A larval duration of 4.5 years suggests that currents could carry larvae very long distances. The longevity exceeds that implied by Scheltema's (1968, 1988) observations of veligers and other larvae transported far from populations of coastal adults. In 4.5 years, at a current speed of 10 cm s–1 (= 0.36 km h–1), a larva could be transported 14,000 km. Currents across ocean basins are commonly this fast or faster (Thorson, 1961; Scheltema, 1971a; Thiel and Gutow, 2004). Implications for transport, however, also depend on the behavior of the larvae and their mortality (Cowen et al., 2000).

Survival of a larval duration of 4.5 years or even 14 months requires an unusually low mortality rate. With an estimated 1.5 x 106 veligers per clutch and one clutch per female per year, annual fecundity is lower than for many sea urchins and bivalves that have much shorter larval periods. Estimated instantaneous mortality rates are commonly about 0.1 d–1 for small larvae in field populations (Strathmann, 1985; Rumrill, 1990; Morgan, 1995; Lamare and Barker, 1999). (These estimates are usually from numbers of larvae at time zero and time t, with the assumption of a constant mortality rate, m: Nt = N0 e–mt.) The mortality rate yielding one survivor after 4.5 years would be 0.0087 d–1, which is half the mortality rate estimated from Johnson's (1939) data on the larger larvae of a spiny lobster (Jackson and Strathmann, 1981). The mortality rate yielding one survivor after 14 months would be 0.033 d–1, near the lower end of estimates for invertebrate larvae. Veligers identified as F. oregonensis do enter the pelagic food chain. Veliger shells were found in the gut contents of three marine birds (two shearwaters and a puffin) from south of the Aleutian Islands between Attu and Adak (A. J. Kohn, University of Washington, pers. comm.).

We do not know when the larvae first became competent for metamorphosis and thus do not know the extent of growth during the competent period. Pechenik et al. (1984) found no significant difference in biomass of veligers of Cymatium parthenopeum with longitude across the Atlantic. Our observations indicate continued growth of veligers of F. oregonensis, but the very slow growth of the older veligers in culture is consistent with observations of near stasis in growth of related veligers in the field.

Senescence might evolve for competent larvae by processes similar to those suggested for evolution of senescence at later stages in life (Williams, 1957). If larval survival beyond a year or two is extremely rare, there should be negligible selection for prolonged maintenance of the ephemeral larval structures and continued capacity for metamorphosis. Selection against such prolonged maintenance of larval and metamorphic capacity would be expected if that maintenance were at the expense of traits that increase numbers surviving and settling earlier. Nevertheless, there was no sign of senescence associated with long larval duration in F. oregonensis. Miller and Hadfield (1990) noted a different effect of prolonged larval life on senescence: the postponement of life-history stages in which deleterious effects of genes are evident. Adding days to larval life by withholding a metamorphic stimulus extended the overall lifespan of the nudibranch Phestilla sibogae by an equal number of days.

To our knowledge, the 4.5-year duration for veligers of F. oregonensis exceeds the longest previously observed pelagic durations for marine larval forms. The inferred minimum duration for the field-collected veliger (>14 months) is close to the longest durations previously observed in culture. Most of the reported very long larval durations are about a year. Examples are about 300 days (mostly during metamorphic competency) for tornariae of the hemichordate Ptychodera flava, inferred from spawning dates and plankton samples (Hadfield, 1978); up to 316 days for veligers of the gastropod Aplysia juliana in culture (Kempf, 1981); 14 months (at least 12 during competency) for non-feeding larvae of the seastar Mediaster aequalis in culture (Birkeland et al., 1971); and 417 days for larvae of the spiny lobster Panulirus japonicus (Sekine et al., 2000). Chaetopterid annelid larvae survived for more than 400 days in the laboratory after collection in the North Atlantic Drift (Scheltema, 1974). Some durations estimated for large larvae of crustaceans and fishes are much more than a year. Examples are the phyllosoma larvae of the decapod crustacean Panulirus cygnus, inferred from overlapping annual cohorts in the plankton (Phillips et al., 1979), and leptocephali of anguillid eels with larval durations of 1 to 3 years (Castle, 1984).


   Acknowledgments
 
This research was supported by NSF grants OCE96-33193, IBN0113603, OCE0217304, and OCE0623102. The Friday Harbor Laboratories of the University of Washington provided facilities. We are grateful to Michelle Woodbury Herko and Sue Brady for help with cultures; to Douglas J. Eernisse, Michael G. Hadfield, Carole S. Hickman, Alan J. Kohn, Jan A. Pechenik, Craig Staude, and anonymous reviewers for advice; to Bruno Pernet for data from his veliger; and to David O. Duggins, Rachel Collin, Roddy Foley, Alan J. Kohn, and Bruno Pernet for specimens from the field.


   Footnotes
 
Received 26 April 2007; accepted 28 June 2007.


   Literature Cited
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Literature Cited
 

    Bandel, K., F. Riedel, and H. Tiemann. 1994. A special adaptation to planktonic life in larvae of the Cassoidea (=Tonnoidea) (Gastropoda). Mar. Biol. 118: 1–108.
    Beu, A. G. 1978. The marine fauna of New Zealand: the molluscan genera Cymatoma and Fusitriton (Gastropoda, family Cymatiidae). N. Z. Oceanogr. Inst. Mem. 65: 5–43.
    Beu, A. G., and W. O Cernohorsky. 1986. Taxonomy of gastropods of the families Ranellidae (=Cymatiidae) and Bursidae. Part 1. Adoption of Ranellidae, and review of Linatella Gray, 1857. N. Z. J. Zool. 13: 241–266.
    Bieler, R. 1983. The amphi-atlantic distribution of Pseudomalaxis lamellifera Rehder. Arch. Molluskenk. 114: 117–123.
    Birkeland C. 1971. Biological observations on Cobb Seamount. Northwest Sci. 45: 193–199.
    Birkeland C., F.-S. Chia, and R. R. Strathmann. 1971. Development, substratum selection, delay of metamorphosis and growth in the seastar Mediaster aequalis Stimpson. Biol. Bull. 141: 99–108.[Abstract/Free Full Text]
    Brante, A. 2006. An alternative mechanism to reduce intracapsular hypoxia in ovicapsules of Fusitrition oregonensis (Gastropoda). Mar. Biol. 149: 269–274.
    Bryan, P. J. 2004. Energetic cost of development through metamorphosis for the seastar Mediaster aequalis (Stimpson). Mar. Biol. 145: 293–302.
    Castle, P. H. J. 1984. Notacanthiformes and Anguilliformes: Development. Pp. 62–63 in Ontogeny and Systematics of Fishes. Spec. Publ. 1. American Society of Ichthyologists and Herpetologists, Lawrence, KS.
    Cowen, R. K., K. M. M. Lwiza, S. Sponaugle, C. B. Paris, and D. B. Olson. 2000. Connectivity of marine populations: open or closed? Science 287: 857–859.[Abstract/Free Full Text]
    Eaton, C. M. 1971. The reproductive and feeding biology of the prosobranch gastropod Fusitriton oregonensis (Redfield) (Fam. Cymatiidae). M.S. thesis, University of Washington, Seattle.
    Emlet, R. B., and O. Hoegh-Guldberg. 1997. Effects of egg size on postlarval performance: experimental evidence from a sea urchin. Evolution 51: 141–152.[Web of Science]
    Fenaux, L., and M. L. Pedrotti. 1988. Metamorphose des larves d'echinides en pleine eau. Pubbl. Stn. Zool. Napoli: Mar. Ecol. 9: 93–107.
    Gofas, S. 2000. Systematics of Planktomya, a bivalve genus with teleplanic larval dispersal. Bull. Mar. Sci. 67: 1013–1023.
    Häcker, V. 1898. Die pelagischen Polychaeten und Achaetenlarven der Plankton-Expedition. Pp. 1–50 in Ergebnisse der Plankton-Expedition der Humboldt-Stiftung, Bd 2. Lipsius & Tischer, Kiel.
    Hadfield, M. G. 1978. Growth and metamorphosis of planktonic larvae of Ptychodera flava (Hemichordata: Enteropneusta). pp. 247–254 in Settlement and Metamorphosis of Marine Invertebrate Larvae, F.-S. Chia and M. E. Rice, eds. Elsevier/North Holland, New York.
    Hadfield, M. G., E. A. Meleshkevitch, and D. Y. Boudko. 2000. The apical sensory organ of a gastropod veliger is a receptor for settlement cues. Biol. Bull. 198: 67–76.[Abstract]
    Jackson, G. A., and R. R. Strathmann. 1981. Larval mortality from offshore mixing as a link between precompetent and competent periods of development. Am. Nat. 118: 16–26.[Web of Science]
    Johnson, M. W. 1939. Production and distribution of larvae of the spiny lobster, Panulirus interruptus (Randall) with records of P. gracilis Streets. Bull. Scripps Inst. Oceanogr. 7(b): 413–462.
    Kawabe, R., K. Nashimoto, K. Kanai, S. Torisawa, and T. Hiraishi. 2000. Gonadal maturation of female Oregon triton Fusitriton oregonensis in south eastern Hokkaido and spawning behavior and rearing. Bull. Fac. Fish. Hokkaido Univ. 51: 95–104.
    Kempf, S. C. 1981. Long-lived larvae of the gastropod Aplysia juliana: Do they disperse and metamorphose or just slowly fade away? Mar. Ecol. Prog. Ser. 6: 61–65.
    Kempf, S. C., and M. G. Hadfield. 1985. Planktotrophy by the lecitotrophic larvae of a nudibranch, Phestilla sibogae (Gastropoda). Biol. Bull. 169: 119–130.[Free Full Text]
    Lamare, M. D., and M. F. Barker. 1999. In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). Mar. Ecol. Prog. Ser. 180: 197–211.
    Laursen, D. 1981. Taxonomy and Distribution of Teleplanic Prosobranch Larvae in the North Atlantic. Dana Report No. 89. Scandinavian Science Press, Copenhagen.
    Lucas, M. I., G. Walker, D. L. Holland, and D. J. Crisp. 1979. An energy budget for the free-swimming and metamorphosing larvae of Balanus balanoides (Crustacea: Cirripedia). Mar. Biol. 55: 221–229.
    Miller, S. E., and M. G. Hadfield. 1990. Developmental arrest during larval life and life-span extension in a marine mollusc. Science 248: 356–358.[Abstract/Free Full Text]
    Morgan, S. G. 1995. Life and death in the plankton: larval mortality and adaptation. pp. 279–321 in Ecology of Marine Invertebrate Larvae, L. McEdward, ed. CRC Press, Boca Raton, FL.
    Mortensen, T. 1898. Die Echinodermenlarven der Plankton-Expedition. Ergebnisse der Plankton Expedition der Humboldt-Stiftung, Bd. 2. Lipsius & Tischer, Kiel.
    Murina, V. 1997. Pelagic larvae of Black Sea Polychaeta. Bull. Mar. Sci. 60: 427–432.
    Pechenik, J. A., and W. D. Heyman. 1987. Using KCl to determine size at competence for larvae of the marine gastropod, Crepidula fornicata (L.). J. Exp. Mar. Biol. Ecol. 112: 27–38.[Web of Science]
    Pechenik, J. A., R. S. Scheltema, and L. S. Eyster. 1984. Growth stasis and limited shell calcification in larvae Cymatium parthenopeum during trans-Atlantic transport. Science 224: 1097–1099.[Abstract/Free Full Text]
    Pechenik, J. A., D. E. Wendt, and J. N. Jarrett. 1998. Metamorphosis is not a new beginning. Bioscience 48: 901–910.[Web of Science]
    Phillips, B. F., P. A. Brown, D. W. Rimmer, and D. D. Reid. 1979. Distribution and dispersal of the phyllosoma larvae of the western rock lobster, Panulirus cygnus, in the south-eastern Indian Ocean. Aust. J. Mar. Freshw. Res. 30: 773–783.
    Pollock, D. E. 1990. Palaeoceanography and speciation in the spiny lobster genus Jasus. Bull. Mar. Sci. 46: 387–405.
    Rumrill, S. S. 1990. Natural mortality of marine invertebrate larvae. Ophelia 32: 163–198.[Web of Science]
    Scheltema, R. S. 1966. Evidence for trans-Atlantic transport of gastropod larvae belonging to the genus Cymatium. Deep-Sea Res. 13: 83–95.
    Scheltema, R. S. 1968. Dispersal of larvae by equatorial ocean currents and its importance to the zoogeography of shoal-water tropical species. Nature 217: 1159–1162.
    Scheltema, R. S. 1971a. Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. Biol. Bull. 140: 284–322.[Abstract/Free Full Text]
    Scheltema, R. S. 1971b. The dispersal of the larvae of shoal-water benthic invertebrate species over long distances by ocean currents. Pp. 7–28 in Fourth European Marine Biology Symposium, D. J. Crisp, ed. Cambridge University Press, Cambridge.
    Scheltema, R. S. 1973. Dispersal of the protozoan Folliculina simplex Dons (Ciliophora, Heterotricha) throughout the North Atlantic Ocean on the shells of gastropod veliger larvae. J. Mar. Res. 31: 11–20.
    Scheltema, R. S. 1974. Relationship of dispersal to geographical distribution and morphological variation in the polychaete family Chaetopteridae. Thalassia Jugosl. 10: 297–312.
    Scheltema R. S. 1988. Initial evidence for the transport of teleplanic larvae of benthic invertebrates across the East Pacific Barrier. Biol. Bull. 174: 145–152.[Abstract/Free Full Text]
    Scheltema, R. S. and M. E. Rice. 1990. Occurrence of teleplanic pelagosphaera larvae of sipunculans in tropical regions of the Pacific and Indian Oceans. Bull. Mar. Sci. 47: 159–181.
    Scheltema, R. S., and I. P. Williams. 1983. Long distance dispersal of planktonic larvae and the biogeography and evolution of some Polynesian and western Pacific mollusks. Bull. Mar. Sci. 33: 545–565.
    Sekine, S., Y. Shima, H. Fushimi, and M. Nonaka. 2000. Larval period and molting in the Japanese spiny lobster Panulirus japonicus under laboratory conditions. Fish. Sci. 66: 19–24.
    Sirenko, B. I. 1993. Shell of molluscs in the ontogeny: its significance for taxonomy and the mistakes of classification. Ruthenica 2: 137–139 (in Russian, English Abstract).
    Somerton, D. A. 1981. Fusitriton oregonensis from the Patton seamount in the Gulf of Alaska. Veliger 24: 185–186.
    Staton, J. L., and M. E. Rice. 1999. Genetic differentiation despite teleplanic larval dispersal: allozyme variation in sipunculans of the Apionsoma misakianum species-complex. Bull. Mar. Sci. 65: 467–480.
    Strathmann, M. F. 1987. Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast. University of Washington Press, Seattle.
    Strathmann, R. R. 1985. Feeding and non-feeding larval development and life-history evolution in marine invertebrates. Annu. Rev. Ecol. Syst. 16: 339–361.[Web of Science]
    Thiel, M., and L. Gutow. 2004. The ecology of rafting in the marine environment. I. The floating substrata. Oceanogr. Mar. Biol. 42: 181–264.
    Thorson, G. 1961. Length of pelagic larval life in marine bottom invertebrates related to larval transport by ocean currents. Pp. 455–474 in Oceanography, M. Sears, ed. AAAS, Washington, DC.
    Williams, G. C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11: 398–411.[Web of Science]
    Yool, A. J., S. M. Grau, M. G. Hadfield, R. A. Jensen, D. A. Markell, and D. E. Morse. 1986. Excess potassium induces larval metamorphosis in four marine invertebrate species. Biol. Bull. 170: 255–266.[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 Biol. Bull.Home page
S. M. Arellano and C. M. Young
Spawning, Development, and the Duration of Larval Life in a Deep-Sea Cold-Seep Mussel
Biol. Bull., April 1, 2009; 216(2): 149 - 162.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Web of Science (2)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Strathmann, M. F.
Right arrow Articles by Strathmann, R. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Strathmann, M. F.
Right arrow Articles by Strathmann, R. R.
Related Collections
Right arrow Development
Right arrow Ecology
Right arrow Evolution
Right arrow Larval Biology
Right arrow Molluscs

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS