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Plasticity of Hatching and the Duration of Planktonic Development in Marine Invertebrates

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Plasticity of Hatching and the Duration of Planktonic Development in Marine Invertebrates

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Plasticity in hatching potentially adjusts risks of benthic and planktonic development for benthic marine invertebrates. The proportionate effect of hatching plasticity on duration of larval swimming is greatest for animals that can potentially brood or encapsulate offspring until hatching near metamorphic competence. As an example, early hatching of the nudibranch mollusk Phestilla sibogae is stimulated by scattering of encapsulated offspring, as by a predator feeding on the gelatinous egg ribbon. When egg ribbons are undisturbed, hatching is at or near metamorphic competence. Disturbance of an unguarded benthic egg mass can insert 4 or more days of obligate larval dispersal into the life history. As another example, the spionid annelid Boccardia proboscidea broods capsules, each with both cannibalistic and developmentally arrested planktivorous siblings plus nurse eggs. Early hatching produces mainly planktivorous larvae with a planktonic duration of 15 days. Late hatching produces mainly adelphophages who have eaten their planktivorous siblings and metamorphose with little or no period of swimming. Mothers actively hatch their offspring by tearing the capsules, and appeared to time hatching in response to their environment and not to the stage of development of their offspring. Higher temperature increased the variance of brooding time. Females appeared to hatch capsules at an earlier developmental stage at lower temperatures. Species that release gametes or zygotes directly into the plankton have less scope for plasticity in stage at hatching. Their embryos develop singly with little protection and hatch at early stages, often as blastulae or gastrulae. Time of hatching cannot be greatly advanced, and sensory capabilities of blastulae may be limited.
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SYMPOSIUM
Plasticity of Hatching and the Duration of Planktonic
Development in Marine Invertebrates
Fernanda X. Oyarzun and Richard R. Strathmann
1
Friday Harbor Laboratories and Department of Biology, University of Washington, 620 University Road, Friday Harbor,
WA 98250, USA
From the symposium ‘‘Environmentally Cued Hatching across Taxa: Embryos Choose a Birthday’’ presented at the
annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2011, at Salt Lake City, Utah.
1
E-mail: rrstrath@u.washington.edu
Synopsis Plasticity in hatching potentially adjusts risks of benthic and planktonic development for benthic marine
invertebrates. The proportionate effect of hatching plasticity on duration of larval swimming is greatest for animals
that can potentially brood or encapsulate offspring until hatching near metamorphic competence. As an example, early
hatching of the nudibranch mollusk Phestilla sibogae is stimulated by scattering of encapsulated offspring, as by a
predator feeding on the gelatinous egg ribbon. When egg ribbons are undisturbed, hatching is at or near metamorphic
competence. Disturbance of an unguarded benthic egg mass can insert 4 or more days of obligate larval dispersal into the
life history. As another example, the spionid annelid Boccardia proboscidea broods capsules, each with both cannibalistic
and developmentally arrested planktivorous siblings plus nurse eggs. Early hatching produces mainly planktivorous larvae
with a planktonic duration of 15 days. Late hatching produces mainly adelphophages who have eaten their planktivorous
siblings and metamorphose with little or no period of swimming. Mothers actively hatch their offspring by tearing the
capsules, and appeared to time hatching in response to their environment and not to the stage of development of their
offspring. Higher temperature increased the variance of brooding time. Females appeared to hatch capsules at an earlier
developmental stage at lower temperatures. Species that release gametes or zygotes directly into the plankton have less
scope for plasticity in stage at hatching. Their embryos develop singly with little protection and hatch at early stages,
often as blastulae or gastrulae. Time of hatching cannot be greatly advanced, and sensory capabilities of blastulae may be
limited.
Introduction
Planktonic development is common in the sea, but
its duration varies widely among marine animals.
Some species lack any planktonic larval stage and
hatch from broods or egg capsules as adult-like ju-
veniles, as in Nucella lamellosa (Miner et al. 2010).
At the other extreme, some animals release gametes
or zygotes into the plankton, where embryos and
larvae develop singly with little protection. Between
these extremes, there are many species in which ini-
tial development in protected broods or egg masses
is followed by development as a swimming larva. In
this study, we present hypotheses on both the con-
sequences of hatching plasticity for duration of
planktonic development and the consequences of
planktonic development for hatching plasticity.
Planktonic larval development is divided into a
period of obligate larval swimming (precompetent
period) before the larva is capable of settlement
and metamorphosis, and a period when the larva
can settle and metamorphose in response to a cue
to a favorable benthic habitat (competent period).
Although dispersal of larvae is commonly less than
dispersal of passive particles (Strathmann et al.
2002a; Shanks 2009), a longer duration of obligate
planktonic development during the precompetent
period is expected to increase the potential for
larval dispersal. The swimming larval stage can
Integrative and Comparative Biology, volume 51, number 1, pp. 81–90
doi:10.1093/icb/icr009
Advanced Access publication May 15, 2011
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contribute greatly to the dispersal of sessile or sed-
entary benthic animals and may increase genetic
exchange among populations (Bohonak 1999; but
see Hart and Marko 2010).
Plasticity in stage at hatching could affect duration
as a planktonic larva and thus the potential for dis-
persal. The extent of this plasticity should be limited
by other life-history traits such as the kind of paren-
tal protection and the type of larval development of
the species. For example, for many marine animals
duration as a planktonic larva is much longer than
the time the larvae are in broods or egg masses. In
such cases, plasticity in stage at hatching may mod-
erate risks but would have relatively little effect on
duration of planktonic development. In the extreme
form of planktonic development, also common,
gametes or zygotes are released into the plankton.
Embryos that develop singly in the plankton hatch
at early stages, often as a blastula or gastrula. In this
study, we first describe two cases in which plasticity
in stage at hatching can greatly affect the duration
from hatching as a swimming larva to the stage at
which the larva becomes competent for settlement
and metamorphosis. We then discuss the kinds of
life histories in which plasticity in hatching might
have a similarly great effect on the duration of obli-
gate larval swimming. We also hypothesize that plas-
ticity in stage at hatching is extremely limited when
embryos develop singly in the plankton.
Hatching plasticity that affects
duration as a planktonic larva
When embryos are protected in benthic broods or
egg masses, they may be released either at a larval
stage that feeds and grows in the plankton or near
the stage of metamorphic competence. When larvae
do not need to feed and grow, the period of swim-
ming before metamorphic competence is usually
less than a day, sometimes seconds or minutes
(Strathmann 2007). In contrast, when larvae feed
and grow in the plankton, this precompetent plank-
tonic period can be weeks or months (Grantham
et al. 2003; Strathmann and Strathmann 2007;
Shanks 2009). Plasticity in hatching can, therefore,
have the greatest proportionate effect on the duration
of the planktonic stage when hatching near compe-
tence is an option. Then, if the period of swimming
before metamorphic competence were to be increased
by only a few days, the duration of obligate swim-
ming would be increased many fold.
Advantages of obligate dispersal by larvae, beyond
that achieved during a brief planktonic period, are
not evident (Strathmann et al. 2002a; Strathmann
2007), and most estimated mortality rates for benthic
broods or egg masses are lower than those for soli-
tary planktonic larvae (Strathmann 1985, 2007;
Rumrill 1990). It would seem advantageous for
larvae in a brood or benthic egg mass to delay hatch-
ing until they are near the stage of metamorphic
competence. However, when a particular egg mass
or brooding parent is attacked, stressed, or otherwise
disturbed, the probability of survival at the seafloor
is then greatly reduced and the plankton can then be
a relatively better option. If attacks, disturbance, or
stresses are frequent, then plasticity in stage at hatch-
ing may evolve. If hatching early in response to a
stimulus indicating risk is to be advantageous, the
capacity to swim should develop well before meta-
morphic competence develops. We therefore expect
plasticity in stage at hatching to evolve when the
relative costs and benefits of benthic and pelagic de-
velopment vary and there are stimuli associated with
those changes in costs and benefits.
Plasticity in hatching from a gelatinous egg mass
of a nudibranch gastropod
Veliger larvae of the aeolid nudibranch Phestilla
sibogae BERGH, 1874, hatch from their individual cap-
sules if the encapsulated embryos are scattered from
a torn gelatinous egg ribbon (Miller and Hadfield
1986; Hadfield et al. 2000; Strathmann et al. 2010).
The tougher outer envelope of the egg ribbon en-
closes a softer gel. Each veliger is in a fluid-filled
capsule surrounded by gel (Fig. 1). A portunid
crab was seen to tear a ribbon and scatter capsules
with embryos in much the same way that a biologist
tears a ribbon to induce hatching (Strathmann et al.
2010). Egg ribbons disappeared when placed with a
portunid and a xanthid crab but not when these
predators were absent. Thus attacks by crabs can
occur, with scattering of embryos in capsules.
Unlike some nudibranchs that are colorful and de-
fended, adults of P. sibogae are cryptic in coloration
and vulnerable to a variety of predators (Gochfeld
and Aeby 1997). The egg ribbons appear to be sim-
ilarly vulnerable, and plasticity in hatching could
adjust the risks of benthic and planktonic
development.
Hatching occurred as early as 4 days after egg
deposition at 23 to 258C when ribbons were torn
(Strathmann et al. 2010). The foot of the early hatch-
lings lacked a propodium (Fig. 1). The early hatch-
lings swam but were not near metamorphic
competence and were not yet able to settle. At
268C, metamorphic competence increases from a
low percent on Days 7 to 8 to increased numbers
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at Days 9 to 10 (Miller and Hadfield 1986).
Undisturbed egg masses hatched as late as Days 9
to 11 at 23 to 258C or as early as 8 days in a trial
at 268C. Late hatchlings had a well-developed pro-
podium (Fig. 1) and were at or near metamorphic
competence. The stimulus for settlement and meta-
morphosis is a water-soluble substance from the
coral prey (Harris 1975; Hadfield 1977; Hadfield
and Pennington 1990; Koehl and Hadfield 2004).
When veligers were removed from undisturbed
hatching egg masses, 20–100% metamorphosed
within a day of exposure to the inducer from the
coral (Strathmann et al. 2010). A few metamor-
phosed nudibranchs were found within hatching
egg masses.
The veligers can, therefore, hatch so late that many
are competent to metamorphose or so early that the
obligate planktonic period can last four or more
days. The period of encapsulation can be reduced
by at least 50% and the precompetent planktonic
period can be increased by 4500%. Scattering of en-
capsulated veligers from the egg ribbon means that
the benthic habitat has become dangerous.
Swimming is then presumably the safer option. In
the absence of disturbance, the veligers hatch when
ready or nearly ready to settle. Duration of precom-
petent swimming by larvae depends on an immediate
indication of risk: scattering of capsules from the egg
ribbon. Obligate dispersal increases when a ribbon is
attacked.
Plasticity in hatching from brooded egg capsules
of a spionid annelid
In the polychaete Boccardia proboscidea HARTMAN,
1940, females deposit capsules with embryos inside
their sand tubes in the intertidal zone. B. proboscidea
is a poecilogonous species: it produces more than
one type of larva (Giard, 1905). Some females pro-
duce two kinds of larvae, planktotrophic larvae
(feeding on the plankton) and adelphophagic larvae
(feeding on nurse eggs and developing siblings),
as well as nurse eggs (Fig. 2A), while other females
produce capsules with only planktotrophic larvae
(Hartman 1941; Gibson et al. 1999). King (1976)
reported that females actively brood their embryos
by cleaning and ventilating the capsules and that
larvae do not liberate themselves when hatching.
Potentially, therefore, females brooding mixed larval
types can decide when to liberate embryos from the
capsules according to environmental conditions and
thereby modify the number and proportion of larval
types and the developmental stage of the liberated
larvae. With early hatching, adelphophages and
planktivores are morphologically indistinguishable
and have an estimated minimum planktonic larval
duration of 2 weeks. With late hatching few plank-
tivorous larvae survive, but those that do survive will
still spend 2 weeks in the plankton because their
development was arrested. In contrast, adelpho-
phages will hatch in a more advanced developmental
stage and their planktonic period will be greatly re-
duced. At its extreme, late hatching will produce no
planktivorous larvae due to sibling cannibalism, and
adelphophages will hatch as metamorphosed juve-
niles so that the longest planktonic larval duration
for that brood is close to zero. A cost of producing
larger offspring by brooding longer would be fewer
broods.
We characterized the brooding behavior of females
with mixed reproductive strategy (producing plank-
totrophs, adelphophages, and nurse eggs) and used
video recordings to document their opening of cap-
sules. We also observed the effect of temperature
experienced by the brooding mother during the
time at which hatching occurred and compared
those times with previous observations on rates of
development. B. proboscidea was collected at False
Bay, Washington, USA. All females were acclimated
in environmental chambers for at least 1 month
before use in experiments. We modified the rearing
Fig. 1 Egg capsules and veligers of Phestilla sibogae. Top: portion
of egg ribbon; scale line ¼200 mm. Bottom left: earliest stage at
hatching; 3 to 4 days after deposition of the eggs; no propodial
bulge on developing foot; scale bar ¼100 mm. Bottom right:
hatching at a later stage; with propodial bulge; scale
bar ¼100 mm.
Hatching plasticity and larval dispersal 83
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methods from those of Gibson et al. (1999). Worms
grew and reproduced in 50-ml glass beakers contain-
ing filtered seawater and sediment; each beaker was
kept inside a 300 cc container of aerated seawater.
Females formed tubes against the bottom of the
glass beakers, and their capsules were visible inside
these tubes (Fig. 2B). Worms were kept at 16:8 L/D
cycle at 208C and fed with a 50:50 mix of Gerber
baby-food cereal and ZoPlan (Advanced Zooplanton
Diet).
Females actively brooded their capsules, frequently
moving their palps around the capsules and remov-
ing foreign particles from the tube. They regularly
mouthed each capsule, presumably cleaning the sur-
face. During most of the brooding period, females
ventilated the capsules by oscillatory movements of
their bodies, increasing frequency at higher
temperatures.
Each of three females that were filmed during the
complete brooding period induced hatching by tear-
ing each capsule until it opened and then expelled
the contents by oscillating her body (Fig. 3).
Opening all the capsules in a clutch took 20 min.
Two of the three females expelled the contents to-
ward her tail; one toward her head. (Tubes of
B. proboscidea are U-shaped and have two openings.)
Liberation of larvae sometimes occurred when many
nurse eggs still remained and also when no nurse
eggs remained.
We assigned 50 females to four different temper-
ature treatments: 11 at 118C, 19 at 208C, 7 at 258C,
and 13 at 308C. They were kept at 208C until they
initiated broods and then randomly assigned to one
of the four temperature treatments until capsules
were hatched. Females were checked daily for liber-
ation of embryos. After the larvae hatched, we
checked for presence of larvae in the water or settle-
ment of juveniles, and we kept females for another
complete brooding period to ensure that they repro-
duced normally at 208C.
Females brooded much longer at lower tempera-
tures, with times ranging from an average of 26 days
(SD ¼2.86) at 118C to an average of 8.9 days
(SD ¼1.5) at 308C (Fig. 4). In addition, the vari-
ance in duration of brooding increased at higher
temperatures (variance: 118C¼8.2; 208C¼17.4;
258C¼60.3), although at 308C, a temperature
lethal to the embryos, the variance in duration of
brooding was 2.2. Increased variance in duration of
brooding at higher temperatures implies a greater
variation in the larval stage at which hatching
occurs within a population. Homogeneity of variance
Fig. 2 (A) Capsule of Boccardia proboscidea with a mixed reproductive strategy. (B) Single frame of video recording of capsules
inside a female’s tube, with female behind the capsules. The other worm present in the beaker is also visible. (Cand D) Swimming
adelphophagic and planktotrophic siblings liberated by the mother under laboratory conditions. (E) Settled juvenile within a day
of being liberated by the mother.
84 F. X. Oyarzun and R. R. Strathmann
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for broods at 11, 20, and 258C was rejected: Levene
stat ¼5.70, df1 ¼2, df2 ¼34, P¼0.007. Qualitative
observations on the stage at which larvae were liber-
ated (e.g. larvae swimming, larvae swimming with
two distinct size classes, juveniles settled) demon-
strated much variation in their stages at hatching,
with instances in which both planktotrophs and adel-
phophages were released as swimmers (Fig. 2C
and D). Sometimes juveniles settled within the
same day they were liberated (Fig. 2E). The earlier
stage at hatching at lower temperature was indicated
by the development rates of individual larvae grown
in Eppendorf tubes from an early stage (three seti-
gers) to metamorphosis at 118and 208C (Oyarzun
2010) (Fig. 4). If this is the case, females are not
simply adjusting the brooding period to match the
developmental state of the larvae, but are changing
the size at which larvae are hatched and consequently
the amount of cannibalism and the potential for dis-
persal. This result resembles the finding that sea slugs
from the genus Alderia produce more planktotrophic
larvae in winter and more lecithotrophic larvae in
summer, possibly as an adaptation to seasonal con-
ditions (Ellingson and Krug 2006). In the case of
B. proboscidea, an effect of temperature on stage at
hatching may be associated with costs of brooding or
other correlates of temperature.
At 308C, females brooded their capsules for nine
days even though embryos were not developing (pre-
sumably due to temperature stress). Those females
stopped brooding only when capsules started to de-
compose, which suggests that females are not aware
of the developmental state of their offspring. A fe-
male’s decision to hatch capsules may therefore be a
response to her own condition rather than a re-
sponse to her offsprings’ needs. When these females
were returned to a temperature of 208C, they laid
Fig. 3 Single frame of video recording and schematic represen-
tation of the opening of a capsule by a female Boccardia
proboscidea. The female is shown pulling one capsule. One of the
capsules has a stronger orange coloration due to the presence of
many nurse eggs. In the video recording the female opened
capsules by pulling each individually until the capsule ruptured
and the content was liberated. Larvae were expelled from the
tube by waving motions of the female’s body.
Fig. 4 Results of the effect of temperature on the length of
brooding time of Boccardia proboscidea.(A) Data from females
with mixed reproductive strategy that were placed at different
temperatures after laying their capsules. (B) The larval growth of
adelphophagic larvae in previous experiments (Oyarzun, 2010).
The upper and lower limits of the adelphophagic larvae at 208C
reflected growth rates of 1 and 1.5 setigers/day, which are the
growth rates at two different concentrations of nurse eggs
(Oyarzun, 2010). Dotted lines show the average time that
females brooded at that temperature.
Hatching plasticity and larval dispersal 85
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capsules that developed normally. In all other treat-
ments embryos developed normally.
At 11, 20, and 258C, 73% of females liberated at
least some swimming larvae (Fig. 2C and D), indi-
cating that although the number of planktotrophs is
not high in this mixed reproductive strategy, dis-
persal of some larvae is common. Releasing larvae
of different sizes potentially ensures that a percentage
of a brood will disperse. Females brooding mixed
planktotrophs, adelphophages, and nurse eggs will
never produce as many planktotrophs as will females
that produce only planktotrophs, but their few
planktotrophic offspring may increase their repro-
ductive success because of catastrophic events.
Are large effects on planktonic larval duration
common?
Our two examples indicate that plasticity in hatching
can (1) occur for benthic broods and egg masses and
(2) greatly extend the length of time the larvae swim
before they become competent to settle and meta-
morphose. Some features of our nudibranch and
spionid examples are not widespread. Phestilla
sibogae is a facultative planktotroph. Boccardia
proboscidea has a peculiar form of poecilogony.
Nevertheless, there are many species that develop
almost to metamorphic competence while brooded
or encapsulated. In such cases, plasticity in hatching,
if it occurs, could greatly extend the duration of
swimming as a precompetent larva (Fig. 5).
How widespread, then, is hatching plasticity that
greatly extends planktonic larval durations? Many
animals release swimming larvae at or near meta-
morphic competence. That mode of development
occurs in many marine molluscs, annelids, bryozo-
ans, cnidarians, sponges, and other phyla
(Strathmann 1987, 2007). Another prerequisite, com-
monly met, is that the protected offspring develop
the capacity for swimming well before they would
hatch or be released from an undisturbed egg mass
or brood. Embryos that develop cilia commonly
move within their capsules or surrounding egg jelly
before they hatch. Yet another prerequisite is that the
properties of the egg mass permit early hatching.
Many gelatinous egg masses swell during develop-
ment (Lee and Strathmann 1998), with the gel be-
coming less firm. Walls of many egg capsules become
thinner during development (Kress 1971; Cronin and
Seymour 2000; Brante 2006). At early stages of de-
velopment, protective envelopes are stronger, and
Fig. 5 Diagrams of predicted scope for plasticity in stage or age at hatching in life histories of marine invertebrates. The proportionate
extension of time as a precompetent swimming larva can be greatest when larvae can be released at or near metamorphic compe-
tence. Plasticity in hatching cannot affect duration of larval swimming if capacity for such swimming has been lost (far left). For most
animals that release gametes or zygotes into the plankton, there is less scope for plasticity in stage at hatching because hatching occurs
soon after capacity to swim develops (far right).
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larvae may be unable to escape them, even if they are
motile and capable of receiving a stimulus that indi-
cates risk.
When the developing larva controls hatching,
rather than a brooding mother, there must be a stim-
ulus that it can detect. Chemical or mechanical stim-
uli are a possibility, as described for amphibians
(Gomez-Metre et al. 2008) and for other examples
in this symposium. For Phestilla sibogae, the stimulus
for hatching is unknown but a chemical stimulus
from a predator is not required. The scattering of
encapsulated veligers from the egg mass might
either provide a stimulus for hatching or release
them from an inhibitor of hatching.
When the mother controls hatching, she may be
influenced by costs and benefits in addition to those
from predators or physical disturbance. In Boccardia
proboscidea, for example, costs of prolonged brood-
ing could include fewer broods in a reproductive
season. After the experiment on brood duration, fe-
males reproduced again, even without the presence
of a male, suggesting an ability to store sperm for
long periods. Frequently, females deposited a new set
of capsules in the same place they had deposited the
previous one and during the same day they had lib-
erated their previous brood. Reducing the length of
the brooding period could increase the number of
clutches produced in a reproductive season.
There is a potential conflict between mother and
offspring (Kamel et al. 2010). The mother may ben-
efit from dispersing some offspring by inducing early
hatching because the dispersal could provide a hedge
against a future catastrophe for the local population;
however, for each sibling in a clutch, the probability
of survival to reproduction can be greater if the in-
dividual is retained to an advanced stage of develop-
ment and then settles near the parent in habitat of
proven quality. Structure of the capsule and the
mode of hatching can affect intrafamilial conflicts
and hatching plasticity. Reproduction and develop-
ment of the southern hemispheric species Boccardia
wellingtonensis resembles that of B. proboscidea but
differs in that mothers produce strings of capsules
that are externally connected (Kamel et al. 2010).
The walls that separate one capsule from the next
are thin and usually break during development, cre-
ating connections among capsules that allow adel-
phophages to move to adjacent capsules and ingest
the remaining nurse eggs and planktotrophs. These
connections thus provide greater scope for sibling
cannibalism. In this species, mothers have not been
observed to open egg capsules. The embryos do not
depend on the mother for hatching because the
walls of the capsules become thinner over time
(Oyarzun, unpublished observation). If indeed moth-
ers do not open capsules, then there is less maternal
control of size, number, and dispersal of offspring
than in B. proboscidea;B. wellingtonensis potentially
has both greater scope for sibling conflict and de-
creased maternal control over the embryos once cap-
sules have been deposited. Differences among
Boccardia spp. in types of capsules, types of larvae,
and processes of hatching provide an opportunity to
explore possible relationships between differing reso-
lutions of family conflicts, plasticity in hatching, and
its effect on planktonic larval durations.
Hatching plasticity without a large
effect on the planktonic larval duration
In species without a planktonic larval stage, there is
scope for plasticity in age at hatching (Miner et al.
2010), but hatchlings will be non-swimming (Fig. 5)
unless the animals have retained an encapsulated or
brooded stage with a capacity for swimming. The
possibilities for resurrecting a swimming stage
through hatching plasticity differ among clades.
Some gastropods that are known to hatch as crawl-
ing juveniles have retained a velum with ciliary bands
much like those of planktonic veligers, whereas some
have only a vestige of velar ciliation (Collin et al.
2007).
In species in which hatching is followed by a long
period during which larvae feed and grow, plasticity
in hatching could extend the duration of the swim-
ming stage by only a small relative amount (Fig. 5).
That is because the period during which larvae swim
is long compared to any increased duration from
earlier hatching. Many gastropods, annelids, and
crustaceans have protection of embryos followed by
weeks of precompetent larval growth and develop-
ment in the plankton. Earlier hatching would have
a small effect on duration of the precompetent
planktonic stage.
Barnacles offer an example of hatching plasticity
that appears to have little effect on duration of the
stage at which larvae swim. In Semibalanus
balanoides, hatching occurs when planktonic food
increases in the spring, when the brooding parent
produces a chemical stimulus (Crisp 1956; Barnes
1957; Crisp and Spencer 1968; Clare 1997, 1999;
Vogan et al. 2003). For a particular location and
year, brooding is initiated at widely varying times
during the winter; nauplius larvae are released over
a much shorter period in the spring. To our knowl-
edge, timing of hatching does not change the
number of precompetent larval instars from the six
naupliar stages, and effects of age at hatching on
Hatching plasticity and larval dispersal 87
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duration of nauplius stages have not been noted. In
species of barnacles that have multiple broods per
year, hatching of the first brood may be synchro-
nized by an environmental cue whereas those of later
hatchings are not. For example, in Balanus glandula,
as in S. balanoides, initiation of broods during the
winter is over a long period and release of nauplii
more nearly synchronous, but later in the season;
both initiation and release of broods are asynchro-
nous, and broods do not have long delays in hatch-
ing (E. S. Branscomb, R. R. Strathmann, and
K. Vedder, unpublished data).
It is possible that some kinds of predation can also
stimulate hatching of broods of barnacles. Breaking
up the brood mass is often sufficient to induce
hatching of nauplii (Barnes 1957; Crisp and
Spencer 1968). We expect that a survey of brooding
marine invertebrates will reveal similar examples of
early hatching induced by removing or tearing a
brood mass.
Planktonic development that limits
plasticity in hatching
An entirely planktonic development as a solitary
embryo limits the scope for plasticity in hatching
(Fig. 5). Many marine invertebrates spawn gametes
or zygotes into the plankton. Planktonic embryos
commonly hatch at earlier stages than benthic em-
bryos (Staver and Strathmann 2002; Strathmann
et al. 2002b). Many planktonic embryos hatch as
early as the blastula or gastrula stage of development.
Some sipunculans and other annelids do not hatch
from the envelope; instead cilia protrude through
holes in the egg’s envelope, and it becomes a cover-
ing for the swimming larva (Rice 1973). For animals
that release eggs or zygotes into the plankton but
first swim with muscles, hatching occurs at more
advanced stages, as with tunicate tadpoles and crus-
tacean nauplii. These larvae have more sensory
equipment than that of a blastula or gastrula, but
it is possible that hatching is at the earliest stage at
which swimming is effective. Kiørboe and Sabatini
(1994) observed that copepods with single planktonic
embryos hatch as less differentiated nauplii than
those with broods carried by the mother. One hy-
pothesis is that selection on single planktonic embry-
os has advanced hatching to the earliest stage at
which locomotion is effective. If that is correct,
there might be little advantage in plasticity that pro-
duced still earlier hatching.
For animals that hatch at blastula and gastrula
stages, nervous systems, and sensory organs have
not developed by the time of hatching. However,
hatching is commonly by release of a hatching
enzyme, and if individual cells of the blastulae or
gastrulae are capable of detecting a stimulus, plastic-
ity in hatching in response to the stimulus might
evolve. Under what circumstances might timing of
the change from a protective envelope to swimming
increase safety? The protection afforded by swim-
ming as a blastula as opposed to remaining within
a protective envelope is unclear. Swimming blastulae
are more vulnerable to some (but not all) planktonic
predators than are unhatched blastulae (McDonald
2007). We know of no tests for delay of hatching
in the presence of predators, such as planktonic co-
pepods. A more general advantage of swimming may
be avoidance of the seafloor, where suspension feed-
ers are often abundant. For plasticity that advances
hatching of single planktonic embryos, one might
look for stimuli that are stronger near the seafloor
than higher in the water column. For stimuli that
delay hatching, one might look for stimuli that indi-
cate risks in the water column.
We expect plasticity in hatching to be widespread
among marine invertebrates, but release of gametes
or zygotes to the plankton may preclude or limit that
plasticity, while encapsulation or brooding nearly to
metamorphic competence may maximize the effect
of hatching plasticity on duration as a precompetent
planktonic larva (Fig. 5).
Acknowledgments
We thank the staff of the Friday Harbor
Laboratories, the Kewalo Marine Laboratory, the
Universidad Austral de Chile, and the officers and
staff of SICB for their help with this project.
Suggestions or assistance from K. Andrilenas,
M. J. Bravo, O. Chaparro, M. Groom, M. G.
Hadfield, J. Havenhand, K. L. Martin, B. G. Miner,
B. Pernet, J. Purdy, G. Ruiz-Jones, M. F. Strathmann,
B. J. Swalla, and K. Warkentin are greatly
appreciated.
Funding
The National Science Foundation (OCE0623102,
IOS-136833, IOS-1036933, HRD-0820175); the
Friday Harbor Laboratories of the University of
Washington; the Society for Integrative and
Comparative Biology (SICB) and its divisions
Animal Behavior (DAB), Comparative Physiology
and Behavior (DCPB), Developmental and Cellular
Biology (DDCB), Evolutionary Developmental
Biology (DEDB), and Invertebrate Zoology (DIZ).
88 F. X. Oyarzun and R. R. Strathmann
at University of Washington on September 27, 2011icb.oxfordjournals.orgDownloaded from
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... However, biparental care is extremely rare in animals outside of birds (Kokko and Jennions 2008); a lineage accounting for just~0.6% of described metazoans (Zhang 2013). In contrast, uniparental care of embryos is the most widespread and labile form of parental care in the animal kingdom, occurring in numerous phyla (e.g., annelids [Reish 1957, Kutschera and Wirtz 2001, Fletcher et al. 2009, Oyarzun and Strathmann 2011; arthropods [Tallamy 1984[Tallamy , 2001; bryozoans [Ostrovsky 2008a,b]; chordates [Gross and Sargent 1985, Shine 1988, Furness and Capellini 2019; cnidarians [Larson 2017]; echinoderms [Gillespie and McClintock 2007]; molluscs [Baur 1994, Kamel andGrosberg 2012]; Platyhelminthes [Rawlinson et al. 2008]; poriferans [Szmant 1986, Whalan et al. 2007). Understanding family interactions on a broad scale will require elucidating patterns and mechanisms of change in uniparental care, about which we still know comparatively little. ...
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The veliger larvae of the coral-eating nudibranch mollusc Phestilla sibogae have provided an excellent model for the study of chemical-induction of metamorphosis. They metamorphose only in response to a water-soluble metabolite that escapes from the coral prey of the adult nudibranchs. Metamorphosis, occurring 18-20 h after larvae are exposed to coral, is decisive: larvae attach to a substratum, shed their velar-swimming organs, shell and operculum, and undergo major morphological reorganization. Extraction and HPLC purification of the coral product show it to be a small (<500 MW), polar, water-soluble molecule that is probably effective in inducing metamorphosis at concentrations of 10-10 M or less. The rapidness and cascade nature of metamorphic induction, coupled with the partial or complete inductive action of potassium ions, choline and epinephrine, point to the larval nervous system in the detection of the coral product and the internal mediation of metamorphosis. Problems associated with the isolation and concentration of the coral inducer hamper investigations of the larval receptor and its mode of action.
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Prior to the 1930s, it was a generally accepted notion that larvae of benthic marine invertebrates were, in the timing of their metamosphosis, at the mercy of chance. If the ocean’s currents carried them over substrata suitable for adult life when the time for metamorphosis arrived, they survived; if the substrate were not suitable, the larvae perished. Beginning with observations of Mortensen1 and Day and Wilson2, students of marine ecology began to see that the situation relative to larval settling was more controlled, that larvae could execute a “choice” of substratum. It was additionally recorded that larvae could actually delay metamorphosis until suitable substrata were found3.
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1. The complete life cycles of two coral-eating aeolid nudibranchs, Phestilla melanobranchia Bergh, 1874 and Phestilla sibogae Bergh, 1905, are described. Information on their life histories includes developmental stages and timing, duration of the veliger stage, veliger behavior, factors necessary for settling and metamorphosis, and adult growth rates, fecundity and longevity. The life cycles of the two Phestilla are similar and their physical and behavioral differences are related to the characteristics of their respective coral prey. 2. P. melanobranchia has planktotrophic development, is negatively phototactic when ready to settle, requires close proximity to living dendrophylliid coral tissue for metamorphosis and has a generation time from egg to egg of 60 days. The dendrophylliid corals on which P. melanobranchia feeds are small, patchy and photonegative in distribution. 3. P. sibogae which has now been under serial cultivation for four years, has lecithotrophic development, is positively phototactic when ready to settle, requires only a chemical factor from living Porites tissue for metamorphosing and has a generation time of 38 days. The Porites corals which P. sibogae feeds on are large, very common and photopositive in distribution. 4. Differences in predation pressure and prey tissue utilization efficiency are proposed as factors influencing the evolution of a significantly faster generation time in Phestilla sibogae than in the closely related P. melanobranchia.
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