Download Larval Release Rhythms of Decapod Crustaceans

BULLETIN OF MARINE SCIENCE, 41(2): 165-176, 1987
LARVAL RELEASE RHYTHMS OF DECAPOD CRUSTACEANS:
AN OVERVIEW
Richard
B. Forward, Jr.
ABSTRACT
Decapod crustaceans release larvae rhythmically in relation to lunar, light-dark and tidal
cycles. Rhythms occur in a wide range of species. Those rhythms related to lunar phase are
usually semilunar with larval release mainly occurring at the time of largest amplitude nocturnal ebb tides, which usually correspond to spring tides at the new and full moon. Semilunar
rhythms are most common among littoral and supralittoral species and depend upon when
in the lunar month the female lays her eggs and the length of embryo development. The
specific time of larvae release depends upon the interaction of LD and tidal cycles. Release
relative to the LD cycle occurs most often in the first half of the night. If timing is related to
tides, releases always occur around the time of high tide. Rhythms are under endogenous
control. The known zeitgeber for entrainment of lunar, die1 and tidal rhythms are cycles in
moonlight, LD, and salinity, respectively. Other untested environmental cycles may also be
used for entrainment. The site of endogenous control among brachyurans probably varies
with adult habitat. For species living in high littoral and supralittoral areas, the "clock" may
reside in the female while in the sublittoral it resides in either the female or the developing
embryos depending upon the species. The functional significance of the timing of larval
release for each rhythm is usually related to survival of the adult female and her larvae.
Among decapod crustaceans, larval release does not occur randomly, but rather
is precisely timed with respect to cycles in environmental factors. For most species
fertilized eggs are attached to the pleopods located on the ventral side of the
female's abdomen and are carried for a period of days to months before the larvae
are released. At the time of larval release the female usually elevates herself on
her walking legs and vigorously pumps her abdomen back and forth. If the eggs
are ready to hatch, each pump results in the release oflarvae. Larval release occurs
quickly, lasting only a few minutes (DeCoursey, 1979; Ennis, 1973). In the last
few years there have been a number of studies of the timing of larval release as
related to environmental cycles, endogenous control and functional significance
for the female and her larvae. This paper will present an overview of these recent
studies.
TYPES OF LARVAL RELEASE RHYTHMS
The timing of larval release can be related to lunar phase, time of day andlor
phase of the tide. Rhythms have been determined by observing female behavior
and embryo development in the field, larval abundance in the water column and
the specific times females release their larvae in the laboratory. Comparisons
among these measurements indicate that laboratory data provide reasonable estimates of release time in the field (Christy, 1982).
Population rhythms related to the lunar cycle are usually semilunar (14.5-day
cycle) with larvae most often released around the time of spring tides at the new
and full moon (Table 1). This pattern, however, may be poorly developed at the
beginning and end of the breeding season (Wheeler, 1978; Dollard, 1980; Christy,
1982). Only one species (Gecarcinus lateralis from Bermuda) shows a lunar rhythm
with release occurring 4 to 5 nights after the full moon (Wolcott and Wolcott,
1982). At another location (Columbia), however, this species shows a semilunar
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Table I. Larval releases relative to lunar cycle. Field indicates that the method for determining larval
release times was to observe female behavior, egg maturation or abundance of stage I zoeae in the
field. Lab indicates larval release was monitored in the laboratory. Species are listed in order of
supralittoral to sublittoral species
Species
Habitat
Luna rhythm release at full moon
Geearcinus lateralis
supralittoral
Method
field
Semilunar rhythm release at new and full moon
Araetus pisoni
supralittoral
field
Cardisoma guamhumi
supralittoral
field
Geearcinus lateralis
supralittoral
field
Sesarma intermedium
supralittoral
field
Sesarma haematoeheir
supralittoral
lab
field
littoral
Panopeus herbstii
field
littoral
Pinnixa ehaetoperana
field
littoral
field
Sesarma cinereum
Sesarma retieu/atum
Uea minax
Uea pugi/ator
littoral
littoral
littoral
field
lab
field
Ueapugnax
Uea sp.
littoral
littoral
lab
field
Cal/ineetes areuatus
sublittoral
field
Semilunar rhythm but not release at new and full
Cataleplodius taboganus
littoral
lab
Uea pugi/ator
littoral
field
Xanthodius sternberghii
littoral
lab
No semilunar rhythm
Sesarma dehaani
Petrolisthes armatus
Eurypanopeus planus
Cal/ineetes sapidus
Neopanopeus spp.
Pinnixa ehaetopterana
Pinnotheres ostreum
Pinnotheres maeulatum
Rhithropanopeus harrisii
supralittoral
littoral
littoral
sublittoral
sublittoral
sublittoral
sublittoral
sublittoral
sublittoral
field
lab
lab
field
field
field
field
field
lab
Reference
Wolcott & Wolcott, 1982
Warner, 1967
Gilford, 1962; Henning, 1975
Klaassen, 1975
Saigusa and Hidaka, 1978; Saigusa, 1981
Saigusa, 1980
Saigusa and Hidaka, 1978; Saigusa, 1981; 1982
Christy and Stancyk, 1982; Salmon et aI., 1986
Christy and Stancyk, 1982
Seiple, 1979; Dollard, 1980; Christy and Stancyk, 1982
Seiple, 1979; Christy and Stancyk, 1982
Christy, 1982
DeCoursey, 1982; Christy, 1982; Salmon and
Hyatt, 1983
Wheeler, 1978; Christy, 1982
Christy and Stancyk, 1982; Salmon and Hyatt,
1982; DeCoursey, 1983; Salmon et aI., 1986
DeVries et aI., 1983
moon
Christy, 1986
Christy, 1978
Christy, 1986
Saigusa,
Christy,
Christy,
Salmon
Salmon
Salmon
Salmon
Salmon
Forward
1981
1986
1986
et aI., 1986
et aI., 1986
et aI., 1986
et aI., 1986
et aI., 1986
et aI., 1982
rhythm (Klaassen, 1975) with more releases occurring at the full moon than the
new moon. Similarly, among other species having semilunar rhythms, the number
of the releases by a population may vary with lunar phase. For example, populations of the crabs Cardisoma guanhumi (Gifford, 1962), Sesarma haematocheir
(Saigusa and Hidaka, 1978; Saigusa, 1982) and Sesarma intermedium (Saigusa
and Hidaka, 1978) also release more often at the time of full moon than new
moon.
There are three species (Cataleptodius taboganus, Ucapugilator and Xanthodine
sternberghii) that show semilunar periodicities in which releases occur near the
days of the quarter phases of the moon (Table 1; Christy, 1978; 1986). These
findings led Christy (1982) to propose that semilunar rhythms of larval release
are not related to lunar phase but are cued to the time in the lunar cycle of the
FORWARD:
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LARVAL RELEASE RHYTHMS
Table 2. Number of species from different habitats showing each type of rhythm in larval release
Semilunar (from Table I)
Supralittoral
Littoral
Sublittoral
Die! (from Table 3)
Tidal (from Table 4)
Not present
Present
Not present
Present
Not present
5
I
2
6
4
4
5
0
10
4
7
I
0
0
0
Present
I
I
0
largest amplitude nocturnal ebb tides. For these three species the time of larval
release and the largest amplitude tides were similarly shifted from the syzygies.
Semilunar rhythms in larval release are widely distributed among littoral and
supralittoral species (Tables 1 and 2). Sublittoral species usually lack these rhythms.
This trend is further supported by studies of Pinnixa chaetopterana. When adults
occcur in the littoral, a semilunar rhythm is observed (Christy and Stancyk, 1982)
but this rhythm is absent when they occur in the sublittoral (Salmon et al., 1986).
This difference among species cannot be related to the presence or absence of the
semilunar environmental cycles because spring tides can also be sensed in the
shallow sublittoral environment. Thus a semilunar rhythm may be important for
successful larval release among littoral and supralittoral species but not among
sublittoral species.
Rhythms in larval release are also related to the light-dark cycle. These rhythms
again occur in a wide range of species. In addition to those species shown in Table
3, Knudsen (1960) lists four littoral xanthid species that release at night. These
are absent from the table because the precise time of the release is not reported.
In most other cases, larval release occurs in the first few hours of the night phase
(Table 3). This timing is not related to adult habitat, since it is common among
species living in sublittoral, littoral and supralittoral areas (Table 2).
Tidal rhythms in larval release occur among supralittoral, littoral and one
sublittoral estuarine species (Table 2). In these cases releases always occur around
the time of high tide (Table 4). There is no report of a temporal correlation with
low tide. Nevertheless, specific release times within and between species are variable and can occur before, at or after the time of high tide. There are two possible
reasons for the inconsistent relationship to high tide. First, release times are
frequently related to both the LD and tidal cycle (i.e., high tides at night). Thus
if high tide occurs before sunset, releases will occur at the beginning of the night
phase and after high tide. But when some days later, the time of high tide occurs
shortly after sunset, release times correspond to the tide times (Saigusa and Hidaka,
1978; Saigusa, 1981; Bergin, 1981; Forward et al., 1986). A second reason for the
inconsistent relationship is that precise measurements of release times are usually
made in the laboratory. As pointed out by Salmon et al. (1986), larval release is
more tightly synchronized in the field than in the laboratory.
Thus timing can be related to semilunar, diel, and tidal cycles. If all three cycles
are important then most commonly larvae are released at the new and full moon,
in the first few hours of the night phase, and around the time of high tide.
Exceptions to these times are rarely that releases occur at other phases in lunar,
diel or tidal cycles but rather that release times are simply not related to a particular
cycle. For example if release times are not related to lunar or tidal cycles, then
they occur at any time in the lunar month at the beginning of the night phase
(Ennis, 1973; Branford, 1978; Moller and Branford, 1979; Forward et al., 1982).
Even though the above patterns are observed, there can be flexibility in the
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1987
Table 3. Larval release relative to the light dark cycle. "Night" indicates releases occurred throughout
the night while "first half" indicates releases were in the first half of the night phase. Other terms are
as in Table I.
Species
Release during the night
Gecarcinus lateralis
Sesarma dehaani
Sesarma haematocheir
(Izu peninsula population)
Sesarma haematocheir
(Kasaoka population)
Sesarma intermedium
Habitat
Release timer
Method
Reference
supra littoral
supralittoral
supralittoral
first half
first half
first half
field
field
field
Wolcott and Wolcott, 1982
Saigusa, 1981
Saigusa and Hidaka, 1978
Saigusa, 1981
Saigusa, 1981
supralittoral
night
field
supra littoral
first half
field
Cataleplodius taboganus
Petrolisthes armatus
Uca pugilator
littoral
littoral
littoral
first half
night (mostly)
first half
field
field
lab
Xanthodius sternberghii
Homarus american us
Homarus gammarus
littoral
sublittoral
sublittoral
first half
first half
first half
field
lab
lab
Nephrops norwegicus
Rhithropanopeus harrisii
sublittoral
sublittoral
first half
first half
lab
lab
Release at beginning of light phase
Jasus edwardsii
sublittoral
sunrise
lab &
field
MacDiarmid,
Release not related to LD cycle
Eurypanopeus plannus
sublittoral
day & night
lab &
field
Christy, 1986
Saigusa and Hidaka, 1978
Saigusa, 1981
Christy, 1986
Christy, 1986
Bergin, 1981
Salmon et aI., 1986
Christy, 1986
Ennis, 1975
Ennis, 1973
Branford, 1978
Moller and Branford, 1979
Forward et aI., 1982; 1986
1985
type ofrhythm(s) dsplayed depending upon environmental cycles. This is perhaps
best demonstrated in the sublittoral estuarine crab Rhithropanopeus harrisii (Forward et al., 1982). Hatching rhythms were monitored in crab populations from
two estuaries, one of which had semidiurnal tides while the other lacked regular
tides. Light transmission in the tidal estuary was poor and at depths where the
crabs were collected it was doubtful that the LD cycle was perceived. The rhythms
in larval release as monitored in the laboratory were very different for crabs from
each estuary. Those from the non-tidal estuary released in the 2-h interval after
sunset, while releases by crabs from the tidal estuary occurred around the time of
each high tide in the field independent of time of day. These rhythms were not
fixed in each population because ovigerous crabs could be induced to switch
rhythms if exposed to conditions typical of the other estuary (Forward et al.,
1982).
If R. harrissii is subjected to both the diel LD cycle and a tidal cycle in salinity
change in the laboratory, larval release depends upon the time of nocturnal high
tide. Crabs only release at night. If high tide is near the beginning or within 3 h
of the end of the dark phase, releases occur at the beginning of the dark phase.
As high tide moves toward the middle of the night, an increasing proportion of
crabs release around the predicted time of high tide (Forward et al., 1986). This
pattern is very similar to those observed in other crab species in the field (Sesarma
species: Saigusa and Hidaka, 1978; Saigusa, 1981; 1982) and laboratory (Uca
pugilator: Bergin, 1981). Since very different patterns are observed when R. harrisii
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FORWARD: LARVAL RELEASE RHYTHMS
Table 4. Larval release occurs around time of high tide (terms as in Table I)
Species
Habitat
Method
Cardisoma guanhumi
Sesarma dehaani
Sesarma haematocheir
Sesarma intermedium
Cataleplodius taboganus
Eurypanopeus planus
Petrolisthes armatus
Uca minax
Uca pugilator
supralittoral
supralittoral
supralittoral
supralittoral
littoral
littoral
littoral
littoral
littoral
field
field
field
field
field
field
field
lab
lab
Uca pugnax
Uca spp.
Xanthadus sternberghii
Rhithropanopeus harris;;
littoral
littoral
littoral
sublittoral
lab
field
field
lab
Reference
Henning, 1975
Saigusa, 1981
Saigusa and Hidaka, 1978; Saigusa, 1981; 1982
Saigusa and Hidaka, 1978; Saigusa, 1981
Christy, 1986
Christy, 1986
Christy, 1986
DeCoursey, 1979; Salmon et aI., 1986
DeCoursey, 1979; 1983; Bergin, 1981; Salmon
et aI., 1986
DeCoursey, 1979; Salmon et aI., 1986
Salmon et aI., 1986
Christy, 1986
Forward et aI., 1982; 1986
is exposed to either tidal or LD cycles alone, the consistent (between species) but
complex larval release pattern observed when these cycles are presented together
seems to result from the interplay of the times of high tide and night.
ENDOGENOUS
CONTROL:
ZEITGEBER
AND ENTRAINMENT
Rhythms in larval release appear to be under endogenous control. Evidence for
an endogenous rhythm consists of demonstrating that the rhythm (1) persists for
a number of consecutive cycles (e.g., 5-10) in a single individual under laboratory
conditions lacking the environmental cycles corresponding to the rhythm (e.g.,
constant condition) and (2) has a free running period close to but not exactly equal
to the corresponding environmental cycle (semilunar, diel, or tidal). It is difficult
to uniformly apply these criteria to all crustacean hatching rhythms. For most
crab species, larval release occurs as a single event and thus persistence of the
rhythm in a single individual for a number of consecutive cycles cannot be dem-
onstrated. Nevertheless, the rhythmic release of larvae by a population of crabs
can be shown to persist under constant conditions in the laboratory. This demonstration can then be used as evidence for the presence of an endogenous rhythm,
for which a free running period length can be calculated.
Alternatively, this problem does not arise for the lobsters such as Homarus
gammarus (Ennis, 1973) and Nephrops norvegicus (Moller and Branford, 1979),
in which individuals release groups of larvae on consecutive nights for 14 to 42
and 5 to 23 days respectively. Also for the sublittoral crab Rhithropanopeus harrisii
about 20% of the crabs release two groups oflarvae on consecutive nights or high
tides (Forward et aI., 1982). It is not known whether multiple releases are common
among sublittoral species. The following section will present evidence for endogenous semilunar, diel and tidal rhythms. Since the rhythms are endogenous and
releases are adjusted to the timing of natural environmental cycles, the rhythms
must be entrained by cycles in particular environmental events. Possible entrainment cues or zeitgeber will also be considered.
Considering semilunar rhythms, the most convincing demonstration of endogenous control is Saigusa's (1980) work with Sesarma haematocheir in which a
population was maintained in the laboratory under a consistent LD cycle for more
than three months. These crabs were able to release larvae at specific times and
within a few days laid down another clutch of eggs. In this study, hatching was
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1987
monitored for as many as three consecutive releases in a single crab and was
related to the lunar cycle. Part of the population initially released at the time of
the first full moon while the remaining crabs waited until the new moon. Subsequently, crabs laid down new eggsand released again about 30 days later, around
the time of the next full and new moons respectively. Thus, the population appears
to have a semilunar rhythm, but each individual has an endogenous lunar rhythm.
It is logical that lunar and semilunar rhythms in larval release are regulated by
the female because the time in the lunar month of embryo maturation depends
upon the time of oviposition and the length of embryo development. Thus the
day the female lays her eggs determines when in the lunar month the eggs will
subsequently hatch.
For crustaceans showing semilunar rhythms, larval release usually occurs at the
time of new and full moon, at night, around the time of high tide. The semilunar
(lunar) rhythm may be entrained upon cycles in (1) factors that vary with phase
of the moon (e.g., moonlight cycle) and/or (2) factors that vary with the amplitude
of nocturnal ebb tides (Christy, 1982). For Uca pugilator, Salmon et a1. (1986)
showed that releases are not related to the time interval between sunset and
nocturnal high tide which vary on a semilunar cycle. Using this same species,
Christy (1978; 1982) compared releases by populations from areas having spring
tides at the syzygies and at the quarter phases of the moon. Larval release was
different between these populations and always occurred at times of the month
of greatest amplitude ebb tides shrouded in darkness (Christy, 1982). This suggests
that for this species the release rhythm is entrained upon cues associated with
environmental cycles that have a semilunar period. The semilunar cycle in tidal
amplitude is a possibility but at this time there is no clear supporting evidence.
Alternatively, Saigusa (1980) found that a semilunar larval release rhythm of
Sesarma haematocheir could be entrained by a 24.8-h artificial moonlight cycle.
The pattern, however, varied from that in the field as more crabs released at the
time of new moon on the artificial cycle, while in the field the full moon was
favored. S. haematocheir lives in supralittoral hillsides and paddy fields where
they are not directly exposed to tidal changes but would have a clear view of the
moon.
Diel release rhythms similarly persist under constant dark (DO) and light (LL)
conditions in the laboratory. There is, however, some variation with lighting
conditions. Rhythms in Rhithropanopeus harrisii (Forward et a1., 1982), Homarus
gammarus (Ennis, 1973; Branford, 1978) and Nephrops norvegicus (Moller and
Branford, 1979) continue in DD while Uca pugilator (Bergin, 1981) and N. norvegicus (Moller and Branford, 1979) will also persist in LL. The free running
period length for R. harrisii over five cycles in DD was 24 h 33 min (Forward et
a1., 1982). For N. norvegicus the free running period length over seven cycles
varied with lighting conditions being a little longer than 24 h in LL and 22.9 h
in DD (Moller and Branford, 1979).
Clearly, diel rhythms are entrained by the LD cycle. Forward et al. (1982)
demonstrated that Rhithropanopeus harrisii could be switched from a tidal rhythm
to a solar day rhythm by exposure to a LD cycle in the laboratory. In addition,
release times could be phase shifted by altering the timing of the LD cycle. The
release rhythms of the lobsters Homarus gammarus (Ennis, 1973) and Nephrops
norvegicus (Moller and Branford, 1979) are similarly entrained by an LD cycle
but the zeitgeber may be different. Ennis (1973) presents evidence that the onset
of darkness synchronizes the rhythm in H. gammarus, while day length is important for N. norvegicus (Moller and Branford, 1979).
Endogenous tidal rhythms are also observed since larval releases around the
FORWARD:
LARVAL RELEASE RHYTHMS
171
predicted time of high tide persist under nontidal conditions in the laboratory.
Rhythms in Rhithropanopeus harrisii continue under constant conditions (DD)
for at least six cycles with a free running period of 12 h 12 min (Forward et a1.,
1982). Similarly three species of fiddler crabs, maintained in the laboratory under
an LD cycle, release larvae in synchrony with local tides up to 14 days after
removal from the field (Salmon et al., 1986). Specifically, Bergin (1981) found the
fiddler crab Uca pugilator released at the predicted time of nocturnal high tides
for up to 21 days in constant conditions (LL) and had a free running period of
25 h 03 min.
The timing of tidal release rhythms is adjusted to local tidal cycles (Saigusa
1982; Salmon et a1., 1986). The only species for which we have information about
the zeitgeber for entrainment of the tidal release rhythm is the crab Rhithropanopeus harrisii (Forward et a1., 1986). If crabs are collected from an estuary having
irregular tides and exposed to only a semi-diurnal tidal cycle in salinity change
in the laboratory, a tidal rhythm develops in which larval release occurs around
the predicted time of highest salinity (high tide) (Forward et a1., 1986). Thus
salinity cycles can entrain a tidal rhythm. In the case of Sesarma sp. (Saigusa and
Hidaka, 1978) and Uca pugilator (Bergin, 1981), it is unlikely that ovigerous
females are exposed to tidal cycles in salinity, yet they display tidal rhythms. Thus
tidal rhythms in hatching can probably also be entrained by cycles in other environmental factors such as hydrostatic pressure, temperature and mechanical
agitation.
SITE OF ENDOGENOUS CONTROL FOR LARVAL RELEASE
Iflarval release is under endogenous control then the timing may be controlled
by the female, the developing embryos or both. The time of hatching of a clutch
depends upon those events which synchronize development of the embryos and
those which control the actual hatching. An interaction between eggs and female
is probably responsible for synchronized development (Forward and Lohmann,
1983). In preparation for hatching, eggs swell and the outer egg membrane or
chorion breaks leaving a fragile inner egg membrane surrounding the embryo
(Davis, 1968; 1981). Larval release occurs upon breakage of this inner membrane
which is induced by either (1) movements ofthe embryo or (2) vigorous pumping
of the female's abdomen.
The site for the endogenous control of release seems to vary with species. In
the sublittoral lobster Homarus americanus the female controls the time oflarval
release. The egg membranes break in preparation for larval release, which takes
place only upon beating of the female's abdomen. There is no evidence that a
chemical cue or movement of the larvae activate the female's larval release behavior (Davis, 1964; Ennis, 1975).
The site is not so clear in Homarus gammarus. Pandian (1970) and Ennis
(1973) suggest that the embryo controls the time of larval release. Considering
events involved in hatching, Pandian (1970) found that egg permeability changes
which lead to hatching occur within the egg and are presumably not affected by
the female. Ennis (1973) observed that if the ovigerous female was vigorously
shaken shortly before the expected time oflarval release, none ofthe eggs hatched.
Nevertheless, larval release did occur at the proper time. Alternatively, Branford
(1978) argued that the endogenous control is in the female. In the presence of a
LD cycle both isolated eggs and those attached to the female hatch at the same
time. In DD the isolated eggs are arrhythmic but the ovigerous female continues
to release larvae rhythmically. Branford (1978) suggests the endogenous com-
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ponent resides within the female and the eggs have an exogenous rhythm in which
they complete development with the onset of darkness.
In contrast to the lobster, larval release by the subtidal crab Rhithropanopeus
harrisii is clearly controlled by the developing embryos (Forward and Lohmann,
1983). Eggs removed from the female hatch rhyhmically under constant conditions
at about the same time as those attached to the female. The proposed model is
that at the specific time of hatching, a few eggs hatch either by movements of the
embryo or due to breakage by normal movements of the female. Breakage releases
a chemical cue that induces the female to perform a stereotypic larval release
behavior ("pumping") in which she rapidly beats her abdomen. Pumping causes
more eggs to hatch which in tum increases the concentration of the chemical cue,
thereby causing more vigorous pumping. The net result is the synchronized release
oflarvae. Water in which eggs have hatched will induce the female's larval release
behavior (Forward and Lohmann, 1983). The chemical cues were isolated and
identified as a group of approximately 5 dipeptides each containing arginine
(Rittschof et aI., 1985).
The only indication of the endogenous site among high intertidal and supralittoral species is DeCoursey's (1979) study of the fiddler crab Uca minax. If
pleopods with attached eggs are removed from the female during larval release,
very few eggs hatch. This suggests endogenous control resides in the female
(DeCoursey, 1979) and the eggs depend upon physical movement for hatching.
The suggestion that the female has the endogenous clock may be true for the high
littoral and supralittoral brachyuran species.
To explain this conclusion let us consider larval release by Rhithropanopeus
harrisii, the one species for which there is unequivocal evidence that the endogenous site is in the eggs. This species can display either a tidal or die I release
rhythm. The rhythms can be switched if ovigerous crabs are exposed to tidal or
LD conditions longer than 5-6 days before hatching. Attempts to switch the
rhythms are unsuccessful if the eggs are within 5-6 days of hatching. Also if the
crabs are maintained in constant conditions in the laboratory for longer than 7
days, population release times are arrhythmic (Forward et aI., 1986). Thus the
development ofa larval release rhythm depends upon exposure of the developing
embryos to environmental cycles about 5 days before hatching. This timing agrees
with unpublished observations of embryo development in that eye pigments are
first seen about 5 days before hatching. This suggests that the sensory system may
become functional at this time and perceive environmental cycles on which the
release rhythm becomes entrained. Thus if the embryos are the endogenous site
then they must be exposed to environmental cycles at times when they can perceive
these cycles for the hatching rhythm to be developed.
Rhythms in high littoral and semiterrestrial crabs persist without this environmental entrainment. For Uca species, Bergin (1981) and Salmon et al. (1986)
found the tidal rhythm to occur for up to 17 and 14 days in non tidal conditions
in the laboratory respectively. Since these times closely correspond to the maximum length of time a female carries eggs, females carrying embryos for 14-17
days must have been placed under non tidal conditions before the development
of the embryo's sensory and nervous systems. Similarly, Saigusa (1980) maintained Sesarma haematocheir in the laboratory under nonlunar conditions for
longer than 2 months during which some crabs released three broods of larvae at
the time of consecutive new or full moons in the field. In this case the eggs were
deposited in the laboratory and yet the rhythm persisted. Thus the endogenus
clock may reside within the female for these species and perhaps all high littoral
and supralittoral species. It is, however, possible that the female could entrain
FORWARD:
LARVAL RELEASE RHYTHMS
173
the appropriate rhythm in the developing embryos through her interaction with
the embryos.
FuNCTIONAL ADVANTAGES
The foregoing discussion indicates that larval release is rhythmic and precisely
timed with respect to environmental cycles. The most common relationships are
that release occurs at the new and full moon, at night, around the time of high
tide. The convergence in times by different species suggests there are shared
functional advantages. Most of the timing relationships are explained in terms of
survival of the adult female and her larvae. The existence of rhythms themselves
generally serves this function because the aggregation oflarval releases into a small
time interval would tend to swamp potential predators.
Larval release around the time of high tide may function for larval dispersal
and survival. For estuarine species, larvae entering the water column near high
tide would move seaward as the tide recedes. Rapid removal from the release
area of supra littoral species minimizes exposure to larval predators (Salmon et
al., 1986) and potential stranding in shallow areas (Saigusa, 1981; Salmon et al.,
1986). Similarly Christy (1986) implies that release at high tide by coastal species
may lead to dispersal away from the release site and reduced exposure to potential
predators.
In the case of the estuarine crab Rhithropanopeus harrisii, however, it is unlikely
that release at high tide has these advantages because larvae are released in sublittoral areas and field studies (Sandifer, 1973; 1975; Cronin, 1982) indicate massive seaward transport of larvae does not occur. All larval stages are retained in
the area of the adult population (Cronin, 1982). An alternate hypothesis is that
larval release near the time of high tide functions as an adaptation to avoid stressful
or even lethal salinity conditions. Salinity tolerance of estuarine crab larvae is
usually sufficient to cope with the maximum upper salinity values they are likely
to encounter. The real tolerance problem is low salinity which would be experienced at low tide (Forward et al., 1982).
Both Von Hagen (1970) and Saigusa (1981; 1982) also considered the timing
oflarval release to be related to salinity tolerance in estuarine species. They both
suggested that if larvae are released around high tide, the subsequent ebb would
transport them toward the ocean where they would encounter less stressful, high
salinity water. Since Rhithropanopeus harrisii larvae are not transported to the
ocean, larval survival in estuaries may be dependent upon exposure to the highest
possible salinity at the time of release (Forward et al., 1982).
During the LD cycle larvae are usually released at night. The functional advantage suggested most often for this timing is avoidance of predators which
visually sight and actively pursue their prey. This especially applies to supralittoral
females which are vulnerable as they migrate to the water (DeCoursey, 1979;
Bergin, 1981; Wolcott and Wolcott, 1982) and larvae when they are concentrated
at the time of release (Ennis, 1975; Branford, 1978; Christy, 1982; Forward et
al., 1982).
An additional advantage for night time release is reduced exposure to high
temperature (Dollard, 1980). The maximum temperature in shallow areas usually
occurs in summer afternoons. Thus if larvae are released at the beginning of the
night, they would experience declining temperatures initially, which could be
reduced further if they were transported into deeper water.
Saigusa (1982) suggested that the actual time of release is related to the combination of solar day and local tidal cycles. Release times when both cycles are
present suggests a hierarchy in functional advantages relative to each cycle. This
174
BULLETIN OF MARINE SCIENCE, VOL. 41, NO.2,
1987
is best studied in Rhithropanopeus harrisii (Forward et aI., 1986). Release when
exposed to LD or tidal cycles alone occurs at the beginning of the night and around
the time of high tide respectively. When the two cycles are combined, hatching
occurs only at night and is related to high tide only when it occurs between about
2 h after the beginning of the dark phase and 3 to 5 h before the beginning of the
light phase. When high tide is at other times, larvae are released relative to the
LD cycle at the beginning of night, even when low tide occurs near sunset. Since
release only occurs near high tides that fall in a narrow nocturnal interval, factors
which influence hatching relative to the LD cycle must be of greatest functional
importance. Reduced vulnerability to visual predators would then be more important than avoidance of extreme salinities or rapid removal from the release
area.
Saigusa (1982) also suggested that the number of females with mature embryos
is related to the lunar cycle. If a semilunar release rhythm is present then the
greatest numbers ofthese females usually occur at the time of greatest amplitude
nocturnal ebb tides (Christy, 1978; 1982), which most often corresponds to the
time of spring tides at the new and full moon. Initially, Christy (1978) proposed
this timing oflarval release resulted in transport ofthe final larval stage by spring
tidal currents back to substrates suitable for settlement. This hypothesis resulted
from work on fiddler crabs but applies to other estuarine species with similar
rhythms. Unfortunately, even though this hypothesis is intellectually attractive it
was disproven by Christy's (1982) later work in which he demonstrated that (1)
the length oflarval development and hence time spent in the plankton decreased
with the temperature increase during the breeding season, yet the time of release
relative to spring tides did not change, and (2) megalopa settlement did not
correspond to spring tides. Another negative relationship is that semilunar rhythms
are not related to the larval nursery areas (Salmon et aI., 1986). Estuarine species
which have the same nursery areas in the lower estuary and coastal areas mayor
may not have semilunar rhythms.
Semilunar rhythms are most common among littoral and supralittoral species
(Table 4; Salmon et aI., 1986). Release at the greatest amplitude nocturnal ebb
tides results in greatest chance that larvae of estuarine species will be transported
seaward away from the adult habitat (Saigusa and Hidaka, 1978; Saigusa, 1981)
to an area with reduced numbers of planktivorous predators (Christy, 1982).
Species that lack semilunar rhythms have larvae which may remain near the adult
population and frequently have structural (Morgan, 1981; Christy, 1982) and
coloration modification (Christy, 1986) to reduce predation.
FUTURE
DIRECTIONS
Past studies indicate that rhythms in larval release are common among decapod
crustaceans, and in fact, there is no published record indicating that larval release
of a species would be arrhythmic in nature. Such rigid control indicates that the
relationship of release to the timing of environmental cycles must be functionally
important for successful reproduction. Our knowledge of types of rhythms as
related to adult ecology and environment, their functional advantages and the
selective pressures which shape rhythms would benefit from further detailed studies of a diversity of species from a wide range of habitats. The latter is especially
important since our real understanding of the relationship of rhythms to environmental cycles has come from studies of single species living in different habitats
(Christy, 1978; 1982; Saigusa 1981; 1982; Forward et aI., 1982; Salmon et aI.,
1986).
FORWARD:
LARVAL RELEASE RHYTHMS
175
In addition, predation is frequently considered a selective force for the timing
of rhythms. However, in only a few cases have the predators been identified. The
identification of potential predators upon adults and larvae at the time of larval
release and the early phase of larval development would suggest whether larval
release is in fact timed to reduce predation.
Another future area of study concerns the question of whether endogenous
control resides in the female, developing embryos or both. We have a reasonable
model of larval release by sublittoral crabs (Forward and Lohmann, 1983) in
which the control site is the developing embryo. For supralittoral species the
control site appears to be in the female, but definitive proof is needed. If these
generalizations are true then there may be a gradient of control mechanisms, in
which there is dominant control by the embryo of sublittoral species, interaction
between the embryo and female in littoral species and control by the female in
supralittoral species. Thus, an exciting area for future research is the control of
hatching among species living in different areas.
ACKNOWLEDGMENTS
The material is based on research supported by the National Science Foundation under Grant No.
OCE-8313779. I thank Drs. J. Christy, D. Rittschofand M. Salmon and Ms. M. DeVries for critically
reading the manuscript.
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DATEACCEPTED: September 2, 1986.
ADDRESS: Duke University Marine Laboratory, Beaufort, North Carolina 28516, and Zoology Department, Duke University, Durham, North Carolina 27706.