AMER. ZOOL., 26:433-445 (1986)
The Role of Light and Endogenous Factors in the Timing
of the Reproductive Cycle of Typosyllis prolifera
and some other Polychaetes1
HEINZ-DIETER FRANKE
Department of General Zoology, Free University of Berlin,
Berlin, West Germany
SYNOPSIS. Reproductive processes in the syllid polychaete Typosyllis prolifera take an annual,
a lunar-monthly and a daily pattern. Natural light changes (the seasonal change in relative
daylength, the cycle of moonlight, the daily light-dark cycle) seem to provide the principal
environmental information for the synchronization of reproduction with the external
cycles. Both relative solar daylength and the daily light-dark cycle probably act exogenously. Moonlight, in contrast, acts as an entraining zeitgeber to a circalunar clock. Hormones (at least two distinct factors) mediate between the controlling centers and the
peripheral tissues involved in sexual development. The effects of daylength and, indirectly,
moonlight upon sexual development are brought about through the intermediation of
the endocrine system. The exogenous and endogenous mechanisms of reproductive timing
in T. prolifera are compared with those recently reported in some other polychaete species.
INTRODUCTION
cycle, which enables coupling of reproducTiming mechanisms for reproduction tive events to specific phases of the external
serve two functions which as selective fac- cycles. There are a number of different
tors ("ultimate causes"; Baker, 1938) may ways in which environmental variables theaccount for their evolution: They link oretically may operate (Clark, 1979; Olive,
reproduction with times (seasons, phases of 1984). On the one hand they may act
tides, etc.) when the environmental con- directly as (a) "necessary environmental
ditions are favorable for the development conditions" defining periods of time when
of offspring; and they generate some degree reproduction is possible (necessary condiof within-population synchrony, necessary tions satisfied) or not, (b) specific signals
to enhance the probability of fertilization which trigger some critical events of reproparticularly in those species which broad- duction, or (c) parameters controlling the
rate of processes such as oocyte growth.
cast their gametes.
In a number of polychaete species, the On the other hand external factors may
temporal distribution of reproductive pro- serve as zeitgebers which entrain endogecesses in natural populations suggests the nous rhythmic (circannual, circalunar, cirexistence of a complex hierarchy of timing cadian) programs to the respective cycles
mechanisms: Reproduction is timed to a of environmental conditions. Furthermore or less extended annual breeding sea- more, since reproductive processes in polyson, a particular phase of the moon, and a chaetes as in most other animal groups are
particular time of day. This is exemplified usually subject to endocrine control (Olive,
most spectacularly by the Pacific palolo 1979; Franke and Pfannenstiel, 1984),
worm Eunice viridis (Caspers, 1961; Hauen- environmental control may often be
schild et al., 1968), and to a lesser extent exerted through the regulation of endoit also applies to a range of other species crine activities.
such as Typosyllis prolifera (Fig. 1). The phe- In this paper I outline my investigations
nomenon implies an input of environmen- on external and internal control of reprotal information ("proximate causes") from duction in the syllid polychaete Typosyllis
the annual, the lunar and the solar day prolifera, which have revealed that light
changes (seasonal changes in relative daylength, lunar changes in dim nocturnal illu1
From the Symposium on Photoperiodism in the mination, and daily changes of light and
Marine Environment presented at the Annual Meeting
of the American Society of Zoologists, 27-30 Decem- dark) are of major importance to annual,
lunar and daily timing. The findings are
ber 1984, at Denver, Colorado.
433
434
HEINZ-DIETER FRANKE
Swarming
II
III
and
spawning
IV
Annual
0
cycle
(months)
14 .7
Cycle
o f lunation ( d )
Regeneration
of t h e s t o c k
Daily
l i g h t - d a r k
cycle
(hr)
FIG. 1. Diagram summarizing the results of field
studies on reproductive timing in Typosyllis prolifera
in relation to the annual (A), the lunar-monthly (B)
and the daily cycle (C).
compared with those which have become
available in recent years from some other
polychaete species.
Typosyllis prolifera has been raised
through many generations (Franke, 1980).
The species reproduces by stolonization
(Fig. 2). Sexual development (gametogenesis and somatic maturation) is confined to
the posterior part of a worm and culminates in the formation of a specialized
reproductive individual (stolon). This
detaches from the benthic parent stock,
swarms and spawns at the water surface,
and then dies. The stock undergoes postreproductive caudal regeneration and can
stolonize several times during its lifetime.
and
ep
FIG. 2. Diagrammatic representation of the life cycle
of the polychaete Typosyllis prolifera; Pv, proventriculus (after Franke and Pfannenstiel, 1984).
external information for the annual cycle
of breeding. Most suggestions on the role
of temperature, however, are solely based
on correlations established in field studies
(e.g., Bhaud, 1972), whereas experimental
demonstration of a direct causal relationship between reproductive activities and
temperature is limited to a few instances
such as Eulalia viridis (Olive, 19816). Only
recently, for a small number of polychaete
RELATIVE DAYLENGTH AS A REGULATOR
species experimental evidence has been
OF SEASONAL REPRODUCTION
obtained that suggests changes in relative
Although a number of polychaetes have daylength may play a role in the regulation
been reported to breed all year (see of reproductive seasonality.
Reproduction of T. prolifera in the field
Schroeder and Hermans, 1975), most shallow water, temperate species have a more (northern Adriatic Sea) is largely restricted
or less restricted annual breeding season. to the period from late March to early
Among the environmental variables which October, with a peak in May (Fig. 1A).
might exert proximate control over sea- Occasional individuals in reproductive
sonal reproduction is sea temperature. condition, however, may be found at almost
Annual temperature fluctuations are fre- any time of the year. Nothing is known
quently cited as the principal source of about the ecological conditions (ultimate
435
LIGHT AND REPRODUCTION IN TYPOSYLUS
factors) which make this period of the year
more appropriate for reproduction than
others. To identify the proximate factors
which determine the limits of the extended
breeding season, the effects of feeding,
temperature, and daylength on reproductive activity were studied in the laboratory.
Starved worms stop reproducing nearly
immediately, indicating that continuous
food input is necessary for reproduction.
Under conditions of ample food supply,
the existence of two alternative developmental pathways was demonstrated; their
expression was controlled by the daylength
and temperature regime (Franke, 1980,
1983a). Under 10°C and short day photoperiod LD 10:14 ("winter" conditions),
worms undergo slow but steady somatic
growth while stolonization is extremely rare
(nonreproductive development). Under
20°C and long day photoperiod LD 16:8
("summer" conditions) virtually all animals
show reproductive development. This is
characterized by cyclic stolonization of the
individual worms which, based on an
endogenous circalunar program (see next
section), release mature stolons about every
31 days (Franke, 1980). The 31-day period
of the stolonization cycle consists of the
postreproductive regeneration phase
(mean duration 17 days), and the stolonization phase (14 days) during which visible
sexual development takes place culminating in the release of another stolon. Under
a static "summer" regime animals continue with cyclic stolonization throughout
the year, but the population is asynchronous. A sudden change from "summer" to
"winter" conditions suppresses further
reproduction after a latent period of about
2 weeks. In the reverse case, sexual development is initiated (nearly synchronously
in a population) within 2-3 weeks, and
mature stolons are released within about 5
weeks of exposure to "summer" conditions. Worms collected in the field showed
similar responses independent of annual
time.
In a further set of experiments I
attempted to clarify the relative importance of temperature and daylength in the
above response. Groups of animals were
shifted from nonreproductive "winter"
Photoperiod
( hr
l i g h t / day
10
13
17
Temperature
( ° C )
20
FIG. 3. Worms (%) which released a stolon within
45 days after transfer from 10°C/LD 10:14 to various
daylength and temperature regimes; 100-150 singly
kept individuals per experimental group.
conditions to various regimes of constant
temperature and static daylength (Fig. 3).
The findings indicate a synergistic action
of these variables, and the existence of a
critical temperature level between 10°C and
13°C. Below this level, reproduction is
largely prevented independent of daylength. Above the critical temperature the
implementation of nonreproductive/
reproductive development depends on
daylength but is nearly independent of
temperature.
Seasonal photoperiodic responses in
insects, vertebrates and plants are often
associated with a rather well defined, temperature-compensated "critical photoperiod," representing the daylength value at
which the organism changes more or less
abruptly the developmental program
(Bunning, 1973). For T. prolifera a photoperiodic response curve was measured at
14°C and 19°C (approximate sea temperatures at the beginning and ending of the
breeding season) (Fig. 4). The curve was
found to be non-linear, exhibiting a sharp
increase in the percentage of animals which
change from nonreproductive to reproductive development, around 12 hr light
per day at 14°C, and 13 hr light per day at
19°C.The critical photoperiod thus seems
to depend on temperature.
Based upon the foregoing experiments,
availability of food, a certain elevated temperature (critical value between 10°C and
13CC), and a photoperiod above the critical
level (12-13 hr light per day, depending
436
HEINZ-DIETER FRANKE
100
14
T
50
10
Photoperiod
13
( hr
i g h t per
16
day)
FIG. 4. Photoperiodic response curve at 14°C and
19°C: Induction of stolonization in nonreproductive
worms (previously kept at 10°C and LD 10:14); about
100 singly kept worms per experimental group.
on temperature) were identified as "necessary environmental conditions" for
reproduction. It was not clear, though,
which of these factors exert(s) proximate
control over the discrete spring-summer
breeding season, and, furthermore, if the
control of annual reproductive periodicity
involves any element of endogenous long
term programming.
Individuals of T. prolifera are relatively
short-lived. Although in the laboratory they
may occasionally live and reproduce over
nearly 2 years, the vast majority of individuals in the field may have a sub-annual
life cycle which rarely makes reproduction
possible in a second breeding season. The
annual cycle of breeding observed in the
field is thus essentially a population phenomenon. Within the extended breeding
season, however, each adult worm probably stolonizes several times at frequent (circalunar) intervals as suggested by the laboratory findings. According to the
terminology of Olive and Clark (1978), T.
prolifera shows the "semi-continuous" mode
of reproduction (synonymous with "continuous iteroparity"; Bell, 1976). The short
life cycle of the species together with the
findings that the implementation of nonreproductive/reproductive development
can be manipulated independent of real
annual time by artificial daylength regimes,
indicate that seasonal reproduction may
simply be a function of the external conditions experienced and does not involve
any element of endogenous long term timing.
Among the environmental variables
studied, possible changes in feeding conditions as well as cylic variation in sea temperature (11-12°C in January, 22-24°C in
August) do not seem to interfere with the
proximate timing of the natural breeding
season. Although conclusive evidence is difficult to obtain, no findings support the
idea that quantitative or qualitative changes
in nutrient supplies might act as proximate
cues. On the other hand, in the native habitat temperature requirements for sexual
development are satisfied throughout most,
though not all of the year. Consequently,
the annual cycle of relative daylength
rather than the cycle of sea temperature
remains as the most likely regulator of seasonal reproduction, presumably acting as
the major limiting factor which releases
animals from restraint in early spring and
puts them under restraint again in early
fall. And indeed, if we hypothesize that the
light intensity threshold for daylength
measurement in Typosyllis lies at about civil
twilight, and if we consider that initiation
and suppression of reproductive processes
require a latent period of about 2-3 weeks
each, there is good evidence then that both
the initiation and termination of the breeding season in the northern Adriatic Sea
(45CN) are primarily determined by the
passage of daylength from below a critical
level to above it and back. This is furthermore supported by the findings that there
was virtually no variation in the timing of
the breeding season among years.
Besides T. prolifera, photoperiodic effects
involved in seasonal reproduction have
been suggested for the polychaetes Autolytus prolifer (Schiedges, 1979), Harmothoe
imbricata (Garwood, 1980; Garwood and
Olive, 1982) and Kefersteinia cirrata (Olive
and Pillai, 1983). The situation in A. prolifera might be somewhat similar to that in
T. prolifera (long daylength and elevated
temperature stimulate, short daylength and
low temperature inhibit stolonization) but
information is very limited. The situation
LIGHT AND REPRODUCTION IN TYPOSYLLIS
in H. imbricata and/C cirrata, which exhibit
a reproductive strategy quite different from
that of T. prolifera, requires further consideration. The individuals of both species
are long-lived, showing synchronized
breeding once (or twice) a year through
several successive years ("discrete-polytelic" reproduction; Olive and Clark, 1978).
Seasonality of reproduction is, therefore,
a phenomenon which refers to both the
population and the individual. Furthermore, sexual development is a long process
which takes several months, but gametogenic events in a population are nevertheless well synchronized.
It is evident that the control of seasonal
reproduction in discrete-polytelic species
requires different and probably much more
complex timing mechanisms than in species
reproducing semi-continuously. First, a
complex sequence of environmental influences may be expected, which introduce
and reinforce synchronization in a population over the prolonged period of sexual
development (Clark, 1979). Secondly, there
is the possibility that endogenous long term
(circannual) rhythms, entrained by external zeitgebers, might underlie the annual
reproductive cycle. These questions have
been analyzed during recent years in a
number of polychaete species by Olive and
co-workers (reviews by Olive, 1981a, 1984;
Olive and Garwood, 1983). In the context
of this paper, I refer to these investigations
only so far as photoperiodic effects are concerned.
In both H. imbricata and K. cirrata daylength (acting synergistically with temperature) has been shown to influence oocyte
growth rates. In the field, oocyte growth
is timed so that rate control by natural
changes in daylength and temperature
inevitably increases reproductive synchrony ("synchronizing rate effect"). In
contrast to the photoperiodic response in
T. prolifera, the responses in the above
species thus do not refer to an all-or-nothing phenomenon (nonreproductive/
reproductive development) but apply to the
rate of a process. In H. imbricata, acceleration of oocyte growth by increasing daylength is associated with a "critical photoperiod" between 10 and 11 hr light per
437
day. A detailed analysis of this species has
moreover suggested that increasing daylength, in addition to its direct action on
the rate of oocyte growth, may exert a zeitgeber effect on an endogenous rhythmic
program which alters in relation to real
annual time the animals' reactions to the
environmental variables daylength and
temperature.
THE CYCLE OF MOONLIGHT AND
THE TIMING OF MOON-RELATED
REPRODUCTIVE PHENOMENA
Field studies have revealed that swarming and spawning in many polychaete
species are correlated to some extent with
lunar cycles (see Olive and Clark, 1978).
The timing mechanisms underlying these
phenomena only have been investigated in
any detail in Platynereis dumerilii (Hauenschild, 1955, 1960) and Typosyllis prolifera
(Franke, 1980, 1985).
Within the prolonged breeding season,
reproductive processes in the studied natural population of T. prolifera are not distributed at random. A short term rhythm
is expressed in the population, with lunarmonthly peaks of swarming activity coinciding with the second quarter phase of the
moon (Fig. IB). The exact phase of swarming peaks varies slightly within the breeding season: In April/May (sea temperature
~15-16°C) the mean date of peak stolon
abundance is 13 days, in September/October (~ 19-20°C) 8 days after new moon. A
close examination of field samples taken at
daily intervals throughout the lunar month
has shown that the reproductive rhythm is
primarily expressed at the level of sexual
development and does not simply present
a rhythm of swarming behavior (Fig. 5).
Visible sexual development in a population
is initiated rather independent of season
mainly within a few days (25th-28th day)
towards the end of each lunation cycle.
Individuals carrying swarm-ready mature
stolons, however, show a marked lunarmonthly peak abundance in May between
days 10 and 15 , and in September between
days 5 and 10.
I performed laboratory experiments to
explain the above field findings. Individuals freed from constraints by tempera-
438
HEINZ-DIETER FRANKE
decreased temperature) although the phase
(as the period) of the endogenous oscillator
remains unaffected. The clock probably
operates in a similar manner in males and
females, since sexual development in either
30 sex is initiated at (and completed within)
about the same time.
4) The clock seems to run largely independent of the peripheral processes which
10 it controls. Temporary starvation, for
instance, causes a temporary interruption
of cyclic stolonization, but stolonization
15
30
processes before and after the starvation
Cycle of lunation ( d i
period are "in phase" suggesting the operFIG. 5. Changes in the relative abundance of worms ation of an ongoing unaffected clock.
which have just initiated visible sexual development
5) The fact that the lunar cycle of sto(open circles), and of those carrying swarm-ready stolonization
observed in laboratory individlons (closed circles) in samples taken at daily intervals
throughout the lunar month (% of the total numbers uals can be recognized at the level of a field
of collected worms with more than 50 segments). The population (Fig. IB) indicates that phase
graph combines data from field studies in May 1979, and precise period of the clock are subject
1980 and 1984 (after Franke, 1985).
to control by exogenous zeitgebers
(entrainment). Referring to Hauenschild's
ture, daylength and food availability breed pioneering study, the possible zeitgeber
periodically at rather regular lunar- effects of simulated cycles of moonlight
monthly intervals. Rhythmic stolonization were investigated (Fig. 6). Artificial moonin individuals is clearly intrinsic, its timing light (0.3-0.5 lx) on 4 or more successive
being regulated by a mechanism which nights every 30 days (LD 16:8) entrains the
exhibits the fundamental characteristics of individual rhythms, thus causing some synan endogenous "circa"-oscillator (circalu- chrony of stolon release in a previously
asynchronous population. The quality of
nar clock) (Franke, 1985).
1) Under constant conditions stoloniza- entrainment proved to be independent of
tion in an individual manifests as a free- the length of the "moonlit" phase (4 and
running rhythm with a mean period of 12 days), but "moonlight" on only 2 sucabout 31 days, ranging from 29 to 34 days cessive nights every 30 days was ineffective.
in different individuals. Cyclic stoloniza- The peaks of stolon release are phase-set
tion among the individuals of a population by the cessation of nocturnal illumination
(mean time at 20°C: 17 days after "light
is asynchronous.
2) The free-running period of stoloni- off"). The length of the preceding "moonzation is largely unchanged within the bio- lit" phase does not seem to interfere with
logically relevant temperature range from the mechanism of phase-setting. The tem15 to 25°C (Q10-value: 1.04), indicating poral pattern of increasing synchronizatemperature-compensation of the clock. tion under the influence of cyclic zeitgeber
The level of daylength (10-16 hr light per stimuli permits a preliminary insight into
day) is also without significant influence on the mechanism which causes adjustment of
the endogenous clock: Peaks of stolon
the period of the free-running rhythm.
release emerged at the expense of imme3) The endogenous timing mechanism diately following but not of preceding mintriggers the cyclic initiation of sexual ima. This suggests that the oscillator may
development, but does not control its prog- pass through a brief photosensible phase
ress which is clearly dependent on tem- just before it sets in motion the coupling
perature. As a consequence, a change in processes leading to the onset of sexual
temperature results in a phase-shift of the development. Experience of an effective
overt rhythm of stolon release (phase- zeitgeber signal ("light-off" after 4 or more
advance in increased, phase-delay in
439
LIGHT AND REPRODUCTION IN TYPOSYLLIS
0
30
Time
60
( days)
120
FIG. 6. Entrainment of the individual stolonization rhythms in asynchronous cultures by simulated cycles of
moonlight. The horizontal bars indicate the periods with illuminated nights: 2 (A), 4 (B) and 12 (C) successive
nights (0.3-0.5 lx) every 30 days (after Franke, 1985).
successive illuminated nights) during this
sensible phase may induce an advance
phase-shift of the clock, resulting in a
somewhat premature initiation of sexual
development and, consequently, in a premature release of the next stolon. Delay
phase-shifts do not seem to be involved in
the mechanism of entrainment. Moreover,
the duration of sexual development
remains unaffected by zeitgeber signals.
The laboratory findings suggest the following interpretation of moon-related
reproductive timing in the field population
of T. prolifera: Within the extended breeding season, if food is not limiting, each adult
may go through several successive stolonization cycles, the sequence of which is controlled by an endogenous circalunar oscillator. External zeitgeber signals, probably
associated with the cycle of moonlight,
entrain the individual clocks to the external lunar-monthly cycle. As a consequence,
some degree of synchrony is imposed on
the oscillators in a population, manifesting
in the well-defined lunar-monthly population rhythm of breeding. In the entrained
steady state, worms in a population initiate
sexual development preferably within a few
days of each fourth lunar quarter. Once
initiated, sexual development proceeds
autonomously, controlled by a program
which acts as "interval timer" (hourglass).
Worms which initiate sexual development
at about the same time will also reach maturity nearly synchronously, contributing to
a peak abundance of swarm-ready stolons
coinciding with a few days of each second
quarter phase of the moon (14-17 days
after the onset of visible sexual development). Since an increase in temperature
hastens, and a decrease slows sexual development, the phasing of the swarming peaks
within the lunar cycle varies with sea temperature, whereas the onset of sexual
440
HEINZ-DIETER FRANKE
development, which is controlled by the
temperature-compensated clock, is phased
independent of temperature.
The population of Platynereis dumerilii at
Naples (Italy) shows a pattern of breeding
which resembles that of T. prolifera: Reproduction occurs over a prolonged breeding
season with lunar-monthly peaks of swarming (Ranzi, 1931). In contrast to T. prolifera, however, P. dumerilii is monotelic (semelparous), each individual breeding only
once per lifetime. According to the experiments of Hauenschild (1955, 1960), there
is evidence that the lunar periodicity of
swarming in both species is nevertheless
based on essentially the same elements: A
circalunar oscillator inherent in the individual organisms, which is entrained to the
external lunar cycle by zeitgeber stimuli
connected with the cycle of moonlight. The
differences between the two species result
from their quite different reproductive
strategies.
1) Since spawning in P. dumerilii is a onceper-lifetime event, its endogenous rhythm
may be interpreted as a "gated rhythm"
in analogy to the diurnal eclosion rhythms
of some insects (Pittendrigh, 1966; Olive,
1984). Such a rhythm defines recurring
periods of time when a particular event
may occur ("gate open") or may not ("gate
closed"). In the semi-continuously breeding T. prolifera the endogenous rhythm is
directly expressed as an overt rhythm of
reproduction at the individual level, and a
population rhythm is the result of synchronization of these individual reproductive rhythms. An overt aspect of the "gated
rhythm" of P. dumerilii, however, only can
manifest at the level of a synchronized population in which reproduction of different
individuals is staggered over the breeding
season.
2) The endogenous oscillator in T. prolifera, the sexual development of which is
a rapid process completed within 14 to 17
days, operates by (periodic) initiation of the
overall process of sexual development. In
P. dumerilii, in contrast, sexual development takes much more time, and the oscillator only controls the onset of the rapid
final phase of sexual development. In both
species, however, the developmental pro-
cesses initiated by the oscillator follow an
intrinsic program which as an interval timer
serves to maintain synchrony to the time
of sexual maturity.
THE DAILY LIGHT-DARK CYCLE AS A
REGULATOR OF DAYTIME-RELATED
REPRODUCTIVE BEHAVIOR
Swarming and spawning in polychaetes
is often associated with specific times of
day. Odontosyllis phosphorea (at San Diego,
California), for instance, swarms and
spawns within a 30-min period shortly after
sunset (Tsuji and Hill, 1983); epitokes of
Eunice schemacephala do so early in the
morning (Mayer, 1908). The daytime of
swarming in Eunice viridis differs between
the local populations of the Samoa Islands
although the phase differences in local tides
are insignificant (Hauenschild etal, 1968).
Nearly nothing is known in polychaetes
about the mechanisms which control the
distribution of reproductive behavior in
relation to the solar day cycle. The paramount importance of circadian programming throughout eukaryotic organisms
would suggest that swarming is timed by
an endogenous circadian oscillator
entrained to the 24 hr day by zeitgebers
such as the daily light-dark cycle (circadian
"gating" of swarming). Varying daytimes
of swarming in species and populations,
respectively, could result from genetically
fixed differences in the phase of the clock.
A combination of a circa-(semi)lunar and
a circadian timing mechanism, as it controls adult emergence in the midge Clunio
marinus (Neumann, 1966), could serve as
a model to explain moon- and daytimerelated reproductive phenomena in polychaetes. However, there is as yet no conclusive evidence of a circadian involvement
in the timing of swarming behavior in any
polychaete species. On the contrary, in the
two cases studied, daytimes of swarming
seem to be determined by direct environmental input rather than by a circadian
program.
Mature stolons of Autolytus edwardsi kept
under natural light conditions showed
swarming activities at dawn and dusk
(Gidholm, 1969). Artificial prolongation of
the photo- or scotophase resulted in cor-
LIGHT AND REPRODUCTION IN TYPOSYLLIS
441
Pfannenstiel, 1984). The reproductive
endocrinology of male T. prolifera and the
relationship between external and endocrine control of stolonization in this species
have been studied recently (Franke, 1980,
1983a, b). The results are briefly summarized in this section (Fig. 7).
Sexual development is controlled by at
least two distinct hormonal factors, the
sources of which are clearly separated
from each other. One of the factors, presumably a neurosecretion, is released by
the prostomium; a second one, already suggested by previous investigators (Durchon,
1959; Wissocq, 1966), emanates from an
unknown, perhaps non-neuronal source
located in the pharyngeal region, closely
connected with the proventriculus (Fig. 2).
The prostomial factor stimulates, the proventricular factor inhibits the onset of sexual development. The experimental evidence suggests that they together constitute
an endocrine two-step system, sexual
development naturally resulting from a
suppression of proventricular activity by
the prostomial hormone. The alternative
implementation of nonreproductive/
reproductive development under "winter"
and "summer" conditions, respectively, is
clearly correlated with and probably
mediated by a change in the endocrine status of the animals. Similarly, hormones are
involved in the control of the reproductive
rhythm in "summer" animals; they transmit the cyclic signals of the endogenous
clock to the peripheral tissues.
In animals under nonreproductive "winter" conditions, prostomia are endocrinologically inactive; proventriculi, in conENDOCRINE PATHWAYS OF
trast, show high and constant endocrine
REPRODUCTIVE TIMING
activity which prevents reproduction. StoThere is considerable evidence from a lonization in "winter" animals can be
large number of quite disparate animals induced experimentally (1) by implantathat environmental control of develop- tion of a prostomium from a reproductive
mental processes often involves an inter- donor, as well as (2) by extirpation of the
vention of (neuro-)endocrine mechanisms. proventriculus. In the former case, only a
One of the best documented examples is single stolonization process is induced, after
the control of insect diapause by temper- the completion of which the nonreproducature and daylength {e.g., Williams, 1969). tive condition is restored. Removal of the
The endocrine mechanisms intervening in proventriculus, however, results in perthe control of reproduction in polychaetes manent stolonization, i.e., in a close succesare remarkably diverse according to family sion of stolonization processes without
or even to genus (Olive, 1979; Franke and intervening periods of caudal regenerarelated delays of the swarming peaks.
Responses to various artificially manipulated conditions of illumination indicated
that swarming is directly evoked by changes
in light intensities such as naturally occur
at dawn and dusk. A positive phototaxis
may lead activated worms up to the water
surface.
Stolons of T. prolifera can be collected at
the water surface of the native habitat only
within one hour after sunrise (Fig. 1C),
suggesting that swarming and spawning
under natural conditions take place early
in the morning. Laboratory experiments
indicate that a circadian rhythm plays little
or no role in this diurnal pattern (Franke,
unpublished). Probably as an immediate
response to morning sunlight, mature stolons, which are still loosely attached to their
stocks, start vehement undulatory movements, thereby breaking away, and then
swarm up to the water surface. During
swarming, male stolons spawn "spontaneously" {i.e., independent of a present
female), but female stolons usually spawn
only in the presence of a spawning male.
This suggests a mechanism for final adjustment of female spawning, presumably
involving the action of a pheromone which
is released by a spawning male and ensures
shedding of eggs at just the right time and
in the right place. Such pheromones implicated in spawning behavior have been suggested also in some other swarming polychaete species such as Brania clavata
(Hauenschild and Hauenschild, 1951),
Autolytus edwardsi (Gidholm, 1965) and
Platynereis dumerilii (Boilly-Marer, 1974).
442
HEINZ-DIETER FRANKE
10 °c
LD 1 0 : 1 4
20 C
LD 1 6 : 8
C y c l e of
moon l i g h t
Circalunar
clock
Prost omiu m
Endocrine
activities
Proventriculus
I I I J
I
l®I I I I
Overt
rhythm
Non - r e p r o d u c t i v e
Cyclic
stolon
release
FIG. 7. Diagram summarizing the experimental evidence on the role of hormones (prostomial and proventricular factor) in the control of stolonization in male Typosyllis prolifera. 1, entrainment of the circalunar clock
by zeitgebers associated with the cycle of moonlight; 2, stimulation of hormone secretion in the prostomium
at well-defined recurring periods of time controlled by the clock; 3, temporary inhibition of proventricular
secretory activity in response to a hormonal signal of the prostomium; 4, inhibition of sexual development
by the proventricular hormone. R and S, regeneration phase and stolonization phase of the reproductive
cycle. It is unknown whether the prostomium in "winter" animals remains inactive because the clock does
not run in these conditions, or because there is no coupling between an ongoing clock and the prostomial
endocrine center.
tion, until nearly the whole worm has
become transformed into a number of stolons. Reimplantation of the proventriculus
can stop permanent stolonization.
Transfer of nonreproductive "winter"
animals to "summer" conditions provokes
an endocrine activity in the prostomium,
followed by a decrease in proventricular
secretory activity and, ultimately, the onset
of visible sexual development. After two
weeks of exposure to "summer" conditions, worms do not yet show any visible
signs of an imminent onset of sexual development, but their prostomia have now
become able to induce stolonization when
transplanted into "winter" animals.
In animals kept under continuous "summer" conditions, both the prostomium and
the proventriculus probably undergo
rhythmic changes in their endocrine activ-
ities, connected with and probably controlling cyclic stolonization. (1) The endocrine activity of the prostomium may be
subject to control by the circalunar clock:
In in vivo experiments, a prostomial activity
could only be detected within a short period
spanning a few days of the 31-day stolonization cycle. This period coincides with
the late regeneration phase (about 12-14
days after release of the previous stolon),
i.e., with that time when the clock triggers
the onset of the next stolonization process.
Decapitation before this "critical" period
reliably prevents stolonization (except the
proventriculus has been removed too), but
decapitation after this period remains ineffective. (2) In in vivo experiments, proventriculi were found to be significantly
more active during the regeneration than
during the stolonization phase of the
LIGHT AND REPRODUCTION IN TYPOSYLLIS
reproductive cycle. Probably in response
to the prostomial cycle of hormone secretion, proventricular endocrine activity
drops periodically, releasing worms from
endocrine inhibition, and in this way
mediating the cyclic initiation of sexual
development. Towards the end of each stolonization phase, proventriculi restore their
activity and, by inhibiting an immediate
onset of the next phase of sexual development, enable an intermediate period of
caudal regeneration. As in "winter" animals, extirpation of the proventriculus
leads to permanent stolonization.
The concept summarized in Figure 7 is
supported by a variety of experimental
data. Nevertheless, conclusive evidence
requires further investigations, particularly the identification of the cellular
sources of the supposed hormones and,
furthermore, the characterization of the
hormones themselves.
SUMMARY AND CONCLUSIONS
Reproductive processes in the studied
field population of T. prolifera take an
annual (1), a lunar (2), and a daily pattern
(3). It is an interesting feature of this species
that its synchronization with all three
external cycles may primarily be achieved
by exploitation of natural light changes as
sources of environmental information.
(1) Although perhaps a complex of interacting factors is involved in the timing of
reproduction to a spring-summer breeding
season, the seasonal change in relative daylength appears to be of major importance.
It probably acts through direct input as the
limiting "necessary condition" for reproduction, in the absence of an underlying
endogenous program. However, other
types of photoperiodic effects have been
suggested in the discrete-polytelic Harmothoe imbricata and Kefersteinia cirrata:
Daylength as a rate-controlling variable,
and daylength as a zeitgeber to an endogenous circannual rhythm. These findings on a yet very limited number of polychaete species suggest that photoperiodic
responses, well known particularly from
terrestrial and freshwater organisms, can
also be important for the regulation of seasonal reproduction in polychaetes, and that
443
in some instances such as T. prolifera daylength may even be the dominant environmental variable. Critical daylength values
have been determined in T. prolifera and
H. imbricata, yet nothing is known about
the mechanism of daylength measurement
in polychaetes.
(2) The change in dim nocturnal illumination connected with the cycle of lunation (period: 29.5 days) probably provides
the decisive information for the generation and maintenance of the lunar-monthly
population rhythm of breeding. The situation in T. prolifera basically corresponds
with that described nearly 30 years ago in
Platynereis dumerilii. No evidence suggests
that moonlight exerts any direct effect on
developmental a n d / o r behavioral processes. Rhythmic reproduction is rather
based on circalunar oscillators, while
moonlight acts as a zeitgeber which entrains
the individual rhythms and thus permits
their recognition at the population level.
From the results in P. dumerilii and T. prolifera it appears that the cycle of moonlight
plays a major role in generating moonrelated reproductive phenomena in polychaete populations. Nothing is known,
however, about the mechanisms of moonlight perception and a possible involvement of the circadian system in this process.
(3) The daily light-dark cycle probably
controls daytime-related swarming in T.
prolifera and Autolytus edwardsi. In both
species, the light changes may act by direct
input. There is no evidence in any polychaete suggesting a role of circadian programming in diel timing of reproductive
behavior. However, this might change
when the problem is studied in more detail
and in a wider range of species.
Synchronization of reproduction with a
particular phase of the annual cycle may
serve to maximize the survival of offspring
which probably will find most suitable conditions of development at this period of
time. However, the ecological conditions
which make the spring-summer period
more suitable for the development of young
Typosyllis than other times of the year, are
unknown.
Timing of reproductive processes in
444
HEINZ-DIETER FRANKE
relation to the lunar and daily cycles may
be interpreted as a mechanism which, by
generating some within-population synchrony, maximizes the probability of fertilization. It cannot be excluded, however,
that the particular phasing within the lunar
and daily cycles might additionally reflect
an adaptation to some unknown ecologically important environmental changes
associated with these cycles.
As emphasized by Clark (1979), highly
synchronized spawning in a population may
usually result from sequential environmental input at various stages of reproduction.
T. prolifera is a good example of this concept. The initiation of the breeding season
by the increase of daylength beyond a critical level might introduce an initial but
probably (because the critical level may differ slightly among individuals) not very
precise reproductive synchrony in a population. Without reinforcement by specific
environmental signals, even this weak synchrony would gradually be lost during the
breeding season, through natural variation
in the period of the endogenous reproductive rhythms. Synchronization within
the prolonged breeding season involves at
least three separate sequential processes,
relating to both developmental and behavioral aspects of reproduction. The basic
synchronizing influence may result from
the cycle of moonlight which entrains the
circalunar clocks in the individuals. In an
entrained population, worms tend to initiate sexual development more or less synchronously within a few days of each lunar
month. With a constant phase relationship
to the rhythmic initiation of stolonization,
large numbers of animals attain sexual
maturity, and become able to respond to
further synchronizing stimuli, at nearly the
same time. Environmental input at this
stage serves to synchronize the final behavioral processes of reproduction leading to
fertilization. Morning sunlight provokes
synchronous detachment of mature stolons
from their stocks, followed by surface
swarming and, in males, by spawning within
the first hour after sunrise. Spawning in
females, ultimately, is subject to a kind of
fine control, probably mediated by a male
pheromone which ensures the shedding of
eggs in the presence of sperm.
As it is known of other animal groups,
sexual development includes an intervention of hormones between the controlling
centers and the peripheral tissues involved
in sexual and somatic maturation. The
experimental evidence suggests that both
stimulating and inhibiting hormonal activities are involved which may operate
sequentially in the manner of a neuroendocrine second-order system. The cellular
sources of the hormones, their chemical
nature and exact mode of action are
unknown. Environmental factors (daylength, moonlight) which affect the developmental processes of reproduction, probably act through changes in the endocrine
status. External factors (daily light-dark
cycle, pheromones) involved in the timing
of the behavioral processes of reproduction, however, may act through neuronal
activities which ensure the promptness of
the responses.
Despite the considerable gaps which
exist, recent investigations on environmental and endogenous control of reproduction in a range of polychaete species
have yielded some progress in this field,
and have shown the ways which might lead
to a real understanding of how reproductive cycles in this ecologically and phylogenetically important animal group are
coordinated and synchronized.
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