The Periodic Fruiting of Dictyota and Its Relation to the Environment
W. D. Hoyt
American Journal of Botany, Vol. 14, No. 10. (Dec., 1927), pp. 592-619.
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T H E PERIODIC FRUITING O F DICTYOTA AND ITS RELATION T O T H E ENVIRONMENT (Received for publication May 19, 1927)
The periodic production of the sexual cells of Dictyota has been described for Bangor, Wales, and Plymouth, England, by Williams (1905);
for Beaufort, North Carolina, by Hoyt (1907); and for Naples, Italy, by
Lewis (1910). Further studies have now been made a t other places on the
coast of North Carolina, a t Naples, and on material obtained from Jamaica,
and some additional facts have been observed. While these do not seem
to explain the phenomenon, they furnish material which must be considered
and offer suggestions as t o the possible nature of the problem.
At all places where studies have been made, all observed species of
Dictyota produce their sexual cells in periodic crops a t intervals more or
less definitely related t o the tides of each region. The relation to the tides
varies, however, in different localities, and three differenttypes of periodicity
have been observed: one shown by Dictyota dichotoma a t Bangor, Wales;
Plymouth, England; and Naples, Italy; the second shown by all observed
species of Dictyota on the shore of Jamaica; and the third shown by the
species of Dictyota resembling D. dichotoma occurring a t several places on
the coast of North Carolina.
RECORDS
Bangor, Wales
According to Williams (1905)Dictyota dichotoma a t this place produces
its sexual cells a t fortnightly intervals, the rudiments appearing during the
summer a few days before the neap tides, and the mature gametes being
liberated two to three days after the greatest succeeding spring tide. The
time taken by the average of the crop to pass from initiation of rudiments
to liberation of gametes varies from thirteen to sixteen days, seeming to
depend on the number of days between successive spring tides. This tide
interval is said, however, not to affect the time of liberation, but only the
length of time for average development. During October the crops are
1 These studies were assisted by grants from the Elizabeth Thompson Science F u n d ,
the .kmerican Association for the Advancement of Science, and the Department of Botany
of the Carnegie Institution of Washington. The studies a t Beaufort, N. C., were made
while the author occupied a table a t the Fisheries Laboratory a t that place, and additional
material from t h a t vicinity was obtained through the cooperation of the U. S. Bureau of
Fisheries. At Naples t h e author occupied the table of the Smithsonian Institution a t t h e
ZoGlogical Station. T o all of these organizations grateful acknowledgment is made for the
assistance rendered.
592
Dec., 19271
HOYT - PERIODIC FRUITING OF DICTYOTA
593
retarded until the relation between the times of initiation and liberation and
the neap and spring tides is almost reversed. The time taken for development of the average of the crop is, however, not lengthened.
Plymouth, England
At this place also, according to Williams (1905), Dictyota dichotoma
produces its sexual fruits a t fortnightly periods, bearing definite relations
to the tides, but a t different times from those of Bangor. Here rudiments
appear about the time of neap tides and liberation occurs four to six days
after the next greatest spring tide. Here also the length of time for average
development varies with different crops, but is believed by Williams to
depend on the actual height of the tides rather than on the length of the
interval between successive spring tides.
Naples, Italy
As has been described by Lewis (1910) Dictyota a t Naples produces its
sexual cells in more or less definite crops a t fortnightly intervals, the rudiments appearing about the time of the least neap, and the mature gametes
being liberated about the time of the following least neap tide. The length
of time taken for average development of the crop is about fourteen to
fifteen days. The development of a single crop is, however, spread over a
relatively long period so that great differences in the stage of development
of the fruits are found a t the same time. Lewis (1910) has cited the collections of one day to illustrate the differences occurring between the stages of
development of the fruits of different plants. The illustration given is, in
fact, the rule rather than the exception. Moreover, different sori on the
same plant show differences in their stages of development even more
pronounced than those noted by Lewis for different plants. In one third of
the collections examined by the author, male plants were observed bearing
sori in all stages of development from undivided rudiments through mature
and liberated gametes. Moreover, the discharge of mature gametes is
spread over many successive days. Thus one female plant collected on
March 16 with about 2 percent of its sori discharged, and kept under observation in the laboratory, showed approximately the following percentages
of total discharge on the succeeding five days-10 percent, 50 percent, 80
percent, 95 percent, and IOO percent. This, however, is rather an extreme
case. Thus three female plants collected on April 2 were kept under observation in the laboratory. Of these, one when gathered was about 60 percent
discharged, no eggs were shed the next day, and on the following day only
about 10 percent more had been shed. The second when gathered showed a
few eggs shed but no sori completely discharged, by the next day it had shed
about go percent of its crop, and by the following day had practically completed its discharge. The third when gathered had no eggs shed, by the
next day it had discharged about 40 percent, and by the following day about
594
AMERICAN JOURNAL O F BOTXSY
[ T o ] . 14,
95 percent, of its crop. Two days later (on April 6) eight sexual plants
gathered showed complete discharge from six, but the two others were only
about one-third shed. All of these last-mentioned plants bore the new
crop, mostly having undivided rudiments, but a few antheridia showing four
to eight cells in surface view. Plants newly gathered showed the same course
of events as those kept in the laboratory. Of twenty-nine collections made
between March 3 and May 12, nineteen showed undivided rudiments and
twenty-six showed evidence of partial or complete shedding from some or all
of the plants. This being true, and the initiation, de~elopment,and liberation of the sexual products being spread over so long a period, the question
naturally arises as to how we can speak here of periodic crops. In fact, it
was only by tabulating his records in a calendar form that the author was
able to demonstrate satisfactorily the existence of periodicity a t Naples.
IYhen this is done, however, it is evident that crops are produced a t regular
intervals, the mean condition of the sori on the majority of the plants showing formation of rudiments, development of fruits, and liberation of the
sexual cells a t fortnightly intervals. This prolonged period of fruiting, with
its consequent irregularity in individual plants and individual sori, seems an
interesting and suggestive feature, especially when compared with the behavior of plants in Jamaica and on the coast of North Carolina. These
features will be discussed later.
As a t Bangor and Beaufort, plants kept in the laboratory removed from the changing conditions of their environment maintained the same fruiting periods which they showed in their natural habitat. Thus ten plants kept in the laboratory from twenty-four to thirty-five days bore two crops of fruits in regular succession, each plant showing fruits of the same stages as those found on plants brought in from the sea a t the same period. Jamaica
I t has previously been noted by Hoyt (1907) that specimens of Dictyota
from Port Antonio and Port Morant, Jamaica, showed evidence of periodicity in the production of their sexual fruits, and that the female plants from
Port Morant bore crops of two ages, the younger of these having the stage
of development corresponding to that of the sori of the male plants collected
a t the same time. With the aid of a native c ~ l l e c t o r nine
, ~ collections of
Dictyota dentata Lamour. were made a t Hope Bay, Jamaica, a t intervals of
two to four days from October I through October 22, 1907. These contain
forty-one sexual plants, both male and female, so that a fair conclusion regarding the fruiting of D. dentah a t this place may be formed. The most
striking fact noted is that, while all the sexual plants had their fruits a t
about the same stages of development with the apparent production of regular crops, there was no perceptible change in the condition of the crops during
the entire ~ e r i o dof twenty-two days. Of the plants collected during this
These collections as well as those made in 1909 were obtained through the kindly assistance of the late Mr. William Harris.
Dec., r g z j j
HOYT
- PERIODIC
FRUITING O F DICTYOTA
595
time, twenty-one had completed from ten to ninety-nine percent of total
discharge of the sexual cells, fifteen of these having completed a t least ninety
percent. Thirteen plants had their fruits apparently mature, nine of these
having shed a few of their sori, while only two plants had their fruits only
half mature, and these were gathered near the end of the period of collect i o n . V n every collection made during this period of slightly more than
three weeks, every fruiting sexual plant, with the exception of the two noted
above, had its sexual cells mature or partly discharged. The condition of
fruiting was so uniform throughout the whole period that the question arose
as to whether the collections had been properly made and dated. Evidence
furnished by the slips accompanying the collections seems to answer this
question satisfactorily. I t appears, then, that a t Hope Bay Dictyota
dentata produces its sexual cells in regular crops, but that these crops take
so long a time to mature and to be liberated that there is no perceptible
development in them during a period of twenty-two days.
The second fact to be noted here is that the majority of the sexual plants
bore crops of two ages a t the same time. Of the thirty-six plants fruiting
sufficiently for consideration, nineteen (thirteen females and six males) bore
younger sori of a distinctly different age in addition to the crop included in
the enumeration above. Although the older crop may include a few younger
sori, there is a distinct gap between the age of these and the age of the
younger crop, which had its sori in about the stage corresponding to the
antheridia with eight cells in surface view. The fruits of this younger crop
are scattered among the older ones, especially toward the tips and extending
beyond the older fruits toward the apices.
Further collections were made for the author by the same collector
during October, 1909, but with less success, the plants gathered consisting
almost entirely of Sargassum and other large brown algae. Only three
fruiting plants of Dictyota were obtained, all of these being female plants of
D. dentata. Two of these were collected October 5 ; one bore two crops, the
older having eggs apparently mature with a few shed, and the younger
having its fruits about half mature; the other was a small plant bearing only
one crop with its fruits about half mature, apparently corresponding to the
younger crop on the other plant; the third plant was gathered October I I
and bore two crops whose stages of development seemed to correspond
exactly with those of the first plant mentioned under October 5 above,
except that it had shed a few more eggs. While these three plants alone
would be of little value in forming a conclusion, they agree exactly with the
results noted on the plants gathered in 1907, and strengthen the evidence
furnished there.
A collection of twenty-eight plants, including specimens of D. dichotoma
and D. ciliolata Kuetz., gathered a t Kingston, Jamaica, July 28, 1926, was
The five plants not mentioned in this enumeration were fruiting so sparingly t h a t no
conclusions could be drawn from them. The fruits present were, however, in the same
condition as those described above.
596
AMERICAN JOURNAL O F BOTANY
[Vol. 14.
kindly furnished by Professor J ~ h n s o n . ~As is usual with collections from
this region, most of the plants were tetrasporic, but six of these were female
and two were male. Three of these females (one D. dichotoma and two D.
ciliolatu) bore crops of two distinct ages, the older crop being mature or
nearly so, having shed the eggs from a number of its sori, the younger crop
having rudiment.; which were scarcely evident under the microscope. The
other three females bore only one crop, one (D. dichotoma) having young
fruits corresponding to the younger crop, and two (both D. ciliolata) having
fruits mature or nearly so, corresponding to the older crop mentioned above.
The two males were both D. dichotoma and bore fruits of uniform age, all
of these showing one to two cells in surface view, about corresponding to the
younger crop of the females.
The plants from Port Antonio and Port Morant noted by Hoyt (1907)
add to this evidence and, taken with the others mentioned above, suggest
a possible conclusion. Since the plants studied belong to more than one
species and come fram four different localities in four summers, we seem
warranted in making a tentative generalization that, on the coast of Jamaica,
different species of Dictyota show the same type of fruiting, bearing their
sexual cells in regular crops, but so prolonging the period of their development as to produce almost continuous fruiting with a distinct overlapping
of two successive crops and to obscure the regularity in the intervals of their
production. Certainly we cannot, with our present knowledge, predict the
time of fruiting in Jamaica as we can in the other regions where Dictyota
has been studied. This fact, especially when considered in relation to the
tides of the different regions, affords an interesting basis for comparison and
possible generalization.
Beaufort, North Carolina
An account of the fruiting of Dictyota a t Beaufort in the summer of
1906 has been given by Hoyt (1907). Further studies of the fruiting of this
alga have been made there by the author during the summers 1907-1909, and
plants collected according to his directions by members of the laboratory
staff in the summers of 1910, 1912, 1917, and 1921 have been examined.
We thus have partial or more or less complete records for eight summers
extending over a period of sixteen years and are able to generalize about the
behavior of Dictyota in this region. The records obtained are summarized
in table I . From these records the following facts are evident: ( I ) At
Beaufort fruiting of sexual plants always occurs during the spring tides of
the full moon, regardless of whether these are the greater or the lesser set of
spring tides of the lunar month. This relation of fruiting to the time of the
full moon holds so regularly that, when the author wished collections made
and did not have tide tables available, he was able to calculate the times of
fruiting from a calendar giving the date of the full moon. In every year
4 The author is gratefully indebted to Professor D. S. Johnson for this material and t o
Dr. Marshall A. Howe for the determination of the Jamaican species.
Dec., 19.271
HOYT
- PERIODIC
FRUITING O F DICTYOTA
597
collections were made during the spring tides of the new moon in addition
to those made during the full moon, and in not a single instance during the
eight years when records were obtained did the plants fruit a t any time other
than that of the period of the full moon. (2) The time of fruiting and of
liberation of the sexual cells follows the periods of the full moon and the
tides as given in the tide tables, and is not altered by the height of the tides
actually observed. During the four summers 1906-1909 almost daily
records were kept of the tides occurring in the harbor. Due to wind and
other causes, these frequently varied from the heights given in the tables, in
extreme cases low water of one set of tides being higher than high water
of another set; yet the sexual plants of Dictyota fruited at their regular
intervals with no apparent relation to the actual height of water to which
they were exposed. In a few cases (as in October, 1908, and, presumably,
in October, 1921) the weather was cold, and the fruiting of the plants was
retarded and irregular, but in no case did any set of conditions induce fruiting
a t any time other than the regular periods, and in no case was there evident
any relation between the actual height of the tides and the actual days when
fruiting occurred. (3) The time between the general liberation of two successive crops varied between twenty-nine and thirty-one days.6 The time
between the greatest spring tide of the full moon and the subsequent liberation of gametes varied between four and seven days. The time between
the date of the full moon and the subsequent liberation of gametes varied
between five and eight days. (4) The variations in the times of fruiting
within the limits noted above occur not only in different summers but in
different crops in the same summer. These variations do not seem to be
related to the actual height of the tides since, although a t times higher tides
have been followed by later liberations, a t other times periods when tides
were extremely high were followed by liberation a t the same interval as in
periods when tides were extremely low. (5) The number of days between
the general liberation of successive crops corresponds closely to the number
of days between successive full moons and to the number of days between
the greatest spring tides of successive full moons. The period of fruiting
does not always exactly correspond either to the interval between the moons
or to the interval between the tides, but differs from these by not more
than one or two days (except in irregular crops), sometimes being slightly
greater, a t other times slightly less. When it is recalled that it is difficult,
and sometimes impossible, to determine the one day which shall be called
that of the greatest spring tide, it will be realized that the correspondence of
fruiting period to tidal interval may be closer than shown in the table and
may, in fact, be a very exact one. (6) While the development of the crops
may be retarded by unfavorable conditions, their production has not been
Except in the two cases where lateness and irregularity were caused by unfavorable
conditions. The slightly different figures given in 1910 and 1912 are due t o the inability t o
determine, from the collections made for the author, t h e exact day of general liberation.
TABLE
I . Record of Fruiting of Dictyota at Beaz~fort,N. C., with Relation to Tides and Moon
Days
Of
New Moon
I
Tide of: No. of Days Since
Greatest Spring
Tide of Last Full
Full l o o n Moon
~ ~ i l o & ~No.
~ of~ Days
o f Since
" ~ ~
General Libera~~~~h to ~ ~ 1 1
tion of Last
Crop
Month
loon
of present
Day of General Liberation
wit11 Estimated I'ercentage of
Total Discharge of
Eggs
No. of Days After Greatest Spring No. of Days After Tide of Full Full Moon Moon 1906
July 23t
Aug. 4*
29
30
Sept.
29
29
29
31
30
30
Aug. 2I*
2t
Sept. 20*
Oct. 3t
Aug.
6 6 S e ~ t 8,
. 95%
6 6 Oct. 8,85%
5 6 July
5 6 10
1907
June 9t
June 26*
29-30
29
July 25*
29
29
1,
85%
July 9t
Aug. ~ o t
hlay 29t
Aug. 29t
J u l y 31,85%
6 7 Aug. 29,70%
6 6 June
20,98%
5 6 Aug. 23*
29
June IS*
29-30
30
July 14*
29
29
29
July 19,80%
5 6 Aug. 13*
30
30
30
Aug. 18,70%
5 6 Scpt. I I*
29
29
29
Sept. 16,85%
5 6 Oct. IO*
29
29
31-32
Oct. 17, 50% and 18(cold,
irregular)
7-8 8-9 30
I
Juric 271
July 267
30
Sept. 281
29
I
TIDES
CROPS
Days of Greatest Spring Tide of: N o. of Days Since No. of Days from NO. of Days Since
~ ~ M~~~
1 1 of L~~~
Greatest Spnns
~
~ to ~~ ~ 1tGeneral
1 l Libera~
Tide of Last Full M~~~ of present
tion of Last
New Moon
Full Moon
Moon
Crop
Month
Day of General Liberation
with Estimated Percentage of
Total Discharge of
Eggs
No. of Days After
No. of Days After
Greatest Spring
Full Moon
Tide of Full
Moon
I909
M a y 19*
June 17*
July 14t
Aug. 141
4
6
4-5
5-6
Aug. 7,70%
4
6
Sept. 6, 40% and 7, 55%
6-7
6-7
02. 7, 95%
7
8
July 28-29?
5-6?
6-71
Aug. 26-27?
4-5 1
6-i?
Sept. 25-26?
4-5 1
7-8?
June 5 t
30
29
July 4 t
29
30
30
July 8,
Aug. 3*
3@
29
29
Aug. 31*
28
30
3*3
Sept. 30*
30
29
31
July 23t
30
30
Aug. 22*
30
29
29-30?
Sept. 21*
30
29
29-30?
June 9,95%
I
20%
a n d 9, 70%
Sept. 1 3 t
July i *
Aug. 5 t
Sept. g t
1912
Days of Greatest Spring Tide of: No. of Days Since No. of Days From NO. of Days Since
~ ~ M~~~
1 1 of L~~~
1
LiberaGreatest Spnng
~~~~h to ~ ~ 1 General
Tide of Last Full M~~~ of present
tion of Last
New Moon
Full Moon
Moon
Month
Crop
I
Day of General Liberation
w ~ t hEstimated Percentage of
Total Discharge of
Eggs
No. of Days After
Greatest Spring
Tide of Full
Moon
No. of Days After
Pull Moon
0
July 6*
Aug. 4*
Sept. 2*
Oct. I *
>
9
July 25, 85%
6
5
td
30
Aug. 24,90%
6
6
2
30
29
Sept.
4
5
2
29
34?
Oct. 261 (irregular)
July 19t
31
30
Aug. 18*
30
29
Sept. 181
31
30
Oct.
1st
* Greater set of spring tides of lunar month.
1. Lesser set of
spring tides of lunar month.
22
8?
IO?
0
Dec., 19271
HOYT
- PERIODIC
FRUITING O F DICTYOTA
601
advanced or caused a t any time other than the regular ones by any method
of experimentation which has yet been devised. Thus two sexual plants
were placed in lighter and darker boxes and partly submerged in the harbor,
the plants being transferred to the lighter box a t neap and to the darker
box a t spring tides, thus reversing the usual light conditions. This treatment was unfavorable to the plants so that portions of them died, but the
parts that remained alive after exposure, in this way, to two and three sets
of tides, respectively, fruited on the same days as the plants growing under
natural conditions in the harbor. Numerous plants were kept in the
laboratory for periods of from three to eight weeks. Such plants were always injured by the relatively unfavorable conditions, the sori of fruiting
specimens being retarded or checked in their development, and the greater
portions of the plants dying. Some parts, however, remained alive and
frequently formed small side branches. All portions which remained alive
and capable of fruiting, the new branches which had never been subjected
to tidal influences as well as the old parts, bore their fruits a t the same periods
as did the plants growing under natural conditions. Such plants in the
laboratory were often one or two days behind the plants of the harbor in
discharging their sexual cells, but this is probably to be ascribed to the effect
of unfavorable conditions. This conclusion seems warranted by the fact
mentioned above that fruiting plants brought to the laboratory frequently
had the development of their fruits retarded or checked, and by the further
fact that plants in the harbor had their crops retarded and rendered irregular
by unfavorable weather conditions. The remarkable fact is that, under
conditions that are so unfavorable as to kill the greater portions of the plants,
the fragments that remain alive should still retain their fruiting period.
Evidently this periodicity is very firmly impressed on the protoplasm of the
plants. (7) As elsewhere, the non-sexual plants showed no periodicity, but
produced their tetraspores continuously throughout the summer.
The average rate of development of the sexual crop a t Beaufort is shown
in the following schedule.
First day: Sori not visible to naked eye, visible under microscope, sex not distinguishable,
very few older sori.
Second day: Sori not visible to naked eye, clearly visible under microscope, sex not distinguishable, few older sori.
Third day: Sori barely visible to naked eye, sex distinguishable by slight difference in color
of fruits, sterile border cells of male sori beginning to be differentiated, rudiments
undivided.
Fourth day: Male fruits 1-16 cells in surface view, sori of different ages, male sori clearly
visible to naked eye, female slightly so.
Fifth day: Male fruits 2-64 cells in surface view, mostly 16 cells, sori of different ages, both
sexes easily visible to naked eye and easily distinguished.
Sixth day: Male fruits 1 6 6 4 cells in surface view, mostly 16--32.
Seventh day: Male fruits mostly 64 cells in surface view, few 32 cells, very few 16 cells, and
few discharged.
Eighth day: General liberation of gametes.
Ninth day: Liberation of all, or nearly all, remaining gametes.
602
[Vol. 14,
AMERICAN JOURNAL O F BOTANY
The initiation of rudiments usually begins the day before or the day of
full moon (one or two days before the greatest spring tide), and genera1
liberation of the gametes usually occurs six to seven days after the full moon
(five to six days after the greatest spring tide). In individual crops liberation may occur from five to eight days after the full moon (four to seven
days after the greatest spring tide), with corresponding earlier or later
initiation, the fruiting period following the date of the moon more closely
than the date of the spring tide. The following table shows the number of
times when liberation occurred on the respective days after the greatest
spring tide and after the full moon.
Days After Greatest
Spring Tide
a
1
i
No. of liberations.. . . 5
7
6
1
7
Days After Full Moon
5
---- -N o of l i b a t i o n . .
3
1
2
6
7
8
-- 15 3
I
--
I t will be observed that liberation occurred a t a much more regular
interval after the full moon than after the greatest tide, 68 percent of the
observed crops discharging their sexual cells on the sixth day after the full
moon, although this may be due to the difficulty of determining the day of
greatest tide.
In any crop, individual plants, or single branches of a plant, or even
parts of a branch, may vary from the general crop, being either earlier or
later, such variations usually not being greater than one day. Occasionally
the general liberation of gametes may extend over two days, with belated
sori discharging a day later. Considerable variation in the amount of discharge on a single day may occur in the plants during any one season.
Thus in 1909 (see table I ) , the July crop shed about 20 percent on July 8
and 70 percent on July 9 ; the Augujt crop shed about 70 percent on August
7 and the remainder on August 8 ; the September crop shed about 40 percent on September 6 and j j percent on September 7 ; while the October crop
shed about 95 percent (all except the younger fruits a t the tips and a few
scattered sori) on a single day. Such variations are due to differences in
the behavior of individual plants; when a small percentage of crop discharge
occurs, some plants are found to have shed nearly all their sexual cells, while
others have shed few or none.
In general, however, the plants are remarkably uniform in their fruiting,
an average of about 80 percent of their sexual cells being discharged on a
single day and about 60 percent to 70 percent being discharged in a single
half hour. I t appears that many of the fruits that are formed later develop
more rapidly, so that they catch up with the earlier ones, since greater
differences are found in the earlier stages of development than in the later
Dee., 19271
HOYT
- PERIODIC
FRUITING OF DICTTOTA
603
stages or in the time of discharge. A similar behavior was noted by Williams
(1905) in the plants a t Bangor. At Beaufort the fruits begin to appear in
the intermediate parts of the plant that are mature and vigorous, but not
old; from there they extend toward the tips and base, but are never produced
on the old basal portions. On many plants they are formed within 1-2 mm.
of the apex (and occasionally within 0.2 mm. of the apical cell), while on
other plants 1-3 cm. (sometimes u p t o 5 cm.) of the apical portions remain
sterile a t the time of fruiting. These are probably, in the former case, plants
that have for the time ceased their growth and have matured the thallus
up to the apices; and, in the latter case, plants that are growing actively
and have not reached maturity in the apical portions. I t thus seems that
we have, in this alga, conditions of youth, maturity, and old age in different
parts of the same individual. A given portion of the thallus will not fruit
until it has attained a certain condition of maturity (whatever that condition
may be), and becomes incapable of producing reproductive cells when it has
passed into the condition of old age. From these old portions, however,
branches may be given off which, in their turn, pass through similar phases.
Among the fruiting plants are found many small, vigorous individuals which
bear no fruit of any kind. While some of these are probably asexual plants,
others are undoubtedly sexual ones which have not matured sufficiently to
reproduce a t the fruiting season. This is indicated by the fact that such a
plant which appears sterile is sometimes found bearing a few scattered sori
of sexual cells. The behavior of these plants is particularly striking. Since
they continue their growth, and since new sexual plants are constantly
starting from tetraspores that are shed continually throughout the month,
it seems evident that plants and portions of plants which do not reach the
requisite condition of maturity a t one fruiting period do not fruit as soon as
they reach this condition of maturity, but remain growing vegetatively, and
wait to produce their sexual cells when the next fruiting period arrives a t the
time of the next full moon.
The time taken for the development of a crop (from the appearance of
barely discernible rudiments to the general liberation of the sexual cells) is
here about eight days, as compared with ten to thirteen days a t Bangor and
fifteen to sixteen days a t Naples. This fact may be related to the monthly
fruiting a t the former place compared with the fortnightly fruiting a t the
latter ones. I t may be that a t Beaufort (and a t Wrightsville Beach and the
other nearby localities) the plants during their long vegetative period accumulate materials used in fruiting so that they are able to hasten the
process when the fruiting periods arrive. I t seems certain that this fruiting
exhausts the plants to an extent not observed a t Naples and not reported
elsewhere. Whereas a t Naples the fruiting plants appear little, if any,
lighter in color than before, and the cell contents are altered little or not a t
all, a t Beaufort a different state of affairs is observed. Here, toward the
end of the fruiting period, although the plants appear the usual brown to
39 604
AMERICAN JOURNAL O F BOTANY
[Vol. 14.
the naked eye, examination under the microscope shows the appearance of
dark granules within the cells and a slight massing of the chloroplasts. This
condition continues progressively up to about the time of discharge when
sudden changes are evident, especially in the female plants. In these, plants
which before discharge had appeared brown and only slightly lighter than
usual, immediately after discharge appear grayish white. A microscopic
examination shows this to be due not only to the liberation of the dark eggs,
but also to changes within the vegetative cells of the thallus. Most of these
cells in the fruiting regions of the plant now show only a few dark masses
and light granules in their contents, the chloroplasts having almost or quite
completely disappeared. This condition is usually observed in ail parts of
the plant except the sterile tips, bases, and edges. The plants now quickly
become flaccid and disintegrate to a great extent, many of them being washed
from the rocks and lost. Sometimes, however, portions of the plants remain and send out small branches from their surface, edges, and broken tips,
and these branches then produce later crops of fruits. The male plants
(see Hoyt 1920, P1. 94, fig. 3) have changes a t the time of discharge similar
to those shown by the female plants but to a less extent, a fact that is
probably connected with the greater amount of material required for storing
food within the eggs. The chloroplasts of these males do not disappear but
are somewhat clustered toward the center around dark masses, and are
lighter in color than usual, the plants appearing light brown to the naked
eye. The male plants show relatively little disintegration, but, like the
females, usually send out small branches from various parts of the thallus.
The extent to which these changes take place depends on the amount of
fruiting that occurs. Plants bearing only a few sori show only slight changes
and appear the usual dark brown to the naked eye.
Other Localities
Eight collections of Dictyota were made during the summers 1906-1909
in North River and Core Sound a t four places, three to fifteen miles distant
from Beaufort. In every case the stage of fruiting of the sexual plants was
approximately the same as that a t Beaufort on the same day. Three of
these collections showed the same stage as a t Beaufort, three showed a
slightly more advanced stage, while two showed a slightly later stage, the
same locality varying in this respect a t different times. The differences
observed were, however, with one exception, not greater than those found
in individual plants a t Beaufort, and so can not be regarded as the production
of different fruiting periods by direct response to different environmental
conditions.
During the summer of 1909 search for Dictyota was made a t seven other
localities along the coast from North Carolina to Georgia, but this alga was
found only a t Wrightsville Beach, N. C., about one hundred miles distant
from Beaufort. Six collections were made a t this place in July, August,
Dee., 192jl
HOYT - PERIODIC FRljITIXG OF DICTYOTA
60 j
and September, five of these being made during the spring tides of the full
moon, and one during the spring tides of the new moon. The species of
Dictyota occurring here was the same as that a t Beaufort and, as a t Beaufort, was observed to produce its sexual fruits only a t the time of the full
moon. On the same days that records were made by the author a t RTrightsville Beach, plants were collected for him a t Beaufort, so that comparisons
could be made of the condition of the fruits a t these two places on the same
days. These showed that the times of fruiting were identical in the two
localities, the differences being less than those observed in individual plants.
Moreover, liberation was found to occur on the same days, and apparently
a t the same hours.6
TIDES
Since the fruiting periods of Dictyota usually coincide with the tidal
intervals (or with the state of the moon which, in turn, influences tidal conditions), a comparison of the tides in the regions where this alga has been
studied should be considered. The facts as given by the tide tables of the U.
S. Coast and Geodetic Survey are briefly shown in table 3.
hfean Range
of Tides
(Feet)
Near Bangor, Wales . . . . . . . . . . . . . .
Plymouth, England . . . . . . . . . . . . . .
Naples, Italy. . . . . . . . . . . . . . . . . . . .
Beaufort, K.C.. . . . . . . . . . . . . . . . . .
Wrightsville Beach, N. C.. . . . . . . . .
Hope Bay. Jamaica. . . . . . . . . . . . . .
I 7.9
Range of
Spring Tides
(Feet)
Range of
Neap Tides
(Feet)
Difference in
Ranae of
Sprirk and
Neap Tides
(Feet)
r I .5 0.8 2.7 3.4 0.8 I t will be observed that, a t the European localities, Bangor and Plymouth
have relatively huge tides while Naples has almost none-in fact, a t the
last named place, winds may almost or completely obliterate the tides for
short periods. And yet, at all three of these places, Dictyota produces its
sexual fruits a t regular, predictable, fortnightly intervals. At the American
localities, Beaufort and Wrightsville Beach have relatively slight tides.
The other localities near Beaufort have tides similar to those of Beaufort,
but of less range. As a t Naples, so also a t Beaufort and the nearby places,
the winds may cause great variation from the tide tables, so that the low
tides of some days are higher than the high tides of other days. And yet,
a t all of these American localities, Dictyota produces its sexual fruits a t
regular monthly intervals, at the times of the full moon.
The tides a t all the Jamaican stations have the same characters, and
a t Hope Bay they have practically the same range as a t St. Ann's Bay.
The author is indebted t o Professor I. F. Lewis for this observation made on the time
of liberation a t Beaufort.
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AMERICAN JOURNAL O F BOTAKP
[Vol. 14.
Throughout this region the tides, as a t Naples, are almost negligible, but
they differ from those of Naples in their greater irregularity. Here the
intervals between high and low water vary between three and seventeen
hours, and many days during each month have only one period of high and
low water, while other days have the usual two periods. This fact may be
related to the less regular, more prolonged fruiting condition of Dictyota
observed in this region.
TIMEOF DISCHARGE
The sexual plants not only mature the greater part of their fruits within
a single day, but, both a t Beaufort and Naples, liberate the greater part of
their reproductive cells within a single hour. The time of commencing
discharge of the eggs varies, in the laboratory a t Beaufort, between 3.45 and
5.30 A.M. in different crops, even in the same season. Thus, in 1907,
liberation on three days of July and August, including two crops, commenced
a t 4.55 to 5.00 A M . ; in 1908 the times were: July 19, 4.40, July 20, g.jo,
August 18, 4.30, September 17, 5.30; in I909 the times were: July 9, 3.50,
August 8, 3.45, September 7, 5.15. I'l'hen discharge occurred in the earlier
hours, this began before there was the slightest sign of daylight or the
slightest visible lightening of the eastern sky; but when it waited for the
later hours, it began only after daylight was visible, and, in some cases,
after it had been plainly evident for about fifteen minutes. Of the ten days
when the time of discharge of the eggs was observed (in three summers),
this began before daybreak (when no traces of sunlight were evident) on
four days, a t daybreak (u-hen faint lightening of eastern sky was observable) on four days, and after daybreak (when light was plainly discernible)
on two days. Usually liberation of the eggs began slowly, increasing to a
maximum in about ten minutes, maintaining this rate for fifteen to twenty
minutes, then becoming slower, and practically ceasing about an hour after
commencement. About fifty percent to seventy percent of the eggs shed
are discharged within the first half-hour, but a few, and occasionally many,
are sometimes liberated during the next four or five hours, or even later
during the day. I t has not been possible to determine the exact time of
beginning the discharge of sexual cells from plants in the harbor, but a
visit made to these plants a t 7 A.M. on the day of general liberation showed
discharge of the eggs to have occurred as complete1y:as described above for
the laboratory. The time of discharge of the spermatozoids from male
plants could not be determined as accurately as in the case of the eggs.
These seemed to begin a t about the same time a. the female, or possibly a
few minutes later, and to continue their discharge for a longer period.
Because of the lack of facilities the exact time of discharge from sexual
Beach, but plants gathered a t
plants was not determined a t I~Trightsville
7 A.M. on the day of liberation showed discharge as complete as was the
case with the Beaufort plants a t the same hour. I t seems, therefore, that
not only does fruiting take place on the same days, but that liberation of the
sexual cells occurs a t the same hours a t the tu70localities.
Dec.. 19271
HOYT - PERIODIC FRUITING O F DICTYOTA
607
At Naples the discharge of sexual cells from female plants was observed
on one day. At that place liberation began slowly a t 3.50 A.M., reached its
maximum between 4.00 and 4.10, and, except for an occasional egg, was not
observed after 4.20. At the beginning of the process, not the slightest trace
of daylight was evident, and a t the end there was only a slight lightening of
the sky, so that trees were distinguishable as dark masses against a slightly
lighter background. As a t Beaufort, so a t Naples a considerable number of
eggs were shed later in the day, but about ninety percent were discharged
within the first hour of liberation. Since Naples is far distant from Beaufort, and the fruiting behavior of the plants is different in the two localities,
this observation indicates that the liberation of the sexual cells during a
single hour about the time of daybreak is a general behavior for Dictyota.
I t would be interesting to determine the time of discharge of these plants in
Jamaica, where the fruiting is less regular than in the other regions studied.
The asexual plants, both a t Beaufort and a t Naples, contrast with the
sexual plants not only in producing their fruits throughout the month but
also in discharging their reproductive cells throughout the night and day.
Although more tetraspores were liberated during the night than during
the day, these asexual plants have no definite hour for discharging their
reproductive cells, but liberate them throughout both day and night.
Two questions present themselves: (I) How can the general periodic
fruiting of the sexual plants of Dictyota be explained? (2) How can the
monthly fruiting a t Beaufort and nearby places, with its constant relation
to the full moon, be explained? While we cannot answer either of these
questions, certain pertinent considerations present themselves.
Whether in Europe or America, whether exposed to tides of 18 feet
range (as near Bangor) or to tides of 2-4 feet range (as a t North Carolina)
or to tides of 10 inches range (as a t Naples), wherever the tides are regular,
Dictyota produces its sexual fruits in regular periodic crops on days that can
be predicted within a slight margin of error. Where the tides are irregular
(as in Jamaica) Dictyota prolongs the development of its sexual fruits and
overlaps its crops so that there is only a trace (but yet a distinct trace) of
periodicity in its reproduction. At Bangor, a t Plymouth, a t Naples, and a t
Beaufort the tidal relations are different both in the range of the tide and in
the hours a t which low water of the spring tides occurs, and in each of these
places Dictyota has a different schedule for the initiation of its rudiments, for
the time taken for the development of its crops, and for the day of liberation
of its gametes. The hours a t which low water of spring tides occurs (when
the plants are most exposed owing to the lesser depth of water covering
them) is a t Bangor 4-7 A.M. and P.M., a t Plymouth 11 A.M.-2 P.M.,
a t Naples 3-6 A.M. and P.M., and a t Beaufort 1-3 P.M. I t will be seen
that the time of this low water is nearly the same a t Bangor and Naples
9
608
AMERICAN JOURNAL OF BOTANY
[Vol. 14.
and yet the fruiting behavior of Dictyota is very different a t these two places.
At Wrightsville Beach and the four places near Beaufort the tidal relations
are nearly the same as a t Beaufort, and the fruiting behavior of Dictyota is
the same a t all these places. At Naples, where the tides are almost negligible, the development of the crops is much less uniform than a t Wales,
England, or North Carolina, where the tides have greater range. Moreover,
a single species (D. dichotoma) shows the three types of periodicity observed
respectively in Europe, North Carolina, and Jamaica, with a different
fruiting schedule a t each of the five regions where it has been studied (the
tidal conditions being different in each of these regions), while three different
species (D. dichotoma, D. dentata, and D. ciliolata) all show the same fruiting
behavior a t all the localities in Jamaica from which they have been studied
(the tidal conditions being similar in each of these localities), and D.
dichotoma fruits on the same days and apparently on the same hours a t
Beaufort and Wrightsville Beach (where the tidal conditions are closely
similar).
From the above facts it appears that there is a correlation between the
fruiting periods of Dictyota and the tidal conditions to which it is exposed.
That, however, this periodic reproduction is not due to the direct, immediate
response of the plants to tidal stimuli is indicated by the fact that we find
such plants fruiting according to schedule and not according to the tides to
which they are actually exposed, and by the further fact that they continue
their periodic production of crops when entirely removed from tidal influences. At Bangor Williams (1905) found portions of plants kept in the
laboratory for six months (from October to April) producing a succession of
crops a t the same intervals as shown by plants living in the sea; at Naples
Lewis (1910) noted that plants continued their fruiting periods in the
laboratory, and the author observed plants in the laboratory producing
three crops of sexual cells a t the same times as those growing in the harbor;
a t Beaufort Hoyt (1907) found that not only do plants in the laboratory
maintain their fruiting periods, but that new branchei produced in the culture jars and therefore never exposed to tidal influences have the same
periodicity as the plants living in the sea. At each of these places the
plants removed from the influence of the tides keep the periodicity of their
locality; for example, the new branches a t Beaufort fruit only a t the full
moon.
LYhat, then, is the explanation of this behavior of Dictyota? Williams
(1905) believed i t to be the greater amount of light received by the plants
during the low water of spring tides; Lewis (1910) called attention to the
fact that, a t Naples, initiation and liberation begin when low water occurs a t
midday, but notes that this explanation will not suffice for other regions.
Neither of these suggestions will account for the fruiting behavior a t North
Carolina or Jamaica and hence must be regarded as only two among many
possible factors. We cannot assume that a phenomenon so deep-seated as
Dec., 19271
HOTT
- PERIODIC
FRUITIKG OF DICTYOTA
609
this is called forth by one set of factors in one place and by another set in
another place. I t seems that the fruiting behavior of Dictyota (and comparable behavior of other plants and animals) should be considered as truly
a character of the plant (or animal) as is its form or structure. As the form
and structure have been developed by the interaction of external conditions
and the inherent capacity of the protoplasm, so with the periodic habit of
fruiting. We can explain one to the same extent that we can explain the
other, but no further. Neither is dependent on any single factor or group
of factors in the environment, but is the result of the reaction of the plant
to the sum of all the factors of the environment. The differences in fruiting
a t different localities would thus be accounted for by differences in the
environment a t these places, and also by the fact that, a t each place,
Dictyota is isolated from its relatives. As isolation frequently results in
structural differences in both plants and animals, so it may result in differences in reproductive behavior when this behavior is a plastic character of
the organism. The form and structure of Dictyota have been developed in
the environment in which it grows and would, we can surely believe, be
different if the environment were sufficiently different. In fact, the author
has observed that plants growing under different conditions assume unusual
("abnormal") forms (see Hoyt 1920, PI. 94, fig. 2 c and d), and sometimes
show structures bearing little resemblance to the usual Dictyota plants.
In the same way we find that "unfavorable" conditions interfere with the
usual regular fruiting and produce aberrancies in the crops. I t appears that
the fact that, under unusual conditions, variations appear in both the form
and the fruiting habit is significant and indicates that both are called forth
by the reaction of the plant to the different conditions, and that this is true
in the one case in the same way that it is in the other. According to this
view the reason for variations in individual crops and in individual plants is
to be sought not in the action of any single factor but in the reaction of the
plants to the sum of all the factors of the environment. We have noted
that "unfavorable" conditions produce unusual forms and delay and irregularity in fruiting, but we have not found what conditions, if any, can
cause earlier fruiting. I t is to be noted, however, that, in any crop, fruits
appear first on plants and parts of plants that seem to be in a condition of
vigorous maturity, thus emphasizing the importance of the internal factors
in the response of the plant to external conditions.
While this view is less satisfactory than those previously suggested in
that it is less definite, the facts seem to show that we are not warranted in
making it more definite since the behavior does not seem to be due to the
action of any single, specific factor in the environment. This way of regarding the periodic fruiting does not preclude experimentation, but does
show it to be more complex and difficult, and emphasizes the fact that experiments should take into account all the factors and not attempt the
seemingly impossible task of accounting for the behavior in terms of the
reaction to a single varying condition.
610
AMERICAN JOURNAL O F BOTANY
[l'ol. 14.
Other algae have been found to show more or less distinct periodicity in
their sexual reproduction. Williams (1905) gives evidence suggesting the
occurrence of this phenomenon in Dictyopteris (" Haliseris ") ; Wolfe found,
a t Beaufort, some evidence that Padina Vickersiae produces its sexual cells
in periodic crops a t weekly intervals, although in other cases sexual fruits of
different ages were borne on a single plant (Hoyt, 1920, p. 458); ICuckuck
(1904) observed that, a t Helgoland, Nemoderma developed its gonads
during each set of spring tides, and liberated these during the following neap
tides; Kuckuck (1907) states that Halicystis produces its fruits in rhythmic
succession but a t irregular intervals, the fruiting periods being separated by
sterile periods of several days duration; Tahara (1913) observed that, in
Japan, four species of Sargassum and Cystophyllum sisynzbrioides liberate
the oogonia from all plants of a single species a t about the same time, the
crops being produced in a rhythmic manner but a t irregular intervals on
different days for different species. Keefe has found the same manner
of fruiting in Sargassum Filipendula a t LTToods Hole, Mass. Among twentyone liberations recorded during six summers, discharge of oogonia occurred
a t intervals of two to twelve days, but most frequently a t intervals of three
t o five days. The records obtained are shown in table 4.
TABLE4
I
Xurnber of Days in Periods Between Liberation;
2
3
4
5
6
--
I
3
3
1
2
----.
Number of Times When Liberation Was Observed a t Indicated Intervals.. . . . . . . . . . . . . .
5
.-
8 9 1 0 1 1 1 2
--
M
-
---
I
1
I
I
These facts suggest the overlapping of separate crops with a tendency
toward regularity in their production.
From the cases cited it appears that the tendency to produce sexual
fruits in periodic crops is fairly wide-spread. Possibly Sargassum and
Cystophyllum have not yet acquired the habit of correlating their periods
with the regular tidal changes, or they may be less susceptible than the others
to these influences. The irregularity of Halicystis may be due to the fact,
noted by Kuckuck (1907), that this alga grows ten meters below the surface
and so beyond the potent effect of tidal changes, but Dictyopteris also
grows a t considerable depths, being obtained a t Plymouth only by dredging,
and yet seems to have regularity in its fruiting. Evidently further studies
are needed to show the relation between external conditions and the inherent
capacity of the plants in the development of the habit of periodic fruiting.
The advantage of the periodic production of sexual cells and their simultaneous discharge is evident, since the sperms are much more likely to reach
7 The author is indebted to Rev. Anselm M. Keefe for permission to refer t o his unpublished results.
Dec., 19271
HOYT
- PERIODIC
FRUITING O F DICTYOTA
61I
the eggs and accomplish fertilization if both eggs and sperms are matured
and liberated in large numbers within a single hour than if a few eggs and a
few sperms are discharged a t intervals throughout the month. Oltmanns
(1923) lists several genera of green and brown algae which discharge their
sexual cells almost simultaneously a t a definite hour, usually near daybreak,
at times varying, in different genera, from 12-2 A.M. t o 5-8 A.M. In some
cases the discharge occurs punctually within a period of twenty minutes.
Evidently many algae have acquired the advantage of simultaneous liberation of their sexual cells.
While this phenomenon of periodic fruiting seems to have been developed
by the inherent capacities of the plant, it seems that it must have been developed also in response to the factors of the environment. When we consider the close correlation between the fruiting periods and the external
conditions, we are compelled to believe that these periods have been timed
in response to the external conditions. I t seems, then, that we have here a
phenomenon produced in response to rhythmic external factors and yet
maintaining itself for month5 when removed from these rhythmic factors;
and, moreover, occurring in parts which have never been exposed to the
rhythmic external conditions. I t is greatly to be desired that culture
methods may be devised in order that we may learn whether this fruiting
habit is inherited by successive generations grown without the influence of
rhythmic external conditions.
The second problem-that of the relation to the full moon in the fruiting
habit of Dictyota a t Beaufort and nearby places-is still more difficult.
This would be easier if we found that the plants fruited a t the first spring
tide after their development in May or June and then continued their fruiting a t each alternate set of springs, but this is not the case. In 1909 a search
for Dictyota was made on May 14 by an experienced collector a t the Beaufort laboratory without finding a trace of a single plant. The next search
made on June 9 resulted in the finding of numerous plants 20-29 cm. long,
mostly tetrasporic but including two males which had just discharged their
sperms. I t thus seems that, a t this place, Dictyota begins its growth after
the middle of May and is ready to fruit by the end of May or early in June.
The dates of the spring tides of this part of the year are shown as follows:
1906: May 23, new moon, lesser tides
June 7, full moon, greater tides
1907: May 27, full moon, greater tides
June g, new moon, lesser tides
1908: May 29, new moon, lesser tides
June 15, full moon, greater tides
1909: May 19, new moon, greater tides
June 5, full moon, lesser tides
1910: May 23, full moon, lesser tides
June 7, new moon, greater tides
1912: May 29, full moon, lesser tides
June 15, new moon, greater tides
AMERICAN JOURNAL OF BOTANY
1917: May 19, new moon, lesser tides
June 6, full moon, greater tides
1921: May 20, full moon, lesser tides
June 7, new moon, greater tides
I t will be seen that, in some years, the full moon occurs a t a season when
the plants have reached maturity, while in other years the new moon occurs
a t that time. Thus in 1908 the spring tide of the new moon occurred on
May 29, while in 1912 the full moon spring tide occurred on the same date;
in 1906 the full moon spring tide occurred on June 7, while in 1910 and 192I ,
that of the new moon occurred on the same date. Yet in each of these, as
well as in all other years, Dictyota fruited only a t the periods of the full moon.
I t will be noted, also, that sometimes this fruiting coincided with the greater,
and sometimes with the lesser, set of spring tides. I t seems evident, then,
that Dictyota, a t Beaufort and the nearby places, fruits not solely according
to when it reaches maturity or according to the occurrence of greater or lesser
tides, but that, having attained a state of sufficient maturity, it fruits only
a t the time of the next full moon, waiting as long as may be necessary for
this to occur. This necessitates that it shall fruit in some years as early as
June 9, as in 1909, and in other years as late as June 20, as in 1908, which is
what we have found to be the case.
Several animals are known to mature and liberate their sexual cells a t
more or less definite periods corresponding to the phases of the moon, usually
near the time of full moon and often near the time of new moon. A number
of writers have described the behavior of the palolo worm, the best of these
accounts being that of Mayer (1908). This author studied the Atlantic
palolo (Eunice fucata) for nine years a t Tortugas and observed that swarming
regularly occurred within three days of the last quarter of the moon between
June 29 and July 28, but that when this phase of the moon occurred late in
July there was a response to the first quarter as well as the last quarter.
The worms, although inhabiting their burrows in the rocks to a depth of 6
fathoms (about 11 m.), break off their sexual segments a t the appointed
time, and these, swimming to the surface, discharge their sexual cells upon
the appearance of the first faint rays of light. They may, however, discharge before daylight or in darkness, as is done by the palolo worms of
Samoa (Friedlaender, 1898). Some worms swarmed a t the regular time
when the rocks containing them were placed in a floating car (and so removed from the influence of the tides) screened from the sun but open to the
moon, but none ever swarmed when moonlight was prevented from falling
on the rocks in which they lived. The Pa~ificpalolo (Eunice viridis)
similarly swarms on or near the day of the last quarter of the moon in October and November, while the Japanese palolo (Ceratocefihale osawai)
swarms a t the times of the new and full moons. Similarly the "Wawo"
(Lysidice oele) in the Malay Archipelago swarms on the second and third
nights after the full moon of March and April. Other worms show a more
Dec., 19271
HOYT
- PERIODIC
FRUITIKG O F DICTYOTA
613
or less similar behavior. Thus Lillie and Just (1913) found that, a t Woods
Hole, Nereis limbata swarms in four periods corresponding to the lunar
cycles from June to September. These swarms occur from shortly before
full moon to shortly after new moon, having maxima near the times of the
full and new moon, while Hempelmann (1911) states that, a t Naples, the
swarms of Nereis Dumerilii tend to center around the times of the first and
last quarters of the moon. Similarly Just (1914) observed that Platynereis
megalops, a t Woods Hole, swarms from about the time of full moon to new
moon, usually being most abundant about the time of the new moon.
Scott (1909) records that the times of discharging the eggs of Amphitrite
ornata are closely associated with the spring tides, the maxima always occurring within two days of the new or full moon. He suggested that this is to
be related to the higher temperature of the sand flats and the more abundant
food available to the worms a t the low water of spring tides, but this suggestion does not hold for other animals with similar periodic habits.
Among echinoderms Tennent (1910) found that, both a t Beaufort and a t
Tortugas, most of the individuals of Toxopneustes variegatus gathered during
the time of the full moon had discharged their sexual cells. Fox (1923)
observed that Centrechinus setosus a t Suez ripened and shed its germ cells
a t regular periods, reaching their maximum between the first quarter and
the full moon, and falling to zero between the last quarter and the new
moon, those not ripening their cells a t one period waiting to mature and
discharge them a t the next lunar period. In this case there is greater difference in the range of migration of the animals than in range of the tides a t
new and full moon. Strongylocentrotus lividus a t Alexandria, Naples,
Marseilles, and Roscoff, France, on the other hand, showed simultaneous
discharge from the individuals living in the same locality, but no regular
rhythm.
Among molluscs, Grave (1922) records that the chiton Chaetopleura
apiculata discharges its sexual cells a t lunar periods, heavy spawning beginning within a few days of full moon and continuing to about the third
quarter. Mytilus variabilis a t Suez and another species of the same genus
a t Alexandria, however, as observed by Fox (1923), while showing simultaneous discharge, have no regular rhythm, and M. edulis a t Southampton
shows no lunar periodicity.
A fish, Leuresthes tenuis, according to LV. F. and J. B. Thompson (1919),
comes inshore in great swarms on approximately the second, third, and
fourth nights after full moon from March to June. The sexes then pair and
burrow in the sand, where the eggs are laid a t the uppermost level reached
by the waves. This swarming is timed so as nicely to adapt the laying of
the eggs to external conditions. Thus it occurs a t the lower set of spring
tides (those of the full moon), so that the eggs are freed from the sand by
the higher spring tides of the new moon, two weeks later, a t which time they
are ready to hatch; it occurs just about as the highest tides of these springs
6I4
AMERICAN JOURNAL OF BOTANY
[Vol. 14,
are reached so that the following tides do not wash away the eggs; and it
occurs a t about the highest point of the tide, so that the eggs are deposited
in the sand a t the highest level reached by the waves. Evidently the reproductive habits of this fish are timed in relation to external conditions so
that they obtain for the species the greatest possible advantage in the safeguarding of its eggs. This swarming occurred a t the regular time when the
moon was hidden by clouds as well as when it was shining brightly.
From the previous summary of observations five conclusions seem warranted. ( I ) The tendency to produce sexual cells a t periodic intervals is
inherent in many kinds of both plants and animals. (2) When such a
tendency is present there is, a t least in many cases, a further tendency to
correlate the time of reproduction with regularly recurring periodic changes
in the external conditions. (3) The similarity in the behavior of different
plants and animals indicates that these have correlated their periods of
reproduction with similar external factors. (4) The changing external conditions with which the correlation of reproduction is most marked are the
changing phases of the moon, or the changes in the tides effected by the
moon. (5) In many cases the regular periodicity of reproduction has become fixed so that the periods are continued after the external conditions
with which they are correlated are altered.
Fox (1924) shows that, in an echinoid (Strongylocentrotus lividus), the
spawning of one individual stimulates other ripe individuals in the neighborhood to spawn. He states (p. 74): "VIJhatever then may be the cause of
the simultaneous spawning of echinoids in the sea, whether lunar or nonperiodic, it is necessary for the cause to act only on a few individuals, which,
by spawning, will excite their ripe neighbors." This suggestion, however,
fails to account for the fact that these neighbors are ripe a t the same time,
and does not seem to touch the problem of the periodic development of the
sexual cells. This problem seems more deep-seated than would be indicated
by this suggestion or by that of Scott (1909) noted above. The periodicity
does not seem to be due to immediate direct stimulation by external conditions, but does seem to have been developed in relation to such conditions.
We cannot conceive of such regular, rhythmic periodicity in such close
correlation with rhythmic external conditions as having been produced
independently of the conditions. \Ve must, rather, believe that the plants
and animals, having been exposed to regularly recurring changes throughout
numberless generations, have acquired the correlation of their activities to
these changes; and that, in some cases, this periodicity has become deeply
impressed on their protoplasm.
The similarity in the reproductive behavior of some of the animals and
plants is remarkable. In both groups we have some forms reproducing
simultaneously a t irregular periods, some forms reproducing a t regular
periods related to the full moon, and some forms a t regular periods a t other
phases of the moon. In some cases the accounts of reproduction in animals
Dec., 19271
HOYT
- PERlODIC
FRUITING O F DICTYOTA
615
could be used, with only slight changes of wording, to describe the facts as
observed in Dictyota. Such striking similarity inevitably suggests a similar
fundamental cause, but this suggestion can be established only after a more
thorough study of all known cases of periodicity in reproduction and, perhaps, in other activities also.
Whether, in cases of lunar periodicity, we are concerned with correlation with the moon or with tidal changes effected by the moon, we cannot,
a t present, decide with complete assurance. I t is, however, noteworthy
that the periodicity in reproduction may continue irrespective of the tide,
and that, in some cases, this occurs only a t the times of the full moon.
What, if any, may be the nature of the moon's stimulus is not clearly evident.
The statements in the literature regarding the nature of moonlight are
contradictary, some ctating that it is largely polarized, others that it is
polarized no more than sunlight. Acting on this suggestion, several workers
have tested various effects of polarized light. Bryant (1923) split fish and
exposed one half of each to the direct light of a 1000 c.p. electric light about
one foot distant, placing the other half farther off where it received only the
light reflected from a pile of glass plates. In every case the half receiving
reflected light spoiled more quickly than the other. Miss Semmens (1923),
testing the effect of light on the hydrolysis of starch by diastase, found the
action most rapid in polarized light, slower in ordinary light, and practically
absent in the dark; concluding, after varied sets of experiments, that the
evidence was decidedly in favor of the acceleration of the hydrolysis of
starch by polarized light as compared with ordinary light of the same
intensity. She states that "plane-polarized light was found to cause a
definite acceleration of germination and of flower production, but apparently
not to influence the vegetative growth of the stem and leaves." Morrison
(1925) found luminescent bacteria to grow more rapidly in polarized light
than in non-palarized light of equal intensity, or in darkness. Bhatnagar
and La1 (1926) obtained, in all cases tried, increased growth of V i b ~ i o
cholerae and Bacillus typhosus in polarized as compared with that in nonpolarized light. Bhatnagar, Lal, and Mathur (1926) observed increased
elimination of carbon dioxid in rabbits and guinea pigs exposed to polarized
light compared with the amount given off under exposure to non-polarized
light of equal intensity, or in darkness. Macht (1926)' in numerous careful
experiments, found seedlings of lupine and other plants to grow more
rapidly in polarized than in non-polarized light of the same intensity and
observed, moreover, that this increased growth occurred when the stems and
roots were shaded, but not when the seeds were shaded, thus indicating an
effect of the polarized light on the hydrolysis of starch or on other reactions
within the seeds.
Whether these results have any bearing on the problem of reproduction
a t regular phases of the moon can be determined only by further experiment,
but we should recall the statement of Mayer (1908) that the Atlantic palolo
616
AMERICAN JOURNAL OF BOTAST
[Vol. 1 4 ~
worms never swarmed when moonlight was prevented from falling on the
rocks in which they lived. This question is complicated by the fact that
sunlight a t different times of the day and light both of the sun and moon from
different parts of the sky are polarized to different degrees. Observations of
the author on the time of discharge of the eggs of Dictyota suggest that this
occurrence may be related to the action of factors other than visible rays.
This will be discussed in a later paper.
The difference in the fruiting behavior of Dictyota on the shores of
North Carolina from that shown by D. dichotoma on the coasts of Europe
raises the question as to the classification and relationship of the North
Carolina plants. While resembling the species in form and structure,
these differ so markedly and so constantly in their manner of producing their
sexual fruits that they should, it seems, be recognized as a distinct variety.
Neither the form nor the structure nor the fruiting is independent of external
conditions, but of these three the fruiting habit seems most firmly fixed.
M-hereas, under changed conditions, the form is often altered and cell masses
are frequently produced bearing little resemblance to Dictyota, the fruiting,
if occurring a t all, is only slightly delayed, and the regular periods are still
maintained. The fruiting habit thus seems a more constant character of the
plant than are the form and structure and should, therefore, be equally
considered in our classification. An adequate description of a group should
include all characters of every kind which are sufficiently constant to enable
us to distinguish i t from other groups. Only by including all such characters
can we obtain a description which corresponds to the group as it occurs in
nature. We may, then, recognize the plants of North Carolina, and others
with similar features, as forming a distinct variety characterized as follows:
Var. menstrualis var. nov. Like the species in form and structure, but
different from this in producing its sexual fruits in monthly periods.
Plantis forma et structura speciei similibus, sed fructus sexuales menstrualiter producentibus.
SUMMARY
I . All observed species of Dictyota, wherever studied, have been found
t o produce their sexual fruits a t more or less regular periods.
2 . Three different types of periodicity have been observed. On the
coasts of Europe D. dichotoma fruits a t fortnightly intervals a t each set of
spring tides, on the coast of North Carolina a morphologically similar species
fruits only a t the spring tides of the full moon, while in Jamaica all observed
species so prolong the development of their fruits that no change is evident
during a period of three weeks.
3. The fruiting periods seem to be related to the tides, but the relation of
fruiting period to tide is different for each region studied.
4. Wherever the tides are regular, as in England, Wales, Italy, and North
Carolina, whether their range is great or small, the periods are regular and
constant unless retarded by unfavorable conditions; but where the tides are
irregular, as in Jamaica, the periods are scarcely evident.
Dec., 19271
HOYT - PERIODIC FRUITING O F DICTYOTA
617
5. Where the range of tide is very slight, as a t Naples, the development
of the fruiting crops is less uniform than where the range is greater, as in
Wales, England, and North Carolina.
6. A single species shows the three types of periodicity observed, respectively, in Europe, North Carolina, and Jamaica, with a different fruiting
schedule a t each of the five regions where it has been studied, while three
different species show the same fruiting behavior a t all the localities in
Jamaica from which they have been studied.
7. When the tides are altered by the wind, the plants fruit according to
their schedule and not according to the tides to which they are actually
exposed. Similarly when the usual light conditions of the tides are experimentally reversed the plants continue to fruit a t their regular periods.
8. Plants kept in the laboratory removed from tidal influences for several
weeks or months maintain the fruiting periods of their particular locality,
even on new branches produced in the laboratory and therefore never exposed to the influence of the tides.
9. At North Carolina the plants do not fruit a t the first set of spring
tides but, having reached maturity, wait as long a.s may be necessary until
the time of the full moon arrives. The period of fruiting being reached,
the development is more rapid here than in England, Wales, Italy, or
Jamaica, where the fruiting habits are different. The production of the
fruits exhausts the plants here, especially the females, to an extent not
observed elsewhere.
10. At Beaufort and a t Naples the eggs, and apparently the sperms also,
are discharged practically within a single hour, beginning before or about
the time of daybreak.
1 1 . At North Carolina the development is more uniform than observed
elsewhere, an average of about 80 percent of the eggs of each crop being
discharged in a single day, and about 60 percent to 70 percent in a single
half-hour, this usually occurring on the sixth day after the full moon.
12. This periodic simultaneous discharge of the sexual cells is an advantage to the plant, since fertilization will be accomplished more surely
if large numbers of eggs and sperms are liberated in a single hour than if a
few of each are discharged a t intervals throughout the month.
13. The non-sexual plants, which live under the same conditions as the
sexual ones, show no periodicity, but produce their spores throughout the
entire month and discharge them throughout the day and night. There is
thus a striking comparison between the advantage or non-advantage of a
habit to the plant and the formation or non-formation of that habit by the
plant.
14. No single factor or group of factors will account for the fruiting
behavior of Dictyota. As the form and structure have been developed by
the reaction of the inherent capacity of the plant to the sum of all the
factors of the environment, so with the fruiting habit. Neither the form
618 AMERICAN JOURNAL OF BOTANY
[vol. 14.
and structure nor the fruiting habit is caused by external conditions alone,
but both have been developed by the reaction of the plant in relation to the
external conditions.
15. In the case of the fruiting habit, this has been developed so that the
rhythmic fruiting periods are synchronized with rhythmic changes in the
external conditions. The habit has, however, become so impressed on the
plant that the regular periods are maintained for weeks or months after
the plants are removed from the rhythmic external conditions.
16. Several other algae have been found to produce their sexual cells a t
regular intervals related to the tides, while others bear their fruits simultaneously but a t irregular intervals. A number of animals in different groups
are known to reproduce at more or less definite periods related to the phases
of the moon, most often near the full moon. The nature of the moon's
influence, if any, in such cases is not yet evident.
17. The monthly habit of fruiting shown by the plants of Dictyota in
North Carolina, being a more fixed character of the plants than are the form
and the structure, seems to justify the recognition of these as a distinct
variety, in spite of the fact that morphologically they resemble the species
as found in Europe.
18. The known facts suggest that the periodic production of sexual cells
may be much more common than is realized and that further study may
show us factors which are now scarcely suspected. Much more study is
needed before we can understand the observed phenomena.
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The Periodic Fruiting of Dictyota and Its Relation to the Environment
W. D. Hoyt
American Journal of Botany, Vol. 14, No. 10. (Dec., 1927), pp. 592-619.
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Literature Cited
An Analysis of the Spawning Habits and Spawning Stimuli of Chætopleura apiculata (Say)
B. H. Grave
Biological Bulletin, Vol. 42, No. 5. (May, 1922), pp. 234-256.
Stable URL:
http://links.jstor.org/sici?sici=0006-3185%28192205%2942%3A5%3C234%3AAAOTSH%3E2.0.CO%3B2-R
Periodicity in the Production of the Sexual Cells of Dictyota dichotoma
W. D. Hoyt
Botanical Gazette, Vol. 43, No. 6. (Jun., 1907), pp. 383-392.
Stable URL:
http://links.jstor.org/sici?sici=0006-8071%28190706%2943%3A6%3C383%3APITPOT%3E2.0.CO%3B2-Y
Breeding Habits of the Heteronereis Form of Platynereis megalops at Woods Hole, Mass.
E. E. Just
Biological Bulletin, Vol. 27, No. 4. (Oct., 1914), pp. 201-212.
Stable URL:
http://links.jstor.org/sici?sici=0006-3185%28191410%2927%3A4%3C201%3ABHOTHF%3E2.0.CO%3B2-8
Periodicity in Dictyota at Naples
I. F. Lewis
Botanical Gazette, Vol. 50, No. 1. (Jul., 1910), pp. 59-64.
Stable URL:
http://links.jstor.org/sici?sici=0006-8071%28191007%2950%3A1%3C59%3APIDAN%3E2.0.CO%3B2-O
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LINKED CITATIONS
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Breeding Habits of the Heteronereis Form of Nereis Limbata at Woods Hole, Mass
Frank R. Lillie; E. E. Just
Biological Bulletin, Vol. 24, No. 3. (Feb., 1913), pp. 147-160+162-168.
Stable URL:
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The Effect of Polarized Light on the Growth of Luminous Bacteria
T. F. Morrison
Science, New Series, Vol. 61, No. 1580. (Apr. 10, 1925), pp. 392-393.
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Some Egg-Laying Habits of Amphitrite Ornata Verrill
John W. Scott
Biological Bulletin, Vol. 17, No. 5. (Oct., 1909), pp. 327-340.
Stable URL:
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