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Annual Periodicity in the Migration and
Reproduction of Birds
A. J. MARSHALL
Monash University, Clayton, Victoria, Australia
I will now argue that the length of this post-nuptial
regeneration period is adaptive.
Certainly it varies in its duration from species to
species. Numerous lists have been tabulated that show
that the period of post-nuptial regeneration in various
species of North American passerines ends between
October and December. Not until then can they be
photostimulated into sexual activity. Various workers
have Mtered the length of the regeneration period by
means of photoperiodie manipulations [3, 4]. It has
been claimed that birds require a period of short days
and long nights before they can regenerate their sexual
processes. I am not convinced that this evidence has
any wide relevance under natural conditions. Great
numbers of species in the tropics and elsewhere regenerate without the benefit of reduced daylength or
increased nightlength (see below).
However, whether these species do, or do not, actually require short days and long nights to regenerate
their internal apparatus, it is unequivocal that they
come into potential breeding condition during the autumn at a time when there is lacking the full spring
combination of factors appropriate to reproduction.
Nevertheless, a so-called "Indian summer" will very
often allow reproduction even though the young are
usuMly eliminated during the subsequent winter. This
phenomenon may be less prevalent on the North American continent than in the warmer British Isles and
southern Australia, but it sometimes occurs in California and no doubt elsewhere in the United States. Orians
[5], for example, has evidence that in 1959 the sexual
cycle of thousands of Californian tricolored blackbirds
(Agolaius tricolour) had, without the benefit of short
days, become sufficiently regenerated ("prepared")
as early as September. Reproduction occurred. Orians
also collected local records of spasmodic autumn breeding of a wide variety, of other species apparently behaving in much the same manner as has been recorded
from other countries [6].
Generally, however, reproduction in temperate zones
is delayed until the following spring. It is interesting to
reflect that in many species the principal and productive breeding season is the result of a secondary (continuation) rhythm. The primary one is that which in
autumn (in many, but not all, species) follows the postnuptial regeneration period [7].
]n some species the environment allows the primary
The term "annual periodicity" is of course a misnomer. No animal periodicity could be precisely annual. Nevertheless, the kind of periodicity that I want
to discuss is a relatively lengthy one, and in some cases
it may be sufficiently precise to govern the time of
movement to the breeding grounds and thus indirectly
influence the time of reproduction.
At the outset it is essential to separate the factors
that initiate the pre-nuptial movement from those
that culminate reproduction. The former factors merely
ensure that migrants or nomads will start back toward
their traditional breeding grounds in time to come
under the control of the latter factors, i.e., the external
stimuli that operate there and bring the sexual cycle
to culmination. For example, daylength initiates the
seasonal sexual cycle of many Northern Hemisphere
birds in late winter (generally February and perhaps
even as close to the winter solstice as early in January),
but there is no evidence that it governs the actual time
of reproduction. Factors on the breeding site do this.
Thus, after a severe winter, reproduction is usually
delayed. A mild winter and an "early spring" will
ensure an early breeding season [1]. The reproduction
times, then, can differ widely from year to year in the
same locality even though the daylength is constant.
For this reason it is better to speak of stimuli and synchronizers than time-givers. The actual time of reproduction is of no importance in great numbers of
birds and other vertebrates. The essence of their breeding success is efficient synchronization of their internal
processes and specific reproductive behavior forms with
the environment at the period(s) when it becomes most
suitable for the production and survival of young.
The factors that initiate movement to the breeding
ground are both internal and external. The initial critical internal component is length of the post-nuptial
regeneration ("refractory," "preparatory") period because until this ends the reproductive apparatus of the
species remains in negative phase. When individuals
spontaneously emerge from this period they are in a
hormonal condition whereby they can sing, display,
and pair. These activities provide further external
stimuli which help synchronize the sexual processes
of the pair [2]. If the external conditions are appropriate,
the pair or the flock now come under the influence of
external stimuli traditionally significant to reproduction; and this occurs.
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MARSHALL
post-regeneration rhythm to come to fruition. In such
cases the cycle seems to become more or less mechanically cyclical in its operation. Thus, the famous Sooty
Island Tern (Sterna fuscata) of tropical Ascension
Island, which breeds about four times every three
years [8], has no winter to contend with and is apparently assured perennially of an adequate food supply
for its young. These factors allow it to breed irrespective of the cycle of the sun. Broadly, the same may be
true of the Colombian passerine Zonotrichia capensis,
individuals of which Miller [91 has shown to reproduce
twice a year. The same may be the case with the comorants studied on the Victoria Nyanza by Marshall and
Roberts [10] and, likewise, with the passerine Munia
on the equator in Borneo Ill]. It is interesting to reflect
on the probability that special environments, strikingly
different in themselves, but capable of supporting
breeding species throughout the year, have seemingly
moulded the internal machinery of such diverse animals as tern, comorant, and passerine into a common
pattern. Conversely, the congeneric Zonotrichia leucophrys and Z. capensis have developed different cycles
in different environments [4, 9].
I do not believe that the tropical species cited above
are in any way influenced by photoperiodicity. Their
breeding follows the typical regeneration period. When
this ends there is a period of sexual display, acceleration, and finally the culmination of yet another cycle
[12]. On the other hand, my friend Dr. Wolfson insists
that photoperiodic fluctuations are important in the
regulation of the sexual cycles of all birds, tropical
(even equatorial) or otherwise. For a number of reasons
I have never been able to accept this, but Dr. Wolfson
is in the audience and no doubt at the end of the meeting he will tell us why I am wrong.
I believe that daylength is important only to species
for which it is important that it should be important,.
and I now come to some more examples of cycles that
I believe in nature to be uninfluenced by photoperiodic
fluctuations. The first I will choose will be that of the
red-billed dioeh (Quelea quelea) with which Disney,
Lofts, and I [13] are working. This small weaverfinch
occurs in plague proportions in certain of the dryer
parts of Africa.
Although cage experiments show that the sexual
cycle of Quelea quelea [14] retains an innate susceptibility to photostimulation, it is other and various environmental effects (often those arising after rainfall)
that operate in conjunction with the internal rhythm
and so stimulate breeding irrespective of the cycle
of the sun [15].
It was considered of interest to determine whether
the regeneration phase--a temporary period of enforced sterility--intervenes in the reproductive rhythm
of a xerophilous equatorial species for which it is beneficial that reproduction should occur at any time of the
year when rain falls and produces conditions propitious
for breeding and the survival of young.
In parts of East Africa Q. quelea oscillates back and
forth across the equator according to the available food
supply. Thirteen Tanganyika males in full nuptial
plumage were taken from our London colony which
is kept under the equatorial daylength of 12 hours.
These were laparotomized on February 12. The gonads
measured 10 x 5 ram. and were approximately at the
peak of breeding condition. One bird was killed and
found to be in full spermatogenesis.
The 12 survivors were then subjected to a daily
photoperiod of 17 hours. On March 15 they were still
in full nuptial plumage and were again laparotomized.
The testes, however, now measured a mere 1.5 x 1 ram.
Two birds were killed, and their seminiferous tubules
were in the fully metamorphosed condition that indicates the onset of "refractoriness." Of the ten surviving birds, half were then transferred to an equatorial
daylength of 12 hours, and half were retained under
the existing regime.
On March 20 unilateral castrations revealed that
in both groups the gonads of a minority were beginning
to develop. The experiment was terminated on April
6 when the survivors were killed for examination. In
all but two birds primary or secondary spermatocytes
had arisen.
The results indicate that in this xerophilous equatorial species a post-nuptial period of sexual regeneration
exists, but that it is relatively brief. Thus, after each
breeding season the males, at least, progress with little
delay into a condition whereby they can take advantage of propitious breeding conditions whenever these
arise in the arid environment to which they, and
especially their reproductive processes, are adapted.
A remarkable aspect of the reproduction of Q quelea
is the speed with which nest-building and egg-laying
occurs. Within a few days of the arrival of the horde
on a suitable nest site, each male starts to build and
to display vigorously in the incomplete structure. This
attracts a female and copulation has been observed
in and alongside the partly built nest.
Next, I will choose some non-passerines in the form
of two very different Australian ducks that will reproduce, as Frith [16] has shown, at various times of
the year irrespective of the cycle of the sun. Now these
are not tropical birds--they are common at latitude
36~ at which the annual fluctuation in daylength
is greater than that in Tennessee or Turkey. I emphasize
this point to show that there is plenty of photoperiodieity, so to speak, for them to use if it were beneficial for
them to do so. The truth is, of course, that if these
ducks did, in fact, regularly reproduce at any particular phase of the cycle of the sun, they would soon be
naturally eliminated. In their austere, but not desert,
environment they breed in response to chance rainfall
or its effects.
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PERIODICITY IN AVIAN REPRODUCTION
Sexual activity in both grey teal (Anas gibberifrons)
and the pink-eared duck (Malacorhynchus menbranaceus), which exploit temporary floodwaters, is stimulated by increasing water level. In the former species,
actual reproduction occurs quickly and coincides with
the rising of water. In M. membranaceus breeding is
delayed until its decline. As a result, both species will
breed at any time of the year, yet the emergence of
the ducklings of each coincides with an increase of
animal food appropriate to the species (e.g., plankton
in the case of the later-breeding pink-eared duck).
For those familiar with the prolonged social and
sexual display of the Nearctic and Palaeartic mallard
(Anas platyrhynchos) Frith's data on the Australian
A. gibberifrons must be of exceptional interest. In this
opportunist breeder the whole process of display, and
the prospecting of a nest site (in a hollow tree), may
take a mere 10-17 days. The Australian A. superciliosus,
on the other hand, has prolonged autumn and spring
social and pairing displays comparable with those of
the mallard. Despite its unpromising environment,
A. gibberifrons has become, probably, the most successful duck in Australia. We have in this surprising success
a distinct parallel with that of Quelea.
I have never been able fully to convince Dr. Wolfson
of the fact of rainfall-induced reproduction, nor has he
been able to convince me that the cycles of such birds
as the Quelea quelea, grey teal, pink-eared duck, budgerygah (Melopsittacus undulatus) or zebra finch (Poephila castenotis), and many others are photoperiodically
controlled.
We have seen above how the regeneration period of
Quelea quelea (and probably that of the zebra finch
and budgerygah) has been abbreviated and that this
allows the animals again to breed quickly if another
chance rainfall saturates their arid environment and
induces a sufficiently prolific growth of vegetation and
insects for the support of another host of young.
Now I come to one of the most remarkable cycles
of all--that of the short-tailed shearwater (Pu~nus
tenuirostris). Serventy and I [17] have proposed that
in this transequatorial migrant the regeneration period
is adaptive in the opposite direction--that it has been
lengthened, and that this lengthening is a primary
factor in ensuring its astonishingly regular return each
year from the South Arctic and Aleutians to its southern
Australian breeding grounds. First, however, the contra-nuptial journey. The migratory flocks of P. tenuirostris regularly leave these southern Australian breeding
islands in April (autumn) at a time when their principal
food--euphausian plankton--remains abundant, and
when sea temperatures are still higher than at the
November period of ovulation. It was concluded [18]
that the northern journey via Japan to the Aleutian
contra-nuptial ("wintering") areas is probably in obedience to an inherent internal rhythm.
Later in the year, when the millions of southbound
501
birds first make their landfall at the breeding islands
(in the last week in September), gametogenesis is already well advanced. The testes contain bunched
spermatozoa. There is no doubt that both the spring
sexual cycle and this nuptial journey are initiated under
conditions of decreasing daylength while the birds are
still north of the equator. However, the regularity of
their Australian landfall and subsequent egg-laying
(November 19-21 and the following 12 days) seemed
to suggest that the nuptial journey must be "timed"
by some astronomical constant, possibly decreasing
daylengths. No obvious periodic changes that might
operate as precise "timing" factors were observed in
the breeding area.
P. tenuirostris, in common with certain other longdistance migratory shearwaters, molts on the head
and body shortly after egg-laying, but delays the replacement of its wing and tail quills until the completion of the exacting journey across the equator. Like
most other migrants, the species lays down massive
deposits of subcutaneous and peritoneal fat before
migration.
The primary purpose of our preliminary investigations was to try to determine whether decreasing daylength, or internal rhythm, controls the sexual cycle
(and possibly, therefore, the migration). Secondly, it
was desired to discover whether the peculiar molt
rhythm would persist under varying stimuli. Thirdly,
it was considered valuable to record the degree of fat
deposition under such varying conditions in captivity.
A group of breeding adults was caught in the Furneaux group of islands in north-east Tasmania (latitude
40~ 12p S) just before the beginning of the northward
migration of 1957. They were sent by air to the Commonwealth Scientific and Industrial Research Organization Regional Laboratory at Perth, Western Australia
(latittide 32~ and held in captivity for several months
during the period they would normally spend in the
North Pacific. It was found that after some initial
losses those essentially plankton feeders could be maintained on a diet of sliced fish. Experiments were conducted during two successive years.
In 1957 the birds were divided into two groups of 15
individuals each. The first lot was placed under a changing light regime approximating the daylengths to which
traveling wild migrants should be exposed, except that
the total period was telescoped by half. Thus, whereas
the migrating flocks leave the breeding islands about
mid-April and arrive back late in September, the artificial photoperiods in this experiment (successively
equaling those of the equator, Japan, the Aleutians,
the equator, and finally the breeding localities) were
so adjusted that the normal daylength of September
27 was reached on June 27.
The second group of birds was held under natural
Perth daylight (which is longer at the June solstice by
about an hour than at the breeding islands used by the
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MARSHALL
species, but almost 10 hours shorter than at the Aleutians). Some of the birds from both cages were killed
on June 27. The photostimulation experiment was then
terminated, and the survivors of both groups held in
company, under ordinary Perth daylight, until September 29.
(a) Gonad condition on June 27: Despite the striking differences in the light regimes of the two groups of
birds, there was no detectable difference in their gonads.
Males of both groups showed some very slight advancement from the April condition and those that died
during the first fortnight of the experiment. Thus, the
seminiferous tubules of some birds contained up to
three rows of spermatogonia. The diameter of ovarian
oocytes in the single female killed was slightly greater
than the April condition.
(b) Gonad condition on September 29: Four birds
survived to this date. Of three males, one (originally
from the photostimulated group) contained spermatozoa in some seminiferous tubules. Of the other two
males (originally from the natural daylength cage)
one was even more advanced, having bunched spermatozoa. The third male contained numerous primary
spermatocytes in mitosis and a few secondary spermatocytes. The overall size of gonad was slightly, but
definitely, smaller than normal wild birds at the corresponding time. A surviving female (originally from
the photo-stimulated group) had the diameter of the
largest ooeyte measuring 3.1 ram.; that is, within the
range of normal wild birds at the time of landfall.
It was clear, then, that alteration of photoperiodicity,
in the manner conducted in the experiment, had no
great effect on the captive shearwaters. The birds-both experimental and control---that were allowed to
survive came rhythmically into a sexual condition
only a little less advanced than that of the wild population by the date that the latter completed their transequatorial migration around the Pacific.
In 1958 the experiment was repeated with newly
caught adults from the same breeding stations. Again
they were divided into two groups. Half, as before,
were kept under conditions of natural Perth daylight.
The other half were retained under a constant 12 hour
illumination. This is the daylength at the breeding
islands about the time of the exodus migration. This
year birds were held until the period of normal landfall, when the survivors were killed and dissected on
September 29. Three males and three females survived
in the artificially lighted cage and seven males and two
females in the natural light enclosure.
Again there was no appreciable difference in the
sexual condition between the birds in the two cages.
As before, all birds showed some gonad modification,
and in some individuals testis development had almost,
but not quite, reached the stage attained by normal
wild birds at the corresponding time. Four out of the
ten males had produced spermatozoa, and the remain-
der contained primary and sometimes secondary spermatocytes. The range of overall size reached that of
the wild population, but the mean size was significantly
below it. Ovarian development was also slightly advanced, and the largest diameters of oocytes (mean,
2.1 mm.) were slightly inferior to those in normal birds
at the corresponding stage.
Wing and tail molt began in late June and July, but
the molt was protracted and its completion retarded
by comparison with that of wild birds. Both groups of
captives put on appreciable depot fat (corresponding
to "pre-migratory" fat) from mid-August onwards,
reaching a maximum in early September. The weight
trends were identical in the two groups.
These investigations have shown that in this migratory shearwater the breeding rhythm is persistent at
least for one year after the animal is taken out of its
normal environment and exposed to external influences
(photoperiod, temperature, food, and habitat) exceedingly different from normal.
Although gametogenesis, wing molt, and pre-migratory fat deposition took place under these conditions
at approximately the normal periods, there was nevertheless in some individuals a considerable asymmetry
of the seminiferous tubules and a pronounced retardation of spermatogenesis that is never encountered in
the wild population. This suggests that internal events
were tending to drift out of phase with the external
environment and that essential (as yet undetermined)
external influences, possibly including behavior, were
lacking.
In short, we seem to be dealing with a clock; but one
must liken it to a relatively imprecise chain-store variety. It must be put right by external synchronizers at
least once a year.
DISCUSSION
The data presented above admit of the great importance of photoperiodic fluctuations in the timing of the
pre-nuptial journey and the onset of the "spring"
(often in late winter) sexual rhythm in many temperate
zone birds. They also indicate how the post-nuptial
regeneration period has been adapted by natural selection in relation to the environment of the particular
species. They show, too, how exquisitely the behavior
pattern of species may be adjusted to the modified sexual cycle and how this may help make for a startling
reproductive success in seemingly bleak and inhospitable areas of the earth's surface.
In the past, the principally used indicators of sexual
activity have been the gonads. In the immediate future,
interest in the problem will be focused in the hypothalamic region of the brain. After the demonstration
in other groups of the functional significance of the
hypophysial portal system [19], Wingstrand [20] began
work with birds and produced a notably detailed account of the vascular and neural relationships between
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PERIODICITY IN AVIAN REPRODUCTION
the various elements of the hypothalamus and the
subjacent hypophysis. He reported that no observable
neural connection exists between hypothalamus and
adenohypophysis but demonstrated the accumulation
of what appeared to be neurosecretory material in the
median eminence (of the ventral wall of the infundibulure) and followed previous suggestions that there
occurs a humoral transmission of such material down
the hypophysial portal vessels into the pars distalis
(see also Bargmann [21], and Scharrer and Scharrer
[22]). Benoit and Assenmacher [23] further substantiated
the hypothesis in regard to birds.
Oksche et al. [24] have recently reviewed work which
suggests that there occur neural connections between
the retina with a variety of hypothalamic and infundibular structures. They have, moreover, shown that in
the migratory white-crowned sparrow (Zonotrichia
leucophys gambelii) there accumulates in the median
eminence so much neurosecretory material that this
region may probably be regarded as a depot during
the so-called refractory [25] or, in modern terms [12],
regeneration period of the sexual cycle. This is further
evidence that this period is not one of stasis: it is, as
has been emphasized on many occasions, regeneration
or preparation [4] for the forthcoming sexual season.
Oksche et al., then, have shown that there accumulate
in the "neurosecretory hypothalamic nuclei" and median eminence of intact birds extensive deposits of
neurosecretory material after the completion of seasonal
reproduction and that this is depleted after photostimulation (which also leads to gonad enlargement
and deposition of premigratory body fat). Furthermore, in June (summer) the median eminence of castrates contained "substantially more neurosecretory
material" than that of the control birds. In autumn
there were no apparent differences between castrates
and intact birds because of the increased neurosecretory accumulation in the sexually inactive normal animals.
There is an indication, then, that there occurs a
gradual synthesis, transport, and accumulation in
hypothalamus and median eminence of the products of
neurosecretion and that such material is utilized during
the sexual season. Here we may have a process broadly
comparable with the post-nuptial accumulation of
cholesterol-positive lipid material within the new generation of interstitial Leydig cells in the testis of wild,
seasonally breeding birds. This material, too, will be
utilized during the subsequent breeding season in
direct consequence of the influences, mediated via the
pars distalis of the neural substances described by the
various authors cited above.
It is still unknown (a) whether or not the neurosecretory process is continuous, (b) the cause(s) of its postnuptial retention and (c) the factors that operate suddenly to allow its pre-nuptial release.
503
For many years the phrase "pituitary refractoriness"
has been lightly used, even though no anatomical evidence of any such condition has been adduced. The
evidence customarily used to implicate the anterior
lobe could apply equally well to the hypothalamus or
elsewhere. Although there is no acceptable evidence
that birds of any species migrate in the absence of sex
hormones in their bloodstream, there is available inconclusive information that male castrates of the brambling (Fringilla montefringiUa) can come into Zugunrughe [26]. Furthermore, Lofts, Marshall, and Wolfson
[27] and, I understand, Farner [28] have unpublished
evidence that migratory passerines (Juncos hyemalis
in our case) kept at metabolic levels incompatible with
the accumulation of depot fat will nevertheless come
into Zugunrughe after photostimulation.
More and more, then, there emerges evidence which,
however fragmentary, tends to suggest that the deposition of fat and the onset of Zugunrughe may be under
direct hypophysial or even hypothalmic control. So
far nobody with access to considerable numbers of
proven migrants has yet hypophysectomized such birds
and then photostimulated them with a view to measuring their pre-migratory and pre-nuptial fat deposition
and/or fat deposition. That post-nuptial migrants
deposit fat and travel in the absence of sex hormones
has never been in serious doubt.
Demonstrations that the products of neurosecretion
can be dispersed by photostimulation and accumulated
again during the dark period are of great interest, but
they must not be allowed to divert our attention from
a whole galaxy of species of many different avian orders
for which under natural conditions photoperiodic fluctuations are totally unimportant.
The nervous stimuli resulting from the experience
of external factors such as warmth, water, special
vegetation and foods, the mate and the flock, can be
expected to influence the hypothalamus and its products
of some species just as significantly as the photoperiod
may influence them in others. Each wild individual
must find its own innate "species requirement" in the
landscape around it, and if it does not, neither can it
successfully reproduce. We must not try to tie up the
whole gamut of animal reproduction in one neat little
photoperiodic packet. It won't work!
ACKNOWLEDGEMENT
While working in England Dr. Brian Lofts and I
had the greatest difficulty in obtaining adequate numbers of birds that were indubitably migratory. We
have to thank Dr. A. Wolfson for the collection and
dispatch of the group of juncos with which a small
part of the above data was obtained. These experiments
are being continued and extended and will be published
in collaboration elsewhere.
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MARSHALL
CONCLUSIONS
1. There is evidence that more or less stable sexual
periodicities, under partly exogenous and partly endogenous control, exist in wild birds and in some
species probably constitute an important device in the
regulation of migration and reproduction. In at least
one bird, the sooty tern, this innate periodicity permits reproduction four times every three years in one
part of the tropics.
2. The length of the essentially endogenous comp o n e n t - t h e post-nuptial regeneration period--is adaptive. It is lengthy in some species and has become extremely abbreviated in others. These modifications are
in accordance with reproductive needs of the species in
relation to its particular environment.
3. In at least one species the shortening of the regeneration period has been accompanied by an abbreviation of the subsequent sexual display. In several widely
unrelated species, such display has been greatly shortened along with the development of other means for
speedy reproduction.
4. A near annual periodicity occurs in a transequatorial migrant, the short-tailed shearwater. There
is evidence, however, that exogenous stimuli must
operate at least once during the course of each annual
cycle.
REFERENCES
1. MARSHALL,A. J. 1949. Weather factors and spermatogenesis in birds. Proc. Zool. Soc. Lond., (A) 119:
711-716.
2. MARSHALL,F. H. A. 1936. Sexual periodicity and the
causes which determine it. Phil. Trans. Roy. Soc.
(B), 226: 423-456.
3. BURGER, J. W. 1947. On the relation of day-length
to the phases of testicular involution and inactivity of the spermatogenetic cycle of the Starling.
J. Exp. Zool., 105: 259-267.
4. WOLFSON, A. 1959. The role of light and darkness in
the regulation of spring migration and reproductive cycles in birds. Photoperiodism and Related
Phenomena in Plants and Animals, ed. Withrow.
Washington: A.A.A.S.
5. ORIANS, G. 1960. Autumnal breeding in the tricolored Redwing. Auk, 77: 379-398.
6. MARSHALL, A. J. 1952. The interstitial cycle in
relation to autumn and winter sexual behaviour in
birds. Proc. Zool. Soc. Lond., 121: 727-740.
7. MARSHALL,A. J., and C. J. F. COOMBS. 1957. The
interaction of environmental, internal and behavioural factors in the Rook Corvus frugilegus
Linnaeus. Proc. Zool. Soc. Lond., 128: 545-589.
8. CHAPIN, J. P. 1954. The calendar of Widewake Fair.
Auk, 71: 1-15.
9. MILLER, A. H. 1959. Reproductive cycles in an
equatorial sparrow. Proc. Nat. Acad. Sci., 45:
1095.
10. MARSHALL,A. J., and J. D. ROBERTS. 1959. The
breeding biology of equatorial vertebrates: Reproduction of cormorants (Phalacrocoracidae) at
lat. 0 ~ 20' N. Proc. Zool. Soc. Lond., 132: 617-625.
ll. HARRISSON, W. H., and A. J. MARSHALL. Unpublished.
12. MARSHALL,A. J. 1959. Internal and environmental
control of breeding. Ibis, 101: 456-478.
13. DISNEY,H. J. DE S., B. LOFTS,and A. J. MARSHALL.
1959. Duration of the Regeneration Period of the
Internal Reproductive Rhythm in a xerophilous
equatorial bird, Quelea quelea. Nature, 184: 16591660.
14. MARSHALL,A. J., and H. J. DE S. DISNEY. 1956.
Photostimulation of an equatorial bird Quelea
quelea. Nature, 177: 143-144.
15. - - . 1957. Experimental induction of the breeding
season in a xerophilous bird. Nature, 180: 647.
16. FRITH, J. H. 1960. The ecology of wild ducks in New
South Wales. IV. Breeding. C.S.I.R.O. Wildlife
Res., 4: 156-162.
17. MARSHALL,A. J., and D. L. SERVENTY. 1959. Experimental demonstration of an internal rhythm
of reproduction in a trans-equatorial migrant (the
short-tailed Shearwater Puj~nus tenuirostris).
Nature, 184: 1704-1705.
18. - - .
1957. The breeding cycle of the short-tailed
Shearwater, PuOinus tenuirostris Temminck, in
relation to transequatorial migration and environment. Proc. Zool. Soc. Lond., 127: 489-510.
19. HARRIS, G. W. 1948. Neural control of the pituitary
gland. Physiol. Rev., 28: 138-179.
20. WINGSTRAND,S. G. 1951. The Structure and Development of the Avian Pituitary. Gleerup, Lund.
21. BARGMANN,W. 1954. Das Zwischenhirn-Hypophysensystem. Berlin-GLttingen-Heidelberg: Springer.
22. SCHARRER, E., and B. SCHARRER. 1954. Hormones
produced by neurosecretory cells. Recent Progr.
Hormone Res., 10: 183-240.
23. BENOIT,J., and I. ASSENMACHER. 1955. Le controle
hypothalomique de l'activite pr~hypophysaire
gonadotrophe. J. Physiol. (Paris), 47: 427-467.
24. OKSCHE, A., D. F. LAws, F. I. KAMEMOTO,and D.
S. FARNER. 1959. The hypothalamo-hypophysial
neurosecretory system of the white-crowned
sparrow, Zonotrichia leucophrys gambelli. Zeitschr.
Zell., 51: 1-42.
25. BISSONNETTE, T. H., and A. P. WADLUND. 1932.
Duration of testis activity of Sturnus vulgaris in
relation to type of illumination. J. Exp. Biol., 9:
339-350.
26. LOFTS, B., and A. J. MARSHALL. 1960. The experimental regulation of Zugunruhe and the sexual
cycle in the Brambling Fringilla montifringilla.
Ibis, 102: 209-214.
27. LOFTS, B., A. J. MARSHALL, and A. WOLFSON.Un-
published.
28. FARNER,D. S. Personal communication.
DISCUSSION
SEGAL: As a contribution to this portion of the symposium concerned with the longer periodicities, may I
offer the following observations on the pulmonate
gastropod Limax flavus L. I have kept populations of
L. flavus at two temperatures (10 ~ and 20~
with
unchanging photoperiod (LD 11:13) for 3 years. There
were only slight random changes in the relative humidity of the animals' environment (40-65%) over the
3 years. Thus the animals were held under conditions
which eliminated any seasonal change in temperature,
light, and humidity.
The point has been raised, during the symposium,
that the results from studies on animals living under
constant conditions may be unreliable because of the
Downloaded from symposium.cshlp.org on March 4, 2016 - Published by Cold Spring Harbor Laboratory Press
PERIODICITY IN AVIAN REPRODUCTION
very abnormality of the constant conditions. However, since growth and reproduction were not inhibited
in L. flavus, I would not consider their egg laying responses as due to the laboratory environment.
The following table shows the egg laying period of
1st and 2nd generation animals for the years shown.
In summary, I offer the following interpretations of
the data:
1. Limax flavus possesses an annual periodicity of egg
laying which persists for a number of cycles under
constant conditions.
2. In the laboratory, where the animal has no seasonal
clues, the annual cycle gradually shortens.
3. Increasing photoperiod and temperature are not
necessary to initiate egg laying in this species.
gen.
~
1st
20
1st
10
2nd
20
2nd
10
1957
late Aug.Dec. 12
late Aug.Dee. 15
505
1958
Aug. 1-Feb.
15
July 20Oct. 15
Aug. 6Mar. 6
Aug. 7*
1959
May 28Sept. 16
Jul. 1Jan. 3
Jul. 6**
May 1Dec. 26
* A single laying, no further layings until the following May.
** First laying appeared on date shown. All animals of this group killed on July 7 in defective incubator.
Downloaded from symposium.cshlp.org on March 4, 2016 - Published by Cold Spring Harbor Laboratory Press
Annual Periodicity in the Migration and Reproduction
of Birds
A. J. Marshall
Cold Spring Harb Symp Quant Biol 1960 25: 499-505
Access the most recent version at doi:10.1101/SQB.1960.025.01.052
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