AMER. ZOOL., 26:493-501 (1986)
Generation and Regulation of Annual Cycles in
Migratory Passerine Birds1
DONALD S. FARNER
Laboratory of Avian Physiology, Department of Zoology,
University of Washington, Seattle, Washington 98195
INTRODUCTION AND HISTORICAL NOTES
Species of areas with annually seasonal
environments have generally evolved control systems that regulate cyclic reproductive function in a manner that offspring are
produced at times that tend to optimize
survival of both young and parents. Among
the most elegantly precise control systems
are those of migratory passerine species
with widely separated breeding and wintering areas.
Knowledge of annual cycles very likely
became established in the lore and culture
of primitive peoples early in inhabitation
of areas with annually seasonal environments. The precision of yearly cycles in
migration and reproduction was variously
attributed to a mystique of animal wisdom
and to effects of seasonal changes in environment.
For centuries, and indeed even into the
twentieth, hypotheses of causality and control of annual cycles, especially of those of
migration and reproduction, were derived
speculatively from observations of naturalists. For example, von Homeyer (1881)
concluded that daylength, weather, and
trophic resources are the "engines" of
migration. As indicated by the reviews and
discussions of von Lucanus (1929) and
Wachs (1926), hypotheses of the preexperimental era invoked a large variety
of environmental factors and ill-defined
internal rhythms as "causes" of annual
cycles of migratory species.
Although the scientific literature of the
nineteenth century contains several suggestions of a role of daylength in the control of annual cycles in birds (cf. von Ho1
Based on a Past-Presidential Address delivered at
the Annual Meeting of the American Society of Zoologists, 27-30 December 1985, at Baltimore, Maryland.
meyer, 1881), it remained for William
Rowan (1926), from experiments with the
dark-eyed junco, Junco hyemalis, to provide
experimental evidence therefor. 2 Like
many naturalists of the preceding century,
Rowan (1926) retained a somewhat vague
concept that the annual cycle was partially
dependent on " . . . an internal, physiological impelling factor . . . ," which he
believed to be generated by the gonads.
Similarly Bissonnette (1937), after extensive experiments with the European starling, Sturnus vulgaris, invoked " . . . inherent rhythms of the anterior pituitary gland
. . ." in the causality of annual cycles.
Two major philosophic developments of
importance to comprehension of evolution
and control of annual cycles should now
be considered. The first was the dichotomization of functions of environmental factors as 'causes' of annual cycles by Baker
(1938; see also Immelmann, 1972) intow/ftmate and proximate. The former are those
factors that, in the course of evolution, have
exerted selective pressure on control systems such that they cause young to be produced at the optimal time of year. The
latter are factors that function as predictive
information for control systems. For avian
species of seasonal environments in midto-high latitudes, the primary proximate
factor is the annual cycle in daylength.
The second important development was
the removal by Aschoff (1955) of the vague
2
Indirect knowledge of a role of daylength in the
control of testicular function probably existed at least
as early as the 17th century. Dutch bird netters traditionally produced singing decoys of several migratory passerine species by holding captives on artificially short days through spring and early summer
and then transferring them to natural daylength, which
induced the development of song (Hoos, 1937). A
similar scheme was used by Japanese fanciers to induce
song in winter (Soseido-Shuyin, 1710; Senkado, 1779;
Sato, 1808).
493
494
DONALD S. FARNER
the following, primarily as summarized by
Farner and Mattocks (1986) for the whitecrowned sparrow, Zonotrichia leucophrys
gambelii:
(1) Use of predictive information for induction of vernal migration and development of
reproductive system. While birds are still in
the wintering area the system must induce
the migratory state, including essential
changes in metabolism, i.e., programmed
hyperphagia (cf King, 1961), fat deposition {e.g., King and Farner, 1965; Stetson,
1971; King, 1972a; Dolnik, 1975) for use
in migratory flight (cf. Farner et al., 1961),
FIG. 1. The annual cycle of the white-crowned spar- and in behavior, i.e., nocturnal flight (King
row, Zonotrichia leucophrys gambelii. The peripheraland Farner, 1965; Morton, 1967). The sysnumerals are estimates of mean daily expenditures of tem must also initiate and sustain, through
energy in kj per day within the indicated phases of
increased secretion of gonadotropins,
the cycle. See Farner (1980) for bases of the estimates.
Slightly modified from Farner (1980). Courtesy of gametogenic and endocrine functions of
the gonads at such a rate that they are near
Deutsche Ornithologen-Gesellschaft.
reproductive state on arrival in the breeding area at approximately mean optimal
concepts of 'innate' or 'intrinsic' rhythms time for onset of reproductive effort. The
in the generation of annual cycles (Rowan, essential temporal precision of these func1926; Bissonnette, 1937, and many others) tions requires that the system use accurate
from a scientifically unapproachable mys- predictive information derived largely, if
tique by formation of a testable hypothesis. not exclusively, from the annual cycle in
This hypothesis proposes that annual cycles daylength (cf. Farner, 1964a, 1970, 1975,
are based on endogenous circannual 1980; Wingfield and Farner, 1980).
rhythms that are entrained in phase and
(2) Fine temporal adjustment of onset of
in period to precisely annual cycles by a reproduction. Because of year-to-year variZeitgeber, such as the annual cycle in day- ation in the temporal course of phenologic
length. The hypothesis, however, proposes succession in the breeding area, a control
no mechanistic basis for generation of such system that relies solely on daylength as
rhythms. Moreover, as yet, no physiologi- either a driver or Zeitgeber for an endogecally acceptable explanation therefor has nous circannual rhythm, would be unsucbeen forthcoming.
cessful. In Z. /. gambelii, and presumably in
at least some other migratory passerine
CAPABILITIES OF THE CONTROL SYSTEMS
species, use of daylength as predictive
Although the basic function of the annual information functions to bring flocks into
cycle is the production of young at a time the breeding area at approximately the
that optimizes their survival and that of mean time for onset of the annual reprotheir parents, under pressure of natural ductive effort. Thereafter, other inforselection control systems have evolved in mation derived from the environment,
such a manner that other functional ele- physical and biotic, including mates and
ments of the annual cycle occur at rather other conspecifics, is used to synchronize
fixed phase angles with the onset and ter- the beginning of reproductive function
mination of reproduction (Fig. 1). These within pairs and with the phenologic develtemporal relationships among elements of opment of the breeding area. The addithe annual cycle reflect essential capabili- tional information that comes into play at
ties of the control systems of migratory pas- this time can be categorized functionally
serine species. Among these capabilities are in various ways, such as modifying, essential
ANNUAL CYCLES IN MIGRATORY PASSERINE BIRDS
495
supplementary, synchronizing, etc. (e.g., nificance is a projection of LHRH fibers
Thomson, 1949; Immelmann, 1963, 1972; from the preoptic area into the pineal stalk
Farner, 1964a; Farner and Wingfield, that can be demonstrated early in the
1980; Wingfield, 1984, 1985). The sensory development of photorefractoriness (Blahand neuroendocrine bases of processing of ser etal, 1986).
the plethora of environmental information
(4) Separation of ergonically and/or temconstitute a challenge of first magnitude to porally incompatible functions. This capabilinvestigators of the physiology of annual ity is most conspicuous in small migratory
cycles.
species in which metabolic rates are gen(3) Use of predictive information for termi- erally high (Fig. 1). Among other advannation of seasonal reproduction and inductiontages this separation assures a relatively
of post-breeding functions. As a contributor uniform mean daily expenditure of energy
to fitness, the timely termination of the throughout the annual cycle (Farner,
seasonal reproductive effort is second only 1964a; Farner and Mattocks, 1986).
to optimally timed onset thereof. Although
(5) Endocrine and behavioral adjustments
there are several possible mechanisms by for multiple broods and/or re-nesting. Fitness
which the former can be effected (Lofts is enhanced by these phenomena providing
and Murton, 1968) the most prevalent is that timing thereof is such that young are
that of photorefractoriness (for review and produced while environmental conditions
references, see Farner et ai, 1983), a phe- are favorable for survival and in time for
nomenon of the hypothalamus or higher molt and normal onset of migration by both
centers in the central nervous system in offspring and parents. Endocrine features
which the system becomes insensitive to of these phenomena have been described
otherwise stimulatory long days. In Z. /. for Z. leucophrys (E. S. Hiatt, A. R. Goldgambelii, and apparently in at least some smith, and D. S. Farner, submitted ms.;
other species, photorefractoriness, which Wingfield and Farner, 1980; and Wingis physiologically tightly coupled with field and Farner, 1979, respectively).
development of flocking behavior, postnuptial molt and premigratory fattening
PHOTOPERIODIC CONTROL SYSTEMS
(reviews by Farner et al., 1983; Meier and
Russo, 1985), is also induced by long days
The basic features of avian photoperidespite the delay in its overt expression odic control systems were first established
(e.g., Vaugien, 1948; Wolfson, 1952; Far- by Jacques Benoit and colleagues in extenner, 1964a; Moore et al., 1982). Its devel- sive investigations on Pekin drakes (for
opment is independent of circulating sex summary and discussions, see Assenhormones (Wilson and Follett, 1974; Mat- macher, 1958, 1970; Benoit, 1937).
tocks et al, 1976; Mattocks, 1985) and Because there have been several recent
gonadotropin (Matt and Farner, 1979; Far- reviews of these systems and their funcneretal., 1983; Wilson and Donham, 1987). tions (e.g., Farner and Follett, 1979; Farner
Hypothalamic secretion of LHRH is low and Wingfield, 1980; Wingfield and Far(Erickson, 1975; Dawson et al., 1985) al- ner, 1980; Jallageas and Assenmacher,
though the pars distalis remains sensitive 1981; Follett, 1984), I dwell here primarily
to LHRH (Wingfield et al., 1979). The on recent developments, especially those
mechanism of induction remains unclear pertinent to migratory passerine species.
although involvement of thyroid horAvian photoperiodic control systems are
mones (Woitkewitsch, 1940; Wieseltier and
van Tienhoven, 1972; Follett and Nicholls, characterized by encephalic photorecep1984), prolactin (Goldsmith et al, 1985), tors, which, in a sense, were first demonand phase angle between daily rhythms of strated as early as the sixteenth century
circulating prolactin and corticosterone through the practise of muiten by Dutch
(Meier and Ferrell, 1978; Meier and Russo, bird netters. In this process blinded decoys
1985) have been proposed. Of possible sig- of several passerine species were changed
from artificial short days to natural day-
496
DONALD S. FARNER
length in late summer to induce singing
(Hoos, 1937), certainly caused by increased
levels of circulating androgens. However,
it remained for Ivanova (1935) in experiments on house sparrows, Passer domesticus,
and much more extensively, Benoit and his
colleagues {e.g., Benoit, 1935, 1937, 1961)
on Pekin drakes to establish experimentally the role of such receptors in photoperiodically induced testicular development.
The existence of encephalic photoreceptors has now been demonstrated by several
techniques in at least eight species of three
orders of birds. Generally they appear to
occur ventrally in the hypothalamus in the
tuberal region (for review of sites, sensitivity and also involvement of possible roles
of retinal receptors, see Oliver and Bayle,
1982). The extent to which non-visual retinal receptors are involved is not clear;
there are probably interspecific differences. Although apparently in error concerning the infundibular nucleus as a source
of LHRH, these authors (ibid.) present a
testable model of these relationships in the
photoperiodic control of secretion of
LHRH.
In a recent series of ingenious experiments Foster and Follett (1985) have demonstrated that the photopigment in hypothalamic receptors is rhodopsin-like.
However, the receptors themselves have
not yet been identified morphologically. As
in other species thus far studied, the encephalic photoreceptors in Zonotrichia leucophrys, the most extensively studied passerine species, are located ventrally in the
tuberal region of the hypothalamus
(Yokoyama et ai, 1978). Photostimulation
of this area not only induces normal testicular growth, but also the development
of vernal migratory behavior (Yokoyama
and Farner, 1978).
Quantitative demonstration that rates of
photoperiodically induced testicular
growth are precise functions of daylength
(Farner and Wilson, 1957; Dolnik, 1963;
Farner et ah, 1966) opened the question of
the mechanism of measurement thereof.
A series of investigations, beginning with
those of Hamner (1963) on house finches,
Carpodacus mexicanus, and Farner (19646)
on Zonotrichia leucophrys produced data
from several species that are most parsimoniously interpreted in models with circadian oscillators (for resumes, see Farner,
1975; Dolnik, 1976; Pittendrigh and Daan,
1976; Turek, 1978; Meier and Russo,
1985). All models, either explicitly or
implicitly, couple the oscillating system that
measures daylength with endogenous
"master" or "pacemaker" circadian systems. Although these systems have been
extensively characterized in an empirically
formal sense, little is known about their
physiologic basis. Menaker (1982) has proposed that the core of the avian circadian
system consists of elements of diencephalic
origin in the pineal body, retina, and suprachiasmatic nucleus, a concept that has now
been presented in a formal, testable model
by Cassone and Menaker (1985). Although
this model involves some rather seemingly
tenuous assumptions, and is difficult to
rationalize with some published observations, it may well prove to be a heuristically
useful step towards an understanding of
the measurement of daylength in photoperiodic species of birds.
Another significant hiatus in our knowledge of avian photoperiodic control systems is that of the quantitative transduction of information in the form of nerve
impulses received either directly or indirectly from photoreceptors in the ventral
tuberal region of the hypothalamus into
LHRH by neurosecretory cells in the
supraoptic and paraventricular nuclei.
These cells transmit LHRH via relatively
long axons into the median eminence of
the hypothalamus where it is transferred
into blood capillaries of the hypothalamohypophysial portal system which delivers
blood directly into the sinuses of the anterior pituitary gland (Oksche and Farner,
1974). Here gonadotropes respond in a
quantitative manner to LHRH by release
of gonadotropic hormones. Wingfield and
Farner (1980) have presented a general
scheme of these and other relationships
derived largely from investigations on
Zonotrichia leucophrys gambelii, in which we
also erred, in light of more recent information (S. Blahser, A. Oksche, and D. S.
Farner, unpublished results), in designat-
497
ANNUAL CYCLES IN MIGRATORY PASSERINE BIRDS
ing the infundibular nucleus instead of cells
in the supraoptic and paraventricular
regions as the source of LHRH.
INTERACTION OF PHOTOPERIODIC AND
NON-PHOTOPERIODIC INFORMATION IN
WHITE-CROWNED SPARROWS
As noted above, annual cycles produced
by a control system dependent on daylength alone would be unsuccessful. This
is obvious from the well known year-toyear variations in temporal schedules of
phenologic succession in breeding areas to
which adjustment requires the use of nonphotoperiodic modifying information (Farner, 1964a; Morton, 1978; Wingfield,
1980, 1985). Unseasonally inclement
weather or storms also provide modifying
information, depending on time of occurrence in the reproductive period (Wingfield et al, 1983; Wingfield, 1984, 1985).
Inclement weather during feeding of young
results in increased circulating levels of
corticosterone, loss of fat reserves, and
abandonment of nest but without effect on
circulating levels of gonadotropin and sex
hormones so that re-nesting can occur when
weather ameliorates.
Unlike males, in females, which arrive
later in the breeding area, long days have
induced only a partial development of the
reproductive system, although under adequate conditions completion of development can occur in less than ten days. This
means that, in addition to photoperiodic
information, essential supplementary information from the local environment,
including a territory-defending mate (e.g.,
Morton et al, 1985), adequate trophic conditions, etc., is required for final development of the reproductive system. This
"fine-tuning" by use of local information
seems clearly to be an adaptation to the
greater cost of development of the reproductive system and production of eggs on
the part of the female (e.g., King, 19726)
and for enhancement of success in production of young. Interaction between
mates functions as synchronizing information
and also as modifying information in increasing the activity of the endocrine testis of
the male, which is also increased by interaction with males in adjacent territories.
SD elimination of Phr
SD elimination of Phr
FIG. 2. Schematic approximation of the relative roles
of daylength and of modifying, synchronizing and
essential supplemental information from the breeding environment in the annual cycle of the whitecrowned sparrow, Zonotnchia leucophrys gambehi. Ver-
tical axis represents development of gonads from
resting level in winter to functional state. Crosshatched areas indicate development induced beyond
that attained by photoperiodic stimulation alone. Wt)
weight of testes; Wo, weight of ovary; LD, long days;
SD, short days; PhR, photorefractoriness; PnM, postnuptial molt; Mi, migration. From Farner and Gwinner (1980). Courtesy of Academic Press.
Because essentially nothing is as yet
known of the processing of non-photoperiodic information, and because endocrine
correlates of its use varies interspecifically
even in species of closely related genera,
e.g., Zonotrichia leucophrys and the song
sparrow, Melospiza melodia (Wingfield,
1984, 1985), Figure 2 and the remainder
of this section are based, except for comparative notes, largely on the former (for
resumes, see Farner, 1975; Wingfield and
Farner, 1980; Farner and Mattocks, 1986).
All evidence indicates that long days are
essential for the development of the reproductive system, complete in males, but partial in females, which require additional
non-photoperiodic information. Withdrawal of long days at any stage of development is followed by regression of the
reproductive system as circulating levels of
gonadotropins return to minimum levels.
Birds held on short days fail to undergo
gonadal development for at least four years.
As in at least some other passerine species
498
DONALD S. FARNER
(for reviews see, Wolfson, 1970; Dolnik,
1975, 1976; Farner et al, 1983), photorefractoriness develops only under long
days (Moore et al., 1982) and at a rate that
is a direct function of daylength (Moore et
al., 1983). It fails to develop if long days
are withdrawn too early in the cycle (Moore
et al., 1983; D. S. Farner, P. W. Mattocks,
Jr., H. Schwabl, and I. Schwabl-Benzinger,
unpublished results).
Re-nesting may occur if clutch or young
are lost no later than the first week in July.
This delays the onset of postnuptial molt,
probably because of increased levels of sex
hormones (Wingfield and Farner, 1979).
Thereafter, the postnuptial and postjuvenal molts are accelerated so that they are
completed at about the same time as in
non-renesters. This acceleration may be an
effect of shortening days (Moore et al.,
1983), a phenomenon well established for
the chaffinch, Fringilla coelebs, by Dolnik
(1980) and Noskov (1977). Photorefractoriness is terminated by short days after
the termination of autumnal migration (e.g.,
Farner and Mewaldt, 1955), as in at least
several other migratory species (for reviews,
see Wolfson, 1970; Dolnik, 1975, 1976;
Murton and Westwood, 1977; Farner et al.,
1983). In the congeneric white-throated
sparrow, Zonotrichia albicollis, in which photorefractoriness is also terminated naturally by shorter days in autumn, Miller and
Meier (1983) have reported that it can be
terminated by injections of 5-hydroxytryptophan, a precursor of prolactin-releasing
serotonin, and dihydroxyphenylalanine, a
precursor of catacholamines, at an appropriate phase angle.
Because the control systems of Z. /. gambelii are dependent on long days for induction and maintenance of the vernal events
of the annual cycle, in concert with other
environmental information for the control
of reproduction function, and for the
development of photorefractoriness, which
terminates reproduction, the role of the
annual photocycle is frequently designated
as that of a driver. This is in contrast to its
role as a Zeitgeber or synchronizer for species
with endogenous circannual rhythms (e.g.,
Farner, 1985; Farner and Mattocks, 1986).
ENDOGENOUS CIRCANNUAL RHYTHMS
Following the publication of the hypothesis of Aschoff (1955), which for photoperiodic species assigns to the annual cycle
in daylength the role of a Zeitgeber for
endogenous circannual cycles, a substantial
quantity of observations in support thereof
has been forthcoming. Depending on criteria for acceptance, evidence for the existence of endogenous circannual rhythms
has appeared for at least a dozen migratory
passerine species (cf. Berthold, 1974, 1977,
1980; Gwinner, 1977, 1986; see also Murton and Westwood, 1977; Tyshchenko et
al., 1980; Farner, 1985). It must be noted,
however, that these observations have generally been made on birds under constantly
repeated 24-hour photoregimes with fixed
duration of light, i.e., 12L 12D, 14L 10D,
etc. Like King (1968), Hamner (1971), and
others, I (e.g., Farner, 1985) have also questioned whether such photoregimes constitute the "constant conditions" necessary
for unequivocal demonstration of endogenous circannual rhythms, despite ingenious arguments from the aspect of formal
properties of oscillators applied to observations under such conditions (e.g., Aschoff,
1980; Gwinner, 1981, 1986).
Apparently the first unequivocal evidence for an endogenous circannual
rhythm in an avian species is that obtained
by Chandola et al. (1983) from investigations on the spotted munia, Lonchura punctulata, an Indian species that breeds in
autumn after the monsoon. These investigators demonstrated three consecutive
circannual cycles in testicular size with
periods somewhat shorter than one year
under constant conditions, including continuous light, thereby satisfying the most
rigid requirements for demonstration of
such cycles. But also of great importance,
spotted munias held continuously on 12L
12D underwent rather similar cycles,
thereby increasing the probability that the
observations cited in the previous paragraph may indeed indicate cases of genuinely endogenous rhythms. The results of
Chandola et al. (1983) lend credence to the
suggestion (e.g., Farner, 1975) of the evolution of spectrum of avian photoperiodic
ANNUAL CYCLES IN MIGRATORY PASSERINE BIRDS
control systems from those that are dependent on environmental information, with
daylength serving as a driver, to those that
are dependent primarily on endogenous
circannual rhythms, the physiological bases
of which remain unknown, for which the
annual cycle in daylength serves as a Zeitgeber. But as further investigations unfold
the very great variety of adaptations among
control systems, which must reflect a very
great heterogeneity of genetic information
from which genotypes are produced and
selected, it appears increasingly clear that
this generalization is doubtless overly simplistic.
ACKNOWLEDGMENTS
Unpublished results and observations
cited in this communication are from
investigations supported by the National
Science Foundation. I am most grateful to
Professor Shinichi Matsuo who drew my
attention to Japanese books containing
information on the practise of yogai and
informed me of their pertinent contents.
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