AMER. ZOOL., 35:259-273 (1995)
Endocrine Bases of Spatial and Temporal Opportunism in
Arctic-Breeding Birds1
THOMAS P. HAHN 2 , JOHN C. WINGFTELD, RANDALL MULLEN
Department of Zoology, NJ-15, University of Washington, Seattle, Washington 98195
AND
PIERRE J. DEVICHE
Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska 99775
SYNOPSIS. The primary objectives of this paper are to define, explore
the environmental factors favoring, and discuss hypotheses concerning
the endocrine bases of two important arctic breeding strategies that we
call spatial and temporal opportunism. We identify several species that
display spatial opportunism in the Arctic, and one that displays temporal
opportunism. In spatial opportunism, breeding may be highly seasonal
but the locality where individuals breed may change from year to year as
a result of unpredictable spatial distribution of food, nest site availability,
or other factors such as predator abundance. We suggest that flexibility
of the transition from migration to settlement distinguishes spatial opportunists from site-faithful migrants. Thus far, data are available for only
two hypotheses regarding the endocrine basis of this flexibility. Circulating
patterns of testosterone (associated with territory establishment) and corticosterone (associated with migratory activity) appear not to be involved
in the regulation of spatial opportunism in white-crowned sparrows
(Zonotrichia leucophrys gambelii), but more detailed study is necessary.
In temporal opportunism (that may occur simultaneously with spatial
opportunism), temporally variable food availability apparently selects for
the capacity to initiate reproduction across a wide portion of the year.
Tonic activity of the hypothalamo-pituitary-gonad (HPG) axis could provide a mechanism to minimize the delay between discovery of abundant
food and onset of nesting in any season. However, the evidence for one
arctic temporal opportunist, the white-winged crossbill (Loxia leucoptera),
indicates that the HPG axis is not tonically active, but probably switches
off (i.e., becomes photorefractory) in autumn, as for other birds breeding
at these latitudes. Opportunistic breeding very early in the year (e.g.,
March near Fairbanks, Alaska) is associated with increased luteinizing
hormone secretion, probably in response to a combination of abundant
food and social stimuli, after refractoriness dissipates. We have taken the
first step of identifying spatial and temporal opportunism as important
phenomena in the Arctic, and discussing hypotheses related to endocrine
mechanisms. Future research should identify specific environmental cues
involved, and elucidate the neuroendocrine and endocrine mechanisms
underlying these two reproductive strategies.
1
From the Symposium Endocrinology ofArctic Birds
INTRODUCTION
and Mammals presented at the Annual Meeting of the
In many temperate zone habitats, enviAmerican Society of Zoologists, 27-30 December, 1993 r o n m e n t a l variation occurs on a regular seaat
^ S d d r S o O f T h o m a s P. Hahn: Department «onad schedule, and the most favorable seaof Psychology, Johns Hopkins University, Baltimore, son tor breeding can be anticipated using a
Maryland, 21218.
combination of initial predictive cues (e.g.,
259
260
T. P. HAHN ET AL.
photoperiod) to time long-term patterns of
reproductive activity and quiescence, and
supplementary cues {e.g., temperature, food
supply) that permit adjustment of reproductive function to local conditions (Wingfield, 1983; Wingfield and Kenagy, 1991).
Specific locations may be good for breeding
year after year, and individuals of many species either are sedentary or return to the
same location for breeding each year.
Arctic habitats are even more profoundly
seasonal. During much of the year, conditions are inhospitable, and most bird species that breed here migrate to milder climates for the winter. Breeding is restricted
to a few weeks surrounding the summer solstice {e.g., Baker 1938; Irving, 1960). The
brief period of mild temperatures and high
food availability conducive to breeding in
the Arctic selects for the use of the annual
photocycle as an initial predictive cue to
time changes in reproduction, migration and
molt (see Wingfield et al., 1992, 1993).
Physiological responses to photoperiod are
well-studied in a variety of arctic- and temperate-breeding birds {e.g., Follett, 1984;
Farner and Lewis, 1971; Farner and Wingfield, 1980; Wingfield and Farner, 1980),
and we know a great deal about the physiologic basis for seasonality of reproduction
and migration in the arctic environment.
Perhaps paradoxically, another prominent feature of arctic habitats is their unpredictability. For example, how long snow
cover persists into spring, weather during
spring and summer, and abundance of specific insect foods, can vary annually and from
place to place {e.g., Aim et al., 1966, 1973;
Kalela, 1962;Strahler, 1973). This topic has
received much attention from ecologists,
since long-term unpredictability of conditions (as opposed to short-term unpredictability over a few hours, e.g., stress, Wingfield, 1983) appears to contribute to reduced
community stability at high latitudes {e.g.,
Jarvinen, 1979; Hutchinson, 1959;Klopfer
and MacArthur, 1960). Work on mating
systems {e.g., Pitelka et al, 1974) and sitefidelity {e.g., Mikkonen, 1983; Lindstrom,
1987) has revealed that many arctic-breeding birds display "opportunistic" strategies
that permit them to adjust to long-term
unpredictable conditions.
Two distinct components to unpredictability of the environment—spatial unpredictability and temporal unpredictability—
select for two different kinds of opportunistic strategies: spatial opportunism and temporal opportunism. The environmental factors selecting for, and physiologic
mechanisms underlying, these two strategies may differ. Although spatially opportunistic species probably are more prevalent
in the Arctic than temporal opportunists,
both kinds of opportunism can occur at high
latitudes. Other aspects of the biology of
organisms besides the timing or location of
breeding can be opportunistic {e.g., mating
system, spatial dispersion of breeders, see
Pitelka et al., 1974), however, we have chosen to focus only on spatial and temporal
opportunism in this paper. Data on the
endocrine bases of opportunism in the Arctic are as yet scant, but we will present a
general framework of definitions and
hypotheses that can direct further study. We
believe that by studying the selective and
mechanistic bases of opportunism in arctic
birds, we come towards a more general
understanding of how all animals have
evolved to make adjustments to changing
environments.
SPATIAL OPPORTUNISM
Spatial unpredictability results when relevant events in the environment do not
occur reliably at particular locations. In
Australian deserts, for example, rainfall is
spatially erratic (patchy) in any given year,
and the spatial pattern of rainfall varies from
one year to the next. This spatial unpredictability may select for the strategy of spatial opportunism, where birds wander widely
in search of locations with conditions favorable for breeding (Serventy, 1971; Keast,
1959; Immelman, 1963). Many Australian
desert birds also show highly flexible timing
of reproduction with respect to season {i.e.,
temporal opportunism, see below). However it is possible for an organism to breed
on a rigid seasonal schedule yet be a spatial
opportunist. The fact that spatial unpredictability of most arctic habitats is superimposed on a predictable seasonal cycle
means that most spatial opportunists in the
Arctic will also be seasonal breeders.
SPATIAL AND TEMPORAL OPPORTUNISM
Andersson (1980) developed a quantitative model for spatial opportunism that predicts when either of two opposite strategies,
nomadism and site tenacity, will be selectively favored. He assumes an environment
varies in time and space either in a cyclic
(predictable) manner or at random (unpredictable). If conditions conducive to successful breeding recur at regular intervals at
particular locations, nomadism will only be
favored (1) when the probability of finding
a better area to breed by searching is relatively high (also affected by the mobility and
search efficiency of the bird, and by the
abundance and spatial dispersion of good
localities), and/or (2) when the interval
between good seasons at any particular
locality is predictable but relatively long (i.e.,
with respect to the life span of individuals,
see below). Conversely, low probability of
a successful search, and frequent occurrence
ofgood conditions at any particular site, will
tend to favor site tenacity. In an alternative
environment where conditions conducive
to successful breeding only recur at unpredictable intervals at any given location,
nomadism will be favored whenever the
probability of finding a good area by searching exceeds the probability that good conditions will occur at a particular locality in
a given year.
Spatial opportunism may not always be
favored simply because conditions conducive to successful nesting fail to occur every
year at a particular location. In some cases
the probability of finding a better site may
be so low as to favor returning to the same
site year after year, even though breeding
cannot always occur. This prediction is supported by the observation of Marshall (1952)
that many arctic birds (especially long-lived
seabirds for whom suitable nesting areas are
few and far between) sometimes entirely fail
to breed, but still remain near the normal
breeding area throughout the breeding season.
Several species for which there is evidence of spatial opportunism are shown in
Table 1. This list is not intended to be
exhaustive, but reveals that spatial opportunism occurs in a variety of avian taxa,
including at least passeriformes, strigiformes and charadriiformes. Clearly this is
261
not an aberrant strategy, but one of general
significance in the Arctic. We will discuss
two examples, the brambling and the Gambel's white-crowned sparrow, to demonstrate how unpredictability in the environment may select for spatial opportunism.
Brambling (Tringilla montifringilla,):
spatial opportunism based on spatial
variation in food abundance
The brambling is a classic example of a
highly seasonal breeder that relies on changes
in day length to time the cycle of the gonads
and migration (e.g., Dolnik 1963, fide Newton, 1973). It differs from many seasonal
species however, in its erratic movement
patterns, both in winter and with respect to
where it settles to breed in summer. Mikkonen (1983) found that bramblings showed
no breeding site-tenacity in northern Finland (i.e., birds banded one year failed to
reappear the next year). Numbers of caterpillars, Epirrita autumnata, a principal food
of breeding bramblings, fluctuate cyclically
with about 10-12 years between peak numbers at particular localities (Andersson and
Jonasson, 1980,,/k/e Lindstrom, 1987). Caterpillars are abundant for two or 3 consecutive years in each cycle, and peak numbers
of breeding bramblings coincide with peak,
or near-peak, abundance of caterpillars
(Lindstrom, 1987; Hogstad, 1969; Silvola,
1967). In Lindstrom's study (1987) only two
adult bramblings banded on their breeding
grounds were recaptured in subsequent
breeding seasons. One of these, an adult
male, was trapped at its original breeding
location the next year. The other, an adult
female, was found the next year on its new
breeding site 420 km away from the previous breeding location. It is noteworthy that
the single case of site fidelity observed by
Lindstrom (1987) occurred over two years
spanning the peak caterpillar abundance in
the Epirrita cycle at that location.
Optimal conditions for reproduction (i.e.,
peak food abundance) may occur cyclically
at a given location, but the interval (10-12
years) is very great relative to the life expectancy of individual birds. No data are available on longevity of free-living bramblings,
but the closely related chaffinch (F. coelebs)
exhibits mean life expectancy of around 2.5
262
T. P. HAHN ET AL.
TABLE 1. Examples ofarctic-breeding birds that appear to be spatial and temporal opportunists, based on citations
listed at right.
Spatial opportunists
Strigi formes
Tengmalm's owl (Aegolius funereus)
Snowy owl (Nyctea scandiaca)
Short-eared owl (Asio jlammeus)
Charadriiformes
Pomerine jaeger (Stercorarius pomerinus)
White-rumped sandpiper (Calidris fuscicollis)
Curlew sandpiper (Calidris ferrugined)
Little stint (Calidris minuta)
Pectoral sandpiper (Calidris melanotos)
Buff-breasted sandpiper (Tryngites subruficollis)
Passeriformes
Brambling (Fringilla montifringilla)
Redpoll (Carduelis flammed)
White-winged crossbill (Loxia leucoptera)
Temporal opportunist
White-winged crossbill (Loxia leucoptera)
years (Anven and Enemar, 1957; Bergman,
1956), and even this is considered rather
high compared to other European songbirds
(Newton, 1973; Lack, 1954). Clearly, sitefidelity is not a reasonable strategy for the
brambling, since individuals returning
repeatedly to a single site might never experience high abundance of Epirrita. Given
the fact that caterpillar numbers tend to peak
over several years at any given site (see
above), it would not be surprizing if bramblings showed "facultative spatial opportunism," first returning to a good breeding
location used the previous year and only
moving on if caterpillar numbers appeared
to have crashed. However, the available data
(e.g., Lindstrom, 1987) suggest that individuals rarely use this strategy.
Gambel's white-crowned sparrow
(Zonotrichia leucophrys gambeliij:
spatial opportunism based on nest
site availability
This is one of the most intensively studied
bird species concerning effects of environmental cues on timing of the annual cycle
of reproductive physiology, molt and
migration (e.g., Farner and Follett, 1979;
Lofgren et al., 1986
Batzli <?/a/., 1980
Batzli et al., 1980
Batzlief a/., 1980
Pitelka et al., 1974; Holmes and
Pitelka, 1964; Parmelee et al., 1968
Pitelka et al, 1974; Holmes and
Pitelka, 1968
Hilden, 1979 (cites unpublished data)
Pitelka et al., 1974; Pitelka, 1959;
Holmes, 1966
Pitelka et al, 1974; Parmelee et al., 1967
Lindstrom, 1987; Mikkonen, 1983;
Newton, 1973
Newton, 1973
Newton, 1973; Benkman, 1987a, 1990
Newton, 1973; Benkman, 1987a, 1990
Farner and Wilson, 1957; Wingfield and
Farner, 1980, 1993). These birds typically
winter in the American southwest and
migrate to breeding grounds in western
Canada and Alaska (Cortopassi and
Mewaldt, 1965), undergoing gonadal development during the vernal migration (Blanchard and Erickson, 1949; King et al., 1966;
Wingfield and Farner, 1978), with very little
inter-year variation in timing (Wingfield et
al., 1992). Our recent work at Toolik Lake,
on the North Slope of the Brooks Range in
Alaska (68°38'N, 149°38'W), has revealed
that Gambel's white-crowned sparrows display very low site fidelity as estimated by
returns of banded individuals. From 1991
to 1993, we recaptured in subsequent years
less than 7% of Gambel's white-crowned
sparrows banded at Toolik Lake (Table 2).
This low return rate stands in contrast to
the consistently high rate of return of lapland longspurs (Calcarius lapponicus) at the
same locality (Table 2). It is unlikely that
Gambel's white-crowned sparrows have
poor annual survival, because banding studies on their wintering grounds in California
reveal much higher return rates (35%) among
years (Blanchard and Erickson, 1949). It is
263
SPATIAL AND TEMPORAL OPPORTUNISM
TABLE 2. Site fidelity in two passerines breeding at Toolik Lake, Alaska.*
Species
Lapland longspur
1991
1992
136
41
150
0
15
GambeFs white-crowned sparrow
12
1993
54
1
% return
30
36
0
7
* Numbers in each row represent the total banded in one year (first entry in the row) and the number of that
original cohort that was observed or recaptured the following year (second entry in the row). The percent return
column indicates what percentage of the original cohort banded returned to Toolik Lake the following year.
Note: The numbers of birds banded in each year are not indicative of the numbers of breeding birds in the area
in the two years. All of the sparrows banded in 1991 ended up remaining to breed, while most of the birds
banded in 1992 were present only transiently at the beginning of the breeding season when snow still filled all
potential breeding habitat.
more likely that Gambel's white-crowned
sparrows behave as reproductive spatial
opportunists, settling to breed in different
locations each year.
Our observations suggest that unpredictability of nest sites acts as the ultimate factor
{cf. Baker, 1938) selecting for spatial opportunism in this case. In northern Alaska,
white-crowned sparrows nest on the ground
in willow thickets in low-lying areas along
streams and depressions in the tundra. Snow
accumulation in these preferred nesting areas
is much greater than on surrounding open
tundra (Figure IB) and meltoff of this deep
snow (over 2 meters deep in late May of
1992) in the willows takes much longer. This
difference is exaggerated because there is a
non-linear relationship between snow depth
and rate of meltoff. As long as snow depth
exceeds 20-30 cm, melting occurs mostly
from the top down because less than 10%
of incident light reaches the ground (Kirk,
1980). Once snow depth declines to around
30 cm or less, melting can commence from
beneath as well, due to penetration of solar
radiation through to the underlying ground.
Deep snow also becomes more dense as it
partially melts and refreezes. Ultimately
much more energy is required to melt the
last dense remnants completely than would
be required for an equivalent depth of fresh
snow (Kane et ai, 1992). Together, these
phenomena mean that deep snow accumulations (e.g., in willows) will take much
longer to disappear than the shallower accumulations on open areas frequented by lapland longspurs (Fig. 2). Note also that accumulation of new snow on bare ground is
much less than on remaining snow cover
(Fig. 3). Since spring storms are frequent in
the Arctic, this results in even greater snow
depth in the willow thickets and further
delays in meltoff.
When white-crowned sparrows arrive on
the North Slope and begin to seek suitable
nesting sites in mid- to late-May, snow pack
can vary tremendously from year to year,
and is spatially patchy within years. This
results in year-to-year variation in where
earliest onset of nesting will be possible.
Open tundra nesters such as lapland longspurs are not as affected, since snow depth
Snow accumulation
FIG. 1. Comparison of snow cover in the vicinity of
Toolik Lake, Alaska, on 20 May in two different years.
(A) 1991, winter accumulations were light, and virtually all had melted from both open areas and willow
thickets by the time white-crowned sparrows arrived
in mid-May. (B) 1992, winter accumulations were
heavy, and an additional 20 cm of snow fell during
mid-May. Approximately 0.5 m of snow remained on
open tundra, and 2-3 m of snow remained in willow
thickets, when white-crowned sparrows began arriving
on 25 May 1992.
264
T. P. HAHN ET AL.
20 n
c
o
E
u
S 3
05
• p = 0.0001
10-
fu l
1 0 -
o
TIME TO MELT
FIG. 2. Comparison of rate of snow melt at different
depths of snow. Solar radiation can penetrate about
20^-30 cm of snow to underlying tundra, warming it
and causing bottom-up as well as top-down melting.
Only top-down melting occurs at snow depths greater
than 30 cm. Below 20 cm when bottom-up melting
commences, meltoff speeds up. Note that increase in
snow accumulation over 30 cm produces a much greater
increase in melt time.
is usually less than 30 cm in the open and
meltoff is very rapid. In 1991, snow pack at
Toolik Lake was very light and most nesting
areas were already snow-free by the time
white-crowned sparrows arrived in midMay (Figure 1A). Breeding white-crowned
sparrows were abundant in that year, with
a minimum of 21 pairs in the vicinity. In
contrast, snow pack in 1992 was very heavy
(Figure 1B), and a wave of white-crowned
sparrows that passed through Toolik Lake
in late May mostly disappeared well before
the willow thickets were free of snow. Only
3 pairs bred in the vicinity in 1992. In contrast, the willow thickets around ponds near
Siope Mountain by the Sagavanirktok River
(a site about 30 km north of Toolik Lake)
were already nearly free of snow in late May
of 1992 when similar habitat near Toolik
lake still contained 1-2 m of snow. Thus,
there is substantial variation within years
in the time when nest sites become available
at different sites, and these sites can be close
enough together that probability of discovery of suitable breeding habitat if birds continue to search should be high. Under these
conditions Andersson's model would favor
a spatially opportunistic breeding strategy.
Our data on Gambel's white-crowned sparrows are insufficient to tell whether the birds
first check previous nesting areas before
pi oceeding to search elsewhere if those areas
Bare ground
Snow pack
FIG. 3. Accumulation of new snow on bare ground
versus existing snow at Toolik Lake in May, 1992.
Measurements were made at 12 sites on bare ground
and adjacent snow covered areas after a storm deposited about 20 cm of new snow. The accumulation on
existing snow pack is much greater than on bare ground
despite identical precipitation (t = -11.708, P < 0.0001,
df = 22, unpaired and 1-tailed).
are snow-filled. This would require data
from 2 consecutive early meltoff years,
which has as yet not occurred during our
study at Toolik Lake.
Possible endocrine mechanisms of
spatial opportunism
Spatial opportunism in the Arctic must
be achieved by an integration of environmental information. Initial predictive cues
(e.g., photoperiod) induce the bird to migrate
back to the Arctic while preparing the reproductive system for breeding. Supplementary cues such as food supply and nest site
availability that permit individuals to fine
tune when and where they terminate migration and initiate nesting then become relevant. In site faithful species, migration can
be terminated as soon as the individual
reaches the previously determined breeding
site. If upon arrival conditions do not yet
permit onset of nesting, then the bird waits
(i.e., a response to inhibitory supplementary
information, cf. Marshall, 1970; Wingfield,
1983). This is precisely what the site-faithful mountain white-crowned sparrow
(Zonotrichia leucophrys oriantha) does in
the Sierra Nevada of California (Morton,
1978). In contrast, spatial opportunists
would continue to search until they discover
what they consider to be a suitable nesting
SPATIAL AND TEMPORAL OPPORTUNISM
site. If spatial unpredictability is on a relatively small scale {e.g., a few km for a sparrow), then this searching could be little more
than wandering in the general area where
the bird stops migrating. On the other hand,
if spatial unpredictability is more large scale,
as is certainly true for the brambling and
probably often for Gambel's white-crowned
sparrows as well, then the birds may remain
in a migratory state, covering large distances
while searching. In the most extreme case,
nomadic activity would continue throughout the entire breeding season if no place
suitable for nesting is discovered. Thus, we
suggest that the important mechanisms to
understand in spatial opportunism are those
underlying termination of migratory activity and/or settlement in a breeding area. A
variety of endocrine factors have been
implicated in the control of vernal migration (see Wingfield et al., 1990 for review),
suggesting possible mechanisms of regulation of spatial opportunism. We will examine two testable hypotheses here.
1. Testosterone as inhibitor of continued
migratory activity. — With few exceptions
{e.g., brown-headed cowbird, Dufty, 1993),
migratory birds held in captivity throughout the normal breeding season never
develop circulating testosterone (T) levels
as high as free-living birds {e.g., Wingfield
and Farner, 1980). In these birds, spring
migratory restlessness (Zugunruhe) persists
until they become photorefractory in midsummer or on artificial long days (see
Schwabl and Farner, 1989). It has been proposed that elevated T levels associated with
territory establishment and breeding could
serve as an endocrine signal to prevent continued migratory activity on arrival at the
breeding grounds (see Wagner, 1961). It is
thus possible that T levels in captives are
never high enough to terminate migratory
activity. However, Schwabl and Farner
(1989) found no inhibitory effect of T
implants on migratory restlessness of male
Gambel's white-crowned sparrows held in
cages outdoors in Seattle, Washington. In
fact, T implants actually delayed onset of
prebasic molt and development of photorefractoriness, thereby indirectly prolonging
the period of migratory restlessness compared with controls. Even when T-im-
265
planted males were exposed to estrogenimplanted females there was no reduction
in Zugunruhe (Schwabl and Farner, 1989).
So at least under captive conditions a combination of receptive females and elevated
T does not inhibit continued migratory
activity. More studies are necessary to evaluate the potential influence of these variables on migratory activity in free-living
birds.
2. Corticosterone as promoter of persistent
migratory activity.— Corticosterone (B) has
many metabolic and homeostatic effects,
and it has been shown to regulate a variety
of behaviors in diverse taxa (Chester-Jones
et al, 1972; Astheimer et al, 1992). One
hypothesis predicts that elevated levels of
B may promote migratory activity, thereby
preventing settlement on a breeding territory. Dolnik and Blyumental (1967) found
that injections of cortisol (another glucocorticosteroid with effects expected to be
similar to B) induced marked increases in
migratory activity as well as fattening in
chaffinches {Fringilla coelebs). Furthermore, practically elevated circulating corticosterone can inhibit reproductive activities {e.g., parental care, territoriality) without compromising reproductive competence
{e.g., Wingfield and Silverin, 1986). Activity in captive Gambel's white-crowned
sparrows is promoted by B implants if combined with brief deprivation of food
(Astheimer et al., 1992). Together, these two
effects suggest that continued elevation of B
near the end of migration could promote
continued migratory activity {i.e., searching
over a large area for a suitable breeding location) while inhibiting initiation of reproductive behaviors, but permitting completion of reproductive development in
preparation for imminent onset of nesting.
Data regarding the relation between naturally-occurring B levels and migratory state
remain somewhat equivocal. Peczely (1976)
found that in vitro adrenal gland B production of a variety of migratory birds was
highest during the migratory period and relatively reduced during the breeding period.
In free-living male Gambel's white-crowned
sparrows, circulating B levels increase during spring migration (Wingfield and Farner,
1978). However, no such increase occurs in
266
T. P. HAHN ET AL.
drop when birds detect a cue indicative of
a good breeding location. We have some
experimental data pertinent to this issue in
a spatially opportunistic temperate zone
species, the red crossbill (Loxia curvirostra).
These birds normally wander nomadically
in late spring and early summer until they
discover an abundance of developing conico 15
fer cones, their preferred food source {e.g.,
CO
Newton, 1973), and they then settle and initiate reproduction (Benkman, 1987a, 1990;
Coombs-Hahn, 1993). Circulating B levels
of crossbills housed in outdoor aviaries in
Seattle, Washington, increased in both sexes
between mid-May and early July (Fig. 4),
16 MAY
7 JULY
when free-living crossbills normally make
an annual wandering migration in search of
cones (Newton, 1973; Benkman, 1987a).
This is consistent with the hypothesis that
elevated B levels are associated with the
migratory period. However, contrary to our
hypothesis, provisioning of half of the birds
with abundant western hemlock (Tsuga heterophylla) cones did not result in reduced B
% 20
levels (Fig. 4; comparison between cone and
no-cone treatments on 7 July, males: F =
CD
15
0.009, P = 0.927; females: F = 0.002, P =
co
0.963). These data do not support the
I 10
hypothesis that exposure to a stimulus
a
indicative of a favorable nesting location (in
this case, appearance of abundant cones)
precipitates settlement and onset of breeding through a decline in circulating B levels.
16 MAY
7 JULY
Blood samples were collected after only two
FIG. 4. Plasma corticosterone (B) levels in male (A) days of exposure to cones, so it is possible
and female (B) red crossbills held in outdoor aviaries that the birds must experience abundant
and, beginning on 5 July, either provided with fresh
green western hemlock cones on fresh hemlock branches cones for a longer period of time before
(dark bars), or with fresh branches without cones (open endocrine and behavioral effects are
bars). Means and standard errors are plotted. Sample observed. However, Benkman (personal
sizes are 5 to 7 in all cases. Repeated measures ANOVA communication) has noted that whiterevealed no significant treatment effects (cones vs. no
cones) in either sex (both F < 0.4, both P > 0.5), but winged crossbills can initiate nesting in early
a significant date effect in both sexes (both F > 14.0, summer within a few days of arrival in an
both P < 0.005). Post-hoc pairwise comparisons (uni- area with abundant cones. Clearly, addivariate F tests) reveal that all groups showed an increase tional work measuring activity levels and
in B between 16 May and 7 July (all F > 7.4, all P < breeding behaviors is necessary to deter0.03) except for females with cones (F = 3.924, P =
mine the extent to which B plays a role in
0.079).
settlement and onset of breeding in spatial
opportunists.
females, and circulating B levels do not
In summary, spatial opportunism is a
decline in settled breeding birds as compared with individuals still considered to be common strategy in arctic breeding birds.
on migration (Wingfield and Farner, 1978). It permits them to cope with spatial unpreA further prediction of this hypothesis is dictability of such factors as food and nest
that circulating B concentrations should site availability. Preparation of the reproMales
• cores
SPATIAL AND TEMPORAL OPPORTUNISM
ductive system for breeding, and initiation
of migratory activity, are both controlled by
initial predictive cues such as photoperiod
in arctic spatial opportunists; endocrine
mechanisms underlying this component of
the annual cycle need not differ from sitefaithful seasonal breeders. On the other
hand, the environmental cues, and endocrine responses to them, that stimulate settlement (termination of migration) and onset
of nesting in arctic spatial opportunists
require further study.
TEMPORAL OPPORTUNISM
Temporal unpredictability results when
conditions change erratically with respect to
time of year. Birds that can adjust the breeding schedule to changing conditions over a
wide portion of the year should be called
temporal opportunists. While spatial opportunism operates at the transition from
migration to nesting {i.e., gonadal development is already complete), temporal
opportunism may involve substantial alterations in the schedule of gonadal development in addition to onset of nesting. It is
unlikely that any arctic birds exhibit complete temporal flexibility of breeding (i.e.,
no seasonal constraints at all), due to the
extreme nature of the arctic winter. On the
continuum from rigid seasonality to extreme
temporal opportunism (see Coombs-Hahn,
1993), we know of only one arctic/sub-arctic species, the white-winged crossbill (Loxia
leucoptera), that lies near the opportunistic
extreme. Across the boreal forests of northern Canada and Alaska, these birds specialize on the seeds of black spruce (Picea
marina), white spruce {Picea glauca) and
larch (Larix sp., see Benkman, 1987a).
Large-scale spatial variation in seed production by these trees (e.g., Fowells, 1965)
requires that the birds wander widely in
search of good cone crops, and there is substantial uncertainty from year to year in
when/if they will discover sufficient seeds
to support nesting. Typically, they have been
assumed to be entirely opportunistic, capable of responding to an abundance of seeds
by initiating or maintaining breeding at any
time of year (e.g., Newton, 1973). Recent
studies (<?.£., Benkman, 1990, 1992) suggest
that white-winged crossbills seldom (if ever)
267
breed in mid to late autumn. Furthermore,
they molt and regress their reproductive
systems during autumn, even if food remains
abundant (Coombs-Hahn, 1993). Nevertheless, their potential breeding season is
very long, extending from January through
October (Benkman, 1992).
A number of features of their biology permit crossbills to nest successfully under the
short, cold days of winter at mid-high latitudes. Their highly specialized morphology
and behavior facilitate very rapid foraging
rates when conifer cones are mature, partly
open, and still contain numerous seeds
(Benkman, 1987a, b, 1989). Sufficient seeds
to support nesting can persist from maturation of cones in late summer through the
following spring in at least some years
(Benkman, 1990). In addition, like most
cardueline finches, male crossbills feed their
mates on the nest, thus permitting continuous incubation by females during extremely
cold weather (Newton, 1973). Young crossbills appear to be able to live on a diet consisting exclusively (or nearly so) of seeds,
and the slow growth rate of the nestlings
(see Newton, 1973) may in part be due to
this relatively low protein diet. Together,
these features give white-winged crossbills
a unique potential for temporal opportunism, even at the limit of their range around
the Arctic Circle.
Reproductive patterns in central
Alaska in 1992-93
Large numbers of white-winged crossbills
arrived in central Alaska in the early summer of 1992 when large cone crops were
developing on both white and black spruce.
We observed numerous crossbills engaged
in breeding song and display flights near the
northern limit of the spruce forest around
Coldfoot, Alaska (67°N, 150°W) at the
beginning of July (they had been entirely
absent from this area when we visited in
mid-May). Breeding occurred in summer
(July and August) in the vicinity of Fairbanks, Alaska (65°N, 147°W), judging by
behavior of adults and appearance of
recently fledged young during late summer
and early autumn. No evidence of autumn
nesting was noted around Fairbanks, despite
the fact that crossbills and seed-filled cones
268
T. P. HAHN£T^i.
Male white-winged crossbills
MAR
APR
MAY
JUN
Female white-winged crossbills
MAR
APR
MAY
JUN
FIG. 5. Pattern of plasma luteinizing hormone (LH)
between March and June, 1993, in male (A) and female
(B) white-winged crossbills caught in Fairbanks, Alaska.
Means and standard errors are plotted. There were no
significant differences between sexes (2-way ANOVA,
P = 0.17), but there was a significant effect of month
(P = 0.035). The only significant pairwise difference
between months occurred between April and June
(Tukey test, P < 0.05). Sample sizes are as follows:
females, March (2), April (5), May (7), June (7); males,
March (8), April (8), May (7), June (6).
remained abundant. The single adult male
captured during November, 1992, was in
advanced prebasic molt, and had regressed
gonads (diameter of left testis 2.5 mm, by
laparotomy). These observations are consistent with the interpretation that an
autumn hiatus in reproduction occurs in
these birds (see Benkman, 1992; CoombsHahn, 1993).
In the vicinity of Fairbanks, crossbills
began showing signs of reproductive activity (singing, fragmenting of flocks) during
winter (February/March). Circulating levels
of luteinizing hormone (LH) in birds caught
beginning in March were already elevated
(Fig. 5), suggesting that they may already
have been breeding then. New fledglings
began to appear in early April. Allowing for
a 22 day nestling period and 13 days of
incubation (see Benkman, 1992), adults
must have been reproductively competent
by late February, consistent with our LH
data (Fig. 5). Reproductive development
(i.e., increasing gonadotropin levels and
maturation of the gonads after autumn
regression) must have been underway no
later than early February, an extremely early
date for small passerine birds around Fairbanks.
LH levels declined significantly in both
sexes between April and June (Fig. 5). Other
avian species in the area were only just
beginning nesting (many migrants had only
recently arrived) when white-winged crossbills were terminating reproduction. At this
time white-winged crossbills normally
embark on their annual migration in search
of new developing cones (Benkman, 1987a,
1992). If this search is successful, breeding
could resume later in summer (probably a
common event in both white-winged and
red crossbills, see Benkman, 1987a, 1992;
Coombs-Hahn, 1993).
Environmental cues and endocrine
mechanisms of temporal opportunism in the
white-winged crossbill
Temporal opportunists in general are
usually thought to remain physiologically
ready or nearly ready to breed at all times
(FarnerandServenty, 1960;Serventy, 1971),
initiating nesting rapidly whenever conditions become favorable. Food supply has
long been presumed to be the environmental factor regulating timing of crossbill
breeding (see Newton, 1973; Benkman,
1990). We did not collect data on patterns
of spruce seed abundance around Fairbanks. However our data on white-winged
crossbills are consistent with the general
pattern that is emerging from a variety of
studies. Benkman (1990, 1992) indicates
that white-winged crossbills, like the closely
269
SPATIAL AND TEMPORAL OPPORTUNISM
related red crossbills (Loxia curvirostra, see
Coombs-Hahn, 1993), do not breed during
mid- to late-autumn (November, December). We suggest that this is probably due
to a photorefractory period, since gonadal
regression and onset of molt occurs even
before seed abundance declines, at least in
temperate zone Engelmann spruce (Picea
engelmannii) forests (Coombs-Hahn, 1993).
They are, however, able to breed in response
to abundant conifer seeds throughout the
rest of the year (January through October,
Benkman, 1990, 1992). At lower latitudes,
egg-laying can resume by the beginning of
January if seeds are abundant (see Benkman, 1990, 1992). Our data from Fairbanks
indicate that recrudescence must have been
underway by some time during February
(see above) consistent with the hypothesis
that abundant food (seeds of white and/or
black spruce) may have been the stimulus
for reproductive development following
dissipation of (presumed) refractoriness.
Abundant food alone is probably not a
sufficient cue to bring white-winged crossbills into breeding condition in winter. Male
red crossbills held on natural photoperiod
in the absence of females do not show complete reproductive development in winter
even if food is provided ad libitum (Hahn,
in press). Furthermore, male red crossbills
held in outdoor flight cages with ad libitum
food display increased LH secretion (Fig.
6b) and rapid growth of the gonads (Fig. 6a)
in January only if they are housed with
mates. The males in the single sex group
had smaller gonads and lower LH levels even
though they could see females interacting
with mates in adjacent aviaries.
Thus, it appears that opportunism in
crossbills is tempered by a seasonal reproductive hiatus in autumn, perhaps due to a
photorefractory period. Winter reproductive development can occur after the refractory period is over when food is abundant,
but may require behavioral interactions in
addition to abundant food for maximum
development. Crossbills do not maintain
tonically high gonadotropin secretion, as
proposed by Farner and Serventy (I960) for
other temporal opportunists. Rather,
opportunistic reproductive development in
winter appears to be regulated by an increase
s
D6CB*B1
JANUARY
FfflRUAHY
C
<
0-
DATE
FIG. 6. (A) Gonadal development between midDecember and late January/early February in male red
crossbills held in outdoor aviaries as single male-female
pairs (open circles) or an all male group (opaque circles). Means and standard errors are plotted. Repeated
measures ANOVA showed a significant main effect of
laparotomy date (F = 94.591, P < 0.0001), due to
growth of gonads in both treatments between first and
second laparotomies (pairs, n = 4, F = 57.834, P <
0.0001; group, n = 9, F = 37.529, P < 0.0001). There
was no main effect of treatment (groups vs. pairs, F 1.324, P > 0.274), but a significant interaction between
treatment and laparotomy date (F = 8.582, P = 0.014)
indicating that gonads grew more rapidly in the paired
than in the grouped males. (B) Changes in plasma LH
levels between mid-December and late January in male
red crossbills held in outdoor aviaries as single malefemale pairs (dark bars) or an all male group (open
bars). Means and standard errors are plotted. LH levels
increased significantly in the paired birds (n = 4, F —
16.975, P = 0.02), but not in the grouped birds (n 9, F = 0.007, P = 0.934), and were significantly greater
in the paired birds than the grouped birds on 29 Jar.uary (F = 13.598, P = 0.004) but not on 8 December
(F = 0.129, P = 0.727).
270
T. P. HAHN ETAL.
in gonadotropin levels (e.g., LH), just as is
spring reproductive development in seasonal breeders.
CONCLUSIONS
We have described two important phenomena in the Arctic, spatial and temporal
opportunism. The two phenomena often
operate at different points in the annual
cycle—i.e., temporal opportunism can
involve either timing of onset of nesting in
individuals that are already reproductively
competent, or flexibly timed gonadal recrudescence, or both. In contrast, spatial
opportunism (at least in the absence of temporal opportunism) involves only the onset
of nesting when birds make the transition
from migration to settlement and breeding.
A wide variety of endocrine processes could
be involved in these phenomena, and we
discuss only a few possibilities.
We have pieced together data on spatial
opportunism from disparate sources and
species, and a concentrated study of the cues
and endocrine mechanisms involved in a
single species with strong spatial opportunism, such as the brambling, could resolve
many of the questions we have raised. The
specific cues to which the birds are sensitive
must be clearly established. These could be
food itself, behavioral interactions with
conspecifics, specific characteristics of the
habitat (e.g., nesting sites), or most likely
an integrated response to these and perhaps
other cues. It would then be useful to document the endocrine correlates of the transition from migration to settlement and
breeding in the wild, including changes in
gonadotropins, sex steroids, adrenal steroids, and perhaps metabolic hormones such
as thyroid hormones, insulin, and glucagon.
Experimental studies should seek to determine if a causal relation exists between
changes in these hormones and transitions
from migratory to breeding behavior, and
should consider the possibility that no
humoral signal may be involved at all, but
only changes mediated within the brain
itself. In the long run it would be particularly
useful to determine what time windows,
presumably dictated by initial predictive
cues, exist for the expression of spatial
opportunism, and how the passage of time
through the potential breeding season influences the tendency of individuals to settle
for less than optimal conditions to cease
migration and attempt to nest. This tendency may differ among long-lived spatial
opportunists, such as snowy owls or some
shorebirds, and very short-lived ones such
as bramblings.
Future research on the cues and mechanisms underlying temporal opportunism in
the Arctic should concentrate on the basis
of the autumnal hiatus in breeding and on
the flexible resumption of breeding in winter. Do crossbills possess a photoperiodically regulated refractory period, expressed
at the hypothalamic level, that prevents
them from responding to all manner of cues,
as is the case in many temperate-zone passerines (see Ball, 1993)? Evidence from red
crossbills suggests that this may be the case
(Hahn, in press). We are currently conducting experiments with white-winged
crossbills to determine whether hypothalamic changes in gonadotropin-releasing
hormone (the neuropeptide that regulates
production and secretion of pituitary
gonadotropins) between summer (breeding), autumn (non-breeding), and winter
(potentially breeding) mirror those seen in
seasonal species such as starlings, as they
change from photostimulated to photorefractory to photosensitive (e.g., Foster et ai,
1987). These studies will provide a basis for
further investigation of the specific combinations of cues regulating flexibly timed
reproductive development in winter, and the
underlying neuroendocrine mechanisms.
We emphasize, finally, that the objective
of this contribution to the symposium has
not been to establish definitively the endocrine bases of spatial and temporal opportunism in birds of the Arctic, but rather to
stimulate interest in, and provide a basis
for, their further study. We believe that
understanding these processes in arcticbreeding birds will have important implications for mechanisms regulating reproductive flexibility in general.
ACKNOWLEDGMENTS
Many of the investigations reported above
were supported by grant numbers DPP8901228, DPP-9023834, and DPP-9300771
SPATIAL AND TEMPORAL OPPORTUNISM
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