The Auk 113(3):558-564, 1996
MODULATION
OF THE
NEOTROPICAL
ADRENOCORTICAL
MIGRANTS
DURING
STRESS RESPONSE AUTUMN
IN
MIGRATION
REBECCAL. HOLBERTON, TMJEFFREY D. PARRISH,2 AND JOHN C. WINGFIELD3 •Departmentof Biology,Universityof Mississippi, University,Mississippi 38677,USA; 2Department of EcologyandEvolutionary Biology,BrownUniversity, Providence,Rhode Island 02912, USA; and
3Department of Zoology,NJ-15, Universityof Washington, Seattle,Washington 98195, USA
ABSTRACT.--$easonal changes in corticosteronemetabolism have been implicated in the migratory physiologyof passerines.To investigatehow this hormonemight relate to migratory conditionin free-living birds,we comparedplasmalevelsof corticosterone in response to captureand handling stressin premigratoryand migrating Gray Catbirds (Dumetellacarolinensis). Lean, premigratorycatbirdsexhibitedstressresponses typicalof other nonlipogenic, nonhyperphagicbird speciessampledon the breeding or wintering grounds(i.e. low levels of corticosteroneat capture followed by significantincreasesover I h). In contrast,fat, migratory catbirdssampled later in the seasonshowed significantly higher baseline levels of corticosteroneat capture and no significant increasein hormone levels with handling time. We also sampled a group of migrating Yellow-rumped Warblers (Dendroicacoronata)at a stopoversite. Like catbirds,migrating warblers exhibited an absenceof a stressresponse, with no significantchangein corticosterone levelswith captureand handling stress.Unlike birds sampledon the breeding grounds,there was no relationship between corticosterone levelsat captureand fat scoresin premigratoryand migratorycatbirds,or in the migratory warblers.These resultssupportour Migration-ModulationHypothesisregardingseasonal changesin corticosteronelevels,viz.: (1) an absenceof a relationshipbetween fat deposition and baselinecorticosteronelevels illustratesthe permissivenature of the hormone, which remainselevatedthroughoutthe migratoryperiodto facilitatehyperphagiaand lipogenesis independent of short-termchangesin energeticcondition;and (2) further elevation of corticosteronein responseto acute stressis suppressedduring migration to protect skeletal muscleneededfor flight. Received 25 April 1995,accepted 14 July 1995.
RECENT RESEARCH on Neotropicalmigrantshas focusedon habitat selection,foraging ecology, and conservationissuesrelated to stopoversites, with lessemphasison physiologicaladaptations associatedwith their migration (e.g. Loria and Moore
1990, Martin
and Karr 1990, Kuenzi
et
Phillips 1976). It is released rapidly into the bloodstreamin responseto a variety of stressors (Holmesand Phillips 1976,Siegel 1980,Harvey et al. 1984). A rise in corticosterone in the blood-
stream promotes gluconeogenesisto increase glucosesubstrates,often at the expenseof muscle tissue(Holmes and Phillips 1976).Theseen-
al. 1991,Haganand Johnston1992).Indeed, recent studies on the physiology of passerines ergy substrateshelp an individual meet addiduring migrationhave focusedprimarily on Old tional energeticdemandsthat occurduring peWorld species(Schwablet al. 1991,Bairlein and riodsof extremestresssuchasstorms,attackby Totzke 1992, Gwinner et al. 1992, Jenni and predators,or foodshortage(Wingfieldet al. 1983, Jenni-Eiermann 1992). Like Old World miHarvey et al. 1984,Cherel et al. 1988,Smith et grants, many Neotropical migrants interrupt al. 1994,Wingfield 1994). An individual's responsivenessto a stressor their autumn journey to the wintering grounds to rest and refuel.
As food and weather
become
(i.e. amount and rate of corticosterone release
lesspredictable,migrants may faceenergy and time constraintsin their ability to replenish fat reservesquickly and efficiently. Corticosteroneis the primary glucocorticoid and hormone of stress in birds (Holmes and
E-mail:
[email protected] 558
from adrenal tissue) can be measuredby repeatedbloodsamplingfor a period of time after captureand handling, activitiesassumedto be stressfulto free-living birds (e.g. Wingfield et al. 1992).The protocolof repeatedsamplingafter capturehas becomethe acceptedparadigm for measuringthe sensitivityof an individual's
July1996]
Corticosterone Response DuringMigration
hormonal responseto stress.In general, birds sampledduring benign weather conditionson the breeding or wintering grounds exhibit a stressresponseto captureand handling characterized by low baseline levels at the time of capture followed by a significantincreasein corticosterone over a 30- to 60-min period (Wingfield et al. 1992;Holberton and Wingfield 1994;Smith et al. 1994; Wingfield et al. 1994a,
predictedthat:(1) birdsin migratorycondition would exhibithigherlevelsof the hormonethan
thosein premigratorycondition,and (2) actively migratingbirdswouldsuppress the stress responseby showingno significantincreasein the hormonefollowing capture(which presumably involvesstress). STUDY SITE AND METHODS
b; Holberton et al. 1996). An increase in for-
aging activity (i.e. hyperphagia and searching for food) and lipogenesisare among the shortterm effectsof higher levels of corticosterone (Wingfield and Silverin 1986, Berdanier 1989, Gray et al. 1990,Astheimer et al. 1992).Among its chronic or long-term effectsis catabolicactivity on skeletal muscle as a glucose/energy source,often a last resortif adequatefood does not becomeavailable(Holmesand Phillips 1976, Siegel 1980,Wingfield and Silverin 1986,Chefel et al. 1988,Gray et al. 1990). The associationsamong corticosterone,hyperphagia,and lipogenesisare highly relevant to bird migrationphysiology.Indeed, the latter two characteristicsare used to define migratory condition in captive birds. In spite of the potential benefit of a typical corticosteronestress response, however,activelymigratingbirdsmay be faced with
a conflict
between
the hormone's
lipogenic activity and its catabolic action on muscle. If migrating birds maintain elevated corticosteronelevels to facilitate foraging and lipogenesis,they may, unlike non-lipogenic birds, suppressadditional increasesin the hormone (e.g. in responseto stress)to protectmuscle needed for long-distance flight. Several studies
have
shown
that corticosterone
secre-
tion in responseto handling stresscan be suppressed,but these data come from studiesof amphibians(Paolucciet al. 1990),reptiles(Bradshaw 1975), and birds (Wingfield et al. 1983, Wingfield et al. 1992,Holberton and Wingfield unpubl.data)during the breedingseason,when hormonelevels typically are low already. We investigatedthe seasonalnature of corticosteronesecretionin two speciesof free-living Neotropicalmigrants,the Gray Catbird (Dumetella carolinensis)and the Yellow-rumped Warbler (Dendroica coronata), at an autumn stopover site in coastalNew England. We testedtwo hypotheses,collectivelyreferred to as the Migration-Modulation Hypothesis. Given corticosterone'seffect on lipogenesis and hyperphagia and its catabolicactivity on muscle,we
559
Studysite.--In autumn1993we collectedbloodfrom Gray Catbirdsand Yellow-rumpedWarblerson Block Island (41øN, 71øE),which is a 2,900-ha landmass located 19 km south of the coast of Rhode
Island.
Birds
were capturedon ClayheadPreserveat the northern tip of the island, where many migrants congregate (Able 1977). The habitat where birds were netted con-
sistedprimarily of early successionalcoastalshrubland dominated by northern arrowwood (Viburnum recognitum),black chokeberry (Pyrus melanocarpa), northern bayberry (Myrica pennsylvanica), shadbush (Amelanchier spp.), and poisonivy (Rhusradicans). Bird capture,plasmacollection,and weather.--Birds were capturedin mist nets throughoutthe daylight hours. From a vantage point away from the nets,we recordedthe exacttime when eachbird was captured. Immediatelyafter capture,birdswere extractedfrom the net and a blood sampletaken by puncturing the wing vein with a 27-gaugeneedle.The time of completion of the first blood sample was recorded for each bird. All samplesincluded in this study were obtained within 2 min of capture, which represents ascloselyaspossiblethe pre-disturbancelevel of hormone and is referred to as baseline (i.e. time = 0) in
our analyses.To completethe stressseriesfor each individual,the time of eachsubsequent samplingwas based on the time of capture for that individual. Smallermigrants(all warblers)were bled at 5, 20, and 60 min after capture,whereas larger migrants (all catbirds)were bled at 5, 10, 30, and 60 min after capture. At each sampling time we collected50 to 100 •L of blood in a heparinized capillary tube. This proceduretook lessthan one minute. Bloodsampleswere kept on ice in a small cooleruntil centrifuged 2 to 4 h later. Plasmawas then recovered from each sample with a 50-•L Hamilton syringe and kept frozen in microcentrifugetubesuntil assayedfor corticosterone by radioimmunoassay asdescribedin Wingfield et al. (1992).
Birdswere kept individually in small cloth bags betweensamplingtimes.After eachstressserieswas completed, birds were banded with a U.S. Fish and Wildlife Service aluminum band and processedfor body mass(+ 0.1 g), fat score(scale0-5; see Helms and Drury 1960),and presenceof molt. Although the sexof the warblerscouldbe determinedby plumage and wing measurements, and hormone levels may differ betweenthe sexes(Wingfield 1994),we pooled
560
HOLBERTON, PARRISH, ANDWINGFIELD
[Auk,Vol. 113
90-
8
o
60-
=* 50-
• 40-
_o 30-
0
0.5
I
I!11
2 2.5 3 3.5 4 fat score
FIG. 1. Fat scoresof premigratory (hatched bars) and migratory (solid bars)Gray Catbirdscapturedat
;20-
•
10-
•
0
FIG.2.
•
10
20
30
40
50
60
time after capture (min) Plasmacorticosteroneconcentration (mean
+ SE)asa function of handling time after capturefor premigratory (open circles;n = 16) and migratory (solid circles;n = 6) Gray Catbirds sampled for the stress response in autumn.
Block Island, Rhode Island, autumn 1993.
the sexesbecauseof small sample sizes. To reduce measurementerror, all fat scoreswere taken by the sametwo people throughout the study. We assigned half-values(e.g. 0.5, 1.5, 2.5) to birds that could not be placedinto fat classesunambiguously.Because corticosteronelevels can be affected by weather conditions (Wingfield et al. 1983, Smith et al. 1994), we obtained local data on precipitation, dry air temperature (_+ IøC), and wind speed and direction. Data were compiledon the day before and the day of sampling to look for possibleeffectson hormone levels.
RESULTS
for only 14 of the 22 catbirdsowing to problems with clotting or too little plasma for reliable analyses.Therefore, in lieu of a repeatedmeasures ANOVA,
we used a two-factor ANOVA
(with log [X + 1] transformation) to compare corticosteronelevels relative to capture and handling stressbetween the two groups of catbirds (see Keppel [1982] and Zar [1984]). Migratorystatusexplaineda significantamount of variation in corticosterone release in catbirds (F
= 9.28, df = 1 and 84, P = 0.003;Fig. 2). There alsowas a significantoverall effectof sampling time after captureon plasmacorticosteronelevels (F = 4.41, df = 4 and 84, P = 0.003) for all
tured in early autumn (24-25 September),15 were undergoingheavymolt. As a group,these birds were lean, with 50% of them having no
catbirds. The pattern of hormone release did not differ between the two groups,becausethe interaction between migratory statusand hormone levels at sampling time after capture was not significant (F = 1.55, df = 4 and 84, P =
visible fat (median fat score = 0.25, range 0 to
0.194).
3; Fig. 1). Basedon molt and the absenceof fat deposition,we classifiedthese individuals as premigratory.Five of six catbirdscapturedtwo weekslater (10-17 October)had completedmolt. These birds had significantly greater fat reservesthan those captured during the earlier samplingperiod (median fat score= 2.75,range 0 to 4; Mann-Whitney U-test, P < 0.05), with four of them having fat scoresof 2.5 or higher (Fig. 1). We consideredthis latter group to be in migratory condition. No catbirdscaptured during the premigratorysamplingperiodwere recapturedduring the migratorysamplingpe-
Differencesbetweencatbirdsin premigratory and migratory condition were evident in corticosterone levels at the time of capture. Catbirds in migratory condition had higher levels of corticosteroneat the time of capture (• = 56.16 _+SE of 14.26ng/ml) than did premigratory catbirdssampledearlier in the season(• = 25.02 _+ 4.74 ng/ml; Mann-Whitney U-test, P < 0.05; Fig. 2). In addition, premigratory catbirds showed a significant increasein hormone levels between capture (t = 25.02 + 4.74 ng/ ml) and 30 min after capture (t = 55.33 + 3.98 ng/ml; paired t-test, P = 0.0001;Fig. 2). In migratorycatbirds,there was no differencein corticosteronelevels at capture (œ= 56.16 _+14.26
Gray Catbirds.--Catbirds are summer residents on Block Island. Of the 16 catbirds cap-
riod.
We were able to obtain complete stressseries
July1996]
Corticosterone Response DuringMigration
125'
561
4
-.-- 100o
ß
75-
o 0
e o
50-
ß
0
0
0
o
0
0
250
Plasma corticosterone
1.5 fat score
2
2.5
land, Rhode Island, autumn 1993.
stressresponsein 12 Yellow-rumped Warblers capturedduring the later sampling period (10-
fat score FIG. 3.
I
FIC. 4. Fat scoresof 12 Yellow-rumped Warblers captured on stopover during migration at Block Is-
E 8
0.5
concentration
at the
17 October). Based on calendar date, we con-
time of capture as a function of fat scorein premigratory (open circles) and migratory (solid circles) Gray Catbirds.
sideredthesewarblersto be actively migrating through the site. Although Yellow-rumped Warblers do not deposit large amounts of fat during fall migration (Holberton pers.obs.),we
ng/ml) vs. 30 min after capture (œ= 70.78 + 11.75 ng/ml; paired t-test, P = 0.267; Fig. 2).
detected
We found
no evidence
that weather
account-
ed for the abovedifferences.During the earlier sampling period (24-25 September), nighttime temperaturesreached a low of 10øC,and daytime temperaturesranged from 18-21øC.Winds were light throughout the period. During the later sampling period (10-17 October), daytime temperatures were similar to those recorded
earlier, ranging from 12-21øC,and winds again were light. Nighttime temperatures fell to 710øCduring this period. No precipitation occurred during either sampling period. Neither group of catbirds showed a significant correlation
stored
fat in 75% of the individuals
captured (Fig. 4). Like catbirds in migratory condition,this group of warblersfailed to show a significantchangein corticosterone levelswith time after capture(F = 0.33, df = 3 and 42, P = 0.806;Fig. 5). Becausethere was little variation in hormone levels at the time of capture (see Fig. 5), there was no correlation between corticosteronelevels and fat scores(n = 9, Kendall's Z = -1.01, P = 0.312). DISCUSSION
The resultsfrom this preliminary study support both aspectsof the Migration-Modulation
between corticosterone level at Hypothesis. First, catbirds in migratory condithe time of captureand fat score(premigratory: tion had higher levels of corticosteroneat the n = 16, Kendall's Z = -0.54, P = 0.587; migra- time of capture than did catbirds that were actory: n = 6, Z = 1.32,P = 0.188;Fig. 3). However, tively molting and had little or no stored fat. Figure 3 illustratesthe trend between the lower This suggeststhat catbirdssampledlater in the hormone values measuredin the earlier group seasonhad increasedplasmacorticosteronelevof lean birds and the higher hormone values els concomitant with, or as a consequenceof, measured in the later, fatter birds (groups coming into migratory condition. Indeed, corpooled, n = 22, Z = 1.66, P = 0.097). ticosterone'spositive effect on behaviors such Yellow-rurnped Warblers.--Inthe absenceof a ashyperphagiaand searchingactivities,in concompleteseriesof samplesfor all individuals, junction with its lipogenic activities(Wingfield we used single-factorANOVA to look for the and Silverin 1986, Gray et al. 1990), would be
562
HOLBERTON, PARRISH, ANDWINGFIELD
ers et al. 1993, Smith et al. 1994), weather is not
60'
believed to have been a factor in the temporal difference
----- 50-
in hormone
levels
or the stress re-
sponsein our study. Weather conditions were mild and similar both before and during each sampling period. Therefore, differences in the patterns of hormone release between premi-
o
o
[Auk,Vol. 113
40-
gratoryand migratorycatbirdsprobablyreflect-
o
ß
ed an intrinsic changein migratory status.These results support an earlier model proposed by Meier and Farner(1964),where seasonalchanges in daily patternsof corticosterone,in conjunction with prolactin, could explain the onset and termination of migratorybehavior(but seeVleck
:30-
o o
1: o
20-
o
E
et al. 1980).
lOo
0
:3'0 4'o
time after capture (min) FIG. 5.
Plasmacorticosteroneconcentration (mean
+ SE)asa function of handling time after capturefor 12 Yellow-rumped Warblers sampled for the stress responseduring autumn migration.
beneficialto migrantsas they prepare to meet the increased energy demand of migratory flight. The secondaspectof the Migration-Modulation Hypothesisrefers to the apparent conflict that theseelevatedlevelsof hormonemay impose on migrants. Unlike the premigratory catbirds in this study (and other birds in non-
If corticosteronefacilitates fattening during migration, one might expect leaner birds (i.e. with a greater need to depositfat) to have higher baseline
levels
of the
hormone
than
fatter
birds that are ready to resume migration. Our resultsare equivocalfor migratory catbirdsregarding this point, perhaps becauseof small sample sizes. However, the Yellow-rumped Warblers
did not show the variation
corticosterone
levels
that would
in baseline
be needed
to
find such a relationship between fat reserves and corticosteronelevels. This suggeststhat elevated hormone levels, in conjunction with suppression of the stress response, are maintained throughout the migration period regardlessof short-term fluctuations in energetic condition (Schwabl et al. 1991; but see Ramen-
ofskyet al. 1995).Clearly,further studyis needmigratorycondition;Wingfieldet al. 1992,1994a, ed to discern the exact relationships between
b; Smith et al. 1994; Holberton and Wingfield corticosteronelevels and energetic condition unpubl. data), catbirdsin migratory condition during stopover. appearedto suppressthe typicalstressresponse. An important assumptionof our MigrationThesebirds failed to show a significantincrease Modulation Hypothesis is that our capture and beyondelevatedlevels at the time of capture handling paradigmwasstressfulenough to elicit and those measured 30 min later, a time when
maximal
most birds express maximal levels of corticosterone in this type of sampling paradigm
birds during the nonmigratory seasonrespond
(Wingfieldet al. 1992;Holbertonand Wingfield
that increaseforaging behavior and lipogenesis
amounts
to storms with
of corticosterone
elevated
release.
If
levels of corticosterone
1994;Smith et al. 1994;Wingfield et al. 1994a,b). (Wingfield et al. 1983, Wingfield and Silverin Moreover, although we were unable to obtain 1986, Gray et al. 1990, Astheimer et al. 1992), comparablesamplesfrom Yellow-rumped War- then how do migrants that apparently suppress biers before they came into migratory condi- this responserespond to such stressors?In an tion, they, too, failed to show a significant attemptto reachthe wintering groundsquickly change in corticosteronelevels with handling to compete for wintering sites (Alerstam and time, a pattern now known in many other spe- Lindstr•3m 1990, Holmes and Sherry 1992, ciesof passerinesduring migration (Holberton Stutchbury1994),migrantsmay alreadybe forand Moore unpubl. data). aging at their maximum potential during stopAlthough weather can influence plasma lev- overs, and additional corticosterone will have els of corticosterone(Wingfield et al. 1983,Rog- no further effect on behavior. It may only be
July1996]
Corticosterone Response DuringMigration
during periods of extreme stress(which were not present in our study) that fat reservesare exhausted and skeletal muscle mobilized,
at
which time migrantsmight exhibit dramaticincreasesin corticosterone levels (see Gwinner et al. 1992).
landbirds.
563
Smithsonian
Institution
Press, Wash-
ington, D.C. HARVEY, S., J. G. PHILLIPS,A. REES,AND T. R. HALL. 1984. Stressand adrenal function. Journal of Ex-
perimental Zoology 232:633-645. HELMS, C. W., AND W. H. DRURY. 1960. Winter and
migratory weight and fat: Field studieson some North Americanbuntings.Bird-Banding31:1-40. HOLBERTON,R. L., AND J. C. WINGFIELD. 1994. Ad-
ACKNOWLEDGMENTS
renocortical responsesto stressin Antarctic sea-
We thank Mrs. F. David Lapham and The Nature Conservancyfor the generoususe of their land, Megan Whitman and Scott Comings for assistancein the field, and Lynn Erckmanand Tim Boswell for assistance in the laboratory. Ellen Ketterson,Gary Miller, Ken Able, John Carlson, Chris Sims, and an anonymous
reviewer
read
earlier
versions
of the
manu-
script.
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