Moore et al. 2002

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Latitudinal variation in plasma testosterone levels in birds of

the genus Zonotrichia

Ignacio T. Moore,a,* Nicole Perfito,a Haruka Wada,b Todd S. Sperry,a

and John C. Wingfielda

a Department of Zoology, Box 351800, University of Washington, Seattle, WA 98195, USAb Section of Integrative Biology, Mail Code C0900, University of Texas, Austin, TX 78712, USA

Accepted 18 April 2002

Abstract

Birds breeding in northern latitudes generally have elevated plasma testosterone levels throughout the breeding season with a

peak at the onset of the breeding season. In contrast, tropical birds tend to have extremely low plasma testosterone levels year round

with only a slight increase during breeding. While these patterns have been consistent in the species investigated, closely related

species have not been investigated across a range of latitudes. Birds of the genus Zonotrichia present an ideal opportunity to in-

vestigate latitudinal variation in plasma testosterone levels as breeding populations occur from northern Alaska to southern Ar-

gentina. We studied three taxa of Zonotrichia: (1) Gambels white-crowned sparrows, Zonotrichia leucophrys gambelii, breeding at

high latitude in northern Alaska, (2) Puget Sound white-crowned sparrows, Z. l. pugetensis, breeding at mid-latitude in Washington

state, and (3) an equatorial population of the rufous-collared sparrow, Z. capensis, in Ecuador. To compare both baseline breeding

and maximal testosterone levels, males from the three taxa were either bled immediately upon capture during the breeding season or

first challenged with gonadotropin-releasing hormone (GnRH) and then bled. As a control, another group of birds experienced a

saline challenge. Two-way ANCOVA, with treatment and taxa as factors and testis volume as a covariate, showed a significant effect

of treatment on plasma testosterone levels. There was also a significant interaction between taxa and treatment. Contrary to ex-

pectations, the equatorial species exhibited greater plasma testosterone levels in response to the GnRH challenge than the high

latitude species. There were no differences between the mid- and high-latitude species. The equatorial species had the smallest

average testis size and within each taxa there were no relationships between plasma testosterone and testis size. These data suggest

that latitudinal clines in plasma testosterone levels in Zonotrichia do not follow previously described patterns and that tropical birds

can have levels of testosterone similar to northern latitude species.

2002 Elsevier Science (USA). All rights reserved.

Keywords: Testosterone; GnRH; Zonotrichia capensis; Zonotrichia leucophrys; Bird; Tropics; Arctic

1. Introduction

Studies of a wide variety of vertebrates have estab-

lished important roles for the sex steroid hormone tes-

tosterone in reproduction and territorial aggression

(Nelson, 1995; Wingfield and Kenagy, 1991). Field in-

vestigations have revealed complex seasonal patterns of

testosterone levels in free-living vertebrates, especially

birds (Wingfield et al., 1997) with patterns differing

dramatically even among closely related taxa (Wingfield

and Farner, 1978a,b, 1980). Some of the variationwithin birds appears to be associated with differences in

latitude of the breeding site (Wingfield et al., 1992,

1997). Species breeding in northern latitudes frequently

have shorter breeding seasons than lower latitude

breeding species (Wingfield et al., 1997) and corre-

sponding shorter periods of elevated testosterone.

However, northern latitude species also tend to have

testosterone peaks of greater magnitude associated with

socially unstable situations during territory establish-

ment (Hunt et al., 1995). These elevations in plasma

testosterone levels above baseline breeding levels

occur during the breeding season when the testes are

General and Comparative Endocrinology 129 (2002) 1319

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GENERAL AND COMPARATIVE

ENDOCRINOLOGY

* Corresponding author. Fax: 206-543-3041.

E-mail address: [email protected] (I.T. Moore).

0016-6480/02/$ - see front matter 2002 Elsevier Science (USA). All rights reserved.

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recrudesced and are consistent across species breeding

in the high arctic (Hunt et al., 1995).

Equatorial species of birds generally have extremely

low plasma steroid levels and/or low amplitude cycles

(Dittami, 1986, 1987; Dittami and Knauer, 1986;

Gwinner and Scheuerlein, 1999; Hau, 2001; Hau et al.,

2000; Levin and Wingfield, 1992; Lormee et al., 2000;Wikelski et al., 2000) with possible slight elevations in

plasma testosterone in males occurring during times ofbreeding (Wingfield et al., 1991). Testosterone levels are

generally maximal during periods of social instability,

such as after conspecific territorial challenge (Hau, 2001;

Wikelski et al., 1999b). While it is not clearly understood

why equatorial birds generally have low plasma testos-

terone levels, this trend is consistent across a variety of

new and old world equatorial species. A few investiga-

tors have proposed evolutionary explanations for low

testosterone in male tropical birds. For example, the

potential of greater exposure to parasites in the tropicsand the immunosuppressive effects of testosterone have

been advanced as a potential explanation for this ob-

servation (Folstad and Karter, 1992; Hillgarth et al.,

1997; Levin and Wingfield, 1992; Moller, 1998; Peters,

2000; Saino et al., 1995). Fewer extra-pair fertilizations

in tropical species has also been advanced to explain

lower plasma testosterone levels in tropical birds (Stut-

chbury and Morton, 2001). Few studies have investi-

gated the proximate causes for the observed differences

in plasma testosterone between tropical and temperate

zone bird species. Understanding the physiological

mechanisms underlying differences in plasma testoster-

one, such as differences in activity of the hypothalamic

pituitarygonadal (HPG) axis, can give further insightinto ultimate causes for observed differences.

We investigated the plasma testosterone response to

stimulation in three taxa of emberizine sparrows of the

genus Zonotrichia. These three taxa have different sea-

sonal patterns of territoriality and reproduction associ-

ated with their respective breeding latitudes. We tested

the hypothesis that there is a positive relationship be-

tween both basal and maximum plasma testosterone

levels and latitude of the breeding population. To test

this hypothesis we captured birds breeding at different

latitudes and obtained blood samples immediately orchallenged the captured birds with the same dose of

gonadotropin-releasing hormone (GnRH) and mea-

sured resulting plasma levels of testosterone.

2. Methods

2.1. Study animals

Gambels white-crowned sparrow, Zonotrichia leu-

cophrys gambelii, (GWCS) is a long distance migrant (as

much as 5000km) that overwinters in the southwestern

United States and northern Mexico and breeds in

Alaska during the brief summer period (Blanchard and

Erickson, 1949; Cortopassi and Mewaldt, 1965; King

et al., 1966). Maximum testosterone levels are associated

with territory establishment at the beginning of the

breeding season and levels remain elevated for as little as

one week (Hunt et al., 1995; Wingfield and Farner,1978a). However, males breeding at the northern limit

of the range do not show an increase in plasma levels oftestosterone in response to short-term territorial chal-

lenges (Meddle et al., 2002). We investigated this species

at the summer breeding grounds at the Toolik Field

Station, Alaska (68N latitude, 720 m elevation) and

during fall migration in central Washington (Sunnyside,

WA; 46N latitude, 235 m elevation).

The Puget Sound white-crowned sparrow, Zonotri-

chia leucophrys pugetensis, (PWCS) is a short distance

migrant that breeds west of the Cascade-Sierra Moun-

tain divide from southern British Columbia to northernCalifornia. Breeding occurs for an extended period

during the late spring and summer (Blanchard, 1941;

Cortopassi and Mewaldt, 1965). This species exhibits

social modulation of plasma testosterone levels with

plasma testosterone levels rising in response to short-

term territorial challenges (Wingfield and Hahn, 1994).

This species overwinters from southern Oregon to cen-

tral California. We investigated this species during the

early part of the breeding season at Pack Experimental

Forest in western Washington (47N latitude, 275 m

elevation).

The equatorial population of the rufous-collared

sparrow, Zonotrichia capensis, (RUFS) we studied is

non-migratory and breeds in the high Andes near Pa-pallacta, Ecuador (0210 S latitude, 3300 m elevation).

This species ranges from southern Mexico to southern

Argentina. Previous studies have described year-round

reproduction in a population in Columbia (Miller, 1961,

1962; Miller and Miller, 1968). We chose the Papallacta,

Ecuador population for its proximity to the equator and

the relative aseasonal nature of the environment at the

high elevation site near the equator. These birds appear

to be socially monogamous and pairs occupy the same

home ranges year round and defend them when breed-

ing. In addition, these birds have extended breedingseasons but a synchronized pre-basic molt. However,

they do not appear to respond to short-term territorial

challenges with an increase in plasma testosterone (I.T.

Moore, in review).

2.2. GnRH challenge

Birds were challenged with GnRH to measure the

absolute responsiveness of the HPG axis in terms of

plasma levels of testosterone (Levin and Wingfield,

1992; Wingfield and Farner, 1993; Wingfield et al.,

1991). Male birds from the three species were challenged

14 I.T. Moore et al. / General and Comparative Endocrinology 129 (2002) 1319

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with the major gonadotropin-releasing hormone

(GnRH) in passerine birds, chicken-1 (Glu 8) luteinizing

hormone releasing hormone (Sherwood et al., 1988).

Birds were captured in mist-nets, either passively or at-

tracted with short bouts (10 min or less) of prerecorded

playback of conspecific song. Previous studies have

found no effect of less than 10 min of conspecific songplayback on plasma testosterone levels in birds (Wing-

field and Wada, 1989) and we saw no difference betweenbirds captured by the two methods. Upon capture in-

dividuals were randomly assigned to a treatment group.

Experimental animals (hereafter referred to as the

GnRH group) were challenged with a jugular injection

of 500 ng of chicken-1 GnRH (Sigma L0637) dissolved

in 10lL of lactated saline. This dose of GnRH elicits a

rapid and maximal activation of the HPG axis (Wing-

field and Farner, 1993). To control for the experimental

manipulation a second group received a 10lL jugular

injection of lactated saline alone (hereafter referred to asthe saline group). Birds from these two groups were bled

30 min after treatment. A third group of birds received

no treatment or injection and were bled within 10 min of

capture (hereafter referred to as the control group). This

group was therefore indicative of baseline hormone

levels. All blood samples were obtained by puncturing

the alar wing vein and collecting the blood in heparin-

ized micro-capillary tubes. During the period between

capture and blood sampling, birds were isolated in small

cloth bags. After blood sampling, laparotomies were

performed to measure the length and width of the left

testis. Testis volume was calculated using a formula for

ellipsoid cylinders (4=3pa2b, where a is half the testiswidth and b is half the length).

GWCS were sampled during the early breeding sea-

son (June 517, 2000) at Toolik Field Station, Alaska.

The fall sampling period consisted of birds captured

during fall migration (SeptemberOctober, 2000) in

eastern Washington and held in outdoor aviaries at the

University of Washington for a period of approximately

one month before sampling (October 31November 3,

2000). GWCS are known to acclimate to captive con-

ditions during this period (Wingfield et al., 1982). All

these individuals were adults, judging from plumage,

and should have been photosensitive at that time(Wingfield and Farner, 1978a). During both sampling

periods, birds were randomly divided into the three

groups (N 8 each): (1) control, (2) saline, and (3)GnRH. PWCS were captured during the early breeding

season (May 218, 2000) from Pack Experimental For-

est in western Washington and randomly assigned to

one of the three treatment groups: (1) control (N 8),(2) saline (N 8), and (3) GnRH (N 9). RUFS weresampled from August 18September 13, 2000 near Pa-

pallacta, Ecuador and randomly assigned to one of

the three treatment groups: (1) control (N 34), (2)

saline (N 8), and (3) GnRH (N 12). This period is

equivalent to pre-breeding in northern latitude species

and no individuals were in molt.

Blood samples were stored on ice until return from

the field each day when the plasma was separated and

frozen until the hormone assays were completed. All

blood samples were analyzed in duplicate by radioim-

munoassay following the procedures of Wingfield et al.(1991). Limits of detection for the assay were 0.06

0.19 ng/mL depending on the volume of the plasmasample (range 17555lL). The samples were run in four

assays with intraassay and interassay variations of 10%

and 15%, respectively. Samples from GWCS and PWCS

were analyzed in a direct assay, with no chromatogra-

phy, and thus measured total androgen. RUFS samples

were assayed after short column chromatography and

measured testosterone alone.

2.3. Statistics

Differences in plasma testosterone levels were ana-

lyzed in a two-way ANCOVA with species and treat-

ment as factors and testis volume as a covariate. We

excluded the fall GWCS samples from the model be-

cause non-breeding season samples were only collected

for that species. However, they do provide a useful

comparison as a non-breeding group. Testosterone lev-

els were not normally distributed and were log10 trans-

formed prior to analysis. Homogeneity of slopes was

confirmed to proceed with the ANCOVA. Post hoc

analysis was done using Fishers LSD. Statistical

analyses were done using Systat 9.0 and Statview 5.0.

Differences in plasma testosterone levels within the

fall GWCS samples were analyzed by ANOVA. Todetermine if plasma testosterone levels were related to

reproductive condition, the relationships between testis

volume and plasma testosterone levels were analyzed by

linear regression analysis. Differences in testis volume

between treatment groups within species were analyzed

by ANOVA.

3. Results

After accounting for species, there was a significanteffect of treatment on plasma testosterone levels (Fig. 1;

F2;91 16:18; P < 0:001). The plasma testosterone levelsin the GnRH group were significantly higher than in the

control P < 0:001 or saline groups (P < 0:001) and thecontrol group was higher than the saline group

(P 0:015). There was no effect of testis volume (Fig. 2;F1;91 1:65; P 0:20). After accounting for treatmenteffects, species does not explain a significant amount of the

variationthat is left (F2;91 0:24; P 0:79)but there wasa significant interaction between species and treatment

(F4;91 4:05; P 0:005). Post hoc analysis showed

the following differences within each species. The

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RUFS-GnRH group had significantly higher plasma

testosterone than the RUFS-control P < 0:001 andRUFS-saline P < 0:001 groups. The PWCS-GnRHgroup had significantly higher plasma testosterone than

the PWCS-saline group P < 0:001and the PWCS-salinegroup had significantly lower plasma testosterone levels

than the PWCS-control group P < 0:001. There wereno significant differences between the GWCS treatment

groups P > 0:05. For the between species analysis we

report the differences between similar treatment groups.

The RUFS-GnRH group had significantly higher plasma

testosterone levels than the GWCS-GnRH group

(P 0:02) but was not different from PWCS-GnRH(P 0:24). There were no differences in plasma testos-terone between the control groups P > 0:05. ThePWCS-saline group had significantly lower testosterone

levels than the GWCS-saline group (P 0:03) but notdifferent from the RUFS-saline group (P 0:15).

Within the spring GWCS samples, there were no sig-

nificant relationships between plasma androgen levels

and testis volume within the GnRH group (linear re-

gression, r2 0:275; P 0:18), saline injected (linearregression, r2 0:13; P 0:38) or control birds (linearregression, r2 0:001; P 0:95). During this samplingperiod all birds had maximally recrudesced testes so there

were no differences in testis volume between the treatment

groups (F4;34 1:16; P 0:33). During the fall, therewas no difference in plasma androgen levels between the

treatment groups (Fig. 1, F2;21 1:85; P 0:18) or intestis volume between the treatment groups (F2;21 1:38; P 0:26).

For the PWCS, there were no relationships betweenplasma androgen levels and testis volume within the

GnRH treated (linear regression, r2 0:11; P 0:39),saline injected (linear regression, r2 0:25; P 0:20) orcontrol birds (linear regression, r2 0:24; P 0:21).During this sampling period all birds had maximally

recrudesced testes so there were no differences in testis

volume between the treatment groups (F2;22 1:35;P 0:28).

For the RUFS, there were no significant relationships

between plasma androgen levels and testis volume

within the GnRH treated (Fig. 3, linear regression,

r2 0:09; P 0:34), saline treated (linear regression,

Fig. 2. RUFS had smaller testes, averaged across all three treatment

groups, but greater variation than either PWCS or GWCS during the

spring breeding period. Bars represent the average and standard de-

viations of the data for each treatment group for each species. GWCS-fall birds had completely regressed gonads with an average volume of

0:59mm3.

Fig. 3. There is no relationship between plasma testosterone levels and

testis size in male RUFS in either of the three treatment groups. There

was great variation in both testis volume and plasma testosterone

levels in all three groups during the period of this study. Even males

with regressed testes were capable of producing elevated plasma tes-

tosterone levels.

Fig. 1. Baseline and maximal plasma testosterone levels in male birds

of the genus Zonotrichia from different latitudes. There was a signifi-

cant effect of treatment as well as the interaction of species and

treatment on plasma testosterone levels. Presented comparisons arelimited to within species and within the same treatment groups across

species. Different letters above the groups signify significant differences

P< 0:05. GWCS-fall samples were not statistically compared withthe other groups because they were sampled during a unique period

not replicated in the other species.


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r2 0:41; P 0:09) or control birds (linear regression,r

2 0:11; P 0:07). However, there were significantdifferences in testis volume between the treatment

groups (F2;49 3:22; P 0:049) with the GnRH groupbeing significantly greater than the saline group

(P 0:016). There was great variation in testis volume

(range: 5324 mm3) in male RUFS.

4. Discussion

In this study, we investigated congeneric birds that

breed at different latitudes to determine whether latitu-

dinal variation in basal and peak plasma testosterone

levels followed patterns previously described across spe-

cies and families of birds. We hypothesized, based on

these previous studies, that plasma testosterone would be

positively associated with the latitude of the breeding site,

with higher baseline and peak breeding levels in thenorthern populations. However, we found that the

equatorial population of RUFS had higher maximal

levels of plasma testosterone than the high-latitude

breeding GWCS. There was also no difference in plasma

testosterone levels between the mid- and high-latitude

breeding species. It is worth noting that the apparent

difference in maximal androgen levels between the RUFS

and the GWCS and PWCS is probably even greater than

we document. For the RUFS samples, we used column

chromatography to separate the androgens from one

another before the radioimmunoassay and thus only

measured testosterone. For the GWCS and PWCS sam-

ples we used a direct assay, without chromatography, and

measured plasma levels of total androgen (at least tes-tosterone and dihydrotestosterone which have 60% cross-

reactivity with the antibody we used; Wien Laboratories,

Succasunna, NJ). Therefore the differences between these

species are probably even greater than reported here. The

lower testosterone levels in the saline group relative to the

controls probably represents the effect of 30 min of con-

finement before the blood sample was obtained.

Previous studies of tropical birds from multiple

families have reported extremely low plasma levels of

testosterone, relative to northern temperate species,

throughout the reproductive cycle (Dittami, 1986, 1987;Dittami and Knauer, 1986; Gwinner and Scheuerlein,

1999; Hau, 2001; Hau et al., 2000; Levin and Wingfield,

1992; Lormee et al., 2000; Wikelski et al., 1999a, 2000).

For example, the well-studied male spotted antbird,Hylophylax naevioides naevioides, from Panama, has

consistently low plasma testosterone levels and yet is

territorial year-round (Hau, 2001; Wikelski et al., 2000).

The spotted antbird also has only a small rise in plasma

testosterone in response to GnRH challenge (M. Hau,

personal communication). The tropical white-browed

sparrow weavers, Plocepasser mahali, have a luteinizing

hormone surge in response to GnRH challenge that is

similar to northern latitude birds (Levin and Wingfield,

1992; Wingfield et al., 1991). However, the accompanying

rise in testosterone is much lower than in northern lati-

tude birds, suggesting that the differences may lie at the

level of the testis. Paradoxically, testis levels of testos-

terone are similar to northern latitude species (Levin and

Wingfield, 1992). However, as many of the tropical spe-cies that have been examined come from exclusively

tropical families, it is very difficult to make comparisonswith northern latitude species. In the current study, we

investigated three congeneric emberizine sparrows whose

breeding grounds span almost 70 latitude. To our

knowledge, RUFS are the first equatorial species to have

levels of testosterone comparable to northern latitude

species. Thus, it appears that the low levels of testosterone

so far reported in other tropical birds are not the result of

tropical distribution alone. In contrast to many other

equatorial species, male RUFS near Papallacta, Ecuador

are not aggressive year round (I.T. Moore, in review) andthus are more similar in terms of seasonal territorial be-

havior to their northern congeners. Papallacta, Ecuador

is also at high elevation while other studies of tropical

birds have been done at relatively low altitude. It is pos-

sible that high altitude has made the habitat in Papallacta

similar to higher latitude areas. Further studies need to be

completed on tropical species along an altitudinal cline to

investigate whether this is a potential factor in plasma

testosterone levels, territoriality and seasonal breeding.

In addition, studies of species with an equatorial phylo-

genetic history, such as the spotted antbird (Hau, 2001),

versus species such as RUFS, that breed at many lati-

tudes, need to be performed to determine the importance

of phylogenetics in hormone-behavior differences.The biological significance of the extreme elevation in

plasma testosterone levels is unclear in male RUFS.

Free-living male RUFS can be caught with high plasma

testosterone levels but do not respond to short-term

territorial challenges with increases in plasma testoster-

one (I.T. Moore, in review). It is possible that testos-

terone is elevated only during extended periods of social

instability and supports the aggressive behaviors neces-

sary at that time to claim the territory (Smith, 1978).

Such a relationship has been described in the spotted

antbird where territorial challenges of greater than 2 hare necessary to elicit an increase in plasma testosterone

(Wikelski et al., 1999b). It is also possible that baseline

levels in male RUFS are high enough to support

aggressive territorial behaviors and an increase is not

necessary. Low levels of testosterone are sufficient to

support the aggressive territorial behavior in the spotted

antbird and northern latitude song sparrows, Melospiza

melodia, during the non-breeding season (Hau et al.,

1999; Soma et al., 2000a,b). Future studies will

investigate the role of testosterone, both at basal and

elevated plasma levels, in social interactions in the male

RUFS.


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Male PWCS show social modulation of plasma tes-

tosterone as they exhibit an increase in plasma testos-

terone in response to simulated territorial intrusions

during the breeding season (Wingfield and Hahn, 1994).

However, the GnRH stimulated levels we report here

are higher than reported in response to simulated terri-

torial challenges (Wingfield and Hahn, 1994) but aresimilar to maximal levels resulting from social instability

during the breeding season (Wingfield and Farner,1978b). This indicates that social cues can be an im-

portant regulator of plasma testosterone levels. Male

GWCS breeding in northern Alaska, at the limit of their

range, do not show social modulation of plasma tes-

tosterone levels (Meddle et al., 2002) and our data

suggest that plasma testosterone levels are indeed max-

imal or close to maximal at this time of year (Wingfield

and Farner, 1978a). Thus, RUFS are similar to GWCS

in not showing social modulation of plasma testosterone

levels but the reason is different as the HPG axis inRUFS is not maximally activated and can respond to

stimulation, such as a GnRH challenge, as in PWCS.

RUFS were able to respond to stimulation of the

HPG axis regardless of gonad size. The ability of male

RUFS with relatively regressed gonads to produce ex-

tremely high plasma testosterone levels within 30 min

suggests that these birds are capable of initiating tes-

tosterone dependent activities during most periods of the

reproductive cycle. The RUFS samples were collected

during a month long period when individuals were found

in most reproductive states, including actively breeding,

but none of the individuals had as completely regressed

testes as the GWCS sampled in the fall. Further studies

support the idea that this period is roughly equivalent topre-breeding in northern temperate species (I.T. Moore,

unpublished data). It is possible that male RUFS may be

insensitive to GnRH challenge during other times of the

year (e.g., molt) when the testes are fully regressed. In

contrast, male PWCS and GWCS exhibit synchronized

seasonal gonadal growth and a positive correlation with

plasma testosterone across seasons but not within any

particular season (Wingfield and Farner, 1978a,b). We

did not see a testosterone response in male GWCS

challenged with GnRH during the fall, when they were

photosensitive but their testes were fully regressed(Wingfield and Farner, 1978a). During this period, the

anterior pituitary of GWCS is sensitive to GnRH

(Wingfield and Farner, 1993) suggesting that the gonads

are less sensitive to the luteinizing hormone resulting

from the bolus injection of GnRH.

Acknowledgments

We thank the Fundacion Terra and the Termas de

Papallacta in Ecuador, especially Patricio Pillajo, and

the staff at the Toolik Lake Field Station in Alaska. We

thank L. Belden and W. Goymann for statistical advice

and critically reading the manuscript and L. Erckmann

for steroid assay assistance. This research was approved

by the University of Washington IACUC. This research

was supported by NSF OPP-9911333 and IBN-9905679

to J.C.W. I.T.M. was supported by a NSF Minority

Postdoctoral Fellowship DBI-9904144-001. T.S.S. wassupported by an NIH Reproductive Biology Training

Grant to the University of Washington.

References

Blanchard, B.D., 1941. The white-crowned sparrows, Zonotrichia

leucophrys, of the Pacific Seaboard: environment and annual cycle.

Univ. Calif. Publ. Zool. 46, 1178.

Blanchard, B.D., Erickson, M.M., 1949. The cycle in the Gamble

sparrow. Univ. Calif. Publ. Zool. 47, 255318.

Cortopassi, A.J., Mewaldt, L.R., 1965. The cirumannual distribution

of white-crowned sparrows. Bird-Banding 36, 141169.

Dittami, J.P., 1986. Seasonal reproduction, moult and their endocrinecorrelates in two tropical Ploceidae species. J. Comp. Physiol. B

156, 641647.

Dittami, J.P., 1987. A comparison of breeding and molt cycles and life

histories in two tropical starling species: the blue-eared glossy

starling, Lamprotornis chalybaens, and Ruppels long-tailed glossy

starling, L. purpuropterus. Ibis 129, 6985.

Dittami, J.P., Knauer, B., 1986. Seasonal organization of breeding and

molting in the fiscal shrike. J. Ornithol. 127, 7984.

Folstad, A., Karter, A.J., 1992. Parasites, bright males and the

immunocompetence handicap. Am. Nat. 139, 603622.

Gwinner, E., Scheuerlein, A., 1999. Photoperiodic responsiveness of

equatorial and temperate-zone stonechats. Condor 101, 347359.

Hau, M., 2001. Timing of breeding in variable environments: tropical

birds as model systems. Horm. Behav. 40, 281290.

Hau, M., Wikelski, M., Soma, K.K., Wingfield, J.C., 2000. Testoster-

one and year-round territorial aggression in a tropical bird. Gen.

Comp. Endocrinol. 117, 2033.

Hau, M., Wikelski, M., Wingfield, J.C., 1999. Environmental control

of reproduction in a neotropical rainforest bird. In: Adams, N.J.,

Slowtow, R.H. (Eds.), Proceedings of the 22nd International

Ornithological Congress. Birdlife, Durban, South Africa, pp. 1720

1739.

Hillgarth, N., Ramenofsky, M., Wingfield, J., 1997. Testosterone and

sexual selection. Behav. Ecol. 8 (1), 108109.

Hunt, K., Wingfield, J.C., Astheimer, L.B., Buttemer, W.A., Hahn,

T.P., 1995. Temporal patterns of territorial behavior and circulat-

ing testosterone in the lapland langspur and other arctic passerines.

Am. Zool. 35, 274284.

King, J.R., Follett, B.K., Farner, D.S., Morton, M.C., 1966. Annualgonadal cycles and pituitary gonadotropins in Zonotrichia leucoph-

rys gambelii. Condor 68, 476487.

Levin, R.N., Wingfield, J.C., 1992. The hormonal control of territorial

aggression in tropical birds. Ornis. Scand. 23, 284291.

Lormee, H., Jouventin, P., Lacroix, A., Lallemand, J., Chastel, O.,

2000. Reproductive endocrinology of tropical seabirds: sex specific

patterns in LH, steroids, and prolactin secretion in relation to

parental care. Gen. Comp. Endocrinol. 117, 413426.

Meddle, S.L., Romero, L.M., Astheimer, L.B., Buttemer, W.A.,

Moore, I.T., Wingfield, J.C., 2002. Steroid hormone interrelation-

ships with territorial aggression in an arctic-breeding songbird,

Gambels White-crowned Sparrow, Zonotrichia leucophrys gam-

belii. Horm. Behav. 42, 212221.

Miller, A.H., 1961. Molt cycles in equitorial Andean sparrows. Condor

63, 143161.


7/31/2019 Moore et al. 2002

7/7

Miller, A.H., 1962. Bimodal occurence of breeding in an equitorial

sparrow. Proc. Natl. Acad. Sci. USA 48, 396400.

Miller, A.H., Miller, V.D., 1968. The behavioral ecology and breeding

biology of the Andean sparrow, Zonotriachia capensis. Caldasia 10,

83154.

Moller, A.P., 1998. Evidence of larger impact of parasites on hosts in

the tropics: investment in immune function within and outside the

tropics. Oikos 82, 265270.Nelson, R.J., 1995. An Introduction to Behavioral Endocrinology.

Sinauer Associates, Sunderland, MA.

Peters, A., 2000. Testosterone treatment is immunosuppressive in

superb fairy-wrens, yet free-living males with high testosterone are

more immunocompetent. Proc. R. Soc. London B 267, 883889.

Saino, N., Moller, A.P., Bolzern, A.M., 1995. Testosterone effects on

the immune system and parasite infestations in the barn swallow

(Hirundo rustica): an experimental test of the immunocompetence

hypothesis. Behav. Ecol. 6 (4), 397404.

Sherwood, N.M., Wingfield, J.C., Ball, G.F., Dufty, A.M., 1988.

Identity of gonadotropin-releasing hormone in passerine birds:

comparison of GnRH in song sparrow (Melospiza melodia) and

starling (Sturnus vulgaris) with five vertebrate GnRHs. Gen.

Comp. Endocrinol. 69, 341351.

Smith, S.M., 1978. The underworld in a territorial sparow: adaptivestrategy for floaters. Am. Nat. 112, 571582.

Soma, K.K., Sullivan, K.A., Tramontin, A.D., Saldanha, C.J., Schlin-

ger, B.A., Wingfield, J.C., 2000a. Acute and chronic effects of an

aromatase inhibitor on territorial aggression in breeding and

nonbreeding male song sparrows.J. Comp. Physiol. A 186, 759769.

Soma, K.K., Tramontin, A.D., Wingfield, J.C., 2000b. Oestrogen

regulates male aggression in the non-breeding season. Proc. R. Soc.

London B 267, 10891096.

Stutchbury, B.J.M., Morton, E.S., 2001. Behavioral Ecology of

Tropical Birds. Academic Press, San Diego.

Wikelski, M., Hau, M., Robinson, W.D., Wingfield, J.C., 1999a.

Seasonal endocrinology of tropical passerines: a comparative

approach. In: Adams, N.J., Slowtow, R.H. (Eds.), Proceedings of

the 22nd International Ornithological Congress. Birdlife, Durban,

South Africa, pp. 12241241.

Wikelski, M., Hau, M., Wingfield, J.C., 1999b. Social instability

increases plasma testosterone in a year-round territorial neotrop-

ical bird. Proc. R. Soc. London B 266, 551556.

Wikelski, M., Hau, M., Wingfield, J.C., 2000. Seasonality of repro-

duction in a neotropical rain forest bird. Ecology 81 (9), 2458

2472.

Wingfield, J.C., Farner, D.S., 1978a. The annual cycle of plasma irLH

and steroid hormones in feral populations of the white-crowned

sparow, Zonotrichia leucophrys gambelii. Biol. Reprod. 19, 1046

1056.

Wingfield, J.C., Farner, D.S., 1978b. The endocrinology of a naturallybreeding population of the white-crowned sparrow (Zonotrichia

leucophrys pugetensis). Physiol. Zool. 51, 188205.

Wingfield, J.C., Farner, D.S., 1980. Environmental and endocrine

control of seasonal reproduction in temperate zone birds. Prog.

Reprod. Biol. 5, 62101.

Wingfield, J.C., Farner, D.S., 1993. Endocrinology of reproduction in

wild species. In:Farner, D.S., King, J.R., Parkes, K.C. (Eds.), Avian

Biology, vol. 9. Academic Press, San Diego, CA, pp. 163327.

Wingfield, J.C., Hahn, T.P., 1994. Testosterone and territorial behav-

iour in sedentary and migratory sparrows. Anim. Behav. 47, 7789.

Wingfield, J.C., Hahn, T.P., Levin, R., Honey, P., 1992. Environmen-

tal predictability and control of gonadal cycles in birds. J. Exp.

Zool. 261, 214231.

Wingfield, J.C., Hegner, R.E., Lewis, D., 1991. Circulating levels of

luteinizing hormone and steroid hormones in relation to socialstatus in the cooperatively breeding white-browed sparrow weaver,

Plocepasser mahali. J. Zool. Lond. 225, 4348.

Wingfield, J.C., Jacobs, J., Hillgarth, N., 1997. Ecological constraints

and the evolution of hormonebehavior interrelationships. In:

Carter, C.S., Lederhendler, I.I., Kirkpatrick, B. (Eds.), The

Integrative Neurobiology of Affiliation, vol. 807. New York

Academy of Sciences, New York, pp. 2241.

Wingfield, J.C., Kenagy, G.J., 1991. Natural regulation of reproduc-

tive cycles. In: Pawg, P.K.T., Schreibruan, M.P. (Eds.), Vertebrate

Endocrinology: Fundamentals and Biomedical Implications, vol. 4.

Academic Press, San Diego, pp. 181241.

Wingfield, J.C., Smith, J.P., Farner, D.S., 1982. Endocrine responses

of white-crowned sparrows to environmental stress. Condor 84,

399409.

Wingfield, J.C., Wada, M., 1989. Changes in plasma levels of

testosterone during malemale interactions in the song sparrow,

Melospiza melodia: time course and specificity of response. J.

Comp. Physiol. A 166, 189194.


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