General and Comparative Endocrinology 163 (2009) 201–207

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General and Comparative Endocrinology

journal homepage: www.elsevier .com/locate /ygcen

Environment, glucocorticoids, and the timing of reproduction

Stephan J. Schoech a,*, Michelle A. Rensel a, Eli S. Bridge a,1, Raoul K. Boughton a,b, Travis E. Wilcoxen a

a Department of Biology, University of Memphis, 3774 Walker Avenue, Memphis, TN 38152, USAb Archbold Biological Station, 123 Main Drive, Venus, FL 33860, USA

a r t i c l e i n f o

Article history:Received 5 August 2008Revised 10 September 2008Accepted 26 September 2008Available online 1 October 2008

Keywords:CorticosteroneStressTiming of breedingEnvironmental perturbation

0016-6480/$ - see front matter � 2008 Elsevier Inc. Adoi:10.1016/j.ygcen.2008.09.009

* Corresponding author. Fax: +1 901 678 4746.E-mail address: sschoech@memphis.edu (S.J. Scho

1 Present address: University of Oklahoma, OklahoChesapeake, Norman, OK 73019, USA.

a b s t r a c t

Glucocorticoids mediate glucose availability under stressful and non-stressful conditions and, therefore,are essential for life. However, data across taxa demonstrate that chronic or elevated secretion of corti-costerone or cortisol (CORT) can have negative effects at many levels and can trigger physiological orbehavioral responses that may delay or, even halt reproduction. We present a brief overview of the effectsthat glucocorticoids, primarily the avian form, corticosterone, can have on the reproductive axis. Consid-erable data have demonstrated that environmental perturbations can result in elevated CORT levels thatalter a bird’s investment in current reproduction. Studies in our laboratory have shown a link betweenCORT and timing of reproduction in Florida scrub-jays: in ‘‘bad” years, clutch initiation dates are posi-tively correlated with baseline CORT levels of female breeders. Also, population-level differences in CORTlevels may explain timing of reproduction as lower CORT levels in suburban-dwelling jays are coupledwith early breeding.

Most research on stress and CORT concentrates on transient effects of CORT secretion. However, devel-opmental CORT exposure, either from the yolk or embryo, may have long-term effects upon adult pheno-type. For example, CORT levels in nestling scrub-jays predicts later ‘personality,’ as levels were highlycorrelated (r2 = 0.84) with fearfulness at 7 months of age. One can imagine that such ‘personality’ traitsmight also translate into differential success in gaining a territory or a mate. While speculative, it may bethat early CORT exposure effectively programs adult behaviors that have wide ranging effects, includingupon reproduction.

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1. Introduction

We have learned a considerable amount about the effects ofenvironmental perturbations on the hypothalamo–pituitary–adre-nal (HPA) axis’ production and secretion of glucocorticoids over thepast several decades. We have also gained insight into the meansby which glucocorticoids can negatively impact the reproductiveaxis (hypothalamo–pituitary–gonadal [HPG] axis) at multiple lev-els (for review, see Breuner et al., 2008). Despite our knowledgeof these relationships, relatively little is known about the interac-tion between environment, glucocorticoids, and timing of breedingin free-living animals. Although some studies provide insight intothis matter, most fail to track animals to the time when they repro-duce, usually because experiments elucidating the mechanismswhereby glucocorticoids impact the central nervous system(CNS) or gonads necessitate sacrificing the animals.

Despite having a myriad of effects upon multiple systems, theprimary function of corticosterone (CORT), the primary avian glu-

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ech).ma Biological Survey, 111 E.

cocorticoid, is to facilitate glucose release for utilization duringvaried challenges. In response to an acute stressor, such as attackby a predator, the adrenal medulla releases epinephrine (EPI) andnorepinephrine (NE) which facilitate the ‘immediate’ response tothe stimulus (e.g., increases of heart and respiration rates, glucoseavailability, and blood flow to muscles used in the fight-or-flightresponse). CORT is subsequently released by the adrenal cortex.If the stimulus is short-lived, there will be a transitory spike inCORT levels a few minutes after the stimulus, though should thestimulus be sustained, CORT levels will remain elevated for a con-siderable time before returning to pre-stress levels upon adrenalexhaustion, negative feedback of the CORT signal, or cessation ofthe stimulus. Use of the capture stress paradigm of Wingfieldet al. (1992) has demonstrated the nature of the CORT profile fortime periods that vary from 30 to 180 min in a number of species,although few studies prolong capture stress long enough to charac-terize the adrenal exhaustion phase. A number of factors may con-tribute to variance among baseline CORT levels, the CORT responseto a stressor, or both. (1) Body mass is often inversely related toCORT levels (Smith et al., 1994; Schoech et al., 1997, 1999). (2)CORT levels of individuals or populations often differ between-sea-sons or life-history stages (Goymann et al., 2006; Sorato and Kotrs-chal, 2006; Newman et al. 2008). (3) Birds that live in severe

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environments in which the opportunity to re-nest, should a nestfail or be abandoned, often exhibit a dampened CORT responseduring the breeding season (e. g., Wingfield et al., 1994a,b). (4)Similarly, birds with experimentally enlarged broods displayeddampened CORT responses to stress (Lendvai et al., 2007). (5)The length of the breeding season or latitude, two factors thatare often inter-correlated, may affect the HPA axis (see Goymannet al., 2006).

In this paper, we first briefly review some of the evidence thatglucocorticoids impinge on the avian HPG axis. Subsequently, wepresent a bit of background on environmental effects upon theHPA axis: a section that will provide a ‘mini-review’ with examplesof how an animal’s environment can stimulate the HPA axis. Final-ly, we present data on the interaction between environment, glu-cocorticoids, and reproduction in our study species, the Floridascrub-jay (Aphelocoma coerulescens). Because this paper is basedupon an oral presentation at the quadrennial International Sympo-sium on Avian Endocrinology, the vast majority of the examples weconsider throughout are avian. Thus, the glucocorticoid of interestis corticosterone (but see Schmidt and Soma, 2008), although inmammalian systems it may be corticosterone, cortisol, or both.

1.1. Glucocorticoid effects on the avian HPG axis

One of the first avian studies to experimentally link CORT withthe reproductive axis was conducted by Wilson and Follett (1975)who implanted CORT within the basal hypothalamus of tree spar-rows (Spizella arborea) and found a marked reduction in both plas-ma luteinizing hormone (LH) levels and gonadal growth rates.Somewhat paradoxically, tree sparrows that received CORT im-plants in the field failed to express negative effects upon levels ofreproductive hormones (e.g., testosterone, T; dihydrotestosterone,DHT; and LH: Astheimer et al., 2000). Subsequent research hasshown that CORT not only acts via numerous central sites todown-regulate the gonadotropin-releasing hormone (GnRH) sys-tem, but CORT binding sites within the gonad facilitate down-reg-ulation of enzymatic systems that regulate T production, as well asincrease the likelihood of Leydig cell apoptosis (Moore and Zoeller,1985; review in Wingfield and Farner, 1993). Salvantes and Wil-liams (2003) administered exogenous CORT to female zebrafinches and found (1) decreased vitellogenin production, (2) de-creased number of pairs initiating reproduction (56% vs. 100% ofcontrols), and (3) for those CORT-treated females that did lay, an8-day delay in clutch initiation.

Gonadotropin-inhibiting hormone (GnIH), a recently discoveredpeptide that plays a role in down-regulation of the HPG axis (Bent-ley et al., 2006; Ubuka et al., 2006; Greives et al., 2008), may medi-ate CORT’s effects upon the GnRH system. Calisi et al. (2008)exposed house sparrows to a standard 1 h capture and handlingstress protocol and found that these birds had significantly morecells that expressed GnIH immunoreactivity within the paraven-tricular nucleus (PVN) than did unstressed control birds. Consis-tent with an anti-gonadal and anti-reproduction role for GnIH inthis instance is their finding that there was no effect during the fallwhen all birds had relatively high numbers of cells expressingGnIH immunoreactivity. Although work is ongoing to isolate CORTreceptors on GnIH cells in birds (Calisi, personal communication),to date receptors have been identified on GnIH neurons of rats (Kir-by et al., 2007).

1.2. Environmental effects on glucocorticoid secretion

Wingfield (1985a) first published an example of an environ-mental perturbation that was directly linked to increased plasmaCORT levels in a study of song sparrows (Melospiza melodia). A latespring snow storm led to markedly increased plasma CORT levels

along with decreased estradiol levels in females. While CORT levelsreturned to pre-storm levels within a week and a half, plasmaestradiol remained depressed for considerably longer and, whencompared to the previous year, the mean lay date was delayedby 1 week. It is likely that the snow cover led to decreased foodavailability which drove the CORT increase, as food restriction gen-erally results in elevated CORT levels (Harvey et al., 1980; Lynnet al., 2003). Given the above evidence of direct effects of CORTupon the HPG axis, it seems likely that the increased CORT levelswere a key factor in the decreased estradiol levels and delayedbreeding in the Wingfield (1985a) study. However, one cannot ruleout central or peripheral effects that may be mediated by otherendocrine or neurocrine secretions. There has been a regular pro-cession of newly discovered metabolic hormones for which a fullrange of functions is only revealed some time after the initial char-acterization. For instance, there is some evidence that ghrelin andleptin (which may not exist in birds, see Sharp et al., 2008), in addi-tion to their roles in food intake and metabolism, modify reproduc-tive function. Tena-Sempere et al. (2007) posit that these twohormones, as well as numerous other neuropeptides of central orperipheral origin (see Greives et al., 2008), ‘‘may jointly cooperateto modulate a wide set of reproductive functions, thereby contrib-uting to the physiologic integration of energy balance and repro-duction.” These ideas are based primarily upon mammalianstudies and it must be noted that study of these and other peptidesthat have been implicated in mammalian reproduction is some-what lagging in birds.

While most think of climatic events when considering environ-ment, in the broadest sense an animal’s environment encompassesfar more than just weather. For example, several studies have doc-umented that the presence of a predator can affect plasma CORTlevels. Silverin (1998) found that pied flycatcher males (Ficedulahypoleuca) exposed to a live-mount of a weasel during the nestbuilding period had elevated levels of CORT following 10 min ofexposure. Similarly, great tits (Parus major) in an aviary that wereexposed to a stuffed owl responded with elevated CORT levels(Cockrem and Silverin, 2002). In the same publication, CORT levelsin free-living tits so treated exhibited a trend toward an increase.In an observational study, male tropical stonechats (Saxicola torqu-ata axillaris) whose territories were shared with predatory fiscalshrikes (Lanius collaris) had elevated baseline CORT levels, suggest-ing chronic stress (Scheuerlein et al., 2001). Although a direct linkbetween CORT and reproduction was not established, the research-ers note that stonechat pairs sharing their territory with shrikesdelay initiating, and are less likely to initiate, a second clutch thanare nearby birds without shrikes.

Interactions with conspecifics can also be ‘stressful.’ Simulatedterritorial intrusions (STI), in which either a live or a stuffed birdis presented to a territory holder along with conspecific song play-back, are valuable in elucidating the nature of the testosterone re-sponse to a perceived conspecific challenge (Wingfield, 1985b).However, in some species this protocol has been found to resultin elevated levels of CORT. Male pied flycatchers responded to aterritorial intrusion by elevating both T and CORT levels (Silverin,1998). In contrast, blue tits (Cyanistes caeruleus) responded to STIswith elevated CORT levels while exhibiting decreased T levels (Lan-dys et al., 2007). Further, Landys et al. (2007) used a meta-analysisof the studies to date that have used STIs and found that single-brooded species, like the blue tit, consistently elevate CORT whileexhibiting either no change or decreased T levels.

The social interactions that are a part of an animal’s environ-ment are not limited to those coming from outside of the socialgroup. For instance, Angelier et al. (2007) note that in newlyformed pairs of black-legged kittiwakes (Rissa tridactyla), bothmales and females had higher baseline CORT levels than estab-lished pairs, perhaps resulting from poor cohesion in shared duties

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or general anxiety with a new mate. Remage-Healey et al. (2003)noted similar patterns in a study with captive zebra finches (Taeni-opygia guttata). Of special interest to our research group are studiesof social groups, specifically cooperative breeders and especiallythose species for which there is only one breeding pair in a group.To explain reproductive quiescence, it has been postulated that thenonbreeder helpers in a group, which are invariably subordinate tothe breeders, are ‘psychologically castrated’ (see Brown, 1978).This hypothesis predicts that nonbreeders are reproductively sup-pressed through dominant/subordinate interactions that act to ele-vate CORT levels, thereby down-regulating HPG axis function. Ofthe too few studies that have addressed this issue in avian cooper-ative breeders, there is little evidence to suggest that this hypoth-esis has merit (Schoech et al., 1991, 1997; Mays et al., 1991;Wingfield et al., 1991; but see Rubenstein, 2007). However, thisis a common and recurring theme in cooperatively breeding mam-mals in which it is not uncommon to find reproductive skew en-forced via active social suppression accompanied with increasedlevels of CORT and decreased HPG axis function of helpers (seeYoung et al., 2006; Young, in press and citations within).

1.3. Humans and their effects upon the environment

An increasingly prominent element of all species’ environmentis human presence and activity. The influence of humans can rangefrom indirect effects, such as exposure to contaminants, whichmay alter HPA axis function, to occasional direct contact with hu-mans, to consistent ‘‘cohabitation.” There is considerable evidencethat all of the above types of encounter can be ‘stressful.’ For exam-ple, blood levels of lead in nestling white storks (Ciconia ciconia)were positively correlated with maximal CORT levels (Baos et al.,2006). Paradoxically, overall highest levels were found in the refer-ence population rather than in the contaminant-exposed colony.Several researchers have examined the effects of human visitationat penguin colonies with findings that vary by species. Magellanicpenguins (Spheniscus magellanicus) in tourist areas exhibit a damp-ened responsiveness to stress, suggesting habituation (Walkeret al., 2006). Conversely, yellow-eyed penguins (Megadyptes antip-odes) appear to be sensitized to tourists as birds in tourist areashave higher stress-induced CORT levels and lower reproductivesuccess than birds rarely visited (Ellenberg et al., 2007).

Although many avian species cannot coexist with humans andrapidly disappear as we encroach on their habitat, there are a num-ber of species that seemingly thrive in cities; e.g., house sparrows(Passer domesticus) and European starlings (Sturnus vulgaris). Whilethere is a growing interest in urban ecology and demography (seeMarzluff et al., 2001), there have been few investigations into thestress physiology associated with urban life. Comparisons of city(Munich) and nearby forest-dwelling European blackbirds (Turdusmerula) found that the former had functional gonads from 3(males) to 4 (females) weeks earlier than birds in natural habitat(Partecke et al., 2005). A follow-up study with hand-reared birdsfound that city birds also had a dampened CORT response to cap-ture and handling (Partecke et al., 2006). The authors interpret thisfinding as a micro-evolutionary change allowing urban-dwellingbirds to cope with a stressful environment. Conversely, Bonieret al. (2007) found that male white-crowned sparrows (Zonotrichialeucophrys), but not females, in cities had higher baseline CORTthan conspecifics in natural habitat.

Our study group has examined numerous environmental vari-ables to address our observation that Florida scrub-jays in a subur-ban development consistently breed earlier than jays in naturalhabitat at nearby (10 km) Archbold Biological Station (ABS) (Scho-ech and Bowman, 2001, 2003). Suburban jays’ baseline CORT levelsare less than one half those of ‘wildland’ jays (2.16 ± 0.28 vs.4.81 ± 0.33 ng/ml), and Schoech et al. (2004) speculate that the

higher CORT in the wildlands might act as a ‘brake’ on the HPGaxis, thereby offering a partial explanation for their later breeding.However, a follow-up study in which wildland jays received exog-enous CORT failed to support this explanation as CORT-dosed birdsdid not delay clutch initiation (Schoech et al., 2007a). It should benoted that the CORT doses administered increased CORT levelsmarkedly over the short-term (representative of an ‘‘acute” stressresponse), thus failing to chronically elevate CORT and confound-ing interpretation. Subsequent research to determine whetherthe low levels in suburban jays reflected habituation or a compro-mised HPA axis due to chemical contaminant exposure suggeststhat neither of these postulated underlying causes has merit, asthere was no between-population difference in the CORT responseto capture stress, whereas both predict a dampened CORT responseto a stressor (Schoech et al., 2007b). Interestingly, suburban jaystended to have a more robust response as was indicated by a morerapid rate of increase over the initial 5 min of capture.

1.4. Manipulating the environment with supplemental food: lessonsfrom Florida scrub-jays

In the decision to reproduce, resource availability in the form offood can operate at both the proximate and ultimate levels (Lack,1968; Perrins, 1970): food supplementation studies have beenused to address questions across levels (see Schoech and Hahn,2008; Schoech et al., 2008 and citations within). Conceptually, sucha technique can be viewed as a method of altering an animal’senvironment. In a series of experiments beginning in 1993, Scho-ech and colleagues have used food supplementation of coopera-tively breeding Florida scrub-jays to investigate both thephysiological mechanisms linking food availability and timing ofreproduction (Schoech, 1996; Schoech and Bowman, 2001, 2003;Schoech et al., 2004, 2007a,b) as well as whether there are fitnessbenefits (Schoech et al., 2008).

Food supplemented Florida scrub-jays invariably advance lay-ing, although the degree is lessened in ‘good’ years and increasedin ‘bad’ years (see Reynolds et al., 2003; Schoech et al., 2007b,2008; see below). In some years, jays provided with high qualitysupplemental food (i.e., high in fat and protein) not only advancedlaying, but had lower baseline CORT levels than control jays andbirds that were provided a high fat but low protein supplement(Schoech et al., 2004). However, whether or not food supplementa-tion affects plasma CORT levels also appears to vary between years,assumedly with varying conditions and resource availability (seeSchoech et al., 2007b). Although definitively linking environmentalconditions, plasma CORT, and timing of reproduction in this spe-cies is difficult (in part due to its threatened status that rules outsome manipulative study), the responses to supplemental foodand the natural variation in these three variables addressed beloware suggestive of causal links.

Over the last 8 years (2001–2008), we have tracked all of thedemographic aspects of the study population of Florida scrub-jaysthat occupy the southern part of ABS, and collected hundreds ofblood samples from which we’ve determined baseline levels ofCORT. For all jays in our population, we: (1) track fates from theegg through death; (2) determine sex, status (breeder or non-breeding helper), and age; (3) locate all nests and determine layingand hatching dates and order, as well as fledging dates; and (4)monitor survivorship to independence (�70 days post-hatch) andbeyond, including recruitment into the breeding population. Jayswere trapped in continuously monitored Potter traps, therebyassuring that an initial blood sample to measure baseline CORTwas collected within 2–3 min (see Schoech et al., 1991, 1997,1999; Romero and Romero, 2002). Samples were later assayed inthe Schoech lab at the University of Memphis. While we conductedfood supplementation studies during this period, the findings pre-

Fig. 1. First clutch initiation date for each of the 8 years of the study. Data areshown as means ± SEM. Numbers in parentheses represent sample size followed bythe mean number of young per territory that reached nutritional independence atapproximately 70 days-of-age.

Fig. 2. Baseline corticosterone levels of female breeders plotted against the day ofthe year that a given female initiated her clutch. Samples are depicted by year-class:closed circles represent data from ‘bad’ years (long-dash best fit line), open circlesrepresent data from ‘average’ years (short-dash best fit line), and closed trianglesrepresent data from ‘good’ years (dotted best fit line). Categorization of year-classesis defined in the text.

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sented here are only for non-supplemented jays, although someindividuals may have been supplemented in previous years.

Mean clutch initiation dates between years varied by 9 daysduring this time (Fig. 1), a surprisingly small variance based uponlong-term monitoring that has documented inter-year variance inlay dates of approximately 1 month (Schoech, 1996). As is impliedabove and as lay dates suggest, not all years are equal and gener-ally, earlier breeding occurs in ‘good’ years that are also character-ized by high offspring productivity. Conversely, ‘bad’ years arecharacterized by later breeding and lower productivity. The meannumber of young to reach independence during the study rangedfrom 0.3 to 1.0 individual per group with an overall mean of 0.58young. However, in some years there is a degree of disconnect fromthis general truism and timing of breeding does not linearly predictproductivity. Therefore we used lay date and number of indepen-dent young produced for each of the 8 years in a principal compo-nents analysis: PC1 explained 81.3% of the variance. Based uponPC1, years were ranked and assigned as good (PC1 < �1.0: 2002and 2008), average (�1.0 > PC1 < 1.0: 2003, 2004, 2005, and2006), and bad (PC1 > 1.0: 2001 and 2007).

To examine the association between baseline CORT and yearquality, we used an ANCOVA with year-class (good, average, orbad), sex, and reproductive status (breeder or nonbreeding helper)as factors and date of sample collection as a covariate. All sampleswere collected during the prebreeding period, thereby allowing usto assess CORT levels when the decisions of when to initiate aclutch are made. Only year-class explained CORT levels(F2,236 = 3.24, P = 0.04). Neither sex (F1,236 = 0.09, P = 0.76), status(F1,236 = 0.46, P = 0.50), date (F1,236 = 1.06, P = 0.31), nor any of theinteraction terms approached statistical significance. We reranthe analysis with non-significant terms removed and found thestatistical relationship between year-class and baseline CORT wasstrengthened (ANOVA; F2,250 = 4.66, P = 0.01). Bonferroni-correctedpairwise comparisons found that CORT levels in bad years(4.94 ± 0.46 ng/ml) were higher than during average years(3.38 ± 0.25 ng/ml: P = 0.01), though levels during good years(4.42 ± 0.71 ng/ml) did not differ from either of the other twocategories.

Although our initial analysis noted no differences by sex orbreeding status, because the breeding female is almost certainlythe ‘‘decider” of when or if to initiate a clutch, we further examinedthe relationship between baseline CORT levels and lay dates inbreeder females. When all data were collapsed across years, therewas a significant relationship between baseline CORT and first

clutch initiation date (regression: F1,74 = 4.13, p = 0.046), althoughCORT explained only 5.3% of the variance. We further examinedthis relationship by each of the 3-year-classes and found that theoverall significance is likely due to the relatively strong predictivevalue of CORT on lay date during bad years (F1,22 = 10.44, p = 0.004,r2 = 0.32; see Fig. 2). However, there was no relationship betweenthese two variables in either average (F1,32 = 1.40, p = 0.25,r2 = 0.04) or good years (F1,16 = 1.31, p = 0.27, r2 = 0.08).

These findings offer some support for the hypothesis that envi-ronmental conditions affect plasma CORT levels which in turn mayinfluence the timing of reproduction. While our data do not over-whelmingly support this hypothesis, the somewhat elevated base-line CORT during bad years and the relatively strong relationshipbetween these levels and lay date are intriguing. What specificallymade the 2 years, 2001 and 2007, bad years? As noted above, pro-ductivity usually decreases with increasing lay date, though amean delay of just a few days, as is the case for these 2 years,would not be expected to make a substantial difference. Schoech(1996) noted that the exceptionably late and poor breeding seasonof 1992 was presaged by very little rainfall (November–January).Similarly, whereas the mean rainfall of the 6 years designated asgood and average was 13.9 cm for this same 3-month period, itwas 2.24 and 6.78 cm for 2001 and 2007, respectively. Too littlerainfall during this period could have profound effects upon re-source availability as drought conditions lead to poor new plantgrowth which can negatively affect the abundance of the arthropodand vertebrate prey that scrub-jays regularly take. Further, Floridascrub-jays rely on acorn caches during the winter and early springwhen other food sources are scarce (DeGange et al., 1989) and theacorn mast during the late summer and fall of 2006 (which impactsthe subsequent breeding season) was exceptionally poor. Basedupon a long-term annual acorn count at ABS, acorn abundance in2006 was approximately one fifth of the long-term average (Bow-man, unpublished data). Given the association between CORTsecretion and nutritional state, we postulate that poor resourceavailability in bad years results in tonically, albeit mildly, elevatedCORT levels that, in turn, influence the timing of reproduction.These results emphasize the utility of long-term studies in uncov-ering relationships between environmental factors, breeding, andphysiology. Indeed, a study conducted over only 1–2 years wouldlikely miss such a relationship and, thereby conclude that therewas no relationship between CORT and timing of reproduction.

Fig. 3. Baseline corticosterone levels (power transformed data, see Schoech et al.,2007b) of day 11 nestlings plotted against individuals’ overall fearfulness ranking atapproximately 7 months of age. Lower ranks are bolder than higher ranks. Sharedsymbols represent individuals that are siblings.

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1.5. ‘Organizational’ effects of CORT

The organizational–activational dichotomy of hormone actionshas elucidated how hormones can shape an organism’s physiolog-ical and behavioral responses (Phoenix et al., 1959; Goy and Phoe-nix, 1972; Arnold and Breedlove, 1985; Moore, 1991).Developmental effects of hormones are usually considered withreference to sex steroids. However, it has long been known thatdeveloping male embryos of mothers that are stressed duringpregnancy are somewhat feminized, with a number of male-typicalbehavior patterns affected upon reaching adulthood (Nelson,2005). Similarly, post-natal parental care can have critical effectson offspring development that can influence an individual’s adultphenotype and personality (Meaney, 2001; Kim and Diamond,2002; Repetti et al., 2002; Dingemanse et al., 2004; Zhang et al.,2006). For example, in rats, offspring reared by more attentivedams displayed more exploratory behavior and recovered morerapidly following exposure to a stressor (Liu et al., 1997; Weaveret al., 2002; Szyf et al., 2005). Conversely, offspring from less atten-tive mothers were more fearful and had greater stress responses(i.e., increased levels of ACTH and CORT). Weaver et al. (2006)found that the ‘‘high-stress” developmental pathway in rats wasestablished early in life by deactivation of DNA regions that encodeglucocorticoid receptors, thereby affecting adult responses tostressors. Thus, differences in maternal care can direct a perma-nent change in DNA expression that can shape an individual’s per-sonality by forever altering how it responds to environmentalchallenges.

Similar links between developmental stress and adult pheno-type have been observed in birds. For example, in black-legged kit-tiwakes, nutritional stress during development results incognitively and physiologically compromised adults (Kitayskyet al., 2006). Also, western scrub-jays (Aphelocoma californica), aFlorida scrub-jay congener, that were food-restricted as nestlingshad higher baseline CORT levels and more pronounced stress re-sponses at 1year-of-age than ad libitum fed controls (Pravosudovand Kitaysky, 2006). Several recent studies of passerine and non-passerine species have noted links between phenotype (e.g., ‘per-sonality’ and stress responsiveness) and CORT exposure (duringdevelopment or as an adult) that parallel those found in the abovedescribed mammalian research (e.g., European starling, Love andWilliams, 2008; great tit, Carere et al., 2003; Japanese quail [Cotur-nix coturnix]; Hayward and Wingfield, 2004; and see Cockrem,2007 for a review that covers several species).

It has been hypothesized that such ‘programming’ of an individ-ual’s phenotype is adaptive, and that in a fluctuating environment,there is no single optimal phenotype. The quality or quantity ofparental care, therefore, may serve as a signal that directs offspringdevelopment down the path that best ensures survival during thevulnerable, early stages of life (for review, see Koolhaas et al., 1999;Wells, 2003; Zhang et al., 2006). For example, in harsh conditions, ahigh-CORT phenotype may increase an individual’s chances of sur-viving, especially if fearfulness translates into anti-predator behav-ior and if the ability to metabolize stored nutrients (facilitatedthrough CORT secretion) is at a premium.

We reasoned that variance in personality, primarily boldness ortimidity, could have a strong effect on the likelihood that an indi-vidual gains a breeding territory or a mate. In Florida scrub-jaysthere is considerable variance in the time that a young bird re-mains as a helper in its natal territory before becoming a breeder(see Woolfenden and Fitzpatrick, 1984, 1990, 1996). An excitingnew line of research from our group addresses the relationship be-tween a nestling’s environment, its CORT levels, and adult pheno-type; and although it is too early to empirically determine impactson the timing of breeding, we present these findings as an illustra-tion of the organizational effects of CORT.

All nestlings are banded, measured (mass and linear size mea-sures), and a small blood sample is collected on day 11 post-hatch.Each nestling is removed from the nest, bled within 3 min, andmeasured before being returned to the nest; the procedure is thenrepeated for each subsequent nestling. This allows baseline CORTlevels of nestlings to be measured (the HPA axis of 11-day-old nes-tlings is capable of mounting a stress response, Rensel and Bough-ton, unpublished data). In the bad year of 2007 (see above), of the55 nestlings banded and sampled at day 11 only 17 survived toindependence.

We conducted three behavioral tests on 10 of the 17 survivorswhen they were approximately 7 months of age. Prior to testing,the ‘naive’ young were trained to come to a pile of peanuts and,as is their wont; once jays discover peanuts they return to thesource until it’s depleted, eating until satiated and caching the rest.The tests exploited this trait and were video-taped to facilitateindividual identification and accurate time keeping. Test 1, the ringtest, used a bright orange ring 50 cm in diameter and 3 cm highwhich was placed around a peanut pile; the time a jay spent within1 m of the ring before crossing to take a peanut was then mea-sured. For tests 2 and 3, a hidden buzzer beneath the pile or a mov-ing leaf attached to a hidden motor within the pile, respectively,startled subjects; return times were then assessed. The ring testyielded hesitancy times that ranged from 2 to 192 s; however,two of the 10 birds failed to cross the ring during the 1 h allottedtest period. For the sound and motion tests, return times rangedfrom 1 to 57 s and 10 s to 32 min, respectively.

Because the times to complete the test were not normally dis-tributed, for each test birds were ranked from one to 10 (note,the two birds that did not return to cross the ring shared a scoreof nine) with the lowest rank corresponding to the shortest time(i.e., the least fearful individual). An individual’s three ranks weresummed and this total was used to generate an overall fearfulnessrank across the 10 test jays. To test the degree to which early CORTexposure influenced the jays’ ‘personality,’ we regressed the over-all fearfulness rank against nestling CORT levels and found an ex-tremely strong relationship (F1,8 = 41.48, p < 0.001, r2 = 0.84;Fig. 3). Further, seven of the tested jays survived the remainderof the winter and were again tested with the ring test at 1 yearof age. We found that this measure of fearfulness tended to persist(r = 0.68, p = 0.066, n = 7). While the small sample sizes renderdrawing general conclusions problematic, we also observed indica-tions of persistence in stress physiology. For example, (1) baseline

206 S.J. Schoech et al. / General and Comparative Endocrinology 163 (2009) 201–207

CORT levels of 11-day-old nestlings tended to be correlated withlevels at 2.5 months (r = 0.64, p = 0.12, n = 7); (2) as were baselineCORT levels at approximately 2.5 months and 1 year (r = 0.72,p = 0.069, n = 7); and (3) as were maximum CORT levels at approx-imately 2.5 months and 1 year (r = 0.81, p = 0.052, n = 6). We lookforward to gathering further data to determine whether thesetrends persist.

2. Conclusions

We have presented a brief overview of how the environmentalconditions an animal experiences can affect its CORT levels and, insome cases how this can then play a role in determining the timingof reproduction. While there is considerable evidence linking theenvironment and CORT and CORT and the reproductive axis, thereare fewer studies that integrate these three variables. Regardless, itseems clear that elevated CORT levels in response to a plethora ofenvironmental conditions can slow the up-regulation of the HPGaxis, thereby delaying the onset of reproduction. However, it isequally clear that CORT levels are not the sole determinant of whenthe onset of reproduction occurs.

Acknowledgments

S.J.S. thanks John Cockrem, Pierre Deviche, and Wolfgang Goy-mann for inviting him to speak in the Ecology and Evolution sym-posium they convened at the July 2008 International Symposiumon Avian Endocrinology in Leuven, Belgium: this paper is basedupon S.J.S.’s talk at that meeting. During the collection of data de-scribed herein, we were partially supported by NSF funding to S.J.S.(IBN-9983201 and IOS-0346328). M.A.R. has also been funded inpart by Sigma Xi, the American Ornithologists’ Union, and theDepartment of Biology at the University of Memphis: the latterhas provided support for all of the co-authors. Special thanks toS. James Reynolds and Gina Morgan for help with data collectionand multiple aspects of the jay project. Further assistance in thefield came from Jonathan Atwell, Tim Harrison, and numerous fieldassistants. The research was greatly aided by S.J.S.’ collaborationwith R. Bowman at ABS. We thank Dave Freeman for helpful com-ments on an earlier draft of this paper.

References

Angelier, F., Moe, B., Clement-Chastel, C., Bech, C., Chastel, O., 2007. Corticosteronelevels in relation to change of mate in black-legged kittiwakes. Condor 109,668–674.

Arnold, A.P., Breedlove, S.M., 1985. Organizational and activational effects of sexsteroids on brain and behavior: a reanalysis. Hormones and Behavior 19, 469–498.

Astheimer, L.B., Buttemer, W.A., Wingfield, J.C., 2000. Corticosterone treatment hasno effect on reproductive hormones or aggressive behavior in free-living maletree sparrows, Spizella arborea. Hormones and Behavior 37, 31–39.

Baos, R., Blas, J., Bortolotti, G.R., Marchant, T.A., Hiraldo, F., 2006. Adrenocorticalresponse to stress and thyroid hormone status in free-living nestling whitestorks (Ciconia ciconia) exposed to heavy metal and arsenic contamination.Environmental Health Perspectives 114, 1497–1501.

Bentley, G.E., Jensen, J.P., Kaur, G.J., Wacker, D.W., Tsutsui, K., Wingfield, J.C., 2006.Rapid inhibition of female sexual behavior by gonadotropin-inhibitoryhormone (GnIH). Hormones and Behavior 49, 550–555.

Bonier, F., Martin, P.R., Sheldon, K.S., Jensen, J.P., Foltz, S.L., Wingfield, J.C., 2007. Sex-specific consequences of life in the city. Behavioral Ecology 18, 121–129.

Brown, J.L., 1978. Avian communal breeding systems. Annual Review of Ecology andSystematics 9, 123–155.

Breuner, C.W., Patterson, S.H., Hahn, T.P., 2008. In search of relationships betweenthe acute adrenocortical response and fitness. General and ComparativeEndocrinology 157, 288–295.

Calisi, R.M., Rizzo, N.O., Bentley, G.E., 2008. Seasonal differences in hypothalamicEGR-1 and GnIH expression following capture-handling stress in housesparrows (Passer domesticus). General and Comparative Endocrinology 157,278–283.

Carere, C., Groothuis, T.G.G., Möstl, E., Daan, S., Koolhaas, J.M., 2003. Fecalcorticosteroids in a territorial bird selected for different personalities: dailyrhythm and the response to social stress. Hormones and Behavior 43, 540–548.

Cockrem, J.F. 2007. Stress, corticosterone responses and avian personalities. Journalof Ornithology 148 (Suppl. 2). doi:10.1007/s10336-007-0175-8.

Cockrem, J.F., Silverin, B., 2002. Sight of a predator can stimulate a corticosteroneresponse in the great tit (Parus major). General and Comparative Endocrinology125, 248–255.

DeGange, A.R., Fitzpatrick, J.W., Layne, J.N., Woolfenden, G.E., 1989. Acornharvesting by Florida scrub jay. Ecology 70, 348–356.

Dingemanse, N.J., Both, C., Drent, P.J., Tinbergen, J.M., 2004. Fitness consequences ofavian personalities in a fluctuating environment. Proceedings of the RoyalSociety of London. Series B: Biological Sciences 271, 847–852.

Ellenberg, U., Setiawan, A.N., Cree, A., Houston, D.M., Seddon, P.J., 2007. Elevatedhormonal stress response and reduced reproductive output in yellow-eyedpenguins exposed to unregulated tourism. General and ComparativeEndocrinology 152, 54–63.

Goy, R.W., Phoenix, C.H., 1972. The effects of testosterone propionate administeredbefore birth on the development of behavior in genetic female rhesus monkeys.In: Sawyer, C., Gorski, R. (Eds.), Steroid Hormones and Brain Function.University of California Press, Berkeley, pp. 193–201.

Goymann, W., Geue, D., Schwabl, I., Flinks, H., Schmidl, D., Schwabl, H., Gwinner, E.,2006. Testosterone and corticosterone during the breeding cycle of equatorialand European stonechats (Saxicola torquata axillaris and S. t. rubicola). Hormonesand Behavior 50, 779–785.

Greives, T.J., Kriegsfeld, L.J., Bentley, G.E., Tsutsui, K., Demas, G.E., 2008. Recentadvances in reproductive neuroendocrinology: a role for RFamide peptides inseasonal reproduction? Proceedings of the Royal Society, B 275, 1943–1951.

Harvey, W.N., Merry, B.J., Phillips, J.G., 1980. Influence of stress on the secretion ofcorticosterone in the duck (Anas platyrhynchos). Journal of Endocrinology 87,161–171.

Hayward, L.S., Wingfield, J.C., 2004. Maternal corticosterone is transferred to avianyolk and may alter offspring growth and adult phenotype. General andComparative Endocrinology 135, 365–371.

Kim, J.J., Diamond, D.M., 2002. The stressed hippocampus, synaptic plasticity andlost memories. Nature Reviews Neuroscience 3, 453–462.

Kirby, E.D., Ubuka, T., Kaufer, D. Bentley, G.E., 2007. Acute immobilization stressincreases putative gonadotropin inhibitory hormone expression in the rathypothalamus. The 37th Annual Meeting for the Society of Neuroscience, SanDiego, California (Abstract).

Kitaysky, A.S., Kitaiskaia, E.V., Platt, J.F., Wingfield, J.C., 2006. A mechanistic linkbetween chick diet and decline in seabirds? Proceedings of the Royal Society ofLondon. Series B: Biological Sciences 273, 445–450.

Koolhaas, J.M., Korte, S.M., de Boer, S.F., van der Vegt, B.J., van Reenen, C.G., Hopster,H., de Jong, I.C., Ruis, M.A.W., Blokhuis, H.J., 1999. Coping styles in animals:current status in behavior and stress-physiology. Neuroscience and BiobehaviorReviews 23, 925–935.

Lack, D., 1968. Ecological Adaptations for Breeding in Birds. Chapman and Hall,London.

Landys, M.M., Goymann, W., Raess, M., Slagsvold, T., 2007. Hormonal responses tomale–male social challenge in the blue tit, Cyanistes caruleus: single-broodedness as an explanatory variable. Physiological and BiochemicalZoology 80, 228–240.

Lendvai, A.Z., Giraudeau, M., Chastel, O., 2007. Reproduction and modulation of thestress response: an experimental test in the house sparrow. Proceedings of theRoyal Society, B 274, 391–397.

Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S.,Pearson, D., Plotsky, P.M., Meaney, M.J., 1997. Maternal care, hippocampalglucocorticoid receptors, and hypothalamic–pituitary–adrenal responses tostress. Science 277, 1659–1662.

Love, O.P., Williams, T.D., 2008. Plasticity in the adrenocortical response of a free-living vertebrate: The role of pre- and post-natal developmental stress.Hormones and Behavior 54, 496–505.

Lynn, S.E., Breuner, C.W., Wingfield, J.C., 2003. Short-term fasting affects locomotoractivity, corticosterone, and corticosterone binding globulin in a migratorysongbird. Hormones and Behavior 43, 150–157.

Marzluff, J.M., Bowman, R., Donnelly, R., 2001. Avian Ecology and Conservation in anUrbanizing World. Kluwer Academic Press, Norwell, Massachusetts.

Mays, N.A., Vleck, C.M., Dawson, J., 1991. Plasma luteinizing hormone, steroidhormones, behavioral role, and nest stage in cooperatively breeding Harris’hawks (Parabuteo unicinctus). Auk 108, 619–637.

Meaney, M.J., 2001. Maternal care, gene expression, and the transmission ofindividual differences in stress reactivity across generations. Annual Review ofNeuroscience 24, 1161–1192.

Moore, F.L., Zoeller, R.T., 1985. Stress-induced inhibition of reproduction: evidenceof suppressed secretion of LH-RH in an amphibian. General and ComparativeEndocrinology 60, 252–258.

Moore, M.C., 1991. Application of organization–activation theory to alternativemale reproductive strategies: a review. Hormones and Behavior 25, 154–179.

Nelson, R.J., 2005. An Introduction to Behavioral Endocrinology. Sinauer Associates,Inc., Sunderland, MA.

Newman, A.E.M., Pradhan, D.S., Soma, K.K., 2008. Dehydroepiandrosterone andcorticosterone are regulated by season and acute stress in a wild songbird:jugular versus brachial plasma. Endocrinology 149, 2537–2545.

Partecke, J., Schwabl, I., Gwinner, E., 2006. Stress and the city: urbanization and itseffects on the stress physiology of European blackbirds. Ecology 87, 1945–1952.

Partecke, J., Van’t Hof, T.J., Gwinner, E., 2005. Underlying physiological control ofreproduction in urban and forest-dwelling European blackbirds Turdus merula.Journal of Avian Biology 36, 295–305.

S.J. Schoech et al. / General and Comparative Endocrinology 163 (2009) 201–207 207

Perrins, C., 1970. The timing of birds’ breeding seasons. Ibis 112, 242–255.Phoenix, C.H., Goy, R.W., Gerall, A.A., Young, W.C., 1959. Organizing action of

prenatally administered testosterone propionate on the tissues mediatingmating behavior in the female guinea pig. Endocrinology 65, 369–382.

Pravosudov, V.V., Kitaysky, A.S., 2006. Effects of nutritional restrictions duringpost-hatching development on adrenocortical function in western scrub-jays (Aphelocoma californica). General and Comparative Endocrinology 145,25–31.

Remage-Healey, L., Adkins-Regan, E., Romero, L.M., 2003. Behavioral andadrenocortical responses to mate separation and reunion in the zebra finch.Hormones and Behavior 43, 108–114.

Repetti, R.L., Taylor, S.E., Seeman, T.E., 2002. Risky families: family socialenvironments and the mental and physical health of offspring. PsychologicalBulletin 128, 330–366.

Reynolds, S.J., Schoech, S.J., Bowman, R., 2003. Nutritional quality of prebreedingdiet influences breeding performance of the Florida Scrub-Jay. Oecologia 134,308–316.

Romero, L.M., Romero, R.C., 2002. Corticosterone responses in wild birds: theimportance of rapid initial sampling. Condor 104, 129–135.

Rubenstein, D.R., 2007. Stress hormones and sociality: integrating social andenvironmental stressors. Proceedings of the Royal Society, London. Series B:Biological Sciences 274, 967–975.

Salvantes, K.G., Williams, T.D., 2003. Effects of corticosterone on the proportion ofbreeding females, reproductive output and yolk precursor levels. General andComparative Endocrinology 130, 205–214.

Scheuerlein, A., Van’t Hof, T.J., Gwinner, E., 2001. Predators as stressors?Physiological and reproductive consequences of predation risk in tropicalstonechats (Saxicola torquata axillaris). Proceedings of the Royal Society, London.Series B: Biological Sciences 268, 1575–1582.

Schmidt, K.L., Soma, K.K., 2008. Cortisol and corticosterone in the songbird immuneand nervous system: local vs. systemic levels during development. AmericanJournal of Physiology. Regulatory, Integrative and Comparative Physiology 295,R103–R110.

Schoech, S.J., 1996. The effect of supplemental food on body condition and thetiming of reproduction in a cooperative breeder, the Florida scrub-jay(Aphelocoma coerulescens). Condor 98, 234–244.

Schoech, S.J., Bowman, R., 2001. Variation in the timing of breeding in two FloridaScrub-Jay (Aphelocoma coerulescens) populations: do physiologic measuresreflect different environments? In: Marzluff, J.M., Bowman, R., Donnelly, R.(Eds.), Avian Ecology and Conservation in an Urbanizing World. KluwerAcademic Press, Norwell, Massachusetts, pp. 289–306.

Schoech, S.J., Bowman, R., 2003. Does differential access to protein influencedifferences in timing of breeding of Florida Scrub-Jays (Aphelocomacoerulescens) in suburban and wildland habitats? Auk 120, 1114–1127.

Schoech, S.J., Bowman, R., Reynolds, S.J., 2004. Food supplementation and possiblemechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocomacoerulescens). Hormones and Behavior 46, 565–573.

Schoech, S.J., Bowman, R., Bridge, E.S., Morgan, G.M., Rensel, M.A., Wilcoxen, T.E.,Boughton, R.K., 2007a. Corticosterone administration does not affect timing ofbreeding in Florida Scrub-Jays (Aphelocoma coerulescens). Hormones andBehavior 52, 191–196.

Schoech, S.J., Bowman, R., Bridge, E.S., Boughton, R.K., 2007b. Baseline and acutelevels of corticosterone in Florida Scrub-Jays (Aphelocoma coerulescens): effectsof food supplementation, suburban habitat, and year. General and ComparativeEndocrinology 154, 150–160.

Schoech, S.J., Bridge, E.S., Boughton, R.K., Reynolds, S.J., Atwell, J.W., Bowman, R.,2008. Food supplementation: a tool to increase reproductive output? A casestudy in the Threatened Florida Scrub-Jay. Biological Conservation 141, 162–173.

Schoech, S.J., Hahn, T.P., 2008. Latitude affects degree of advancement in laying bybirds in response to food supplementation: a meta-analysis. Oecologia 157,369–376.

Schoech, S.J., Mumme, R.L., Moore, M.C., 1991. Reproductive endocrinology andmechanisms of breeding inhibition in cooperatively breeding Florida scrub jays(Aphelocoma c. coerulescens). Condor 93, 354–364.

Schoech, S.J., Mumme, R.L., Wingfield, J.C., 1997. Breeding status, corticosterone,and body mass in the cooperatively breeding Florida scrub-jay (Aphelocomacoerulescens). Physiological Zoology 70, 68–73.

Schoech, S.J., Ketterson, E.D., Nolan Jr., V., 1999. Exogenous testosterone and theadrenocortical response in Dark-eyed Juncos. Auk 116, 64–72.

Sharp, P.J., Dunn, I.C., Waddington, D., 2008. Chicken leptin. General andComparative Endocrinology 158, 2–4.

Silverin, B., 1998. Behavioral and hormonal responses of the pied flycatcher toenvironmental stressors. Animal Behaviour 55, 1411–1420.

Smith, G.T., Wingfield, J.C., Veit, R.R., 1994. Adrenocortical response to stress in thecommon diving-petrel, Pelecanoides urinatrix. Physiological Zoology 67, 526–537.

Sorato, E., Kotrschal, K., 2006. Hormonal and behavioral symmetries between thesexes in the Northern bald ibis. General and Comparative Endocrinology 146,265–274.

Szyf, M., Weaver, I.C.G., Champagne, F.A., Diorio, J., Meaney, M.J., 2005. Maternalprogramming of steroid receptor expression and phenotype through DNAmethylation in the rat. Frontiers in Neuroendocrinology 26, 139–162.

Tena-Sempere, M., Barriero, M.L., Lage, M., Dieguez, C., Casanueva, F.F., 2007. Role ofleptin and ghrelin in the regulation of gonadal function. Expert Review ofEndocrinology and Metabolism 2, 239–249.

Ubuka, T., Ukena, K., Sharp, P.J., Bentley, G.E., Tsutsui, K., 2006. Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance bydecreasing gonadotropin synthesis and release in male quail. Endocrinology147, 1187–1194.

Walker, B.G., Boersma, P.D., Wingfield, J.C., 2006. Habituation of adult Magellanicpenguins to human visitation as expressed through behavior and corticosteronesecretion. Conservation Biology 20, 146–154.

Weaver, I.C.G., Meaney, M.J., Szyf, M., 2006. Maternal care effects on thehippocampal transcriptome and anxiety-mediated behaviors in the offspringthat are reversible in adulthood. Proceedings of the National Academy ofSciences of the United States of America 103, 3480–3485.

Weaver, I.C.G., Szyf, M., Meaney, M.J., 2002. From maternal care to gene expression:DNA methylation and the maternal programming of stress responses. EndocrineResearch 28, 699.

Wells, J.C.K., 2003. The thrifty phenotype hypothesis: thrifty offspring or thriftymother? Journal of Theoretical Biology 221, 143–161.

Wilson, F.E., Follett, B.K., 1975. Corticosterone-induced gonadosuppression inphotostimulated tree sparrows. Life Sciences 17, 1451–1456.

Wingfield, J.C., 1985a. Influences of weather on reproductive function in femalesong sparrows, Melospiza melodia. Journal of Zoology, London 205, 545–558.

Wingfield, J.C., 1985b. Short term changes in plasma levels of hormones duringestablishment and defense of a breeding territory in male song sparrows,Melospiza melodia. Hormones and Behavior 19, 174–187.

Wingfield, J.C., Deviche, P., Sharbaugh, S., Astheimer, L.B., Holberton, R., Suydam, R.,Hunt, K., 1994a. Seasonal changes of the adrenocortical responses to stress inredpolls, Acanthis flammea, in Alaska. Journal of Experimental Zoology 270,372–380.

Wingfield, J.C., Suydam, R., Hunt, K., 1994b. The adrenocortical responses to stress insnow buntings (Plectrophenax nivalis) and Lapland longspurs (Calcariuslapponicus) at Barrow, Alaska. Journal of Comparative Biochemical PhysiologyC 108, 299–306.

Wingfield, J.C., Farner, D.S., 1993. Endocrinology of reproduction in wild species. In:Farner, D.S., King, J.R., Parks, K.C. (Eds.), Avian Biology, Vol. IX. Academic Press,New York, pp. 163–327.

Wingfield, J.C., Hegner, R.E., Lewis, D., 1991. Circulating levels of luteinizinghormone and steroid hormones in relation to social status in the cooperativelybreeding white-browed sparrow weaver, Plocepasser mahali. Journal of Zoology,London 225, 43–58.

Wingfield, J.C., Vleck, C.M., Moore, M.C., 1992. Seasonal changes in adrenocorticalresponse to stress in birds of the Sonoran Desert. Journal of ExperimentalZoology 264, 419–428.

Woolfenden, G.E., Fitzpatrick, J.W., 1984. The Florida Scrub Jay: Demography of aCooperatively-Breeding Bird. Princeton University Press, Princeton, NJ.

Woolfenden, G.E., Fitzpatrick, J.W., 1990. Florida Scrub-Jays: a synopsis after 18years of study. In: Stacey, P.B., Koenig, W.D. (Eds.), Cooperative Breeding inBirds: Long-Term Studies of Ecology and Behavior. Cambridge University Press,New York, pp. 239–266.

Woolfenden, G.E., Fitzpatrick, J.W.. 1996. Florida Scrub Jay Aphelocoma coerulescens.In: Poole, A., Gill, F. (Eds.), The Birds of North America, No. 228. The Academy ofNatural Sciences, Philadelphia, PA, and the American Ornithologists’ Union,Washington, DC, pp. 1–28.

Young, A.J., in press. The causes of physiological suppression in vertebrate societies:a synthesis. In: Hager R., Jones, C.B. (Eds.), Reproductive Skew in VertebrateSocieties: Proximate and Ultimate Causes. Cambridge University Press,Cambridge.

Young, A.J., Carlson, A.A., Montfort, S.L., Russell, A.F., Bennett, N.C., Clutton-Brock, T.,2006. Stress and the suppression of subordinate reproduction in cooperativelybreeding meerkats. Proceedings of the National Academy of Sciences of theUnited States of America 103, 12005–12010.

Zhang, T.Y., Bagot, R., Parent, C., Nesbitt, C., Bredy, T.W., Caldji, C., Fish, E., Anisman,H., Szyf, M., Meaney, M.J., 2006. Maternal programming of defensive responsesthrough sustained effects on gene expression. Biological Psychology 73, 72–89.