General and Comparative Endocrinology xxx (2008) xxx–xxx

ARTICLE IN PRESS

Contents lists available at ScienceDirect

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 Depart ment of Biol ogy, Uni ver sity of Mem phis, 3774 Walker Ave nue, Mem phis, TN 38152, USAb Arch bold Bio log i cal Sta tion, 123 Main Drive, Venus, FL 33860, USA

a r t i c l e i n f o a b s t r a c t

Article history:

Received 5 August 2008

Revised 10 September 2008

Accepted 26 September 2008

Available online xxxx

Glu co cor ti coids medi ate glu cose avail abil ity under stress ful and non-stress ful con di tions and, there fore,

are essen tial for life. How ever, data across taxa dem on strate that chronic or ele vated secre tion of cor-

ti co ste rone or cor ti sol (CORT) can have neg a tive effects at many lev els and can trig ger phys i o log i cal or

behav ioral responses that may delay or, even halt repro duc tion. We pres ent a brief over view of the effects

that glu co cor ti coids, pri mar ily the avian form, cor ti co ste rone, can have on the repro duc tive axis. Con sid-

er able data have dem on strated that envi ron men tal per tur ba tions can result in ele vated CORT lev els that

alter a bird’s invest ment in cur rent repro duc tion. Stud ies in our lab o ra tory have shown a link between

CORT and tim ing of repro duc tion in Flor ida scrub-jays: in “bad” years, clutch ini ti a tion dates are pos i-

tively cor re lated with base line CORT lev els of female breed ers. Also, pop u la tion-level dif fer ences in CORT

lev els may explain tim ing of repro duc tion as lower CORT lev els in sub ur ban-dwell ing jays are cou pled

with early breed ing.

Most research on stress and CORT con cen trates on tran sient effects of CORT secre tion. How ever, devel-

op men tal CORT expo sure, either from the yolk or embryo, may have long-term effects upon adult phe-

no type. For exam ple, CORT lev els in nest ling scrub-jays pre dicts later ‘per son al ity,’ as lev els were highly

cor re lated (r2 = 0.84) with fear ful ness at 7 months of age. One can imag ine that such ‘per son al ity’ traits

might also trans late into dif fer en tial suc cess in gain ing a ter ri tory or a mate. While spec u la tive, it may be

that early CORT expo sure effec tively pro grams adult behav iors that have wide rang ing effects, includ ing

upon repro duc tion.

© 2008 Else vier Inc. All rights reserved.

Key words:

Cor ti co ste rone

Stress

Tim ing of breed ing

Envi ron men tal per tur ba tion

1. Intro duc tion

We have learned a con sid er able amount about the effects of

envi ron men tal per tur ba tions on the hy po thal amo–pitu i tary–adre-

nal (HPA) axis’ pro duc tion and secre tion of glu co cor ti coids over the

past sev eral decades. We have also gained insight into the means

by which glu co cor ti coids can neg a tively impact the repro duc tive

axis (hy po thal amo–pitu i tary–gonadal [HPG] axis) at multiple lev-

els (for review, see Breu ner et al., 2008). Despite our knowl edge of

these rela tion ships, rel a tively little is known about the inter ac tion

between envi ron ment, glu co cor ti coids, and tim ing of breed ing in

free-living ani mals. Although some stud ies pro vide insight into

this mat ter, most fail to track ani mals to the time when they repro-

duce, usu ally because exper i ments elu ci dat ing the mech a nisms

whereby glu co cor ti coids impact the cen tral ner vous sys tem (CNS)

or gonads neces si tate sac ri fic ing the ani mals.

Despite hav ing a myr iad of effects upon multiple sys tems, the

primary func tion of cor ti co ste rone (CORT), the primary avian glu-

co cor ti coid, is to facil i tate glu cose release for uti li za tion dur ing

0016-6480/$ - see front matter © 2008 Else vier Inc. All rights reserved.

doi:10.1016/j.ygcen.2008.09.009

Please cite this article in press as: Scho ech, S.J. et al., Environment, gluc

(2008), doi:10.1016/j.ygcen.2008.09.009

* Cor re spond ing author. Fax: +1 901 678 4746.

E-mail address: sscho ech@mem phis.edu (S.J. Schoech).

1 Pres ent address: Uni ver sity of Okla homa, Okla homa Bio log i cal Sur vey, 111 E.

Ches a peake, Nor man, OK 73019, USA.

var ied chal lenges. In response to an acute stressor, such as attack

by a pred a tor, the adre nal medulla releases epi neph rine (EPI) and

nor epi neph rine (NE) which facil i tate the ‘imme di ate’ response to

the stim u lus (e.g., increases of heart and res pi ra tion rates, glu cose

avail abil ity, and blood flow to mus cles used in the fight-or-flight

response). CORT is sub se quently released by the adre nal cor tex. If

the stim u lus is short-lived, there will be a tran si tory spike in CORT

lev els a few min utes after the stim u lus, though should the stim u lus

be sus tained, CORT lev els will remain ele vated for a con sid er able

time before return ing to pre-stress lev els upon adre nal exhaus tion,

neg a tive feed back of the CORT sig nal, or ces sa tion of the stim u lus.

Use of the cap ture stress par a digm of Wing field et al. (1992) has

dem on strated the nature of the CORT pro file for time peri ods that

vary from 30 to 180 min in a num ber of spe cies, although few stud-

ies pro long cap ture stress long enough to char ac ter ize the adre nal

exhaus tion phase. A num ber of fac tors may con trib ute to var i ance

among base line CORT lev els, the CORT response to a stressor, or

both. (1) Body mass is often inversely related to CORT lev els (Smith

et al., 1994; Scho ech et al., 1997, 1999). (2) CORT lev els of indi vid-

u als or pop u la tions often dif fer between-sea sons or life-his tory

stages (Goy mann et al., 2006; Sor a to and Ko trs chal, 2006; New man

et al. 2008). (3) Birds that live in severe envi ron ments in which the

oppor tu nity to re-nest, should a nest fail or be aban doned, often

ocorticoids, and the timing of reproduction..., Gen. Comp. Endocrinol.

2 S.J. Scho ech et al. / General and Comparative Endocrinology xxx (2008) xxx–xxx

ARTICLE IN PRESS

exhibit a damp ened CORT response dur ing the breed ing sea son

(e. g., Wing field et al., 1994a,b). (4) Sim i larly, birds with exper i-

men tally enlarged broods dis played damp ened CORT responses to

stress (Lend vai et al., 2007). (5) The length of the breed ing sea son

or lat i tude, two fac tors that are often inter-cor re lated, may affect

the HPA axis (see Goy mann et al., 2006).

In this paper, we first briefly review some of the evi dence that

glu co cor ti coids impinge on the avian HPG axis. Sub se quently, we

pres ent a bit of back ground on envi ron men tal effects upon the

HPA axis: a sec tion that will pro vide a ‘mini-review’ with exam-

ples of how an ani mal’s envi ron ment can stim u late the HPA axis.

Finally, we pres ent data on the inter ac tion between envi ron ment,

glu co cor ti coids, and repro duc tion in our study spe cies, the Flor ida

scrub-jay (Ap he lo co ma coe rules cens). Because this paper is based

upon an oral pre sen ta tion at the qua dren nial Inter na tional Sym po-

sium on Avian Endo cri nol ogy, the vast major ity of the exam ples we

con sider through out are avian. Thus, the glu co cor ti coid of inter est

is cor ti co ste rone (but see Schmidt and Soma, 2008), although in

mam ma lian sys tems it may be cor ti co ste rone, cor ti sol, or both.

1.1. Glu co cor ti coid effects on the avian HPG axis

One of the first avian stud ies to exper i men tally link CORT

with the repro duc tive axis was con ducted by Wil son and Fol lett

(1975) who implanted CORT within the basal hypo thal a mus of

tree spar rows (Spiz el la ar bo rea) and found a marked reduc tion in

both plasma lutein iz ing hor mone (LH) lev els and gonadal growth

rates. Some what par a dox i cally, tree spar rows that received CORT

implants in the field failed to express neg a tive effects upon lev els

of repro duc tive hor mones (e.g., tes tos ter one, T; dihy dro tes tos ter-

one, DHT; and LH: Ast hei mer et al., 2000). Subsequent research has

shown that CORT not only acts via numer ous cen tral sites to down-

reg u late the gon a do tro pin-releas ing hor mone (GnRH) sys tem, but

CORT bind ing sites within the gonad facil i tate down-reg u la tion of

enzy matic sys tems that reg u late T pro duc tion, as well as increase

the like li hood of Ley dig cell apop to sis (Moore and Zo el ler, 1985;

review in Wing field and Far ner, 1993). Sal van tes and Wil liams

(2003) admin is tered exog e nous CORT to female zebra finches and

found (1) decreased vitel lo genin pro duc tion, (2) decreased num-

ber of pairs ini ti at ing repro duc tion (56% vs. 100% of con trols), and

(3) for those CORT-treated females that did lay, an 8-day delay in

clutch ini ti a tion.

Gon a do tro pin-inhib it ing hor mone (GnIH), a recently dis cov-

ered pep tide that plays a role in down-reg u la tion of the HPG axis

(Bent ley et al., 2006; Ubuka et al., 2006; Grei ves et al., 2008), may

medi ate CORT’s effects upon the GnRH sys tem. Cal is i et al. (2008)

exposed house spar rows to a stan dard 1 h cap ture and han dling

stress pro to col and found that these birds had sig nifi cantly more

cells that expressed GnIH immu no re ac tiv ity within the para ven-

tric u lar nucleus (PVN) than did unstressed con trol birds. Con sis-

tent with an anti-gonadal and anti-repro duc tion role for GnIH in

this instance is their find ing that there was no effect dur ing the

fall when all birds had rel a tively high num bers of cells express-

ing GnIH immu no re ac tiv ity. Although work is ongo ing to iso late

CORT recep tors on GnIH cells in birds (Cal is i, per sonal com mu ni-

ca tion), to date recep tors have been iden ti fied on GnIH neu rons of

rats (Kir by et al., 2007).

1.2. Envi ron men tal effects on glu co cor ti coid secre tion

Wing field (1985a) first pub lished an exam ple of an envi ron-

men tal per tur ba tion that was directly linked to increased plasma

CORT lev els in a study of song spar rows (Me losp iza melo dia). A late

spring snow storm led to mark edly increased plasma CORT lev els

along with decreased estra diol lev els in females. While CORT lev-

els returned to pre-storm lev els within a week and a half, plasma

Please cite this article in press as: Scho ech, S.J. et al., Environment, gluco

(2008), doi:10.1016/j.ygcen.2008.09.009

estra diol remained depressed for con sid er ably longer and, when

com pared to the pre vi ous year, the mean lay date was delayed by

1 week. It is likely that the snow cover led to decreased food avail-

abil ity which drove the CORT increase, as food restric tion gen er-

ally results in ele vated CORT lev els (Har vey et al., 1980; Lynn et al.,

2003). Given the above evi dence of direct effects of CORT upon the

HPG axis, it seems likely that the increased CORT lev els were a key

fac tor in the decreased estra diol lev els and delayed breed ing in the

Wing field (1985a) study. How ever, one can not rule out cen tral or

periph e ral effects that may be med i ated by other endo crine or neu-

ro crine secre tions. There has been a reg u lar pro ces sion of newly

dis cov ered met a bolic hor mones for which a full range of func tions

is only revealed some time after the ini tial char ac ter iza tion. For

instance, there is some evi dence that ghre lin and lep tin (which

may not exist in birds, see Sharp et al., 2008), in addi tion to their

roles in food intake and metab o lism, mod ify repro duc tive func-

tion. Tena-Sem pere et al. (2007) posit that these two hor mones,

as well as numer ous other neu ro pep tides of cen tral or periph e ral

ori gin (see Grei ves et al., 2008), “may jointly coop er ate to mod u-

late a wide set of repro duc tive func tions, thereby con trib ut ing to

the phys i o logic inte gra tion of energy bal ance and repro duc tion.”

These ideas are based pri mar ily upon mam ma lian stud ies and it

must be noted that study of these and other pep tides that have

been impli cated in mam ma lian repro duc tion is some what lag ging

in birds.

While most think of cli matic events when con sid er ing envi ron-

ment, in the broad est sense an ani mal’s envi ron ment encom passes

far more than just weather. For exam ple, sev eral stud ies have doc-

u mented that the pres ence of a pred a tor can affect plasma CORT

lev els. Silv er in (1998) found that pied fly catcher males (Fice du la

hyp ol eu ca) exposed to a live-mount of a weasel dur ing the nest

build ing period had ele vated lev els of CORT fol low ing 10 min of

expo sure. Sim i larly, great tits (Pa rus major) in an avi ary that were

exposed to a stuffed owl responded with ele vated CORT lev els

(Coc krem and Silv er in, 2002). In the same pub li ca tion, CORT lev els

in free-living tits so treated exhib ited a trend toward an increase.

In an obser va tional study, male trop i cal ston ech ats (Saxi co la tor qu-

at a ax il lar is) whose ter ri to ries were shared with pred a tory fis cal

shrikes (La nius col lar is) had ele vated base line CORT lev els, sug gest-

ing chronic stress (Sche uer lein et al., 2001). Although a direct link

between CORT and repro duc tion was not estab lished, the research-

ers note that stone chat pairs shar ing their ter ri tory with shrikes

delay ini ti at ing, and are less likely to ini ti ate, a sec ond clutch than

are nearby birds with out shrikes.

Inter ac tions with con spe cifi cs can also be ‘stress ful.’ Sim u lated

ter ri to rial intru sions (STI), in which either a live or a stuffed bird

is pre sented to a ter ri tory holder along with con spe cific song play-

back, are valu able in elu ci dat ing the nature of the tes tos ter one

response to a per ceived con spe cific chal lenge (Wing field, 1985b).

How ever, in some spe cies this pro to col has been found to result

in ele vated lev els of CORT. Male pied fly catch ers responded to a

ter ri to rial intru sion by ele vat ing both T and CORT lev els (Silv er in,

1998). In con trast, blue tits (Cy an istes caeru le us) responded to STIs

with ele vated CORT lev els while exhib it ing decreased T lev els

(Lan dys et al., 2007). Fur ther, Lan dys et al. (2007) used a meta-

anal y sis of the stud ies to date that have used STIs and found that

sin gle-brooded spe cies, like the blue tit, con sis tently ele vate CORT

while exhib it ing either no change or decreased T lev els.

The social inter ac tions that are a part of an ani mal’s envi ron-

ment are not lim ited to those com ing from outside of the social

group. For instance, Ange lier et al. (2007) note that in newly formed

pairs of black-leg ged kit tiwa kes (Ris sa tri dac tyla), both males and

females had higher base line CORT lev els than estab lished pairs,

perhaps result ing from poor cohe sion in shared duties or gen-

eral anx i ety with a new mate. Re mage-Hea ley et al. (2003) noted

sim i lar pat terns in a study with cap tive zebra finches (Ta e ni o py-

corticoids, and the timing of reproduction..., Gen. Comp. Endocrinol.

S.J. Scho ech et al. / General and Comparative Endocrinology xxx (2008) xxx–xxx 3

ARTICLE IN PRESS

gia gut ta ta). Of spe cial inter est to our research group are stud ies

of social groups, spe cifi cally coop er a tive breed ers and espe cially

those spe cies for which there is only one breed ing pair in a group.

To explain repro duc tive qui es cence, it has been pos tu lated that the

non breeder help ers in a group, which are invari ably sub or di nate

to the breed ers, are ‘psy cho log i cally cas trated’ (see Brown, 1978).

This hypoth e sis pre dicts that nonb ree ders are repro duc tively sup-

pressed through dom i nant/sub or di nate inter ac tions that act to

ele vate CORT lev els, thereby down-reg u lat ing HPG axis func tion.

Of the too few stud ies that have addressed this issue in avian

coop er a tive breed ers, there is little evi dence to sug gest that this

hypoth e sis has merit (Scho ech et al., 1991, 1997; Mays et al., 1991;

Wing field et al., 1991; but see Ru ben stein, 2007). How ever, this is a

com mon and recur ring theme in coop er a tively breed ing mam mals

in which it is not uncom mon to find repro duc tive skew enforced

via active social sup pres sion accom pa nied with increased lev els of

CORT and decreased HPG axis func tion of help ers (see Young et al.,

2006; Young, in press and cita tions within).

1.3. Humans and their effects upon the envi ron ment

An increas ingly prom i nent ele ment of all spe cies’ envi ron ment

is human pres ence and activ ity. The influ ence of humans can range

from indi rect effects, such as expo sure to con tam i nants, which may

alter HPA axis func tion, to occa sional direct con tact with humans,

to con sis tent “cohab i ta tion.” There is con sid er able evi dence that

all of the above types of encoun ter can be ‘stress ful.’ For exam-

ple, blood lev els of lead in nest ling white storks (Ci co nia ci co nia)

were pos i tively cor re lated with max i mal CORT lev els (Baos et al.,

2006). Par a dox i cally, over all high est lev els were found in the ref-

er ence pop u la tion rather than in the con tam i nant-exposed col ony.

Sev eral research ers have exam ined the effects of human vis i ta tion

at pen guin col o nies with find ings that vary by spe cies. Mag el lanic

pen guins (Sphe nis cus mag ell an i cus) in tour ist areas exhibit a damp-

ened respon sive ness to stress, sug gest ing habit u a tion (Walker et

al., 2006). Con versely, yel low-eyed pen guins (Meg a dyp tes antip o-

des) appear to be sen si tized to tour ists as birds in tour ist areas have

higher stress-induced CORT lev els and lower repro duc tive suc cess

than birds rarely vis ited (El len berg et al., 2007).

Although many avian spe cies can not coex ist with humans and

rap idly dis ap pear as we encroach on their hab i tat, there are a

num ber of spe cies that seem ingly thrive in cit ies; e.g., house spar-

rows (Passer do mes ti cus) and Euro pean star lings (Stur nus vul ga ris).

While there is a grow ing inter est in urban ecol ogy and demog ra-

phy (see Marz luff et al., 2001), there have been few inves ti ga tions

into the stress phys i ol ogy asso ci ated with urban life. Com par i sons

of city (Munich) and nearby for est-dwell ing Euro pean black birds

(Tur dus mer u la) found that the former had func tional gonads from

3 (males) to 4 (females) weeks ear lier than birds in nat u ral hab i tat

(Parte cke et al., 2005). A fol low-up study with hand-reared birds

found that city birds also had a damp ened CORT response to cap-

ture and han dling (Parte cke et al., 2006). The authors inter pret this

find ing as a micro-evo lu tion ary change allow ing urban-dwell ing

birds to cope with a stress ful envi ron ment. Con versely, Bon ier et al.

(2007) found that male white-crowned spar rows (Zonotrichia leu-

coph rys), but not females, in cit ies had higher base line CORT than

con spe cifi cs in nat u ral hab i tat.

Our study group has exam ined numer ous envi ron men tal vari-

ables to address our obser va tion that Flor ida scrub-jays in a sub-

ur ban devel op ment con sis tently breed ear lier than jays in nat u ral

hab i tat at nearby (10 km) Arch bold Bio log i cal Sta tion (ABS) (Scho-

ech and Bow man, 2001, 2003). Sub ur ban jays’ base line CORT lev-

els are less than one half those of ‘wild land’ jays (2.16 ± 0.28 vs.

4.81 ± 0.33 ng/ml), and Scho ech et al. (2004) spec u late that the

higher CORT in the wild lands might act as a ‘brake’ on the HPG

axis, thereby offer ing a partial expla na tion for their later breed ing.

Please cite this article in press as: Scho ech, S.J. et al., Environment, gluco

(2008), doi:10.1016/j.ygcen.2008.09.009

How ever, a fol low-up study in which wild land jays received exog-

e nous CORT failed to sup port this expla na tion as CORT-dosed birds

did not delay clutch ini ti a tion (Scho ech et al., 2007a). It should be

noted that the CORT doses admin is tered increased CORT lev els

mark edly over the short-term (rep re sen ta tive of an “acute” stress

response), thus fail ing to chron i cally ele vate CORT and con found-

ing inter pre ta tion. Subsequent research to deter mine whether the

low lev els in sub ur ban jays reflected habit u a tion or a com pro mised

HPA axis due to chem i cal con tam i nant expo sure sug gests that nei-

ther of these pos tu lated under ly ing causes has merit, as there was

no between-pop u la tion dif fer ence in the CORT response to cap-

ture stress, whereas both pre dict a damp ened CORT response to a

stressor (Scho ech et al., 2007b). Inter est ingly, sub ur ban jays tended

to have a more robust response as was indi cated by a more rapid

rate of increase over the ini tial 5 min of cap ture.

1.4. Manip u lat ing the envi ron ment with sup ple men tal food: les sons

from Flor ida scrub-jays

In the deci sion to repro duce, resource avail abil ity in the form of

food can oper ate at both the prox i mate and ulti mate lev els (Lack,

1968; Per rins, 1970): food sup ple men ta tion stud ies have been used

to address ques tions across lev els (see Scho ech and Hahn, 2008;

Scho ech et al., 2008 and cita tions within). Con cep tu ally, such a

tech nique can be viewed as a method of alter ing an ani mal’s envi-

ron ment. In a series of exper i ments begin ning in 1993, Scho ech

and col leagues have used food sup ple men ta tion of coop er a tively

breed ing Flor ida scrub-jays to inves ti gate both the phys i o log i cal

mech a nisms link ing food avail abil ity and tim ing of repro duc tion

(Scho ech, 1996; Scho ech and Bow man, 2001, 2003; Scho ech et al.,

2004, 2007a,b) as well as whether there are fit ness ben e fits (Scho-

ech et al., 2008).

Food sup ple mented Flor ida scrub-jays invari ably advance lay-

ing, although the degree is less ened in ‘good’ years and increased

in ‘bad’ years (see Rey nolds et al., 2003; Scho ech et al., 2007b,

2008; see below). In some years, jays pro vided with high qual ity

sup ple men tal food (i.e., high in fat and pro tein) not only advanced

lay ing, but had lower base line CORT lev els than con trol jays and

birds that were pro vided a high fat but low pro tein sup ple ment

(Scho ech et al., 2004). How ever, whether or not food sup ple men ta-

tion affects plasma CORT lev els also appears to vary between years,

assum edly with vary ing con di tions and resource avail abil ity (see

Scho ech et al., 2007b). Although defin i tively link ing envi ron men tal

con di tions, plasma CORT, and tim ing of repro duc tion in this spe-

cies is dif cult (in part due to its threatened sta tus that rules out

some manip u la tive study), the responses to sup ple men tal food

and the nat u ral var i a tion in these three vari ables addressed below

are sug ges tive of causal links.

Over the last 8 years (2001–2008), we have tracked all of the

demo graphic aspects of the study pop u la tion of Flor ida scrub-jays

that occupy the south ern part of ABS, and col lected hun dreds of

blood sam ples from which we’ve deter mined base line lev els of

CORT. For all jays in our pop u la tion, we: (1) track fates from the egg

through death; (2) deter mine sex, sta tus (breeder or non-breed-

ing helper), and age; (3) locate all nests and deter mine lay ing and

hatch ing dates and order, as well as fledg ing dates; and (4) mon i tor

sur vi vor ship to inde pen dence (»70 days post-hatch) and beyond,

includ ing recruit ment into the breed ing pop u la tion. Jays were

trapped in con tin u ously mon i tored Potter traps, thereby assur ing

that an ini tial blood sam ple to mea sure base line CORT was col-

lected within 2–3 min (see Scho ech et al., 1991, 1997, 1999; Ro mer o

and Ro mer o, 2002). Sam ples were later assayed in the Scho ech lab

at the Uni ver sity of Mem phis. While we con ducted food sup ple-

men ta tion stud ies dur ing this period, the find ings pre sented here

are only for non-sup ple mented jays, although some indi vid u als

may have been sup ple mented in pre vi ous years.

corticoids, and the timing of reproduction..., Gen. Comp. Endocrinol.

4 S.J. Scho ech et al. / General and Comparative Endocrinology xxx (2008) xxx–xxx

ARTICLE IN PRESS

Fig. 1. First clutch ini ti a tion date for each of the 8 years of the study. Data are shown

as means ± SEM. Num bers in paren the ses rep re sent sam ple size fol lowed by the

mean num ber of young per ter ri tory that reached nutri tional inde pen dence at

approx i mately 70 days-of-age.

Fig. 2. Base line cor ti co ste rone lev els of female breed ers plot ted against the day of

the year that a given female ini ti ated her clutch. Sam ples are depicted by year-class:

closed cir cles rep re sent data from ‘bad’ years (long-dash best fit line), open cir cles

rep re sent data from ‘aver age’ years (short-dash best fit line), and closed tri an gles

rep re sent data from ‘good’ years (dot ted best fit line). Cat e go ri za tion of year-clas ses

is defined in the text.

Mean clutch ini ti a tion dates between years var ied by 9 days

dur ing this time (Fig. 1), a sur pris ingly small var i ance based upon

long-term mon i tor ing that has doc u mented inter-year var i ance in

lay dates of approx i mately 1 month (Scho ech, 1996). As is implied

above and as lay dates sug gest, not all years are equal and gen er-

ally, ear lier breed ing occurs in ‘good’ years that are also char ac-

ter ized by high off spring pro duc tiv ity. Con versely, ‘bad’ years are

char ac ter ized by later breed ing and lower pro duc tiv ity. The mean

num ber of young to reach inde pen dence dur ing the study ranged

from 0.3 to 1.0 indi vid ual per group with an over all mean of 0.58

young. How ever, in some years there is a degree of dis con nect

from this gen eral tru ism and tim ing of breed ing does not lin e arly

pre dict pro duc tiv ity. There fore we used lay date and num ber of

inde pen dent young pro duced for each of the 8 years in a prin ci pal

com po nents anal y sis: PC1 explained 81.3% of the var i ance. Based

upon PC1, years were ranked and assigned as good (PC1 < ¡1.0:

2002 and 2008), aver age (¡1.0 > PC1 < 1.0: 2003, 2004, 2005, and

2006), and bad (PC1 > 1.0: 2001 and 2007).

To exam ine the asso ci a tion between base line CORT and year

qual ity, we used an ANCOVA with year-class (good, aver age, or

bad), sex, and repro duc tive sta tus (breeder or non breed ing helper)

as fac tors and date of sam ple col lec tion as a covar i ate. All sam ples

were col lected dur ing the pre breed ing period, thereby allow ing

us to assess CORT lev els when the deci sions of when to ini ti ate a

clutch are made. Only year-class explained CORT lev els (F2,236 = 3.24,

P = 0.04). Nei ther sex (F1,236 = 0.09, P = 0.76), sta tus (F1,236 = 0.46,

P = 0.50), date (F1,236 = 1.06, P = 0.31), nor any of the inter ac tion

terms approached sta tis ti cal sig nifi cance. We reran the anal y sis

with non-sig nifi cant terms removed and found the sta tis ti cal rela-

tion ship between year-class and base line CORT was strength ened

(ANOVA; F2,250 = 4.66, P = 0.01). Bon fer ron i-cor rected pair wise com-

par i sons found that CORT lev els in bad years (4.94 ± 0.46 ng/ml)

were higher than dur ing aver age years (3.38 ± 0.25 ng/ml: P = 0.01),

though lev els dur ing good years (4.42 ± 0.71 ng/ml) did not dif fer

from either of the other two cat e go ries.

Although our ini tial anal y sis noted no dif fer ences by sex or

breed ing sta tus, because the breed ing female is almost cer tainly

the “decider” of when or if to ini ti ate a clutch, we fur ther exam-

ined the rela tion ship between base line CORT lev els and lay dates in

breeder females. When all data were col lapsed across years, there

was a sig nifi cant rela tion ship between base line CORT and first

clutch ini ti a tion date (regres sion: F1,74 = 4.13, p = 0.046), although

CORT explained only 5.3% of the var i ance. We fur ther exam ined

Please cite this article in press as: Scho ech, S.J. et al., Environment, gluc

(2008), doi:10.1016/j.ygcen.2008.09.009

this rela tion ship by each of the 3-year-clas ses and found that the

over all sig nifi cance is likely due to the rel a tively strong pre dic tive

value of CORT on lay date dur ing bad years (F1,22 = 10.44, p = 0.004,

r2 = 0.32; see Fig. 2). How ever, there was no rela tion ship between

these two vari ables in either aver age (F1,32 = 1.40, p = 0.25, r2 = 0.04)

or good years (F1,16 = 1.31, p = 0.27, r2 = 0.08).

These find ings offer some sup port for the hypoth e sis that envi-

ron men tal con di tions affect plasma CORT lev els which in turn

may influ ence the tim ing of repro duc tion. While our data do not

over whelm ingly sup port this hypoth e sis, the some what ele vated

base line CORT dur ing bad years and the rel a tively strong rela tion-

ship between these lev els and lay date are intrigu ing. What spe cif-

i cally made the 2 years, 2001 and 2007, bad years? As noted above,

pro duc tiv ity usu ally decreases with increas ing lay date, though

a mean delay of just a few days, as is the case for these 2 years,

would not be expected to make a substantial dif fer ence. Scho ech

(1996) noted that the excep tion ably late and poor breed ing sea son

of 1992 was pre saged by very little rain fall (Novem ber–Jan u ary).

Sim i larly, whereas the mean rain fall of the 6 years des ig nated as

good and aver age was 13.9 cm for this same 3-month period, it was

2.24 and 6.78 cm for 2001 and 2007, respec tively. Too little rain fall

dur ing this period could have pro found effects upon resource avail-

abil ity as drought con di tions lead to poor new plant growth which

can neg a tively affect the abun dance of the arthro pod and ver te-

brate prey that scrub-jays reg u larly take. Fur ther, Flor ida scrub-

jays rely on acorn caches dur ing the win ter and early spring when

other food sources are scarce (DeG ange et al., 1989) and the acorn

mast dur ing the late sum mer and fall of 2006 (which impacts the

subsequent breed ing sea son) was excep tion ally poor. Based upon

a long-term annual acorn count at ABS, acorn abun dance in 2006

was approx i mately one fifth of the long-term aver age (Bow man,

unpub lished data). Given the asso ci a tion between CORT secre tion

and nutri tional state, we pos tu late that poor resource avail abil ity

in bad years results in ton i cally, albeit mildly, ele vated CORT lev els

that, in turn, influ ence the tim ing of repro duc tion. These results

empha size the util ity of long-term stud ies in uncov er ing rela tion-

ships between envi ron men tal fac tors, breed ing, and phys i ol ogy.

Indeed, a study con ducted over only 1–2 years would likely miss

such a rela tion ship and, thereby con clude that there was no rela-

tion ship between CORT and tim ing of repro duc tion.

ocorticoids, and the timing of reproduction..., Gen. Comp. Endocrinol.

S.J. Scho ech et al. / General and Comparative Endocrinology xxx (2008) xxx–xxx 5

ARTICLE IN PRESS

Fig. 3. Base line cor ti co ste rone lev els (power trans formed data, see Scho ech et al.,

2007b) of day 11 nes tlings plot ted against indi vid u als’ over all fear ful ness rank ing at

approx i mately 7 months of age. Lower ranks are bolder than higher ranks. Shared

sym bols rep re sent indi vid u als that are sib lings.

1.5. ‘Orga ni za tional’ effects of CORT

The orga ni za tional–ac ti va tion al dichot omy of hor mone

actions has elu ci dated how hor mones can shape an organ ism’s

phys i o log i cal and behav ioral responses (Phoe nix et al., 1959; Goy

and Phoe nix, 1972; Arnold and Breed love, 1985; Moore, 1991).

Devel op men tal effects of hor mones are usu ally con sid ered with

ref er ence to sex ste roids. How ever, it has long been known that

devel op ing male embryos of moth ers that are stressed dur ing

preg nancy are some what fem i nized, with a num ber of male-typ-

i cal behav ior pat terns affected upon reach ing adult hood (Nel son,

2005). Sim i larly, post-natal paren tal care can have crit i cal effects

on off spring devel op ment that can influ ence an indi vid ual’s

adult phe no type and per son al ity (Mea ney, 2001; Kim and Dia-

mond, 2002; Re pet ti et al., 2002; Dinge manse et al., 2004; Zhang

et al., 2006). For exam ple, in rats, off spring reared by more atten-

tive dams dis played more explor atory behav ior and recov ered

more rap idly fol low ing expo sure to a stressor (Liu et al., 1997;

Weaver et al., 2002; Szyf et al., 2005). Con versely, off spring from

less atten tive moth ers were more fear ful and had greater stress

responses (i.e., increased lev els of ACTH and CORT). Weaver et al.

(2006) found that the “high-stress” devel op men tal path way in

rats was estab lished early in life by deac ti va tion of DNA regions

that encode glu co cor ti coid recep tors, thereby affect ing adult

responses to stress ors. Thus, dif fer ences in mater nal care can

direct a per ma nent change in DNA expres sion that can shape an

indi vid ual’s per son al ity by for ever alter ing how it responds to

envi ron men tal chal lenges.

Sim i lar links between devel op men tal stress and adult phe no-

type have been observed in birds. For exam ple, in black-leg ged

kit tiwa kes, nutri tional stress dur ing devel op ment results in cog-

ni tively and phys i o log i cally com pro mised adults (Ki tay sky et al.,

2006). Also, western scrub-jays (Ap he lo co ma cal i for ni ca), a Flor-

ida scrub-jay con ge ner, that were food-restricted as nes tlings had

higher base line CORT lev els and more pro nounced stress responses

at 1year-of-age than ad libi tum fed con trols (Prav osudov and Ki tay-

sky, 2006). Sev eral recent stud ies of pas ser ine and non-pas ser ine

spe cies have noted links between phe no type (e.g., ‘per son al ity’ and

stress respon sive ness) and CORT expo sure (dur ing devel op ment or

as an adult) that par al lel those found in the above described mam-

ma lian research (e.g., Euro pean star ling, Love and Wil liams, 2008;

great tit, Ca re re et al., 2003; Jap a nese quail [Co tur nix co tur nix];

Hay ward and Wing field, 2004; and see Coc krem, 2007 for a review

that cov ers sev eral spe cies).

It has been hypoth e sized that such ‘pro gram ming’ of an indi-

vid ual’s phe no type is adap tive, and that in a fluc tu at ing envi ron-

ment, there is no sin gle opti mal phe no type. The qual ity or quan-

tity of paren tal care, there fore, may serve as a sig nal that directs

off spring devel op ment down the path that best ensures sur vival

dur ing the vul ner a ble, early stages of life (for review, see Ko o lhaas

et al., 1999; Wells, 2003; Zhang et al., 2006). For exam ple, in harsh

con di tions, a high-CORT phe no type may increase an indi vid ual’s

chances of sur viv ing, espe cially if fear ful ness trans lates into anti-

pred a tor behav ior and if the abil ity to metab o lize stored nutri ents

(facil i tated through CORT secre tion) is at a premium.

We rea soned that var i ance in per son al ity, pri mar ily bold ness

or timid ity, could have a strong effect on the like li hood that an

indi vid ual gains a breed ing ter ri tory or a mate. In Flor ida scrub-

jays there is con sid er able var i ance in the time that a young bird

remains as a helper in its natal ter ri tory before becom ing a breeder

(see Wool fen den and Fitz pa trick, 1984, 1990, 1996). An excit-

ing new line of research from our group addresses the rela tion-

ship between a nest ling’s envi ron ment, its CORT lev els, and adult

phe no type; and although it is too early to empir i cally deter mine

impacts on the tim ing of breed ing, we pres ent these find ings as an

illus tra tion of the orga ni za tional effects of CORT.

Please cite this article in press as: Scho ech, S.J. et al., Environment, gluco

(2008), doi:10.1016/j.ygcen.2008.09.009

All nes tlings are banded, mea sured (mass and lin ear size mea-

sures), and a small blood sam ple is col lected on day 11 post-hatch.

Each nest ling is removed from the nest, bled within 3 min, and

mea sured before being returned to the nest; the pro ce dure is then

repeated for each subsequent nest ling. This allows base line CORT

lev els of nes tlings to be mea sured (the HPA axis of 11-day-old nes-

tlings is capa ble of mount ing a stress response, Ren sel and Bough-

ton, unpub lished data). In the bad year of 2007 (see above), of the

55 nes tlings banded and sam pled at day 11 only 17 sur vived to

inde pen dence.

We con ducted three behav ioral tests on 10 of the 17 sur vi vors

when they were approx i mately 7 months of age. Prior to test ing,

the ‘naive’ young were trained to come to a pile of pea nuts and, as

is their wont; once jays dis cover pea nuts they return to the source

until it’s depleted, eat ing until sati ated and cach ing the rest. The

tests exploited this trait and were video-taped to facil i tate indi vid-

ual iden ti fi ca tion and accu rate time keep ing. Test 1, the ring test,

used a bright orange ring 50 cm in diam e ter and 3 cm high which

was placed around a peanut pile; the time a jay spent within 1 m

of the ring before cross ing to take a peanut was then mea sured.

For tests 2 and 3, a hid den buzzer beneath the pile or a mov ing leaf

attached to a hid den motor within the pile, respec tively, star tled

sub jects; return times were then assessed. The ring test yielded

hes i tancy times that ranged from 2 to 192 s; how ever, two of the

10 birds failed to cross the ring dur ing the 1 h allot ted test period.

For the sound and motion tests, return times ranged from 1 to 57 s

and 10 s to 32 min, respec tively.

Because the times to com plete the test were not nor mally dis-

trib uted, for each test birds were ranked from one to 10 (note, the

two birds that did not return to cross the ring shared a score of

nine) with the low est rank cor re spond ing to the short est time

(i.e., the least fear ful indi vid ual). An indi vid ual’s three ranks were

summed and this total was used to gen er ate an over all fear ful-

ness rank across the 10 test jays. To test the degree to which early

CORT expo sure influ enced the jays’ ‘per son al ity,’ we regressed the

over all fear ful ness rank against nest ling CORT lev els and found an

extremely strong rela tion ship (F1,8 = 41.48, p < 0.001, r2 = 0.84; Fig.

3). Fur ther, seven of the tested jays sur vived the remain der of the

win ter and were again tested with the ring test at 1 year of age. We

found that this mea sure of fear ful ness tended to per sist (r = 0.68,

p = 0.066, n = 7). While the small sam ple sizes ren der draw ing gen-

eral con clu sions prob lem atic, we also observed indi ca tions of per-

sis tence in stress phys i ol ogy. For exam ple, (1) base line CORT lev els

corticoids, and the timing of reproduction..., Gen. Comp. Endocrinol.

6 S.J. Scho ech et al. / General and Comparative Endocrinology xxx (2008) xxx–xxx

ARTICLE IN PRESS

of 11-day-old nes tlings tended to be cor re lated with lev els at 2.5

months (r = 0.64, p = 0.12, n = 7); (2) as were base line CORT lev els at

approx i mately 2.5 months and 1 year (r = 0.72, p = 0.069, n = 7); and

(3) as were max i mum CORT lev els at approx i mately 2.5 months

and 1 year (r = 0.81, p = 0.052, n = 6). We look for ward to gath er ing

fur ther data to deter mine whether these trends per sist.

2. Con clu sions

We have pre sented a brief over view of how the envi ron men tal

con di tions an ani mal expe ri ences can affect its CORT lev els and, in

some cases how this can then play a role in deter min ing the tim ing

of repro duc tion. While there is con sid er able evi dence link ing the

envi ron ment and CORT and CORT and the repro duc tive axis, there

are fewer stud ies that inte grate these three vari ables. Regard less,

it seems clear that ele vated CORT lev els in response to a pleth ora

of envi ron men tal con di tions can slow the up-reg u la tion of the

HPG axis, thereby delay ing the onset of repro duc tion. How ever, it

is equally clear that CORT lev els are not the sole deter mi nant of

when the onset of repro duc tion occurs.

Acknowl edg ments

S.J.S. thanks John Coc krem, Pierre De vi che, and Wolf gang Goy-

mann for invit ing him to speak in the Ecol ogy and Evo lu tion sym po-

sium they con vened at the July 2008 Inter na tional Sym po sium on

Avian Endo cri nol ogy in Leu ven, Bel gium: this paper is based upon

S.J.S.’s talk at that meet ing. Dur ing the col lec tion of data described

herein, we were par tially sup ported by NSF fund ing to S.J.S. (IBN-

9983201 and IOS-0346328). M.A.R. has also been funded in part by

Sigma Xi, the Amer i can Orni thol o gists’ Union, and the Depart ment

of Biol ogy at the Uni ver sity of Mem phis: the lat ter has pro vided

sup port for all of the co-authors. Spe cial thanks to S. James Rey-

nolds and Gina Mor gan for help with data col lec tion and multiple

aspects of the jay pro ject. Fur ther assis tance in the field came from

Jon a than At well, Tim Har ri son, and numer ous field assis tants. The

research was greatly aided by S.J.S.’ col lab o ra tion with R. Bow man

at ABS. We thank Dave Free man for help ful com ments on an ear lier

draft of this paper.

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