Handling during pregnancy in the blue fox (Alopex lagopus):
the inﬂuence on the fetal gonadal function
Ludmila V. Osadchuk,
Bjarne O. Braastad,
and Morten Bakken
Institute of Cytology and Genetics, Siberian Department of the Russian Academy of Sciences, Novosibirsk, 630090 Russia
Department of Animal Science, Agricultural University of Norway, P.O. Box 5025, N-1432
Received 30 September 2002
In previous studies it has been shown that handling produced stress in pregnant blue fox vixens increasing plasma level and
adrenal in vitro production of cortisol. Moreover, this treatment increased plasma cortisol levels in the fetuses. The present study
was designed to examine eﬀects of a 1-min daily handling stress applied to pregnant blue fox vixens on fetal gonadal steroidogenesis.
Plasma concentrations of oestradiol and testosterone, gonadal content and gonadal in vitro production of these steroids, and re-
sponse to exogenous hCG as well as gonadal weights, and anogenital distances were measured in control (C, n ¼ 69) and stressed (S,
n ¼ 54) fetuses on 47–48 days of pregnancy. Maternal stress induced a suppression of gonadal steroidogenesis in the fetuses. The
decreased testosterone content in the testes and oestradiol content in the ovaries were demonstrated in stressed fetuses compared
with control (testosterone: 4:91 Æ 0:46 vs. 7:35 Æ 0:87 ng/both testes, P < 0:05; oestradiol: 29:1 Æ 3:4 vs. 46:5 Æ 4:9 ng/both ovaries,
P < 0:05). The ovarian oestradiol in vitro production in female fetuses from stressed mothers was decreased in comparison with
control (3:69 Æ 0:39 vs. 7:52 Æ 1:51 pg/ovary/h, P < 0:05). The same diﬀerence was observed between stressed and control male
fetuses in the testosterone testicular response to hCG (5:34 Æ 0:64 vs. 8:73 Æ 0:40 ng/testis/h, P < 0:05). The ovarian weight from
stressed fetuses was lower in comparison with control (12:9 Æ 0:7 vs. 16:8 Æ 0:6 mg, P < 0:05). The anogenital distance in female
fetuses from stressed vixens was also reduced (0:6 Æ 0:03 vs. 0:8 Æ 0:02 cm, P < 0:01). These results indicate that prenatal stress
resulted in a signiﬁcant reduction of hormonal and morphometric measures of the reproductive system in blue fox fetuses with more
drastic eﬀects in female fetuses.
Ó 2003 Elsevier Science (USA). All rights reserved.
Keywords: Prenatal handling stress; Blue fox fetuses; Gonads; Testosterone; Oestradiol
The blue fox is a species that has been bred in fur farms
for more than a century. It may be thought that because of
very short history of domestication this species is practi-
cally wild especially taking into account some eﬀects of
farm conditions, like human contact. Most of farm bred
blue foxes show predominantly fear and defensive re-
sponses to human contact. Results of earlier experiments
indicated that contact with humans or even the mere
presence of a human is a stressor for blue and silver foxes
(Moe and Bakken, 1996, 1997; Pedersen, 1994; Rekil
et al., 1997, 1999). In commercial fox production, han-
dling is a more frequent type of contact of humans with
animals and farm-bred blue foxes are commonly handled
in connection with mating, insemination or transporta-
tion. Previous studies revealed that handling is a mild
stressor for farmed foxes resulting in activation of the
hypothalamic–pituitary–adrenal (HPA) axis indicated by
increased plasma cortisol concentrations or adrenal cor-
tisol production in vitro (Moe and Bakken, 1996, 1997;
Osadchuk et al., 2001a).
It is well established that stress associated with a
stimulation of the HPA axis negatively inﬂuences re-
productive events as well as the hypothalamic–pitui-
tary–gonadal (HPG) axis (Asher et al., 1996; Einarsson
et al., 1996; Magiakou et al., 1997; Marchlewska-Koj,
1997; Rivier and Rivest, 1991; Tilbrook et al., 2000).
General and Comparative Endocrinology 132 (2003) 190–197
GENERAL AND COMPARATIVE
Corresponding author. Fax: +7-3832-33-12-78.
E-mail address: firstname.lastname@example.org (L.V. Osadchuk).
0016-6480/03/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved.