Introduction
Small mammals in the Northern Hemisphere often have a broad spectrum of
population dynamics and seasonal fluctuations. Any pattern of population
dynamics is caused by changes in demographic parameters (Inchausti et
al., 2009). Thus, knowledge regarding the factors influencing
demographic parameters is of great importance for understanding
population dynamics.
In iteroparities such
as microtine rodents, density
dependence in reproduction plays an important role in stabilising
population dynamics via immediate negative feedback from population
density to reproductive output (Ostfeld et al., 1993). Although research
regarding density dependence has often been criticised
(Krebs, 2002), density-dependent
reproduction does occur in seasonal territorial microtine rodents with
strong social effects on demographic parameters during breeding season,
such as the grey-sided vole (Clethrionomys rufocanus ) (Saitoh,
1981), meadow vole (Microtus pennsylvanicus )
(Ostfeld et al., 1993), water vole
(Arvicola terrestris ) (Saucy, 1994), common vole (Microtus
arvalis ) (Inchausti et al., 2009) and bank vole (Clethrionomys
glareolus ) (Koskela et al., 1999) and Yangtze vole (M. fortis
calamorum ) (Zhang et al., 2010). The mechanisms underlying
density-dependent reproduction are associated with direct and indirect
interactions among individuals, such as consumptive and non-consumptive
competition (Rödel et al., 2004), as well as social suppression for
juvenile maturation (Saitoh, 1981).
Christian (1971) suggested that density-dependent reproduction might be
the result of increased adrenocorticotropic hormone secretion in
response to increased density and decreased or suppressed reproduction.
However, Christian’s research has been criticised because it was largely
performed on captive animals in a laboratory setting (Krebs & Myers,
1974; Lee & McDonald, 1985); moreover, there has been limited evidence
supporting their hypothesis. Nonetheless, studies have shown that
factors known to influence density dependence of reproduction, such as
social interference and antagonistic interactions, are normally
modulators of individual stress responses in the population and act as
stressors to activate the hypothalamic-pituitary-adrenal axis and
subsequent secretion of glucocorticoids (GC), a critical hormone in
stress response (Sheriff et al., 2009). Studies on free-living,
non-social, territorial vertebrates demonstrated that population density
is usually positively associated with GC levels (see review by Creel et
al., 2013, but see Harper &
Austad, 2004; Kuznetsov et al., 2004; Charbonnel et al., 2008). In voles
specially, increase in population density was associated with an
increase in corticosterone levels (Boonstra & Boag, 1992; Novikov &
Moshkin, 1998; Bian et al., 2015). For some social mammals living in
groups, dominant individuals have higher reproductive success and
heightened GCs level (see review by Sapolsky, 2005); however, evidence
from laboratory studies and free-ranging iteroparous territorial rodents
have shown that chronically elevated GC concentrations inhibit the
gonadal axis function and lead to a negative effect on reproduction (see
review by Creel et al., 2013). Thus,
density-dependent reproduction in
microtine rodents may be the result of elevated corticosterone
concentrations in response to increased density.
In the present study, we investigated the effects of density-induced
stress on reproduction via manipulation of the population density in the
root vole (Microtus oeconomus ). This is part of a larger
multifaceted project examining the effects of density-induced maternal
stress on population dynamics. Parental enclosures for breeding
offspring were established by introducing six and thirty adults of each
sex in low- and high-density enclosures, respectively, in 2012 and 2015.
Our previous papers have reported that high parental population density
was approximately three times higher compared with low parental
population density at the end of the experimental period in 2012 (Bian
et al., 2015). Moreover, the population under high-density conditions
showed higher mean faecal corticosterone metabolite (FCM) levels than
the population under low-density conditions in both 2012 (Bian et al.,
2015) and 2015 (Yang et al., 2018). In this study, we present
unpublished data from the same parental populations in 2012 and 2015,
which include recruitment and proportion of reproductive conditions and
the numbers of male and female founders in both years. We separately
tested the difference in reproductive traits between high-and
low-density parental populations, and analysed how the number of
founders and FCM levels affected reproduction by the recursive model in
the structural equation model (SEM). We aimed to test the hypothesis
that density-dependent reproduction in voles may be due to the
suppressive effects of density-induced stress on reproduction. We
predicted that a high-density population would have lower recruitment
and the proportion of reproductive condition, and the effects of founder
number on both reproductive traits would be mediated by FCM levels.