Reproductive phenology in red deer is adjusted by selection to promote births to occur at the most favourable time in spring (Landete-Castillejos et al. 2003). For females, access to high-quality forage is critical to meet the marked increase in energy demands during late gestation and lactation (Asher et al. 1996; San Miguel et al. 1999; Landete-Castillejos et al. 2003; Perea & Gil 2014), and it has direct consequences for both offspring and maternal survival (Clutton-Brock et al. 1987 a,b; Plard et al. 2014).
In agreement with previous studies (Mitchell & Lincoln 1973; Clutton-Brock et al. 1983; Peláez et al. 2017), we evidenced that age and thoracic circumference, as the main proxy for female body mass, had a negative effect on the mating date. We found that one-year-old females are the latest to conception, followed by hinds older than 10 years. These results suggest that the reproductive senescence of females in Mediterranean ecosystems probably occurs after the age of 10 years, in contrast to previous studies from red deer populations in northern Europe (Nussey et al. 2006, 2009; Mysterud et al. 2001; Loison et al. 2004). As capital breeders, hinds optimise their investment in reproduction according to their fat reserves (Clutton-Brock et al. 1982; Landete-Castillejos et al. 2003, 2009; Carrión et al. 2008) so conception dates can differ between individuals and years to avoid compromising female reproduction (Clutton-Brock et al. 1989; Asher & Pollard, 2002; Pettorelli et al. 2005; Asher, 2020; Millán et al. 2022). Delaying the mating time has negative consequences for both female red deer and foetus body condition (Mateos et al. in prep.) and is also associated with lower reproductive rates (Millán et al. 2022). The ability of the females at a given time to cope with gestation and lactation will determine the associated costs (Garratt et al. 2020). According to our results, this balance depends mainly on females’ age, which may promote young to delay the conception date in order not to incur extreme reproductive costs that are difficult to overcome if they do not have sufficient body reserves (Pettorelli et al. 2005; Millán et al. 2022). Thus, here we showed that for hinds in Mediterranean ecosystems, there is an optimum in reproductive phenology that is age and body condition dependent (Peláez et al. 2017).
We also found that in low competition contexts high-body mass females have shown earlier conceptions than in high competition populations. In contrast, the mating date for low body mass females is similar in both types of population. This result is probably due to differences in the mating date synchrony between high and low-competition populations (see Fig. 1). In red deer, differences in the sex structure of the population have consequences in the harem size that males can gather during the rut (Clutton-Brock et al. 1992; Carranza & Valencia 1999; Bonenfant et al. 2004). In female-biased populations, hinds aggregate in large groups defended by high-rank males (Clutton-Brock et al. 1992). The high density of females congregated may favour the oestrus synchrony (Langvatn et al. 2004; Mysterud et al. 2008) but just in good condition females (Clutton-Brock et al. 1983). Our results indicated that late conceptions are less common in low-competition populations and are mainly belong to low-body mass females. However, in high competition populations asynchrony conceptions occurred independently of females body mass. Reduced synchrony in the timing of female oestrus affects offspring survival (Peláez et al. 2017), caused by the decoupling of calving and the period of maximum food availability (Bughalo & Milne 2003). As asynchronous reproduction increases, females' fitness is compromised and their resilience to environmental perturbations is reduced (Boutin & Lane 2014). These results are relevant since in populations with high mate competition, increased reproductive asynchrony may mean that females suffer the costs of reproduction, but these are also magnified by the scarce and low predictable food availability after the gestation period and during lactation (Clutton-Brock et al. 1983; Hamel et al., 2010; Festa-Bianchet et al. 2019).
Male-female interactions produce conflict situations when the sexes differ on the optimal value of a shared trait (Chapman et al. 2003; Arnqvist & Rowe 2005). In the conventional scenario, where the competitive strategies of males aim to ensure mates while those of females focus on assuring resources and avoiding predation, sexual conflicts can arise when these interests clash (Arnqvist 2005). Female conception is not an independent behaviour but is directly dependent on interaction with males and their behaviour. During the rutting season, females are interested in large areas where food quality is high, and they are mainly monopolised by dominant males (Carranza & Valencia 1999; Carranza et al. 2005). Through these movement patterns during the rut, females can obtain indirect benefits, in terms of offspring (i.e. genetic) or direct benefits, by obtaining safe places to avoid continued harassment by other males, avoid predation and increase food availability (Clutton-Brock et al. 1996; Carranza & Valencia 1999; Carranza et al. 2005).
Under intense male-male competition situations, the coercion pressure on females by males is also high (Bonenfant et al. 2004). A shift in the space-use behaviour of females is expected in these circumstances (Carranza & Valencia 1999). Thus, as intrasexual competition increases (due to the higher proportion of males), harassment to females should also raise (Clutton-Brock et al. 1992; Carranza & Valencia 1999), and suboptimal resource use occurs (Carranza & Valencia 1999). This situation may affect more intensely younger and inexperienced females, who are also in lower positions in their dominance’ hierarchy. This may imply suboptimal conceptions for females in general, but especially for 1 year-old-females. However, our results show that these behavioural changes in the use of available resources do not affect juvenile (2 years old) and subadults (3–4 years old) females in the same way, suggesting that this could be the ideal time for conception at these ages in both types of populations (Clutton-Brock 1985). Future studies should examine the extent to which mating competition between males affects reproductive behaviour and, consequently, the conception date of adult females considering senescent hinds.
Our results have so far been approached through the perspective of female red deer. However, male reproductive phenology is also crucial to the timing of conception and should be interpreted as a trade-off between female ovulation timing and the intensity of sexual selection (Mysterud et al. 2008). Males modulate their investment in mating competition according to the likelihood of reproductive success and to avoid incurring in associated costs (i.e. loss of body mass, injuries after fights, etc. Clutton-Brock et al. 1989; Carranza et al. 2020 a,b). Previous studies have shown that late births are mainly sired by younger males (Soay sheep: Preston et al. 2001; Red deer: Mysterud et al. 2008). In high mating-competition populations, it is expected that prime-age males will primarily target adult and quality (in terms of body mass) females that ovulate earlier (Preston et al. 2005; Mysterud et al. 2008). Younger males with low competitive ability might even improve their body condition during the rut due to low reproductive effort while prime males are monopolizing most females and wait to the last period of the rut for one-year-old females to ovulate (Preston et al. 2005).
Although increased asynchrony and delayed conceptions under conditions of intense male competition might have some implications for population dynamics (due to lower offspring survival, Peláez et al. 2022), our results show that the effects are mostly affecting young females rather than being a general effect in the population. However, these results also reveal that females not only need to reach a physiological status to optimize pregnancy timing, but probably also a learning period including behavioural issues to cope with harassment pressure from males in high mate-competition situations. This is also supported by the result that increased condition (thoracic circumference) does not translate into earlier gestation in young females under high competition scenarios compared to those in low competition populations. These possible costs for young females in situations of intense male-male competition may in turn be an element of selection, resulting in females that are less able to handle interactions with males and deal with this conflict being less likely to succeed in terms of reproduction.
In this work, we compare reproductive phenology in female red deer under two different scenarios regarding male-male competition. Despite finding a delay in conception in the youngest females (one-year-old) in highly competitive populations, it is worth asking what level of intrasexual competition we would find under natural or unmanaged conditions. Both types of populations have similar densities of individuals (Torres-Porras et al. 2009). However, it is possible that in highly competitive populations there would be higher spatial aggregation of males and females during the mating season due to human management (e.g. supplementary food supply or habitat management) or female clumping to mating areas (Carranza & Valencia 1999). Future studies can examine the role of population density and spatial aggregation during the rutting season in the timing of females of different ages and variable body conditions becoming pregnant and associate this with the importance of environmental conditions in determining the availability and distribution of resources. A key advantage of studying two scenarios of varying intrasexual competition in wild red deer populations is that it provides an opportunity to highlight processes that are otherwise overlooked.