Phenology is a crucial structuring factor in many areas of ecology and evolution, comprising the temporal intersection between key biological events and an organism’s environment (Forrest & Miller-Rushing 2010). Recent climate warming has significantly advanced the phenology of a wide range of taxa in many ecosystems (Root et al. 2003; Parmesan 2007; Thackeray et al. 2010), with change progressing at an unprecedented rate and predicted to continue (IPCC 2007). Therefore, there is an urgent need to determine how different species respond to climate change. However, the majority of studies have investigated changes in birds and insects, with comparatively few on mammals (Parmesan 2007; Bronson 2009; but see: Inouye et al. 2000; Sinclair, Mduma & Arcese 2000; Coulson et al. 2003; Réale et al. 2003; Durant et al. 2005; Post & Forchhammer 2008; Ozgul et al. 2010; Moyes et al. 2011). Moreover, studies have focused on species exhibiting clear seasonality in breeding, and here we focus on evaluating phenological responses of an animal that breeds year round.
Phenology and synchrony of births comprise a vital component of a species’ overall reproductive strategy that has been selected to optimise production of surviving offspring (Stearns 1992). Ungulate reproduction varies in timing between rigidly seasonal and continuous, depending primarily on the seasonality of climate and food availability and quality (Bronson 1989). In general, seasonality is more pronounced at higher latitudes because of greater annual variation in temperature; but can also occur in the tropics because of strongly seasonal rainfall, both of which influence seasonal patterns of primary production (Bronson 1989; Sinclair, Mduma & Arcese 2000). For example, deer from the genus Odocoileus exhibit highly seasonal breeding at northern latitudes, asynchronous breeding with a pronounced spring peak in Florida, but breed year round at their extreme southern range in Venezuela (Brokx 1972; Richter & Labisky 1985). Lactation is known to be the most energetically demanding period of the annual reproductive cycle in female ungulates, and females that match this to the peak of newly emergent forage plant tissue with high digestibility and nutritional value have been shown to have higher fitness (Robbins 1983; Festa-Bianchet 1988; Clutton-Brock 1991). Variation in birth phenology within an ungulate species is also known to be linked to climate. Calving dates of red deer, Cervus elaphus, were delayed following years of high autumn rainfall (Nussey et al. 2005). Moyes et al. (2011) found that six phenological traits in red deer advanced temporally, correlated with the timing of local plant growth. Other factors also constrain the seasonality and the degree of synchrony of mammalian reproduction: inter- and intra-specific (density) competition for resources; predation avoidance by adjusting birth synchrony; and dietary strategy, with generalists being less vulnerable to seasonal changes in specific food types (Bronson 1989; Sinclair, Mduma & Arcese 2000; Loe et al. 2005).
Feral herbivores have been shown to differ from their wild counterparts in the seasonality of their reproductive cycles (Setchell 1992). Domesticated modern pigs breed year round, unlike their European wild boar, Sus scrofa, ancestors which have strongly seasonal breeding patterns (Eckstein & Zuckerman 1956; Bronson 1989), while Soay sheep, Ovis aries, and mouflon cross-bred with domestic sheep (Ovis gmelini musimon × Ovis sp.) exhibit earlier age at first reproduction and higher twinning rates than their wild counterparts (Clutton-Brock & Pemberton 2004; Garel et al. 2005). Such differences are a consequence of artificial selection during domestication which aims to maximise reproductive performance, via selection for traits accelerating the onset of reproductive maturity and improved fecundity. Despite the fact that feral ungulates are increasingly important components of ecosystems (Grange, Duncan & Gaillard 2009), relatively little is known about the potential impacts of environmental change on their reproductive phenology.
Currently, there are few studies evaluating whether species are shifting their phenology sufficiently to match changes in the environment by evaluating fitness consequences of such shifts and population growth trajectories (Visser & Both 2005). Herbivores have been shown to exhibit both negative and positive fitness consequences to climate change. Large herbivores in the high arctic exhibiting highly seasonal reproduction, timed to coincide with the peak plant growing season (Post et al. 2003), have become increasingly mismatched in the timing of their breeding from the onset in forage plant growth, resulting in increased offspring mortality and reduced production (Post & Forchhammer 2008). Conversely, in systems where trophic mismatch is not apparent, climate warming can have a positive effect, with birth weights of red deer being heavier following warmer springs with corresponding increased survival rates (Albon, Clutton-Brock & Guinness 1987). Moyes et al. (2011) found no temporal changes in offspring survival of red deer, despite significant advances in breeding phenology. However, feral populations that have been selectively bred to maximise reproductive output are predicted to be more elastic in their phenological response to climate change and to show different responses from their wild counterparts. Selection for maximal reproductive output and elastic responses in phenology have also been shown to have negative fitness consequences (reduced population growth rates). Feral Camargue prime-aged female horses, Equus caballus, maintained high levels of fecundity at high population densities, despite depleting food resources, at the expense of their survival probabilities (Grange, Duncan & Gaillard 2009). Cattle are also predicted to experience negative impacts of climate change via reduced nutritional quality of grassland forage associated with increased temperature (Craine et al. 2010).
Here, we evaluate changing phenology in Chillingham cattle, a previously husbanded herbivore living in an unmanaged state since at least the 16th century (termed feral hereafter). This herd exhibits year-round breeding (Hall & Hall 1988), despite its environment showing strong seasonality in climate and vegetation dynamics (Armstrong et al. 1997). Historical domestication of Chillingham cattle is predicted to have influenced their phenology, leading to aseasonal reproduction, and contrasting responses to environmental change from those expected in wild ungulates. In this study, we use a 60-year data set of cattle birth dates to test five hypotheses (Table 1) to evaluate how breeding phenology has changed over time, the environmental correlates of these changes and whether such changes are impacting on population demography.
|H1||Median birth phenology has advanced over time in cattle at a greater rate to that reported for other wild taxa.||Feral ungulates show enhanced reproductive output and different seasonal breeding patterns compared with their wild ungulate counterparts. We therefore predict that feral populations will show greater elasticity in phenological response than wild ungulates owing to previous selection for enhanced reproductive output.||Eckstein & Zuckerman 1956; Bronson 1989; Setchell 1992; Clutton-Brock & Pemberton 2004; Garel et al. 2005|
|H2||The proportion of births in winter and spring show the greatest change (increase) over time.||Winter and spring months show the greatest evidence of climate warming in the northern hemisphere, driving a significant advance in the forage plant growing season||Schwartz, Ahas & Aasa 2006;.|
|H3||Conditions (winter/spring temperatures or onset of plant growth) immediately prior to or during spring are negatively correlated with spring conceptions (hence winter births).||There is much evidence from ungulates that poor forage conditions prior to conceptions result in females being in poor condition and unable to or delaying conception.||Chapman, Furlong & Harris 1997; Langvatn et al. 2004; Griffiths et al. 2010|
|H4||The proportion of spring conceptions (hence winter births) is positively associated with herd density.||There is evidence from Soay sheep and red deer that high winter density leads to poorer quality young (lower body weight) and to earlier born young.||Clutton-Brock et al. 1992; Forchhammer et al. 2001; Coulson, Milner-Gulland & Clutton-Brock 2000; Coulson et al. 2003|
|H5||Cattle recruitment (defined as the number of calves produced per adult female that survive to their first census) is negatively associated with breeding phenology (proportion of winter births).||Historical artificial selection for fecundity leads to high reproductive output, even when conditions are not optimal (for example high herd density or births during winter when conditions are relatively harsh) and at the expense of survival of breeding females or young.||Clutton-Brock et al. 1992; Grange, Duncan & Gaillard 2009|