The problem of arrival time and prelaying period in migratory birds
[Update: thoughts in this post contributed to Kristensen et al. (2015).]
Climate change has caused an advance in phenological events in many species (Forchhammer et al. 1998, Chmielewski & Rotzer 2001, Parmesan & Yohe 2003, Edwards & Richardson 2004, Menzel et al. 2006, Beebee 2009). In migratory birds, the effects of warming flow causally up the trophic levels. For example, warmer temperatures lead to earlier plant phenology (e.g. budding) (Menzel et al. 2006, Schwartz et al. 2006, Primack et al. 2009), which leads to earlier peaks in the abundance of foods (e.g. insect larva) that are important to raising nestlings (Visser et al. 1998), which puts pressure upon birds to advance their own breeding timetable. In general, birds have responded to warming weather by advancing their own phenology. Migratory birds are both arriving earlier (Huppop et al. 2003, Parmesan & Yohe 2003, Drent et al. 2003, Lehikoinen et al. 2004, Jonzen et al. 2006) and laying earlier (Crick et al. 1997, Crick & Sparks 1999, Both et al. 2004) in recent years. However, the responses have not been uniform: different populations of even the same species evidence quite different phenological responses (Both & Visser 2001), and in some populations the advance in arrival time and laying time has not kept pace with the advance in the food peak (e.g. Both & Visser 2001, Both et al. 2006) creating a `mismatch’ between hatching time and nestling food.
Predicting the response is complicated because matching the food peak is the result of two separate variables that are under (at least partial) behavioural control: the time of arrival to the breeding site after migration, and the delay between arrival and the start of breeding. It is possible for one to respond and not the other. For example, Both (2010) contrasted a population of Dutch flycatchers to Finnish flycatchers, the former advanced their laying date but not arrival date, and the latter advanced arrival but not laying. This raises the question: under what circumstances will migratory birds respond by advancing one trait but not the other versus advancing both traits?
Mismatch is particularly important from a conservation perspective because it has been implicated in population declines (Both et al. 2006, Goodenough 2009). Typically, it is assumed that pressure to lay earlier can translate to pressure to arrive earlier, and so mismatch is ultimately attributed to inflexibility in the arrival time (Drent et al. 2003). External factors thought to constrain arrival time include: unresponsiveness in the proximate cue to initiate migration (Both & Visser 2001), decoupling of proximate cues from timing of ecologically relevant events (e.g. due to differential warming) (Visser et al. 2004, Ludwig et al. 2006), conditions en-route (Both et al. 2005), and conditions in other parts of the year (Gordo et al. 2005, Swanson & Palmer 2009). However, there is a growing literature suggesting that mismatch may be adaptive in certain circumstances (Singer & Parmesan 2010, Visser et al. 2012, Johansson & Jonzen 2012b). Further, there is some evidence that birds were mismatched historically, that the laying date that maximises reproductive success is typically earlier than the laying date in most birds (Lack 1968; Perrins 1970; Perrins & Moss 1975; Drent 2006).
Migratory birds must time their spring arrival and nesting to satisfy multiple fitness objectives. They must arrive early enough to compete and acquire a quality nesting site (Brooke 1979, Arvidsson & Neergaard 1991, Lundberg & Alatalo 2010, Aebischer et al. 1996, Lozano et al. 1996, Kokko 1999), but not so early that they die in early-season cold weather (Newton 2007, Kokko 1999). Food availability at the breeding site often has a peaked temporal profile such that food is very abundant for a short period of time (Sanz 2001, Visser et al. 2006, Veen et al. 2010). Therefore, birds must also time their arrival such that there is adequate time to gather the resources needed for egg production (Perrins 1970, Nager 2006), and time their nesting and laying so that nestlings can take advantage of these food peaks (Veen et al. 2010). We could break this problem down into the component parts influencing individual fitness: adult survival, territory acquisition, hatching success, and fledging success.
The probability of adult survival is dependent upon the arrival time such that early arrival imposes a greater survival cost. This reflects food scarcity and harsh weather conditions on arrival (Newton 2007, Kokko 1999), and is supported by evidence that earlier arrivers have higher condition (Flood 1984, Francis & Cooke 1986, Møller 1990, Rotti et al. 1993, Møller 1994, Andersson & Gustafsson 1995, Lozano et al. 1996), the reasoning being that only individuals in good condition can survive the harsher early-season.
However, early arrival also confers a fitness benefit: the probability that the male will obtain a quality breeding territory to subsequently attract a mate and produce a clutch (Brooke 1979, Arvidsson & Neergaard 1991, Lundberg & Alatalo 2010, Aebischer et al. 1996, Lozano et al. 1996, Kokko 1999). This benefit of early arrival is relative: if all individuals arrive at the same time, then territory acquisition is some function of how many nesting sites are available compared to how many individuals are competing for those sites. However, if an individual arrives earlier than the population average it will have the advantage in gaining a territory.
Once the bird has arrived, it must gather resources for egg production (Perrins 1970, Nager 2006). The longer the prelaying period is the better the female body condition and clutch size possible (Rowe et al. 1994, Pettifor et al. 2001, Descamps et al. 2011) and the more egg-specific resources that can be gathered for manufacturing the egg (Nager 2006). However, resource availability during the pre-laying period is variable (Gauthier 1993), with food availability lower earlier in the season (Perrins 1970), and birds expending more energy during cold conditions (te Marvelde et al. 2012). This implies that the rate at which key nutrients for egg-production can be acquired will also be dependent upon how early in the season the prelaying period is, and thus also a function of arrival time. Note that it is possible for the rate of resource gain to constrain the laying date (Lepage et al. 2000). Also, early egg-laying can incur an adult survival cost (Nilsson 1994, Visser & Lessells 2001, Brinkhof et al. 2002), so there is some feedback here to the above-mentioned adult survival fitness component.
Finally, nestling food availability is typically a hump-shaped curve (Sanz 2001, Visser et al. 2006, Veen et al. 2010), potentially with multiple peaks (Verboven et al. 2001). Fledging success depends upon food availability during the nestling period, and so depends upon the match between the hatching time and the integral of this food availability curve over the period (Veen et al. 2010).