Many birds initiate incubation before their clutch is complete, which causes eggs to develop and hatch asynchronously (Clark & Wilson 1981; Stoleson & Beissinger 1995) and often results in the mortality of the smallest chicks. Most studies of hatching asynchrony have focused on identifying an adaptive function for the nestling size disparities that result from asynchronous hatching (Amundsen & Slagsvold 1991; Nilsson 1995; Stoleson & Beissinger 1995). The possible functional significance of the early onset of incubation has received scant attention, despite the fact that early incubation is the proximate cause of hatching asynchrony. Potential benefits include protection of eggs from brood parasitism (Wiley & Wiley 1980; Lombardo et al. 1989; Romagnano, Hoffenberg & Power 1990), predators (Amundsen & Stokland 1988; Bollinger, Bollinger & Malecki 1990), or intra- or interspecific competitors looking for nest sites (Beissinger & Waltman 1991; Beissinger 1996; Beissinger, Tygielski & Elderd 1998). Initiating incubation before the clutch is completed could also serve to maintain the viability of early laid eggs (Hussell 1985; Arnold, Rohwer & Armstrong 1987; Veiga 1992). This last hypothesis in particular, the ‘egg viability hypothesis’, may be broadly applicable among birds.
The egg viability hypothesis proposes that avian parents may maximize the hatchability of eggs by initiating incubation before their clutch is completed because the viability of unincubated eggs declines over time (Arnold et al. 1987; Ewert 1992). Temperature is the most critical condition affecting hatchability of unincubated eggs, although humidity, gaseous environment, egg orientation and egg turning are also important (Wilson 1991; Deeming 1992; Fasenko et al. 1992; Meijerhof 1992). Embryos are especially susceptible to death from overheating, are less affected by exposure to cool temperatures, and are susceptible to developmental failure under moderate temperature conditions (Webb 1987).
Hatching failure may often occur because development can begin below normal incubation temperatures. For almost all birds, optimal temperatures for normal embryonic development fall within a narrow range between about 36 and 38 °C, although incubation temperatures recorded in the field can often be a few degrees lower (Drent 1975; Webb 1987; Rahn 1991). Avian embryos do not develop below 24–27 °C (Rol’nik 1970; White & Kinney 1974; Wilson 1991), and this threshold is known as physiological zero (Drent 1973; O’Connor 1984; Webb 1987). When birds in temperate springtime climates delay incubation until the last egg, cold torpor suspends development of earlier eggs, which allows development and hatching to be synchronous (Drent 1975; Ewert 1992). The viability of unincubated eggs maintained in cold torpor declines slowly (Decuypere & Michels 1992; Ewert 1992). However, if ambient temperatures fall between physiological zero and normal incubation temperatures, some, but not all, embryonic tissues begin to develop in the absence of incubation. Prolonged exposure to temperatures above physiological zero yet below normal incubation levels results in unsynchronized growth, abnormal development and embryo mortality (Romanoff & Romanoff 1972; Wilson 1991; Deeming & Ferguson 1992). Development of neurological and brain tissues in very young embryos seems to be particularly sensitive to prolonged exposures to temperatures in this range (Webb 1987). Thus, once development begins, parent birds might be obliged to begin incubation early to maintain the viability of early laid eggs.
A decline in the viability of eggs resulting from prolonged exposure to ambient temperatures has been long known in synchronously hatching domestic fowl but was only recently demonstrated under field conditions in waterfowl (Drent 1973, 1975; Arnold et al. 1987; and references therein). Eggs showed a marked decline in hatchability when exposed to ambient temperatures for 5–10 days in a high latitude temperate site (Arnold et al. 1987; Arnold 1993). A similar effect was demonstrated more recently in an altricial bird, the house sparrow (Passer domesticus Linnaeus) in a Mediterranean climate. Eggs left unincubated for 3 or more days had lower hatching success than those unincubated for shorter periods, and hatching asynchrony increased later in the breeding season when ambient temperatures exceeded physiological zero (Veiga 1992; Veiga & Viñuela 1993). The effects of maintaining unincubated embryos in environments where ambient temperatures are regularly above physiological zero yet below incubation temperatures, such as tropical lowlands, are poorly known (Grant 1982). Presumably, egg viability should decline more rapidly in such environments.
In this paper we present the results of experiments designed to test the egg viability hypothesis in the green-rumped parrotlet (Forpus passerinus Linnaeus), a small Neotropical parrot. This species lays very large clutches for a tropical bird, which hatch extremely asynchronously (Beissinger & Waltman 1991). It inhabits hot, humid, tropical savannahs where the potential negative effects of ambient temperatures on unincubated eggs are likely to be especially pronounced. Our previous studies found no significant benefit to parents or offspring from asynchronous hatching in an extensive examination of the fitness consequences and costs of reproduction, but found clear costs in the form of reduced survival of penultimately and last-hatched young compared to synchronously hatched chicks (Stoleson & Beissinger 1997).
We tested the effects of high ambient temperatures on unincubated parrotlet eggs by experimentally subjecting newly laid eggs to varying lengths of exposure to ambient conditions and then returning them to active nests to be incubated normally by parrotlet parents. Unlike prior studies (Arnold et al. 1987; Veiga 1992), we assigned each experimental egg a control to account for differences in parental behaviour and nest microhabitat. We also monitored thermal conditions in holding boxes. The hatching success of experimental eggs was compared to unmanipulated control eggs to test the predictions that: (i) exposure of newly laid eggs to ambient temperatures above physiological zero should induce some embryological development even in the absence of incubation (because of this preincubation development, exposed eggs should require less incubation time to hatch than nonexposed eggs subject to similar incubation patterns); (ii) exposure to ambient temperatures should reduce the hatchability of eggs, and the reduction in hatchability should be proportional to the length of exposure; (iii) a greater proportion of embryo mortality in exposed eggs should occur after moderate to advanced development, rather than early development, because prolonged exposure to temperatures above physiological zero but below normal incubation temperatures should result in more embryos experiencing abnormal development; and (iv) the probability of hatching should be related to temperature extremes, duration of exposure to temperatures from 27 to 34 °C, or both.