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Geographic Variation in Avian Incubation Periods and Parental Influences on Embryonic Temperature

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Geographic Variation in Avian Incubation Periods and Parental Influences on Embryonic Temperature ORIGINAL ARTICLE doi:10.1111/j.1558-5646.2007.00204.x GEOGRAPHIC VARIATION IN AVIAN INCUBATION PERIODS AND PARENTAL INFLUENCES ON EMBRYONIC TEMPERATURE Thomas E. Martin,1,2 Sonya K. Auer,1,3,4 Ronald D. Bassar,1,3,5 Alina M. Niklison,1,6 and Penn Lloyd1,7 1United States Geological Survey Montana Cooperative Wildlife Research Unit, University of Montana, Missoula, Montana 59812 2E-mail: [email protected] 4E-mail: [email protected] 5E-mail: [email protected] 6E-mail: [email protected] 7Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch 7701, South Africa E-mail: [email protected] Received March 1, 2007 Accepted June 13, 2007 Theory predicts shorter embryonic periods in species with greater embryo mortality risk and smaller body size. Field studies of 80 passerine species on three continents yielded data that largely conflicted with theory; incubation (embryonic) periods were longer rather than shorter in smaller species, and egg (embryo) mortality risk explained some variation within regions, but did not explain larger differences in incubation periods among geographic regions. Incubation behavior of parents seems to explain these discrepancies. Bird embryos are effectively ectothermic and depend on warmth provided by parents sitting on the eggs to attain proper temperatures for development. Parents of smaller species, plus tropical and southern hemisphere species, commonly exhibited lower nest attentiveness (percent of time spent on the nest incubating) than larger and northern hemisphere species. Lower nest attentiveness produced cooler minimum and average embryonic temperatures that were correlated with longer incu- bation periods independent of nest predation risk or body size. We experimentally tested this correlation by swapping eggs of species with cool incubation temperatures with eggs of species with warm incubation temperatures and similar egg mass. Incu- bation periods changed (shortened or lengthened) as expected and verified the importance of egg temperature on development rate. Slower development resulting from cooler temperatures may simply be a cost imposed on embryos by parents and may not enhance offspring quality. At the same time, incubation periods of transferred eggs did not match host species and reflect intrinsic differences among species that may result from nest predation and other selection pressures. Thus, geographic variation in embryonic development may reflect more complex interactions than previously recognized. KEY WORDS: Development rates, developmental trade-offs, egg temperature, life history, nest attentiveness, nest predation, parental care, passerines. 3Present Address: Department of Biology, University of California, Riverside, CA 92521 C 2007 The Author(s). Journal compilation C 2007 The Society for the Study of Evolution. 1 Evolution MARTIN ET AL. The rate of embryonic development is of great interest because it and Weimerskirch 2001). Incubation period is positively related can have critical fitness consequences, and interspecific variation to adult survival probability (Ricklefs 1993; Martin 2002), which is thought to be explained by three factors. Allometric constraints may reflect enhanced mechanisms for survival afforded by slower cause longer developmental periods in larger species (Rahn and development, although direct tests of such functional relationships Ar 1974; Case 1978; Arendt 1997). Shorter development peri- are lacking. ods, however, can be favored by greater predation risk (Case An alternative possibility is that longer-lived species, as com- 1978; Bosque and Bosque 1995; Martin 1995, 2002; Arendt 1997; mon in the tropics and southern hemisphere, invest less effort Remeˇs and Martin 2002). At the same time, faster development in incubation that reduces egg temperatures and slows develop- for a given mass can trade-off with intrinsic features (e.g., lo- ment (Martin 2002). Long-lived species should invest less effort comotor performance, immune function) of offspring that affect in reproduction than shorter-lived species to reduce adult mor- fitness of later stages, and may thereby favor slower development tality risk, even at a cost to offspring (Williams 1966; Charnov (Case 1978; Arendt 1997, 2003; Billerbeck et al. 2001; Brommer and Schaffer 1973; Law 1979; Michod 1979; Barbraud and 2003; Shine and Olsson 2003). Yet, the ability of allometry, mor- Weimerskirch 2001; Ghalambor and Martin 2001). Incubation is tality risk, and intrinsic trade-offs to explain geographic variation energetically expensive and can influence future reproduction and in development rates among species is relatively untested. survival (Bryan and Bryant 1999; Reid et al. 2000; Visser and Les- As typical of other taxa, incubation periods of birds gener- sels 2001). Thus, tropical and southern hemisphere bird species ally are longer in larger species across taxonomic orders (Rahn and may invest less time and energy in incubation and thereby slow de- Ar 1974; Ricklefs and Starck 1998). The longer time needed for velopment by causing cooler embryo temperatures (Martin 2002). proliferation of more and larger cells of larger species is a reason- Embryo temperature may be important because bird embryos able and well-documented expectation (Case 1978; Arendt 1997; are effectively ectothermic and depend on the presence of incu- Ricklefs and Starck 1998). Yet, incubation periods appeared not bating parents for warmth (White and Kinney 1974). Embryonic to be constrained by body or egg size within a sample of passer- temperature variation is characteristic of many true ectotherms be- ines from two latitudes (Martin 2002). The potential indepen- cause of variation in where parents place eggs in the environment. dence of incubation periods of passerines from body and egg size A critical consequence of such variation is that development takes (Martin 2002) suggest that their embryonic development rates longer for eggs placed in cooler incubation environments among within and among geographic regions are subject to influences conspecific ectotherms, and also yields smaller and/or lower qual- beyond simple allometric constraints. ity hatchlings (Webb and Cooper-Preston 1989; Shine et al. 1997; Increases in time-dependent mortality such as nest predation Qualls and Andrews 1999; Shine and Olsson 2003; Hare et al. favor shorter developmental periods (Case 1978). Egg predation 2004). If slow development in birds also results from cool embry- risk, however, is unlikely to explain broad geographic variation in onic temperatures, then offspring quality may be compromised passerine incubation periods (Martin 1996, 2002). Incubation pe- (Olson et al. 2006), rather than enhanced. The ability of parental riods are commonly longer for species in the tropics and southern behavior and egg temperatures to explain interspecific variation hemisphere compared with related species in the north temperate in incubation periods of birds has been debated (Boersma 1982; region (Martin 2002, Chalfoun and Martin 2007), although nest Ricklefs 1984; Tieleman et al. 2004). Yet, broad and stringent predation rates are either similar or greater in these southern loca- tests of temperature influences on interspecific and geographic tions (Skutch 1949; Maclean 1974; Robinson 1990; Major 1991; variation in incubation periods are lacking. Here, we examine Martin et al. 2000, 2006). Thus, the long incubation periods of these alternative hypotheses based on detailed study of 80 passer- many tropical and southern hemisphere species oppose expecta- ine species on three continents (North America, South America, tions from nest predation risk (Martin 1996, 2002), and emphasize and Africa). the importance of understanding alternative causes of geographi- cal variation in embryonic development rates. Indeed we can ask Methods more generally why a species should ever develop slowly given STUDY SYSTEM the accumulating risk of mortality? We studied 80 passerine species (Appendix) at four sites on three One possibility is that slower development may allow greater continents. Study sites were high-elevation (2300 m elevation) development of intrinsic features that enhance performance and mixed forest in Arizona (34◦N latitude), Yungas forest (1000 m) in longevity (Ricklefs 1993; Arendt 1997, 2001, 2003; Billerbeck northwestern Argentina (26◦S), cloud forest (1400–2000 m) in the et al. 2001; Brommer 2003; Shine and Olsson 2003). Increased northern Andes of Venezuela (9◦N), and coastal dwarf shrubland longevity may be more important than increased risk of offspring near Cape Town, South Africa (34◦S) (see Martin 1998; Mar- mortality in long-lived species that depend on iteroparity across tin et al. 2000, 2006; Nalwanga et al. 2004 for descriptions of years to enhance fitness (Williams 1966; Law 1979; Barbraud study sites). 2 EVOLUTION 2007 GEOGRAPHIC VARIATION IN INCUBATION PERIODS NEST PREDATION, INCUBATION PERIODS, AND failing batteries or poorly sealed holes. We sought to sample six PARENTAL CARE SAMPLING nests per species, but samples varied from two to nine, with 12 and Study sites were searched for nests during entire breeding seasons 15 nests for two species, and an average of 5.6 nests per species. in 1988–2005 in Arizona, 1997–1999 in Argentina, 2000–2004 in South Africa, and 2002–2006 in Venezuela. For species examined EGG TRANSFER EXPERIMENT here, large numbers of nests were monitored for nest predation and To test the ability of egg temperature to influence developmental
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