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Growth Rate Variation Among Passerine Species in Tropical and Temperate Sites: an Antagonistic Interaction Between Parental Food Provisioning and Nest Predation Risk

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Growth Rate Variation Among Passerine Species in Tropical and Temperate Sites: an Antagonistic Interaction Between Parental Food Provisioning and Nest Predation Risk ORIGINAL ARTICLE doi:10.1111/j.1558-5646.2011.01227.x GROWTH RATE VARIATION AMONG PASSERINE SPECIES IN TROPICAL AND TEMPERATE SITES: AN ANTAGONISTIC INTERACTION BETWEEN PARENTAL FOOD PROVISIONING AND NEST PREDATION RISK Thomas E. Martin,1,2 Penn Lloyd,3,4,5 Carlos Bosque,6,7 Daniel C. Barton,3,8 Atilio L. Biancucci,3,9,10 Yi-Ru Cheng,3,11,12 and Riccardo Ton3,13 1U. S. Geological Survey Montana Cooperative Wildlife Research Unit, University of Montana, Montana 59812 2E-mail: [email protected] 3Montana Cooperative Wildlife Research Unit, University of Montana, Missoula, Montana 59812 4Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch 7701, South Africa 5E-mail: [email protected] 6Departamento Biologıa´ Organismos, Universidad Simon Bolivar, Caracas, Venezuela 7E-mail: [email protected] 8E-mail: [email protected] 9E-mail: [email protected] 11E-mail: [email protected] 13E-mail: [email protected] Received September 16, 2010 Accepted January 3, 2011 Causes of interspecific variation in growth rates within and among geographic regions remain poorly understood. Passerine birds represent an intriguing case because differing theories yield the possibility of an antagonistic interaction between nest predation risk and food delivery rates on evolution of growth rates. We test this possibility among 64 Passerine species studied on three continents, including tropical and north and south temperate latitudes. Growth rates increased strongly with nestling predation rates within, but not between, sites. The importance of nest predation was further emphasized by revealing hidden allometric scaling effects. Nestling predation risk also was associated with reduced total feeding rates and per-nestling feeding rates within each site. Consequently, faster growth rates were associated with decreased per-nestling food delivery rates across species, both within and among regions. These relationships suggest that Passerines can evolve growth strategies in response to predation risk whereby food resources are not the primary limit on growth rate differences among species. In contrast, reaction norms of growth 10Present address: P.O. Box 1927, Normal, Alabama 35762. 12Present address: Endemic Species Research Institute, Ming-shen East Road, Chichi Township, Nantou County, Taiwan. C 2011 The Author(s). Evolution C 2011 The Society for the Study of Evolution. 1607 Evolution 65-6: 1607–1622 THOMAS E. MARTIN ET AL. rate relative to brood size suggest that food may limit growth rates within species in temperate, but not tropical, regions. Results here provide new insight into evolution of growth strategies relative to predation risk and food within and among species. KEY WORDS: Food limitation, growth rates, life history, nest predation, parental care, passerines, provisioning rate. Growth rates of offspring vary extensively among species of all Martin 2004). The same relationships are expected across species taxa (Case 1978; Roff 1992; Arendt 1997; Dmitriew 2011). Inter- where evolution of slower growth can adjust food demands to specific variation in growth and development rates is even greater supply rates (Lack 1968; Martin 1987), but tests across species across geographic regions, such as tropical versus temperate (e.g., are lacking. Ricklefs 1976; Case 1978; Martin and Schwabl 2008; Cox and Food delivery rates may not be influenced by food availabil- Martin 2009). Causes of variation in growth rates of offspring ity alone. Increased nest predation risk can cause fewer feeding are important to understand because growth rates can influence trips by parents to reduce the risk of predators discovering nests offspring phenotypes and quality, thereby creating major fitness (Fig. 1B; Skutch 1949; Martin et al. 2000a,b; Eggers et al. 2005; consequences (Linden´ et al. 1992; Roff 1992; Arendt 1997). Yet, Fontaine and Martin 2006; Massaro et al. 2008). Greater pre- our understanding of potential causes of growth rate variation dation risk, therefore, can cause a proximate slowing of growth among species with diverse life histories within and among geo- via reduced food delivery within bird species (Scheuerlein and graphic regions remains weak. Gwinner 2006; Thomson et al. 2006), as commonly seen in other Two ecological factors (food limitation and juvenile pre- taxa (reviewed in Dmitriew 2011). Similarly, species with re- dation risk) are thought to play key roles in growth rate vari- duced feeding rates from higher predation risk may evolve slower ation within constraints imposed by allometric scaling across growth to adjust food demands to supply rates. The slower growth taxa (Case 1978; Arendt 1997; Dmitriew 2011). Food Limita- observed for many tropical species (i.e., Ricklefs 1976; Cox and tion: Greater food limitation can serve as a proximate cause Martin 2009) might reflect such effects given commonly higher of slower growth within species (Lack 1968; Crossner 1977; predation risk in many tropical sites and expected reductions in Martin 1987; Richner et al. 1989; Arendt 1997; Naef-Daenzer feeding rates (i.e., Skutch 1949; Martin 1996). Reductions in feed- and Keller 1999; McAdam and Boutin 2003). Greater food limi- ing rates from increased risk of predation, thus, may cause both tation also may favor evolution of slower growth among species, proximate and evolutionary slowing of growth rates (Fig. 1A,B). although such possibilities are relatively uninvestigated (Case Increased nest predation risk, however, is expected to favor 1978; Arendt 1997). Juvenile predation: Greater risk of juvenile evolution of faster, rather than slower, growth to minimize expo- predation can favor evolution of faster growth to minimize expo- sure time to predators (Fig. 1C; Case 1978; Bosque and Bosque sure time to predators (Williams 1966; Lack 1968; Case 1978; 1995; Remesˇ and Martin 2002). Bird species differ in nest pre- Bosque and Bosque 1995; Martin 1995; Arendt 1997; Remesandˇ dation risk based on their nest sites (Martin 1995; Fontaine et al. Martin 2002). Yet, increased predation risk in many systems 2007), and exhibit faster growth and shorter nestling periods when causes reduced feeding activity, which can slow growth rate via risk of nest predation is higher (Bosque and Bosque 1995; Remesˇ food limitation (Van Buskirk 2000; Altwegg 2002; Benard 2004; and Martin 2002; Ferretti et al. 2005). Food delivery could fa- see review in Dmitriew 2011). Thus, the relative importance and cilitate faster growth with increased predation risk if per-nestling interactions of offspring predation and food limitation may be feeding rates increased with nest predation risk (Fig. 1D) through critical to evolution of growth strategies but, as described below, mechanisms such as decreased brood size (number of nestlings) may include alternatives that have not been considered. (Slagsvold 1982; Martin 1995; Martin et al. 2000a; Doligez and Altricial birds provide an interesting group to study food lim- Clobert 2003; Eggers et al. 2006). However, no study has ex- itation and offspring predation because their relative influences amined per-nestling feeding rates relative to nest predation risk have been widely debated (reviewed in Martin 1987, 1992, 1996; across species. Lima 2009; Martin and Briskie 2009). Food limitation is com- An antagonistic interaction between food delivery and nest monly invoked as the dominant influence in birds (Lack 1968; predation (Fig. 1E) could arise if growth rates increase (Fig. 1C) Martin 1987) with expectations that growth rates increase with whereas per-nestling feeding rates decrease (Fig. 1F; e.g., Skutch the rates that parents deliver food per offspring (Fig. 1A). Greater 1949; Sargent 1993) with increasing predation risk. Independence food abundance can yield increased food delivery rates by parents of growth rates and food delivery is possible through evolution and faster growth rates within bird species at a proximate level of strategies that shift allocation of resources between growth (Naef-Daenzer and Keller 1999; Tremblay et al. 2003; Lloyd and rate and development of internal systems (Ricklefs 1968, 1993; 1608 EVOLUTION JUNE 2011 GROWTH RATE VARIATION Figure 1. Three alternative hypotheses for evolutionary influences of nest predation and food limitation on growth rates, holding any mass effects constant. (A) If food limitation exerts selection on evolution of growth rates, growth rate should increase with per-nestling feeding rate (Naef-Daenzer and Keller 1999; Tremblay et al. 2003; Lloyd and Martin 2004). (B) Feeding rates may be influenced by nest predation risk or food availability. If nest predation exerts selection on evolution of feeding rates, then total feeding rates (total number of feeding-trips by both parents h−1) should decrease with increased predation risk (Skutch 1949; Martin et al. 2000a,b; Fontaine and Martin 2006). An additive effect of food availability will cause deviations in total feeding rates for a given nest predation rate (the gray arrows). A dominant role of food availability could eliminate a relationship with nest predation. (C) If nest predation exerts selection on evolution of growth rates, species with higher nest predation risk are expected to evolve increased growth rates (Case 1978; Arendt 1997; Remesˇ and Martin 2002). (D) Per-nestling provisioning may increase with nest predation risk if brood size is also reduced. This result can allow increased growth rates with greater predation risk through reduced food limitation
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