Effect of Ephemeral Food Restriction on Growth of House Sparrows

—We tested for the presence of compensatory growth (i.e. faster age-specific growth) following ephemeral periods of food restriction in altricial nestlings using the House Sparrow (Passer domesticus) as a model species. To simulate periods of poor food conditions, we raised nestlings in captivity, fed them a synthetic diet, and held them at constant body mass for 48 h beginning on either day 3 or 6 of life. Controls were fed according to an age-specific feeding schedule that yielded normal growth curves. During realimentation, restricted nestlings did not achieve a faster rate of growth than that of controls. Instead, these nestlings either died (all controls lived) or gained mass at a rate similar to that of controls. Consequently, restricted nestlings reached asymptotic mass two days later than control nestlings. Growth of culmen and tarsus was not affected, but growth of the eighth primary was reduced for several days in nestlings restricted at day 6 (i.e. late restricted), although this difference disappeared by the age of fledging. Because surviving nestlings achieved only a 15.9% increase in food consumption compared with unrestricted controls and were unable to translate it into a faster rate of growth, the nestlings may have been growing at a maximum rate. We found no differences between late-restricted and unrestricted nestlings in % water, % protein, % lipid, and % ash. The two groups were of similar maturity as measured by % body water and the water index. Our results are consistent with current theory in that periods of food restriction delayed the schedule of mass accretion by the length of the restriction period. Although House Sparrows have a labile growth rate and developmental time, our results did not support the hypothesis of compensatory growth. Based on this and one other study, compensatory growth does not appear to occur in altricial birds. Received 6 May 1998, accepted 16 June 1999. POSTNATAL GROWTH IN BIRDS is a period of rapid mass gain, tissue maturation, and anatomical development. Given these changes, postnatal growth is viewed as one of the most energetically demanding periods in a bird’s life cycle (Ricklefs 1983). Numerous hypotheses have addressed how growth rates are ecologically adapted and potentially constrained (e.g. Lack 1968, Ricklefs 1969, Lilja et al. 1985, Bosque and Bosque 1995). To date, it has been generally accepted that the transition from neonate to fledgling is a relatively fixed process. However, a growing body of literature indicates that growth and development can be quite variable. Sources of this variation include habitat differences (Richner et al. 1989), levels of food abundance (Martin 1987, Cruz and Cruz 1990), diet quality (Boag 1987, Johnston 1993), parasite loads (Møller 1990, Clayton and 1 Present address: Department of Fisheries and Wildlife, Michigan State University, East Lansing, Michigan 48824, USA. E-mail: [email protected] Tompkins 1995), weather (Murphy 1985, Keller and Van Noordwijk 1994), and asynchronous hatching (Nisbet et al. 1995). Of these sources, food abundance and diet quality are of particular interest because they represent the energy and nutrients necessary for growth and development. Different species may respond in markedly different fashions to fluctuations in food abundance or quality. For example, nestling Zebra Finches (Taeniopygia guttata) fed a low-quality diet gained mass slower, reached a lower adult mass, and had shorter tarsi than control birds fed a diet that was richer in protein (Boag 1987). Similarly, studies of European Robins (Erithacus rubecula) and Carrion Crows (Corvus corone) have shown that ephemeral periods of poor food conditions result in abnormal growth, permanent stunting, lower fledging mass, and/or increased mortality (Lees 1949, Richner et al. 1989). In contrast, European Swifts (Apus apus; Lack and Lack 1951), Mangrove Swallows (Iridoprocne albilinea; Ricklefs 1976), House Martins (Delichon urbica; Bryant 1978), and January 2000] 165 Food Restriction and Growth White-fronted Bee-eaters (Merops bullockoides; Emlen et al. 1991) resumed normal growth rates with no detrimental effects following ephemeral periods of poor food conditions. The ability to adjust growth rate, or the time to reach a developmental endpoint, to prevailing food conditions is termed labile development, which is a form of developmental plasticity (Smith-Gill 1983, Schew and Ricklefs 1998). Within the context of developmental plasticity lies an interesting but poorly studied phenomenon known as compensatory (i.e. catchup) growth. Compensatory growth is best defined as an accelerated growth rate relative to age that occurs after a period of poor food conditions or environmental perturbations (Bohman 1955). True compensatory growth is marked by the addition of protein, minerals, and water. This is important to note because growth in its proper sense is represented by increases in protein and skeletal development, not increased fat deposition (Maynard et al. 1979). Originally described in poultry and other agricultural animals (Wilson and Osbourn 1960), compensatory growth has been observed in numerous taxa including invertebrates (Calow and Woolhead 1977), fish (Dobson and Holmes 1984), amphibians (Alford and Harris 1988), and mammals (Wilson and Osbourn 1960). Among birds, compensatory growth has been demonstrated in one precocial species (Japanese Quail [Coturnix japonica]; Schew 1995), one semiprecocial species (Jackass Penguin [Spheniscus demersus]; Heath and Randall 1985), and one semialtricial species (American Kestrel [Falco sparverius]; Negro et al. 1994). Notably scarce are tests of compensation in altricial birds. Konarzewski et al. (1996) tested for compensation in the Song Thrush (Turdus philomelos) following a period of food restriction and found no increase in growth rate. However, nestlings were overfed 24 h a day for two days and then sacrificed. Thus, no measure of growth until fledging or adulthood was obtained. The only other study investigating compensatory growth in altricial nestlings found no accelerated growth in European Starlings (Sturnus vulgaris; Schew 1995). Nevertheless, given the number of altricial species that exhibit labile development, coupled with the lack of studies, the presence of compensatory growth in altricial birds remains open to question. Accelerated growth after food restriction in altricial birds would indicate that the normal growth rate is not at the physiological maximum, but rather operates in some optimal manner (Schew and Ricklefs 1998). The question of optimality versus maximality is important because several hypotheses hold that altricial growth rates are maximal, being limited only by some physiological bottleneck. In particular, growth is thought to be limited by bottlenecks in either tissue maturity or the digestive system (e.g. Ricklefs 1969, 1979; Lilja et al. 1985, Konarzewski 1988; Ricklefs et al. 1994). As such, accelerated growth would indicate that nestlings are not growing maximally and hence are not limited by a physiological bottleneck. Another question that can be addressed when investigating accelerated growth is the concept of absolute time schedules. If fledging is a relatively fixed event chronologically, then two possibilities exist following an environmental perturbation: (1) accelerated growth resulting in ‘‘normal’’ fledging mass; or (2) normal or retarded growth resulting in decreased fledging mass. Thus, if compensatory growth or subnormal fledging mass were observed following an ephemeral period of poor food conditions, it would suggest that fledging or asymptotic mass occurs at a relatively fixed time in the nestling’s life cycle. Because of the short developmental time in altricial birds, the observation of compensatory growth could significantly alter the view of fixed growth and development. We used ephemeral food restrictions to simulate environmental perturbations as a means to slow growth and development. Following the restriction, food provisioning became unlimited to allow nestlings an opportunity to respond. Here, we report on the response of nestling House Sparrows (Passer domesticus) to these conditions and discuss the implications for altricial birds.