Food provisioning in relation to reproductive strategy in altricial birds: a comparison of two hypotheses.
Two, not mutually exclusive, hypotheses were summarized by Lack (1968) to explain how parental provisioning rates should relate variation in reproductive traits. The first hypothesis assumes clutch size to be closely adjusted by the amount of food the parents are able to provide during the period when nestlings' food demands are highest (Lack 1947, 1966). Thus, large provisioning rates should be found in species with large clutch sizes. Several studies have demonstrated the importance of food for intraspecific variation in avian reproductive performance (for reviews, see Martin 1987; Boutin 1990). The second hypothesis assumes that rapid growth rates to reduce predation losses influence provisioning rates. Selection for short fledging periods should lead to investment of the available resources into rapid growth rates, rather than increased offspring number. In accordance with this hypothesis, species nesting on the ground, and therefore more susceptible to nest predation, have higher growth rates (Ricklefs 1968a) and smaller clutch sizes (Saether 1985; Kulesza 1990) than species nesting in concealed nests. Thus, the energetic input into the nests should be independent of clutch size according to this hypothesis.
A problem which is frequently encountered in comparative studies (Harvey and Mace 1982; Pagel and Harvey 1988; Harvey and Pagel 1991) is the confounding effects of body weight. Differences in clutch size and provisioning rate are related to differences in body weight, i.e., large birds lay a smaller number of eggs (Saether 1987) and have offspring that grow more slowly (Ricklefs 1973) but need more energy (Calder 1984) than those of smaller birds.
In this paper I use a recently developed comparative technique (Harvey and Pagel 1991) to show that, after accounting for the effects of body weight and common ancestry, clutch size in altricial birds is most closely associated with the amount of food that the parents are able to provide to their offspring.
METHODS AND MATERIALS
This study is based on provisioning rates from 73 species. The data include species from the orders Sphenisciformes, Procellariiformes, Pelecaniformes, Falconiformes, Charadriiformes, Strigiformes, Apodiformes, Coraciiformes, and Passeriformes. Only studies which measured the actual amount of food brought to the nest were included in the analysis. This was measured in two ways. In some species (e.g., marine species) the amount of food brought to the nest was the difference between the weight of the offspring just before and after feeding. When multiplied by the feeding rate, an estimate of the provisioning rate per 24 h was obtained. In other species (e.g., raptors) the food provisioning rate was estimated from the weight of prey items taken to the nest during a certain period. Since the provisioning rate was often dependent on the age of the nestlings, the mean rate during the period of highest demand (the asymptotic value) was used in the comparisons. For smaller species this usually occurred during the period when they grow from 25% to 75% of their fledgling weight. To compare species with different diets, the provisioning rates of mass were expressed in terms of energetic content of the diet, assuming mean energetic content of 3.97 kJ [g.sup.-1] for fish, 4.35 kJ [g.sup.-1] for krill, 3.47 kJ [g.sup.-1] for squid (Croxall et al. 1985), 8.4 kJ [g.sup.-1] for mammals, 5.4 kJ [g.sup.-1] for birds (Robbins 1983), and 23.01 kJ [g.sup.-1] (dry weight) for insects (Bryant and Westerterp 1983). The data are listed in the appendix.
Modal clutch size was estimated from the data bases of Croxall (1984), Saether (1987), or of single-species studies of breeding biology. Growth curves of nestlings were characterized by the logistic growth constant K. Most values were taken from Ricklefs (1968a, 1973), Croxall (1984), and Bortolotti (1986). In some cases, values were computed from raw data by the method described by Ricklefs (1968a). A complete data set, including values for food provisioning rates, body weight, clutch size (modal size), and growth rate, was available for 52 species.
Common ancestry is a problem in examinations of adaptive variation in comparative data sets (Ridley 1983; Harvey and Pagel 1991). If variation in a character (e.g., clutch size) has evolved within lineages, rather than separately for each species, taxonomic lineages with many species will be overrepresented in the analyses, while those with only a few species will be underrepresented. Hence, species do not represent independent values. A test of the adaptive significance of variation in a character (e.g., clutch size) must therefore consider this phylogenetic effect.
Felsenstein (1985) suggested a method that produces a set of independent comparisons among pairs of species and higher nodes of the phylogeny, based on the assumption that the difference between a pair of taxa that share an immediate common ancestor is independent of differences elsewhere in the phylogenetic tree. However, the method is dependent on the true bifurcating branching pattern of the phylogeny being known. Therefore, I used a modification of Felsenstein's method based on incompletely known phylogenies (Harvey and Pagel 1991; Harvey and Purvis 1991). A standardized linear contrast for each variable was computed according to Pagel (1992). Because the sum of these linear contrast coefficients must be zero, they can be considered a weighted difference score (Harvey and Pagel 1991). If the taxonomy is a coarse representation of the unknown bifurcating phylogenetic relationship between species, such a standardized linear contrast can be calculated for each node in the phylogenetic tree. In such a way, the information contained in n daughter taxa is reduced to a single value for each variable. Accordingly, each taxon then contributes only one independent value for each variable in the analyses. If a positive relationship between two variables exists, a positive relationship between their contrasts is expected, using a regression through the origin (Garland et al. 1992), with the number of data points equal to the number of taxa for which it was possible to compute a contrast. For other examples of applications of this method in comparative studies, see Harvey and Pagel (1991), Pagel and Harvey (1989), and Trevelyan et al. (1990).
This method assumes that evolution behaves like a random-walk process, that is, that the rate of evolutionary change per unit branch length is equal in all branches of the phylogeny (Harvey and Pagel 1991). In order to check whether the contrasts were adequately standardized, I plotted the value of the contrast against the variance of the raw contrast. In no case was a significant correlation found, thus supporting our branch-length assumption. Garland et al. (1992) found that correlations between the standardized contrasts using four different branch-length assumptions were quite similar. Furthermore, the independence of the residuals of the regression involving the standardized contrasts were examined by the Durbin-Watson test statistic, which in none of the cases was significant (P [greater than] 0.1).
TABLE 1. The linear regression (through the origin) between the standardized contrast coefficient for provisioning rate of energy (kJ/24h) by the parents to the offspring, clutch size (eggs), growth rate, and body weight (g) (logarithmically transformed values) in altricial birds. Dependent Independent variable variable Slope [r.sup.2] n Provisioning rate body weight 1.03 0.42(***) 45 Clutch size provisioning rate 0.03 0.03 45 Growth rate provisioning rate -0.06 0.06 20 *** P [less than] 0.001.
Taxonomic classification based on DNA-DNA hybridization techniques probably represents the best way of reconstructing the branching pattern of the phylogeny of living birds (Harvey and Pagel 1991). Accordingly, the taxonomy follows Sibley et al. (1988) for tribes and above, whereas the generic and species classification follows Howard and Moore (1984). All analyses are made on logarithmically transformed values.
Clutch size among species was significantly correlated with the amount of energy provisioned to the offspring (r = 0.33, n = 72, P [less than] 0.01). In contrast, differences in growth rate were unrelated to variation in provisioning rate (r = 0.04, n = 53, P [greater than] 0.1). When the effects of body size were removed by a partial-correlation analysis, however, both reproductive traits correlated significantly with provisioning rate ([r.sub.P] = 0.79, P [less than] 0.001 for clutch size and [r.sub.P] = 0.71, P [less than] 0.01, n = 52 for growth rate). Thus, species with the ability to provide a relatively (for their body weight) large amount of food to their offspring produced more offspring, which grew faster than species with lower provisioning rates.
In order to control for the effects of phylogeny, standardized linear contrasts for provisioning rate, clutch size, and growth rate were computed. The provisioning rate of altricial birds increased significantly with body weight, using a regression through the origin. However, no significant correlation occurred either between the standardized contrast coefficients for clutch size and provisioning rate, or between the standardized contrast coefficients for growth rate and provisioning rate. Thus, variation in both life-history traits was independent of the amount of food provided.
This lack of relationship between the two reproductive traits and provisioning rate could be caused by a covariation with body size. Accordingly, a significant negative relationship was found between the standardized contrast coefficients for growth rate and body weight (r = -0.56, n = 20, P [less than] 0.01). This shows that the development time of altricial species increases with adult size (Ricklefs 1973). On the contrary, variation in body weight did not explain any significant proportion of the variance in clutch size (r = 0.11, n = 45, P [greater than] 0.1).
A positive relationship occurred between the standardized contrasts for clutch size and provisioning rate after controlling for the effects of body weight (fig. 1a, r = 0.34, n = 45, P [less than] 0.05). No positive association was found between the contrasts for growth rate and provisioning rate after controlling for the effects of body weight (fig. 1b, r = -0.02, n = 20, P [greater than] 0.1). Thus, for any given body size, taxa with a relatively high provisioning rate lay relatively larger clutches.
These relationships were summarized in a multiple-regression analysis through the origin. The standardized contrasts for clutch size showed a significantly positive correlation to the contrasts for provisioning rate (b = 0.10, t = 2.80, P [less than] 0.05) and growth rate (b = 0.39, t = 2.75, P [less than] 0.05) but only a weak negative correlation with body weight (b = -0.17, t = 2.02, P [less than] 0.1). On the contrary, a similar multiple-regression analysis of the standardized contrasts for growth rate showed that only the clutch size yielded a significant effect (b = 0.80, t = 2.75, P [less than] 0.05). Thus, a positive covariation existed between clutch size and nestling growth rate, whereas clutch size was also dependent on an ecological variable, that is, the ability of the parents to provide food to their offspring.
In birds, metabolic rates scale allometrically with body weight (Bennett and Harvey 1987; Nagy 1987). Walsberg (1983) found that peak expenditure per nestling scaled with body weight to the power of 0.528. According to the relationship presented in table 1, the total amount of food brought to nest also increases with body weight, suggesting a larger burden to the parents of small as opposed to large, species to satisfy the requirements of the nestlings. However, the slope (1.03) of food provisioning rate on body weight is very similar to an isometric slope of 1, showing that large species do not provide relatively more food to the nest for a given body weight than small species. The residual variation around this relationship between energy demand and body weight is still considerable, suggesting that ecological factors also may be important in determining the brood's energy requirements.
The significant effect of clutch size on growth rate suggests that these traits do not evolve independently of each other. However, there is no support for an evolutionary trade-off between a large clutch size and a rapid growth rate (Lack 1968; Ricklefs 1968b). On the contrary, they were positively related. This supports previous analyses (Saether 1987) which show that a short development time is found in taxa with large clutch sizes.
The significant relationship between clutch size and the amount of energy provided to the offspring, even after accounting for the effects of body weight shows that a large reproductive rate evolves in species with a high provisioning rate. Three mechanisms may explain such a relationship between provisioning and clutch size. First, if all species feed their offspring at the maximum rate, the present results suggest that food limits the reproductive output, as first argued by Lack (1947, 1968). Thus, larger clutch size should be found among species that live in the most productive environments.
Second, a difference in provisioning rate may occur if some species have more energy to spend on nesting than others. Some species may be more efficient in using the food resources available in the environment than others. Analysis of the energy expenditure during the breeding season shows large variation (Nagy 1987). Some evidence suggests, however, that the maximum sustained working level of a parent bird feeding its offspring scales allometrically with body weight, irrespective of clutch size, and is about 4 times the basal metabolic rate (Drent and Daan 1980). Furthermore, no consistent relationship between relative energy expenditure and food provisioning rate was found in 10 bird species (Bryant 1988). Thus, a positive relationship between the rate of energy provisioning to the offspring and the daily energy expenditure by the adults is unlikely to explain the differences across species in their ability to provide food to their offspring.
Third, the birds may not feed the brood at their maximum capacity. A magnitude of factors may regulate clutch size of altricial birds (Murphy and Haukioja 1987; Godfray et al. 1991). For example, it has been suggested that to increase the probability of future survival, parents in long-lived species should use only a small proportion of their available energy on breeding (Goodman 1974). A small clutch size may also be favored in order to reduce the number of visits to the nests, thereby reducing the attraction of nest predators (Lack 1968). The lower provisioning rate among species with small clutch size may reflect a smaller demand. Thus, reduction in clutch size may have evolved to reduce the parental effort needed to raise the offspring to independence.
No evidence was found to connect rapid growth rates with high provisioning rates. A change in development time is likely to involve changes in several physiological and anatomical processes, which are likely to impose strong constraints on variation in nestling growth rates (Ricklefs 1979, 1983). Such physiological constraints are likely to be more similar for closely related species than for more distantly related taxa. Thus, when correcting for common ancestry, it was not unexpected that the relationship between growth rate and provisioning rate recorded in the raw data disappeared.
Although I cannot conclusively identify the mechanism behind the regulation of reproductive output in altricial birds, I suggest that the present results support previous analyses of the importance of food limitation for life-history evolution (Martin 1987; Boutin 1990). Several theoretical analyses have documented that variation in adult mortality rate has a strong impact on the evolution of life-history characteristics (Charlesworth 1980; Charnov 1991). Across European bird species, clutch size decreases with delayed maturity and increased adult survival rate (Saether 1988). Similar relationships have also been observed in other taxa (Promislow and Harvey 1990). The present results (fig. 1) show that ecological factors affecting the ability of the parents to provide food to their offspring may constrain an evolutionary response in reproductive rates to a change in other life-history traits, for example, to increased mortality. In birds, as well as in other taxa, such a relationship between ecological variables and life-history variation has been difficult to demonstrate (Patridge and Harvey 1988). Thus, identifying how different environmental characteristics influence food provisioning rates may provide an important link between ecology and life-history variation.
I am grateful to A. Purvis, O. Bakke, and M. Heim for help in the data analysis. D. Anderson, M. Elgar, J. Felsenstein, I. Flemming, T. Hanley, P. H. Harvey, J. Linell, A. P. Moller, E. Roskaft, T. Slagsvold, and R. Trevelyan kindly commented on previous drafts.
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|Title Annotation:||includes appendix|
|Date:||Aug 1, 1994|
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