SEVERAL STUDIES IN Europe and North America have suggested links among soil acidification, soil calcium depletion, and reduced avian population sizes or impaired avian reproduction.^1,2,3 Birds may be particularly sensitive to soil calcium depletion because they require large amounts of calcium to successfully produce eggshells and raise young.^4,5 For example, to produce a single clutch of eggs, some small bird species require more calcium than is in their entire skeleton.⁶ Small songbirds, which do not store much calcium for reproduction and do not have enough calcium in their normal diets to produce eggs, must rely on calcium-rich food supplements (particularly snails) at the time of reproduction.^5,7 The availability of snails is typically related to the availability of calcium in the soil, because snails require high levels of calcium to produce highly calcified exoskeletons and to reproduce.^3,8 In areas of Europe where acidic deposition has driven down snail abundance, songbirds have laid eggs with thin or even no eggshells.³ Calcium has also been observed to limit clutch size, reproductive success, and skeletal development of chicks.^9,10

Understanding the relationships between forest songbirds and soil calcium availability is of great importance in the northeastern United States, where decades of acidic deposition and forest harvesting and aging have resulted in chronically acidified forest soils with depleted calcium availability.^11,12,13 The majority of forested lands in the northeastern United States have naturally acidic soils that are sensitive to acid inputs and receive high levels of acidic atmospheric deposition.¹⁴ Approximately 17% of U.S. forest soils exceed critical acidic deposition loads, with the greatest concentration of acidified forests in the Northeast.¹⁵ In a previous study,¹ we reported preliminary results of a large-scale soil-liming experiment conducted, in part, to determine whether songbird abundance and breeding performance were related to soil calcium availability. We observed a positive response in bird abundance (all species) to liming 3 years after calcium addition, but we did not observe effects of liming on territory size, density, or breeding performance of the focal species, the Ovenbird (Seiurus aurocapilla). We hypothesized that, given more time, we would observe positive responses by Ovenbirds to liming and the increased availability of calcium-rich food, and thus we returned 2 years later to test our hypothesis. We also tested the hypothesis that Ovenbird abundance and breeding performance would be related to soil calcium availability across a natural soil-calcium gradient.

Although forest soils in the northeastern United States have low and declining levels of calcium availability and experience high levels of acid deposition, the severe reproductive anomalies that have been observed in acidified areas of Europe³ have not been seen in North American birds.¹⁶ Nonetheless, some evidence suggests that habitat quality of forest songbirds—and, consequently, their abundance—may be restricted by soil calcium availability.^2,17 However, we lack knowledge of the mechanism(s) by which low and declining soil calcium is related to declines in bird abundances. Potential mechanisms include either reduction of calcium needs by reducing reproductive output or enlargement of territory size (and consequent drop in population density) to provide a sufficient supply of calcium-rich foods for eggshell production and for feeding nestlings.

In the present study, we quantified the relationship between soil calcium and Ovenbird population parameters and breeding performance on experimental and observational plots. Ovenbirds are Nearctic—Neotropical migrants that breed throughout northeastern forests.¹⁸ They forage on forest-floor invertebrates, the abundance and distribution of which are typically linked to soil condition. Ovenbird nests are also accessible because they are located on the ground.^18,19 We hypothesized that birds in acidified forests are calcium-limited and that bottom-up processes of nutrient availability influence Ovenbird populations. Consequently, forests with higher soil calcium availability should provide better habitat for Ovenbirds via greater availability of calcium-rich food to support egg production. Thus, we predicted increases in reproductive output and eggshell thickness, and decreases in territory size, in response to observed increases of soil calcium and snail abundance that followed our liming treatment. In addition, in areas that varied naturally in soil calcium availability, we predicted higher reproductive output, thicker eggshells, and smaller territories in areas with higher soil calcium. Although many factors can influence bird territory size,²⁰ we predicted—on the basis of our hypothesis of calcium limitation and relationships between habitat quality and calcium availability—that calcium availability would be a strong driver of both bird density and territory size.

CALCIUM MANIPULATION

We conducted a liming experiment at four 100-ha forest sites in central Pennsylvania. We measured Ovenbird territory size and quantified breeding performance in 2008 and compared the data with our observations made before (2003) and for 3 years after (2004–2006) dolomitic limestone sand was applied to two of the four sites.¹ Lime was applied at 4,500 kg ha^-1 using a modified log skidder.¹ We evaluated the effect of liming using the confidence intervals around a time × treatment interaction parameter in a before—after control—impact analysis.²¹ Liming successfully increased soil calcium and snail abundance.¹ For details on methods, see our earlier study.¹ Results are presented as means ± SE.

We observed a positive effect of liming on territory density, but no effect on territory size (Fig. 1). Territory density increased by 0.15 ± 0.02 territories ha^-1 on limed sites from before liming to 5 years after, whereas no change occurred on control sites (0.04 ± 0.04 change in territories ha^-1). New territories were formed within areas on limed sites that were previously unoccupied, resulting in an increase in territory density without a decrease in territory size (Fig. 2).

We used the number of nests found in each 100-ha site over the entire season by S.E.P., the primary individual to locate nests in all years, as a proxy of nest density (nest density index). Using this measure, we observed a positive effect of liming on the nest density index (Fig. 1). The nest density index did not change from before liming to 5 years after liming on control sites (0.05 ± 0.13 change in number of nests) but increased sevenfold on limed sites (0.38 ± 0.09 change in number of nests).

We also observed larger clutch sizes on limed sites. Comparisons were restricted to nests completed before 15 June (to limit the sample to first nests of the season) and were made by comparing nests from limed and unlimed sites because we did not find enough nests at each site in every year to support a year-by-year analysis. Modal clutch size at both limed and control sites was 5 eggs, but 6-egg clutches were observed only on limed sites (Fig. 3), and overall mean clutch size was larger on limed sites (Table 1). We observed no differences in egg size, shell thickness, or shell mass between limed and control sites in the years after liming (Table 1). Nest success (survival of eggs and nestlings to fledging) did not differ substantially between limed (Mayfield nest success = 0.44; 95% confidence interval [CI]: 0.31–0.63) and unlimed (0.31; 95% CI: 0.19–0.51) sites.

FIG. 1.

Ovenbird territory size, territory density, and nest density index (number of nests found by one common observer per 100-ha site, ± SE) for each year on control (open squares) and lime-treated (closed circles) sites with model lines and the confidence intervals for the time × treatment interaction parameter to indicate the fit of the model to the data. Treatment was applied between 2003 and 2004. Differences in the slope of the model lines from 2003 (before liming) to 2008 (after liming) on limed compared with control sites indicate an effect of liming on that variable, as measured using the time × treatment interaction. Asterisk indicates confidence intervals (in parentheses) of the time × treatment interaction that excluded zero and thus indicated a significant effect of liming on that variable.

FIG. 2.

Ovenbird territories on a lime-treated site in Pennsylvania (A) in 2003, before lime application; and (B) in 2008, 5 years after lime application. Polygons represent individual Ovenbird territories, and the rectangle represents the 30-ha gridded area used for mapping territories.

FIG. 3.

Proportion of Ovenbird nests found in the early breeding season (before 15 June) with each clutch size on control (n = 33) and limetreated (n = 28) sites during the years after liming (2004, 2005, 2006, and 2008), and on seven low-soil-calcium (<7.0 meq Ca per 100 g; n = 19) and seven high-soil-calcium (>8.9 meq Ca per 100 g; n = 37) sites in 2006, 2007, and 2008, in Pennsylvania.

OBSERVATIONAL STUDY

We conducted an observational study at fourteen 100-ha forest sites throughout central Pennsylvania. We chose seven sites located on bedrock with a limestone component as “high-calcium” sites (mean = 14.6 ± 2.0 meq Ca per 100 g; range: 8.9–23.4) and seven sites located on bedrock without a limestone component as “low-calcium” sites (mean = 6.2 ± 0.3 meq Ca per 100 g; range: 5.3– 7.0). We visited sites for an equivalent number of days to collect data on Ovenbird territory size and breeding performance. We also calculated the proportion of territories with nests, the date of clutch initiation for the earliest nest, and the mean number of nests found in territories with nesting Ovenbirds. Because Ovenbirds raise a single brood each year and nest success did not differ between low- and high-calcium sites (below), the number of nests per territory represents the propensity of females to renest following nest failure. Snail abundance was positively correlated with soil calcium (r = 0.78, P < 0.001). Four of the 14 sites were defoliated by Gypsy Moth (Lymantria dispar) larvae during the study. Gypsy Moth defoliation can affect the abundance of breeding birds, so we added a Gypsy Moth term to the statistical models.²²

TABLE 1.

Differences in Ovenbird clutch size and egg measurements from nests found early in the season (before 15 June) between control and lime-treated sites in all years after liming (2004, 2005, 2006, and 2008) and between seven low-soil-calcium (<7.0 meq Ca per 100 g) and seven high-soil-calcium (>8.9 meq Ca per 100 g) sites in 2006, 2007, and 2008 in Pennsylvania. Ninety-five percent confidence intervals [CIs] are in parentheses; asterisks denote CIs that exclude zero, indicating a difference between the two groups.

We observed positive relationships between soil exchangeable calcium and Ovenbird territory density, nest density index, proportion of territories with nests, and number of nests found in each territory with nesting birds (Fig. 4). We observed negative relationships between soil calcium and territory size and the date of clutch initiation for the earliest nest (Fig. 4). We found between 1 and 23 nests at each site. Because we found few nests at most of our low-calcium sites, we compared sites on the basis of bedrock geology for nest and egg analyses. We observed larger clutch sizes at the high-calcium sites than at the low-calcium sites for nests completed before 15 June (Table 1 and Fig. 3). As in the liming experiment, we observed no relationships between soil calcium and egg size, shell thickness, and shell mass (Table 1). Nest success did not differ between high-calcium (Mayfield nest success = 0.22; 95% CI: 0.14–0.34) and low-calcium (0.25; 95% CI: 0.13–0.47) sites.

DISCUSSION

The increase in territory density and clutch size in response to our addition of calcium to soils demonstrates causality and establishes that soil calcium is an important determinant of Ovenbird habitat quality. Our experimental results are supported by the relationships between calcium availability and both territory density and clutch size under natural conditions in the observational study. We used territory density and size, as well as reproduction, as indicators of habitat quality because density alone can be a misleading indicator of habitat quality and reproductive potential.²³ Because Ovenbird habitat quality was positively related to soil calcium, depletion of soil calcium by acid deposition could potentially negatively affect Ovenbird abundance and productivity. This conclusion, which is likely applicable to other Nearctic—Neotropical migratory songbirds breeding in eastern forests, provides strong support for the conclusions of the indirect, correlative studies that identified a link between high levels of acid deposition and declining forest songbird abundances in North America. ^2,17

Our results and those of other studies suggest that snail availability was an important link between soil calcium and Ovenbird territory density and breeding performance. ^1,3 Increases in snail availability could directly affect clutch size and the probability that females produced clutches by increasing the calcium in bird diets. Indirectly, increased snail availability could make the tradeoff between acquiring calcium-rich and energy-rich food more manageable, giving females the opportunity to acquire more energy, or other resources, for reproduction. We also observed increases in bird densities with increased soil calcium, which indicates a likely indirect effect of calcium availability. Potentially, the increase in population and individual productivity could result in greater recruitment in future years. Also, if birds are using habitat variables related to soil calcium to evaluate habitat quality, these indicators would result in more bird territories. In the observational study, many habitat features changed with soil calcium, including snail abundance and vegetative characteristics that Ovenbirds could use to evaluate habitat quality. In the liming study, however, we observed very little change in vegetation (S. E. Pabian unpubl. data), which suggests that, of the variables that we measured, snails were the most likely mechanism for changes in Ovenbird abundance and reproduction.

FIG. 4.

Relationships between soil calcium and Ovenbird territory size, territory density, nest density index (number of nests found by one common observer per 100-ha site), proportion of territories with at least one nest, mean number of nests found within territories with nesting Ovenbirds, and the date that we observed the first nest with one egg at 14 sites across central Pennsylvania (2006–2008). Model lines were calculated using the 10 sites not defoliated by Gypsy Moths. The 95% confidence intervals (CIs; in parentheses) for the slope parameter estimates are included in each graph for model evaluation. Asterisk indicates that the CI excluded zero and therefore indicated a significant relationship of a variable with soil calcium (or snail abundance).

More fertile soils usually have higher productivity, as measured by the yield in crops or timber that a soil can support. Similarly, for forest songbirds, fertile soils with more calcium were more productive. The addition of limestone sand increased soil calcium availability by approximately 2.3-fold,¹ which resulted in a 1.8-fold increase in Ovenbird territory density and 1.1× larger clutch sizes. If we assume similar nesting success (as we documented) and renesting rates, the increase in territory density and clutch size yielded twice as many young from experimentally limed plots as from control sites. Extrapolating from the observational study produced a similar conclusion. Given the 0.05 territories ha^-1 increase in territory density for every 10% increase in natural soil calcium, and 9.5% larger clutch sizes on high-calcium sites, we would expect a 2.82-fold difference in productivity between our lowest (5.3 meq Ca per 100 g) and our highest-calcium site (without Gypsy Moths; 12.6 meq Ca per 100 g). Further, renesting rate is higher in areas with higher soil calcium, potentially making the difference even greater. The predicted increases in productivity are also based on the assumption that survival of young is equal once they have fledged, but other research has shown that birds supplemented with calcium often produce larger fledglings²⁴ and that larger fledglings often exhibit higher first-year survival.²⁵ Higher potential recruitment of young fledged from sites with more calcium available would magnify the difference in productivity between low- and high-calcium sites.

Surprisingly, we observed evidence of calcium limitation without observing thin eggshells. Although thin eggshells were one of the most extreme warning signs of the negative effects of acid deposition on forest birds in Europe,³ researchers have failed to find evidence of severe reproductive anomalies in the acidified forests of North America^16,26 and in other studies across northeastern forests.^27,28,29 Like other North American studies, our study found no evidence of thin eggshells, even in low-calcium forests with some of the highest levels of acid deposition in the country and soil calcium levels comparable to those in Europe, where thin eggshells were observed.^1,3,25 We found no relationships between any eggshell measurements and calcium availability and actually observed some of the thickest eggshells from sites with the lowest soil calcium levels.

A potential mechanism that explains low bird abundance without thin eggshells in areas with extremely low soil calcium is that bird species studied in North America simply forgo reproduction when they cannot find enough calcium. We found nests in a lower proportion of territories at sites with low soil calcium, possibly because some pairs did not reproduce or because some males did not attract mates. Birds may compensate for thin eggshells by using protoporphyrin pigmentation to strengthen thin eggshells.³⁰ However, a preliminary examination of Ovenbird eggshell pigmentation yielded no evidence for relationships between the density or size of pigmented patches and soil calcium or eggshell thickness (S. E. Pabian unpubl. data).

Although we observed no relationships between soil calcium availability and eggshell thickness, we found a strong trend toward thinner eggshells at our sites with high soil calcium. Similarly, Taliaferro et al.¹⁶ observed a trend toward thinner eggshells in Black-throated Blue Warblers (Dendroica caerulescens) nesting in a northeastern U.S. forest with higher natural availability of soil calcium. Although counterintuitive, it is important to note that the extremely low frequency of hatching failure that we detected (<1% of eggs) suggests that even the thinnest eggshells in our study were thick enough to avoid reproductive problems. Ovenbirds on sites with low calcium started laying eggs later in the season and rarely laid a replacement clutch if the initial attempt failed. Potentially, females at low-calcium sites responded to the low availability of dietary calcium by delaying initial egg laying in order to find enough resources to reproduce and invest more in their eggs because it was their only attempt for the season. By contrast, at sites with higher soil calcium, we observed earlier dates of first nesting and up to three renesting attempts by females whose previous nests failed. Potentially, females at these sites responded to the high availability of dietary calcium by investing slightly less calcium in their eggs because they had the opportunity and nutritional resources to renest.

In conclusion, Ovenbird habitat quality was linked to soil calcium availability and there is now experimental evidence that calcium limitation exists in forest songbirds in North America. The positive responses of territory density and clutch size to liming provided evidence of strong bottom-up control of avian population processes in a nutrient-depleted forest. Our finding that birds can be calcium-limited without displaying obvious reproductive problems, in contrast to what has been observed in Europe,¹⁰ suggests the possibility that effects of calcium limitation on other avian species of eastern forests may be widespread but go undetected because of their subtle effects. Our results provide strong, experimental evidence to support the correlations observed by James et al.¹⁷ and Harnes et al.² of low or declining populations of forest songbirds in acidified forests in North America. We therefore posit that reductions in soil calcium, in addition to habitat loss and fragmentation, are contributing to declines in the abundance of songbirds in acidified forests.