Productivity per nest attempt. Average productivity per nest attempt across time at 5%, median, and 95% observed values of forest cover (23%, 53%, and 94%, respectively) for a balanced population of three songbird species in a study of brood parasitism and nest predation in Missouri, USA, 1991–2010. Error bars represent 95% confidence intervals and are offset for visual clarity. doi:10.1371/journal.pone.0047591.g006 

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... of possible values that was constrained by each term’s standard error. We then calculated productivity as fledging brood size 6 nest survival probability. We repeated this 10,000 times and treated the mean value as a point estimate of productivity and the 2.5% and 97.5% values as the confidence limits. All analyses were performed using SAS [29]. Mean values are presented with standard errors unless otherwise indicated. Forest cover in the 10 counties surrounding our nests increased 7% (640,628 ha to 682,725 ha) between 1989 and 2010 according to FIA data. In contrast, NLCD data from a 10-km radius surrounding each nest suggested that forest cover declined by 1.8% from 1992 to 2001, and by 0.4% from 2001 to 2006. Of the nests monitored wherein contents were reliably observed, 423 of 1,524 (28%) bunting nests, 76 of 1,021 (7%) flycatcher nests, and 79 of 367 (22%) cardinal nests were parasitized. All three species were well represented across the gradient of forest cover (Fig. 2; bunting mean: 58 6 1%, range: 23–95%; flycatcher mean: 70 6 1%, range: 23–95%; cardinal mean: 44 6 1%, range: 23– 95%). Forest cover strongly influenced parasitism rates with a mean predicted parasitism rate of 33% (95% CI: 28–37%) for a population of nests balanced across species at 23% forest cover (the 5 th percentile of observed forest cover values) versus 3% (95% CI: 2–4%) for a population of nests at 94% forest cover (the 95 th percentile). A parameter for year was in the two best-supported parasitism rate models, which combined for 100% of the overall weight of evidence (Table 1). Parasitism rates differed between species and declined across time (Fig. 3a). A parameter for year was also in the top two parasitism intensity models, which combined for 98% of the overall weight of evidence (Table 1). The mean number of cowbird eggs per parasitized nest differed among species (buntings: 1.43 6 0.03; flycatchers: 1.09 6 0.04; cardinals: 1.23 6 0.06) and declined across time (Fig. 3b). There was a substantial effect of brood parasitism on fledging brood size; fledging brood sizes were greater for unparasitized versus parasitized nests for buntings (2.79 6 0.12 versus 1.47 6 0.14 fledglings), flycatchers (2.50 6 0.13 versus 1.17 6 0.15 fledglings), and cardinals (2.82 6 0.15 versus 1.50 6 0.16 fledglings). The best- supported model for fledging brood size did not include a covariate for year, but there was considerable model-selection uncertainty (Table 1), and model-based predictions of fledging brood size increased across time (Fig. 4) because the predictions incorporated the negative association between parasitism rates and year. The effect size of the increase in fledging brood size from 1991 to 2010 was greater for nests as forest cover declined, with a 22% increase in brood size for nests at 23% forest cover (1.83 6 0.09 in 1991 versus 2.35 6 0.19 in 2010) compared to a 3% increase for nests at 94% forest cover (2.83 6 0.13 versus 2.93 6 0.31; Fig. 4). The total effective sample size [38] for our nest survival analysis was 33,698. There was considerable model-selection uncertainty, with the best-supported model having 24% of the overall weight of evidence (Table 2). There was limited support for our prediction that temporal variation in nest survival was nest stage-specific. A model with a stage 6 year interaction term was the second-best supported in the candidate set, but overall models with this term only had 41% of the cumulative AIC weight. Model-averaged estimates of nest survival for each stage were contrary to our predications; there was an insubstantial increase in nest survival across time during laying and incubation stages but not during the nestling stage (Fig. 5a). There was also limited support for our prediction that temporal trends in nest survival would be landscape-specific. The forest cover 6 year interaction term did not appear in any of the top three models (Table 2), and although there was a small increase in overall nest survival across time, the difference between landscapes was relatively constant (Fig 5b). Instead, the best predictor of nest survival was parasitism status, as evidenced by the substantial improvement in model likelihood between the model with species, stage, and habitat type variables (AIC = 10,292.25) and the same model that also included parasitism status (AIC = 10,231.41; Table 2). This effect was not due solely to nest abandonment or the total loss of host young to cowbirds, as a post hoc analysis that included only successful nests and those that failed because of nest predation indicated that the period survival rate (i.e., cumulative survival probability across all three nest stages) for parasitized nests (0.14, 95% CI: 0.11–0.18) was substantially lower than for unparasitized nests (0.26, 95% CI: 0.24–0.29). The influence of landscape forest cover on fledging brood size and nest survival led to a substantial increase in overall productivity as forest cover increased (Fig. 6). Similar to the fledging brood size results upon which estimates were partly based, the effect size of the increase in productivity from 1991 to 2010 was larger as forest cover declined, with a 30% increase in productivity for nests at 23% forest cover (0.38, 95% CI: 0.21– 0.48 in 1991 versus 0.55, 95% CI: 0.35–0.76 in 2010) compared to a 10% increase for nests at 94% forest cover (0.84, 95% CI: 0.67– 1.02 versus 0.93, 95% CI: 0.68–1.20; Fig. 6). Several factors may have contributed to cowbird declines in Missouri during 1966–2010. Cowbird abundances increase with proximity to grazing livestock [39], and cattle production in Missouri in 2009 declined . 40% from its peak in 1975 [40]. Further, although landscape forest cover remained largely unchanged at the 10-km scale surrounding the nests we monitored, increased forest cover throughout Missouri (FIA data suggest an 11% increase in forested acreage between 1989 and 2010) may also reduce regional cowbird densities by reducing habitat used for foraging and/or increasing the distance between spatially distinct foraging and breeding habitats [41]. Other factors that limit bird populations such as broad climatic patterns [42] may also affect cowbird abundances. Regardless of the mechanisms driving cowbird declines, our data from 20 years of monitoring nests at five Missouri sites suggest productivity of three songbird species increased concurrent with these declines. Our results also provide further evidence of the negative effect of forest fragmentation on songbird productivity, though these effects may be changing over time. Concordant with documented declines in cowbird abundance, the rate and intensity of parasitism declined substantially during 1991–2010 for the three species we studied. Parasitized nests of most passerine bird species exhibit reduced host productivity [8], an effect that is more pronounced in nests with . 1 cowbird nestling [43]. Declines in the rate and intensity of parasitism between 1991 and 2010 at our study sites resulted in increased predicted fledging brood sizes as forest cover declined, where cowbirds are most abundant and parasitism rates are highest. Population dynamics of songbirds are most sensitive to changes in adult and post-fledging survival, but fledging brood size can be an important determinant in population stability [44]. Because parasitism rates increase and nest survival rates decrease with increasing forest fragmentation in the Midwest [6], and because cowbirds are established nest predators that depredate nests more frequently in fragmented landscapes [13], we predicted that nest survival rates would increase as cowbird abundances decreased across time, more so in fragmented landscapes where cowbirds are abundant. Further, we predicted that changes in nest survival would be stage-specific because cowbirds should have little incentive to depredate nests when hosts are laying eggs. However, nest survival only increased modestly over time, and there was considerable uncertainty surrounding our predictions (Fig. 5b). Further, nest survival increased in a manner contrary to both of our predictions. This is perhaps unsurprising given the diverse suite of predators known to contribute to overall rates of predation in our study system [35,36] that also have exhibited long-term population changes. For example, Blue Jays ( Cyanocitta cristata ) are frequent predators during incubation [35] and have declined 1.1% annually in Missouri during 1991–2010 (95% CI: 2 2.0, 2 0.3%; [15]), which may contribute to the temporal patterns of predation we observed during the laying and incubation stages. By contrast, populations of Broad-winged Hawks ( Buteo platypterus ) and Barred Owls ( Strix asio ), frequent predators that depredate nests almost exclusively during the nestling stage [35], may have increased substantially in Missouri during 1991–2010 (Broad-winged Hawk: 4.3% [95% CI: 2 0.5, 9.2%], Barred Owl: 5.8% [95% CI: 3.3, 8.9%]; [15]). Correlations between broad-scale predator population trends and local demographic metrics should be interpreted with caution, but they are concordant with previous studies relating predator abundance and avian reproductive performance [45]. Lower nest survival and reduced fledging brood sizes associated with low landscape forest cover led to a substantial negative correlation between forest cover and our combined productivity metric (i.e., host young produced per nest attempt). With predicted productivity values $ 50% lower at 23% forest cover compared to 94% forest cover regardless of year (Fig. 6), our data serve as a stark reminder of the negative effects of forest fragmentation on breeding birds in the midwestern United States as described by Robinson et al. [6]. We suggest that cowbirds may be an under- acknowledged mechanism behind reduced nest survival in fragmented landscapes. The presence of a cowbird nestling can result in zero host young fledging from on otherwise ...

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... indicated that the period survival rate (i.e., cumulative survival probability across all three nest stages) for parasitized nests (0.14, 95% CI: 0.11–0.18) was substantially lower than for unparasitized nests (0.26, 95% CI: 0.24–0.29). The influence of landscape forest cover on fledging brood size and nest survival led to a substantial increase in overall productivity as forest cover increased (Fig. 6). Similar to the fledging brood size results upon which estimates were partly based, the effect size of the increase in productivity from 1991 to 2010 was larger as forest cover declined, with a 30% increase in productivity for nests at 23% forest cover (0.38, 95% CI: 0.21– 0.48 in 1991 versus 0.55, 95% CI: 0.35–0.76 in 2010) compared to a 10% increase for nests at 94% forest cover (0.84, 95% CI: 0.67– 1.02 versus 0.93, 95% CI: 0.68–1.20; Fig. 6). Several factors may have contributed to cowbird declines in Missouri during 1966–2010. Cowbird abundances increase with proximity to grazing livestock [39], and cattle production in Missouri in 2009 declined . 40% from its peak in 1975 [40]. Further, although landscape forest cover remained largely unchanged at the 10-km scale surrounding the nests we monitored, increased forest cover throughout Missouri (FIA data suggest an 11% increase in forested acreage between 1989 and 2010) may also reduce regional cowbird densities by reducing habitat used for foraging and/or increasing the distance between spatially distinct foraging and breeding habitats [41]. Other factors that limit bird populations such as broad climatic patterns [42] may also affect cowbird abundances. Regardless of the mechanisms driving cowbird declines, our data from 20 years of monitoring nests at five Missouri sites suggest productivity of three songbird species increased concurrent with these declines. Our results also provide further evidence of the negative effect of forest fragmentation on songbird productivity, though these effects may be changing over time. Concordant with documented declines in cowbird abundance, the rate and intensity of parasitism declined substantially during 1991–2010 for the three species we studied. Parasitized nests of most passerine bird species exhibit reduced host productivity [8], an effect that is more pronounced in nests with . 1 cowbird nestling [43]. Declines in the rate and intensity of parasitism between 1991 and 2010 at our study sites resulted in increased predicted fledging brood sizes as forest cover declined, where cowbirds are most abundant and parasitism rates are highest. Population dynamics of songbirds are most sensitive to changes in adult and post-fledging survival, but fledging brood size can be an important determinant in population stability [44]. Because parasitism rates increase and nest survival rates decrease with increasing forest fragmentation in the Midwest [6], and because cowbirds are established nest predators that depredate nests more frequently in fragmented landscapes [13], we predicted that nest survival rates would increase as cowbird abundances decreased across time, more so in fragmented landscapes where cowbirds are abundant. Further, we predicted that changes in nest survival would be stage-specific because cowbirds should have little incentive to depredate nests when hosts are laying eggs. However, nest survival only increased modestly over time, and there was considerable uncertainty surrounding our predictions (Fig. 5b). Further, nest survival increased in a manner contrary to both of our predictions. This is perhaps unsurprising given the diverse suite of predators known to contribute to overall rates of predation in our study system [35,36] that also have exhibited long-term population changes. For example, Blue Jays ( Cyanocitta cristata ) are frequent predators during incubation [35] and have declined 1.1% annually in Missouri during 1991–2010 (95% CI: 2 2.0, 2 0.3%; [15]), which may contribute to the temporal patterns of predation we observed during the laying and incubation stages. By contrast, populations of Broad-winged Hawks ( Buteo platypterus ) and Barred Owls ( Strix asio ), frequent predators that depredate nests almost exclusively during the nestling stage [35], may have increased substantially in Missouri during 1991–2010 (Broad-winged Hawk: 4.3% [95% CI: 2 0.5, 9.2%], Barred Owl: 5.8% [95% CI: 3.3, 8.9%]; [15]). Correlations between broad-scale predator population trends and local demographic metrics should be interpreted with caution, but they are concordant with previous studies relating predator abundance and avian reproductive performance [45]. Lower nest survival and reduced fledging brood sizes associated with low landscape forest cover led to a substantial negative correlation between forest cover and our combined productivity metric (i.e., host young produced per nest attempt). With predicted productivity values $ 50% lower at 23% forest cover compared to 94% forest cover regardless of year (Fig. 6), our data serve as a stark reminder of the negative effects of forest fragmentation on breeding birds in the midwestern United States as described by Robinson et al. [6]. We suggest that cowbirds may be an under- acknowledged mechanism behind reduced nest survival in fragmented landscapes. The presence of a cowbird nestling can result in zero host young fledging from on otherwise successful nest because of egg removal or destruction (e.g., [46]), host ejection [47], or host mortality due to competition [48]. In addition, louder and more frequent begging by cowbird young [9] and increased parental activity at nests with cowbird young [49] may result in higher predation risk [50] and contribute to lower rates of nest survival for parasitized nests as seen here and elsewhere [51,52]. The negative effects of parasitism on fledging brood size and nest survival (and thus on our productivity measure) combined with the fact that cowbirds depredate nests more frequently in less forested landscapes [13] suggest that cowbirds may be a primary cause of the forest fragmentation effect on songbird productivity in the Midwest. Despite the substantial decline in predicted parasitism rates during 1991–2010, the concomitant increase in productivity was comparatively modest because the strongly negative impact of parasitism on the productivity of a single nest is muted across a population of nests wherein most are not parasitized and many parasitized nests are depredated. Nevertheless, lower landscape forest cover was associated with a greater increase in predicted productivity, which provides support for our hypothesis that temporal trends in productivity should be landscape-specific. It also suggests that some habitat patches that were formerly population sinks ( sensu [53]) may now produce enough young to be considered sources, which exemplifies the potential value of incorporating temporally dynamic source-sink models into the management of migratory songbirds. We stress that the patterns we observed in Missouri almost assuredly do not apply throughout the extensive range of the Brown-headed Cowbird. The BBS data suggest that temporal trends in cowbird abundances are not uniform; 19 U.S. states have seen substantial cowbird declines between 1966–2010, but 12 states have had significant increases in cowbird abundances during the same timespan [15]. Furthermore, current abundance trends may not persist into the future, as it is possible that current cowbird declines are part of a long-term population oscillation. Only seven states had significant declines during 2000–2010, and even though cowbird abundance has declined in Canada throughout the entire BBS survey period (1.5% annual decline [95% CI: 2 2.2, 2 1.0%]), they actually increased in abundance during 2000–2010 (2.4% annual increase [95% CI: 0.9, 4.1%]; [15]). Finally, Missouri is near the historical center of the cowbird breeding range [54,55] where abundances are typically highest [17], and it may be difficult to detect biologically meaningful changes in the effect of cowbirds on productivity in locations where cowbird abundances are substantially lower. Predictive models designed to assess the effects of climate change on wildlife distributions and abundances into the next century are increasingly common in the literature. Such models will be most useful when they incorporate important biotic interactions [56,57] such as those between brood parasites and their host species. Given the inherent complexity of virtually all ecosystems, any such model is likely to be surrounded by substantial uncertainty. Nevertheless, our study underscores the fact that critical demographic parameters are not static in time but can instead exhibit long-term temporal trends. Demographers rely upon empirical data collection to parameterize their models, but our data demonstrate that values derived from older studies may not be reflective of current or future conditions. Studies such as this that monitor populations across extended time periods are essential if we are to accurately predict future trends in the abundance, occurrence, or productivity of ...

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... 10 counties surrounding our nests increased 7% (640,628 ha to 682,725 ha) between 1989 and 2010 according to FIA data. In contrast, NLCD data from a 10-km radius surrounding each nest suggested that forest cover declined by 1.8% from 1992 to 2001, and by 0.4% from 2001 to 2006. Of the nests monitored wherein contents were reliably observed, 423 of 1,524 (28%) bunting nests, 76 of 1,021 (7%) flycatcher nests, and 79 of 367 (22%) cardinal nests were parasitized. All three species were well represented across the gradient of forest cover (Fig. 2; bunting mean: 58 6 1%, range: 23–95%; flycatcher mean: 70 6 1%, range: 23–95%; cardinal mean: 44 6 1%, range: 23– 95%). Forest cover strongly influenced parasitism rates with a mean predicted parasitism rate of 33% (95% CI: 28–37%) for a population of nests balanced across species at 23% forest cover (the 5 th percentile of observed forest cover values) versus 3% (95% CI: 2–4%) for a population of nests at 94% forest cover (the 95 th percentile). A parameter for year was in the two best-supported parasitism rate models, which combined for 100% of the overall weight of evidence (Table 1). Parasitism rates differed between species and declined across time (Fig. 3a). A parameter for year was also in the top two parasitism intensity models, which combined for 98% of the overall weight of evidence (Table 1). The mean number of cowbird eggs per parasitized nest differed among species (buntings: 1.43 6 0.03; flycatchers: 1.09 6 0.04; cardinals: 1.23 6 0.06) and declined across time (Fig. 3b). There was a substantial effect of brood parasitism on fledging brood size; fledging brood sizes were greater for unparasitized versus parasitized nests for buntings (2.79 6 0.12 versus 1.47 6 0.14 fledglings), flycatchers (2.50 6 0.13 versus 1.17 6 0.15 fledglings), and cardinals (2.82 6 0.15 versus 1.50 6 0.16 fledglings). The best- supported model for fledging brood size did not include a covariate for year, but there was considerable model-selection uncertainty (Table 1), and model-based predictions of fledging brood size increased across time (Fig. 4) because the predictions incorporated the negative association between parasitism rates and year. The effect size of the increase in fledging brood size from 1991 to 2010 was greater for nests as forest cover declined, with a 22% increase in brood size for nests at 23% forest cover (1.83 6 0.09 in 1991 versus 2.35 6 0.19 in 2010) compared to a 3% increase for nests at 94% forest cover (2.83 6 0.13 versus 2.93 6 0.31; Fig. 4). The total effective sample size [38] for our nest survival analysis was 33,698. There was considerable model-selection uncertainty, with the best-supported model having 24% of the overall weight of evidence (Table 2). There was limited support for our prediction that temporal variation in nest survival was nest stage-specific. A model with a stage 6 year interaction term was the second-best supported in the candidate set, but overall models with this term only had 41% of the cumulative AIC weight. Model-averaged estimates of nest survival for each stage were contrary to our predications; there was an insubstantial increase in nest survival across time during laying and incubation stages but not during the nestling stage (Fig. 5a). There was also limited support for our prediction that temporal trends in nest survival would be landscape-specific. The forest cover 6 year interaction term did not appear in any of the top three models (Table 2), and although there was a small increase in overall nest survival across time, the difference between landscapes was relatively constant (Fig 5b). Instead, the best predictor of nest survival was parasitism status, as evidenced by the substantial improvement in model likelihood between the model with species, stage, and habitat type variables (AIC = 10,292.25) and the same model that also included parasitism status (AIC = 10,231.41; Table 2). This effect was not due solely to nest abandonment or the total loss of host young to cowbirds, as a post hoc analysis that included only successful nests and those that failed because of nest predation indicated that the period survival rate (i.e., cumulative survival probability across all three nest stages) for parasitized nests (0.14, 95% CI: 0.11–0.18) was substantially lower than for unparasitized nests (0.26, 95% CI: 0.24–0.29). The influence of landscape forest cover on fledging brood size and nest survival led to a substantial increase in overall productivity as forest cover increased (Fig. 6). Similar to the fledging brood size results upon which estimates were partly based, the effect size of the increase in productivity from 1991 to 2010 was larger as forest cover declined, with a 30% increase in productivity for nests at 23% forest cover (0.38, 95% CI: 0.21– 0.48 in 1991 versus 0.55, 95% CI: 0.35–0.76 in 2010) compared to a 10% increase for nests at 94% forest cover (0.84, 95% CI: 0.67– 1.02 versus 0.93, 95% CI: 0.68–1.20; Fig. 6). Several factors may have contributed to cowbird declines in Missouri during 1966–2010. Cowbird abundances increase with proximity to grazing livestock [39], and cattle production in Missouri in 2009 declined . 40% from its peak in 1975 [40]. Further, although landscape forest cover remained largely unchanged at the 10-km scale surrounding the nests we monitored, increased forest cover throughout Missouri (FIA data suggest an 11% increase in forested acreage between 1989 and 2010) may also reduce regional cowbird densities by reducing habitat used for foraging and/or increasing the distance between spatially distinct foraging and breeding habitats [41]. Other factors that limit bird populations such as broad climatic patterns [42] may also affect cowbird abundances. Regardless of the mechanisms driving cowbird declines, our data from 20 years of monitoring nests at five Missouri sites suggest productivity of three songbird species increased concurrent with these declines. Our results also provide further evidence of the negative effect of forest fragmentation on songbird productivity, though these effects may be changing over time. Concordant with documented declines in cowbird abundance, the rate and intensity of parasitism declined substantially during 1991–2010 for the three species we studied. Parasitized nests of most passerine bird species exhibit reduced host productivity [8], an effect that is more pronounced in nests with . 1 cowbird nestling [43]. Declines in the rate and intensity of parasitism between 1991 and 2010 at our study sites resulted in increased predicted fledging brood sizes as forest cover declined, where cowbirds are most abundant and parasitism rates are highest. Population dynamics of songbirds are most sensitive to changes in adult and post-fledging survival, but fledging brood size can be an important determinant in population stability [44]. Because parasitism rates increase and nest survival rates decrease with increasing forest fragmentation in the Midwest [6], and because cowbirds are established nest predators that depredate nests more frequently in fragmented landscapes [13], we predicted that nest survival rates would increase as cowbird abundances decreased across time, more so in fragmented landscapes where cowbirds are abundant. Further, we predicted that changes in nest survival would be stage-specific because cowbirds should have little incentive to depredate nests when hosts are laying eggs. However, nest survival only increased modestly over time, and there was considerable uncertainty surrounding our predictions (Fig. 5b). Further, nest survival increased in a manner contrary to both of our predictions. This is perhaps unsurprising given the diverse suite of predators known to contribute to overall rates of predation in our study system [35,36] that also have exhibited long-term population changes. For example, Blue Jays ( Cyanocitta cristata ) are frequent predators during incubation [35] and have declined 1.1% annually in Missouri during 1991–2010 (95% CI: 2 2.0, 2 0.3%; [15]), which may contribute to the temporal patterns of predation we observed during the laying and incubation stages. By contrast, populations of Broad-winged Hawks ( Buteo platypterus ) and Barred Owls ( Strix asio ), frequent predators that depredate nests almost exclusively during the nestling stage [35], may have increased substantially in Missouri during 1991–2010 (Broad-winged Hawk: 4.3% [95% CI: 2 0.5, 9.2%], Barred Owl: 5.8% [95% CI: 3.3, 8.9%]; [15]). Correlations between broad-scale predator population trends and local demographic metrics should be interpreted with caution, but they are concordant with previous studies relating predator abundance and avian reproductive performance [45]. Lower nest survival and reduced fledging brood sizes associated with low landscape forest cover led to a substantial negative correlation between forest cover and our combined productivity metric (i.e., host young produced per nest attempt). With predicted productivity values $ 50% lower at 23% forest cover compared to 94% forest cover regardless of year (Fig. 6), our data serve as a stark reminder of the negative effects of forest fragmentation on breeding birds in the midwestern United States as described by Robinson et al. [6]. We suggest that cowbirds may be an under- acknowledged mechanism behind reduced nest survival in fragmented landscapes. The presence of a cowbird nestling can result in zero host young fledging from on otherwise successful nest because of egg removal or destruction (e.g., [46]), host ejection [47], or host mortality due to competition [48]. In addition, louder and more frequent begging by cowbird young [9] and increased parental activity at nests with cowbird young [49] may result in higher predation risk [50] and contribute to lower rates of nest survival for parasitized nests as seen here and elsewhere [51,52]. The negative effects of parasitism on fledging ...