We selected publications that described the effect of reduction or addition of avian or mammalian predators on avian or mammalian prey, excluding livestock and other non-native prey species. Studies that had removed both native and introduced predators were excluded, if the effects of these predator groups could not be separated. Acceptable prey responses to predator manipulations were classified as either population size or reproductive responses. Population size responses included those measured directly, as density, minimum numbers known to be alive, numbers of breeding pairs (as an index of population size), rate of increase or survival; and catch-per-unit effort indices such as the number of animals per area, trapline or transect. Reproductive responses included numbers of juveniles or broods produced, numbers of females with young, nesting success, survival of young and mean recruitment. Per capita measures, such as brood size per hen, number of juveniles per hen, number of broods per pair, number of fledglings/ducklings per pair, number of chicks fledged per pair, number of fawns/100 does, etc., were not included. The studies also had to have been run for long enough (one prey generation or more) for a prey demographic response to be possible. The studies measuring other parameters or using other units than those described were omitted. No authors were contacted to obtain missing data.
The 45 replicated experiments (table S1 in electronic supplementary material) were examined for publication bias using the normal quantile plot method (Wang & Bushman 1998), and no evidence of publication bias was found (figure S1 in electronic supplementary material). This analysis was not possible for unreplicated studies and, therefore, the publication of such studies may have been biased towards large positive effects of predator removal on prey. However, it is rather unlikely that the results, whether significant or not, of very expensive, long-lasting predator manipulation experiments would remain unpublished, strongly reducing the likelihood for the file-drawer problem (Rosenthal 1979) particularly in this meta-analysis.
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For each replicated study, we calculated the standardized effect size as Hedges' d using MetaWin v. 2.1 (Rosenberg et al. 2000). There are also other metrics available for this type of primary data (means, variances and sample sizes), such as the log response ratio lnR (Rosenberg et al. 2000), but we chose d because our data were not suitable for use of the response ratio (e.g. in some studies, the control group value was zero; Hedges et al. 1999). Positive values of d indicate that the predator treatment had a positive effect on prey species, zero means that there was no difference between treatment and control, and negative values signify a greater response in controls. For studies that reported the responses of multiple prey species to predator manipulation, we used the mean effect size across all species to retain independence. In one study, predators had been both added and removed; also here a mean effect for the whole study was calculated from the effect sizes of both treatments.
Our first prediction was that introduced predators should have more pronounced effects than native predators on the population sizes and reproductive outputs of their prey. To test this prediction with the 45 replicated experiments, we carried out a categorical summary analysis using the homogeneity statistic, Q, in MetaWin v. 2.1. As with variance in ANOVA, the total heterogeneity QT can be partitioned into QM, the variation explained by the model, and QE, the residual error variance (Rosenberg et al. 2000). Continuous summary analysis (weighted linear regression) was used to determine whether d was affected by the spatial or temporal scale of the studies. We used random effects models and conducted resampling tests with 4999 iterations. Bias-corrected confidence intervals were used to evaluate the probability at 0.05. All tests were two-tailed.
To expand the coverage of research that has evaluated the impacts of predation, we conducted a similar analysis on the unreplicated predator removal experiments. Altogether, 34 unreplicated studies fulfilled the criteria, but two were excluded as they reported earlier stages of experiments that were represented in the analysis by later, more inclusive papers. In two cases, different aspects of the same experiment were reported in separate papers, which were then combined to gain one effect size. One study consisted of six experiments at different locations, which were therefore treated as independent studies in the dataset. Hence, the final dataset has 35 rows (table S2 in electronic supplementary material).
We classified the traits of the unreplicated experimental systems as described previously and defined the effect size as Xe/Xc, where Xe and Xc are the treatment and control prey responses, respectively. A ratio over 1 means that predator manipulation had a positive effect on the prey species, while a ratio up to 1 means that manipulation did not affect the prey species or the effects were negative. These unreplicated data cannot be analysed using typical meta-analysis approaches; therefore, we tested for differences in effect size in the study traits using Student's t-test with the Satterthwaite option for heteroscedastic variances (procedure TTEST, SAS Statistical Package, v. 9.1; SAS Institute, Cary, NC, USA). Effect size was ln transformed to meet the assumptions of normality.
Finally, a generalized linear model was built in order to further test our first and second predictions (i.e. that alien predators would have more impact than native predators on prey populations and that predation impacts would be greater on prey in island ecosystems compared with mainland ecosystems), and to explore possible interactions of the different explanatory variables. Neither MetaWin nor t-test allows the simultaneous analysis of multiple factors, and the sample sizes of replicated and unreplicated experiments alone were too small for such an analysis. Therefore, we pooled population size responses of the replicated and unreplicated experiments using Xe/Xc as the effect size measure. The model was fitted with a negative binomial distribution of the response and a log link function with the negative binomial GLM (glm.nb) procedure in the MASS library of S-Plus (v. 6, Insightful Corporation, Seattle, USA).
In the replicated experiments, the effects of introduced predators on prey were more than double those of native predators (figure 1a; QM=4.96, d.f.=1, p=0.020). Further partitioning revealed very striking effects of introduced predators in Australia compared with other parts of the world. The mean effect size of prey responding to the removal of introduced predators in Australia (all mammalian responses) was twofold higher than that of prey responding to introduced predators elsewhere and threefold higher when compared with native predators generally (figure 1b; QM=7.07, d.f.=2, p=0.022).
Mean effect sizes of prey in replicated predator manipulation experiments. (a) Effects of native and introduced predators and (b) effects of native and introduced predators, with the effects of introduced predators divided between Australian experiments and experiments conducted elsewhere. Effect size is calculated as Hedges' d. Bars represent 95% bias-corrected confidence intervals.
There was a significant difference between population size effects and reproductive responses in the experiments, the latter being larger (table 1). Therefore, we reanalysed the data from only those experiments where population size responses were measured. The analysis of population size responses revealed the significant overall difference between alien and native predators again and also a significant difference between native and alien predators outside Australia (table 1). This is probably because most of the studies on reproductive responses had manipulated native predators (table S1 in electronic supplementary material).
Of the 35 unreplicated experiments included in the analyses, 13 removed alien predators (table S2 in electronic supplementary material). Six studies were from islands, 12 were from Australia and New Zealand and 17 were from mainland areas. Twenty-two studies examined the responses of mammalian prey, while the rest investigated birds. Eighteen studies recorded population size responses, and six reported reproductive responses. In 11 studies, both responses were measured but, as in the replicated studies, only population size responses were used. There was no difference between the two responses in the pooled data (t=1.18, d.f.=13.7, p=0.258; reproduction: back-transformed ln(Xe/Xc)=1.681, lower 95% CL=0.881, upper 95% CL=3.210, n=6; population size: back-transformed ln(Xe/Xc)=2.486, lower 95% CL=1.449, upper 95% CL=3.863, n=29).
Analyses of the unreplicated studies yielded remarkably similar results to those of the replicated experiments (figure 2). The effects of introduced predators were on average 2.5 times higher than for native predators (figure 2a; t=2.22, d.f.=16.3, p=0.041), but again the difference appeared to be influenced mainly by the large effects in Australian studies (figure 2b). There were no obvious biases in effect size resulting from study duration or spatial coverage (Spearman's rank correlation, rs=0.246, p=0.16, n=35 and rs=0.184, p=0.31, n=33, respectively).
Mean effect sizes of prey in unreplicated predator manipulation experiments. (a) Effects of native and introduced predators and (b) effects of native and introduced predators, with the effects of introduced predators divided between Australian experiments and experiments conducted elsewhere. Effect size presented as back-transformed ln(Xe/Xc), where Xe and Xc are the treatment and control prey responses, respectively. Bars represent 95% confidence intervals.
Effects of explanatory variables on prey population size responses in a total of 60 replicated and unreplicated predator manipulation experiments. (a) The summary statistics of the stepwise model selection procedure based on AICc values. The main explanatory variables in the model were origin of predator (O; native versus introduced), type of manipulation (Mtype; open area versus predator exclosure), predator class (PC; mammal, bird and both) and location (L; mainland versus island) with their second-order interactions. Predator/prey weight ratio (Pw), manipulation area (Marea) and duration of manipulation (Mtime) were included as continuous variables. k, number of parameters in each model; log (L), value of the maximized log-likelihood function; Δi, AIC difference; wi, Akaike weights. (b) The medians and tenth and ninetieth centiles of the main variables and predator originlocation interaction.
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