Conceived and designed the experiments: MM JS. Analyzed the data: MM PA. Wrote the paper: MM PA JS.
The authors have declared that no competing interests exist.
Hyperpredation refers to an enhanced predation pressure on a secondary prey due to either an increase in the abundance of a predator population or a sudden drop in the abundance of the main prey. This scarcely documented mechanism has been previously studied in scenarios in which the introduction of a feral prey caused overexploitation of native prey. Here we provide evidence of a previously unreported link between Emergent Infectious Diseases (EIDs) and hyperpredation on a predator-prey community. We show how a viral outbreak caused the population collapse of a host prey at a large spatial scale, which subsequently promoted higher-than-normal predation intensity on a second prey from shared predators. Thus, the disease left a population dynamic fingerprint both in the primary host prey, through direct mortality from the disease, and indirectly in the secondary prey, through hyperpredation. This resulted in synchronized prey population dynamics at a large spatio-temporal scale. We therefore provide evidence for a novel mechanism by which EIDs can disrupt a predator-prey interaction from the individual behavior to the population dynamics. This mechanism can pose a further threat to biodiversity through the human-aided disruption of ecological interactions at large spatial and temporal scales.
Pathogens can exert a large influence on ecological interactions from the individual to the ecosystem level
In 1988 a major viral outbreak of Rabbit Hemorrhagic Disease (RHD) rapidly spread throughout Spain
Here we compile long-term hunting bag records for the European rabbit and the red-legged partridge
In a broad sense, hyperpredation can be defined as an enhanced predation pressure on a secondary prey due to either: a) an increase in the abundance of the predator population caused by an abrupt increase in the abundance of its main prey; or b) a sudden drop in the abundance of the main prey
The population trajectory of both prey species is shown in
The vertical line in the figure denotes the temporal location of the RHD outbreak. Within each graph, the small figure shows the change in predation after the RHD outbreak, defined as the percentage shift in the relative abundance of each species in the diet of three major shared predators (see
Outside the triangle, populations tend to extinction, and below the parabola multiannual cycles arise; within the area between the triangle and the parabola the system exhibit dampened stability (on the right) or two-years cycles (on the left). The grey and black solid square depict the parameter combination for the European rabbit and red-legged partridge model, respectively. Open squares denote the parameter combination for the same model but without the state-space component (
Species & model | BIC | ||||||
−0.035 (0.039) | — | — | — | 0.025 (0.011) | 0.003 (0.004) | 41.625 | |
1.055 (0.937) | — | — | −0.187 (0.160) | 0.023 (0.013) | 0.004 (0.004) | 44.927 | |
0.313 (0.164) | — | — | 0.019 (0.011) | 0.004 (0.004) | |||
−0.230 (0.853) | — | 0.099 (0.154) | 0.020 (0.011) | 0.004 (0.005) | 35.822 | ||
0.232 (0.295) | −0.486 (0.255) | — | 0.010 (0.009) | 0.004 (0.004) | 33.261 | ||
−0.266 (0.775) | 0.143 (0.301) | −0.456 (0.246) | 0.118 (0.145) | 0.012 (0.009) | 0.004 (0.005) | 33.283 | |
0.000 (0.030) | — | — | — | 0.014 (0.006) | 0.002 (0.002) | 41.651 | |
0.736 (0.698) | — | — | −0.126 (0.120) | 0.014 (0.006) | 0.002 (0.002) | 44.720 | |
0.127 (0.131) | −0.140 (0.141) | — | — | 0.014 (0.007) | 0.002 (0.002) | 31.936 | |
0.169 (0.762) | −0.138 (0.157) | — | −0.008 (0.135) | 0.016 (0.009) | 0.002 (0.002) | 35.822 | |
0.157 (0.090) | — | 0.005 (0.005) | 0.002 (0.002) | ||||
0.527 (0.530) | −0.068 (0.095) | 0.005 (0.005) | 0.003 (0.002) | 33.875 |
The range of possible models within the saturated one is ordered for each species according to increasing complexity. The modelled population process, denoted by the state variable
Bayesian Information Criterion; the model minimizing this quantity is selected as the best descriptor of the dataset within the pool of fitted models, and is shown in bold type.
To the best of our knowledge, we have provided the first evidence of an enhanced predation pressure on a secondary prey due to the population collapse of a primary prey induced by an EID. After a RHD outbreak, the reduced abundance of rabbits might force predators to focus on the partridge populations, therefore causing a numeric reduction in its population as well. Empirical evidence suggests that the prevalence of acquired immunity through antibodies to RHD increased during the mid-1990s in at least some local rabbit populations
The thickness of each arrow denotes the numerical intensity of the interaction, while the thickness of each box represents the relative contribution of each species/community to the intensity of the multi-species interaction. Before the outbreak of the Rabbit Hemorrhagic Disease (RHD), the predators community fed differentially upon both prey species according to “average” traits (individual preferences, life-history, etc.) and environmental factors (local prey availability, etc.). At the onset of the RHD outbreak, the abundance of the host species, which is the main prey, drops abruptly, so the intensity of predation shifts towards the secondary prey. This causes its population abundance to decrease accordingly. Once the proportion of immunized hosts begins to increase, the intensity of the inter-specific interaction returns to the “average” (pre-outbreak) levels. The population sizes of both prey species begin to rise as well at this stage. However, a proportion of RHD viruses can prevail in the host population.
Although a specific prediction of the EID-mediated hyperpredation hypothesis is a significant cross-species correlation in the abundance of both prey, we recognize that some external factors, such as climate and habitat conditions, could act to synchronize their population dynamics. Nevertheless, these factors should have no obvious impact on the feeding behavior of major predators, which conspicuously changed after the RHD outbreak, and we have already shown that climate seems to have no effect on the dynamics of neither prey population. In addition, the structure and functioning of Mediterranean ecosystems are strongly dependent on rainfall fluctuations
Besides hyperpredation, other factors might have acted to reduce partridge populations. Specifically, habitat destruction and deterioration, over-hunting and the use of pesticides have been claimed as factors triggering declines of local partridge populations, but it is also known that other local populations increased at the same time
Another possibility is that during the low-abundance period of both prey some predators responded numerically by reducing their populations as well; this could have released both prey populations from predation and further enhance synchrony. However, we emphasize that this possibility is not incompatible with the EID-mediated hyperpredation. Moreover, there is no global evidence that the predator populations responded numerically during this period, and the available evidence suggests in fact that many local populations of the raptors considered in the present study increased due to efficient conservation measures
Overall, using data from two key game species, we have provided evidence for a novel pathway by which EIDs can disrupt a predator-prey interaction from the individual behavior to the population dynamics. Due to multiple introductions and/or translocations of pathogens by humans, one of the major current threats of EIDs is an extremely fast and unpredictable rate of spatial spread of the disease
To model the population dynamics of the European rabbit and the red-legged partridge, we gathered hunting bag data from the Spanish Ministry of Agriculture, Fisheries and Food. Available data span the 50 Spanish provinces from 1986 to 2003. However, the rabbit is native only to the 45 continental provinces, so we used data for those areas. Because hunting effort can influence the number of rabbits and partridges hunted
To asses the numeric role of rabbits and partridges as prey for the Iberian predators (raptors and carnivorous mammals), we used our own field data and also conducted a bibliographic review of published data on feeding ecology of their predators (
In order to test for cross-species correlation in the population dynamics, we fitted a log-linear (Gompertz) model of population growth to the abundance of each species
We tested for cross-species correlation in the population dynamics of the partridge and rabbit populations using the point estimates for the hidden states in
The Monte Carlo trace of the three Markov Chains (shown in green, red and blue) is shown for each parameter in the state-space model selected as the most parsimonious by the BIC, for both the European rabbit (a) and the red-legged partridge (c). Each chain was initiated with slightly different parameter values. Also shown are the probability density kernels of each parameter, constructed after joining the three chains. The autocorrelation plot is shown for each chain after thinning the MCMC samples every 20 iterations, for both the European rabbit (b) and the red-legged partridge (d). Finally, the Gelman-Rubin statistic calculates the rate of convergence of each chain across the MCMC simulation. A value near to 1 indicates a correct convergence of the chain.
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We are very grateful for the valuable suggestions and data provided by E. Virgós and C. Calvete. The comments of W. Getz and two anonymous reviewers greatly improved a previous version of the manuscript. We would also like to thank F. Hiraldo for its unconditional support.