(C) PLOS One [1]. This unaltered content originally appeared in journals.plosone.org. Licensed under Creative Commons Attribution (CC BY) license. url:https://journals.plos.org/plosone/s/licenses-and-copyright ------------ More pests but less pesticide applications: Ambivalent effect of landscape complexity on conservation biological control ['Patrizia Zamberletti', 'Inrae Biostatistique Et Processus Spatiaux', 'Inra-Paca', 'Avignon', 'Khadija Sabir', 'Institute Of Horticultural Production Systems', 'Leibniz University Hannover', 'Hannover', 'Thomas Opitz', 'Olivier Bonnefon'] Date: 2022-01 In agricultural landscapes, the amount and organization of crops and semi-natural habitats (SNH) have the potential to promote a bundle of ecosystem services due to their influence on ecological community at multiple spatio-temporal scales. SNH are relatively undisturbed and are often source of complementary resources and refuges, therefore supporting more diverse and abundant natural pest enemies. However, the nexus of SNH proportion and organization with pest suppression is not trivial. It is thus crucial to understand how the behavior of pest and natural enemy species, the underlying landscape structure, and their interaction, may influence conservation biological control (CBC). Here, we develop a generative stochastic landscape model to simulate realistic agricultural landscape compositions and configurations of fields and linear elements. Generated landscapes are used as spatial support over which we simulate a spatially explicit predator-prey dynamic model. We find that increased SNH presence boosts predator populations by sustaining high predator density that regulates and keeps pest density below the pesticide application threshold. However, predator presence over all the landscape helps to stabilize the pest population by keeping it under this threshold, which tends to increase pest density at the landscape scale. In addition, the joint effect of SNH presence and predator dispersal ability among hedge and field interface results in a stronger pest regulation, which also limits pest growth. Considering properties of both fields and linear elements, such as local structure and geometric features, provides deeper insights for pest regulation; for example, hedge presence at crop field boundaries clearly strengthens CBC. Our results highlight that the integration of species behaviors and traits with landscape structure at multiple scales is necessary to provide useful insights for CBC. In the agricultural context, the loss of semi-natural surfaces often results in high pest abundance requiring elevated pesticide loads. Habitat heterogeneity resulting from the agricultural intermixing of arable fields and semi-natural areas is key to allow organism fluxes across agro-ecological interfaces by influencing ecological processes. Semi-natural habitats (SNH) are often restricted to linear structures, such as hedgerows, but they play an important role by hosting a large number of species. However, the effect of hedgerows is controversial, as it could result in a positive, ineffective or negative effect for CBC. Usually, the impacts of landscape structure on pest population dynamics and resulting CBC are assessed through field experiments with a specific focus, which cannot be generalized, lack flexibility and are limited by the need to manipulate relatively large landscapes. Here, we tackle the challenge to investigate the controversial role of semi-natural habitats for CBC by presenting a simulation-based approach, which allows us to characterize the joint influence of landscape structure and species traits on CBC service. Our study corroborates that spatial heterogeneity, species traits and their interactions are fundamental for CBC. We show that hedge presence alone is not sufficient to lead to strong pest reduction, but hedge-based predators help to maintain the pest density under the pesticide threshold. Instead, SNH presence coupled with appropriate predator traits leads to stronger decrease of pest population. Moreover, we highlight an important scaling effect of SNH, which at the local scale has an even more important impact on CBC as local properties are considered. A major goal of this work is to implement a general simulation-based approach to obtain theoretical insights on CBC by incorporating landscape effects and species traits, which can serve as basis to formulate practical recommendations. In order to assess what are the main factors that influence the predator-pest population densities in complex landscapes, following questions are investigated: (i) Can landscape composition and configuration reduce the number of pesticide applications by enhancing CBC? (ii) How do species traits related to dispersal, predation and population demography modify the effect of landscape heterogeneity? Specifically, we develop a stochastic landscape model to simulate realistic agricultural landscape compositions and configurations of fields and linear elements for crop and semi-natural allocation. The generated landscapes are used as spatial support over which we simulate spatially explicit predator-pest dynamics. The population model accurately links 2D diffusion on surface, 1D diffusion on linear elements, and the flux interchanges among them to put particular attention on the linear element integration; see S1 and S2 Videos. Predators use hedges as their natural habitat where their population naturally develops, but they can also move into crop field to feed on pests. Pests consider crop fields as their natural habitats where they show positive growth, while they are not influenced by hedge elements. Our study explores how the joint consideration of spatial heterogeneity, landscape structure, species traits and their interactions helps to achieve effective CBC. We present and discuss results in the following sections; the technical description of our model and statistical methods is given in Model and method section. In general, the impacts of landscape structure on pest population dynamics are investigated through empirical correlative approaches with global descriptors at landscape level, due to the difficulty of manipulating large landscapes for local analyses and due to the lack of the spatio-temporal dimension. The main drawback of these approaches is the difficulty of linking correlation levels to population dynamic processes, such as local population growth or migration behavior [ 22 ]. A complementary approach, combining theoretical modeling and computer simulations, consists in coupling generative landscape models with population dynamics models to explore how different landscape configurations, including the hedge network structure, affect CBC [ 23 ]. While SNH favours the presence or abundance of functional groups of organisms in landscapes, it can also result in ineffective conservation biological control (CBC) [ 12 , 13 ] with no, or even negative effects on pest control [ 12 – 14 ]. A meta-analysis revealed that pest pressure in complex landscapes is reduced in 45% of cases, not affected in 40% of cases and increased in 15% of cases [ 9 ]. The analysis in [ 15 ] highlights the difficulty of stating general and systematic pest and predator interactions and responses; it is based on a very large pest control dataset from which a remarkable variability in pest and enemy responses to different landscape metrics is found. For example, the effect of landscape structure on pests remains inconclusive, as many crop pests also benefit from nearby non-crop habitat [ 12 – 14 ]. It may occur that SNH offers more complementary resources to pests rather than to predators to complete their life cycle [ 6 ]. Predator abundance is not always enough to guarantee a consistent reduction of pest species [ 16 ] in case of the presence of alternative prey (known as dilution effect) [ 17 ], or increased intra-guild predation [ 18 ]. Life history traits, in particular those traits related to mating systems, competitive skills, movement abilities and habitat use, are also of major importance by affecting species’ responses to landscape heterogeneity and being readily linked with ecological processes [ 19 ]. Thus, effect direction and magnitude jointly depend on organisms and landscapes under study [ 20 , 21 ]. Agricultural landscape simplification results in substantial loss of semi-natural mosaics and of non-crop field margins. It is often associated with high pest abundance, which in turn requires a higher pesticide input [ 1 , 2 ]. Consequently, a negative relationship emerges between intensity of agriculture and agricultural landscape biodiversity [ 3 ] because of a partial replacement and suppression of the ecological services provided by communities of beneficial organisms [ 4 , 5 ]. Habitat heterogeneity is key to allow cross-system fluxes of organisms across agro-ecological interfaces by influencing ecological dynamics within those habitats [ 6 , 7 ] and potentially increasing predator abundance and diversity in agricultural systems [ 8 , 9 ]. In addition, complex landscape favours habitat and resource diversity for predators thanks to increased availability of alternative preys, higher microclimate heterogeneity, the presence of refuges from their own predators and for overwintering [ 10 ]. In arable land, semi-natural habitat (SNH) is typically restricted to hedgerows. These linear structures play an important role as relatively perennial line corridors because of their temporal stability with respect to crop fields. Their presence supports predator dispersal and movement to escape from disturbances and to find food resources scattered in time and space [ 11 , 12 ]. Locally, presence of pesticide applications is negatively influenced by field area and perimeter (E Area = −0.32 ± 0.01, E Perimeter = −0.10±0.03). These effects reflect both a slower pest diffusion in large fields and higher predator incoming fluxes to fields with long perimeter. Conversely, when pesticide applications occurred in a field, the total number of pesticide applications increases with field perimeter due to spillover form the neighborhoods. An increase in the number of adjacent crop fields produces a positive effect on the presence ( ) and number ( ) of pesticide applications, while an increase in the number of adjacent hedges leads to a negative effect on the presence ( ) and number ( ) of pesticide applications. Whereas in the global model the increase of hedge proportion is associated with a positive effect on the presence of pesticide applications, we attribute the negative effect at local level to the fact that the predator tends to locally maintain the pest density under the pesticide threshold, especially after a first pesticide application. The number of pesticide applications in adjacent fields is positively correlated to their local presence ( ) and number ( ), indicating local proliferation of the pest. Fig G in S1 Text shows all estimated local effects and confidence intervals for pesticide application presence/absence and number, see also Table 1 . By checking the sensitivity of our results with respect to the pesticide application variables (i.e., pesticide application efficacy [optimal vs realistic] and pesticide thresholds [low vs high], see S1 Text ), we find that there is no variation of the direction of the estimated effects, but the magnitude of the effect can increase or decrease depending on the scenario considered. Specifically, when pest reduction is lower due to low pesticide efficacy, or, when pest reduction is slower due to an elevated pesticide threshold, hedges show a more important effect in slowing down pest dynamics thanks to predator presence providing a more efficient CBC. As expected, crop proportion as well as spatial crop and hedge aggregation (E φ = 0.55 ± 0.02), have a strong positive effect on pest density. Both variables interact negatively ( ), as high aggregation results in an increase of the size of contiguous crop fields, which lowers the effect of increased crop proportion. The positive effect of crop proportion is lowered by its interaction with hedge proportion and also with predator migration from hedge to fields . Counterintuitively at first sight, an increase in hedge proportion has a positive effect on pest density. Indeed, predator presence over all the landscape helps to stabilize the pest population by keeping it under the thresholds that would trigger a pesticide application. This is further confirmed by the fact that hedge proportion ( ), predator spillover from hedges to fields ( ) and concurrence of high crop proportion and aggregation ( ) have a positive effect on the presence of pesticide applications, but a negative effect on pesticide application numbers ( ). The sensitivity analysis of standard deviation of model outputs across landscape replicates gives different importance to the input variables as compared to the mean values. For the predator density, crop proportion (P c ), predator migration (ρ 12 ), hedge proportion (P h ) and spatial crops and hedges aggregation (φ) explain respectively 55%, 19%, 9% and 9% of the variability of model outputs ( Fig 1A left). For the pest and pesticide applications, results are consistent with the results obtained for the mean. However, interactions between model parameters are important to explain variations in the standard deviation of predator and pest density, as well as of pesticide applications among landscape replicates. This implies that particular landscape structures, characterized by a combination of several descriptors, have to be considered to fully understand the drivers of predator-pest dynamics. Fig 1 shows the results of a Sobol sensitivity analysis, where sensitivity indices are denoted by I variable in the following and are calculated from replicated simulations with the same underlying parameter configuration. The sensitivity analysis of the mean of model outputs across landscape replicates ( Fig 1A right) shows that variations in mean predator population density are mainly explained by predator migration ( ) and by the proportion of hedges ( ), whereas interactions among parameters have little impact on the outputs. For the mean pest population density and the average number of pesticide applications, crop proportion ( and , respectively) and pest growth rate ( and , respectively) are the most important parameters to explain model output variability, again with only little interaction between model parameters ( Fig 1B right). Complete results for pesticide applications are given in the S1 Text . 3 Discussion Sustainable management of pests and diseases in agro-ecosystems requires a better understanding of how landscape structure drives and alters population dynamics. By simulating different landscape configurations including linear corridors, and the predator-pest dynamics, the present research aims at characterizing the joint influence of landscape structure and species traits on CBC service. Our study corroborates that spatial heterogeneity, landscape structure (i.e., the size and physical arrangement of patches), species traits and their interactions play a key role for CBC. High crop proportion is the major determinant of increasing pest population and results in an increased number of pesticide applications over the whole landscape. Indeed, increasing crop proportion in fragmented landscapes ensures food availability to the pest all over the landscape [1,2,12]. In highly aggregated landscapes, the size of contiguous crop patches is already large enough to sustain a relatively large pest population, thus lowering the effect of an increase in crop proportion [14]. The effects of crop proportion and spatial crop and hedge aggregation are intimately linked to pest growth rate and dispersal capability. Indeed, unfavorable landscape properties for the pest (i.e., low proportion and high fragmentation) can be compensated by a higher growth rate. However, the effect of dispersal is a double-edged sword since high dispersal helps spreading on fragmented landscapes but comes with a larger amount of propagules lost in unsuitable habitats, potentially leading to a dilution effect [3,24,25]. As expected, hedge proportion (i.e., SNHs) positively affects predator presence in agricultural landscapes. In addition, the predator’s ability to move between SNHs and crop habitats is the parameter that increases most strongly the predator density, since it enables predators to reach complementary resources in crop fields more easily. Predator fluxes from adjacent habitat is reported to have a major impact on pest populations in crop fields [3,12,26]. Spillover from hedges to fields not only depends on predator propensity to forage outside their natural habitat, but also on semi-natural patch connectivity and on crops and predator reservoir interface [27]. Thus, different combinations of SNH proportion and aggregation influence landscape structural connectivity and are also important determinants of predator efficiency in regulating crop pests [27]. In our representation, hedges are modeled as a source of predators where these have logistic growth. This is a simplification for predator dynamics in their natural habitat, as we do not consider potential prey presence in hedges and predator foraging behavior in crop fields. For example, the growth rate, instead of being constant, could depend on the time spent in the fields and on the number of consumed preys. In addition, predating rate and consumption rate are crucial in determining the efficiency of CBC [28]. Here, these parameters are not identified as influential in the dynamics, maybe because they are assumed identical (parameter β in our model). Finally, another strong assumption of our model is that we refer to a selective pesticide application which does not affect predator mortality, such that we do not explore a broad-spectrum pesticide scenario. In general, broad-spectrum pesticides are more commonly applied [17], but there are pest management programs where selective insecticides have been proved to be particularly effective in combination with a CBC strategy by weaving together direct targeted reduction in pest numbers with predator conservation [17,29]. Moreover, introducing broad-spectrum pesticide application effects may result in secondary pest breakouts [30–32], where pests benefit from the predator reduction. Then, additional pesticide loads would be necessary to decrease pest density, which in turn continuously decimates the predator population [33]. Therefore, the effect of SNH and predators, and their relationships for CBC outcomes, would be confused and masked. In our work, an indirect effect could be observed: in crop fields, a positive predator growth rate relies only on pest availability, such that a strong pest reduction due to pesticide applications is automatically translated into a strong impact on predator density when such pesticide applications occur. In our analysis, we found that the predator’s ability to disperse from hedges to crop fields has a major influence on pest density and related pesticide applications. High crop proportion enhances pest density, but this effect is counter-balanced by the joint effect of hedge proportion and predator spillover from hedges to fields, which favors predator pressure and reduces pesticide applications. Indeed, hedges ensure an increased functional landscape connectivity, which enables predators to successfully disperse and feed on complementary resources in the fields. Interestingly, however, we found that if SNHs can sustain a high population of predators [25], this is not sufficient to achieve a decrease in pest density. Indeed, by keeping the pest population density under the pesticide application threshold, the predator population can favor its spread across the landscape, thus increasing pest density at the landscape scale, even if fewer pesticide applications are applied. Most of the studies consider the amount of SNH as a proxy for predator presence and focus on how landscape structure directly influences CBC. However, as highlighted by our results (see also [34]), the extent to which species are influenced by landscape heterogeneity depends on their traits. For example, [35] argue that predators with an oriented movement are better able to deliver pest control services. They discuss the interplay among predator mobility, proportion of crop and SNHs. More generally, predator fluxes from SNH are expected to be particularly strong when (i) predator attack rates on prey are high, (ii) predator movement abilities are substantial, and (iii) predator mortality rates in the recipient habitat are low [34]. However, we point out that the predator we model is a generalist predator that does not show strong aggregation behaviour towards pests. Pests represent a predator resource in field, but predators can persist in the landscape also without pests as they have a positive growth in hedges. Different outcomes would be probably observed when considering a specialist predator showing an aggregating behaviour around local pest outbreaks [36]. As for example in [36], specialist predators are found to be more effective agents in suppressing local outbreaks than generalist ones. The amount of predator spillover from hedges to fields, and the distance over which pest and predator can spread, both depend on local configurational variables such as field size, shape, amount of shared edge, and connectivity [20]. Large fields can support high pest volumes, but it has been demonstrated that the relationship between field size and pest density can take several forms depending on assumptions, conditions and species considered [37]. Our results show a negative effect of large field area on the need and quantity of pesticide applications, which, according to [37], may come from the elevated growth rate of the prey combined with its good dispersal ability. By contrast, a high number of pesticide applications is favoured by long field perimeters, as these facilitate high fluxes of pest coming in from surrounding fields. However, when a hedge is present on a field boundary, we observe a reduction in numbers of pesticide applications, as there is an increase of predator spillover from hedges into fields [9]. Interestingly, we show a contrasted effect of hedges depending on the scale considered. At global scale, the proportion of hedges shows a positive effect on pest density and has a negative effect only on the presence of pesticide application. At local scale, an elevated number of hedges on crop boundaries shows an even more important impact on CBC by negatively affecting both the local presence and number of pesticide applications [25]. Landscape simplification is a major driver of pest abundance and consequently has strong impacts on the necessity of pesticide applications and their frequency. We find that natural habitat enhances predator population, but it does not systematically translate into a strong correlation with pest density decrease. However, a relatively high predator density often helps maintaining pest density below the threshold level above which pesticides are applied, thus preventing highly localized pest densities. However pest population can already have a moderate density level over substantial surfaces and therefore may quickly propagate in every point of the space. Indeed, in our model the hedges are generally expected to play a positive role, but our results at global scale show that the final outcome must be analyzed in a much more nuanced way. By contrast, predator spillover from hedges to fields is fundamental for CBC; it reduces pest density and guarantees high predator fluxes and different habitat connectivity. At field scale, landscape geometric features, hedge presence and habitat connectivity are able to influence predator-pest dynamics, and therefore they affect the number of pesticide applications. This highlights the importance of conducting a multi-scale analysis to consider the differences in outcomes at landscape and patch scale for pest CBC [14]. In most of our analyses, we considered global outputs by averaging pest and predator densities over crop fields. However, populations are obviously structured in space and time. Thus, a complementary analysis studying how landscape structure impacts spatio-temporal predator-pest dynamics would bring deeper insights on pest outbreak determinants. Moreover, a larger number of pest and predator species, inter/intra-species interactions and also different trophic network structures, could be considered in future work to better understand the role of pest and predator diversity on CBC efficacy. [END] [1] Url: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1009559 (C) Plos One. "Accelerating the publication of peer-reviewed science." 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