Modelling the effect of field margins on parasitoid-host interactions

Transcription

1 Modelling the effect of field margins on parasitoid-host interactions Tom Brand

2 Modelling the effect of field margins on parasitoid-host interactions Thesis report Student: Tom Brand WUR student number: Course code: BFS Supervisors: Dr Felix Bianchi (WUR) & Dr Gerard Driessen (VU) 2

3 Contents Contents... 3 Abstract... 4 Introduction... 5 Material and Methods... 8 Results Discussion References Appendix I Parameters used in the model Appendix II Sensitivity analysis at low aphid densities Appendix III Sensitivity analysis at high aphid densities Appendix IV aphid and parasitoid population dynamics in time

4 Abstract An increase in species interaction within agricultural landscapes could improve ecosystem services by for example applying top-down pressure on pest species populations. Previous studies have shown that agricultural field margins can, as a form of managed habitat, contribute to parasitoid mediated pest control. Where general predators prey on a wide range of species, parasitoid wasps are specialists that parasitize one or a small group of hosts. As many species of parasitoid do not feed on their host during the adult life stages other sources of nutrition are required to enhance longevity. Nutrients that enhance longevity are acquired from sugar resources like flowering plant nectar. Additionally agricultural landscapes with annual crops allow for minimal parasitoid hibernation survival. In such areas perennial field margins can provide hibernation habitat, which contributes to an early response to host emergence and long term pest control. To explain the underlying mechanisms that determine the respective influence of annual field margins with flowering plants and perennial field margins on parasitoid-host interaction, and how proportion and distribution of fields containing field margins affects aphid densities and parasitism, mathematical spatial models are used. To appropriately apply the effect of an annual field margin on mean parasitoid longevity within a spatial grid that represents an agricultural landscape, an individual based model was used to study the effect of a flower strip on individual parasitoids within a single field. This was then combined with the currently knowledge on parasitoid hibernation survival and applied to a landscape model that simulates parasitoid host interaction. Simulations by the landscape model show that perennial and annual field margins can both effectively increase aphid suppression on a larger then within field spatial scale. The results show how parasitoid dispersal capacity and field distribution influence pest suppression in fields with and without field margins. Though the path to enhancing biological control through enhancing parasitoid longevity is not straightforward. Improving the effectiveness of annual field margins can lead to unpredictable seasonal pest suppression due to the rapid rise and fall of both parasitoid and host populations. Combine those findings with the more stable effect of perennial field margins, namely increased parasitoid density and parasitism rate in relation to the fraction of fields with perennial field margins, and the possibilities for future studies on bio control through enhancing parasitoid host interaction look very exciting. 4

5 Introduction While synthetic insecticide use is still standard practice for most of the global food production, the environmental costs of these practices and the potential of low-input farming practices have become more appreciated by society and governments (BANR, 2003; EU directive 2009/128/EC). Intensive farming practices can cause natural ecosystem services to degrade, for instance by providing a less suitable habitat such that the number of natural enemies can be reduced and with that valuable biocontrol services. Reduced natural enemy populations can release insect herbivores from top-down control and may lead to increased risk of pest outbreaks and the associated use of synthetic insecticide applications (Daily 1997). In turn, an increase in predation and parasitism within agricultural landscapes can improve top-down regulation of pest species (Halaj and Wise 2001), which in turn would allow for the reduction of chemical input in farming practices. The potential of natural enemies as biological pest control agent has been studied for many decennia, documenting both successes and failures (Howarth 1991). More recent studies have shown that the potential of natural enemies to control pests depends on the habitat that agricultural ecosystems provide for predators and parasitoids (Landis et al. 2000, Bianchi et al. 2006). Here, we will explore two important functions habitats can provide for natural enemies: (i) winter survival and (ii) nectar. Non-crop habitats, such as woody and herbaceous perennial field margins provide undisturbed host plants and soil, and can function as micro habitats that are less exposed and disturbed than agricultural fields (Dix et al. 1995). This allows these areas to function as hibernation sites for parasitoids (Geiger et al 2005) and other natural enemies (Geiger et al. 2008). Hence, perennial field margins could possibly improve recolonisation of natural enemies to agricultural fields. Recolonisation is important as insect populations decline seasonally in agricultural areas due to seasonality, harvesting of the crops and ploughing of the field (Geiger et al. 2005, Pereira et al. 2010). Another ecologically beneficial landscape element are annual field margins that contain flowering plants. Flowering plants provide an alternative food source for predator and parasitoid species as these often require an additional food source besides their main prey/host species (Siekmann et al. 2001, Lee et al. 2006). The pest regulating effect of natural enemies is therefore at least in part - dependent on the resources and overwintering habitat an area provides. Annual flower strips can only boost parasitism rates up to a critical distance. As parasitoid species often cannot acquire resources from their hosts in their adult life stage, they require plant derived resources from nectar. Laboratory experiments have shown that when a sugar solution is available parasitoid longevity can be increased by approximately 100% in Aphidius rhopalosiphi and 50% in Diaeretiella rapae (Tylianakis et al. 2004). Using microcosm experiments nectar provided by buckwheat (Fagopyrum esculentum) has been shown to substantially enhance parasitoid lifetime fecundity (Winkler et al. 2006). Wackers and coworkers demonstrated that Diadegma semiclausum wasps (n=12) with nectar supply were able to parasitize more than 300 Plutella xylostella (diamondback moth) per individual, with 5

6 an average of 390 ± 31 caterpillars parasitized per wasp. In the control group, where the wasps were given no nutrient supply, 3 of the 11 introduced wasps were able to parasitize the host animals, averaging 3.7 ± 3.2 caterpillars per wasp. This dependency on frequent nectar consumption is further explained by the inability to store energy in lipids, an adaptation found in many parasitoid species (Visser and Ellers 2008). Parasitoid wasps cannot acquire nectar from a number of plant species due to an incompatibility between wasp and flower anatomy, hence within agricultural landscapes annual flower strips planted with flowering plants that do have accessible and available nectar can provide a unique source of nutrition (Wäckers 2004, Bianchi and Wäckers 2008, Nafziger Jr and Fadamiro 2011). To help explain the underlying mechanisms that determine the effect of annual flower strips, mathematical spatial models have been used. Bianchi and Wäckers (2008) modelled foraging parasitoid behaviour using a spatially explicit model. Results from these model simulations suggest that the often observed increase in parasitoid density near strips can be attributed to nectar feeding leading to higher parasitoid longevity, rather than the aggregation of parasitoids from surrounding areas towards flowering strips. Understanding the mechanisms that cause flower strips to influence parasitism, should allow us to assess the spatial extent of the influence zone of annual flower strip on parasitoids. Crop habitats are typically disturbed environments. For instance, crop harvesting can compromise parasitoid survival between growth seasons. Without hibernation sites annual fields have to rely solely on parasitoid migration or reintroduction to re-establish populations in the crop. This gives areas with hibernation sites a distinct advantage due to earlier recolonisation by a potentially larger number of parasitoids. This suggests that perennial strips that provide hibernation sites for parasitoids could increase parasitoid survival. Although host plants in perennial strips can enhance the survival rate of parasitoids during winter, field experiments have shown that pupae are vulnerable to external factors such as exposure to harsh weather and predation (Geiger et al. 2005). The potential effect of enhanced winter survival on pest regulation was shown in species interaction experiments using pea aphids, Acyrthosiphon pisum, and their parasitoid Aphidius ervi. These experiments showed that larger parasitoid populations at the start of a growth season were more capable at suppressing early aphid population growth than small initial parasitoid populations. Furthermore, unreliable viability of small populations causes variance in parasitism percentages that can be reduced with increased population size (Rauwald and Ives 2001). These results suggest that perennial strips can enhance parasitoid mediated pest control at the start of the growth season. The impact of annual flower strips and perennial field margins on parasitoid populations and the associated parasitism rates can potentially be influenced by factors beyond the field scale. A recent study by Bianchi et al. (2013) on the interaction between conventional and organic farming practices suggests that landscape composition in terms of field exposed to insecticide applications (conventional fields) or not (organically managed fields), and parasitoid dispersal were important factors for parasitism rates and pest regulation. In this 6

7 study the proportion and distribution of conventional and organic fields within a landscape influenced pest regulation in both conventional and organic field types. Findings like these indicate that habitat management to enhance the effectiveness of natural enemies as biocontrol agents should not only focus at the field scale, but should also should incorporate the landscape context. The aim of this study is to assess the effect of flowering plants, hibernation sites and landscape composition on parasite-host dynamics at a landscape scale, using a modelling approach. Firstly, the effect of flowering plants will be assessed through the use of annual field margins. Therefore, how does enhanced parasitoid longevity mediated by annual field margins influence parasitoid host interactions and the associated pest densities within an agricultural landscape? Based on current knowledge, enhanced parasitoid longevity mediated by annual strips can enhance parasitism, and thereby reducing associated pest densities within an agricultural landscape (Winkler et al. 2006, Bianchi and Wäckers 2008). Secondly, can hibernation sites provided by perennial field margins reduce aphid densities by enhancing winter survival of parasitoids? Based on the small existing body of literature hibernation habitat provided by perennial field margins improve host regulation by reducing recolonisation time of parasitoids (Geiger et al. 2005). Lastly, the influence of landscape composition on parasite-host dynamics at a landscape scale will be assessed. Does parasitoid dispersal capacity and fields with field margins distribution influence aphid parasitism rates and densities for the whole landscape or individual fields? The landscape study by Bianchi et al. (2013) suggests that reduced parasitoid movement and clustering of fields will increase parasitoid-host interaction in fields with annual and/or perennial field margins. A spatial modelling approach where the factors proposed in the hypotheses can be controlled, allows for the exploration of parasitoid-host interactions within landscapes consisting of fields with annual and perennial field margins. 7

8 Material and Methods A spatial model was developed to explore the parasitoid-host interactions in landscapes with different proportions and types of field margins using a 2-step approach. In the first step, we assessed the maximum distance from which parasitoids can benefit from nectar resources provided by flowering field margins. For this purpose we used a detailed individual-based model parameterized for Aphidius ervi (Haliday) (Hymenoptera: Braconidae), which simulates the foraging behaviour (i.e. nectar feeding vs. searching for hosts), energy balance, movement, parasitism and longevity of parasitoids (Vollhardt et al 2010). This exploration provided us an estimate of the spatial extent of the influence zone of flowering field margins on parasitoids. In the second step, we adapted an existing spatially-explicit model for parasitoid-host interactions at the landscape scale for A. Ervi and pea aphids Acyrthosiphon pisum (Harris) (Homoptera: Aphididae) by incorporating the effect of nectar resources and hibernation habitat provided by field margins (Bianchi et al 2013). We scaled the size of the spatial units (cells) from which the landscape was built up to the spatial extent of the influence zone of flowering field margins on parasitoids (as assessed in step 1). This procedure allowed us to scale up the effect for field margins on parasitoid-host interactions from the within field scale (step 1) to the landscape scale (step 2). Step 1: assessing spatial extent of the influence zone of flowering field margins on parasitoids For the within-field simulation experiment a field of 50 by m made up of 400 by 402 grid cells was considered. Each cell had a size of 12.5 by 12.5 cm. The field represents an agricultural winter wheat field that is composed of winter wheat and a flower strip in the centre (Figure 1). The cells either contained winter wheat or flowers. Winter wheat is a host plant for cereal aphids, whereas flowers represent a nectar food resource for parasitoid. Host feeding, as an alternative food source, was not included in the model. This was done to study the importance of flowering plants for parasitoids that can t obtain nutrition from their host. To simulate different aphid infestation levels, aphid density maps with a low and high aphid density were constructed. In these maps aphids were randomly distributed with mean Figure 1 Agricultural field schematic containing a flower strip (black line) and the transect along which parasitoids were released (grey line). aphid densities of respectively two and ten aphids per 12.5 x 12.5 cm cell containing winter wheat. In cells with flowers aphid densities were 50% lower. A single adult female parasitoid was considered of which the longevity, movement, feeding and parasitism were simulated. The parasitoid could move through the field as it searched for hosts and flowers. Parasitoid preference for hosts and flowers was dependent on its energy status. A low energy status results in a preference for feeding while a high energy status creates a preferences for parasitism. Parasitoid energy reserves were reduced by 8

9 factors that consume energy: a maintenance cost per minute in the form of respiration and an additional cost for movement per meter during foraging behaviour. The energy reserves could only be replenished when parasitoid found and fed on flowering plants. To search a parasitoid has a perception range of four cells on each side of the cell it resides in. Each simulated action or event has a given time cost. Parasitoids can continue living until their energy status reaches 0, or until their longevity exceeds their maximum lifespan. The mechanisms that influence parasitoid foraging behaviour are described in further detail in the article that published the model (Vollhardt et al 2010). To assess the spatial extent of the influence zone of flowering field margins on parasitoids, parasitoids were released on a transect perpendicular to the flower strip (grey line in Figure 1). One individual was placed at every cell of this row, effectively distributing wasps evenly along the entire width of the field. This distribution enabled the exploration of the influence of the flower strip on the parasitoid foraging behaviour and longevity. To estimate the spatial extent of the influence of the flower strip, nectar feeding was first observed along the X-axis using Figure 3. In simulations that were visualised in Figure 3 parasitoid longevities near the centre of the X-axis and close to the flower strip were substantially higher than further away from the flower strip. Based on this it was estimated that within an approximate 10m range around the centre of flower strip parasitoids could be affected. Taking the mean longevity within a 10 meter distance from the flowering plants and comparing that to the mean longevity outside this range provides an estimate of the longevity increase flowering plants can provide within that range (table 2). To test the robustness of the longevity increase and the 10m range of influence we performed an sensitivity analysis of 12 included parameters (described in appendix 1) to determine both the impact of individual parameters (Appendix 2 and 3) and whether parasitoids would remain uninfluenced outside the 10m range. The results of the sensitivity analysis can in this manner help assess the spatial extent and show which parameters have the highest impact on the spatial extent of the influence zone of flowering field margins on parasitoids. Step 1b: Hibernation survival on host plants by parasitoids Where annual flower strips focus on improving an areas habitat suitability of parasitoid populations during the growth season, perennial strips near agricultural fields could potentially improve parasitoid hibernation survival. This can be beneficial as parasitoid survival is expected to be very low during winter in agricultural fields after crop harvest. Enhanced winter survival in herbaceous perennial strips can improve early recolonisation of parasitoids, enabling a quicker response when pest species such as aphids colonise crops (Rauwald and Ives 2001). Parasitoid winter survival is taken as the hibernation survival between growth seasons and was based on the results found by Geiger et al (2005). In this study Diaeretiella rapae (mummy) densities were measured on host plants at two sites in The Netherlands in the months of December, January and February during the winter of Using densities 9

10 measured at the research site near Achterberg (The Netherlands), where parasitoid densities were highest and decreased the most, hibernation survival estimates were created for the between season period used in the landscape model (see step 2). At this site there were approximately 55 mummies per plant in December, and densities were reduced to approximately 8 mummies per plant in February. Although no live Brevicoryne brassicae were found on the host plants in the study by Geiger et al (2005), the potential benefit of perennial field margins for pest species cannot be ignored. Therefore, improved hibernation survival that perennial field margins provide will not be implemented differently for hosts and parasitoids. Step 2: Parasitoid host interactions at the landscape scale For up scaling of the parasitoid foraging behaviour from the within-field level to the landscape level, integrating the effects of flowering and perennial field margins was done by recognising two types of fields: fields with and without a field margin. The landscape generated within this model is a grid of 50 x 50 cells that represent 20 x 20m fields. The model recognizes two types of cells within the landscape, fields influenced by annual or perennial strips and uninfluenced fields. In these cells depending on the scenario applied, parasitoid longevity and/or between season survival was increased as an effect of the resources and shelter provided by the strips. Although parasitoids and hosts interact at the field scale (parasitism), their population dynamics are connected through parasitoid and host dispersal at the landscape scale. The model does not include alternative hosts or natural enemies. Parasitoid-host dynamics, species interactions, survival rate and fecundity are described using a stage structured model. Using a Leslie matrix (Caswell 1989) a density-independent survival is given to all five host life stages and fecundity ( ) to the adult life stage. To account for the carrying capacity of fields a density-dependent mortality was included for all host stages, on the total density of hosts at time. Mortality causes other than parasitoids are implicitly incorporated into this survival. Without parasitoids host dynamics within a cell is given by Where represents the five aphid life stages, four juvenile stages and one adult stage, in a 5 x 1 Leslie matrix vector with densities of the five host life stages at time 10

11 The model assumes that the four immature life stages last the same time (two days), thus the development time of host stage sets the time scale of the model. Parasitoids have host life stage ( ) specific attack rates given by, while parasitoids also have an overall attack rate or search efficiency ( ). The density of adult parasitoids then determines the proportion of hosts in life stage that are parasitized: Using these proportions the following matrix gives the proportion of hosts that are not parasitized, and with that the host dynamics found within individual fields Parasitoid larvae require five host-development time units to kill their host and initiate pupation. Because parasitized first-instar aphids always reach adulthood before mummies are formed, we assumed that larval parasitoids go through all five host developmental stages, during which time they suffer density-dependent survival equal to that of unparasitized aphids (Rauwald and Ives 2001). The pupal stage takes three time units during which survival is given by ( ). The adult stage of parasitoids is assumed to have survivorship ( ), which results in total parasitoid survival being displayed as This means that parasitoid population at time t is given by the element of Y(t) being adults, y(t). This can be displayed as vector Y(t), with the last 11

12 Where is the identify matrix and is an matrix with ones in the top row and zeros elsewhere to aggregate new parasitoid larvae from all possible parasitized host life stages. (Bianchi et al 2013). For the dispersal of hosts and parasitoids it was assumed that a fraction of adult hosts and of adult parasitoids can disperse among fields. For adult hosts a global dispersal is assumed in which individuals disperse to any cell in the grid with equal probability; this dispersal is consistent with the biology of aphids, as these can be carried great distances once in flight (Taylor 1986). For parasitoids dispersal is spatially restricted, whereby the probability of an adult parasitoid dispersing a distance follows a rotationally symmetric negative exponential function. This results in that most of the dispersing adults, that leave the natal field, to move to directly adjacent fields. Important to note is that this allows a fraction of adults to remain in the natal field, even if the dispersal capacity is 1 (Bianchi et al 2013). Parameterization and scenario studies Baseline parameter values from Bianchi et al. (2013) were unchanged, unless mentioned below as an adaptation required to incorporate the field strip effects. Parasitoid mean longevity found outside the range of influence of annual strips (as described in step 1), were applied as the base longevity for fields without a flower strip. To simulate the effect of nectar feeding in fields with annual strips the survival rate of adult parasitoids ( ) was increased to enhance mean longevity. In these fields parasitoid longevity is raised to resemble the mean longevity found within 10m of the flower strip, as described by the within field model in step 1. To explore the potential of further enhanced longevity in parasitoids, scenarios with an improved annual field strip effect are simulated where parasitoids have a mean longevity twice as high as found within flower strip influence range using the within field model. To incorporate the effect of disturbances (e.g. harvesting and ploughing) and adverse weather conditions during winter a mortality event was introduced at the end of the growing season. We assumed an average growth season of 150 days (75 time steps), after which the mortality event takes place accounting for parasitoid and host mortality during winter. This is implemented as a single mortality event after which only a fraction of the population survive. This fraction is in fields without perennial strips, 0.01 in fields with a perennial strip and 0.05 in field with an improved perennial strip. Parasitoid survival fractions are based on field observations by (Geiger et al. 2005), where the survival trend during the months of December January and February show a 5% aphid hibernation survival on host plants. Early-season, long distance aphid colonization is described as a uniform aphid introduction blanket over the whole landscape. Adding growth seasons and perennial field margins that provide habitat for winter survival, provides an opportunity to study the importance of parasitoid and aphid between season survival. 12

13 To determine the potential of field margins for enhancing aphid suppression, different field margin types were created with annual and/or perennial field margin effects (Table 1). In all landscapes, hosts and parasitoids are randomly introduced in 10% of the fields with host densities 10 times higher than parasitoid densities. The results from the landscape model were studied approached using three methods. Table 1 Overview of field margin types. Field margin types include annual and perennial field margins, which may impact parasitoid longevity (L) and hibernation survival (H). Field margin effects on longevity and hibernation survival are either classified as low, middle or high. Field margins Between season Parasitoid adult Description survival (fraction) longevity (days) Hlow+Llow No functional field margin Hlow+Lmid Annual field margin Hlow+Lhigh Improved annual field margin Hmid+Llow Perennial field margin Hmid+Lmid Perennial + annual field margin Hmid+Lhigh Perennial + improved annual field margin Hhigh+Llow Improved perennial field margin Hhigh+Lmid Improved perennial + annual field margin Hhigh+Lhigh Improved perennial + improved annual field margin First, to determine the effect of field margins on parasitoid host dynamics in time, host load (the cumulative host days across all fields in the landscape during the recording period) and mean parasitism rate (proportion of host load parasitized during the recording period) were calculated. Secondly, the effect of field margins on parasitoid-host interactions may extend beyond the fieldscale. To explore this further, five scenarios were created using landscapes of which 10% of the fields contained field margins. Simulation entailed 900 time steps, representing 12 years. To reduce the effect of the initial host and parasitoid release and to allow the perennial field margins to present their potential, a 300 time step (4 years) burn in period was used, the remaining 600 time steps (8 years) were used to determine differences between host load and parasitism. For these simulations five designs were used (Table 2): Scenario A, which we will use as a reference to compare the other scenarios with, fields with field margins are randomly distributed within a landscape and parasitoid dispersal is set at the standard value as chosen by Bianchi et al (2013). In scenario B field distribution is clustered rather than random, these spatial patterns are shown in Figure 2. In scenario C aphids only survive in field margins, while in scenario D aphids do not survive in field margins but are homogeneously introduced to the landscape at the start of each growth season. In scenario E parasitoids have a reduced dispersal capacity, the fraction of parasitoid that can migrate to nearby fields remains 1, the distance moved is however reduced from 3 to 1 cell. Table 2 Overview of the five scenarios on parasitoid-host interaction at the landscape scale. 13

14 Scenarios A (reference) B C D E Description Random field distribution and unaltered parameters Clustered field distribution Aphid hibernation survival altered, early season aphid introduction blanket removed Aphid hibernation survival altered, perennial field margins do not improve aphid hibernation survival Reduced parasitoid movement, distance moved from natal field in other scenarios D=3 in this scenario D=1. Lastly, the model was used to simulate parasitoid host dynamics, along a gradient of fraction of fields with field margins ranging between 0-100%. To reduce the standard deviation between samples it was decide to use 15 repetitions when calculating the aphid and parasitoid load as a function of fraction of fields with field margins. 14

15 Results Assessing spatial extent of the influence zone of flowering field margins on parasitoids Adult parasitoids that emerge within 10 meters of the flower strip have an on average higher longevity, parasitism and distribution potential than parasitoids that emerge outside this range (Table 2). The life history data of parasitoids that originate within a 10 m-range of flower strips have a higher SEM, which is caused by nectar feeding events that create the variations in energy available to parasitoids. Table 2 Individual based model output; parasitoid longevity, number of aphids parasitized and meters dispersed at low and high aphid densities far away and close to the flower strip. Aphid density Distance to flower strip Longevity (days) Parasitism (aphid) Dispersal (m) Mean SEM Mean SEM Mean SEM Low <10m e >10m High <10m e >10m Figure 2 Parasitoid longevity (days) along the width of a field (in metres) with a flow strip in the centre. 15

16 The robustness of the model output was tested using a sensitivity analysis for the variables: parasitoid longevity, parasitism rate and dispersal. The percentage of nectar feeding events of the total number of feeding events in the field, that take place within 10m of the flower strip was used to further assess whether parasitoid were not affected by the flower strip beyond this distance. In all of the scenarios tested in the sensitivity analysis, more than 99.5% of the nectar feeding events were within the chosen range of 10 m (Appendix II and III). The results of this analysis allowed me to properly implement the effect of a flower strip to the landscape model. The sensitivity analysis revealed that parasitoid dispersal was most sensitive for changes in the model parameters, followed by longevity and lastly parasitism (Appendix I). When outside the range of influence of the flower strip parasitoid dispersal was most sensitive for an increase in the energy cost of movement ( % variation depending on aphid density), inside this range the amount of energy acquired during nectar feeding was the most influential for parasitoid dispersal ( % variation). Longevity of the parasitoids was most sensitive to the amount of energy acquired during nectar feeding ( variation), lower initial energy status (3% variation) and the cost for movement (2% variation). Parasitism was most affected by 10% changes in the movement costs ( % variation) outside flower strip range, same as at high aphid densities inside this range (7% variation), at a low aphid density inside the flower strip range a 10% increase of the energy acquired during a nectar feeding event had the most influence (8.2% variation). This sensitivity analysis indicates that especially variation in the energy acquired during nectar feeding has an strong effect on parasitoid longevity. Interestingly, parasitoid dispersal and parasitism efficiency were more strongly affected by movement costs. Parasitoid host interactions at the landscape scale The results of the landscape scale parasitoid-host interactions are presented in three sections. Firstly, the dynamics of parasitoid-host population interactions were studied for the different annual and perennial strip types while keeping the proportion of fields containing strips in the landscapes fixed at 10%. Second, the relative aphid load and fraction of parasitism are explored in fields with and without annual and perennial strips for the different strip types when 10% of the fields contain strips. Thirdly, how aphid and parasitoid loads and fraction of Figure 3 Snapshots of the spatial pattern of hosts (left) and parasitoids (right) after 480 time steps in random (top) and clustered (bottom) distributed fields. Each cell represents a field with or without a field margin. Dark and light cells represent high and low population densities, respectively. 16

17 parasitism are influenced when the proportion of fields containing strips on the landscape ranges from 0 100% was explored. The aphid and parasitoid densities were differently affected by the field margin types, during the first 450 time steps (Figure 4). The individual simulations showed that annual and perennial field margins types improved aphid control during the growth season. Planting a field margin that either influences longevity or hibernation survival, on 10% of the agricultural fields, decreased the cumulative host days of the whole landscape by %, when combining the two effects they can be decreased by %. Figure 4 shows that field margin types that enhance parasitoid longevity cause enhanced parasitoid population growth early in the growth season for annual field margins. Field margin types that enhance hibernation survival affect aphid load by removing a portion of the parasitoid population recovery time, which is caused by the larger number of parasitoids and aphids that survive the winter period. Additionally, the aphid load trends shows that the benefits field margins provide for hibernation survival and parasitoid longevity are not completely additive. Figure 4 Simulated aphid and parasitoid population dynamics for a six-year period. Simulations represent field margin types (table 1), with increasing hibernation survival from top to bottom and mean parasitoid longevity increasing left to right. Aphid load (X) is given relative to the aphid load found in the simulation with the lowest aphid longevity and hibernation survival. In these simulations 10% of the fields contain field margins and are randomly distributed within a landscape. 17

18 The effect of field margins on parasitoid-host interactions may be may extend beyond the field scale. To efficiently compare the results calculated for the different scenarios (Table 2 and Figure 5), the relative aphid load and parasitism rates of simulations with improved annual and improved perennial field margins were used (Table 2). In scenario A, which we will use as a reference to compare the other scenarios with, fields with field margins are randomly distributed within a landscape and parasitoid dispersal is set at the standard value as chosen by Bianchi et al (2013). In this scenario the aphid density and the fraction of aphids parasitized is more or less the same in fields with and without field margins (relative aphid load in fields with margins was 0.718, in fields without margins and for the entire landscape 0.736). Clustering of fields with and without field margins (Scenario B) enhances the effectiveness of field margins (relative aphid load in fields with field margins was 0.611, in fields without field margins and for the entire landscape 0.745). These differences in aphid load and parasitism in landscapes with random and clustered fields (Fig. 5A vs B) was caused by the change in average distance between fields with and without field margins (Fig. 2). In scenario C perennial field margins does not improve aphid hibernation survival, this had a substantial impact on the effect field margins has on aphid density and the parasitism rate. In this scenario aphid load is only reduced in simulations with improved perennial field margins (Fig. 5C, field margin types with Hhigh). This effect is the result of parasitoids not having enough hosts to adequately recover from the population bottleneck between growth seasons. The reduced recovery potential causes the parasitoid population to fail before the end of the burn in period and the observation period of these simulations starts (after 300 time steps, 4 years). The field margin type with an improved annual and improved perennial field margin effect in scenario C had a relative aphid load of in fields with field margins, in fields without and for the entire landscape. In scenario D removing of the improved hibernation survival by perennial field margins for aphids had little effect on the aphid density and parasitism, as compared to the base scenario. The respective aphid loads for fields with and without a field margin were and 0.737, while it averaged for the landscape. In the scenario where parasitoid have poor dispersal capacity (scenario E), there is a more substantial difference in aphid density and parasitism between fields with and without field margins (Figure 5 scenario E vs A). Reduced parasitoid dispersal results in a relative aphid load of in fields with field margins, in fields without margins and for the whole landscape. To investigate how the proportion of fields with a field margin influences the parasitoid and host population dynamics, the effect of field margins was considered for the entire landscape (Figure 6). The first observation that can be made is that in all simulations where field margins increase parasitoid longevity or hibernation survival, aphid load decreases as the proportion of fields with field margins increases. Next are the graphs that represent relative parasitoid load and fraction of parasitism. In these graphs the trends initially show steep growth curves that become saturated or negative as the proportion of fields with a 18

19 field margin increases. Field margin types that have an improved annual field margin effect and therefore affect parasitoid longevity the most, lead to the most unstable correlations between parasitoid-host dynamics and the proportion of fields with a field margin. Potential causes of these trend deviations will be explored in the discussion. Two field margin types where field margins improved hibernation survival (Hhigh+Llow, Hhigh+Lmid), are the simulations that have the highest parasitoid load when the proportion of fields with a field margin was high. Field margin types that improve parasitoid longevity most (Lhigh), have the most substantial decline in parasitoid load after the initial increase, resulting in the three trends with the highest parasitoid longevity having the lowest parasitoid load when all fields contain field margins. 19

20 Random fields Clustered fields No aphid blanket No perennial field margin effect on aphids Reduced parasitoid migration distance Figure 5 Relative aphid load (left) and parasitism rates (right) in fields without (black) and with field margins (white). For these scenarios and different parameter values 10% of landscape area are fields with field margins. (A) random field distribution, normal dispersal capacity of parasitoids, aphids survive in field margins and are newly introduced to the landscape at the start of a new growth season. (B) clustered field distribution, normal dispersal capacity of parasitoids, aphids survive in field margins and are newly introduced to the landscape at the start of a new growth season. (C) random field distribution, normal dispersal capacity of parasitoids, aphids only survive in field margins. (D) random field distribution, normal dispersal capacity of parasitoids, aphids do not survive in field margins but are newly introduced to the landscape at the start of a new growth season. (E) random field distribution, poor dispersal capacity of parasitoids, aphids survive in field margins and are newly introduced to the landscape at the start of a new growth season. 20

21 Fraction fields containing field margins Figure 6 Relative aphid load (left), relative parasitoid load (middle) and the fraction of aphid parasitized (right) as function of the proportion of fields containing field margins. The three variables were measured in scenarios with a hibernation survival in field margins that is low (black), medium (dark grey) or high (light grey) and have a longevity benefit that is low (solid), medium (dashed) or high (dotted). These scenarios are further described in table 1. 21

22 Discussion Important findings presented in this study included (i) the respective influence of flowering and perennial field margins on parasitoid-host inter-action, and (ii) how proportion and distribution of fields containing field margins affects aphid densities and parasitism. Introducing perennial as an alternative to annual field margins had a more substantial impact on parasitoid host dynamics. This is especially apparent in landscapes where few fields contained field margins, indicating that a lack of hibernation sites severely limits parasitoid mediated host suppression. The importance of stimulating Aphidius ervi population recovery, through the enhanced survival of various parasitoid life stages, has been reported before (Rauwald and Ives 2001). The impact of multi-season parasitoid mediated pest suppression within a landscape was studied by analysing aphid abundance and parasitism. Landscapes where improved annual field margins were present in 10% of the agricultural fields, aphid abundance was decreased twice as effectively compared to landscapes with normal annual field margins. At a small ecological scale parasitoid time and egg limitation dominate parasitoid-host interaction (Rosenheim 1999). As mentioned before this can be influenced through food availability, enhancing local parasitism rates (Winkler et al. 2006). Considering normal annual field margins improved parasitoid longevity with 2.1 days in fields with field margins and improved annual field margins with 7.4 days, the efficiency of increasing parasitoid longevity to reduce aphid abundance is not linear at the landscape scale. Explaining this can be done by looking at the parasitoid-host dynamics in time (Figure 4). In this figure simulations with improved annual field margins show stronger variations in parasitoid and host densities between seasons. This is explained by parasitoid populations being very successful during one season, by reducing aphid densities to such an extent that very few parasitoids remain for the start of the next season. Which could explain the multi-season efficiency of improved annual field margins. Furthermore, fluctuations in parasitoid efficiency would be impractical for biological control purposes. Lastly, these dynamics in time show the importance of perennial field margins for areas where parasitoids are not reintroduced every season. In simulations without perennial field margins, parasitoid populations do not recover until late in the season when few parasitoids emerge after hibernation at the start of a new season. These findings underline the importance of both field margin types for multi-season pest control. To stay within the explorative scope of this study, approaches were taken that avoid a model which loses functionality due to being too complex while taking in consideration ecological mechanisms that influence parasitoid-host dynamics. The spatial extent of flowering field margin on parasitoid longevity that was found within a single field could not be directly applied to the landscape in an effective manner. To avoid distorting the spatial influence it was decided to work with the 20x20m fields in the landscape model. This approach allowed for substantial changes in longevity to be realistically applied to relatively small areas. This 22

23 effect is in accordance with our own within-field results; mean longevity of significantly enhanced for parasitoids emerging within 10 meters of a flower strip while parasitoids emerging outside this range are hardly affected, and results found in another study where the individual based model was used to study within-field effects of flower strips (Bianchi and Wäckers 2008). Field margins, whether annual or perennial, cause increased parasitoid densities. These parasitoid densities cause a relatively high number of parasitoids to migrate away from these fields, which in turn increases parasitoid density in neighbouring fields. This kind of spill over effect of small areas, as compared to large areas becoming influenced to a lesser extent, is a more realistic scenario according to the parasitoid distribution mechanism found in within field studies (Bianchi and Wäckers 2008). How increased migration away from natal fields affects parasitism and aphid densities within a landscape is presented by the differences in Figure 5A (base) and 5E (enhanced parasitoid dispersal). These results show that the increased parasitoid migration to neighbouring fields, causes the influence of field margins to be distributed more homogeneous over the landscape, while reducing the field margin effect within the fields with the field margins. Clustering of fields with field margins influenced parasitoid-host dynamics, by reducing the average distance between them. The results of this is shown by the differences in Figure 5A (base) and 5B (clustered fields). In landscapes where fields with field margins are clustered, aphid control is enhanced for field with field margins, it did not however change the mean aphid density of the whole landscape. Field distribution and parasitoid migration influence parasitoid-host dynamics locally, while hardly influencing a landscapes total aphid load, suggesting that the most effective approach for managing the ecosystem services parasitoids depends on local pest regulation goals. For example, clustering fields with field margins and restricting parasitoid dispersal in areas where aphids loads are expected to be high, can result in more effective pest regulation. Parasitoid-host dynamics were substantially altered by the absence of aphids spreading homogenously across the landscape at very low densities during early growth season, as can be seen by the difference between Figure 5A (base) and 5C (No early season aphid blanket ). These results show essentially the absence of parasitism in landscapes that do not have improved perennial field margins. The homogenous blanket of aphids that is introduced at the start of the season, provides parasitoids with more hosts to recover from winter. This aphid dispersal mechanism was applied due to the well documented migration capacity of aphids (Ragsdale et al. 2011). The substantial impact of this mechanism on parasitoid-host dynamics within this model requires further analysis. While the mechanics should be further investigated, these initial findings suggest that parasitoid populations can poorly recover after the winter period without adequate host densities. An ecological factor that wasn t included in the model are generalist predators, but could potentially influence the effect field margins have on parasitoids. Specifically, perennial field margins can have a beneficial effect on predator populations (Denys and Tscharntke 2002). An increase in generalist predators could then lead to a rise in intra-guild predation (Brodeur 23

24 and Rosenheim 2000). While studying the potential effect this has on biological control, a study by Snyder and Ives (2003) found that the pea aphid (Acyrthosiphon pisum) population growth reduction caused by general predators and the parasitoid Aphidius ervi was additive, despite parasitoid density being 50% lower due to the presence of the predators. This study also suggests that later in the growth season when aphid and parasitoid densities decrease, predation might endanger parasitoid overwintering potential. As such intra-guild predation is also a concern that has been expressed when considering the effectiveness of perennial field margins. The early emergence of generalist predators within perennial field margins can help regulate the aphid population early in the growth season (Landis and Werf 1997, Boreau de Roince et al. 2013), but it can also reduce the number of parasitoid mummies (Snyder and Ives 2003), potentially further delaying the parasitoid response to the aphid population growth. Based on the findings presented above, parasitoid predation by generalist predators will have a marginal effect during the growth season while exerting a stronger effect outside the growth season. Parasitoid host interactions at the landscape scale, conclusion. This study has shown that field margins can be used within agricultural landscapes to help reduce pest densities. While surprisingly little is published about the effects of hibernation on the feasibility of using parasitoids as biocontrol agents, from this study we can conclude that perennial field margins can potentially enhance parasitoid densities. Though the coupled system between parasitoid and host lends itself well for effective host reduction, it also makes the system instable as the scenarios with altered aphid distribution and enhanced parasitoid longevity showed in two different ways. New methods of applying field margins within landscapes that can realise field margin potential, could help future agricultural landscapes maintain and improve beneficial parasitoid host interaction. 24

25 References Bianchi, F., C. J. H. Booij, and T. Tscharntke Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proceedings of the Royal Society B-Biological Sciences 273: Bianchi, F. J. J. A., A. R. Ives, and N. A. Schellhorn Interactions between conventional and organic farming for biocontrol services across the landscape. Ecological Applications 23: Bianchi, F. J. J. A. and F. L. Wäckers Effects of flower attractiveness and nectar availability in field margins on biological control by parasitoids. Biological Control 46: Boreau de Roince, C., C. Lavigne, J. F. Mandrin, C. Rollard, and W. O. Symondson Early-season predation on aphids by winter-active spiders in apple orchards revealed by diagnostic PCR. Bull Entomol Res 103: Brodeur, J. and J. A. Rosenheim Intraguild interactions in aphid parasitoids. Entomologia Experimentalis et Applicata 97: Daily, G. C Nature's services. Societal dependence on natural ecosystems. Island Press, Washington, DC.. Denys, C. and T. Tscharntke Plant-insect communities and predator-prey ratios in field margin strips, adjacent crop fields, and fallows. Oecologia 130: Dix, M. E., R. J. Johnson, M. O. Harrell, R. M. Case, R. J. Wright, L. Hodges, J. R. Brandle, M. M. Schoeneberger, N. J. Sunderman, R. L. Fitzmaurice, and L. J. Young Influences of trees on abundance of natural enemies of insect pests: a review. Agroforestry Systems 29: Geiger, F., F. J. J. A. Bianchi, and F. L. Wäckers Winter ecology of the cabbage aphid Brevicoryne brassicae (L.) (Homo., Aphididae) and its parasitoid Diaeretiella rapae (McIntosh) (Hym., Braconidae: Aphidiidae). Journal of Applied Entomology 129: Geiger, F., F. L. Wäckers, and F. J. J. A. Bianchi Hibernation of predatory arthropods in seminatural habitats. BioControl 54: Halaj, J. and D. H. Wise Terrestrial trophic cascades: How much do they trickle? American Naturalist 157: Howarth, F. G Environmental Impacts of Classical Biological Control. Annual Review of Entomology 36: Landis, D. A. and W. Werf Early-season predation impacts the establishment of aphids and spread of beet yellows virus in sugar beet. Entomophaga 42: Landis, D. A., S. D. Wratten, and G. M. Gurr Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology 45: Lee, J. C., D. A. Andow, and G. E. Heimpel Influence of floral resources on sugar feeding and nutrient dynamics of a parasitoid in the field. Ecological Entomology 31: Nafziger Jr, T. D. and H. Y. Fadamiro Suitability of some farmscaping plants as nectar sources for the parasitoid wasp, Microplitis croceipes (Hymenoptera: Braconidae): Effects on longevity and body nutrients. Biological Control 56: Pereira, J. L., M. C. Picanco, E. J. Pereira, A. A. Silva, A. Jakelaitis, R. R. Pereira, and V. M. Xavier Influence of crop management practices on bean foliage arthropods. Bull Entomol Res 100: Ragsdale, D. W., D. A. Landis, J. Brodeur, G. E. Heimpel, and N. Desneux Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56: Rauwald, K. S. and A. R. Ives Biological control in disturbed agricultural systems and the rapid recovery of parasitoid populations. Ecological Applications 11: Rosenheim, J Characterizing the cost of oviposition in insects: a dynamic model. Evolutionary Ecology 13: Siekmann, G., B. Tenhumberg, and M. A. Keller Feeding and survival in parasitic wasps: sugar concentration and timing matter. Oikos 95:

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27 Appendix I Parameters used in the model Parameters Value Unit description ar 4 integer Perception range for aphids fr 4 integer Perception range for flowers dm 0.5 min Duration of a single cell movement dn 5 min Duration of nectar feeding event dp 14 min Duration of parasitisation event ds 6 min Duration of search event em 7 1/day Egg maturation rate en 1 J Energy acquired during nectar feeding hs 2 Dimensionless Slope of aphid preference curve as function of parasitoid energy status mo 0.01 J/m Cost per meter displacement expressed in energy units per meter re J/min Respiration, maintenance cost of parasitoid st 1 Dimensionless Stochastic factor for perception of landscape 27

28 Appendix II Sensitivity analysis at low aphid densities For this sensitivity analysis the parameters aphid detection range and flower detection range were not tested at 10% variation but rather at 25%. This was required because these parameters were measured in integers, the base number of integers is four and could therefore vary by a minimum of 25%. Outside flower strip range Within flower strip range Parameter Deviation (%) Longevity (%) Parasitism (%) Dispersal (%) Longevity (%) Parasitism (%) Dispersal (%) ar fr dm dn dp ds em en hs mo re st

29 Appendix III Sensitivity analysis at high aphid densities For this sensitivity analysis the parameters aphid detection range and flower detection range were not tested at 10% variation but rather at 25%. This was required because these parameters were measured in integers, the base number of integers is four and could therefore vary by a minimum of 25%. Outside flower strip range Within flower strip range Parameter Deviation Longevity Parasitism Dispersal Longevity Parasitism Dispersal (%) (%) (%) (%) (%) (%) (%) ar fr dm dn dp ds em en hs mo re st

30 Appendix IV aphid and parasitoid population dynamics in time Simulated aphid and parasitoid population dynamics for an eight-year period. Scenarios represented by the simulations are described in the top right corner of the right graph, for more information on field margin properties see table 1 (material and methods). In these scenarios simulations presented in the left column had a low proportion (10%) of fields that contain field margins. In the simulations presented within the right column, a high proportion (90%) of the fields contain field margins. For all simulation fields were randomly distributed within a landscape. low high Fraction of fields containing field margins 30

31 low high Fraction of fields containing field margins 31