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Article

Habitat Modification Alters Food Web Interactions with Focus on Biological Control of Aphids in Apple Orchards

by
Ammar Alhmedi
1,*,
Tim Belien
1 and
Dany Bylemans
1,2
1
Research Station for Fruit (Pcfruit Npo), 3800 Sint-Truiden, Belgium
2
Department of Biosystems, KU Leuven, 3001 Leuven, Belgium
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(7), 5978; https://doi.org/10.3390/su15075978
Submission received: 26 February 2023 / Revised: 21 March 2023 / Accepted: 28 March 2023 / Published: 30 March 2023
(This article belongs to the Special Issue Biocontrol for Sustainable Crop and Livestock Production)
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Abstract

:
To date, direct interactions between pests and natural enemies are often considered in biocontrol programs. Recently there has been an increase of evidence for the importance of third-party mediated indirect interactions in determining the population dynamics of insects. Predicting the strength of such interactions remains a central challenge in biocontrol assessments. Here, two field experiments were performed in two years to investigate to which extent Dysaphis plantaginea Passerini, Aphis pomi De Geer, and Myzus cerasi Fabricius might indirectly interact through shared natural enemies and ants. We first studied the population dynamics of target insects in isolated orchards of apples and cherries. Secondly, we investigated how the spatial coexistence of aphid-infested cherries can indirectly affect the population dynamics of apple aphids via natural enemies and ants. In the first experiment, nine parasitoid species were recorded on apple and cherry aphids, among them were three species in common. Six predatory families were found on cherry and apple aphids, while only one ant species, Lasius niger L., was found associating with these aphids. In the second experiment, temporal variation in the natural enemy-mediated apparent competition between M. cerasi and apple aphids was found. The cherry aphid is likely to be an important source of natural enemies that attack apple aphids early in the season. Significantly reduced numbers of ants associating with apple aphids in the intercropping habitat were found. Our results emphasize the importance of considering indirect interactions in the designing of pest management strategies.

1. Introduction

The dynamics of apple aphid communities, like other insects, depend on direct and indirect interactions. While a growing number of studies have examined the impact of indirect interactions between herbivorous insects mediated by natural enemies on arthropod communities [1,2,3,4,5], research on the effects of indirect interactions between aphids mediated by ants is limited [6,7,8]. Many aphid species, such as rosy apple aphid (RAA), Dysaphis plantaginea, green apple aphid (GAA), Aphis pomi, and black cherry aphid (BCA), Myzus cerasi, are involved in mutualistic relationships with ants [9,10,11]. Aphids, as important honeydew producers, derive several benefits from mutualism with ants, including increased protection against natural enemies, while ants benefit from obtaining sugar-rich honeydew excreted by aphids [10]. The nature of seasonal interactions between ants tending aphids and natural enemies is a vital element of biological control. The aphid farming–protection behavior of ants affects the performance of natural enemies by reducing their successful attack rates on aphid colonies [10].
Understanding the factors that shape insect communities is an essential step for selecting appropriate plant candidates that could promote biological control in the farming system. Among these factors, the role of natural enemy-mediated indirect interaction among herbivore species in structuring insect communities has been well investigated [4,12,13,14,15]. Theoretical analysis suggests that the effects of indirect interactions between herbivore species through shared natural enemies on pest control can vary from beneficial to detrimental [16,17]. Positive impacts occur when alternative prey increases the population of natural enemies and the associated functional control services against the target herbivore [18]. Conversely, negative impacts can arise when alternative prey reduce the population of natural enemies and subsequently lower the attack rates on the target herbivore due to preference or avoidance behaviors. However, empirical studies that support these kinds of quantitative network-based predictions are very limited [2,5].
Developing eco-friendly and sustainable pest management practices in agriculture requires a deep understanding of the interactions between pests, alternative prey, associated ants, and natural enemies within multiple interaction systems. In this context, studying quantitative natural enemy overlap diagrams can help in providing such knowledge by exploring the key mechanisms that indirectly influence the population dynamics of the insect community in a particular agrosystem. Like other insect communities, aphids and their natural enemies experience strong seasonal variation in their biotic and abiotic environments. Thus, an analysis of seasonal abundances is needed to understand how target insects interact during the season. The role of indirect effects in structuring insect community is still a controversial point. It has been reported that indirect effects mediated by biotic and abiotic factors can be more important than direct effects in influencing community structure [19,20,21,22]. However, it remains unclear how to include indirect effects into predictions of community responses to landscape changes.
In Europe, several beneficial guilds (predators, parasitoids, and pathogens) have been recorded in aphid colonies from apple and cherry orchards [23,24,25,26]. To date, enhancing natural enemies in fruit orchards relies on the intercropping system with herbaceous plants [27] and establishing strips of flowering plants combined with naturally grown weeds. Many studies have investigated the potential of (wild-) flower strips within habitat management strategies in agroecosystems to enhance the conservation of natural enemies and related functional services [28,29]. To our knowledge, only a few studies have evaluated the potential of woody plants to enhance the biological control of aphids in fruit orchards [30]. Selecting appropriate insectary plants for a given pest depends on their functional services in enhancing the efficiency of natural enemies on the target crop [29].
The aphids RAA and GAA are considered among the serious pests of apples, particularly in the organic farming system, causing significant plant damage [23,31,32]. In particular, RAA can cause yield reductions, reported from 30% [33] to 80% [34]. Enhancing biological control of these aphids is a major challenge due to the strong mutualistic interaction with ants. Thus, the candidate plants should not only provide alternative food, but also being able to modify the behavior of attending ants on apple trees [35,36]. A central question addressed here was how will aphid-based food webs change as their environment is modified? In the present study, we aimed to answer the following questions: (1) To what extent does the natural enemy community overlap among the studied aphid species? (2) To what extent does the empirical data support the quantitative food web which emerged from the theoretical prediction? (3) Are cherries infested with black cherry aphids able to improve the biological control of apple aphids?

2. Materials and Methods

2.1. Unconnected Patches

2.1.1. Study Site

The experimental orchards were organic apple and cherry orchards (50°46′21.9″ N 5°09′35.6″ E) located near the city of Sint-Truiden, Limburg province, eastern Belgium. This agricultural region has a temperate climate and a long history of fruit culture. Respectively, three and five cherry and apple orchards, each with trees that are more than 10 years old, were selected based on their availability. The distances between orchards of the same fruit crop ranged from 1 to 10 km. The size of studied orchards ranged from approximately 0.5 to 1 ha.

2.1.2. Population Dynamic

In 2015, from 20 April to 6 July, once a week, 20 trees per orchard and 2 shoots (one-year-old growths) per tree were randomly selected and scanned for target organisms. On each selected shoot, aphid populations on the ten apical leaves per selected shoot were quantified using six infestation categories, A = no aphids, B = 1–10 aphids, C = 11–50 aphids, D = 51–100 aphids, E = 101–200 aphids, F = more than 200 aphids. Concerning the natural enemies, the functional stages of target predators and parasitoids observed on the selected shoots were counted. Parasitoid mummies detected on each shoot were sampled and transported to the laboratory for morphological identification of the emerged adults using current identification keys [37,38,39,40]. Presence and absence parameters were used in the qualitative assessments of aphid-tending ants.

2.2. Connected Patches: Intercropping Experiment

2.2.1. Experimental Design

In 2016, the study was carried out in an organic apple orchard of the fruit research station (pcfruit). In this experiment, the potential of cherry trees to enhance apple aphid biocontrol was evaluated using the Topaz cultivar (6-years-old trees), which is highly vulnerable to aphid infestation and was grown in a 1-ha orchard. In this orchard, a plot of 5 rows, ≈88 m long, was selected for executing the intercropping experiment. The plot was split into 4 equal blocks, with each block comprising of 5 rows and 20 apple trees, along with 1 cherry tree in each row. In March 2016, 20 young trees (3-years old) of sweet cherry P. avium (Skeena cultivar) with similar size of ≈100 cm were planted in the intercropping plot. The distance between apple trees was 1 m, while the distance between each two rows was 3.5 m. A cherry-free apple plot of a similar size and blocks was chosen at a distance of 60 m from the intercropping plot and served as the control. All cherry trees in the study were free of aphid eggs; thus, we artificially infested them with BCA during the second week of April when the cherry trees were in the phenological stage BBCH 56 (open cluster). Each tree was infested with a total of 20 mixed-age individuals consisting of adults and old instars of nymphs, with each tree bud receiving five individuals (one adult and four nymphs). For infesting the study trees, we used BCA cherry aphids that were reared under greenhouse conditions on cherry seedlings.

2.2.2. Sampling

From 20 April to 6 July, we conducted weekly visual counts of aphids, associated ants, and natural enemies (functional stages of target predators and parasitoid mummies) on cherry trees and on 20 randomly selected apple trees per plot, with 5 trees per block and 2 shoots per tree. We used the same scores mentioned above in the field monitoring study to quantify aphid populations. Concerning ant populations, the present individuals observed within one minute on the selected shoots were quantified using the following scale, A = no ants, B = 1–5 ants, C = 6–10 ants, and D = >10 ants. Parasitoid mummies recorded on the selected shoots were sampled weekly and maintained in a condition-controlled room at 20 ± 1 °C, a photoperiod of 16 h:8 h (L:D), and 60% ± 5% relative humidity until the adult emergence. All emerged parasitoids were identified to species level using current identification keys (references as cited above in Section 2.1.2), while predators were identified to family level. The damage (curled leaves) caused by apple aphids was evaluated weekly on the ten apical leaves of selected shoots using three damages categories: healthy = no curled leaves, DA ≤ 50% curled leaves, DB > 50% curled leaves). The curled leaves per shoot (one-year-old growths) were counted and then the percentage of damaged leaves per shoot was calculated.

2.3. Data Analysis

2.3.1. Food Web

Pooled data of aphids and their natural enemies were used in the construction of all quantitative food webs and overlap diagrams. Host-natural enemy matrices were created to draw quantitative food web graphs and to assess the strength of direct and indirect interactions following Müller et al. [12], using the bipartite package implemented in Mathematica 5.0. Three quantitative indices were calculated: (i) the effective prey/host range per natural enemy; (ii) the effective natural enemy range per aphid species; and (iii) the potential trophic link strength among target species. Thus, for each studied aphid species, the overall and seasonal potential apparent competition index was calculated. Seasonal analysis included the abundance data collected during two periods, first from 20 April to 31 May, and second from 1 June to 6 July. Based on the number of natural enemies connecting aphid species, this index ranges from 0 (no sharing of natural enemies) to 1 (highest sharing of natural enemies), representing the fraction of natural enemies shared between aphid species. The width of the link at aphid species A, for example, is a measure of the importance of linked aphid species B as a source of natural enemies that feed on species A. The asymmetric connecting link suggests that one species has a strong effect on another but not vice versa. The strength calculation of apparent competition, quantitative food webs, and overlap diagrams were performed in Mathematica 5.0 [41].

2.3.2. Statistical Analyses

The collected data of target organisms were pooled per week, and then the data were compared between cherry-intercropped apples and control apples. The effects of the intercropped system on the population dynamic of aphids (mean numbers), ants, and natural enemies (total numbers) were evaluated using the chi-square goodness-of-fit test for each sample date. Relationships between aphids, associated leaf damages, ants, and their natural enemies (NE) were worked out by Pearson’s correlation analysis and principal component analysis (PCA) using XLSTAT 2016 and the ggplot2 package in R [42]. Leaf damage across sampling time data was subjected to analysis of variance (ANOVA) using a generalized linear model (GLM) to determine the significance (p ≤ 0.05) of differences between intercropped and control apples. Data were subjected to variance homogeneity analysis (Levene’s test) when needed, and if p ≤ 0.05, a data transformation procedure was applied. ANOVA analyses and chi-square goodness-of-fit test were performed in Minitab 18 software.

3. Results

3.1. Unconnected Patches

3.1.1. Population Dynamic

First, nymphs (natural population) of all target aphids were observed on apple and cherry trees since the first week of April 2015. Cherry aphids (BCA) started clearly increasing since the first week of May and reached their peak during the first week of May. One week later, both apple aphids RAA and GAA reached their peak on apple trees. The populations of natural enemies associated with these aphids exhibited to a large extent a similar trend of occurrence (Figure 1). In total, we recorded 224 parasitoids belonging to 9 species of Braconidae and 348 predatory individuals belonging to 6 predatory families (Cecidomyiidae, Forficulidae, Syrphidae, Chrysopidae, Coccinellidae, Anthocoridae). All parasitoids and potentially all predator species found on BCA colonies have been also observed on apple aphids (Figure 2). Among parasitoids, Ephedrus persicae (code 5) was the main species on RAA and BCA, while Binodoxys angelicae (code 4 see Table 1) was the predominant species on GAA. The parasitoid Ephedrus plagiator (code 6, see Table 1) was the third important parasitoid, with almost symmetrical occurrence on all target aphids. In the predator community, the Cecidomyiidae and Syrphidae were the most abundant. Concerning the ant population, only one species, Lasius niger, was found associated with the studied aphids. The ants were active early in the season before aphid appearance, and the highest activity of ants in aphid colonies was observed in June. In addition to transferring aphids to enemy-free leaves, aggressive behaviors of ants against natural enemies, ranging from excluding to devouring, were frequently observed on cherry and apple aphid colonies.

3.1.2. Species Interactions

A summary quantitative food web was constructed describing the whole community structure using the aphid, parasitoid, and predator abundances (Figure 2, left panel). Lower bars represent the aphids, and the top bars represent the natural enemies; the width of each bar is proportional to total abundance of the given species. Natural enemies and aphids are linked by triangular links. For each aphid species, the width of each link denotes the relative abundance of beneficial species compared to other natural enemies of that aphid. A quantitative natural enemy overlap diagram, representing the strength (link width) of apparent competition between target aphids, is shown in Figure 2 (right panel). At each vertex, the white disc size is proportional to the number of natural enemies observed on that aphid species, and black disc size denotes the proportion of natural enemies from which they recruit, potentially developing on the same aphid species. The quantitative overlap diagram (Figure 2) constructed on the basis of total data shows two patterns of natural enemy mediated-indirect effects between BCA and apple aphids: symmetric effect between BCA and RAA (dRAA,BCA = 0.37, dBCA,RAA = 0.36), and asymmetric effect between BCA and GAA (dGAA,BCA = 0.36, dBCA,GAA = 0.16).

3.2. Connected Patches: Intercropping Experiment

3.2.1. Population Dynamic

In this experiment, the population of cherry aphids and their natural enemies reached first peak levels before the remarkable increase in the population of apple aphids which was registered during the last week of May 2016 (Figure 1). The annual average number of aphid individuals per week registered on intercropped apple shoots was significantly lower than on control shoots (apple parcels without cherry intercropping) (χ2 = 268.245, DF = 1, p < 0.001). Significantly higher natural enemies were recorded on aphid colonies infesting intercropped apple shoots compared to control shoots (χ2 = 9.762, DF = 1, p = 0.002). There was no correlation between the seasonal abundances of BCA infesting the intercropped cherries and natural enemies observed on either apple or cherry trees. A summary of data correlation patterns between target organisms, including the aphid-associated leaf damage recorded in intercropped and control apple parcels, is presented in Figure 3. However, the principal component analysis (PCA) applied on the cumulative abundances showed a positive correlation between natural enemies and aphids infesting intercropped apple trees. The PCA applied on the whole dataset of the intercropping trial clearly showed the variation patterns in the abundances of aphids, ants, and natural enemies recorded on intercropped cherries and apples compared to control apples (Figure 4). Higher numbers of ants associating with aphid colonies were observed in control apples compared to intercropped ones (χ2 = 14.617, DF = 1, p < 0.001).
Statistical analysis of seasonally cumulative responses of apple leaves to aphid infestation is shown in Figure 5. Overall, there were no significant differences between intercropped and control apples concerning their leaf responses to aphid infestation. To evaluate seasonal leaf damage, the data of curled leaves collected in different time periods (early season from 20 April to 31 May, and late season from 1 June to 6 July) were analyzed separately. Aphid-infested trees exhibited different responses to aphid feeding during the second period. Statistically, apple aphids generated significantly more leaf damage on the control apples but only during the second period of the season (damage A: F1,8 = 5.94, p = 0.041; damage B: F1,8 = 21.48, p = 0.002). Moreover, during same period, there were significantly more healthy leaves (non-curled) found on the cherry-intercropped apples (F1,8 = 8.90, p = 0.018).

3.2.2. Species Interactions

In total, 953 beneficial individuals belonging to 6 families of parasitic wasps (Hymenoptera: Braconidae) and 5 predatory insect groups (Cecidomyiidae, Forficulidae, Syrphidae, Coccinellidae, Anthocoridae) were observed in aphid colonies (Figure 6). Among the parasitoids, E. persicae (82.86%) followed by B. angelica (8.05%) and E. plagiator (7.53%) were the most abundant species on the studied aphids, while no mummies were found in GAA colonies infesting control apple trees. Overall, we observed significantly more parasitoid mummies in aphid colonies associated with intercropped apples compared to control ones (χ2 = 111.964, DF = 1, p < 0.001). Among the predators, Cecidomyiidae, Syrphidae, and Coccinellidae were the most abundant (Figure 6). Statistically, there were significantly higher numbers of predators on aphid colonies infesting intercropped apples compared to control ones (χ2 = 26.667, DF = 1, p < 0.001).
In the seasonal overlap diagram (Figure 7) for the first period, most predators and parasitoids attacking aphid species on the intercropped apples tended to have developed on the BCA population infesting cherry trees (for GAA, dGAA,BCA = 0.890; for RAA, dRAA,BCA = 0.812). For the subsequent period, lower indirect effects of BCA mediated by natural enemies on apple aphids were found (for GAA, dGAA,BCA = 0.432; for RAA, dRAA,BCA = 0.456). Overall, the quantitative overlap diagram constructed from the whole data (Figure 7) showed only an asymmetric pattern of natural enemy-mediated indirect effects either between BCA and RAA (0.592 and 0.305, respectively), or between BAC and GAA (0.570 and 0.061, respectively). In contrast with apple aphids, especially GAA, dBCA,BCA = 0.087, and less for RAA, dRAA,RAA = 0.337, most of natural enemies found on BCA colonies have likely developed been on same the aphid (dBCA,BCA = 0.633).

4. Discussion

We have shown in the intercropping experiment that the fate of an important population proportion of apple aphids (RAA and GAA) on apple trees depends, to a large extent, on whether it develops adjacent to populations of cherry aphids (BCA) with which it never directly competes, but with which it shares natural enemies. The number of beneficial species recorded on apple trees varied between years but remained relatively constant in cherry trees despite the difference in weather conditions, landscape structure, and cultivars. Many factors, such as size/scale of habitat and weather conditions, can contribute to the between-year variation of insect diversity, and these have long been studied [4,43,44]. The present study provides new insights into the functional relationship between apple trees and insect communities after the introduction of aphid-infested cherry trees. Thus, our field study supported the idea that combining insectary plants with cropping plants may have the potential to improve crop protection via the enhancing of pest biocontrol and the reducing of leaf damage. Previous studies have reported that woody plants provide important services (nectar, pollen, alternative prey, shelter, etc.) for beneficial organisms [15,26,30,45,46]. To our knowledge, the strategy investigated in our work was the first attempt to evaluate the potential role of fruit trees as insectary plant candidates for aphid control in apple orchards. The target pests in our study were aphids that start causing damage from the early phenological stages of apple trees. Therefore, candidate plants should be able to provide pest control services early in the growing season. An early establishment of insectary plants in the agroecosystems will provide important functional services by increasing the buildup of the first generation of natural enemies which lead, therefore, to enhanced pest control [47]. BCA aphids were previously observed to start their activity early in the season on cherry trees [24,48] which could potentially provide early functional services for aphid control in apple orchards via the early buildup of beneficial populations.
We constructed and described quantitative food webs of a community structure, including three aphids linked with several parasitoid and predator species. The present field experiment provided evidence that cherry trees promote aphidophagous insects, and they likely contribute to the regulation of aphid populations in apple orchards via their shared natural enemies. All common predators (except for Anthocoridae) and parasitoids observed on cherry trees have been found in higher densities on intercropped apples compared to control apples. In other words, BCA-infested cherry trees have likely supplied the apple orchard with extra numbers of parasitoids and predators, especially E. persicae, E. plagiator, Cecidomyiidae, and Syrphidae. Moreover, cherry trees likely played another important role, one represented by reduced numbers of ants associating with aphid colonies on the intercropped apples. However, predators tend to be more important than parasitoids for apple aphid control, possibly because the parasitoids themselves are highly vulnerable to the attack of hyperparasitoids [49] and often devoured by aphid predators [50,51,52].
Indirect competition between aphids can be driven by an array of interactions with different organisms such as natural enemies and ants. Ants have been shown to display preferences between aphid species for several reasons such as honeydew quantity and quality [53,54]. The coexistence of ant-attending BCA was probably one of reasons explaining the reduced number of ants on aphid colonies infesting intercropped apples compared to those observed on control trees. This situation may have helped natural enemies to increase their performance on apple aphids. Harmon and Andow [55] reported in their study that aphids were more subjected to the attack of natural enemies when only few attended ants were present.
In the case of aphids, cherry aphid BCA and apple aphids RAA and GAA cannot compete directly because they feed on different host plants. In the present study, quantitative food web analysis showed that cherry aphids have been subjected to the attack by parasitoid species and predator species, which have all been observed on apple aphid colonies. However, the potential for sharing beneficial populations between target aphids is likely to be larger early in the season, represented by the high values of apparent competition indices (asymmetric apparent competition) compared to the situation observed from the beginning of 1 June to 6 July 2016. The early intense activity of BCA may support our hypothesis that BCA is an important source of the natural enemies of apple aphids, as demonstrated in the intercropping experiment. To our knowledge, our results are the first empirical evaluation of the indirect effects of the BCA population in structuring the apple aphid population mediated by natural enemies and associated ants. In agroecosystems, the perennial host plants, such as cherries, could have the potential, in time, to increase the strength of natural enemy-mediated apparent competition among insect herbivore communities, potentially leading to enhanced pest biocontrol [56]. Thus, our results reported here support the hypothesis that indirect effects between primary consumers mediated by secondary consumers may be an important element in structuring particular insect communities.
Generally, it is widely believed that pest aphid control can be enhanced if properly selected insectary plants are grown nearby where they can act as an additional source of natural enemies [1,4,57]. The interaction patterns detected in this study between aphids, ants, and natural enemies in different habitats deserve to be investigated in further research on improving the functional control services provided by the insectary plant candidate(s). Such knowledge could reduce chemical applications when natural enemies are well present and well managed, and finally provide healthy products for the end-consumers.

Author Contributions

Conceptualization, A.A., T.B. and D.B.; methodology, A.A.; software, A.A.; validation, A.A., T.B. and D.B.; formal analysis, A.A.; investigation, A.A.; resources, T.B. and D.B.; data curation, A.A.; writing—original draft preparation, A.A.; writing—review and editing, A.A., T.B. and D.B.; visualization, A.A.; supervision, T.B. and D.B.; project administration, T.B. and D.B.; funding acquisition, A.A., T.B. and D.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the European Union, EU-BIOCOMES project 2013-2017, with grant Agreement number: 612713.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data generated or analyzed during this study are included in this article.

Acknowledgments

We thank the growers who allowed us to work in their orchards. We are grateful to the technical team of the Zoology department and the research station for fruit (pcfruit npo) for their help in the technical part of this research and for maintaining the experimental plots.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Seasonal abundance (Mn = mean numbers per shoot) of aphids and their natural enemies (predators and parasitoids) recorded in the field study carried out in 2015 and in the cherry-apple intercrop experiment carried out in 2016. Dark red and green denote, respectively, the abundances of aphids and natural enemies in apples; while light red and green indicate the corresponding abundances in cherries.
Figure 1. Seasonal abundance (Mn = mean numbers per shoot) of aphids and their natural enemies (predators and parasitoids) recorded in the field study carried out in 2015 and in the cherry-apple intercrop experiment carried out in 2016. Dark red and green denote, respectively, the abundances of aphids and natural enemies in apples; while light red and green indicate the corresponding abundances in cherries.
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Figure 2. Summary quantitative food web (left) and overlap diagram (right) constructed using data pooled from the whole study of field monitoring conducted in 2015. In the food web (left), host aphids (bottom) and natural enemies (top) are represented by orange (parasitoids) and green bars (predators), of which the length shows relative abundance. Between top and bottom bars, width of links shows the relative abundance of a particular natural enemy species/family connected with each aphid species. The code numbers for natural enemies are presented in Table 1. In the overlap diagram (right), the width of the line connecting two aphid species is a measure of the importance of connected aphid species as a source of natural enemies that feed on them. For each aphid species, the diameter of the white circle is proportional to the number of natural enemies (predators and parasitoids) observed on that aphid species, and the diameter of the black circle (dii) is proportional to the number of natural enemies potentially developing on the same aphid species from which they recruit.
Figure 2. Summary quantitative food web (left) and overlap diagram (right) constructed using data pooled from the whole study of field monitoring conducted in 2015. In the food web (left), host aphids (bottom) and natural enemies (top) are represented by orange (parasitoids) and green bars (predators), of which the length shows relative abundance. Between top and bottom bars, width of links shows the relative abundance of a particular natural enemy species/family connected with each aphid species. The code numbers for natural enemies are presented in Table 1. In the overlap diagram (right), the width of the line connecting two aphid species is a measure of the importance of connected aphid species as a source of natural enemies that feed on them. For each aphid species, the diameter of the white circle is proportional to the number of natural enemies (predators and parasitoids) observed on that aphid species, and the diameter of the black circle (dii) is proportional to the number of natural enemies potentially developing on the same aphid species from which they recruit.
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Figure 3. Correlation plot showing correlation patterns between the abundance of different target insects recorded on apples and cherries, and the leaf damage measurements (percentage averages per week, healthy = no curled leaves, DA = <50% curled leaves, DB = >50% curled leaves) conducted on intercropped and control apple trees. The correlogram shows correlation coefficients for all pairs of variables. The color legend on the right side for each correlogram shows the correlation coefficients (−1, 1) and the corresponding colors (red, blue). When the correlations were not significantly different, they are colored white.
Figure 3. Correlation plot showing correlation patterns between the abundance of different target insects recorded on apples and cherries, and the leaf damage measurements (percentage averages per week, healthy = no curled leaves, DA = <50% curled leaves, DB = >50% curled leaves) conducted on intercropped and control apple trees. The correlogram shows correlation coefficients for all pairs of variables. The color legend on the right side for each correlogram shows the correlation coefficients (−1, 1) and the corresponding colors (red, blue). When the correlations were not significantly different, they are colored white.
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Figure 4. Principal component analysis (PCA) based on the population interaction of aphids, ants, and natural enemies observed on intercropped (in) and control (C) trees.
Figure 4. Principal component analysis (PCA) based on the population interaction of aphids, ants, and natural enemies observed on intercropped (in) and control (C) trees.
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Figure 5. Percentage of seasonal leaf damage (± SD) recorded on intercropped and control apples on the early (from 20 April to 31 May) and late (from 1st June to 6th July) season 2016 (GLM at p ≤ 0.05, * p ≤ 0.05, ** p ≤ 0.01). DAc and DAin = <50% curled leaves in the control (c) and intercropping (in) plots, DBc and DBin = >50% curled leaves, Hc and Hin = healthy (no curled leaves), D-A = <50% curled leaves. The data that deviated significantly from the rest of the dataset are represented by hollow circles (also known as outliers) plotted outside the whiskers on the plot.
Figure 5. Percentage of seasonal leaf damage (± SD) recorded on intercropped and control apples on the early (from 20 April to 31 May) and late (from 1st June to 6th July) season 2016 (GLM at p ≤ 0.05, * p ≤ 0.05, ** p ≤ 0.01). DAc and DAin = <50% curled leaves in the control (c) and intercropping (in) plots, DBc and DBin = >50% curled leaves, Hc and Hin = healthy (no curled leaves), D-A = <50% curled leaves. The data that deviated significantly from the rest of the dataset are represented by hollow circles (also known as outliers) plotted outside the whiskers on the plot.
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Figure 6. Summary quantitative food web of whole data collected from the intercropping (in) experiment, including control apples (C), carried out in 2016. The web was constructed as in Figure 2, and same arrangement of natural enemies is retained.
Figure 6. Summary quantitative food web of whole data collected from the intercropping (in) experiment, including control apples (C), carried out in 2016. The web was constructed as in Figure 2, and same arrangement of natural enemies is retained.
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Figure 7. Natural enemy quantitative overlap diagrams for the intercropping and control apples in addition to intercropped cherries. These figures show the potential for seasonal and overall apparent competition between study aphid species via the common natural enemies observed in study trees in 2016. The diagrams were constructed as in Figure 2.
Figure 7. Natural enemy quantitative overlap diagrams for the intercropping and control apples in addition to intercropped cherries. These figures show the potential for seasonal and overall apparent competition between study aphid species via the common natural enemies observed in study trees in 2016. The diagrams were constructed as in Figure 2.
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Table
Table 1. Identity of species (parasitoids) or families (predators) in the food webs.
Table 1. Identity of species (parasitoids) or families (predators) in the food webs.
Natural Enemies (Code)
Parasitoids
Aphidius ervi (1), A. matricariae (2), A. urticae (3), Binodoxys angelicae (4), Ephedrus persicae (5), E. plagiator (6), Lipolexis gracilis (7), Praon abjectum (8), Toxares deltiger (9).		Predators
Cecidomyiidae (10), Forficulidae (11), Syrphidae (12), Chrysopidae (13), Coccinellidae (14), Anthocoridae (15).
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Alhmedi, A.; Belien, T.; Bylemans, D. Habitat Modification Alters Food Web Interactions with Focus on Biological Control of Aphids in Apple Orchards. Sustainability 2023, 15, 5978. https://doi.org/10.3390/su15075978

AMA Style

Alhmedi A, Belien T, Bylemans D. Habitat Modification Alters Food Web Interactions with Focus on Biological Control of Aphids in Apple Orchards. Sustainability. 2023; 15(7):5978. https://doi.org/10.3390/su15075978

Chicago/Turabian Style

Alhmedi, Ammar, Tim Belien, and Dany Bylemans. 2023. "Habitat Modification Alters Food Web Interactions with Focus on Biological Control of Aphids in Apple Orchards" Sustainability 15, no. 7: 5978. https://doi.org/10.3390/su15075978

APA Style

Alhmedi, A., Belien, T., & Bylemans, D. (2023). Habitat Modification Alters Food Web Interactions with Focus on Biological Control of Aphids in Apple Orchards. Sustainability, 15(7), 5978. https://doi.org/10.3390/su15075978

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