Agricultural intensification affects communities of plants and arthropods in field borders and their potential to engender biological control

doi:10.21203/rs.3.rs-4329817/v1

In agriculture, spontaneous field border vegetation can engender several benefits, including mitigating soil erosion, increasing carbon retention, conserving pollinators, and promoting biological control. The extension of these benefits can, however, often depend on the context of location and time. As for biological control, field borders can promote natural enemy conservation if the plants therein can provide adequate resources (e.g. shelter, alternative food, microclimate). In the context of location, field borders can be adjacent to areas with varying degrees of agricultural intensification, including fields with annual crops, perennial crops, or forest areas. While many studies have investigated how field borders can influence arthropod communities in adjacent crops, the opposite direction of effect (i.e. how crop areas can influence adjacent field borders) remains an underexplored topic. Therefore, in this three-season study we selected vegetated field borders next to annual crops, perennial crops, and forest areas, to study their communities of spontaneous plants (weeds) and arthropods as well as their potential to engender biological control. In general, our results show that the community composition of plants and arthropods was affected by land use type and season. Furthermore, field border vegetation next to areas with higher level of agricultural intensification (i.e. annual or perennial crops) harbored more herbivores, flowers and natural enemies; although some of these results were season dependent. Lastly, field borders next to annual or perennial crop areas engendered stronger biological control of aphids; possibly due to the alternative food (herbivores/aphids and flowers) provided by the plants therein. Taken altogether, our results reinforce the importance of preserving spontaneous field border vegetation, especially in areas under intensive agriculture management.

field margin

weeds

conservation biological control

habitat manipulation

banker plants

aphids

Field borders (AKA field margins) are often left uncultivated by farmers, thereby engendering places for spontaneous growth of vegetation and consequent sheltering of invertebrates and small-vertebrates (Marshall and Moonen 2002; Aschwanden et al. 2007; Anderson et al. 2013; Mkenda et al. 2019a; Obanyi et al. 2023). Nevertheless, the formation of these vegetational segments at the borders is seldom intentional, and more often it is actually due to the challenges of maneuvering properly the agricultural machinery close to those borders (especially when close to fenced borders). While some farmers may worry about losing farming space for spontaneous vegetation at the borders, many others already acknowledge the potential benefits of these vegetated borders to mitigate soil erosion, increase carbon sequestration, conserve pollinators, and promote sustainable pest management (Balzan and Moonen 2014; D’Acunto et al. 2014; Mkenda et al. 2019ab; Crowther et al. 2023; Aviron et al. 2023). In the context of pest management, several studies have indicated that the border vegetation can promote biological control of pests by conserving natural enemies in the field (Amaral et al. 2013; Bischoff et al. 2016). Specifically, the spontaneous border vegetation can provide natural enemies with resources such as shelter, alternative/complementary food, microclimate, hibernation/aestivation habitat and protection from pesticide sprays (Landis et al. 2000; Tscharntke et al. 2007; Rusch et al. 2010; Gontijo 2019). The presence of spontaneous border vegetation might be particularly relevant in fields containing annual crops where continuous cycles of planting and harvesting (i.e. high disturbance) create a constant necessity for natural enemy protection and recolonization (Wissinger 1995). Nevertheless, despite the potential benefits of border vegetation for pest management, farmers and researchers need some caution as some plant species occurring at the borders might at certain times still favor specific arthropod pests (Bianchi et al. 2006).

It is known that the intensification of land use can have detrimental effects on the diversity of plants and animals, which can significantly impair the functioning of ecosystems (Benton et al. 2003). Such intensification of land use is often done in order to increase agricultural production by means of converting natural and/or semi-natural habitats into arable fields. This intensification of agriculture is also additionally associated with the application of external fossil and agrochemical inputs, which further cause impairments of ecological functions (e.g. pest control, nutrient cycling, crop pollination) (Tscharntke et al. 2005; Rusch et al. 2016). In the context of pest control, various studies have indicated that landscape degradation and simplification caused by agricultural intensification can have negative effects on ecosystem services such as biological control (Thies et al. 2011; Rusch et al. 2016). For example, the destruction of field borders (e.g. hedgerows) contributes to loss of semi-natural habitat and to the further simplification of agricultural landscapes, which can engender a scarcity of food and shelter resources for natural enemies (Robinson and Sutherland 2002; McHugh et al. 2020). Furthermore, in addition to affecting plant and animal diversity, agricultural intensification may as well influence their trophic interactions prompting broader implications for ecosystem functioning (Jonsson et al. 2012; Zhao et al. 2015; Garrett et al. 2022).

Often, field borders with spontaneous vegetation may be adjacent to areas with varying degrees of management/disturbance (i.e. level of agricultural intensification), including areas with annual crops (very high disturbance), perennial crops (high/medium disturbance), and forest areas (low/very low disturbance). It is reasonable to expect that the intensity of land use (i.e. level of management/disturbance) may influence the composition and structure of plant and arthropod communities inhabiting those nearby field borders. While many studies have investigated how field borders can influence the arthropod communities in adjacent crop areas (Balzan and Moonen 2014; Inclán et al. 2016; Luna et al. 2016; Obanyi et al. 2023; Salat-Moltó et al. 2023), the opposite direction of effect (i.e. how crop areas can influence field borders) remains an underexplored topic. Nonetheless, it is noteworthy that these interactions are likely to be bidirectional, where field border vegetation and adjacent crop areas may influence each other. Regardless, understanding the driving forces that influence spontaneous border vegetation, and consequently the community of arthropod pests and natural enemies therein is paramount to devise effective management strategies to promote biological control of pests in the field. Therefore, in this three-season experiment we selected vegetated field borders next to areas with annual crop, perennial crop, and forest, in which we studied the community of spontaneous plants (weeds) and arthropods as well as the potential for biological control in those borders. The varying levels of agricultural intensification in this study, from the highest to the lowest, was represented by fields with annual crop, perennial crop, and forest. Our hypotheses were (i) there would be lower plant and arthropod richness in the borders adjacent to annual crop areas (i.e. higher disturbance), (ii) we would find differences in community composition of plants and arthropods in relation to border location, and (iii) there would be a lower potential for biological control in borders closer to annual crop areas.

Field experiment

The experiment was carried out multiple times (from March to November 2019) in open fields located within a landscape containing mosaics of arable lands and patches of forest (these fields were specifically situated within a radius of 3km around this geographic point: -19.874617, -44.419997). The experimental design consisted of three treatments, for which a selected field border would be next to either (i) forest area (dense natural forest), (ii) perennial crop (i.e. either coffee, guava, citrus, pear or cassava), or (iii) annual crop (i.e., either soybean, maize or wheat). These experimental treatments (i.e. border location) were chosen to depict a gradient of land use intensification, with the greatest agricultural intensification represented by fields containing annual crops (i.e. greatest disturbance) and least intensification in forest patches. At the time of data collection, all annual crops were either at the end of the vegetative stage or in the middle of the reproductive stage (i.e. no crop flowers were present during data collection). This experiment was repeated in three different seasons (i.e. summer, winter and spring) with three replicates per treatment in each season, thereby yielding a total of 27 replicates. None of the borders was repeated across seasons (i.e. in each season a new border was selected according to the treatments). During the summer, winter and spring the minimum-maximum field temperature registered were 24–36°C, 19–30°C, 22–35°C, respectively. In general, each selected border was characterized by a strip of spontaneous vegetation located at the periphery of one side of either an agricultural field (annual or perennial) or forest patch. In the particular case of forests which have very lengthy sides (i.e. edges), any clear discontinuity in border vegetation was used to help visually delineating the beginning/end of the experimental border, and thereby stablishing its length. All selected borders faced their respective treatments on one side (i.e. annual crop, perennial, or forest patch), and an uncultivated area (fallow land) on the other side (Appendix S1: Fig. S1). None of the borders were mowed or treated with pesticides during this study. Likewise, the annual or perennial crops were not sprayed with pesticides, at least ten days prior to data collection. The selected experimental borders had an approximate width of 5.40 ± 0.85m, and a length of approximately 31.20 ± 3.30m (Appendix S1: Table S1). Despite the relative variation in border width and length, we carried out a standardized number of samples (see below) expecting to capture/encompass adequately any inherent proportional difference in plant and arthropod numbers within borders.

Specifically, we measured through samplings the richness of plant species and abundance of arthropods within borders. For plant species richness, all plants within each field border were identified in situ, or collected and taken to the laboratory for further identification. The plant identification in the laboratory was carried out by using reference exsiccata and books under the guidance of a plant specialist. Nonetheless, because of the high number of plant material collected and the appearance of very rare specimens, some of them were identified just as morphospecies. Because not all plant species were identified to the species level, in this current study the terms plant species and plant specimen are interchangeable. As for arthropods, we sampled both herbivores and natural enemies by using the following methods: (i) pitfall traps: these traps consisted of a plastic cup (500 ml) filled with 200 mL of ethanol solution (70%). Three pitfall traps were individually and equidistantly buried for 48 h to the surface level within each field border in a lengthwise direction. After field exposure the traps were taken to the laboratory for identifying and counting the arthropods under stereomicroscope. Pitfall traps were chosen to sample specially epigeal predators and herbivores, which are known to commonly scan the soil surface. (ii) yellow sticky traps: three sticky traps (10 × 30cm) were set up individually and equidistantly on bamboo stakes at 0.8 m suspended from the soil surface for 48 h period within each field border following a lengthwise direction. This sampling method was used to estimate mainly the abundance of flying and apterous arthropods occurring in each field border. The arthropods collected on the sticky traps were also taken to the laboratory for count and further identification under stereomicroscope. Because of the high number of sampled arthropods to process (pitfall + stick traps), it was not possible to identify them all to species level, especially considering the parasitoids. We thus use the terms “taxa” for herbivores and predators, and ‘‘morphospecies’’ for parasitoids in this current study. This level of identification is sufficient for our objectives, since we are more interested in community patterns than the response of individual species. Moreover, we assessed the occurrence of flowers in all borders in each season. To do so, we selected three 30 x 30 cm areas distributed equidistantly lengthwise within each border and recorded the number of flowers on plants therein, regardless of plant species.

The potential for biological control engendered by borders was also investigated by using sentinel collard plants (cultivar Manteiga) infested with aphids. Therefore, weeks prior to the field experiments we cultivated collards under greenhouse conditions in plastic pots of 3L (2 plants per pot) containing regular potting soil. Potted-collards were kept inside organza cages and watered manually about 2–3 times a week until experiment. Additionally, collards were artificially infested with aphids Brevicoryne brassicae inside the cages by placing a detached small collard leaf containing aphids (from a stock colony) atop the clean plants. Infested collards with 4–6 completely expanded leaves were used as sentinel plants in the field, where each selected border had one sentinel plant on both sides (1m away from both sides of each border vegetation). The potted collards were buried to the soil surface level to simulate a realistic situation. All aphids on sentinel plants were counted and adjusted to have approximately equal initial numbers on the day of the experiment setup. Thereafter, the infested plants were allowed to stay in the field for 48 hours. Following the 48-hour field exposure the number of aphids were counted again to estimate any potential increase/reduction in aphids. Furthermore, after the 48-exposure and the aphid counts the sentinel plants were individually enclosed by organza bags, and brought to the greenhouse to later assess any potential parasitism that might have taken place in the field (i.e. to count the number of mummified aphids).

Lastly, we carried out a bibliographic search for published articles that informed which of the plant species identified at the borders would commonly host aphids, and what species those aphids belonged to. We consider this additional information to be important as some spontaneous plants in the borders might host aphids, which often can serve as alternative prey/host for natural enemies. Nonetheless, we did not sample for aphids in situ (i.e. to count visually) on the spontaneous plants at the moment of this study.

Statistical analysis

All analyses were carried out in R statistical software (Development Core Team 2021). To test for differences of the proportion of plant species overlapping among border treatments (i.e. three-border overlap, two-border overlap, zero overlap) we carried out a Pearson’s Chi-squared test through a contingency table analysis. In this analysis, we assumed that the fewer the overlaps of plant species occurring among border treatments the greater the differences in the composition of plant communities occurring in those borders.

The effects of border location, season and their interaction upon the richness of plant species inhabiting the borders were assessed by carrying out a Generalized Linear Model (GLM) analysis. Likewise, the effects of border location, season and their interaction were tested on the abundance of herbivores (all specimens combined), natural enemies (all specimens combined), aphids, thrips or whiteflies by carrying out analyses of covariance (ANCOVA) using the GLM function, in which the richness of plant species was set as the covariate. All analyses aforementioned used a poisson distribution in the models considering the counts of plant species or arthropods to follow such distribution. Thereafter, any significant effect of the border location*season interaction led to posthoc pairwise analyses using the emmeans package (Lenth 2023) to compare within date (season) treatment means in regard to the effect of border location. Lastly, we investigated the effect of border location on the abundance of flowers by carrying out a Kruskal Wallis analysis followed by Bonferroni-adjusted pairwise mean-comparisons.

To investigate whether field location and/or season could affect arthropod community structuring (i.e. composition) in the borders we carried out Non-metric Multi-dimensional Scaling (NMDS) analysis using the package vegan (Oksanen et al. 2022). The analysis was carried out individually for the communities of herbivores, predators and parasitoids. NMDS is a common way to summarize information from multidimensional data into a 2D representation or ordination. In such ordination, the closer two points are, the more similar the corresponding samples are with respect to the variables that were used to plot the NMDS graph. Furthermore, the NMDS analysis generates a ‘stress’ value, which somewhat works as the ‘goodness of fit’ of the data ordination. Specifically, any stress value smaller than 0.2 indicates a good representation of the data. Moreover, anytime the NMDS analysis engendered a stress value smaller than 0.2 we followed up with a ANOSIM test to investigate whether there was a statistical difference between the arthropod communities (i.e. composition) in regard to border location and season. The ANOSIM test examines the relative similarity of samples ‘within’ versus ‘between’ groups, which is based on the Bray-Curtis percent dissimilarity index. This analysis generates a R-statistic value, which varies from 1 (meaning all similar samples come from the same group) to -1 (meaning all similar samples come from different groups). Thus, a significant value of the R-statistic indicates that the community composition differs among borders.

To investigate the potential for biological control, we assumed that any reduction in aphid numbers assessed on sentinel plants at the end of the 48-h field exposure was due to predation, whereas any increase was most likely due to reproduction. The aphid population growth rate was used as a proxy for measuring the impact of biological control (predation + parasitism). To do so, the per capita growth rate of aphids was calculated for each border treatment from each date (season) according to the following formula (Chau et al. 2005).

$$r=\frac{\text{l}\text{n}({N}_{X+1}/ {N}_{X})}{\text{t}}$$

where N_X is the aphid population size at time x, N_X+1 the aphid population size at time x + 1, t is the difference in days between time x + 1 and x, and ln is napierian logarithm. The Nx was represented by the initial aphid counts on sentinel plants, whereas the N_X+1 was represented by the final aphid counts (at the end of 48 hours) minus the number of mummified aphids (counted later after the 48-h exposure) on the same sentinel plants. To assess the impact of biological control on aphid population growth, we subjected the per capita growth rate data to an ANCOVA analysis using the GLM function, where the plant species richness was inserted as the co-variable.

There was a significant difference (χ² = 10.53, P = 0.0324) in the proportions of plant species overlapping in the three border types, two border types, or not overlapping, during each season (Fig. 1). Nevertheless, the plant species overlap occurring among border treatments was very low in any season (i.e. most species did not overlap), suggesting differences in the composition of plant communities in relation to border location (Fig. 1). Additionally, there were a significant effects of border location and border location*season interaction on the richness of spontaneous plant species occurring in the borders (Table 1). Specifically, higher plant species richness was found in the borders next to areas of forest and annual crops during winter and spring (Fig. 2i). A total of 186 plant species/specimens were found occurring in the field borders (Appendix S1: Table S4). In general, the most common plant specimens encountered were in the Families/Genera of Asteraceae, Fabaceae, Poaceae, Ipomea, Amaranthus Desmodium, and Sida (Appendix S1: Table S4). Interestingly, most plant specimens in the Families of Asteraceae or Fabaceae were found almost exclusively in borders next to forest areas, whereas plants in the Poaceae Family were mostly found in borders next to perennial crop areas (Appendix S1: Table S4). From our plant identification, the most common Genera of spontaneous plants known from the literature to harbor aphids were Amaranthus, Baccharis, Bidens, Brachiaria, Chamaesyce, Commelina, Copaifera, Desmodium, Eleusine, Emilia, Lantana, Sida, Siparuna, Solanum, Vernonia, Veronica and Zanthoxylum (Appendix S1: Table S4). Although these plants can harbor a variety of aphid species, the most commonly identified aphid species to occur on those plants according to the literature is Aphis gossypii Glover (Appendix S1. Table S1). Lastly, a higher abundance of flowers in general was found on plants occurring in borders next to annual or perennial crop areas (Fig. 2).

Table 1

Results of statistical analyses concerning the effects of the factors (i) border location (annual crop, perennial crop or forest area), (ii) season (summer, winter, spring), and covariable (iii) plant richness on several response variables.
Response Variables	Effect	Chisq.	P-value
Plant species richness	location	11.18	0.0037
	season	4.35	0.1141
	location*season	10.36	0.0348
Abundance of all herbivores	location	2462.75	< 0.0001
	season	568.56	< 0.0001
	location*season	412.30	< 0.0001
	plant richness†	123.22	< 0.0001
Abundance of all natural enemies	location	152.08	< 0.0001
	season	228.26	< 0.0001
	location*season	280.18	< 0.0001
	plant richness†	106.08	< 0.0001
Abundance of aphids	location	208.45	< 0.0001
	season	45.69	< 0.0001
	location*season	0.70	0.7004
	plant richness†	0.06	0.8096
Abundance of thrips	location	555.26	< 0.0001
	season	282.32	< 0.0001
	location*season	337.62	< 0.0001
	plant richness†	192.40	< 0.0001
Abundance of whiteflies	location	353.75	< 0.0001
	season	578.45	< 0.0001
	location*season	348.98	< 0.0001
	plant richness†	42.63	< 0.0001
Growth rate of aphids (r)	location	5.81	0.0540
	season	3.83	0.1469
	location*season	3.67	0.4515
	plant richness†	0.24	0.6215
Number of flowers	location	8.17	0.0167
†co-variable for the GLM/ANCOVA analysis

The general abundance of herbivores and natural enemies was significantly influenced by all variables (border location, season, border location*season interaction) and co-variable (plant richness) (Table 1). Likewise, all key herbivorous pests (thrips and whiteflies) were also affected significantly by all variables and co-variable, with the exception of aphids which were influenced significantly only by border location and season (Table 1). The abundance of either all herbivores together or aphids alone was significantly higher in field borders next to annual crop areas (Fig. 3ii, Appendix S1: Figs.S2i), whereas the abundance of thrips or whiteflies was more season dependent (Appendix S1: Figs. S2ii and S2iii). Nonetheless, during the summer, the abundance of thrips and whiteflies was also higher in borders next to annual crop areas (Figs. 2ii and 2iii). Additionally, the abundance of aphids alone was also higher in field borders next to perennial crop areas when compared to those next to forest areas (Appendix S1: Fig. S2i). Because aphids were squished and tangled up on the sticky traps it was not possible to safely identify them to Genus/Species level. Some other relatively common general herbivores encountered in the borders were leafhoppers, leaf beetles, dipterans, orthopterans and stink bugs (Appendix S1: Table S2). In regard to natural enemies, the most common predators found were long-legged flies, spiders, rove beetles and wasps (Appendix S1: Table S3). In general, the abundance of predators and parasitoid morphospecies occurring in the borders next to either forest or perennial crop areas was more season dependent, whereas their abundance in the borders next to annual crop areas tended to be high in all seasons (Appendix S1: Table S3).

The Non-metric Multi-dimensional Scaling (NMDS) analyses revealed significant differences in community composition/structuring for the functional groups of herbivores, predators and parasitoids in relation to border location and/or season (Appendix S1: Figs. S3, S4, S5). All NMDS analyses (i.e. for herbivores, predators and parasitoids) produced stress values smaller than 0.2, suggesting a good fit of the data ordination for testing the community structuring. Additionally, the ANOSIM test indicated that both variables border location and season influenced the differences in parasitoid or herbivore communities, whereas for predators only the variable season contributed to differences in community composition (Table 2).

Table 2

Results of ANOSIM test from investigating the effects of border location (annual crop, perennial crop or forest area) and season (summer, winter, spring) on the community composition of arthropods (predators, herbivores, or parasitoids).
Response Variables	Effect	R*	P-value
Predator community composition	location	0.0082	0.3751
	season	0.3000	< 0.001
Herbivore community composition	location	0.2400	0.0027
	season	0.2912	< 0.001
Parasitoid community composition	location	0.3200	< 0.001
	season	0.1100	0.0343
* R-statistic value varies from 1 (meaning all similar samples come from the same group) to -1 (meaning all similar samples come from different groups). A significant value of the R-statistic indicates that the community composition is affected by the corresponding factor (i.e. location or season).

As for the potential of biological control, the ANCOVA analysis showed that only the border location variable affected significantly the aphid per capita growth rate on sentinel plants (Table 1). Specifically, the growth rate of aphids tended to be more negatively affected in the borders next to perennial or annual crop areas (Fig. 4), suggesting a higher potential for aphid biological control being engendered by borders next to arable fields.

Mitigating agricultural intensification has become a vital effort to preserve important ecosystem services as well as to promote food security and healthy environments. In this context, great efforts are underway around the globe to reduce the negative impact of pesticides, which has been one of the main villains of agricultural intensification. At the frontline of this endeavor we have habitat manipulation as a valuable approach to incentivize the natural biological control of pests. In this sense, spontaneous vegetation (i.e. weeds) in field borders have shown the potential to contribute with natural enemy conservation at very low cost (or, at no cost at all) for farmers. However, very little is known about how field borders interact with land use intensification, and how this would play out in the perspective of supporting biological control in the field. In light of that, in the current study we investigated at local scale how the context of land use intensification could influence the communities of plants and arthropods occurring spontaneously in field borders, and whether this could consequently affect the potential of those borders to engender natural biological control.

There was a very low overlap of plant specimens occurring in the different border locations, suggesting an influence of the land use type on the composition of plant communities. Regardless, the plant species richness was significantly higher in borders exposed to extreme levels of agricultural intensification (highest and lowest), i.e. more plant species in the borders next to either annual crop or forest areas. In fact, previous studies have indicated that local factors such as farming type and location can significantly influence the richness and composition of plant species occurring in agricultural fields (Tarmi 2011; Blaix and Moonen 2020; José-María et al. 201; Poinas et al. 2023). Part of these results may be explained by the fact that variation in farming type and location can work as an environmental filter to select distinct functional traits, thereby leading to different plant communities (José-María et al. 2011). Our hypothesis of expecting lower plant species richness in borders next to annual crops was not supported by the data; but instead a higher richness was detected. Regardless, the data suggest that while exposed to opposite levels of agricultural intensification (highest and lowest), the annual crop and forest areas may respectively select/filter distinct plant traits that will result in high plant richness in both border types (with different species composition).

More herbivores (especially aphids) were encountered in borders next to annual or perennial crop areas. This result suggests that spontaneous vegetation bordering arable fields (i.e. with some level of agricultural intensification) will be more prone to harbor more herbivorous insects, most of which in our study apparently are not considered pests. The abundance of natural enemies on the other hand was more season dependent when occurring in borders next to forest and perennial areas, whereas in borders next to annual crop areas their abundance was higher in any season. The more intensive management carried out for crops in arable fields and the lower plant diversity therein may jointly function as a ‘push-force’ driving arthropods to more plant-diverse adjacent areas such as field borders. This may be particularly true in the case of generalist arthropods (e.g. herbivores) that are not directly related to the crop in the arable field, which therefore will seek alternative habitats (i.e. with more resources). Moreover, in the case of natural enemies, the higher abundance of herbivores in borders next to perennial or annual crop areas may work as a ‘pull-force’ because they can often serve as alternative prey/host, which in turn can engender an attraction and subsistence of natural enemies (Settle et al. 1996; Hardwood et al. 2007; Wyss 1996; Gontijo et al. 2018; Rowen et al. 2019). In any case, many previous studies have shown that field borders in fact have greater arthropod abundance and taxon richness than adjacent crop fields (Denys and Tscharntke 2002; Asteraki et al. 2004; Woodcock et al. 2005; Cole et al. 2007; Moreby 2007; Ramsay et al. 2007).

The composition of communities of herbivores and natural enemies in our study was likely to be also indirectly affected by border location and season. This may be so because those variables had a significant effect on the composition of plant communities in the borders, which in turn is expected to consequently influence/drive the composition of higher trophic levels. It is likely that different plant communities in the borders will work to filter distinct arthropod functional traits, which will lead to different community compositions. In fact, various studies and reviews point out to plant functional traits as a selective force that lead to distinct arthropod compositions in a given habitat (Ebeling et al. 2018; Gardarin et al. 2018; Perović et al. 2018; Schuldt et al. 2019; Dominik et al. 2022; Silva et al. 2022). Nevertheless, in our specific case, further studies are necessary to assess how effective spontaneous border vegetation can be in filtering/selecting distinct arthropod functional traits and how this would play out in the context of agricultural intensification.

The border vegetation next to annual or perennial crop areas showed a higher potential to engender biological control, as these borders seemed to affect more negatively the per capita growth of aphids in our study. This result may have been driven by a combination of favorable natural enemy composition and abundance in those borders. In the case of natural enemy abundance, this metric was particularly high in the border vegetation next to annual crop areas, regardless of season. Additionally, the plants in those border locations (annual and perennial) appeared to have more flowers and to harbor more herbivores (specially aphids), both of which can promote biological control through natural enemy conservation. Specifically, flowers and alternative prey are known to often attract and complement natural enemies’ diet, potentially leading to improved biological control of specific pests (Hardwood et al. 2007; Straub et al. 2008; Gontijo et al. 2013; Snyder 2019; Zuma et al. 2023). In regard to providing alternative prey (e.g. aphids), those borders could also be seen as serving the purpose of banker plants, which are known to sustain natural enemies and promote biological control (Frank 2010; Chen et al. 2022; Wang et al. 2022). Our hypothesis of expecting lower biological control close to annual crop borders was not supported by the data; instead a lower potential was detected in borders next to forest areas. In fact, the contribution of forest areas to biological control of pests in nearby fields have yielded mixed results in the past, including positive, negative and neutral effects (Winqvist et al. 2011; Tscharntke et al. 2026). In the case of negative or neutral effects, these might happen because certain types of forests will not filter/select plant or arthropod functional traits that would be conducive to biological control. Nevertheless, further empirical studies are necessary to investigate this assertion.

In conclusion, this multi-season study informs that the potential for field border vegetation to promote biological control will depend on the context of agricultural intensification. Specifically, the land use type had a significant influence on the communities of plants and arthropods inhabiting field borders, therefore turning out to be an important factor to be considered in habitat manipulation. Nonetheless, more studies ought to be carried out in order to investigate the mechanisms that drive this multi-faceted relationship concerning land use type, border vegetation and biological control. In any case, it appears that land use type will influence biological control by selecting/filtering border plants that will conserve/promote natural enemies through the provision of adequate resources. Furthermore, our study reinforces the importance of spontaneous border vegetation, and therefore indicates that it should be incentivized in agroecosystems, especially in areas with annual crops.

Author contributions

LG conceived and designed the experiments. AS, RC, and CM, worked on setting up experiments and collecting data. JS worked on plant identification. LG acquired funding and resources. LG carried out statistical analyses. All authors contributed to writing and revising the manuscript.

Conflict of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data Availability

Data will be made available on request.

Acknowledgments

We wish to thank Prof. Claudio Ronchi for helping identifying some of the border plants. We also want to thank José Hiago Silva and Jakeline Moreirafor helping with some of the data collection. This study was supported by the Brazilian research agency ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq, grant number 301731/2017-9).

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The authors declare no competing interests.

Appendix1Supplementarymaterial.docx
Appendix: Supplementary Material

Agricultural intensification affects communities of plants and arthropods in field borders and their potential to engender biological control

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Version 1

Abstract

Figures

Introduction

Material and Methods

Statistical analysis

Results

Discussion

Declarations

References

Additional Declarations

Supplementary Files

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Version 1