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The aphid food web associated with citrus orchards with a sown ground cover. The ground cover is composed of the sown Poaceae and the spontaneous wild plants. We hypothesized that the ground cover may host aphids which act as alternative prey for parasitoids and predators. Lines with arrows indicate interactions between groups of different trophic levels. Continuous lines indicate confirmed interactions and discontinuous lines indicate unknown interactions. Letters in brackets refer to the objectives exposed in the Introduction section.
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There is increasing interest in the use of sown ground covers in agriculture to provide alternative resources to predators and parasitoids as part of conservation biological control. Nevertheless, there is limited evidence that this approach is effective in commercial orchards, where a wild complex of plants co-occur with the sown plant species. In...
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... is the summation of overall sampling dates, t is the interval between two successive sampling dates (usually 7 days in this study) and x 1 and x 2 are predators/parasitoids counts on those dates. CPreD and CParD values were plotted against time, and linear regressions models were fitted. Once the regression lines were fitted, the analysis of covariance (ANCOVA) allowed comparison of their slopes (which repre- sent their population growth), thus testing the null hypothesis which is the assumption of the homogeneity of regression slopes (population growth does not depend on the interaction between treatment and time) (McDonald, 2009). Generalized linear models were used to determine the differences in aphid damage between soil managements by the percentage of infested shoots. The statistical software package ‘R’ ( ) and its packages “nlme” were used in our analyses. The mean percentages of ground covered by vegetation at the beginning of the sampling period (February) was 59.6%, 74.4%, 54.8% and 33.4% for AU, CD, CU and PP, respectively (see Appendix A: Fig. 3). This percentage decreased in the following two weeks in orchards CD and CU because the ground cover was mowed. At the end of March, the mean percentage of cover increased in all of the orchards, reaching approximately 90%. Finally, at the beginning of the critical period, the mean cover percentages were 91%, 76.5%, 67.3% and 96.5%, in AU, CD, CU and PP, respectively. A total of 21 plant genera belonging to 10 families were identified in the ground cover of the four orchards sampled (see Appendix A: Fig. 1). Plants from the Poaceae family were generally the most abundant throughout the sampling period in orchards AU, CD and PP, representing around 75% of ground cover plants, nev- ertheless the percentage of Poaceae was around 30% in the same period in orchard CU (Fig. 2). The most widely distributed plant genera, all of which were found in every orchards, were the Poaceae genera Bromus , Festuca and Hordeum as well as the genera Malva , Oxalis and Sonchus . Bromus was the only plant genus that persisted in all of the orchards at all dates. Orchard “CD” had the highest number of plant genera (17 recorded genera), whereas orchard “CU” had the low- est number of plant genera (9 genera) (see Appendix A: Fig. 1). Out of the 964 ground cover samples collected, 262 (27.2%) contained aphids. 1843 aphid specimens were extracted from these samples, with a mean of 1.91 ± 0.38 aphids per sample. Aphid abundance was 14.55 ± 2.42 (aphids/m 2 ) in the 73.73 m 2 of the sampled area. Mean aphid abundance was constant until March 27 in the four orchards, except the two first weeks in orchard “CD”, where the number of aphids was higher (Fig. 3). Finally, the aphid abundance increased in all of the orchards at the beginning of the critical period (April 17). Of the 1843 aphids extracted from the ground cover plants, 237 were adults, and 158 of these were identified to species. In order of abundance, these species were A. gossypii Glover ( n = 35), Uroleucon sonchi L. ( n = 32), Sitobion fragariae Walker ( n = 28), Hyperomyzus lactucae L. ( n = 19), Rhopalosiphum padi L. ( n = 19), A. spiraecola Patch ( n = 14), Macrosiphum euphorbiae Thomas ( n = 7) and Myzus persicae Sulzer ( n = 4). A. gossypii , H. lactucae , R. padi and S. fragariae were present in the ground cover of the four orchards sampled (Fig. 3, see Appendix A: Table 2). By contrast, M. euphorbiae and U. sonchi were identified in only two orchards (both in “AU” and “CD”). To analyze the seasonal trends of the aphid species identified, we divided the sampling period into three intervals: February sampling dates, March and April (Fig. 3). The aphid community collected during the sampling period differed among orchards. In February, R. padi , an aphid specialized on monocotyledons (as the Poaceae), was the most abundant species in all of the orchards except “PP”, where A. gossypii was the only identified aphid species. In March, the number of aphid species increased in all orchards, and citrus aphids ( A. spiraecola and A. gossypii ) were abundant only in orchard “PP”. Finally, during the critical period, citrus-infesting aphids were the most abundant in the ground cover of three orchards: AU (61.2%), CU (100%) and PP (63.8%) of the identified specimen. Among the 23 plant genera identified in the ground cover of the four orchards, 16 harbored aphids, whereas the genera Amaranthus , Allium , Convolvulus , Conyza , Senecio , Urtica and Capsella sp. did not. Sonchus sp., Erodium sp. and Bromus sp. were the plant genera with the highest numbers of aphids (see Appendix A: Table. 2). When we calculated the number of aphids per m 2 of each plant genus, Sonchus sp. and Erodium sp. contained more aphids per m 2 than the other plant genera. They were followed by a second group, composed Poaceae genera ( Bromus , Hordeum , and Poa , and some other genera from different families including Malva and Picris . Importantly, no poaceous genus harbored A. spiraecola , and the genera Festuca sp. and Hordeum sp. did not harbor A. gossypii either. In Bromus sp., 0.14 (proportion of aphid species) adult aphids were identified as A. gossypii , 38% were winged. Among the 829 A. spiraecola colonies sampled throughout the assay (496 colonies in orchards with ground cover and 333 in orchards with bare soil), a total of 19,693 aphids and 312 natural enemies (262 Aphididae parasitoids and 50 predators [25 Cecidomyiidae, 12 Chrysopidae, 7 Coccinellidae, 4 Syr- phidae and 2 Theridion sp. individuals]) were counted (see Appendix A: Table 1). There were no significant differences in the ratios of attacked colonies between soil managements during the sampling period (Feb 21 to May 9) ( χ 2 = 0.23, F 1, 1052 = 0.23, P = 0.64) (Fig. 4). However, there were significant differences in the ratio of attacked colonies between management types before the critical period for A. spiraecola infestation (Feb 21 to April 17) ( χ 2 = 4.038, F 1, 683 = 3.89, P = 0.044). On the last sampling date before the critical period (April 10) the ratio of attacked colonies were 0.3 ± 0.1 and 0 ± 0 in cover orchards and bare soil orchards, respectively. The mean cumulative number of predators per day (CPreD) values increased earlier and remained higher in orchards with ground cover management than in those with bare soil (Fig. 5A; see Appendix A: Table 3). The interaction between treatment and date did not affect significantly the population growth of the predators (interaction between treatment and date: F 1, 93 = 0.89, P = 0.35), but there were significant differences between soil managements ( F 1, 93 = 15.25, P Y < 0.001). For parasitoids (CParD), the interaction between treatment and date affected significantly their population ...
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... is the summation of overall sampling dates, t is the interval between two successive sampling dates (usually 7 days in this study) and x 1 and x 2 are predators/parasitoids counts on those dates. CPreD and CParD values were plotted against time, and linear regressions models were fitted. Once the regression lines were fitted, the analysis of covariance (ANCOVA) allowed comparison of their slopes (which repre- sent their population growth), thus testing the null hypothesis which is the assumption of the homogeneity of regression slopes (population growth does not depend on the interaction between treatment and time) (McDonald, 2009). Generalized linear models were used to determine the differences in aphid damage between soil managements by the percentage of infested shoots. The statistical software package ‘R’ ( ) and its packages “nlme” were used in our analyses. The mean percentages of ground covered by vegetation at the beginning of the sampling period (February) was 59.6%, 74.4%, 54.8% and 33.4% for AU, CD, CU and PP, respectively (see Appendix A: Fig. 3). This percentage decreased in the following two weeks in orchards CD and CU because the ground cover was mowed. At the end of March, the mean percentage of cover increased in all of the orchards, reaching approximately 90%. Finally, at the beginning of the critical period, the mean cover percentages were 91%, 76.5%, 67.3% and 96.5%, in AU, CD, CU and PP, respectively. A total of 21 plant genera belonging to 10 families were identified in the ground cover of the four orchards sampled (see Appendix A: Fig. 1). Plants from the Poaceae family were generally the most abundant throughout the sampling period in orchards AU, CD and PP, representing around 75% of ground cover plants, nev- ertheless the percentage of Poaceae was around 30% in the same period in orchard CU (Fig. 2). The most widely distributed plant genera, all of which were found in every orchards, were the Poaceae genera Bromus , Festuca and Hordeum as well as the genera Malva , Oxalis and Sonchus . Bromus was the only plant genus that persisted in all of the orchards at all dates. Orchard “CD” had the highest number of plant genera (17 recorded genera), whereas orchard “CU” had the low- est number of plant genera (9 genera) (see Appendix A: Fig. 1). Out of the 964 ground cover samples collected, 262 (27.2%) contained aphids. 1843 aphid specimens were extracted from these samples, with a mean of 1.91 ± 0.38 aphids per sample. Aphid abundance was 14.55 ± 2.42 (aphids/m 2 ) in the 73.73 m 2 of the sampled area. Mean aphid abundance was constant until March 27 in the four orchards, except the two first weeks in orchard “CD”, where the number of aphids was higher (Fig. 3). Finally, the aphid abundance increased in all of the orchards at the beginning of the critical period (April 17). Of the 1843 aphids extracted from the ground cover plants, 237 were adults, and 158 of these were identified to species. In order of abundance, these species were A. gossypii Glover ( n = 35), Uroleucon sonchi L. ( n = 32), Sitobion fragariae Walker ( n = 28), Hyperomyzus lactucae L. ( n = 19), Rhopalosiphum padi L. ( n = 19), A. spiraecola Patch ( n = 14), Macrosiphum euphorbiae Thomas ( n = 7) and Myzus persicae Sulzer ( n = 4). A. gossypii , H. lactucae , R. padi and S. fragariae were present in the ground cover of the four orchards sampled (Fig. 3, see Appendix A: Table 2). By contrast, M. euphorbiae and U. sonchi were identified in only two orchards (both in “AU” and “CD”). To analyze the seasonal trends of the aphid species identified, we divided the sampling period into three intervals: February sampling dates, March and April (Fig. 3). The aphid community collected during the sampling period differed among orchards. In February, R. padi , an aphid specialized on monocotyledons (as the Poaceae), was the most abundant species in all of the orchards except “PP”, where A. gossypii was the only identified aphid species. In March, the number of aphid species increased in all orchards, and citrus aphids ( A. spiraecola and A. gossypii ) were abundant only in orchard “PP”. Finally, during the critical period, citrus-infesting aphids were the most abundant in the ground cover of three orchards: AU (61.2%), CU (100%) and PP (63.8%) of the identified specimen. Among the 23 plant genera identified in the ground cover of the four orchards, 16 harbored aphids, whereas the genera Amaranthus , Allium , Convolvulus , Conyza , Senecio , Urtica and Capsella sp. did not. Sonchus sp., Erodium sp. and Bromus sp. were the plant genera with the highest numbers of aphids (see Appendix A: Table. 2). When we calculated the number of aphids per m 2 of each plant genus, Sonchus sp. and Erodium sp. contained more aphids per m 2 than the other plant genera. They were followed by a second group, composed Poaceae genera ( Bromus , Hordeum , and Poa , and some other genera from different families including Malva and Picris . Importantly, no poaceous genus harbored A. spiraecola , and the genera Festuca sp. and Hordeum sp. did not harbor A. gossypii either. In Bromus sp., 0.14 (proportion of aphid species) adult aphids were identified as A. gossypii , 38% were winged. Among the 829 A. spiraecola colonies sampled throughout the assay (496 colonies in orchards with ground cover and 333 in orchards with bare soil), a total of 19,693 aphids and 312 natural enemies (262 Aphididae parasitoids and 50 predators [25 Cecidomyiidae, 12 Chrysopidae, 7 Coccinellidae, 4 Syr- phidae and 2 Theridion sp. individuals]) were counted (see Appendix A: Table 1). There were no significant differences in the ratios of attacked colonies between soil managements during the sampling period (Feb 21 to May 9) ( χ 2 = 0.23, F 1, 1052 = 0.23, P = 0.64) (Fig. 4). However, there were significant differences in the ratio of attacked colonies between management types before the critical period for A. spiraecola infestation (Feb 21 to April 17) ( χ 2 = 4.038, F 1, 683 = 3.89, P = 0.044). On the last sampling date before the critical period (April 10) the ratio of attacked colonies were 0.3 ± 0.1 and 0 ± 0 in cover orchards and bare soil orchards, respectively. The mean cumulative number of predators per day (CPreD) values increased earlier and remained higher in orchards with ground cover management than in those with bare soil (Fig. 5A; see Appendix A: Table 3). The interaction between treatment and date did not affect significantly the population growth of the predators (interaction between treatment and date: F 1, 93 = 0.89, P = 0.35), but there were significant differences between soil managements ( F 1, 93 = 15.25, P Y < 0.001). For parasitoids (CParD), the interaction between treatment and date affected significantly their population ...
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... aim of habitat management in conservation biological control is to create a suitable ecological infrastructure to favor natural enemies and to enhance biological control in agricultural systems (Landis, Wratten, & Gurr, 2000; Fiedler, Landis, & Wratten, 2008). In monoculture agroecosystems, natural enemies suffer from a lack of food for adults, alternative prey or hosts, and shelter against adverse conditions (Landis et al., 2000). In the absence of these vital resources, colonization of crops by predators and parasitoids is often much lower than colonization by herbivores (Thies & Tscharntke, 1999). An extensively researched form of habitat management that favors natural enemies in tree crops is the use of ground covers (Landis et al., 2000; Silva, Franco, Vasconcelos, & Branco, 2010). In the last ten years, grass covers have been cultivated with citrus trees both for agronomic reasons (Aucejo, 2005) and because it facilitates the management of the two-spotted spider mite Tetranychus urticae Koch (Prostigmata: Tetranychidae), a key pest in clementines, by both bottom-up and top-down regulation (Aguilar-Fenollosa, Iba nez-Gual, Pascual-Ruiz, Hurtado, & Jacas, 2011a,b). In addition, ground cover management could also enhance the presence of generalist ground-dwelling predators, which can prey on citrus pests inhabiting or pupating on the soil such as the Mediterranean fruit fly Ceratitis capitata Wiede- mann (Diptera: Tephritidae) (Monzo, Molla, Castanera, & Urbaneja, 2009). Aphis spiraecola Patch (Hemiptera: Aphididae) is a key pest of Clementine mandarins, Citrus clementina Hort. ex Tan. (Geraniales: Rutaceae), in the Mediterranean basin (Hermoso de Mendoza, Arouni, Belliure, Carbonell, & Perez- Panades, 2006; Tena & Garcia-Marí, 2011; Vacante & Gerson, 2012). This polyphagous aphid colonizes young, tender clementine shoots in spring (Hermoso de Mendoza et al., 2006) and causes economic losses because it sucks sap, serves as a vector for Citrus tristeza virus, excretes large amounts of honeydew and curls developing leaves while the colony population is growing (Hermoso de Mendoza et al., 2006). To improve the management of aphids in clementines, Hermoso de Mendoza et al. (2006) established intervention thresholds based on the percentage of shoots infested by aphids within a 0.25 m 2 ring throw on the outer canopy of trees. An insecticide application is justified when more than 25% of the shoots are infested. Hereinafter, we refer to the time period during which the percentage of infested shoots reaches approximately 20 to 25%, as the critical period for the management of A. spiraecola on clementines. Citrus, as a permanent and perennial crop, provides an environment in which numerous predators and parasitoids of A. spiraecola readily develop in the spring (Romeu-Dalmau, Espadaler, & Pinol, 2012; Vacante & Gerson, 2012; Gómez- Marco, Tena, Jacas, & Urbaneja, 2015a; Gómez-Marco et al., 2015b). Despite this abundant and diverse complex of natural enemies, biological control of A. spiraecola is generally insufficient because of the asynchrony of predators with aphid population growth (Gómez-Marco et al., 2015a) and the lack of effective parasitoids (Gómez-Marco et al., 2015b). Recently, it has been demonstrated that predators can main- tain aphid densities under the economic threshold if they arrive early in the season, from seven to ten days after A. spiraecola colonizes the spring shoots (Gómez-Marco et al., 2015a). Therefore, we hypothesize that a ground cover that promotes the early establishment of natural enemies, prior to the exponential increase of the aphid (Gómez-Marco et al., 2015a), might facilitate the biological control of A. spiraecola in citrus orchards. To advance the presence of the natural enemies of A. spiraecola in citrus canopies, a ground cover based on grass plants must possess certain key features. For example, the cover should harbor alternative prey or host species, such as other aphids in the appropriate time lag (Wyss, 1995; Welch & Harwood, 2014). This means at the end of winter or early spring, before A. spiraecola infests and damages clementine spring shoots (Gómez-Marco et al., 2015a). On the other hand, this ground cover should not benefit A. spiraecola or other citrus pests, especially Aphis gossypii Glover (Hemiptera: Aphididae). It is known that grass plants do not harbor A. spiraecola (Holman, 2009). However, diverse spontaneous plant species accompanied the sown grass covers (Kruidhof, Bastiaans, & Kropff, 2008), which might reduce the efficacy of the ground cover if they harbor the target pest or reduce the use of pest aphids by natural enemies in the crop. In this study, we first identified and quantified (i) the complex of spontaneous plant species that accompanied sown ground covers based on Poaceae plants as well as (ii) the aphid species inhabiting these plant species in four citrus orchards with ground covers. We then tested (iii) whether this aphid community enhanced the presence of natural enemies in citrus canopies before A. spiraecola infestation and (iv) whether it reduced the damage due to aphids (Fig. 1). To do this, we compared the presence of natural enemies and the damage caused by A. spiraecola in orchards with and without ground cover (bare soil), which is the most common weed management practice in citrus orchards in ...
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... rootstock) located in the Valencia region of eastern Spain (see Appendix A: Table 1). The climate of the region is classified as warm-temperate subtropical with an annual mean temperature of 16.4 ◦ C and rainfall of 458 mm (aver- age of data from 2000 to 2013) (SIAR, 2014). The orchards “PPbs”, “PL”, “PS” and “TA” had bare soil (following the application of herbicides since February 11/14) whereas the orchards “AU”, “CD”, “CU” and “PP” had a sown ground cover crop consisting of a combination of grassy plants ( Festuca arundinacea , Poa sp., Bromus sp., etc.) and a complex of wild plants (see Appendix A: Fig. 1). Crops were at least five years old and their ground cover was mown twice per year: once at the end of winter (first two weeks of February) and again in early summer (first two weeks of June). “AU” and “TA” were surrounded completely by other citrus orchards and the rest were surrounded mostly by citrus orchards, with one side bordering on semi-natural habitat. No aphicides were applied during the sampling period. During the last 4 years, all orchards followed IPM guidelines (Urbaneja, Catalá, Tena, & Jacas, 2014) and were drip irrigated. Citrus size and vigor was similar throughout the orchards with no apparent effect of inter-row cover crop. Orchards were sampled and/or tracked weekly (depending on the season) from mid-February to early May, when A. spiraecola populations decline at the end of the leaf-flushing period (see Appendix: Fig. 2). The plant and aphid complex present in the ground cover of the four orchards was estimated weekly from February 1 to March 27 and once during the following critical period. The critical period in A. spiraecola management (April 22) is defined below in the “ Citrus canopy sampling” section. To determine the percentage of ground cover coverage and describe its plant composition, a ring of 0.25 m 2 was randomly thrown 10 times on the ground cover, and the percentage of ground cover inside each ring was visually estimated. Plants were subsequently identified to genus level and the percentage of each plant genus present inside the ring (for the five most abundant genera) was also visually estimated. To identify and quantify the aphids present in the ground cover, 0.01 m 2 (measured with a loose-leaf ring, 8 cm in diameter) of each plant genera present within the ring was randomly selected, clipped and transported to the laboratory in a plastic bag for aphid identification. A total of 964 ground cover samples were collected (see Appendix A: Table 1). In the lab, plants were examined in detail to collect and identify all of the aphids inhabiting the plants. Aphids were preserved in 70% ethanol, and adult aphids were identified to species (Blackman & Eastop, 1994). To calculate the number of aphids per m 2 of ground cover for each date and sample, we considered also the surface occupied by each plant genus in the ground cover. We assumed that aphids were uniformly distributed within the area occupied by each plant genus. The number of aphids per plant species was calculated as ...
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... sown ground covers based on Poaceae plants as well as (ii) the aphid species inhabiting these plant species in four citrus orchards with ground covers. We then tested (iii) whether this aphid community enhanced the presence of natural enemies in citrus canopies before A. spiraecola infestation and (iv) whether it reduced the damage due to aphids (Fig. 1). To do this, we compared the presence of natural enemies and the damage caused by A. spiraecola in orchards with and without ground cover (bare soil), which is the most common weed management practice in citrus orchards in ...
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... (SIAR, 2014). The orchards "PPbs", "PL", "PS" and "TA" had bare soil (following the application of herbicides since February 11/14) whereas the orchards "AU", "CD", "CU" and "PP" had a sown ground cover crop consisting of a combination of grassy plants (Festuca arundinacea, Poa sp., Bromus sp., etc.) and a complex of wild plants (see Appendix A: Fig. 1). Crops were at least five years old and their ground cover was mown twice per year: once at the end of winter (first two weeks of February) and again in early summer (first two weeks of June). "AU" and "TA" were surrounded completely by other citrus orchards and the rest were surrounded mostly by citrus orchards, with one side ...
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... total of 21 plant genera belonging to 10 families were identified in the ground cover of the four orchards sampled (see Appendix A: Fig. 1). Plants from the Poaceae family were generally the most abundant throughout the sampling period in orchards AU, CD and PP, representing around 75% of ground cover plants, nevertheless the percentage of Poaceae was around 30% in the same period in orchard CU (Fig. 2). The most widely distributed plant genera, all of which were found in ...
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... were the Poaceae genera Bromus, Festuca and Hordeum as well as the genera Malva, Oxalis and Sonchus. Bromus was the only plant genus that persisted in all of the orchards at all dates. Orchard "CD" had the highest number of plant genera (17 recorded genera), whereas orchard "CU" had the lowest number of plant genera (9 genera) (see Appendix A: Fig. 1). Aphid community in the ground ...
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... In Mediterranean biomes, habitat interventions can increase natural enemy diversity and/or abundance in grape (Rosas-Ramos et al., 2019), pear (de Pedro et al., 2020), apple (Santos et al., 2018), olive (Carpio et al., 2019), lemon (Silva et al., 2010) and pomegranate (Kishinevsky et al., 2017) orchard systems. However, most of these studies have focused on i) preserving naturally occurring vegetation, which results in site-specific responses (Gómez-Marco et al., 2016); ii) annual and biennial flower strips, which are costly to re-sow and leads to differences in year-on-year resource availability (Fiedler and Landis, 2007); or iii) agricultural varieties, which may be poorly adapted to the local climate and provide limited support for native natural enemies (Fox and Eisenbach, 1992). However, there is limited research on the value of habitat interventions in citrus (see . ...
... Additionally, tussock-forming grasses, such as S. arundinaceus, provide favourable microclimates for natural enemies during weather extremes (Collins et al., 2003;Luff, 1965). However, when naturally occurring forb species establish in these grass strips, aphid management is enhanced due to the increase in floral resources (Gómez-Marco et al., 2016). By relying on species present in the vicinity, site specific responses can limit the benefits achieved, however, this can be overcome through the inclusion of wildflower species (forbs) in seed mixes used to establish alleyway habitats (Mockford et al., 2023). ...
Contemporary approaches to agriculture must be reimaged to include ecological techniques that maximise ecosystem services, so that food can be produced sustainably whilst simultaneously meeting yield demands. Pest regulation services, harnessed through the conservation of natural enemies in the agri-environment are an economically important service degraded by conventional citrus production practices. For the first time, a sown wildflower strip composed of native forbs and tussock-forming grasses has been investigated for its influence on natural enemies and their pest regulation services in citrus orchards. A novel management strategy was applied, using the predicted generation times of Aonidiella aurantii Maskell (Hemiptera: Diaspididae), a key pest in citrus, to determine whether cutting the wildflower strips could force spill-over of natural enemies onto the adjacent crop, enhancing pest regulation services. Three treatments applied to orange orchard alleyways were compared: i) a control treatment, the standard orchard practice of regular cutting to 5 cm throughout the year, ii) a sown wildflower treatment managed with cutting once a year in February to a height of 10 cm (standard management wildflower treatment, SMWT), and iii) the same sown wildflower treatment but managed with two additional cuts in May and June (active management wildflower treatment, AMWT). Orange tree canopies were sampled for natural enemies, and pest regulation services were quantified using sentinel prey cards baited with Ephestia kuehniella eggs. Natural enemy richness was greatest in canopies with SMWT, supporting a greater relative abundance of primary parasitoids and lower relative abundances of antagonists (ants) compared to the control. This was associated with enhanced pest regulation services (depletion of sentinel prey from baited cards), especially during the early summer months, which coincides with a critical period to control A. aurantii and other key citrus pests. In contrast, AMWT did not enhance natural enemy richness, and pest regulation services were diminished. This study suggests that leaving wildflower strips uncut throughout the season, as in SMWT, may help to mitigate pest incidence through enhanced pest regulation services. Further studies are now required to determine how this would influence populations of target pests.
... 1985). Diversified systems create conditions less favorable for pest arthropods and more conducive for natural enemies (Gómez-Marco et al. 2016;Meyling et al. 2013;Piñero and Manandhar 2015;Ponti et al. 2007). Secondary plants can serve as physical barriers, offer visual and olfactory camouflage, and act as repellents against pests (Finch and Collier 2000;Parolin et al. 2012;Piñero and Manandhar 2015;Root 1973). ...
Diversifying crop habitats and controlling arthropod pests by cultivating “secondary plants” alongside a primary crop is a frequently discussed strategy. The effectiveness of using secondary plants to manage pests varies across countries, and is influenced by factors such as the target pest, plant species, experimental design, and climatic conditions. Consequently, we conducted a study investing the impact of intercropping wheat or barley with additional flower strips on controlling aphid pests in white cabbage fields in Japan and Germany.Query Our results in Japan supported the natural enemies hypothesis, leading to a significant reduction in populations of two pest aphids: the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), and the cabbage aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae). Furthermore, intercropping and/or flower strips increased the proportions of natural enemies, including hoverfly larvae (Diptera: Syrphidae), ladybirds (Coccinellidae: Coleoptera), and parasitoid wasps (Hymenoptera: Braconidae), relative to the aphids. Hoverfly larvae, due to their high abundance, appeared to be Japan’s most effective aphid suppressors. In contrast, in Germany, intercropping and flower strips did not remarkably suppress aphid populations or enhance the presence of the natural enemies, despite a temporary increase in the population density of hoverfly larvae in intercropping. These disparities between the trials in the two countries may be attributed to variations in regional and local biodiversity. This suggests that using secondary plants for pest control should consider the specificities of local environments.
... Habitat heterogeneity's impact on important pests attacking crops in temperate regions, such as aphids, has been extensively studied (e.g. Bosem Baillod et al., 2017;Gómez-Marco et al., 2016;Redlich et al., 2018;Rusch et al., 2016). However, there is little literature addressing this issue on mealybugs, which are major pests in subtropical crops and are expanding into subtropical and temperate ecosystems (Miller et al., 2002;Pellizzari & Germain, 2010). ...
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The proportion of focal crop in the landscape increased the abundance of mealybugs attacking both crops. This effect was found at closer distances (up to ~600 m) in citrus and at both closer and further distances (up to 1250 m) in persimmon.
Non‐crop habitats, both surrounding semi‐natural habitats and ground cover vegetation, decreased the abundance of mealybugs by increasing the activity of their parasitoids in persimmon. Conversely, non‐crop habitats did not decrease the abundance of the main mealybug species attacking citrus, likely because this mealybug species was not attacked by native or naturalized parasitoids.
Synthesis and applications. Our models show that the increase in habitat heterogeneity at local and landscape scales can reduce the abundance of invasive mealybugs in subtropical crops via ‘resource concentration’ and ‘natural enemies’ mechanisms. Therefore, habitat diversification strategies should be considered in the conservation biological control of invasive mealybugs. Importantly, our findings also show that the presence of efficient natural enemies is critical to maximize their control through habitat diversification strategies.
... Such methods negatively impact the richness and abundance of natural enemies and limit pest regulation services (Aguilar-Fenollosa, Ibáñez-Gual, et al., 2011;Gómez-Marco et al., 2016). In Spain, it is becoming increasingly common for growers to leave naturally occurring (unsown) vegetation in alleyways between rows of fruit trees to limit soil erosion, which is managed with regular cutting (Jacas & Urbaneja, 2010). ...
... (Poales: Poaceae)), provide microclimate shelter (Luff, 1965), and sustain alternative prey and hosts (Gómez-Marco et al., 2016) for natural enemies (Thomas et al., 1991). Grass strips sown with S. arundinaceus have been adopted by some Citrus growers to help manage spider mites and thrips (Aguilar-Fenollosa, Ibáñez-Gual, et al., 2011;Jacas & Aguilar-Fenollosa, 2013). ...
... Grass strips sown with S. arundinaceus have been adopted by some Citrus growers to help manage spider mites and thrips (Aguilar-Fenollosa, Ibáñez-Gual, et al., 2011;Jacas & Aguilar-Fenollosa, 2013). Unsown forbs which establish in these otherwise species-poor habitats further enhance the management of aphids (Gómez-Marco et al., 2016), most likely due to the increased provision of pollen for coccinellids and nectar for parasitoids. ...
To support sustainable food production and the delivery of ecosystem services through ecological intensification, wildflower strips have become a popular strategy. Despite their success in temperate orchard systems, they remain understudied in Mediterranean ecosystems, which poses a significant barrier to uptake. In order to further promote their adoption, seed mixes must be optimised for commercial orchard systems and for the Mediterranean climate. Plant species should be selected for their consistent performance, whilst the availability of resources for ecosystem service providers determines the quality of the wildflower strip. In this study, the suitability of 12 native perennial forbs and two tussock-forming grass species for wildflower strips in commercial Citrus orchards was assessed over a 3-year period. Distinct resources for natural enemies according to the different plant growth stages were used an indicator of wildflower strip quality. The wildflower strips were managed under two different cutting strategies: (i) standard management, in which wildflower strips were cut once annually in February, and (ii) active management, in which wildflower strips were cut two additional times each year. The establishment and success of the sown species were compared. The influence of wildflower strips and their management on plant species richness, community structure, and the provision of resources was compared with a control treatment, in which alleyways were managed conventionally by cutting any naturally occurring vegetation to a height of ≤5 cm, four to five times annual. For the first time, the performance of native perennial plant species has been assessed in Mediterranean orchard systems and a seed mix developed for targeting pest regulation services. The wildflower strips were successful in increasing plant species richness and the available resources expected to support natural enemies. However, only wildflower strips managed with cutting once annually enhanced vegetation cover relative to the control, whilst extending the flowering period. This study therefore provides crucial tools for the further development of sustainable approaches to food production in Mediterranean orchard systems.
... maior abundância de predadores em pomares de fruteira com presença de cobertura vegetal também foi relatada por outros autores (Sanguankeo, 2011;Birkhofer et al., 2015;Gómez-Marco et al., 2016;Sommaggio et al., 2018). ...
Almond production is an economically important activity in Portugal where both surface and production have shown a significant increase in the last decade. The almond tree is affected by several diseases and pests that can contribute to the quantitative and qualitative reduction of almond production. Biting-sucking pests (Hemiptera) such as monosteira, aphids, cicadelids, lepidopterans such as anarsia, grapholite, or coleopterans borers, such as capnode can cause, in some cases, significant damage. The aim of this study was to compare the abundance and functional diversity of arthropod communities in almond orchards using different weed management methods (displaced soil and presence of destroyed vegetation cover) in the Trás-os-Montes region. Cover crops had a significant effect on arthropod abundance and diversity. The orchard covered with vegetation (CCV) had the highest number of Araneae, Hemiptera and Neuroptera, while the orchard without vegetation cover (SCV) had the highest number of Coleoptera and Hymenoptera. Regarding the functional groups, the CCV orchard had a higher number of phytophagous and predatory arthropods, while no difference was observed between pollinators and fungivores. The diversity index was significantly higher in the presence of cover vegetation, which also showed greater dominance of hemipterans, namely the pest Monosteira unicostata.
... Consequently, more and more studies are evaluating the role of specific companion plant A. Köneke and R. Uesugi have contributed equally to this work. systems in horticultural crops as an alternative pest control method (Chen et al. 2020;Gómez-Marco et al. 2016;Gulidov and Poehling 2013;Meyling et al. 2013;Ponti et al. 2007;Sekine et al. 2021;Sun and Song 2019). ...
An undersowing system with additional intercropping of flowering plants was assessed in field trials in Germany and Japan to estimate regulating effects on pests and possible negative effects on white cabbage ( Brassica oleracea var. capitata ). In particular, we tested cabbage undersown with wheat ( Triticum aestivum L.) and cabbage undersown with wheat plus additional sweet alyssum ( Lobularia maritima L. Desv.) intercropping. Counts of the aphid species Brevicoryne brassicae (L.) and Myzus persicae (Sulzer), as well as related predators on cabbage plants, were determined. Abundance of Phyllotreta spp. flea beetles and their feeding damage on cabbage plants were recorded and cabbage yield was compared. In both countries, trials showed that wheat undersowing reduced the abundance of M. persicae but not B. brassicae . The occurrence of natural enemies on cabbage plants was not significantly affected by any of the companion plants. Additional sweet alyssum intercropping increased the abundance of adult hoverflies at the German but not at the Japanese location. However, it also significantly increased flea beetle infestation on cabbage plants at both locations. Neither wheat undersowing nor additional sweet alyssum intercropping significantly reduced cabbage harvest weight.
In conclusion, adding companion plants can be a promising method to improve pest control in vegetable crops. However, intercropping crucifer crops with sweet alyssum may not be recommended in regions where flea beetles are a relevant pest because of the observed enhancing effect on them. In contrast, to prove the positive effect of wheat undersowing on white cabbage, results from further years of investigation are needed.
... Diversification of crop habitats generally promotes more diverse arthropod communities and strengthens biological control (Sheehan 1986, Hooks and Johnson 2003, Piñero and Manandhar 2015. Such systems are generally less favorable for pest arthropods and/or more conducive for natural enemies, and consequently, reduce the damage caused by pests (Ponti et al. 2007, Meyling et al. 2013, Piñero and Manandhar 2015, Gómez-Marco et al. 2016. ...
The effects of two possible factors, prevention of pest immigration and enhancement of natural enemies, in suppressing onion thrips, Thrips tabaci L., were estimated in a small-scale experimental system of spring-planted onions intercropped with barley. The population dynamics of the thrips and their potential predatory natural enemies were investigated in four treatments: control (bare ground), insect net barrier, and onion-barley intercropping with or without trimming. We found that intercropping significantly suppressed onion thrips. It is unlikely that this effect was due to the prevention of thrip immigration because they seemed to move over the camouflage and/or physical barriers of the barley and the net barrier surrounding the onions easily. Intercropping with barley significantly increased hoverfly (Syrphidae) larvae numbers on onion leaves, and that of some groups of ground-dwelling predators such as large carnivorous ground beetles (Carabidae), ants (Formicidae), and wolf spiders (Lycosidae). We conclude that the suppression of thrips in this system was associated with the enhancement of hoverfly larvae abundance, mainly Sphaerophoria macrogaster (Thomson) (Syrphidae: Diptera) because they were observed together with thrips on onions and have been reported to predate thrips as well as aphids. Some hoverfly larvae on barley might move to nearby onions to search for new food sources and attack thrips.
... States, intermediate organizations with the predominant participation of researchers and experts, should develop strategies aimed at amalgamating economic productive interests with the protection of pollinator populations and the healthiness of beekeeping products. For example, by encouraging more traditionally managed farms (with certain logical restrictions on the use of pesticides but still guaranteeing good harvests as shown by some works that promote the biological regulation of pests (Gómez-Marco et al., 2016;de Pedro et al., 2021) where these farmers develop mostly extensive crops (soybean, corn, sorghum, wheat, etc.) that usually guarantee profitability to the sector and genuine economic income to the country. These farmers shall simultaneously ensure adequate rotations, applying erosion control and efficient water use practices. ...
There is considerable scientific evidence revealing a decrease in pollinating insects in different ecosystems around the world. In this context, agricultural intensification and the use of phytosanitary products are likely the main causes. This problem is common to many pollinators but of particular ecosystemic, economic and bromatological significance for honey bees (Apis mellifera) since their presence in these landscapes is mainly due to the proximity of apiaries for human food production and because they are the most important biotic pollinators of agricultural crops. In this review, we present a synthesis of the results of several years of research on this topic, as well as potential solutions referenced in the bibliography that might help alleviate the effects of contamination on honey bees and their products. Additionally, we expose the possible limits of the real implementation of such solutions and conclude on the need to implement land-use planning strategies for agricultural systems. Without mitigating actions in the short term, the sustainability of agricultural ecosystems as bee-friendly habitats and the production of foods suitable for human consumption are uncertain.
... In this context, the implementation of IPM requires a thorough knowledge of the community of natural enemies associated to each agroecosystem and their potential for pest control (Crowder and Jabbour, 2014). Several studies in other Mediterranean orchards, such as pepper, citrus and pear, have provided clear evidence that native natural enemies can significantly contribute to regulate populations of phytophagous arthropods (Aguilar-Fenollosa et al., 2011;Gómez-Marco et al., 2016;Sanchez and Lacasa, 2006;Sanchez and Ortín-Angulo, 2012). However, there is a lack of knowledge of the natural enemies associated to open-field melon crops that hampers the establishment of IPM programs that include biological control. ...
... Conventional farming often involves the reiterative use of broad-spectrum insecticides, which are known to greatly reduce the abundance of natural enemies and cause pest resistance leading to pest outbreaks (Hill et al., 2017;Roush and Tabashnik, 1990). Instead, IPM strategies involving low application of insecticides have been reported to be more compatible with natural enemies and more effective pest management strategies than intensive chemical control in different Mediterranean crops (Gómez-Marco et al., 2016;Sanchez et al., 2021aSanchez et al., , 2021bSanchez and Ortín-Angulo, 2012). ...
Pest control in Mediterranean open-field melon crops currently relies on repeated pesticide applications. A lack of IPM programs that taking into account naturally occurring biological control agents in the crop could be due, in part, to a lack of knowledge of the natural enemies associated with melon and their pest control potential. We estimated the abundance of pests and natural enemies in fields managed with a conventional insecticide regime (CPR) and a ‘no insecticide’ regime (NPR), with all fields receiving fungicide applications (sulphur or triadimenol), as required. In a two-year study, six melon fields were sampled periodically during spring and early summer by visual observations of leaves and the extraction of arthropods from flowers using Berlese funnels. The most abundant phytophagous arthropods on melon leaves were thrips (38.9% of total counts), aphids (31.5%), spider mites (26.8%) and whiteflies (2.8%). Aphis gossypii was significantly more abundant in CPR than in NPR fields, whereas whiteflies and thrips had similar abundance in the two treatments. Spider mites were more abundant in NPR than in CPR fields. The main groups of natural enemies on leaves were Orius spp. (76.1% of total counts), phytoseiids (7.4%), predatory thrips (7.1%) and cecidomyiids (5.6%), and all were significantly more abundant in NPR than in CPR fields. The primary predators in flowers were Orius spp. (67.4%) and Aeolothrips spp. (32.6%), and both were significantly more abundant in NPR than in CPR fields. Orius spp. was inferred to be the primary biological control agent of aphids, as few aphids were mummified by parasitoids. The control of aphids by Orius spp. was probably mediated by apparent competition with thrips, which are a preferred prey of Orius spp. In summary, elimination of pesticides from the management regime enhanced the abundance of natural enemies in the melon crop, and natural biological control limited pest infestations in NPR fields as well as did broad-spectrum insecticides in CPR fields. Therefore, IPM strategies for melon production should consider conservation of natural biological control agents as an effective alternative to conventional regimes that rely primarily upon insecticides.
... The selection of optimal plant species for the promotion of natural predators is based on information on the ecological mechanisms of how they benefit the predators. Based on their functions and characteristics, cover crops can be divided into two types: (1) flowering plants that provide pollen and nectar (Gontijo et al., 2013;Lu et al., 2014), and (2) grass plants that provide alternative prey/hosts (Wyss, 1996;Gomez-Marco et al., 2016). Floral resources could benefit the longevity and fecundity of predators (Robinson et al., 2008;He et al., 2021) and also increase the natural enemy assemblages (Cloyd, 2020). ...
Sowing plants that provide food resources in orchards is a potential habitat management practice for enhancing biological control. Flowering plants (providing pollen and nectar) and grasses (providing alternative prey) can benefit natural enemies in orchards; however, little is known about their relative importance. We studied the effect of management practices (flower strips, grass strips, and spontaneous grass) on arthropod predators under organic apple management regimes in apple orchards in Beijing, China. Orchards located at two different sites were assessed for 3 years (2017–2019). The cover crops had a significant impact on the abundance and diversity of arthropod predators. The grass treatment consistently supported significantly greater densities of alternative prey resources for predators, and predators were more abundant in the grass than in the other treatments. The Shannon–Wiener diversity was significantly higher for the cover crop treatment than for the control. Community structure was somewhat similar between the grass and control, but it differed between the flower treatment and grass/control. Weak evidence for an increase in mobile predators (ladybirds and lacewings) in the orchard canopy was found. Ladybirds and lacewings were more abundant in the grass treatment than in the other treatments in 2019 only, while the aphid abundance in the grass treatment was lowest. The fact that grass strips promoted higher predator abundance and stronger aphid suppression in comparison to the flower strips suggests that providing alternative prey for predators has great biocontrol service potential. The selection of cover crops and necessary management for conserving natural enemies in orchards are discussed in this paper.
