3.1. Influence on Beneficial Entomofauna
White mustard is a pollen- and nectar-giving plant. It attracts natural enemies by providing shelter and food resources. For instance, adult hoverflies (Diptera: Syrphidae), whose larvae are natural enemies of pests (mainly aphids), feed upon the nectar and pollen [
16]. The flower pollen is a source of amino acids, carbohydrates, sugars, proteins, and other organic and inorganic substances that are indispensable for energy generation and egg laying. Furthermore, these compounds are necessary for the proper growth and development of other important aphid predators, such as lady beetles (Coleoptera: Coccinellidae) [
26]. Several authors highlighted the influence of nectar and pollen composition and flower structure on the occurrence, fecundity, and lifespan of natural enemies of pests [
27,
28], and flowering white mustard was found to be one of the plants most frequently visited by beneficial insects [
16,
18].
Table 1 presents information about the effects of white mustard proximity on beneficial invertebrates.
The presence of white mustard in broad bean inter-rows positively impacted the abundance of hoverflies [
18]. It increased the number of Syrphidae larvae on broad beans by 1-, 3-, and 5-fold in three consecutive years of study, respectively, compared to broad bean monoculture. The study also documented an increased number of eggs laid by hoverflies (by 2 eggs more/plant in the 1st year; 3 eggs more/plant in the 2nd year; and 1 more egg/plant in the 3rd year) compared to the monoculture of broad beans. Colley and Luna [
16] examined a range of flowering plant species to determine which were most attractive to aphidophagous hoverflies. They found that white mustard flowers are generally as attractive to feed as the flowers of other insectary plants. At the Oregon State University vegetable research site, mustard attracted a higher number of adult aphidophagous hoverflies (4 adults per 2 min) on the second sampling date (14 July) compared to sweet alyssum (3 adults per 2 min), buckwheat (
Fagopyrum esculentum Moench) (3 adults per 2 min), and calendula (
Calendula officinalis L.) (2.25 adults per 2 min) in bloom, with the exception of coriander (4 adults per 2 min). However, on the other sampling dates, white mustard had an intermediate visit status (1 adult per 2 min on the 1st sampling date (7 June) at the OSU site) or was relatively undervisited (on 24th July, 30th July, 13th August, 21st August, 29th August, and 2nd September) in relation to other flowers. The reason for the effect on these later dates was that after 14th July, mustard stopped blooming. At other sites (Persephone and Denison Farm), white mustard was not visited by hoverflies. The availability of other flowers may have influenced their preference. In contrast, the use of white mustard as living mulch did not enhance predatory insect abundance in zucchini (
Cucurbita pepo L.) [
29]. There was no significant variation in the mean densities of syrphids between white mustard–zucchini and monoculture zucchini plantings. The higher density of aphids present in the monoculture may have been responsible for the lack of difference in Syrphidae density. Furthermore, mustard sown one week after transplanting broccoli (
Brassica oleracea L.) did not significantly affect the number of Syrphid larvae that were preying on cabbage aphids,
Brevicoryne brassicae L. (Hemiptera: Aphididae) [
30], while white mustard sown simultaneously with broccoli increased the density of Syrphid larvae only by 14.2% compared to broccoli monoculture. In a laboratory experiment, Laubertie et al. [
31] investigated the efficacy of flowering plant species in enhancing longevity and several fecundity-related parameters of one of the most common hoverfly species,
Episyrphus balteatus Deg (Diptera: Syrphidae). The result showed very low-level performance of adult females of
E. balteatus in terms of the number of females that laid eggs (3), longevity (16 days), and duration of oviposition (2.7 days), which were fed on pollen and nectar from white mustard compared to those fed on buckwheat (number of females that laid eggs = 7; longevity = 45.30 days; mean duration of oviposition = 27.50 days); alyssum (number of females that laid eggs = 4; longevity = 31.8 days; mean duration of oviposition = 17.25 days); and coriander (number of females that laid eggs = 11; longevity = 23.7 days; mean duration of oviposition = 13 days). However, oviposition rate (46.6 eggs/day) was greatly enhanced by feeding on pollen and nectar from mustard compared to feeding on buckwheat (16.91 eggs/day), phacelia (
Phacelia secunda J.F.Gmel.) (41.30 eggs/day), coriander (19.50 eggs/day), and sweet alyssum (16.26 eggs/day).
Adding white mustard as a companion plant to broad bean plants influenced the predator–prey ratio and the number of adult lady beetles [
18]. In one year (2015) of a three-year study, the mean number of adult lady beetles per broad bean plant in treatments with white mustard was twice as high as in monoculture. However, in the two other years of study, the mean abundance of lady beetles per broad bean plant was higher in monoculture (0.094 adults/plant in 2016 and 0.219 adults/plant in 2017) compared to white mustard treatments (0.022–0.087 adults/plant in 2016 and 0.044–0.104 adults/plant in 2017). In addition, the findings showed that the number of lady beetle egg clutches laid on broad bean plants grown near mustard did not differ significantly from monoculture across the years of study. The proximity of white mustard to broad beans did not influence the dynamics of lady beetle occurrence either. The analysis of lady beetle occurrences in 2015 and 2016 indicated their relatively late appearance on broad bean plants, both cultivated in the vicinity of white mustard and in the control. However, for the whole observation period in 2017, its number stayed at a low, almost stable level. In contrast, the number of aphids per one predator in the white mustard treatments compared to the monoculture was between 1.0 and 12.0 times lower for lady beetle larvae and between 3.8 and 7.2 times lower for adult lady beetles, depending on the year of the study and the treatment, meaning that the lady beetle’s ability to reduce aphid populations was significantly higher in the mustard treatments. Other research on the influence of white mustard used as living mulch in zucchini on coccinellids showed that their mean population density was not significantly different between monoculture and white mustard–zucchini treatment at Waimanalo, Oahu, throughout the season [
29]. White mustard was destroyed by a soil-borne pathogen,
Pythium sp., before transplanting the zucchini, so a natural succession of weeds was allowed to occur. This might be the reason that there was no difference in lady beetle abundance. On the other hand, at a different site (Poamoho), the mean population density of coccinellids per zucchini leaf in monoculture was significantly higher than that on zucchini with white mustard used as living mulch.
Among the natural enemies of pests, a significant role is played by predatory bugs from the Anthocoridae (Hemiptera) family. In the beating samples (branch hit with a rubber stick, causing insects to fall into the plastic bag), Winkler et al. [
32] observed more predatory bugs,
Anthocoris nemoralis Fabr., in the 5th sampling week (approx. 4 more adults/40 beats) near flowering strips, which included
S. alba in pear (
Pyrus communis L.) orchards, compared to trees neighbored by grass strips. On other sampling weeks, the average number of adults was quite similar (1st and 6th weeks: 1 more adult/40 beats; 4th week: 1 less adult/40 beats), or they were not observed (2nd and 3rd weeks). Analogously, the authors observed more individuals of
A. nemoralis nymphs in the 4th (approx. 11 more nymphs/40 beats) and 5th weeks (approx. 2 more nymphs/40 beats) of sampling on trees adjacent to flowering plots compared to trees neighbored by grass strips. The authors did not find any
A. nemoralis nymphs, either in treatments with flowering strips or grass strips, on another three-sampling days. There was no difference in the density of
A. nemoralis nymphs between the treatments in twig samples.
Quantifying the effects of various nectar sources on parasitoid survival and fecundity provided important insight into which plant species should be retained or introduced into the agroecosystem. Wild mustard (
Sinapis arvensis L.) increased the longevity of the aphid parasitoid
Aphidius colemani Viereck (Hymenoptera: Braconidae) (2–4 days for females and 1–2 days for males) compared to the control (1–3 for females and 1 for males) [
33]. There was also a significant difference in the mean egg number laid by parasitoids between the mustard and the control (water). Mustard treatment resulted in 180 eggs per female, while the mean egg number in control was 110 eggs per female at 24 h after release. Furthermore, wild mustard inclusion resulted in an increased parasitism rate (43.3%) of green peach aphids,
Myzus persicae Sulzer (Hemiptera: Aphididae), through an increase in
A. colemani survival and egg load compared to the control (20.7%). In New Zealand, Tompkins et al. [
34] analyzed how the nectar from white mustard can affect parasitoid fitness. They observed that the provision of nectar solutions significantly increased (female: 82–85 days and male: 51–56 days) the lifespan of the parasitoid
Diadegma semiclausum Hellen. (Hymenoptera: Ichneumonidae) when compared to those fed with tap water (female: 69 days and male: 60 days). White mustard flower nectar had a great effect on the average number of parasitoids and parasitism of the Scolytus elm bark beetle,
Scolytus scolytus Fabr. (Coleoptera: Curculionidae) [
35]. In the catch trunks alongside the areas growing mustard, the numbers of parasitoids were higher (average of 5.53 parasitoids per dm
2 of bark) in the first generation than in the control (average of 2.92 parasitoids per dm
2 of bark). Similarly, in the second generation, the average number of parasitoids in the control catch trunks was only 1.66 parasitoids per dm
2 of bark, while in the catch trunks near the mustard-growing area, it was 3.12 parasitoids per dm
2 of bark. White mustard also positively affected the parasitism of the elm bark beetle. In the first generation, the parasitism of the pest in the vicinity of white mustard plants was 41.21%, while in the control catch trunks, it reached 23.06%. In the second generation, for the catch trunks near the mustard plants, there were 47.44% parasitized bark beetles, and in the control, only 29.02%. White mustard increased parasitism by
Aphidius spp. on the aphids
Metopolophium dirhodum Walker (Hemiptera: Aphididae) and
Sitobion avenae Fabricius (Hemiptera: Aphididae) on cereal crops [
36]. The results showed that the overall aphid parasitism reached 70% in cereals (wheat and barley (
Hordeum vulgare L.)) plots close to mustard cover crops and 60% in cereal plots close to grassy margins (control). Winkler et al. [
37] conducted experiments to analyze the exploitation of white mustard by
Cotesia glomerata L. (Hymenoptera: Braconidae) and
D. semiclausum, parasitoids of
Plutella xylostella L. (Lepidoptera: Plutellidae) and
Pieris spp. (Lepidoptera: Pieridae). The results indicated that when
C. glomerata was exposed to white mustard, it survived for 8–15 days, compared to 2.1 days on average in the control (exposed to water). However, provision with white mustard flowers did not increase the longevity of
D. semiclausum. The results of this study contradicted the findings of Tompkins et al. [
34] above. The difference in the results may be due to variations in temperature and humidity during the experiments. For Winkler et al. [
37], the experiment cages were placed at 22 °C with 16 h of light and 8 h of darkness and high relative humidity (90 ± 5% r.h.). On the other hand, for Tompkins et al. [
34], the cages were placed at 20 ± 2 °C with 70% relative humidity and 16 h of light and 8 h of darkness. Mustard nectar did not significantly increase the longevity of
Microctonus hyperodae Loan & Lloyd (Hymenoptera Braconidae), a parasitoid of the Argentine stem weevil,
Listronotus bonariensis Kuschel (Coleoptera: Curculionidae), compared to the water treatment [
28]. The possible reason could be that it may not be able to collect mustard nectar.
When multiple crops are grown together, crop mixtures can provide diverse plant types with easily decomposable residues that support soil biota [
38]. Studies showed that white mustard increased soil fauna activity. For instance, in the first year of study, the average number of
Amara aenea De Geer beetles (Coleoptera: Carabidae) was higher in a mustard/buckwheat/canola management system (white mustard, followed by buckwheat, followed by winter canola (
Brassica napus L.)) (78 beetles/trap) compared to all other management systems (11 beetles/trap) (oat–pea/rye–hairy vetch: spring oat (
Avena sativa L.) and field pea (
Pisum sativum L.), followed by cereal rye (
Secale cereale L.) and hairy vetch (
Vicia villosa Roth); oat–red clover: spring oat and red clover; fallow: bare fallow where weeds were controlled with tillage and no crop was grown) [
39]. The dense canopy cover of flowering mustard could serve as a good habitat in a mustard/buckwheat/canola management system. In the next year of study,
A. aenea abundance declined to near zero (
n = 4 total across all the treatments). Furthermore, carabid beetles (Coleoptera: Carabidae) were found in significantly higher numbers (4–21 beetles/m
2) on sugar beet (
Beta vulgaris L.) with white mustard compared to sugar beet with phacelia (2–17 beetles/m
2) [
40]. White mustard plots may have had more predatory arthropods because this plant left more organic material on the soil surface than phacelia. Groeneveld and Klein [
41] investigated the effect of a pennycress (
Thlaspi arvense L.)–corn double-cropping (harvesting of two crops in one calendar year) system on ground beetle diversity in comparison to three commonly applied corn rotations: mustard–corn (
Zea mays L.), green fallow (land with spontaneous natural growth)–corn and bare fallow (land remaining uncropped for a season)–corn. The results indicated that the mustard–corn rotation harbored higher ground beetle abundance in comparison with the green fallow–corn and bare fallow–corn rotation. However, the overall abundance of beetles was lower than in the pennycress–corn double cropping system.
Table 1.
Effects of white mustard on beneficial insects in different crops. Data on other mustard species are marked with relevant superscripts (1).
Table 1.
Effects of white mustard on beneficial insects in different crops. Data on other mustard species are marked with relevant superscripts (1).
Crop | Exp. Type | Duration | Benefited Organisms | Effect | Notes | Ref. |
---|
Hoverflies |
Broad bean | Field | 3 years | Syrphidae generally | Positive | Number of larval end eggs increased. | [18] |
-- | Field | 1 year | Syrphidae generally | Higher number of adult feeding visits in comparison to alyssum, buckwheat, and calendula. | [16] |
Broad bean | Greenhouse | 1 year | Episyrphus balteatus Deg. | Greater oviposition rate on mustard pollen and nectar compared to buckwheat, phacelia, coriander, and alyssum. | [31] |
Negative | Lower longevity, number of female eggs laid, and duration of oviposition compared to buckwheat, alyssum, and coriander. |
Zucchini | Field | 2 years | Syrphidae generally | No effect | Densities of adult syrphids are similar in monoculture and white mustard–zucchini intercrop. | [29] |
Broccoli | Field | 1 year | Syrphidae generally | Number of larvae increased by 14.2%. | [30] |
Lady beetles |
Broad bean | Field | 3 years | Lady beetles generally | Positive | Higher number of adults, but only in one year of study. Lower number of aphids per one predator. | [18] |
Zucchini | Field | 2 years | Lady beetles generally | No effect | Density of adult coccinellids is similar in monoculture and in treatment with mustard mulch at one site. | [29] |
Negative | Lower number of adult coccinellids in treatment with mustard at a different site. |
Anthocorids |
Pear orchard | Field | 1 year | Anthocoris nemoralis Fabr. | Positive | More nymphs and adults in beating samples. | [32] |
No effect | Density of nymphs is similar in trees adjacent to flowering strips and grass strips in twig samples. | |
Parasitoids |
-- | Laboratory | 1 year | Aphidius colemani Viereck | Positive | Longer lifespan, a higher number of eggs per female, and a higher parasitism rate. | [33] (1) |
-- | Laboratory | 1 year | Diadegma semiclausum Hellen. (Hymenoptera: Ichneumonidae) | | Increased lifespan of adults. | [34] |
Oak/hornbeam and elm | Field and laboratory | 1 year | Ecphylus silesiacus Ratz. Coeloides scolyticida Wesmael | | Higher number of parasitoids. Higher parasitism rate of the elm bark beetle. | [35] |
Cereals, wheat, and barley | Field | 1 year | Aphidius spp. | | Higher aphid parasitism than close grassy margins. | [36] |
-- | Field | 1 year | Cotesia glomerata L. | | Increased longevity. | [37] |
-- | Laboratory | 1 year | Microctonus hyperodae Loan & Lloyd | No effect | No effect on longevity. | [28] |
-- | Laboratory | 1 year | D. semiclausum | No effect on longevity. | [37] |
Epigeal and soil fauna |
Multiple cover crops | Field | 2 years | Amara aenea De Geer | Positive | Higher number of beetles in mustard/buckwheat/canola systems of management than in other systems. | [39] |
Sugar beet | Field | 2 years | Carabid beetles | Higher number of beetles compared to phacelia. | [40] |
Corn | Field | 2 years | Carabid beetles | Higher abundance of beetles in mustard–corn rotation in comparison with green fallow–corn and bare fallow–corn (however, lower compared to the pennycress–corn double cropping). | [41] |
3.2. Influence on Pests
The use of insectary plants to attract natural enemies can improve pest control through biological means. Moreover, based on the “enemy hypothesis”, the control of herbivores by their natural predators is predicted to be more effective in diversified crop environments compared to simplified ones. This is because natural predators may be more prevalent in habitats that provide a wider range of prey–host species and microhabitats for them to exploit [
42].
White mustard found wide application as a component of mixed cultivations due to its limiting effects on insect pests (
Table 2). Intercropping broad bean with white mustard increased the predation by hoverflies and lady beetles on
Aphis fabae Scop. (Hemiptera: Aphididae) [
18]. It was observed that the average number of
A. fabae on broad beans was significantly lower in treatments where mustard was present. Specifically, the counts were 2, 9, and 7 times lower in the 1st, 2nd, and 3rd years of the study, respectively, when compared to the homogeneous broad beans. According to this report, the number of aphids per hoverfly larva was 2–11 times higher in the homogenous broad bean (control) than in the white mustard treatments, depending on the treatment and the year of study. In the case of lady beetle larvae, the aphid–lady beetle larva ratio was 1–12 times lower in the vicinity of white mustard compared to the control, depending on the year of study and treatment. Likewise, the number of aphids per lady beetle adult in mustard treatments was reduced by 3.8–7.2 times compared to the control in two out of three years of the study. Similarly, it was reported that the mean number of aphids was lower in broad bean plants accompanied by white mustard in strips (1.64 aphids/plant) and in inter-rows (6.89 aphids/plant) than for monotypic cultivation (pure stand) (11.44 aphids/plant) [
43].
White mustard sown one week after transplanting broccoli tended to reduce the number of
B. brassicae [
30]. Aphid mean density in broccoli monoculture amounted to 0.31 aphids/g of fresh plant biomass, and when mustard accompanied the broccoli, it reached 0.16 aphids/g of fresh plant biomass. Mustard as living mulch can be a useful tool in controlling pests in zucchini crops [
29]. In one site, the mean number of apterous melon aphids,
Aphis gossypii Glover (Hemiptera: Aphididae), was significantly reduced in the mustard–zucchini system on specific sampling dates after zucchini transplanting, i.e., day 30 after transplanting (nearly 5 aphids/leaf), day 37 (10 aphids/leaf), day 44 (nearly 80 aphids/leaf), and day 53 (nearly 100 aphids/leaf) compared with bare ground zucchini (no mustard mulch) (nearly 15 aphids/leaf on day 30, 50 aphids/leaf on day 37, 190 aphids/leaf on day 44, and 380 aphids/leaf on day 53). White mustard had similar success in reducing the mean number of alatae aphids on the 37th day after planting (nearly 0.5 aphids/leaf), the 44th (nearly 2.5 aphids/leaf), and the 53rd (nearly 1.3 aphids/leaf) compared to bare ground zucchini (nearly 1 aphid/leaf, 3.5 aphids/leaf, and 5 aphids/leaf on the 37th, 44th, and 53rd days after planting, respectively). However, on the 30th day after planting, there was no significant difference in the density of alatae aphids between the white mustard–zucchini system and the bare ground zucchini. In other sites, the population response of apterous and alatae aphids to white mustard mulch varied.
Daniarzadeh et al. [
44] examined the influence of different trap crops on the population of
P. xylostella adults. A higher mean number of diamondback moth adults was observed in white mustard (8.74 adults/plant) compared to common cabbage (
Brassica oleracea L.) (control treatment) (1.00 adult/plant). However, the mean total number of larvae and pupa of the diamondback moth observed was higher on the control (common cabbage) (1.34 larvae plus pupa/plant) than on white mustard (1.05 larvae plus pupa/plant) during the growing season.
White mustard was also used as a trap crop, protecting cabbage from cabbage flea beetles,
Phyllotreta spp. (Coleoptera: Chrysomelidae) [
45]. The results indicated that the average indices of feeding damage by adult
Phyllotreta spp. were significantly higher (ranging from 2.2 to 4.0) in white mustard compared to cabbage (ranging from 1.9 to 3.0), depending on the study year and experiment site. A positive correlation was found between the content of epiprogoitrin (one of the glucosinolates occurring in different
Brassica species), present in white mustard leaves and flowers, and the feeding intensity of cabbage flea beetles [
46].
The use of white mustard caused a significant decrease in the development of
Meloidogyne spp. in tomato crops, with an effectiveness of 46.38% compared to the control [
47]. The mechanism by which white mustard suppresses nematodes is through the production of allelopathic compounds. Furthermore, white mustard caused up to a 57.9% reduction in the
Meloidogyne javanica Treub population in tomatoes compared to the control (without white mustard) [
48]. The results showed no significant difference between the effectiveness of white mustard and the nematicide Fenamiphos 40EC in this experiment.
Winkler et al. [
32] found no significant difference in density of pear psylla larvae,
Cacopsylla pyri L. (Hemiptera: Psyllidae), between trees adjacent to flowering strips with white mustard and trees adjacent to grass strips (control). In pear trees accompanied by flowering strips, the average population density of
C. pyri larvae was highest in weeks 24 (190 larvae/20 twigs) and 25 (200 larvae/20 twigs), decreased in week 26 (115 larvae/20 twigs), and reached extremely low levels in weeks 28 and 29. In pear trees adjacent to grass strips, there were 180 larvae/20 twigs in week 24, 160 larvae/20 twigs in week 25, and 110 larvae/20 twigs in week 27. Moreover, there were no significant differences in the severity of squash silverleaf,
Bemisia argentifolii Bellows and Perring (Hemiptera: Aleyrodidae), disorder on zucchini plants between monoculture and white mustard treatments [
29].
Table 2.
Effect of white mustard on pests in different crops.
Table 2.
Effect of white mustard on pests in different crops.
Crop | Exp. Type | Duration | Notes | Ref. |
---|
Positive effect |
Broad bean | Field | 3 years | Reduced abundance of Aphis fabae Scop. Reduced aphid–hoverfly larvae/lady beetle larvae/lady beetle adult ratio. | [18] |
2 years | Reduced abundance of Aphis fabae Scop. | [43] |
Zucchini | Field | 2 years | Reduced number of Aphis gossypii Glover. | [29] |
Cabbage | Field | 1 year | Reduced number of Brevicoryne brassicae L. | [30] |
1 year | Higher number of adult Plutella xylostella L. compared to cabbage. | [44] |
2 years | Higher index of feeding damage by adult Phyllotreta spp. than on the cabbage. | [45] |
Tomato | Greenhouse | 3 years | Reduced infestation by Meloidogyne spp. | [47] |
1 year | Reduced population of Meloidogyne javanica Treub. | [47] |
No effect |
Pear orchard | Field | 1 year | Density of Cacopsylla pyri L. larvae on trees near flowering strips, including white mustard, is similar to trees near grass strips. | [32] |
Zucchini | Filed | 2 years | No differences in the mean ratings of silverleaf, Bemisia argentifolii Bellows and Perring, symptoms on zucchini among monoculture and white mustard treatments. | [29] |
Negative effect |
Cabbage | Field | 1 year | Higher number of larvae and pupa of Plutella xylostella L. on the cabbage compared to white mustard used as a trap crop. | [44] |