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Article

Intraspecific and Interstage Similarities in Host-Plant Preference in the Diamondback Moth (Lepidoptera: Plutellidae)

by
Francisco Rubén Badenes-Pérez
1,2,* and
David G. Heckel
1,*
1
Max Planck Institute for Chemical Ecology, 07745 Jena, Germany
2
Instituto de Ciencias Agrarias, Consejor Superior de Investigaciones Científicas, 28006 Madrid, Spain
*
Authors to whom correspondence should be addressed.
Horticulturae 2023, 9(1), 39; https://doi.org/10.3390/horticulturae9010039
Submission received: 29 November 2022 / Revised: 19 December 2022 / Accepted: 24 December 2022 / Published: 31 December 2022
(This article belongs to the Special Issue Implementation of IPM Measures in Vegetable Cropping Systems)
Browse Figure
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Abstract

:
The diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), is an important insect pest of cruciferous crops. Understanding its preference patterns can lead to more efficient management methods, such as trap crops. Several strains of P. xylostella were used to test whether there were differences in oviposition preference in a four-choice setting, on abaxial versus adaxial leaf surfaces in 28 different plant species, and on substrates with different concentrations of sinigrin (allylglucosinolate). Additionally, the larval preference of P. xylostella was studied with 17 plant species of known glucosinolate content that were compared to Arabidopsis thaliana L. in two-choice tests. Our research shows that the diet on which P. xylostella has fed hardly affects multiple-choice host-plant preference, abaxial and adaxial oviposition preference, or oviposition response to pure glucosinolates. Our study also shows that glucosinolate content affects larval preference, which together with the known correlation between glucosinolate content and P. xylostella oviposition, indicates that crops with high glucosinolate content could be more susceptible to damage by P. xylostella than crops with low glucosinolate content. These findings are discussed in regards to their significance in the management of P. xylostella.

1. Introduction

The diamondback moth Plutella xylostella L. (Lepidoptera: Plutellidae) is considered one of the most damaging insect pests of cruciferous vegetables [1,2]. Management of P. xylostella is mostly through using insecticides [3,4,5,6], but the ability of P. xylostella to develop resistance to insecticides, combined with concerns on the negative effects of insecticide use, have stimulated interest in developing alternative management techniques such as trap crops and host-plant resistance [7,8,9].
The host range of P. xylostella includes mainly glucosinolate-containing plants in the family Brassicaceae [7,10,11]. Larvae of P. xylostella have sulfatases that allow them to desulphate glucosinolates [12], and glucosinolates and their hydrolysis products have been shown to be oviposition and feeding stimulants for adults and larvae, respectively [10,13,14,15,16,17]. However, different strains of P. xylostella show differences in adaptation to different diets and host-plants and, in several cases, it has been shown that P. xylostella can use plants outside the family Brassicaceae as host-plants [10,18,19,20]. For example, in Kenya, larvae of P. xylostella were found feeding on plants of the pea Pisum sativum L. (Fabaceae), adjacent to a cabbage field that had been heavily infested by the insect [21]. In a study conducted with 30 different plant species, plant glucosinolate content was shown to increase oviposition and larval survival in different P. xylostella strains reared on cabbage (DBM-C) and on two glucosinolate-free diets, either artificial wheat-casein diet (DBM-G88) or pea leaves (DBM-P) [10]. However, it is unknown if in P. xylostella, larval preference is equally influenced by glucosinolates as in the case of oviposition preference. In field experiments, densities of larvae of P. xylostella were higher in lines of Arabidopsis thaliana L. and Brassica oleracea L. (Brassicaceae) with higher glucosinolate content [22,23]. However, on other studies conducted with A. thaliana and B. oleracea, the performance of P. xylostella larvae could not be explained by glucosinolate content [24,25,26,27], and one study conducted with Brassica rapa L. (Brassicaceae) found that herbivory by P. xylostella larvae increased with glucosinolate content up to an intermediate maximum, decreasing thereafter [28]. Larvae of P. xylostella can move among adjacent plants and some neonates can travel distances of more than 1 m [29].
Different lepidopteran populations of the same species can show different oviposition preferences [30,31]. In P. xylostella, host-plant use can also be affected by previous experience, which can be used to induce oviposition on non-host plants [32,33,34,35]. Two-choice tests conducted comparing 30 plant species to A. thaliana on the DBM-C, DBM-G88, and DBM-P strains of P. xylostella showed that, overall, they had similar oviposition preferences [10]. However, the response of different strains could differ when offered more than two host-plants in oviposition preference tests. Offering multiple host-plants to P. xylostella simultaneously can alter host-finding behavior and reduce oviposition [36]. Furthermore, it is unknown if there could be within-plant differences in oviposition preference, such as abaxial versus adaxial, among P. xylostella strains reared on very different diets.
The main goal of this research was to compare host-plant preference among different P. xylostella strains and between larvae and ovipositing adults. For this purpose, we collected abaxial and adaxial oviposition data on 28 plant species, using the P. xylostella strains DBM-C, DBM-G88, and DBM-P, to test if these could differ among the different strains. Furthermore, multi-preference oviposition tests were conducted with these and two additional P. xylostella strains reared on rape (DBM-W and DBM-NOQA). These multi-preference experiments were conducted to test if there were differences among the different strains in a setting with three different oviposition substrates besides the plant on which the insects were reared. As pure individual glucosinolates have also been shown to act as oviposition stimulants in P. xylostella [20,37,38,39], here we also compared the oviposition response of the strain DBM-C and the strain DBM-G88 (the strain that has been reared the longest without glucosinolates) to different concentrations of the pure glucosinolate sinigrin (allylglucosinolate). We hypothesized that P. xylostella could lose its ability to detect pure glucosinolates after many generations without glucosinolate exposure in its diet. Furthermore, using 18 different plant species of known glucosinolate content, we tested whether larval preference is influenced by glucosinolate content and if larval preference is correlated to oviposition preference in P. xylostella. Understanding the preference of P. xylostella may lead to more effective trap crops.

2. Materials and Methods

2.1. Plant Species and Plutella xylostella Strains Tested

The plants used in the experiments are shown on Table 1. Among the 28 plant species tested, 20 belong to 11 subfamilies in the family Brassicaceae, and 7 belong to the families Caricaceae, Cleomaceae, Gyrostemonaceae, Limnanthaceae, Moringaceae, Resedaceae, and Tropaeolaceae (order Brassicales) [40] (Table 1). Additionally, P. sativum was used as a control plant without glucosinolates. Seeds of A. thaliana Columbia-0 and G-type Barbarea vulgaris R.Br. were provided by the Nottingham Arabidopsis Stock Centre at Sutton Bonington, UK, and by Dr. Niels Agerbirk, respectively. Seeds of Alyssum argenteum All. were purchased from Jelitto (Schwarmstedt, Germany). Seeds of Brassica napus L. and Nasturtium officinale W. T. Aiton were purchased from Rieger-Hofmann GmbH (Blaufelden-Raboldshausen, Germany). Seeds of the collards Brassica oleracea var. acephala, cultivar Green Glaze, which produces glossy and waxy plants, were purchased from Pennington Seed (Madison, GA, USA). Seeds of Cardamine pratensis L. and Iberis amara L. were purchased from Rühlemann’s (Horstedt, Germany). All other seeds, including also those of cabbage, B. oleracea var. capitata cultivar Gloria, and pea, P. sativum cultivar Oregon Sugar Pod, were purchased from B & T World Seeds (Aigues-Vives, France). Arabidopsis thaliana plants were grown in a climate chamber (10:14 h light:dark, 21 ± 2 °C and 55 ± 5 RH). The other plant species were grown in a greenhouse (16:8 h light:dark, 25 ± 3 °C). Plants were grown in 7 × 7 × 8 cm pots containing a substrate of peat moss and clay, and fertilized every two weeks with an all-purpose fertilizer (Ferty® 3, Planta Düngemittel GmbH, Regenstauff, Germany). Plants were 5- to 6-weeks-old at the beginning of the experiments.
Five strains of P. xylostella were used in the experiments. Two strains came from Kenya, one (DBM-C) was collected in a cabbage field in 2002, and the other (DBM-P) was collected in a pea field in 2000, and since collection they were continually reared on cabbage and pea plants, respectively. Another strain (DBM-G88) was collected in 1988 in Geneva, NY, USA, and since then was reared on a wheat germ-casein artificial diet [41]. Two additional strains were reared on rape, a field selected strain resistant to Bacillus thuringiensis toxin Cry 1Ac (DBM-NOQA) [42] and a strain collected near Adelaide, Australia in 1987 and maintained in the laboratory feeding on rape at the Waite Agricultural Research Institute [43]. Insects of the strains DBM-C and DBM-P were donated to us by Dr. Bernhard Löhr, while insects of the strains DBM-G88 and DBM-NOQA were donated to us by Drs. Anthony Shelton and Bruce Tabashnik, respectively. Insects of the DBM-W strain were obtained from the Waite Institute at the University of Adelaide, Australia. Insects were reared in environmental growth chambers (16:8 h light:dark, 21 ± 2 °C and 55 ± 5 RH). Throughout the experiments, the number of individuals of each strain was always >250. Insects of these five P. xylostella strains completed at least 14 generations per year on the diet and conditions on which they were reared. Before carrying out the experiments described here, insects were continuously and exclusively feeding on cabbage (DBM-C), on artificial diet (DBM-G88), on peas (DBM-P), and on B. napus (DBM-NOQA and DBM-Waite) for more than 100 generations.

2.2. Multiple-Choice Oviposition Preference Experiments

Multiple-choice oviposition preference experiments were conducted with one cabbage plant, one pea plant, one rape plant, and one strip of aluminium foil (approximately 2.5 × 12.0 cm). The strip of aluminium foil was placed in the center of a Petri dish (9 cm diameter), and it had previously been dipped into autoclaved cabbage juice (65 g of cabbage in 500 mL of water), as in Shelton et al. [41]. Three 1.5-mL samples of this autoclaved cabbage juice were analyzed to check if they contained any glucosinolates. Glucosinolate content of these cabbage juice samples was determined following the procedure described in Badenes-Pérez et al. [16] and no glucosinolates were detected. The multiple-choice oviposition experiments were conducted in screened cages 60 × 60 × 60 cm. Multiple cages were used, each of which was considered a replicate. In each cage, the four possible oviposition substrates (one potted plant of each cabbage, rape, and pea, and the Petri dish with aluminium foil), were placed at a distance of approximately 20 cm from the middle of the cage, leaving approximately 28 cm between adjacent oviposition substrates. Three pairs of P. xylostella moths (three females and three males, <3 days old) were released in each cage. To provide a food source for them, a small plastic cup with a 10% sugar solution on cotton was placed in the middle of each cage. The experiment was replicated five times for each of the insect strains. Two days after releasing the moths, the number of eggs on each plant was counted.

2.3. Abaxial vs. Adaxial Preference

Oviposition experiments to determine P. xylostella preference for abaxial vs. adaxial leaf surfaces in each plant species were conducted in two-choice experiments in comparison with A. thaliana (i.e., one plant of any of the tested types versus one plant of A. thaliana). The experimental arenas were screened cages 32.5 × 32.5 × 32.5 cm. Multiple cages were used for replication. Two pairs of moths (<3 days old) were released in each cage, which contained a small plastic cup with a 10% sugar solution on cotton to feed the moths. The experiment was replicated at least three times for each insect strain and plant comparison. Two days after releasing the insects, the number of eggs on each plant was counted and the location where eggs were found on the leaves (either abaxial or adaxial side) was recorded.
When moths approach a plant to oviposit, the adaxial side of the leaves is more exposed to the insects than the abaxial side, so an additional experiment was conducted with detached A. thaliana leaves to remove this effect. In this experiment, two leaves of similar size (approximately 4.5 cm long) were placed horizontally, parallelly aligned, and 2 cm apart in the center of a 9 cm Petri dish. Of these two leaves, one was placed with the abaxial side facing upwards and the other one was placed with the adaxial side facing upwards. Leaves were secured in this position by attaching them to the bottom of the Petri dish with transparent 1.9 cm wide ScotchTM tape (3M, Minneapolis, MN, USA) that covered approximately 1 mm of the two margins of the leaf at opposite sides of the midrib. The Petri dish was placed in the center of a screened cage (32.5 × 32.5 × 32.5 cm) and one pair of moths (<3 days old) of the strain DBM-C was released in each cage, which contained a small plastic cup with a 10% sugar solution on cotton to feed the moths. Multiple cages with each with one Petri dish each containing the two A. thaliana leaves were used, each of which was considered a replicate. The experiment was replicated 20 times. One day after releasing the insects, the number of eggs on each plant was counted.

2.4. Oviposition Preference Experiments with Sinigrin

Oviposition preference was also studied using different concentrations of sinigrin in pure form. These tests were conducted with DBM-C and DBM-G88, the latter being the P. xylostella strain that had been feeding on glucosinolate-free diet for the longest time. Pure sinigrin (Acros Organics, Geel, Belgium) was applied in 160 µL solutions in HPLC-grade water to one fourth of a 90 mm diameter Whatman® filter paper disk (Whatman International Ltd., Maidstone, UK). The tip of each fourth filter paper section was cut by 0.5 cm to avoid contact between the two pieces of filter paper that were placed opposed to each other on a Petri dish (9 cm diameter). Treatments were randomly assigned, and multiple Petri dishes were used, each of which was considered a replicate. Concentrations of sinigrin were compared in the following two-choice comparisons: 10−7 vs. 10−6 M, 10−6 vs. 10−5 M, 10−5 vs. 10−4 M, 10−4 vs. 10−3 M, and 10−3 vs. 10−2 M. One pair of moths were placed in each Petri dish. The numbers of eggs laid on each of the filter paper sections were counted one day after releasing the moths. The experiment was replicated 3–17 times for each comparison of glucosinolate concentrations and only replicates in which two or more eggs were laid on the filter paper were considered.

2.5. Larval Preference Experiments

Two-choice experiments were conducted to compare preference of 3rd instar DBM-C larvae between A. thaliana and each of the 18 plant species tested. Plants were cut from the crown so only foliage was offered to the larvae. Plants were placed randomly on opposite sides of a plastic container that was used as experimental arena, at about 5 cm from the center of the container. A total of 5 larvae were placed in the center of the experimental arena and their preference was assessed after 24 h by recording on what plant type each larva was found. The experiment was replicated 4–10 times for each comparison between A. thaliana and the other plant species. The experimental arenas were 22.0 × 28.0 × 18.0 cm plastic boxes with a modified lid with a mesh to allow air into the box. Multiple boxes were used, each of which was considered a replicate. A larval preference index (LPI) was calculated as the number of larvae found on each individual plant plus one divided by the number of larvae found on the A. thaliana plant that it was compared with in the same box plus one. A LPI = 1 indicated no difference in larval preference between A. thaliana and the alternative plant species it was compared with; a LPI < 1 indicated that A. thaliana would tend to be preferred; and a LPI > 1 indicated that larvae of P. xylostella would tend to prefer the alternative plant species over A. thaliana. LPI data were compared to data on an oviposition preference index (OPI) that had been calculated in previous research with plants of the same species and age [10]. This allowed us to calculate the correlation between LPI and OPI. Data on glucosinolate content for plants of the same species and age were also taken from Badenes-Pérez et al. [10]. Glucosinolates were grouped as aliphatic with sulfur-containing side chains (AS), other aliphatic (AO), benzenic (BEN), and indolic (IN). In order to take into account the effect of the diversity of glucosinolates in each plant species, we used the number of different glucosinolates per plant species (glucosinolate richness, S) and a glucosinolate complexity index (GCI), similar to the previously proposed chemical complexity index [44,45]. The GCI was calculated as the sum of the Shannon’s diversity index from the four chemical classes of glucosinolates (HA) and the Shannon’s diversity index from the relative concentrations of all individual glucosinolates (HB) [10,44].

2.6. Statistical Analysis

For each P. xylostella strain, differences in oviposition preference in multi-choice tests were analyzed using a Kruskal–Wallis test (p ≤ 0.05) with SPSS® version 24. The significance values of Kruskal–Wallis tests were adjusted by the Bonferroni correction for multiple tests. Data comparing larval preference, oviposition preference between abaxial and adaxial leaf surfaces, and oviposition preference between substrates with concentrations of sinigrin were analyzed using a one-tailed, two-sample test of proportions using STATA® version 15.1 with significance at p ≤ 0.05. Kruskal–Wallis tests and tests of proportions were performed with untransformed data. Correlations between LPI and glucosinolate content and glucosinolate diversity as well as between LPI and OPI were performed using a two-tailed Spearman’s correlation with SPSS®.

3. Results

3.1. Multiple-Choice Oviposition Preference Experiments

For the four P. xylostella strains tested (DBM-W, DBM-NOQA, DBM-C, and DBM-P) there were significant differences in oviposition preference among the four possible oviposition substrates (cabbage, rape, pea, and aluminum foil) (p ≤ 0.05) and rape was the most preferred host-plant, while pea and aluminium foil were the least preferred oviposition substrates (Figure 1, Table S1). Unlike the other three P. xylostella strains tested, for the strain DBM-NOQA, oviposition on rape and on aluminium foil was not significantly different.

3.2. Abaxial vs. Adaxial Preference

When comparing the three P. xylostella strains tested (DBM-C, DBM-G88, and DBM-P), there were no significant differences in oviposition preference in terms of abaxial versus adaxial oviposition in each of the plants tested (p ˃ 0.05) (Table S2). When analyzing each strain separately for each plant type, preference for adaxial surfaces occurred in A. argenteum, waxy B. oleracea var. acephala, and I. amara in the three P. xylostella strains (Table 2). A preference for adaxial surfaces was also observed in glossy B. oleracea var. acephala for DBM-C and DBM-G88; in L. douglasii for DBM-C; in S. officinale for DBM-G88; and in C. spinosa, E. cheiri, P. sativum, and R. odorata for DBM-P. Preference for abaxial surfaces was only found in C. bursa-pastoris and T. majus for DBM-P. For the other plant species tested, differences in oviposition preference between abaxial and adaxial leaf surfaces were not statistically significant (p > 0.05). The experiment with detached leaves of A. thaliana showed no significant differences between abaxial and adaxial oviposition (Table 2).

3.3. Oviposition Preference Experiments with Sinigrin

For the two strains of P. xylostella tested, DBM-G88 and DBM-C, moths always laid more eggs on the filter paper with higher concentrations of sinigrin (Table 3).

3.4. Larval Preference Experiments

Larvae of P. xylostella preferred B. juncea and S. officinale over A. thaliana, while A. thaliana was preferred over A. argenteum, C. bursa-pastoris, M. oleifera, P. sativum, and R. odorata (Table 4). In the set of plant species tested, LPI and OPI were positively correlated, and LPI was positively correlated with the glucosinolate diversity indexes S, HA, and GCI, as well as to total content of glucosinolates and one type of aliphatic glucosinolates (AO) (Table 5 and Table S3). For these plant species, OPI was positively correlated to the same parameters as LPI and, additionally, it was positively correlated to IN and AS.

4. Discussion

The tested strains of P. xylostella had overall similar oviposition preferences in multi-choice tests and in abaxial/adaxial leaf surfaces. This and previous research [9] shows that, overall, the diet on which P. xylostella has fed hardly affects oviposition preference between plants. This indicates that in P. xylostella, preimaginal conditioning does not significantly affect oviposition preference in adults, as it has also been shown in other insects as opposed to what would be expected from the Hopkins’ host-selection principle by which insects demonstrate a preference for the host species on which they have developed [46,47]. This also shows that in P. xylostella there seems to be a strong selection for following particular cues for ovipositing on plants and that these are not affected by long-term diet and host-plant exposure. Among these oviposition preference cues, glucosinolate content seems to be an important one, which is shown by the correlation found between host-plant glucosinolate content and oviposition [10] as well as by the preference for higher concentrations of sinigrin shown here with the strains DBM-C and DBM-G88. The resistance of DBM-NOQA to B. thuringiensis Cry 1Ac toxin also did not affect oviposition preference in the tests in which this P. xylostella strain was used.
Although there were no significant differences in abaxial and adaxial oviposition among the P. xylostella strains tested, oviposition occurred preferentially on the adaxial leaf surface, except in C. bursa-pastoris and T. majus in the case of the DBM-P strain, which mostly laid the eggs on the abaxial surface of these host-plants. Abaxial and adaxial preference can also influence management of P. xylostella. For example, some insecticide sprayers deposit more insecticide on the adaxial than on the abaxial leaf surface [48,49]. Rainfall and sprinkler irrigation can also wash off eggs and larvae of P. xylostella [11,50,51,52,53] and in cabbage, P. xylostella egg susceptibility to rainfall is higher on the adaxial than on the abaxial leaf surface [53]. It is unknown why P. xylostella shows these oviposition preferences for either adaxial or abaxial surfaces depending on the plant species. The plant cuticle can play an important role in insect-plant interactions [54]. Insects use plant secondary metabolites as ’fingerprints’ to recognize host-plants and oviposit on them [55,56,57]. Although plants may contain sufficient amounts of glucosinolates on the leaf surface to be perceived by P. xylostella, higher concentrations (2- to 10-fold) of glucosinolates on the plants Barbarea rupicola Moris and Barbarea verna (Mill.) Asch. (Brassicaceae) were not correlated with oviposition preference for either leaf surface [38]. Similarly, in A. thaliana, despite differences in glucosinolate content between abaxial and adaxial leaf surfaces [58], we found no oviposition preference differences in P. xylostella for any of the leaf sides. Glucosinolates are not the only plant compounds active as oviposition stimulants for P. xylostella and other specialists of Brassicaceae [7,14,59]. Waxes can also affect P. xylostella oviposition [60,61,62]. Trichome density, which has been shown to affect oviposition preference in P. xylostella [63], could also be different between the abaxial and adaxial of the plants tested. Moreover, the rugosity of the surface can increase the ovipositional preference of P. xylostella [20] and, in general, defense from natural enemies has also been shown to affect oviposition preference in insects [64,65,66]. The green leaf volatile (Z)-3-hexenyl acetate has also been shown to be an attractant to mated P. xylostella females [67], and this and other green leaf volatiles make P. xylostella oviposit preferentially on the adaxial leaf side of Brassica rapa var. perviridis L. (Brassicaceae) [68].
Pure glucosinolates have been shown to have a quantitative effect on P. xylostella oviposition, which oviposits more on substrates with higher concentrations of glucosinolates than on substrate with lower glucosinolate concentrations [16,38]. Here the DBM-C and DBM-G88 strains behaved similarly in preferring the higher concentrations of sinigrin. However, moths of the DBM-P did not oviposit at all on the substrate with the lowest concentration of sinigrin (10−7 M) and this could indicate that they have lost some sensitivity to detect glucosinolates after long-term rearing without glucosinolate exposure.
In our study there was a positive correlation between LPI and OPI. Besides being correlated, both OPI and LPI responded similarly to glucosinolate content and glucosinolate diversity in the plants tested, except for AS and IN content, which was significantly correlated with OPI but not with LPI. This could indicate that AS and IN content is less important for host-plant choice in P. xylostella larvae than for adults, at least when considering the set of plant species tested. Two isothiocyanates derived from glucoiberin and glucoraphanin (AS) have been shown to be oviposition stimulants for P. xylostella [14]. However, larvae of P. xylostella are also known to be stimulated by glucoiberin and glucobrassicin [13], which are AS and IN, respectively, and herbivory by P. xylostella decreased in A. thaliana mutants with reduced AS and IN content compared to wildtype A. thaliana plants with higher AS and IN content [25]. Besides glucosinolates, flavonoids have also been shown to act as feeding stimulants for larvae of P. xylostella [13].
Our results with P. xylostella larvae and adults, together with previously known oviposition and survival data [10], indicate that plants with higher glucosinolate content are likely to be more attractive to P. xylostella. Even though glucosinolates can provide some degree of resistance against generalist insects [69,70,71,72], in locations where P. xylostella is abundant, using crop varieties that have low glucosinolate content could reduce damage by this insect. On the other hand, the preference of P. xylostella for host-plants with high glucosinolate content should be taken into account in the choice of trap crops to be deployed for the management of this insect.

5. Conclusions

The tested strains of P. xylostella had, overall, very similar oviposition preferences in four-choice tests, in abaxial/adaxial leaf sides, and in substrates with different concentrations of sinigrin. In four-choice tests, the preferred host was B. napus and the least preferred host was P. sativum. Preference for adaxial leaf surfaces occurred in A. argenteum, waxy B. oleracea var. acephala, and I. amara in the three P. xylostella strains tested. Preference for adaxial leaf surfaces was also observed in glossy B. oleracea var. acephala for DBM-C and DBM-G88; in L. douglasii for DBM-C; in S. officinale for DBM-G88; and in C. spinosa, E. cheiri, P. sativum, and R. odorata for DBM-P. Preference for abaxial leaf surfaces was only found in C. bursa-pastoris and T. majus for DBM-P. For the other plant species tested, differences in oviposition preference between abaxial and adaxial leaf surfaces were not significant. The two P. xylostella strains tested with sinigrin, DBM-G88 and DBM-C, preferred to oviposit on the substrates with higher concentrations of sinigrin. Host-plant preference in P. xylostella larvae and ovipositing adults were positively correlated and both larvae and ovipositing moths responded similarly to glucosinolate content and glucosinolate diversity, except for AS and IN content, which for the plants tested, was significantly correlated with oviposition preference, but not with larval preference.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae9010039/s1, Table S1: Test statistic and p-values of Kruskall–Wallis tests comparing differences in oviposition on four different oviposition substrates (cabbage, rape, pea, and aluminium foil) for the strains DBM-W, DBM-NOQA, DBM-C, and DBM-P of P. xylostella. The significance values have been adjusted by the Bonferroni correction for multiple tests. Significant p-values (p ≤ 0.05) are shown in bold type; Table S2: Comparison of the preference between abaxial and adaxial leaf surfaces among the three P. xylostella strains reared on cabbage (DBM-C), artificial diet (DBM-G88), and pea (DBM-P). Oviposition preference data were analyzed using a one-tailed, two-sample test of proportions (p ≤ 0.05) comparing the percentages of the total number of eggs laid on the abaxial side of leaves (n = 3–96, except in the case of C. papaya for DBM-C, where n = 2).; and Table S3: Total glucosinolate content (TOT) and content of aliphatic glucosinolates with sulfur-containing side chains (AS), other aliphatic glucosinolates (AO), benzenic glucosinolates (BEN), and indolic glucosinolates (IN) for each of the plant types tested (A). Glucosinolate richness (S), Shannon’s diversity index for the four glucosinolate classes (HA), Shannon’s diversity index for the relative concentrations of all individual glucosinolates (HB), and chemical complexity index for glucosinolates (CCI) for each of the plant types tested (B). Values based on means across replicates taken from Badenes-Pérez et al. 2020 [10].

Author Contributions

F.R.B.-P. and D.G.H. conceived and designed the research. F.R.B.-P. conducted the experiments, analyzed the data, and wrote the paper. All authors have read and agreed to the published version of the manuscript.

Funding

Open Access funding provided by the Max Planck Society.

Data Availability Statement

The data that support the findings of this study are available from the lead author upon reasonable request.

Acknowledgments

We thank Jutta Steffen and Christin Heinrich, for insect rearing or technical assistance during the experiments, Birgit Hohmann for help cultivating plants, Michael Reichelt and Jonathan Gershenzon for help with glucosinolate analysis, Anthony M. Shelton, Bernhard Löhr, and Bruce Tabashnik for providing P. xylostella insects, and Niels Agerbirk for providing B. vulgaris seeds.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Horticulturae 09 00039 g001 550
Figure 1. Mean ± SE eggs laid by P. xylostella strains DBM-W, DBM-NOQA, DBM-C, and DBM-P in a multi-choice setting consisting of cabbage, rape, pea, and aluminium foil. Significant differences (p ≤ 0.05) in oviposition preference of each P. xylostella strain are shown with different lowercase letters.
Figure 1. Mean ± SE eggs laid by P. xylostella strains DBM-W, DBM-NOQA, DBM-C, and DBM-P in a multi-choice setting consisting of cabbage, rape, pea, and aluminium foil. Significant differences (p ≤ 0.05) in oviposition preference of each P. xylostella strain are shown with different lowercase letters.
Horticulturae 09 00039 g001
Table
Table 1. Plants used in the different experiments conducted to determine abaxial vs. adaxial oviposition preference (AA) and larval preference (LP).
Table 1. Plants used in the different experiments conducted to determine abaxial vs. adaxial oviposition preference (AA) and larval preference (LP).
FamilySpeciesCommon NameExperiment
BrassicaceaeAethionema cordifolium DC.Lebanon stone cressAA
BrassicaceaeAlyssum argenteum All.Yellow tuftAA, LP
BrassicaceaeArabidopsis thaliana (L.) Heynh.Thale cressAA
BrassicaceaeArabis caucasica Willd.Mountain rock cressAA, LP
BrassicaceaeBarbarea vulgaris R.Br.WintercressAA
BrassicaceaeBiscutella laevigata L.Buckler mustardAA
BrassicaceaeBrassica juncea (L.) Czern.Indian mustardAA, LP
BrassicaceaeBrassica napus L.CanolaAA
BrassicaceaeBrassica oleracea var. capitata L.CabbageAA
BrassicaceaeBrassica oleracea var. acephala L.Glossy collard greensAA
BrassicaceaeBrassica oleracea var. acephala L.Waxy collard greensAA
BrassicaceaeBunias orientalis L.Turkish rocketAA
BrassicaceaeCapsella bursa-pastoris (L.) Medik.Shepherd’s purseAA, LP
BrassicaceaeCardamine pratensis L.Cuckoo flowerAA
BrassicaceaeDiplotaxis muralis (L.) DC.Annual wall rocketAA, LP
BrassicaceaeEruca sativa Mill.Arugula, rucolaAA, LP
BrassicaceaeErysimum cheiri (L.) CrantzWallflowerAA, LP
BrassicaceaeIberis amara L.Bitter candytuftAA, LP
BrassicaceaeLepidium sativum L.Garden cressAA; LP
BrassicaceaeNeslia paniculata (L.) Desv.Ball mustardAA
BrassicaceaeNasturtium officinale W. T. AitonWatercressAA
BrassicaceaeSisymbrium officinale (L.) Scop.Hedge mustardAA, LP
CaricaceaeCarica papaya L.PapayaAA, LP
CleomaceaeCleome spinosa L. Spider flowerAA, LP
FabaceaePisum sativum L.PeaAA, LP
GyrostemonaceaeCodonocarpus cotinifolius (Desf.) F.Muell.Bell-fruit treeAA
LimnanthaceaeLimnanthes douglasii R. Br.Douglas’ meadowfoamAA
MoringaceaeMoringa oleifera Lam.Drumstick treeAA, LP
ResedaceaeReseda odorata L.Common mignonetteAA, LP
TropaeolaceaeTropaeolum majus L.Garden nasturtiumAA, LP
Table
Table 2. Two-choice preference between abaxial and adaxial leaf surfaces shown as the percentage of eggs laid abaxially (mean ± SE) in each of the tested plants in three P. xylostella strains reared on cabbage (DBM-C), artificial diet (DBM-G88), and pea (DBM-P). Data on the differences between the percentages of eggs laid abaxially and adaxially were analyzed using a one-tailed, two-sample test of proportions (p ≤ 0.05). The test compared the percentages of eggs laid abaxially and adaxially for each plant type and P. xylostella strain (n = 3–96, except in the case of C. papaya and M. oleifera, and for DBM-C, N. paniculata for DBM-G88, and R. odorata for DBM-P in which n = 2). Significant p-values are shown in bold type. The experiment with detached leaves of A. thaliana is shown as “A. thaliana, detached”.
Table 2. Two-choice preference between abaxial and adaxial leaf surfaces shown as the percentage of eggs laid abaxially (mean ± SE) in each of the tested plants in three P. xylostella strains reared on cabbage (DBM-C), artificial diet (DBM-G88), and pea (DBM-P). Data on the differences between the percentages of eggs laid abaxially and adaxially were analyzed using a one-tailed, two-sample test of proportions (p ≤ 0.05). The test compared the percentages of eggs laid abaxially and adaxially for each plant type and P. xylostella strain (n = 3–96, except in the case of C. papaya and M. oleifera, and for DBM-C, N. paniculata for DBM-G88, and R. odorata for DBM-P in which n = 2). Significant p-values are shown in bold type. The experiment with detached leaves of A. thaliana is shown as “A. thaliana, detached”.
% Abaxial Oviposition as Mean ± SE, Test Statistic, and p-Value
DBM-CDBM-G88DBM-P
A. cordifolium11.15 ± 4.41, z = 2.70, p = 0.003 *11.98 ± 4.75, z = 2.63, p = 0.004 *8.71 ± 4.15, z = 2.84, p = 0.002 *
A. argenteum4.87 ± 2.23, z = 3.12, p ≤ 0.001 *4.11 ± 1.29, z = 3.19, p ≤ 0.001 *1.40 ± 0.95, z = 3.39, p ≤ 0.001 *
A. thaliana53.41 ± 1.66, z = 0.95, p = 0.17250.00 ± 1.25, z = 0.00, p = 0.50050.33 ± 0.11, z = 0.09, p = 0.464
A. thaliana, detached57.34 ± 4.47, z = 0.92, p = 0.178--
A. caucasica60.83 ± 4.67, z = 0.76, p = 0.22352.72 ± 7.43, z = 0.21, p = 0.41831.12 ± 8.16, z = 1.32, p = 0.094
B. vulgaris50.38 ± 11.71, z = 0.00, p = 0.50052.22 ± 3.68, z = 0.14, p = 0.44558.84 ± 4.61, z = 0.62, p = 0.266
B. laevigata56.33 ± 4.28, z = 0.34, p = 0.41656.99 ± 3.04, z = 0.49, p = 0.31443.55 ± 5.82, z = 0.42, p = 0.339
B. juncea52.09 ± 6.11, z = 0.14, p = 0.44564.76 ± 2.64, z = 0.24, p = 0.40337.10 ± 3.20, z = 0.21, p = 0.418
B. napus53.06 ± 8.35, z = 0.21, p = 0.41844.99 ± 5.25, z = 0.35, p = 0.36538.24 ± 8.10, z = 0.83, p = 0.203
B. oleracea (cabba.)32.90 ± 11.86, z = 1.18, p = 0.11935.33 ± 11.43, z = 1.04, p = 0.14939.68 ± 15.71, z = 0.49, p = 0.312
B. oleracea (g. co.)17.62 ± 3.31, z = 2.22, p = 0.013 *21.20 ± 3.80, z = 2.01, p = 0.022 *30.10 ± 5.39, z = 1.39, p = 0.083
B. oleracea (w. co.)4.17 ± 4.17, z = 3.19, p ≤ 0.001 *19.53 ± 9.99, z = 2.08, p = 0.019 *10.00 ± 6.12, z = 2.53, p = 0.006 *
B. orientalis44.50 ± 9.38, z = 0.42, p = 0.33931.49 ± 10.47, z = 1.32, p = 0.09448.83 ± 6.77, z = 0.06, p = 0.475
C. bursa-pastoris40.71 ± 16.36, z = 0.57, p = 0.285n/a81.67 ± 8.22, z = 1.81, p = 0.035 **
C. pratensis47.50 ± 4.61, z = 0.14, p = 0.44545.37 ± 7.23, z = 0.24, p = 0.40352.67 ± 3.60, z = 0.21, p = 0.418
C. papaya55.88 ± 8.82, z = 0.24, p = 0.40559.22 ± 7.30, z = 0.51, p = 0.30534.77 ± 5.04, z = 0.73, p = 0.231
C. spinosa33.46 ± 6.85, z = 1.08, p = 0.14128.50 ± 7.69, z = 1.45, p = 0.07325.53 ± 9.47, z = 1.66, p = 0.048 *
C. cotinifolius38.95 ± 8.37, z = 0.62, p = 0.26756.02 ± 10.57, z = 0.34, p = 0.36740.04 ± 8.81, z = 0.63, p = 0.263
D. muralis49.53 ± 7.85, z = 0.00, p = 0.50048.85 ± 3.11, z = 0.07, p = 0.47241.46 ± 5.55, z = 0.62, p = 0.266
E. sativa36.16 ± 3.12, z = 0.97, p = 0.16632.24 ± 3.96, z = 1.25, p = 0.10628.85 ± 6.63, z = 1.45, p = 0.073
E. cheiri69.29 ± 2.96, z = 1.20, p = 0.11550.46 ± 6.89, z = 0.00, p = 0.50023.80 ± 6.18, z = 1.80, p = 0.036 *
I. amara22.12 ± 4.74, z = 1.94, p = 0.020 *25.69 ± 6.98, z = 1.66, p = 0.048 *13.34 ± 5.97, z = 2.56, p = 0.005 *
L. sativum71.84 ± 4.52, z = 1.52, p = 0.06454.46 ± 2.66, z = 0.28, p = 0.39126.93 ± 8.21, z = 1.59, p = 0.055
L. douglasii24.15 ± 1.33, z = 1.80, p = 0.036 *36.00 ± 1.51, z = 0.97, p = 0.16626.90 ± 5.39, z = 1.59, p = 0.055
M. oleifera46.43 ± 3.57, z = 0.16, p = 0.436n/an/a
N. officinale58.54 ± 5.58, z = 0.39, p = 0.34858.79 ± 1.83, z = 0.15, p = 0.44247.10 ± 5.05, z = 0.34, p = 0.366
N. paniculata60.00 ± 30.55, z = 0.62, p = 0.26673.21 ± 1.79, z = 0.92, p = 0.179n/a
p. sativumn/an/a0.00 ± 0.00, z = 2.00, p = 0.023 *
R. odorata48.33 ± 25.87, z = 0.10, p = 0.46143.75 ± 25.77, z = 0.45, p = 0.3257.87 ± 4.56, z = 2.38, p = 0.009 *
S. officinale35.31 ± 5.99, z = 1.04, p = 0.14925.45 ± 3.72, z = 1.66, p = 0.048 *33.07 ± 6.74, z = 1.18, p = 0.119
T. majus75.93 ± 14.46, z = 1.27, p = 0.100n/a83.65 ± 12.71, z = 2.15, p = 0.016 **
* Adaxial leaf surface preferred. ** Abaxial leaf surface preferred.
Table
Table 3. Oviposition preference of P. xylostella strains reared on cabbage (DBM-C) and on artificial diet (DBM-G88) on filter paper impregnated with different concentrations of sinigrin. Data were analyzed using a one-tailed, two-sample test of proportions (p ≤ 0.05). Only the comparisons were more than one egg was laid on filter paper were considered (n = 3–17). For each comparison, means within a row followed by different superscript letters are significantly different.
Table 3. Oviposition preference of P. xylostella strains reared on cabbage (DBM-C) and on artificial diet (DBM-G88) on filter paper impregnated with different concentrations of sinigrin. Data were analyzed using a one-tailed, two-sample test of proportions (p ≤ 0.05). Only the comparisons were more than one egg was laid on filter paper were considered (n = 3–17). For each comparison, means within a row followed by different superscript letters are significantly different.
DBM-CDBM-P
Sinigrin Concentration (M)Lower ConcentrationHigher ConcentrationTest Statistic and p-ValueLower ConcentrationHigher ConcentrationTest Statistic and p-Value
10−3 vs. 10−235.5 ± 9.0 a64.5 ± 9.0 bz = 1.70, p = 0.04525.0 ± 5.5 a75.0 ± 5.5 bz = 2.92, p = 0.002
10−4 vs. 10−326.6 ± 7.5 a73.4 ± 1.7 bz = 2.29, p = 0.01115.5 ± 9.8 a84.5 ± 9.8 bz = 3.09, p = 0.001
10−5 vs. 10−428.5 ± 7.5 a71.5 ± 7.5 bz = 1.82, p = 0.03422.5 ± 11.1 a77.5 ± 11.1 bz = 2.33, p = 0.010
10−6 vs. 10−515.4 ± 7.8 a84.6 ± 7.8 bz = 1.70, p = 0.04526.8 ± 10.8 a73.2 ± 10.8 bz = 1.74, p = 0.041
10−7 vs. 10−622.9 ± 11.1 a77.1 ± 11.1 bz = 2.03, p = 0.0210.0 ± 0.0 a100.0 ± 0.0 bz = 2.45, p = 0.007
Table
Table 4. Two-choice larval preference index (LPI) given as mean ± SE in larvae of P. xylostella (DBM-C). Data were analyzed using a one-tailed, two-sample test of proportions comparing the relative percentages of choices made between A. thaliana (p ≤ 0.05) (n = 4–8). Significant differences are shown in bold type. Oviposition preference index (OPI) values taken from Badenes-Pérez et al. [10].
Table 4. Two-choice larval preference index (LPI) given as mean ± SE in larvae of P. xylostella (DBM-C). Data were analyzed using a one-tailed, two-sample test of proportions comparing the relative percentages of choices made between A. thaliana (p ≤ 0.05) (n = 4–8). Significant differences are shown in bold type. Oviposition preference index (OPI) values taken from Badenes-Pérez et al. [10].
LPI, Test Statistic, and p-ValueOPI, Test Statistic, and p-Value
A. argenteum0.31 ± 0.11, z = 3.20, p ≤ 0.001 *0.08 ± 0.02, z = 2.11, p = 0.018 *
A. caucasica0.87 ± 0.12, z = 0.38, p = 0.3520.43 ± 0.05, z = 0.98, p = 0.164
B. juncea4.14 ± 0.69, z = 2.52, p = 0.012 **1.71 ± 0.25, z = 0.59, p = 0.278
C. bursa-pastoris0.17 ± 0.01, z = 3.80, p ≤ 0.001 *0.03 ± 0.03, z = 2.30, p = 0.011 *
C. papaya0.23 ± 0.06, z = 2.41, p = 0.008 *0.05 ± 0.05, z = 2.25, p = 0.012 *
C. spinosa0.25 ± 0.05, z = 2.15, p = 0.032 *0.09 ± 0.05, z = 2.06, p = 0.020 *
D. muralis1.71 ± 0.34, z = 0.85, p = 0.1971.51 ± 0.17, z = 0.49, p = 0.312
E. sativa1.42 ± 0.21, z = 0.57, p = 0.2851.35 ± 0.25, z = 0.29, p = 0.384
E. cheiri0.69 ± 0.10, z = 1.34, p = 0.0900.22 ± 0.18, z = 1.71, p = 0.043*
I. amara0.49 ± 0.09, z = 1.41, p = 0.0790.72 ± 0.46, z = 0.78, p = 0.217
L. sativum1.69 ± 0.18, z = 1.21, p = 0.1144.28 ± 1.74, z = 1.18, p = 0.120
M. oleifera0.22 ± 0.06, z = 2.55, p = 0.005 *0 ± 0, z = 2.45, p = 0.007 *
p. sativum0.17 ± 0.01, z = 2.69, p = 0.004 *0 ± 0, z = 2.45, p = 0.007 *
R. odorata0.24 ± 0.05, z = 2.27, p = 0.011 *0.36 ± 0.30, z = 1.47, p = 0.071
S. officinale3.10 ± 0.66, z = 2.09, p = 0.018 **6.67 ± 2.04, z = 1.67, p = 0.048 **
T. majus1.33 ± 0.22, z = 0.50, p = 0.3080.04 ± 0.04, z = 2.16, p = 0.016 *
* A. thaliana preferred, ** Plant species compared to A. thaliana preferred.
Table
Table 5. Significance of correlations between plant glucosinolate content, larval preference index (LPI), and oviposition preference index (OPI) in the plants tested. Two-tailed Spearman’s rho correlations (n = 16) were performed. The effect of the diversity of glucosinolates was analyzed taking into account the glucosinolate richness (S), Shannon’s diversity index for the four glucosinolate classes (HA), Shannon’s diversity index for the relative concentrations of all individual glucosinolates (HB), and glucosinolate complexity index (GCI) for each plant (A). Besides total glucosinolate content (TOT), four different classes of glucosinolates were distinguished, aliphatic with sulfur-containing side chains (AS), other aliphatic (AO), benzenic (BEN), and indolic (IN) (B). Significant p-values (p ≤ 0.05) are shown in bold type.
Table 5. Significance of correlations between plant glucosinolate content, larval preference index (LPI), and oviposition preference index (OPI) in the plants tested. Two-tailed Spearman’s rho correlations (n = 16) were performed. The effect of the diversity of glucosinolates was analyzed taking into account the glucosinolate richness (S), Shannon’s diversity index for the four glucosinolate classes (HA), Shannon’s diversity index for the relative concentrations of all individual glucosinolates (HB), and glucosinolate complexity index (GCI) for each plant (A). Besides total glucosinolate content (TOT), four different classes of glucosinolates were distinguished, aliphatic with sulfur-containing side chains (AS), other aliphatic (AO), benzenic (BEN), and indolic (IN) (B). Significant p-values (p ≤ 0.05) are shown in bold type.
A
p-Value and Correlation Coefficient of Spearman’s Rho Correlation
OPISHAHBGCI
LPIp ≤ 0.001; 0.864p = 0.007; 0.641p = 0.010; 0.624p = 0.063; 0.476p = 0.010; 0.623
OPI-p = 0.011; 0.614p = 0.002; 0.723p = 0.086; 0.443p = 0.005; 0.668
B
p-Value and Correlation Coefficient of Spearman’s Rho Correlation
TOTAOBENINAS
LPIp = 0.015; 0.594p = 0.016; 0.590p = 0.673; −0.115p = 0.137; 0.388p = 0.064; 0.473
OPIp = 0.002; 0.716p = 0.024; 0.561p = 0.630; −0.131p = 0.033; 0.533p = 0.049; 0.498
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Badenes-Pérez, F.R.; Heckel, D.G. Intraspecific and Interstage Similarities in Host-Plant Preference in the Diamondback Moth (Lepidoptera: Plutellidae). Horticulturae 2023, 9, 39. https://doi.org/10.3390/horticulturae9010039

AMA Style

Badenes-Pérez FR, Heckel DG. Intraspecific and Interstage Similarities in Host-Plant Preference in the Diamondback Moth (Lepidoptera: Plutellidae). Horticulturae. 2023; 9(1):39. https://doi.org/10.3390/horticulturae9010039

Chicago/Turabian Style

Badenes-Pérez, Francisco Rubén, and David G. Heckel. 2023. "Intraspecific and Interstage Similarities in Host-Plant Preference in the Diamondback Moth (Lepidoptera: Plutellidae)" Horticulturae 9, no. 1: 39. https://doi.org/10.3390/horticulturae9010039

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