1. Introduction
In Mexico, there are more than 59 races of maize (
Zea mays L.), each associated with specific origins, distribution, and geographic regions [
1]. These maize races present genetic diversity related to their biological and anthropocentric processes, their selection, their adaptation, and the cultivation of different niches and ecological biotypes in various socioeconomic conditions, which has generated a wide diversity of maize. This is a fundamental feature of programs and strategies to improve agricultural challenges [
2,
3].
World corn production for the 2020/2021 agricultural cycle was 1120.65 million metric tons [
4]. Corn production is affected between 6% and 19% due to herbivore by arthropod pests [
5]. However, climate change has increased the metabolic rates and winter survival of arthropods, which coupled with a global average surface temperature increase of 2 °C may cause maize yield losses of up to 30% of damaged crops caused by insects and mite pests [
6,
7]. Corn cultivation is susceptible to attack by different insect pests, such as
Ostrinia nubilalis Hübner (Lepidoptera: Crambidae),
Spodoptera frugiperda Smith (Lepidoptera: Noctuidae),
Mythimna separata Walker (Lepidoptera: Noctuidae), and
Rhopalosiphum maidis Fictch (Hemiptera: Aphididae) [
8,
9,
10]. Regarding the damage caused by feeding of spider mites (Acari: Tetranychidae) to corn crops, around 43 species have been reported, clustered into 5 genera,
Eutetranychus (Banks) (2 spp.),
Oligonychus (Berlese) (19 spp.),
Panonychus (Yokoyama) (1 sp.),
Petrobia (Murray) (1 sp.), and
Tetranychus (Dufour) (20 spp.) [
11].
Tetranychus urticae Koch and
Oligonychus pratensis Banks are considered important pests in corn crops because the feeding damage of these mites causes large grain yield losses in corn [
7,
12]. In California, USA, Bacon et al. [
13] reported a reduction in corn yield of up to 32% due to damage caused by
T. urticae. In Texas, feeding damage of
O. pratensis can cause economic losses between USD 97.80 and USD 489.00 when silage prices range from USD 10.00 to USD 50.00 per hectare [
14].
The Tetranychidae family includes more than 1300 phytophagous species, clustered into 86 genera, divided into 2 subfamilies, Bryobinae and Tetranychinae, distributed throughout the world [
11]. Around one hundred species of Tetranychidae are considered pests, and a little more than ten are considered major pests [
11,
15]. Most of these pests belong to the genera
Tetranychus Dufour,
Panonychus Yokoyama,
Oligonychus Berlese, and
Eutetranychus Banks [
15]. Mites species belonging to these genera are important pests for many crops, fruit trees, vegetables, and ornamentals, and can naturally and temporarily inhabit weeds [
15]. The red spider mite,
Tetranychus merganser Boudreaux (Acari: Tetranychidae), causes severe damage by feeding on different plants crops, such as papaya (
Carica papaya L.), chili (
Capsicum annuum L.), and prickle pear cactus (
Opuntia ficus-indica L.) Miller [
11]. In Spider Mites Web for Tetranychidae,
Z. mays was not found to be a host plant for
T. merganser [
11]. This mite is distributed in China, Mexico, Unites States and Thailand [
11]. The damage caused by the feeding of
T. merganser is severe, destroying the epidermal tissue, the parenchyma, and the chloroplasts of the leaves, which affects the growth, development, and production of the host plant. This damage manifests as white spots near the leaf veins and when the host plant reaches a high population of red spider mite, the spots can merge, causing leaves to turn completely white [
16,
17].
Before the domestication of plants for agricultural purposes, plants survived and became resistant due to adaptation and natural selection [
18]. The effects of resistant plants on pest arthropods can manifest as antibiosis, antixenosis, tolerance, or a combination of these. Antibiosis occurs when the biology of the pest arthropod is negatively affected. Antixenosis occurs when the plant generates anti-feeding and anti-oviposition effects on pest arthropods. Tolerance is a polygenic trait that enables a plant to resist or recover from damage caused by an arthropod pest [
18,
19]. Plant secondary metabolites, also called allelochemicals, such as alkaloids, flavonoids, terpene lactones, and phenols, affect the health, behavior (antixenosis), growth, or population biology (antibiosis) of an insect or mite [
18].
The resistance of different maize inbred lines to
T. urticae [
20,
21],
T. cinnabarinus [
22,
23], and
O. pratensis [
7,
12] have been evaluated. However, there are few studies on the resistance of plants to
T. merganser [
24,
25]. Chacón-Hernández et al. [
24] evaluated the resistance of three accessions of piquin pepper (
C. annuum L. var.
glabriusculum (Dunal) Heiser and Pickersgill) and bean (
Phaseolus vulgaris L.) to
T. merganser. Moreover, Treviño-Barbosa et al. [
25] evaluated the resistance of seven host plant species (
Thevetia ahouai (L.) A. DC.,
C. papaya,
P. vulgaris,
Moringa oleifera Lam.,
Pittosporum tobira (Thunb.) W.T. Aiton,
Helietta parvifolia (Gray) Benth.,
C. annuum var.
glabriusculum) to red spider mite. Furthermore, Ullah et al. [
26] and Reyes-Perez et al. [
27] evaluated the performance of
T. merganser at different temperatures. The growth parameters of the population of
T. merganser, such as the rate of development, survival, reproduction, and longevity are a function of temperature [
24,
25,
26,
27]. In a review carried out in the Web of Science database, no report was found on the resistance of
Z. mays to
T. merganser, because the red mite is not a pest of the corn crop. However, the red mite has shown potential as an invasive species and has expanded its range of host plants and it is considered a potential pest in Mexican agriculture [
28]. This research aimed to assess antibiosis and antixenosis as resistance mechanisms in eleven native maize races cultivated in Tamaulipas, Mexico, to
T. merganser under laboratory conditions, as well as to obtain information on the chemical composition and morphological characteristics of these maize races, to identify the most resistant maize races for their possible incorporation into breeding programs.
3. Discussion
Phytophagous arthropods identify their host plant as a food source, but the quality and quantity of the food source are important factors affecting the longevity and fecundity of herbivorous arthropods [
29,
30]. Our results showed that maize races affected the behavior (antixenosis) and biology (antibiosis) of
T. merganser. At each observation time (24, 48, and 72 h), the feeding, oviposition, and fecundity of the red spider mite were affected by the different races of maize. The results of antixenosis at observation times show that Elotes Occidentales × Tuxpeño, Tuxpeño, and Vendeño races reduced the oviposition and feeding of
T. merganser, while oviposition and feeding by red spider mite increased on the Celaya race. The non-preference of the red spider mite for some races of maize could be due to differences in the total concentration of flavonoids (
Table 2), the thickness of the leaf, and the number of stomata present in the leaf (
Table 3). Secondary metabolites such as flavonoids can deter oviposition and feeding of a phytophagous arthropod [
18,
31,
32]. The thickness of the leaf can be a physical barrier so that mites such as
Tetranychus urticae Koch and
T. lintearius Dofour cannot feed on
Phaseolus vulgaris L. (Fabaceae) and
Ulex europaeus L. (Leguminosae), respectively [
33,
34]; therefore, these spider mites insert their stylet into the stomata so they can feed on their host plants [
34].
The literature does not refer to other studies on the resistance of maize races to
Tetranychus spp. However, other studies have evaluated the antibiosis and antixenosis of maize inbred lines to
Tetranychus spp. and
Oligonychus sp. and their findings are very similar to ours. Additionally, oviposition, growth rate, and feeding rate differ between maize races. Mite fecundity is affected by plant secondary metabolites, leaf nutrition, leaf age, and leaf surface structure [
35]. Tadmor [
23] reported differences in the number of eggs laid per day per female of
T. cinnabarinus on ten inbred maize lines. They documented performance from 0.2 to 1.4 E/F/D in four days. While Paoulo et al. [
36] found no difference in the number of eggs laid by
T. urticae on maize plants reinfested with the spider mite compared to plants with mites. They concluded that there is a direct resistance induction of
Z. mays to
T. urticae. Bui et al. [
7] evaluated the resistance of 38 inbred maize lines to
T. urticae and
O. pratensis. They found that
T. urticae (median ~8–50) exhibited greater variation than
O. pratensis (median ~30–50) when compared with progeny per female (eggs and viable mites, all stages) in six days of evaluation under greenhouse conditions; meanwhile, Bui et al. [
12] evaluated inbred maize W22, from which Ds transposon insertions were recovered in three genes responsible for DIMBOA-Glc synthesis—BX1, BX2, and BX6. They found that the number of progeny per female of
T. urticae and
O. pratensis on the inbred maize line (M22) and on the mutants maize (bx1::Ds, bx2::Ds, and bx6::Ds) were different and similar, respectively.
Other studies have reported that the number of eggs laid by
T. merganser is related to the host plant [
24,
25]. Chacón-Hernández et al. [
24] reported lower oviposition of
T. merganser female (66.00 ± 15.31, 66.33 ± 8.67 and 44.33 ± 21.40) on three accessions (BGH-425, BGH-426 and Ch1) of
C. annuum var.
glabriusculum than on
P. vulgaris (166.00 ± 7.23) at 120 h, under laboratory conditions at 27 ± 2 °C, 60–70% RH and a photoperiod of 12:12 L:D; meanwhile, Treviño-Barbosa et al. [
25] reported that the daily oviposition rate of the red spider mite was higher in
C. papaya (7.46 ± 0.18 eggs/female/day) than on
P. vulgaris (4.41 ± 0.22),
M. oleifera (3.57 ± 0.12),
C. annuum var.
glabriusculum (2.92 ± 0.12),
H. parvifolia (1.49 ± 0.04),
P. tobira (1.10 ± 0.09), and
T. ahouai (0.97 ± 0.09) at 28 ± 1 °C, 70–80% relative humidity and photoperiod of 12:12 L:D. These variations could be attributed to differences in plant species and cultivar types, as they may have differences in nutrient content, morphological characteristics and in secondary metabolite levels, as well as environmental factors [
26,
35,
37,
38,
39].
Resistant plants cause mites not to feed, causing them to be thin and weak, or if they do feed, they cannot digest the food material, causing them to swell and turn black [
40]. In the Tabloncillo × Tuxpeño and Vandeño races, feed intake of
T. merganser was lower compared with other maize races (
Table 4) and by visual observations, we found that the red spider mites were thinner in these maize races than in the others. This may be due to the differences in the morphological characteristics and secondary metabolites. Secondary metabolites such as flavonoids and phenols that were found stored in the cell walls of leaves deter feeding and oviposition of arthropods [
18]. Hence, the maize races differ in their suitability as possible hosts for red spider mites when measured in terms of fecundity and as resources for feeding. In this regard, Ullah et al. [
40] documented that
T. urticae and
T. kanzawai cause different feeding damage rates in 23 cultivars and 20 lines of cucumber (
Cucumis sativus L.). Bynum et al. [
14] reported that
T. urticae caused different feeding damage rates in 12 maize inbred lines. Besides, Bui et al. [
7] documented that
T. urticae causes the highest feeding damage rate on maize inbred line B73 than
O. pratensis. Treviño-Barbosa [
25] reported a higher feeding damage of
T. merganser in
C. papaya (47.00 ± 0.73%) than to
P. vulgaris (40.67 ± 1.76%),
M. oleifera (32.33 ± 1.76%),
C. annuum var.
glabriusculum (30.67 ± 1.20%),
H. parvifolia (27.00 ± 2.52%),
P. tobira (26.33 ± 3.18%), and
T. ahouai (24.33 ± 0.67%) at 28 ± 1 °C, 70–80% relative humidity, and photoperiod of 12:12 L:D.
In this research work, the antibiosis of the different maize races was indicated by the growth rate (ri). Although the MANOVA did not show significant differences in the growth rate of the red spider mite between the maize races, the PCA showed a strong inverse relationship between the ri and the Elotes Occidentales × Tuxpeño race and to a lesser extent with the Tuxpeño and Vandeño in the different observation times (see
Figure 2,
Figure 4 and
Figure 6). Factors such as survival and fertility rate affect ri; hence, ri adequately summarizes the physiological qualities of an insect with its ability to increase its population [
41]. In addition, this parameter is the most appropriate for evaluating plants resistance to herbivorous arthropods. The PCA showed that the immature mites, oviposition, and growth rate of
T. merganser were inversely related with the Elotes Occidentales × Tuxpeño, Vandeño and Tuxpeño races. In addition, these maize races did not present differences in the total phenols concentration. This bioactive compound present in maize plants may be an antibiosis factor for herbivorous arthropods, such as
Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae),
Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) [
42], and
Sesamia nonagrioides Lefèbvre (Lepidoptera: Noctuidae) [
43,
44]. On the other hand, Agut et al. [
45] found that flavonoid compounds such as p-coumaric acid present in
Citrus aurantium (L.) caused resistance to
T. urticae. This secondary metabolite participates in the biosynthesis of lignin polymers, resulting in the formation of physical barriers to reduce the palatability of the plant [
46]. Native maize races, such as the Tuxpeño race, contain high contents of p-coumaric acid [
47].
Cultivars that support low population densities of herbivorous arthropods are an important part of pest management [
48]. To conclude, this research showed that
T. merganser feeds and develops in the eleven native maize populations, but also showed that the Elotes Occidentales × Tuxpeño, Tuxpeño, and Vandeño races are resistant to red spider mite. This resistance is due to their morphological characteristics and the secondary metabolites present in their leaves. Further, research is necessary on the behavior and biology of
T. merganser under field conditions. Such research might give us a clearer idea of the effects of the red spider mite on the yield of the maize races.