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Article

Temperature-Driven Selection of Predatory Mirid Bugs for Improving Aphid Control in Sweet Pepper Crops

by
Meritxell Pérez-Hedo
,
Virginia Pedroche
and
Alberto Urbaneja
*
Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Protección Vegetal y Biotecnología, Unidad de Entomología, Carretera CV-315, Km 10′7, 46113 Moncada, Spain
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(5), 572; https://doi.org/10.3390/horticulturae9050572
Submission received: 24 March 2023 / Revised: 4 May 2023 / Accepted: 9 May 2023 / Published: 11 May 2023
(This article belongs to the Special Issue Innovative Integrated Pest Management (IPM) Systems in Orchards and Vegetable Crops)
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Abstract

:
Recent studies have suggested that predatory mirid bugs may be an effective alternative for controlling aphids in sweet pepper greenhouses. This study examined the effect of three constant temperatures (18, 24, and 30 °C) on the life history traits of predatory mirid species Nesidiocoris tenuis, Macrolophus pygmaeus, and Dicyphus bolivari, preying on the aphid Myzus persicae nicotianae in sweet pepper plants. As the temperature increased, the survival rate decreased for M. pygmaeus and D. bolivari, while for N. tenuis, it was the opposite, and their survival increased. When considering all the biological traits studied together, the estimated intrinsic rate of increase (rm) decreased as the temperature increased for M. pygmaeus and D. bolivari. In contrast, the rate increased as the temperature increased for N. tenuis. These results suggest that M. pygmaeus and D. bolivari are better adapted to lower temperatures than N. tenuis, which is more adapted to warm temperatures. The implications of these results for improving the biological control of aphids in sweet pepper greenhouses through the use of mirid bugs are discussed in relation to different temperature regimes.

1. Introduction

Sweet pepper cultivation in greenhouses is one of the largest crops in which the use of augmentative biological control is more established in the Mediterranean basin [1,2]. Most sweet pepper pests can be controlled by releasing natural enemies, so pesticides are not commonly used. The main pest in sweet pepper cultivation in greenhouses is western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Tripidae), primarily because they act as a vector of the tomato spotted wilt virus (TSWV) [3,4]. Additionally, the sweet potato whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) is a significant secondary pest that harms crops by removing sap and degrading fruit quality through the accumulation of sooty mold [5,6].
Two significant milestones have taken place in this crop to deal with these two key pests [7]. Firstly, from the end of the 1990s, the use of the predatory mite Amblyseius cucumeris (Oudemans) (Acari: Phytoseiidae) and the minute pirate bug Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) for thrips control became common [8], whereas at the beginning of this decade, the parasitoid Eretmocerus mundus Mercet started to be released for whitefly control [6,9,10]. The combined use of A. cucumeris and O. laevigatus was highly successful in controlling thrips in cropping systems where planting typically occurred in late fall and harvests ended in late summer due to favorable weather conditions for the establishment of both natural enemies [11] and low pest pressures at the beginning of the crop [12]. Nevertheless, in cropping systems where planting occurs in summer and ends in the following spring, this biocontrol approach was not effective, mainly due to the adverse weather conditions of high temperature and low relative humidity [13,14] and the high pest pressure at the beginning of the crop [15]. Furthermore, the use of E. mundus significantly reduced but did not eliminate the need for additional pesticide treatments against B. tabaci [16]. This second milestone occurred with the emergence of the biological control market of the predatory mite Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) [17]. The replacement of A. cucumeris with A. swirskii in the biocontrol package for this crop, which is well-adapted to arid conditions [18,19], resulted in the effective control of both B. tabaci and F. occidentalis, as this phytoseiid is highly effective against both pests under a wide range of climatic conditions [15,20]. Since incorporating A. swirskii into the pest control program for sweet pepper, biological control has become widespread in almost all sweet pepper cropping areas (i.e., approximately 8500 ha in Southeastern Spain) [1,7,21,22]. However, managing some secondary pests, such as aphids, still requires selective pesticide applications [1]. Despite the availability of commercial biocontrol agents for common aphid species in sweet pepper, such as Myzus persicae (Sulzer), Myzus persicae nicotianae Blackman, Aphis gossypii Glover, Macrosiphum euphorbiae Thomas and Aulacorthum solani Kaltenbach (Hemiptera: Aphididae), they are not always effective enough [23,24]. The need for multiple releases of natural enemies increases the final cost of the biocontrol program for this crop [25,26,27].
One alternative to improve the biological control of aphids might be the use of predatory mirid bugs (Hemiptera: Miridae), which, due to their zoophytophagous behavior, can establish in a sweet pepper crop before aphid infestations [25,28,29,30]. Previous studies suggest the positive role that predatory mirids Nesidiocoris tenuis (Reuter), Macrolophus pygmaeus Rambur, and Dicyphus bolivari Lindberg (Hemiptera: Miridae) could have in controlling aphids in sweet pepper plants [25,28,31,32]. Pérez-Hedo et al. (2015) demonstrated that females of the three predatory mirids, N. tenuis, M. pygmaeus, and D. bolivari, actively preyed on M. persicae and were strongly attracted to the odor of infested M. persicae plants. Furthermore, the three species of mirids could reproduce on aphids and establish themselves on sweet pepper plants at temperatures between 23 and 27 °C, relative humidity of 65 ± 10%, and under natural photoperiods (approximately 14L: 10D), significantly reducing the number of M. persicae per leaf. The performance of the three species of mirids in reducing M. persicae populations was similar in these experiments [28]. Going further, Bouagga et al. [30] tested the combined use of either N. tenuis or M. pygmaeus with A. swirskii as a potential method for controlling thrips, whiteflies, and aphids in sweet pepper crops. These authors demonstrated that integrating one of these mirids with the already established predator A. swirskii could enhance sweet pepper pest management since a satisfactory control of the three pests was accomplished. However, the effectiveness of these predatory mirid bugs may vary depending on temperature, and in sweet pepper crops, different climatic conditions could be found depending on the planting period. The climatic conditions will impact these predatory mirids’ establishment, spread, and overall effectiveness. Laboratory experiments were conducted to study the influence of temperature on the predation capacity and life history traits of these three mirid species when feeding on the tobacco aphid, M. persicae nicotianae Blackman.

2. Materials and Methods

2.1. Experimental Insects

The red clonal colonies of the tobacco aphid, M. persicae nicotianae, were initiated in 2013 with individuals collected in sweet pepper fields located in the Valencia province (Spain). These colonies were maintained on pesticide-free potted sweet pepper plants (var.” Lipari,” Clause Spain S.A.U., Almería, Spain) and housed in a climatic chamber at 25 ± 2 °C, 60–80% RH and a 16:8 h (L:D) photoperiod at Instituto Valenciano de Investigaciones Agrarias (IVIA). Rearing took place in screened cages (120 × 70 × 125 cm), where groups of six sweet pepper plants (approximately 25 cm high) were introduced weekly.
Dicyphus bolivari individuals were initially collected in Valencia province (Spain) tomato fields. They were then reared on pesticide-free tomato seedlings “Optima” (Seminis Vegetable Seeds, Inc., Almería, Spain) using frozen eggs of the factitious prey Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae) as food, while N. tenuis and M. pygmaeus adults were obtained from a commercial supplier (NESIBUG® and MYRICAL®; Koppert Biological Systems, S.L., Águilas, Murcia, Spain). Each bottle held about 500 individuals, including both mature nymphs and young adults that were no more than three days old. The specimens were fed a diet of E. kuehniella eggs (FJ Calvo, Koppert BS; Personal Communication).

2.2. Predation Capacity

The predatory capacity of female individuals from the three studied species of Miridae was evaluated and compared at three constant temperatures: 30 ± 1 °C, 24 ± 1 °C, and 18 ± 1 °C, representing the thermal regimes found in protected sweet pepper crops. Three plastic cages measuring 60 × 60 × 60 cm (BugDorm-2; MegaView Science Co., Ltd.; Taichung, Taiwan) were each populated with one of the three tested predatory mirid species, with 95–100 adult mirids of each species (2–4 days old). In each cage, the individuals were starved of prey for 24 h before use. Additionally, four non-infested sweet pepper plants without flowers (25 cm high) were introduced in each cage during the prey starvation period to allow the mirids to adapt to sweet pepper plants. None of the three species of mirids exhibited cannibalistic behavior. Myzus persicae nicotianae-infested leaves were detached from infested plants of the stock colony. Using a stereoscopic binocular microscope and a small brush, the fourth instar nymphs of M. persicae nicotianae were carefully chosen and transferred onto sweet pepper leaves in Petri dishes (9 cm in diameter). The fourth nymphal instars of M. persicae nicotianae were readily distinguishable based on their morphology [33]. Each of the three predator species’ females was exposed to 20 fourth instar nymphs, with soaked cotton plugs providing water. For each temperature and species, fifteen replicates were carried out. After 24 h, the predators were removed from the arenas, and the number of nymphs consumed was determined.

2.3. Developmental Time and Juvenile Survivorship

Ten adult couples (approximately less than 4 days old) of each predator species were released separately in methacrylate cages (40 × 40 × 40 cm) with four sweet pepper plants for 24 h. After that, plants bearing predator eggs were removed and cut into small sections, placed on Petri dishes (60 mm in diameter) with filter paper to avoid excess humidity, and were maintained at three studied temperatures 18 °C, 24 °C, and 30 °C. Egg hatching was monitored daily by examining the dishes. Any newly hatched nymphs less than 24 h old were transferred individually into 30 mm Petri dishes. The predators were provided with second to third-instar nymphs of M. persicae nicotianae, sweet pepper leaf disks with a diameter of 20 mm, and water-soaked cotton wool to serve as a water source. Around 10–12 nymphs of M. persicae nicotianae were added per Petri dish, which always exceeded the daily consumption rate of nymphs for the three tested mirids. The development and survival of the nymphs were observed daily using a stereomicroscope until they reached adulthood or died. The Petri dishes were kept in a climatic chamber at three different temperatures, with a relative humidity of 65 ± 5% RH and a photoperiod of 14:10 h (L:D).

2.4. Reproductive Parameters

Newly emerged adults of N. tenuis, M. pygmaeus, and D. bolivari, which were reared from nymphs at three different temperatures (18 °C, 24 °C, and 30 °C), were transferred in pairs (one female and one male) to plastic cups (370 cm3) containing a tender apical sweet pepper flush (approximately 14 cm) with second and third instar nymphs of M. persicae nicotianae that were provided as food ad libitum. The water in the bottom cup was accessed by pushing the apical sweet pepper flushes through a hole in the inner cups. Following the methodology of Abbas et al. [34], adapted from Sánchez et al. [35], the larger plastic cups were positioned inside smaller ones (230 cm3) and filled with water. The bigger cups were then secured with a rubber band and covered with a fine mesh.
Every 5 days, pairs of adults were relocated to a fresh plastic cup with fresh M. persicae nicotianae nymphs until the female’s death. A young male (obtained from the corresponding immature bioassay) was given to each female to guarantee to mate during her lifetime, and when it perished, it was substituted. Every day, adult mortality was monitored, and every other day, the hatching of eggs laid in the cups by the females was observed. To determine the sex ratio of the offspring, female offspring were reared to adulthood in the same containers and under the same environmental conditions as their birthplace and provided with ad libitum E. kuehniella eggs.

2.5. Demographic Growth Indexes

Demographic indices were then calculated and compared for the three studied constant temperatures (18 °C, 24 °C, and 30 °C). Daily survival values and the number of offspring produced by the females were used to construct life tables. The intrinsic rate of increase (rm; females/female/day), the net reproductive rate (R0; female eggs/female), and generation time (T; days) following demographic growth parameters were generated [36,37]. The standard error for rm, R0 and T was estimated using the Jackknife technique on raw data. This involved calculating the per capita rm, R0 and T by omitting one replicate per trial and repeating this process until pseudo-values were obtained for all possible omission cases. The standard error was then computed using the Jackknife formula. [38].

2.6. Statistical Analysis

The effect of the predator species on the predation capacity and life history traits (development time from eggs to adult and per each nymphal stage; lifetime fertility, female longevity; progeny sex ratio, and the three demographical indexes) for each temperature were subjected to a two-way analysis of variance and Tukey’s test was used for mean separation (p < 0.05).

3. Results

3.1. Predation Capacity

The three species of mirids preyed on M. persicae nicotianae at the three tested temperatures (Figure 1). Nesidiocoris tenuis preyed on more nymphs of M. persicae nicotianae than M. pygmaeus and D. bolivari (F2,126 = 23.78, p < 0.001), and predation was significantly different between the temperatures (F2,126 = 17.38, p < 0.001). An interaction between the species and temperature was found (F2,126 = 6.28, p = 0.0001). As depicted in Figure 1, the positive response of N. tenuis to increasing temperatures was distinct from the other two species.

3.2. Developmental Time and Survivorship of Immatures

The duration of the egg stage was longer in D. bolivari compared to M. pygmaeus, and M. pygmaeus had a longer duration than N. tenuis (F2,467 = 4263, p < 0.001) (Figure 2A). Additionally, significantly different durations were observed among each of the three temperatures studied (F2,467 = 383.4, p < 0.001), with a significant interaction existing between both factors (species and temperature) (F4,467 = 37.56, p < 0.001), indicating that each species responded differently to the temperature.
Development of M. pygmaeus and D. bolivari only occurred at 18° and 24 °C, whereas N. tenuis could develop at the three temperatures tested (Figure 2B,C). The duration of the nymph stage and the total duration from egg to adult varied among the three mirid species, with D. bolivari exhibiting the longest duration, M. pygmaeus showing an intermediate duration, and N. tenuis displaying the shortest duration (Nymphs: F2,213 = 90.49, p < 0.001; Total: F2,213 = 152.2, p < 0.001). Both periods had longer durations at 18 °C compared to 24 °C (Nymphs: F1,213 = 1596, p < 0.001; Total: (F1,213 = 3091, p < 0.001). Additionally, an interaction was observed between both factors (Nymphs: F2,213 = 10.37, p < 0.001; Total: (F2,213 = 21.53, p < 0.001).
The survival of the three predatory mirid bugs at the three temperatures assayed is shown in Figure 3. The temperature significantly influenced the survival of the three mirid species (F2,412 = 32.44, p < 0.001), which also varied among the species (F2,412 = 17.78, p < 0.001). The survival of M. pygmaeus and D. bolivari was similar, decreasing as the temperature increased. This trend was different for N. tenuis, whose survival increased at higher temperatures, resulting in an interaction between the two factors analyzed (species and temperature) (F2,412 = 18.47, p < 0.001).

3.3. Reproductive Parameters

The temperature significantly affected lifetime fertility (F1,72 = 16.98, p < 0.001), female longevity (F1,73 = 41.46, p < 0.001), and the progeny sex-ratio (F1,48 = 9.945, p = 0.003) for the three predatory mirid bugs tested (Table 1). Because no nymph of M. pygmaeus and D. bolivari reached adulthood, reproductive parameters could only be obtained for N. tenuis at 30 °C. Dicyphus bolivari and M. pygmaeus produced significantly more nymphs than N. tenuis (F2,72 = 6.253, p = 0.003). Although the progeny of N. tenuis at 18 °C was almost negligible, it increased at higher temperatures, in contrast to the decrease observed in M. pygmaeus and D. bolivari. This resulted in a significant interaction between the two factors under study (F2,72 = 19.0, p < 0.001). Female longevity was higher in D. bolivari than in M. pygmaeus and N. tenuis (F2,73 = 12.58, p < 0.001). An interaction was found for female longevity between the temperature and species (F2,73 = 3.729, p = 0.029). The sex ratio was significantly skewed toward females in the case of D. bolivari and N. tenuis when compared to M. pygmaeus (F2,48 = 14.27, p < 0.001), with no interaction found between the temperature and species (F2,48 = 0.1532, p = 0.858).
Age-specific fertility depended on the age of the female, and this relationship was stronger as temperatures increased (Figure 4). At 18 °C (Figure 4A), the shape of the age-specific fertility curve was very smooth for D. bolivari: the rate slowly increased until around 2 nymphs per day 30 days after emergence, which was maintained for almost 40 additional days and then decreased. Similarly, M. pygmaeus reached around 3 nymphs per day 10 days after emergence, holding this rate for about 10 extra days, then slowly falling until day 35. The daily fertility for N. tenuis was almost nil at this temperature. At 24 °C (Figure 4B), the shape of the age-specific fertility curve changed considerably: it continuously and sharply decreased from the beginning for N. tenuis and M. pygmaeus, whereas it was smoother for D. bolivari. At 30 °C (Figure 4C), N. tenuis behaved similarly at 24 °C.

3.4. Demographic Indexes

The generation time (T) significantly decreased as the temperature increased in the three predatory mirid species (F1,72 = 12,733, p < 0.001) and was significantly different between the three predatory mirids (F2,72 = 1644, p < 0.001) (Figure 5A). Generation time was higher for D. bolivari than for M. pygmaeus, and these values for both species were higher than that of N. tenuis at 18 and 24 °C, reflecting more accelerated reproduction for N. tenuis. Because both D. bolivari and M. pygmaeus could not successfully develop at 30 °C, generation time was zero, whereas N. tenuis was similar to that obtained at 24 °C. The estimated reproductive rate (R0) was significantly different between temperatures (F1,72 = 2026, p < 0.001) and species (F2,72 = 996.5, p < 0.001) (Figure 5B). For M. pygmaeus and D. bolivari, R0 decreased as the temperature increased to reach the value of zero at 30 °C. However, in the case of N. tenuis, this reproductive parameter increased from 18 °C to 24 °C and slightly decreased to 30 °C. The estimated intrinsic rates of increase (rm) were significantly different between temperatures (F1,72 = 72.31, p < 0.001) and species (F2,72 = 318.5, p < 0.001) (Figure 5C). The intrinsic rate of increase decreased as temperatures increased for M. pygmaeus and D. bolivari, whereas it increased for N. tenuis (Figure 5C). An interaction was found between the temperature and mirid species for the estimated demographic parameters (T: F2,72 = 156.5, p < 0.001; R0: F2,72 = 1678, p < 0.001 and rm: F2,72 = 5985, p < 0.001).

4. Discussion

In this study, we provide a detailed and comprehensive analysis of the influence of temperature on the biology of three mirids that are susceptible to use against aphids in sweet pepper crops. Our results showed that life history parameters varied considerably among the three predator species and were consistent with many previous studies on the influence of temperature on the three mirid species studied in this work [31,35,39,40,41,42,43,44,45,46,47,48,49,50,51]. The difference in temperature sensitivity between N. tenuis, M. pygmaeus and D. bolivari was widely known. Our results confirm that when preying on M. persicae nicotianae on sweet pepper, N. tenuis was more thermophilic compared to M. pygmaeus and D. bolivari. Of the three species, D. bolivari was the best-adapted species for temperate climates. These differential traits between the two species explain their different geographical distribution [52,53]. As an illustration, in the Iberian Peninsula, M. pygmaeus and D. bolivari were predominantly located in the northern region, while N. tenuis was commonly found in the southern region [53]. This geographical distribution could be associated with the temperature variation from north to south. In addition to their geographical distribution, their adaptation to temperatures was also related to their varying crop presence in regions where these species overlapped. In fact, in the horticultural crops of the Valencian Community (eastern half of the Iberian Peninsula), it is typical for D. bolivari to appear and establish itself at the start of the crop when average temperatures are below 20 °C, only to disappear and be replaced by N. tenuis in the spring when temperatures consistently exceed 20 °C.
In addition to temperature, intraguild interactions should also be considered in the coexistence of mirid species [54,55,56]. However, a comprehensive analysis of all potential interactions is necessary when accounting for the factors that may affect them. Apart from temperature, other factors are equally or even more critical in impacting these intraguild interactions, such as the type and availability of prey or crops [54,56,57,58,59]. As an example of this complexity, for N. tenuis and D. bolivari, the main cause of temporal displacement in horticultural open fields of the Valencian Community was N. tenuis’s superior competitive ability due to its better adaptation to higher temperatures and ability to deplete food sources for D. bolivari [55]. Contrary to this, in a controlled climate such as the Dutch greenhouses, releasing D. bolivari from the nursery could regulate unwanted infestations of N. tenuis. Dicyphus bolivari acts as an intraguild predator, reducing the plant damage caused by N. tenuis [60].
Among the previously described factors that can have a greater impact on the biology of mirids is the type of prey they consume [61,62,63]. Our work demonstrates that M. persicae nicotianae is not the most effective prey for development, as its biotic potential is relatively low compared to the results obtained in other studies with different types of prey [35,39,43,48,63,64]. For example, Perdikis and Likouressis [63] observed that M. pygmaeus, when feeding on M. persicae, had better biological parameters than those obtained in the present study with M. persicae nicotianae. Even M. pygmaeus could complete its cycle and reproduce at 30°, which was not achieved in our research. Therefore, this seemed to confirm the lower suitability of M. pygmaeus nicotianae as prey compared to M. persicae. In addition to the already known drawbacks of M. persicae nicotianae in comparison to M. persicae sensu stricto, such as (i) having evolved an enhanced tolerance to pyridine alkaloid nicotine, a natural insecticide produced by tobacco and other Solanaceae [65], and (ii) showing reduced sensitivity to neonicotinoids due to their chemical relationship with nicotine [66], our results also demonstrated its inferior quality as prey for mirids. Jalali and Michaud [67] already observed that M. persicae nicotianae had lower nutritional value for the ladybug Adalia bipunctata (L.) (Coleoptera: Coccinellidae) when aphids were developed on sweet pepper.
Our results clearly show the effect of temperature on the three mirid species. Temperature can affect the efficacy of predatory mirids in several ways, including (i) their development rate, survival and reproductive success: temperature changes, which can alter the development time and survival of mirids and can also affect their ability to reproduce and control pest populations, and (ii): their activity level: predatory mirids are ectothermic, meaning their body temperature is dependent on the environment, and therefore, changes in temperature can affect their metabolism and activity levels, leading to changes in their ability to locate and consume prey. The intrinsic rate of development of D. bolivari and M. pygmaeus decreases as temperature increases, while the opposite occurs with N. tenuis. However, another critical parameter that is known for practical use in biological control strategies is its predation potential related to activity level. This work shows how the three species prey on different amounts of aphids in 24 h at the three studied temperatures. Nesidiocoris tenuis maintains the highest prey ratios at all three temperatures, especially at 30 °C, doubling the number of prey consumed compared to the other two species. Therefore, although this temperature is a crucial factor and its influence is evident in various studied biological parameters, relying solely on the intrinsic rate of development as a precise parameter from which to infer its predation capacity and potential as a biological control agent may not be accurate. To this end, van Lenteren et al. [68] developed the term “pest kill rate,” where all the biological parameters were integrated with the prey capacity. The pest kill rate is the average number of pests killed per day during the lifespan of the natural enemy in question. This kill rate is, therefore, a much more accurate parameter for comparing predators than the intrinsic rate of development. However, the design of our study did not include this possibility, and we did not approach the experimental design by evaluating the parameters necessary to estimate the kill rate; certainly, for future work, this would be the next step: the estimation of the kill rate for predators.
Mirids are not widely used in augmentative biological control programs for pepper crops when managing aphids in the Mediterranean Basin. However, several studies have shown their great potential for controlling this pest. Messelink et al. [69] showed that the preventive release of M. pygmaeus and D. tamaninii together with supplemental food (eggs of the flour moth Ephestia kuehniella Zeller and decapsulated cysts of the brine shrimp Artemia franciscana Kellogg) controlled the populations of M. persicae in sweet peppers. Bouagga et al. [30] demonstrated how using mirids (either N. tenuis or M. pygmaeus) combined with the predatory mite A. swirskii provided control over the three major pests affecting sweet peppers in Southern Europe: thrips, whitefly, and aphids. However, if O. laevigatus was used instead of mirids, the control of aphids could not be achieved. Despite these findings, mirids are still not widely utilized in commercial greenhouse sweet pepper cultivation.

5. Conclusions

Temperature is a critical factor in the success of predatory mirids and as biological control agents. Temperature changes can affect various aspects of their biology and behavior, such as their rate of development, activity level, and reproductive success. Based on the findings of this study, M. pygmaeus and D. pygmaeus appeared to be effective in temperate climates where temperatures were moderate and moderate changes occurred throughout the year. Meanwhile, N. tenuis is more suitable for warmer climates with higher temperatures. When selecting a species of mirid for controlling aphid populations, it is essential to consider the environment and temperature of the target area. The results of this study underscore the importance of temperature in the effectiveness of predatory mirids and highlight the need to understand how temperature affects their biology and behavior to develop effective strategies for using them as biological control agents against pests.

Author Contributions

Conceptualization, M.P.-H. and A.U.; methodology, M.P.-H. and A.U.; formal analysis, M.P.-H. and A.U.; investigation, M.P.-H., V.P. and A.U.; resources, M.P.-H. and A.U.; data curation, M.P.-H., V.P. and A.U.; writing—original draft preparation, M.P.-H. and A.U.; writing—review and editing, M.P.-H. and A.U.; supervision, M.P.-H. and A.U.; project administration, M.P.-H. and A.U.; funding acquisition, M.P.-H. and A.U. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the project by grant PID2020-113234RR-I00 from the Spanish Ministerio de Ciencia e Innovación through the Agencia Estatal de Investigación (co-financed European Regional Development Fund, ERDF) and by the project “Sostenible” GVA-IVIA-52202 from the Instituto Valenciano de Investigaciones Agrarias (IVIA) of the Generalitat Valenciana, which is eligible for co-financing from the European Union through the ERDF Operational Program.

Data Availability Statement

The data that support the findings of this study are openly available in the Zenodo repository at https://doi.org/10.5281/zenodo.7599935 (accessed on 19 April 2023).

Acknowledgments

The authors thank Koppert B.S. Spain for supplying Nesidiocoris tenuis and Macrolophus pygmaeus adults and Miquel Alonso-Valiente (IVIA) for technical support.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Number (mean ± SE) of fourth instar nymphs of M. persicae nicotianae consumed by females of N. tenuis, M. pygmaeus and D. bolivari on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05).
Figure 1. Number (mean ± SE) of fourth instar nymphs of M. persicae nicotianae consumed by females of N. tenuis, M. pygmaeus and D. bolivari on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05).
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Figure 2. Mean (± SE) duration (days) of egg (A), nymphs (B) and total development from egg to adult (C) of N. tenuis, M. pygmaeus and D. bolivari preying on M. persicae nicotianae on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05). * At 30 °C, neither M. pygmaeus nor D. bolivari completed their development, so the two-way ANOVA was only applied to 18 °C and 24 °C.
Figure 2. Mean (± SE) duration (days) of egg (A), nymphs (B) and total development from egg to adult (C) of N. tenuis, M. pygmaeus and D. bolivari preying on M. persicae nicotianae on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05). * At 30 °C, neither M. pygmaeus nor D. bolivari completed their development, so the two-way ANOVA was only applied to 18 °C and 24 °C.
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Figure 3. Instar-specific survival (%) of the immature stages of N. tenuis, M. pygmaeus and D. bolivari when preying on M. persicae nicotianae on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05).
Figure 3. Instar-specific survival (%) of the immature stages of N. tenuis, M. pygmaeus and D. bolivari when preying on M. persicae nicotianae on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05).
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Figure 4. Age-specific fertility (number of N1 produced/female/day ± SE) of N. tenuis, M. pygmaeus and D. bolivari preying on M. persicae nicotianae on sweet pepper leaf discs at 18 (A), 24 (B) and 30 ± 1° C (C) and 14:10 h L:D.
Figure 4. Age-specific fertility (number of N1 produced/female/day ± SE) of N. tenuis, M. pygmaeus and D. bolivari preying on M. persicae nicotianae on sweet pepper leaf discs at 18 (A), 24 (B) and 30 ± 1° C (C) and 14:10 h L:D.
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Figure 5. Mean (± SE) generation time T (days) (A), net reproductive rate R0 (females/female) (B) and intrinsic rate of increase rm (females/female/day) (C) for N. tenuis, M. pygmaeus and D. bolivari preying on M. persicae nicotianae on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Means values accompanied by the same letter are not significantly different (Tukey test; p > 0.05). Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05). At 30 °C, neither M. pygmaeus nor D. bolivari completed their development so two-way ANOVA was only applied to 18 °C and 24 °C.
Figure 5. Mean (± SE) generation time T (days) (A), net reproductive rate R0 (females/female) (B) and intrinsic rate of increase rm (females/female/day) (C) for N. tenuis, M. pygmaeus and D. bolivari preying on M. persicae nicotianae on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Means values accompanied by the same letter are not significantly different (Tukey test; p > 0.05). Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05). At 30 °C, neither M. pygmaeus nor D. bolivari completed their development so two-way ANOVA was only applied to 18 °C and 24 °C.
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Table
Table 1. Mean (± SE) lifetime fertility (total offspring produced/female), female longevity (days) and progeny sex ratio (percentage of females/total offspring) of N. tenuis, M. pygmaeus and D. bolivari preying on M. persicae nicotianae on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05). * At 30 °C, neither M. pygmaeus nor D. bolivari completed their development so two-way ANOVA was only applied to 18 °C and 24 °C.
Table 1. Mean (± SE) lifetime fertility (total offspring produced/female), female longevity (days) and progeny sex ratio (percentage of females/total offspring) of N. tenuis, M. pygmaeus and D. bolivari preying on M. persicae nicotianae on sweet pepper leaf discs at 18, 24 and 30 ± 1 °C and 14:10 h L:D. Uppercase letters indicate significant differences between mirid species, while lowercase letters denote differences between temperatures (Two-Way ANOVA; Tukey-test; p < 0.05). * At 30 °C, neither M. pygmaeus nor D. bolivari completed their development so two-way ANOVA was only applied to 18 °C and 24 °C.
Temp.InstarN. tenuisM. pygmaeusD. bolivari
18 °CLifetime fertility0.9 ± 0.5 Ba
(n = 10)		12.2 ± 1.8 Aa
(n = 13)		20.6 ± 5.3 Aa
(n = 10)
Female longevity29.4 ± 4.2 Ba
(n = 11)		44.1 ± 2.6 Ba
(n = 13)		75.5 ± 13.4 Aa
(n = 10)
Progeny
sex-ratio		75.0 ± 25.0 Aa
(n = 4)		52.8 ± 2.1 Ba
(n = 12)		93.1 ± 3.6 Aa
(n = 7)
24 °CLifetime fertility7.3 ± 1.0 Bb
(n = 21)		3.2 ± 0.7 Ab
(n = 12)		2.7 ± 0.7 Ab
(n = 10)
Female longevity17. 1± 2.0 Bb
(n = 21)		17.8 ± 3.6 Bb
(n = 12)		29.3 ± 3.8 Ab
(n = 10)
Progeny
sex-ratio		50.9 ± 7.0 Ab
(n = 16)		42.0 ± 6.2 Bb
(n = 5)		75.8 ± 9.2 Ab
(n = 6)
30 °CLifetime fertility6.4 ± 1.6
(n = 11)		**
Female longevity7. 2± 1.3
(n = 11)		**
Progeny
sex-ratio		62.0 ± 0.1
(n = 6)		**
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Pérez-Hedo, M.; Pedroche, V.; Urbaneja, A. Temperature-Driven Selection of Predatory Mirid Bugs for Improving Aphid Control in Sweet Pepper Crops. Horticulturae 2023, 9, 572. https://doi.org/10.3390/horticulturae9050572

AMA Style

Pérez-Hedo M, Pedroche V, Urbaneja A. Temperature-Driven Selection of Predatory Mirid Bugs for Improving Aphid Control in Sweet Pepper Crops. Horticulturae. 2023; 9(5):572. https://doi.org/10.3390/horticulturae9050572

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Pérez-Hedo, Meritxell, Virginia Pedroche, and Alberto Urbaneja. 2023. "Temperature-Driven Selection of Predatory Mirid Bugs for Improving Aphid Control in Sweet Pepper Crops" Horticulturae 9, no. 5: 572. https://doi.org/10.3390/horticulturae9050572

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