Macrolophus pygmaeus Rambur (Hemiptera: Miridae) is a generalist predatory mirid widely used in augmentative biological control of various insect pests in greenhouse tomato production in Europe, including the invasive tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera, Gelechiidae). However, its biocontrol efficacy often relies on the presence of alternative prey. The present study aimed at evaluating the effect of various prey foods (Ephestia kuehniella eggs, Bemisia tabaci nymphs, Tuta absoluta eggs and Macrosiphum euphorbiae nymphs) on some life history traits of M. pygmaeus. Both nymphal development and adult fertility of M. pygmaeus were significantly affected by prey food type, but not survival. Duration of nymphal stage was higher when M. pygmaeus fed on T. absoluta eggs compared to the other prey. Mean fertility of M. pygmaeus females was greatest when fed with B. tabaci nymphs, and was greater when offered M. euphorbiae aphids and E. kuehniella eggs than when offered T. absoluta eggs. Given the low quality of T. absoluta eggs, the efficacy of M. pygmaeus to control T. absoluta may be limited in the absence of other food sources. Experiments for assessing effectiveness of generalist predators should involve the possible impact of prey preference as well as a possible prey switching.
Citation: Sylla S, Brévault T, Diarra K, Bearez P, Desneux N (2016) Life-History Traits of Macrolophus pygmaeus with Different Prey Foods. PLoS ONE 11(11): e0166610. https://doi.org/10.1371/journal.pone.0166610
Editor: Patrizia Falabella, Universita degli Studi della Basilicata, ITALY
Received: June 21, 2016; Accepted: October 13, 2016; Published: November 21, 2016
Copyright: © 2016 Sylla et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: ata are from the Tuta absoluta study whose authors may be contacted at email@example.com
Funding: We express our sincere gratitude to IRD (AIRD) under Grant PEERS-BIOBIO-2013, CIRAD (Action incitative 2014), and IFS for financial support.
Competing interests: The authors have declared that no competing interests exist.
The tomato leaf miner, Tuta absoluta (Meyrik) (Lepidoptera, Gelechiidae) is a major invasive pest. Originating from South America, T. absoluta was first detected in Spain in 2006 and has spread to several European, Middle Eastern, Africa North of the Sahel and sub-Saharan Africa countries [1–3]; the infestation is likely to persist even in Northern parts of the Eurasian continent  as the pest is able to overwinter successfully e.g. in Belgium . Losses can reach 100% of both field and greenhouse production for fresh market due to leaf mining and fruit damage. Tomato growers often rely on systematic use of insecticides to control T. absoluta infestations, with potentially undesired side effects on non-target organisms [5,6], and potential selection of insecticide-resistant T. absoluta populations [7,8]. Integrated pest management (IPM) is promoted by FAO and Europe (Directive 2009/128/EC) as a sustainable approach to crop protection that minimizes the use of pesticides. It is based on the combination of preventive methods and monitoring of pests and their damage, but also on the use of biological, physical, and other sustainable non-chemical methods if they provide suitable pest control. Biological control (BC) which relies on the use of living organisms (natural enemies) to reduce pest populations is a key component of IPM [1,9,10]. It includes classical (introduction of natural enemies to a new area), augmentation (supplemental release of natural enemies), and conservation BC (habitat managed to favor natural enemies). However, biological control is not widely implemented in pest management programs, mostly due to growers’ lack of knowledge on biology and ecology of both pests and their natural enemies.
Generalist predators are known to greatly contribute to biological control of many agricultural pests in the word . In the last five years, studies have documented the biology and effectiveness of the zoophytophagous predatory Macrolophus pygmaeus Rambur (Hemiptera, Miridae) to control various crop pests [12,13] Those predatory mirids are efficient natural enemies for controlling whiteflies, thrips, aphids, mites and lepidopteran pests [14–17]. Recent results showed that M. pygmaeus is also a suitable predator of the invasive pest T. absoluta [2,10,18,19], This predatory mirid is a key component of newly developed integrated pest management (IPM) for tomato crops in Europe. However, predatory mirids need alternative prey to establish and increase their populations . For example, studies showed that M. pygmaeus populations increase when they feed on Ephestia kuehniella (Lepidoptera, Pyralidae) eggs and Artemia cysts as alternative food sources [21–23]. Moreover, it has been shown that T. absoluta on tomato plants as exclusive food source was insufficient to obtain a significant and stable M. pygmaeus population, compared to feeding on E. kuehniella eggs on tomato . However, the association of Bemisia tabaci (Gennadius) (Hemiptera, Aleyrodidae) and T. absoluta as food source for M. pygmaeus provides effective pest control [24,25]. Macrosiphum euphorbiae (Thomas) and Myzus persicae (Sulzer) (Homoptera, Aphididae) are the rare aphid species that can survive on tomato plants . Some studies indicate that Macrolophus basicornis (Hemiptera: Miridae) can survive and reproduce with M. euphorbiae aphids as prey, but that this food source negatively affects female fertility . Studies on the seasonal abundance of aphids and their natural enemies in tomato fields in 1992–1993 in Greece showed that M. pygmaeus was the most important predator of aphids [26,28]. M. pygmaeus develops also well on the aphid M. persicae on pepper and tomato [26,29]. However, little is known on M. pygmaeus fitness when feeding of M. euphorbiae. The present study aimed at comparing nymphal development time and reproductive performance of M. pygmaeus when preying T. absoluta eggs, E. kuechniella eggs, B. tabaci nymphs, or M. euphorbiae aphids.
Materials and Methods
Plants and insects
Plants used in the experiments were 5 week-old tomato plants, Solanum lycopersicum L. (cv Marmande) grown in climatic chambers at 24 ± 1°C, 60 ± 5% RH, and photoperiod16L: 8D. T. absoluta, B. tabaci and M. euphorbiae were reared on caged tomato plants (120 x 70 x 125 cm) in climatic chambers at 24 ± 1°C, 60 ± 5% RH, and photoperiod16L: 8D. Both B. tabaci and T. absoluta insects originated from a lab colony, respectively reared on tobacco and tomato plants. M. euphorbiae aphids were collected from INRA-ISA tomato greenhouses. M. pygmaeus adults and E. kuehniella eggs were provided by Biotop (Livron-sur-Drôme, France).
Development time and juvenile survival of M. pygmaeus were assessed according to different food sources: (a) T. absoluta eggs, (b) B. tabaci nymphs, (c) M. Euphorbiae nymphs and (d) E. kuehniella eggs. Newly emerged M. pygmaeus nymphs (at stage N1) were individually transferred into 10-ml tubes with one tomato leaflet. Every two days, tubes were checked for nymphal stage. Food was supplied every two days and the quantity offered depended on the nymphal stage of the predator. Food quantity offered to each nymphal stage was estimated following a preliminary experiment in the laboratory. M. pygmaeus nymphal stages N1, N2, N3, N4, and N5, were respectively offered 10, 18, 24, 32, 36 T. absoluta eggs, 8, 12, 16, 24, 24, 28 E. kuehniella eggs, 20, 24, 24, 40, 40 B. tabaci nymphs, and 20, 20, 30, 30, 30 M. euphorbiae nymphs. The tomato leaflet was changed when necessary. Nymphal development and survival were checked daily until either death or adulthood. Nymphs that died on the first day of the experiment were replaced by new ones, as it was assumed that this was not due to prey food. Each test was replicated 30 times.
Ten newly emerged pairs of M. pygmaeus adults originating from the previous bioassay were transferred to ventilated plastic cups (7 cm-diameter, 10 cm-height) containing 5-week old tomato plants. M. pygmaeus adults were fed with respective food until the female died. Each pair was transferred to a new plastic cup with another tomato plant every 4 days. For each plastic cup, total offspring (first-instar nymphs) produced per female was recorded twelve days later because, by counting nymphs, as eggs laid by M. pygmaeus on plant stems are hardly visible.
Analyses were performed with the R software version 3.2.2 (R Development Core Team). Prior to analysis, data from experiment were tested for normality (Shapiro-Wilk test) and homogeneity of variances (Bartlett test). Development time (from N1 to N5) of nymphs and fecundity (number of first instar nymphs produced per female) were analyzed using generalized linear models (GLM) based respectively on a Poisson (link = log) and a Gaussian (link = identity) distribution. Post hoc multiple comparisons of mean values were performed using the Newman–Keuls method (package multcomp). Survival rates were compared using a Kaplan Meier survivorship test (SPSS).
A significant effect of prey food on the development time (N1 to N5) of M. pygmaeus was observed (F3, 103 = 16.6, P < 0.001). M. pygmaeus required more time to reach the adult stage when offered exclusively T. absoluta eggs, compared to E. kuehniella eggs, M. euphorbiae and B. tabaci nymphs (Fig 1). However, prey food did not affect survival of M. pygmaeus Kaplan Meier survivorship (Breslow Generalized Wilcoxon test); χ2 = 3.182; df = 3; P = 0.364 (Fig 2). A significant effect of prey food on the number of first-instar nymphs produced per female was observed (F3, 36 = 142.9, P ˂ 0.001). Mean fertility of M. pygmaeus females was greatest when fed with B. tabaci nymphs, and was greater when offered M. euphorbiae aphids and E. kuehniella eggs than when offered T. absoluta eggs (Fig 3).
Bars topped by same letter are not statistically different (P < 0.05).
The present study showed a longer duration of nymphal development and lower fertility of M. pygmaeus when fed with T. absoluta eggs, compared to other prey foods such as E. kuehniella eggs, B. tabaci nymphs and M. euphorbiae nymphs. Our results support a previous study showing that fertility was lower when M. pygmaeus were fed with T. absoluta eggs compared to E. kuehniella eggs . However, authors did not show significant differences between prey foods regarding development time. T. absoluta eggs are probably of low nutritional quality for the generalist predator M. pygmaeus, and its role as a biocontrol agent is probably limited in the absence of other food sources. Other studies showed that M. pygmaeus can exhibit prey switching when foraging in patches with disproportionate densities of T. absoluta and B. tabaci . This particular behavior might result in effective regulation of both prey populations [24,25]. The same phenomenon has been observed for the generalist predator, Orius insidiosus (Hemiptera:Anthocoridae), in presence of the soybean aphid [31,32]. Thus, alternative prey could provide good control of T. absoluta by increasing density of M. pygmaeus populations .
Higher fitness was observed when M. pygmaeus fed on M. euphorbiae nymphs. Our results corroborate previous studies [17,27,33–34] indicating that aphids in general are good prey for M. pygmaeus. These authors showed that M. persicae as a food source increases M. pygmaeus longevity and reproduction rate, especially when these aphids were reared on pepper plants. Thus, nutritional value of aphids is probably linked to host plant quality or aphid adaptation. Lykouressis et al.  reported similar trend when Aphis fabae solanella (Hemiptera, Aphididae) were fed on Solanum nigrum L. compared to Dittrichia viscosa (L.) Greuter, (Asteraceae). Opposite effect was observed with other aphid species. For example, development of M. pygmaeus was inhibited when fed on A. gossypii on cucumber or Capitophorus inulae (Homoptera: Aphididae) on D. viscosa . Fitness of predators such as M. pygmaeus might depend not only on the type of prey food but also on the host plant of the prey. It could also depend on both the host plant and genotype of the prey. For example, fitness of A. gossypii on different host plants such as cucumber, cotton, okra and eggplant, depends on genotype (host races) .
Integrated pest management (IPM) strategies are being increasingly used in open field and greenhouse crops [37–39]. In the last three decades, invasive pests such as the leafminer, Liriomyza trifolii (Diptera: Agromyzidae), thrips, Frankliniella occidentalis (Thysanoptera: Thripidae) and the whitefly B. tabaci [24,25,40] have posed a major threat for the continuous production of vegetable crops. Nowadays, these pests are fully integrated in agro-ecosystems and are successfully controlled by IPM programs based on the use of natural enemies, particularly generalist predators . The same trend has been experienced for the control of aphids [41,42] and T. absoluta [10,20,43]. Our results show that M. euphorbiae, as an aphid species capable of colonizing tomato crops, is of good quality as food source for M. pygmaeus. They also confirm that B. tabaci and E. kuehniella are of good quality as food source for M. pygmaeus. They could be useful for IPM programs to control T. absoluta pest when present simultaneously in tomato crops. These results indicate that experiments on predation should involve preference and prey switching of M. pygmaeus in order to assess the effectiveness of generalist predators to efficiently control T. absoluta infestations.
We express our sincere gratitude to IRD (AIRD) under Grant PEERS-BIOBIO-2013, CIRAD (Action incitative 2014), and IFS for financial support. We thank Edwige Amiens-Desneux and Han Peng (INRA) for input and advice during the experiments.
- Conceived and designed the experiments: SS ND.
- Performed the experiments: SS TB PB ND.
- Analyzed the data: SS.
- Contributed reagents/materials/analysis tools: SS TB KD PB ND.
- Wrote the paper: SS TB ND.
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