Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Life-History Traits of Macrolophus pygmaeus with Different Prey Foods

  • Serigne Sylla ,

    syllaserigne2@gmail.com

    Affiliations Université Cheikh Anta Diop (UCAD), Equipe Production et Protection Intégrées en Agroécosystèmes Horticoles - 2PIA, Faculté des Sciences et Techniques, Dakar, Senegal, BIOPASS, ISRA-UCAD-IRD, Dakar, Senegal

  • Thierry Brévault,

    Affiliations BIOPASS, ISRA-UCAD-IRD, Dakar, Senegal, CIRAD, UPR AIDA, F-34398 Montpellier, France

  • Karamoko Diarra,

    Affiliation Université Cheikh Anta Diop (UCAD), Equipe Production et Protection Intégrées en Agroécosystèmes Horticoles - 2PIA, Faculté des Sciences et Techniques, Dakar, Senegal

  • Philippe Bearez,

    Affiliation INRA (French National Institute for Agricultural Research), Univ. Nice Sophia Antipolis, CNRS, UMR 1355–7254, Institut Sophia Agrobiotech, 06903, Sophia Antipolis, France

  • Nicolas Desneux

    Affiliation INRA (French National Institute for Agricultural Research), Univ. Nice Sophia Antipolis, CNRS, UMR 1355–7254, Institut Sophia Agrobiotech, 06903, Sophia Antipolis, France

Life-History Traits of Macrolophus pygmaeus with Different Prey Foods

  • Serigne Sylla, 
  • Thierry Brévault, 
  • Karamoko Diarra, 
  • Philippe Bearez, 
  • Nicolas Desneux
PLOS
x

Abstract

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.

Introduction

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 [13]; the infestation is likely to persist even in Northern parts of the Eurasian continent [2] as the pest is able to overwinter successfully e.g. in Belgium [4]. 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 [11]. 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 [1417]. 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 [20]. 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 [2123]. 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 [20]. 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 [26]. 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 [27]. 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).

Feeding bioassays

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.

Statistical analyses

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).

Results

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).

thumbnail
Fig 1. Median duration of nymphal stages (days ± SEM) of Microlophus pygmaeus fed on Tuta absoluta eggs, Ephestia kuehniella eggs, M. euphorbiae nymphs or Bemisia tabaci nymphs.

Bars topped by same letter are not statistically different (P < 0.05).

https://doi.org/10.1371/journal.pone.0166610.g001

thumbnail
Fig 2. Mean survival (± SEM) of immature stages of Macrolophus pygmaeus fed on Tuta absoluta eggs, Ephestia kuehniella eggs, Macrosiphon euphorbiae nymphs or Bemisia tabaci nymphs.

https://doi.org/10.1371/journal.pone.0166610.g002

thumbnail
Fig 3. Mean fertility (number of first-instar nymphs ± SEM) of Macrolophus pygmaeus fed on Tuta absoluta eggs, Ephestia kuehniella eggs, Macrosiphon euphorbiae nymphs or Bemisia tabaci nymphs.

Bars topped by same letter are not statistically different (P < 0.05).

https://doi.org/10.1371/journal.pone.0166610.g003

Discussion

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 [20]. 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 [30]. 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 [25].

Higher fitness was observed when M. pygmaeus fed on M. euphorbiae nymphs. Our results corroborate previous studies [17,27,3334] 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. [35] 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 [26]. 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) [36].

Integrated pest management (IPM) strategies are being increasingly used in open field and greenhouse crops [3739]. 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 [10]. 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.

Acknowledgments

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.

Author Contributions

  1. Conceived and designed the experiments: SS ND.
  2. Performed the experiments: SS TB PB ND.
  3. Analyzed the data: SS.
  4. Contributed reagents/materials/analysis tools: SS TB KD PB ND.
  5. Wrote the paper: SS TB ND.

References

  1. 1. Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, et al. Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci. 2010;83: 197–215.
  2. 2. Desneux N, Luna MG, Guillemaud T, Urbaneja A. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci. 2011;84: 403–408.
  3. 3. Guillemaud T, Blin A, Le Goff I, Desneux N, Reyes CM, Tabone E, Tsagkarakou A, et al. The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Sci Rep. 5:8371. pmid:25667134
  4. 4. Van Damme V, Berkvens N, Moerkens R, Berckmoes E, Wittemans L, De Vis R, et al. Overwintering potential of the invasive leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) as a pest in greenhouse tomato production in Western Europe. J Pest Sci. 2015;88: 533–541.
  5. 5. Biondi A, Desneux N, Siscaro G, Zappalà L. Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: Selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere. 2012;87: 803–812. pmid:22342338
  6. 6. Desneux N, Decourtye A, Delpuech J-M. The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol. 2007;52: 81–106. pmid:16842032
  7. 7. Campos MR, Silva TBM, Silva WM, Silva JE, Siqueira HAA. Spinosyn resistance in the tomato borer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Pest Sci. 2015;88: 405–412.
  8. 8. Roditakis E, Vasakis E, Grispou M, Stavrakaki M, Nauen R, Gravouil M, et al. First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci. 2015;88: 9–16.
  9. 9. Urbaneja A, Desneux N, Gabarra R, Arnó J, González-Cabrera J, Mafra Neto A, et al. Biology, ecology and management of the South American tomato pinworm, Tuta absoluta. Potential Invasive Pests Agric Crops. 2013;3: 98.
  10. 10. Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnò J, Bayram A, et al. Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci. 2013;86: 635–647.
  11. 11. Symondson WOC, Sunderland KD, Greenstone MH. Can Generalist Predators Be Effective Biocontrol Agents?1. Annu Rev Entomol. 2002;47: 561–594. pmid:11729085
  12. 12. Perez-Hedo M, Urbaneja A. Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci. 2015;88: 65–73.
  13. 13. Perez-Hedo M, Bouagga S, Jaques JA, Flors V, Urbaneja A. Tomato plant responses to feeding behavior of three zoophytophagous predators (Hemiptera: Miridae). Biol Control. 2015;86: 46–51.
  14. 14. Alomar Ò, Goula M, Albajes R. Colonisation of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agric Ecosyst Environ. 2002;89: 105–115.
  15. 15. Castañé C, Zapata R. Rearing the predatory bug Macrolophus caliginosus on a meat-based diet. Biol Control. 2005;34: 66–72.
  16. 16. Castañé C, Arnó J, Gabarra R, Alomar O. Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control. 2011;59: 22–29.
  17. 17. Perdikis D, Fantinou A, Lykouressis D. Enhancing pest control in annual crops by conservation of predatory Heteroptera. Biol Control. 2011;59: 13–21.
  18. 18. Han P, Bearez P, Adamowicz S, Lavoir A-V, Amiens-Desneux E, Desneux N. Nitrogen and water limitations in tomato plants trigger negative bottom-up effects on the omnivorous predator Macrolophus pygmaeus. J Pest Sci. 2015;88: 685–691.
  19. 19. Urbaneja A, Montón H, Mollá O. Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol. 2009;133: 292–296.
  20. 20. Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A. A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. BioControl. 2014;59: 175–183.
  21. 21. Perdikis D, Lucas E, Garantonakis N, Giatropoulos A, Kitsis P, Maselou D, et al. Intraguild predation and sublethal interactions between two zoophytophagous mirids, Macrolophus pygmaeus and Nesidiocoris tenuis. Biol Control. 2014;70: 35–41.
  22. 22. Put K, Bollens T, Wäckers FL, Pekas A. Type and spatial distribution of food supplements impact population development and dispersal of the omnivore predator Macrolophus pygmaeus (Rambur) (Hemiptera: Miridae). Biol Control. 2012;63: 172–180.
  23. 23. Vandekerkhove B, Parmentier L, Van Stappen G, Grenier S, Febvay G, Rey M, et al. Artemia cysts as an alternative food for the predatory bug Macrolophus pygmaeus. J Appl Entomol. 2009;133: 133–142.
  24. 24. Jaworski CC, Chailleux A, Bearez P, Desneux N. Apparent competition between major pests reduces pest population densities on tomato crop, but not yield loss. J Pest Sci. 2015;88: 793–803.
  25. 25. Bompard A, Jaworski CC, Bearez P, Desneux N. Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol. 2013;55: 433–440.
  26. 26. Perdikis DC, Lykouressis DP. Life table and biological characteristics of Macrolophus pygmaeus when feeding on Myzus persicae and Trialeurodes vaporariorum. Entomol Exp Appl. 2002;102: 261–272.
  27. 27. DíazI HLB, LouzadaII E, MouraII N, de los Ángeles Martínez M, RiveroI VEPB. Life table of Macrolophus basicornis (Hemiptera: Miridae) preying on Myzus persicae (Sulzer) and Macrosiphum euphorbiae (Thomas)(Hemiptera: Aphididae). Rev Protección Veg. 2014;29: 94.
  28. 28. Perdikis DC, Lykouressis DP, Economou LP. The influence of temperature, photoperiod and plant type on the predation rate of Macrolophus pygmaeus on Myzus persicae. BioControl. 1999;44: 281–289.
  29. 29. Perdikis DC, Lykouressis DP. Myzus persicae (Homoptera: Aphididae) as suitable prey for Macrolophus pygmaeus (Hemiptera: Miridae) population increase on pepper plants. Environ Entomol. 2004;33: 499–505.
  30. 30. Jaworski CC, Bompard A, Genies L, Amiens-Desneux E, Desneux N. Preference and Prey Switching in a Generalist Predator Attacking Local and Invasive Alien Pests. Dickens JC, editor. PLoS ONE. 2013;8: e82231. pmid:24312646
  31. 31. Desneux N, O’neil RJ, Yoo HJS. Suppression of population growth of the soybean aphid, Aphis glycines Matsumura, by predators: the identification of a key predator and the effects of prey dispersion, predator abundance, and temperature. Environ Entomol. 2006;35: 1342–1349.
  32. 32. Desneux N, O’Neil RJ. Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions. Bull Entomol Res. 2008;98: 631–639. pmid:18845007
  33. 33. Perdikis DC, Lykouressis DP. Myzus persicae (Homoptera: Aphididae) as Suitable Prey for Macrolophus pygmaeus (Hemiptera: Miridae) Population Increase on Pepper Plants. Environ Entomol. 2004;33: 499–505.
  34. 34. Pérez-Hedo M, Urbaneja A. Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci. 2015;88: 65–73.
  35. 35. Lykouressis D, Giatropoulos A, Perdikis D, Favas C. Assessing the suitability of noncultivated plants and associated insect prey as food sources for the omnivorous predator Macrolophus pygmaeus (Hemiptera: Miridae). Biol Control. 2008;44: 142–148.
  36. 36. Carletto J, Lombaert E, Chavigny P, BréVault T, Lapchin L, Vanlerberghe-Masutti F. Ecological specialization of the aphid Aphis gossypii Glover on cultivated host plants. Mol Ecol. 2009;18: 2198–2212. pmid:19635073
  37. 37. Lenteren JC van. Success in Biological Control of Arthropods by Augmentation of Natural Enemies [Internet]. Springer Netherlands; 2000. Available: http://link.springer.com/chapter/10.1007/978-94-011-4014-0_3
  38. 38. Bockmann E, Hommes M, Meyhofer R. Yellow traps reloaded: what is the benefit for decision making in practice? J Pest Sci. 2015;88: 439–449.
  39. 39. Nogia VK, Meghwal RR. Resistance in cotton strains and cultivars to Bemisia tabaci (Hemiptera: Aleyrodidae): leaf shape. Entomol Gen. 2014;35: 11–19.
  40. 40. Jiao XG, Xie W, Guo LT, Liu BM, Wang SL, Wu QJ, Zhang YJ. Differing effects of cabbage and pepper on B and Q putative species of Bemisia tabaci. J Pest Sci. 2014;87: 629–637.
  41. 41. Losey JE, Denno RF. Positive predator-predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology. 1998;79: 2143–2152.
  42. 42. LaRock DR, Ellington JJ, others. An integrated pest management approach, emphasizing biological control, for pecan aphids. Southwest Entomol. 1996;21: 153–166.
  43. 43. Chailleux A, Desneux N, Arnó J, Gabarra R. Biology of two key palaearctic larval ectoparasitoids when parasitizing the invasive pest Tuta absoluta. J Pest Sci. 2015;87: 441–448.