Invasive pest species may strongly affect biotic interactions in agro-ecosystems. The ability of generalist predators to prey on new invasive pests may result in drastic changes in the population dynamics of local pest species owing to predator-mediated indirect interactions among prey. On a short time scale, the nature and strength of such indirect interactions depend largely on preferences between prey and on predator behavior patterns. Under laboratory conditions we evaluated the prey preference of the generalist predator Macrolophus pygmaeus Rambur (Heteroptera: Miridae) when it encounters simultaneously the local tomato pest Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and the invasive alien pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). We tested various ratios of local vs. alien prey numbers, measuring switching by the predator from one prey to the other, and assessing what conditions (e.g. prey species abundance and prey development stage) may favor such prey switching. The total predation activity of M. pygmaeus was affected by the presence of T. absoluta in the prey complex with an opposite effect when comparing adult and juvenile predators. The predator showed similar preference toward T. absoluta eggs and B. tabaci nymphs, but T. absoluta larvae were clearly less attacked. However, prey preference strongly depended on prey relative abundance with a disproportionately high predation on the most abundant prey and disproportionately low predation on the rarest prey. Together with the findings of a recent companion study (Bompard et al. 2013, Population Ecology), the insight obtained on M. pygmaeus prey switching may be useful for Integrated Pest Management in tomato crops, notably for optimal simultaneous management of B. tabaci and T. absoluta, which very frequently co-occur on tomato.
Citation: Jaworski CC, Bompard A, Genies L, Amiens-Desneux E, Desneux N (2013) Preference and Prey Switching in a Generalist Predator Attacking Local and Invasive Alien Pests. PLoS ONE 8(12): e82231. https://doi.org/10.1371/journal.pone.0082231
Editor: Joseph Clifton Dickens, United States Department of Agriculture, Beltsville Agricultural Research Center, United States of America
Received: June 16, 2013; Accepted: October 22, 2013; Published: December 2, 2013
Copyright: © 2013 Jaworski 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.
Funding: This work was supported by funds from Plant Health & Environment and Environment and Agronomy Departments of INRA, and from the French ministry of agriculture (CASDAR Project 10063) to ND. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: Dr. Nicolas Desneux is currently an Academic editor of PLOS ONE, but this does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials.
In ecosystems, species interact directly or indirectly resulting in both short-term effects on species abundance and density, and long-term effects on population dynamics [1-4]. Unlike direct interactions, indirect interactions are mediated by a third organism and may occur between organisms separated in time or space [1,5,6]. Generalist predators are likely to trigger indirect interactions among prey species owing to their capacity to attack different prey [7-9]. The nature or strength of predator-mediated indirect interactions may change over time, but are predicted to be generally positive at time scales shorter than the predator generation time (apparent mutualism or commensalism) [2,4,10]. The dispersion of predation pressure among multiple available prey species may result in increased prey population densities compared to densities in single prey systems.
The nature of indirect interactions depends in part on predator preference [11,12]. Some of the prey characteristics that influence predator preference are nutritional quality of the prey and the ease of attack it presents . Predation on prey of highest nutritive value increases the predator's fitness (higher survival, fecundity, etc...), although this prey may not be systematically preferred . Capture success generally depends on prey mobility and access to a refuge (enemy-free space) [12,13].
Generalist hemipteran predators more frequently attack mobile prey: they are able to detect movements and hunt mobile prey [12,14], whereas they tend to move randomly on plants to find stationary prey . When foraging, predators may also rely on some chemical cues to locate non-mobile prey such as semiochemicals resulting from prey oviposition or herbivore-induced plant volatiles (e.g. synomones) . The tendency of a predator to choose a given prey type over another may change as the relative frequencies of the prey species in the predator’s environment change. Switching from one prey to the other occurs when the predator over-attacks the most abundant prey, and almost ignores the rarest one . Prey switching has a stabilizing effect on prey populations as relatively scarce prey species are freed from predation and relatively common prey suffer it more frequently. Under this condition of disproportionate predation on more abundant prey, species neither go extinct nor proliferate [7,18]. This stabilizing effect of generalist predators on prey populations may have useful application for simultaneously managing multiple pest species in agro-ecosystems. Moreover, it may be a great help when developing biological control against invasive alien pest species. Invasive alien species generally have high capacities for proliferation; they may be strong competitors for resources and they may escape predation from their natural enemies when invading new regions [19,20]. Generalist predators, when switching between pests, may (i) help reduce overall pest pressure on crops and (ii) prevent new infestations by invasive alien pests [7,21].
We studied the predation behavior of the generalist mirid bug Macrolophus pygmaeus Rambur (Heteroptera: Miridae) feeding on two prey species, the local tomato pest Bemisia tabaci biotype Q (Gennadius) (Hemiptera: Aleyrodidae) and the invasive alien pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). The South American tomato pinworm T. absoluta is a major pest on tomato . It recently invaded Spain (2006) and quickly spread throughout the Afro-Eurasian continent . The larvae cause dramatic yield decreases in tomato crops (up to 100%) by mining the leaves, stems and fruits of the plants . Bemisia tabaci Biotype Q is a whitefly species from Europe [24-27] and a major pest in tomato crops causing direct and indirect (by vectoring viruses) damage [28,29]. Macrolophus pygmaeus is often used as a biocontrol agent against whiteflies (including B. tabaci). This predator also feeds on various other prey such as thrips, aphids, mites, and the eggs and larvae of Lepidoptera [30,31], notably T. absoluta [4,22,32]. It shows switching behavior when attacking whiteflies and other prey species . Macrolophus pygmaeus, being native of Europe, has co-evolved with B. tabaci; it may show both preference and adaptation to this prey over recently invading alien species such as T. absoluta. Conversely, native prey may have evolved defense mechanisms against native predators that alien prey have not developed. As evolutionary naive prey, alien prey may suffer higher predation pressure than the native prey in the invaded area [20,33]. The predation behavior of M. pygmaeus when encountering both the local (B. tabaci) and invasive alien (T. absoluta) pests has not been described yet; it could affect efficacy of this predator as a biocontrol agent in tomato crops.
In this context, under laboratory conditions, we studied (i) the predation activity of M. pygmaeus in prey complex showing various ratios of local (B. tabaci) vs. alien (T. absoluta) prey numbers, (ii) the preference of M. pygmaeus for B. tabaci vs. T. absoluta, and (iii) potential Prey switching of M. pygmaeus between B. tabaci and T. absoluta when encountering both prey at various densities.
Materials and Methods
The plants used in the experiments were tomato plants, Solanum lycopersicum L. cv. Marmande, grown in climatic chambers (23±1°C, 65±5% RH, 16L:8D) in individual plastic pots (diameter 26 cm). The prey B. tabaci and T. absoluta were reared on tobacco and tomato plants respectively, in separate cages, in a climatic chamber (23±1°C, 65±5% RH, 16L:8D). The predator M. pygmaeus was provided by Biotop© (InVivo AgroSolutions) and reared on tomato leaves (complemented with Ephestia kuehniella [Lepidoptera: Pyralidae] eggs) and maintained in growth chambers (23±1°C, 65±5% RH, 16L:8D). All predators used in the experiments lacked any previous experience of predation on B. tabaci or on T. absoluta, i.e. they were naive on these two prey. Each predator was isolated individually in a glass tube with a piece of tomato stem 24h before beginning each experiment.
We studied the predatory behavior of M. pygmaeus in prey patches containing varying densities of B. tabaci and T. absoluta, on individual tomato plants (thereafter: microcosms), using a 2 x 2 x 4 factorial design. The first two-level treatment varied the predator stage tested (adult or juvenile). The second two-level treatment varied the presence of T. absoluta in the microcosms. The third four-level treatment varied the ratio between B. tabaci and T. absoluta in the prey complex introduced into the microcosms, while the total number of prey per microcosm remained constant at 40. The ratios tested of B. tabaci - T. absoluta were 40-0, 30-10, 20-20 and 10-30. No group was tested with T. absoluta as the sole prey because such a scenario would not be realistic for European tomato crops since whiteflies always infest the tomato crops before T. absoluta arrives.
The prey and predator treatments chosen for the study were based on knowledge from the literature and from pilot experiments carried out in the lab. First, the predatory behavior of M. pygmaeus may change during its development; juveniles are assumed to have a lower satiety level than adults [30,34,35] and predatory behavioral pattern of Hemipteran juveniles can differ partially from those of adults . Second, pilot experiments showed that predation on B. tabaci eggs by M. pygmaeus was quite marginal (< 5% of B. tabaci eggs attacked by the predator when providing 20, 30 or 40 eggs on a single leaflets, n=30 replicates per density tested). In addition, M. pygmaeus attacked very few T. absoluta old larvae (L3-L4) when compared to young larvae (L1-L2) or eggs of T. absoluta (< 3% of predation on L3-L4 during pilot experiments in Petri dishes, see also ). Therefore, the developmental stages of the prey used during the experiments were third nymph instars of B. tabaci, T. absoluta eggs, and T. absoluta young larvae (L1-L2). Third, at 25°C on tomato plants, the natural mortality of eggs and larvae of T. absoluta is low (2-15% depending on the T. absoluta stage considered, Table S1) and egg incubation and L1+L2 development times are very close (4.1±1.4 days and 4.8±0.5 days respectively) . Therefore, when T. absoluta was used as prey, we used equal numbers of eggs and young larvae (L1-L2) in an attempt to create proportions of T. absoluta juvenile stages believed to occur naturally in tomato crops.
Following the design of previous studies [15,38], microcosms were created by placing a clear acetate cylinder over an individually potted tomato plant (4-week old plants with four fully expended leaves were used). Cylinders had a mesh (350 μm) top for ventilation. They were 35 cm high x 15 cm in diameter and sand was placed on the soil surface to provide a substrate into which the cylinder could be easily pushed to ensure a complete seal. All experiments were carried out at a temperature of 25±1°C, 70±5% RH and a 16L:8D photoperiod. For each B. tabaci - T. absoluta prey complex tested, crawlers of B. tabaci (first nymph instars, see ) were distributed equally among the leaves of the tomato plant with a fine brush, and nymph survival was checked 2 hours later under a microscope to ensure effective settlement of the nymphs. Plants were then placed in a climatic chamber for 7 days, sufficient time to allow B. tabaci nymphs to reach the third instar. After the 7-day period, T. absoluta eggs (laid for less than 10h ) and T. absoluta larvae (L1-L2) were deposited equally among the leaves of the tomato plant. The prey complex was allowed to settle for two hours on the plant before a single one predator (adult or juvenile) was introduced to each microcosm. The microcosms were then placed in growth chambers (25±1°C, 65±5% RH, 16L:8D). After 48h, the number of each prey type attacked by the predator was counted under a microscope.
Fifteen adult predators and 24 juvenile predators were exposed to each of the four B. tabaci - T. absoluta prey complexes. In all, 60 replicates were conducted with adult predators and 96 with juvenile predators. Data from microcosms in which the predator died or metamorphosed to an adult during the experiment were discarded from the analyses.
Normality of datasets was assessed using a Shapiro-Wilk test, and statistical analyses were carried out with R software, version 2.14.1 (R Foundation for Statistical Computing). In order to characterize how the various treatments impacted M. pygmaeus predation, we used two types of analyses.
- 1. To assess the effect of (i) the predator stage, (ii) the presence of T. absoluta (in the prey complex), and (iii) the various B. tabaci-T. absoluta prey ratios (in the prey complex) on M. pygmaeus predation activity, the total number of prey attacked per microcosm was analyzed using a GLM analysis with the ‘‘predator stage’’, “T. absoluta presence”, and ‘‘B. tabaci - T. absoluta prey ratio” as main factors.
- 2. We used Manly’s modeling works [41,42] to assess (i) the preference of M. pygmaeus for either B. tabaci or T. absoluta in the microcosms, and (ii) Prey switching in M. pygmaeus when encountering various prey ratios (B. tabaci vs. T. absoluta) in the microcosms. In the general formula of Manly, a preference for a given prey is scored as a deviation in the number of individuals of a given prey type selected for a particular action from the number of this prey type available for the action. We used the number of prey attacked as the selected action and the number of prey per prey type in the microcosm as the number of available prey. As M. pygmaeus may feed differently on egg and L1-L2 of T. absoluta , we distinguished attacks occurring on T. absoluta larvae from those on T. absoluta eggs (as well as B. tabaci nymphs). Manly’s βj of the jth prey type for predation event (with three prey types being considered) was estimated using the equation (18) of Manly et al. :
j =1, 2, 3
Ai was the number of individuals of a given prey type i available for predation by M. pygmaeus (= total number of prey available for predation) and ri was the number of a prey type i that have not been attacked (with xi the number of a prey type i attacked and xi+ri=Ai). The number of prey types was n=3 and βj = 1/ n when prey were chosen randomly (for all j). The decrease of available prey as predation occurred during the experiment was approximated with the use of logarithms [41,42]. The preference of M. pygmaeus for a given prey type over other ones (per prey complex tested, i.e. per B. tabaci - T. absoluta ratio) was tested by comparing Manly’s Beta values among T. absoluta eggs, T. absoluta larvae and B. tabaci; we used an ANOVA followed by a Tukey’s post hoc test for multiple comparisons. In addition, the occurrence of a Prey switching in M. pygmaeus was tested using a Student’s t-test that compared estimated βj values from expected values [31,41,42].
The statistical results of the GLM analysis are summarized in Table 1. The total predation activity of M. pygmaeus in the microcosms (i.e. all prey attacked, pooled per microcosm) varied significantly between the predator stages (significant ‘Predator stage’ factor); there was higher predation by adults than by juveniles (Figures 1 and 2). By contrast, neither the presence of T. absoluta nor the prey ratio (B. tabaci – T. absoluta) in the microcosm affected the predation activity of M. pygmaeus (non significant ‘Tuta absoluta’ and ‘Prey ratio’ factors). However, the ‘Predator stage’ and ‘Tuta absoluta’ factors did interact significantly; suggesting that the effect of predator stage on predation activity was function of the presence or not of T. absoluta. The presence of T. absoluta in the prey complex led to an increased predation for adults (Figure 1) whereas it led to a reduced predation activity for juveniles (Figure 2). In addition, impact of predator stage was also function of the B. tabaci – T. absoluta ratio (significant interaction between ‘Predator stage’ and ‘Prey ratio’ factors). When the prey ratio was biased toward T. absoluta, the predation activity of adult predators increased by up to 30% (Figure 1). By contrast, an increased proportion of T. absoluta in the prey ratio led to a reduction of predation activity by juveniles (Figure 2); it decreased by up to 20.5% when B. tabaci represented only 0.25 of prey available in the microcosms.
|Source of variation||Degrees of freedom||Chi-square||p-value|
|Predator stage x Tuta absoluta||1||15.14||< 0.001|
|Predator stage x Prey ratio||3||20.67||< 0.001|
Mean number (±SEM) of prey attacked by M. pygmaeus adult predators per prey type and as function of the various B. tabaci and T. absoluta prey ratio (Prey complex) tested in the microcosms. Dark grey: predation on B. tabaci nymphs; medium grey: predation on T. absoluta eggs; light grey: predation on T. absoluta larvae.
Mean number (±SEM) of prey attacked by M. pygmaeus juvenile predators per prey type and as function of the various B. tabaci and T. absoluta prey ratio (Prey complex) tested in the microcosms. Dark grey: predation on B. tabaci nymphs; medium grey: predation on T. absoluta eggs; light grey: predation on T. absoluta larvae.
The assessment of predator preference was based on the analyses of Manly’s Beta values (βj). For all B. tabaci-T. absoluta prey ratios tested, B. tabaci was the significantly preferred prey in half of the cases. It was the preferred prey for adult predators when tested at the 30-10 B. tabaci – T. absoluta ratio (Figure 3, F2,32 = 6.024, P = 0.008) and the preferred one for juvenile predators when tested at the 30-10 and 20-20 B. tabaci – T. absoluta ratio (Figure 4, F2,47 = 9.622, P < 0.001 and F2,44 = 4.409, P = 0.018, respectively). Similar situations occurred for T. absoluta eggs, except that this prey type was preferred in two cases by juvenile predators (at 20-20 and 10-30 B. tabaci – T. absoluta ratio, Figure 4, F2,44 = 4.409, P = 0.018 and F2,44 = 8.726, P = 0.001, respectively), and only once for adult predators (at 10-30 B. tabaci – T. absoluta ratio) (Figure 3, F2,35 = 10.667, P < 0.001). When compared to other prey types, T. absoluta larvae were the preferred prey only when adult predators were in microcosms containing the 10-30 B. tabaci – T. absoluta ratio. By contrast, for juvenile predators T. absoluta larvae were less preferred for all the tested prey ratios.
Manly’s Beta values (± SE) for M. pygmaeus adult predators in three-prey patches (B. tabaci nymphs, T. absoluta eggs and T. absoluta larvae) with various B. tabaci – T. absoluta prey ratios (Prey complex). Dotted line represents the expected βj value against which calculated βj values for each prey are compared (Student’s t-test, significance difference with expected βj values are indicated by arrows, at the 0.05 level). Different letters for a given B. tabaci – T. absoluta prey ratio indicate significantly different βj values between the three prey types (P > 0.05, ANOVA with Tukey’s post-hoc analysis).
Manly’s Beta values (± SE) for M. pygmaeus juvenile predators in three-prey patches (B. tabaci nymphs, T. absoluta eggs and T. absoluta larvae) with various B. tabaci – T. absoluta prey ratios (Prey complex). Dotted line represents the expected βj value against which calculated βj values for each prey are compared (Student’s t-test, significance difference with expected βj values are indicated by arrows, at the 0.05 level). Different letters for a given B. tabaci – T. absoluta prey ratio indicate significantly different βj values between the three prey types (P > 0.05, ANOVA with Tukey’s post-hoc analysis).
Prey switching in Macrolophus pygmaeus
When exposed to the various B. tabaci - T. absoluta prey ratios in the microcosms, Prey switching was observed in both adult and juvenile predators; they over-attacked the most abundant prey when the prey complex was either biased toward B. tabaci or toward T. absoluta (Figures 3 and 4). More specifically, when B. tabaci was the predominant prey (30-10 B. tabaci-T. absoluta ratio) the calculated βj values for B. tabaci were significantly higher than the expected βj values (predator adults: Figure 3, t = 2.514, df = 11, P = 0.036; predator juveniles: Figure 4, t = 3.561, df = 15, P = 0.003). By contrast at that prey ratio, the βj values for T. absoluta larvae were significantly lower than the expected βj values for this prey type (predator adults: Figure 3, t = - 2.139, df = 11, P = 0.045; predator juveniles: Figure 4, t = -2.363, df = 15, P=0.032). In a similar way, when T. absoluta was the predominant prey, i.e. at ratio 10-30 B. tabaci-T. absoluta, the calculated βj values for B. tabaci were significantly lower than the expected βj values (predator adults: Figure 3, t = - 3.902, df = 11, P = 0.002; predator juveniles: Figure 4, t = - 3.603, df = 14, P = 0.003). However, the βj values for T. absoluta eggs were significantly higher than the expected (βj values for this prey type) at the 10-30 B. tabaci - T. absoluta prey ratio (predator adults: Figure 3, t = 2.873, df = 11, P = 0.015; predator juveniles: Figure 4, t = 2.584, df = 14, P=0.022). When B. tabaci and T. absoluta were evenly present in the microcosms (ratio 20-20 B. tabaci-T. absoluta), no prey was over- or under-attacked by the predator (all P ≥ 0.102) except for T. absoluta larvae that were les attacked by predator juveniles than predicted by the expected βj value (Figure 4, t = - 2.853, df = 14, P=0.013).
Our study confirmed the predation of M. pygmaeus on the local pest B. tabaci and the invasive pest T. absoluta as previously reported by Bompard et al. . We further demonstrated that, in the short term, preference toward a given prey type depended on the ratio between the prey species B. tabaci and T. absoluta on the tomato plant. In addition, we showed that the presence of T. absoluta on the plant affected the predation activity of M. pygmaeus in opposite ways for predator adults and juveniles: the presence of T. absoluta induced an increase of predation by predator adults whereas it led to decreased predation by juveniles. That decrease for juveniles was mainly due to low predation on T. absoluta larvae; the more T. absoluta larvae present in the prey complex, the lower the overall predation activity by predator juveniles. We demonstrated that M. pygmaeus can exhibit Prey switching  when foraging in areas where both T. absoluta and B. tabaci are present in varying proportion; the predator consistently showed disproportionately high and low predation on the most abundant and the rarest prey, respectively.
Overall, the predation activity of M. pygmaeus juveniles was lower than predation by adults, as already highlighted in a previous study . We believe this may result from the limited ability of juveniles to attack T. absoluta larvae. We noted that adult and juvenile predators attacked a similar number of B. tabaci nymph when the nymph was the sole prey in the microcosms (comparison of adult and juvenile predators for the prey ratio 40-0 B. tabaci – T. absoluta in Figures 1 and 2). This lower predation activity of juveniles on T. absoluta larvae may be due to the prey size relative to the predator size, which can impact prey preference in generalist predators . This possibility is consistent with the increased predation activity recorded for predator adults when T. absoluta larvae were present in the microcosms since predator adults are bigger than juveniles and more able to attack bigger prey. Morphological characteristics of M. pygmaeus juveniles, such as a shorter rostrum than adults, may also explain the low predation on T. absoluta larvae since juveniles may not be able to attack T. absoluta that are hidden inside mines in tomato leaves; attacking these larvae requires piercing both the tomato leaf and larvae cuticle. In our study, M. pygmaeus juveniles took likely more time to attack T. absoluta larvae than to attack B. tabaci nymphs and T. absoluta eggs. The presence of T. absoluta larvae in a prey patches may lead to an overall reduced efficiency of M. pygmaeus juveniles as predators. By contrast, M. pygmaeus adults showed increased predation activity when T. absoluta larvae were present in the prey patch.
When considering the M. pygmaeus population as a whole (i.e. adults + juveniles) the net outcome of the reduced predation activity of juveniles coupled with the increased predation activity of adults is unclear. However, a previous study demonstrated the positive effect of T. absoluta presence on the biocontrol of B. tabaci by M. pygmaeus in tomato greenhouses . This suggests that the positive effect on adult predation activity might overwhelm the negative effect on juvenile activity. In our study M. pygmaeus juveniles did show an active predation behavioral pattern despite T. absoluta larvae presence; they may still participate noticeably in pest regulation on the tomato plants despite presence of T. absoluta larvae.
Prey preference in generalist predators is driven by trade-offs among various mechanisms, notably the ease of attacking different prey as well as the differing nutritional value of the various prey to the predator . The ease of attacking a given prey depends on various characteristics, the main factors are (i) the capacity to detect prey, (ii) how easy the predator can access to prey, (iii) the defenses exhibited by prey against predators, and (iv) the capacity to effectively feed on prey [15,44-46]. Hemipteran predators are able to forage specifically for mobile prey by detecting prey movements, whereas they forage for non-mobile prey through random movements both on and among plants that may host prey [14,15,47]. In our study, the only mobile prey was T. absoluta larvae. However, T. absoluta larvae spend most of their time feeding and moving in leaf mines where they are less accessible to predators . This possibility to benefit from spatial refuges within the plant could explain the lower predation on this prey type . A higher predation rate on eggs than on larvae of T. absoluta has already been reported in a previous study ; however this study was not based on choice tests while our study further documented M. pygmaeus preference between T. absoluta eggs and larvae in a choice scenario.
Several factors may explain a possible preference of the predator for T. absoluta eggs over B. tabaci nymphs. This preference may occur because handing time (i.e. time between first encounter with a prey and the end of predation event, see ) of T. absoluta egg by M. pygmaeus is much faster than on B. tabaci nymph (20-30 min. and 4-5 min., respectively, Jaworski CC, personal observation). In addition, T. absoluta is a lower quality food than B. tabaci for M. pygmaeus; during a pilot experiment, we observed lower fecundity and longevity of M. pygmaeus fed on T. absoluta eggs than when fed on B. tabaci nymphs (Figure S1), and a recent study also reported poor nutritional value of T. absoluta eggs for M. pygmaeus . Moreover, we suppose the size of the two prey to be of low importance because they are in the same size range (400µm. for T. absoluta eggs vs. 500µm for B. tabaci nymphs [51,52]).
In our study, the absence of a clear preference of M. pygmaeus between T. absoluta eggs and B. tabaci nymphs highlighted the importance of Prey switching  in the predation behavior of this predator. Predation preference depended strongly on the relative abundances of the prey species, with a disproportionately high predation on the most abundant prey and a disproportionately low predation on the rarest prey. Such Prey switching had been previously reported for M. pygmaeus preying upon B. tabaci and the spider mites  and it is thought to be exhibited by many generalist predators . Clumped and patched prey distributions are common in natural conditions, leading to spatial heterogeneities and context-dependent predation behaviors. Prey switching can enable predators to maximize food intake by increasing foraging time in patches showing high density of one prey type ; M. pygmaeus likely benefits from such adaptative behavior when foraging in crops where B. tabaci and T. absoluta co-occur.
Our study confirmed the ability of M. pygmaeus to attack T. absoluta (already suggested by previous results under greenhouse and laboratory conditions, respectively [4,37,46]) and demonstrated that the predator is able to switch between the alien and the local prey when foraging in habitats hosting both prey. However, the low nutritive quality of T. absoluta for M. pygmaeus ( and Figure S1) tempers any conclusion about its potential to be a good candidate for the biological control of T. absoluta in tomato crops (at least not as the key natural enemy of T. absoluta in tomato crops if not included in a broader IPM program; see ). Using M. pygmaeus as a biocontrol agent against T. absoluta would require the presence of an alternate prey to sustain growth of the predator population. In a situation requiring simultaneous control of both B. tabaci and T. absoluta, the presence of T. absoluta might disrupt the biocontrol of B. tabaci in the short term because M. pygmaeus would spend time attacking T. absoluta eggs and larvae (larvae to a lesser extent). Greenhouse experiments showed a transient disruption of the predation on B. tabaci by M. pygmaeus when T. absoluta was present in the tomato crop, but the control of B. tabaci populations was enhanced in the long terms . The Prey switching exhibited by M. pygmaeus when encountering both B. tabaci and T. absoluta prey might prevent fast population growth of either of the two prey (as stressed in other studies on generalist predators [7,17,54]). If Prey switching is maintained at larger scales (agro-ecosystem) it may help regulating both prey populations simultaneously to low densities. Macrolophus pygmaeus could be useful for IPM programs since the probability for both B. tabaci and T. absoluta to be present simultaneously in tomato crops is high in numerous areas cropped with tomato in Afro-Eurasia [22,23]. The presence of B. tabaci on tomato crops early in the season may help M. pygmaeus populations to establish prior to T. absoluta infestation. The knowledge gained during our studies ( and the present study) and previous theoretical works on Prey switching suggest that M. pygmaeus may not attack T. absoluta before this prey becomes abundant in the field [17,54]. However, a small primary infestation of tomato plants by T. absoluta may rapidly lead to very high population densities owing to its high reproduction rate  and the capacity of M. pygmaeus to effectively limit T. absoluta population growth could be exceeded [4,55]. In addition, the fact that T. absoluta is a low quality food for M. pygmaeus may be detrimental in the long term to value of the biocontrol service provided by M. pygmaeus. High rates of attacks on prey without a significant increase in predator fitness have already been reported for Hemipteran predators in laboratory and field studies [8,15] and such predation behavior may lead to a relatively good control of T. absoluta by M. pygmaeus in the short term. However, the predator's biocontrol efficacy may be reduced in the long term by its lower population growth when consuming prey of poor nutritive value. Prey switching in M. pygmaeus when attacking B. tabaci and T. absoluta needs to be further assessed at larger scales including direct field observations along with an assessment of the impact of poor quality food on the ability of this predator to provide useful biocontrol services [4,56].
Natural mortality of T. absoluta under laboratory conditions at the various instars. Survival of T. absoluta from egg to adulthood was evaluated by placing T. absoluta eggs individually (n=60) in aerated plastic boxes (diameter: 110 cm, height: 2 cm, with a circular opening made of nylon mesh netting, 350 mm2) together with a single tomato leaf. The tomato steam was inserted in a tube containing water. Boxes were placed in rearing chambers (23±1°C, 65±5% RH, 16L:8D) and we followed T. absoluta development until death or adulthood.
(A) Mean longevity (± SEM) of Macrolophus pygmaeus adult (in days) and (B) mean daily fertility (± SEM) of M. pygmaeus (offspring per day per female). Longevity and fecundity were evaluated by placing M. pygmaeus adults individually (n=40) in aerated plastic boxes (diameter: 110 cm, height: 2 cm, with a circular opening made of nylon mesh netting, 350 mm) together with a single tomato leaf (replaced every day for further assessment of offspring production). The tomato steam was inserted in a tube filled with water. Insects were provided daily with the prey ad libitum (B. tabaci nymphs and T. absoluta eggs) accordingly to respective treatment. Boxes were placed in rearing chambers (23±1°C, 65±5% RH, 16L:8D). Histograms bearing different letters are significantly different to each other (P < 0.05, GLM followed by a Tukey’s post-hoc test). GLM results: (A) Chi-square = 6.60, df = 2, P = 0.037; (B) Chi-square = 13.26, df = 2, P = 0.001.
We thank Antonio Biondi, Anaïs Chailleux, Tim Oppenheim and two anonymous reviewers for helpful comments on the manuscript, Philippe Bearez for assistance throughout the experiments and Jacques Frandon (Biotop, invivo AgroSolutions) for providing some biological materials.
Conceived and designed the experiments: ND CJ AB LG EAD. Performed the experiments: CJ AB LG EAD. Analyzed the data: ND CJ AB. Contributed reagents/materials/analysis tools: ND. Wrote the manuscript: ND CJ.
- 1. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25: 443-466. doi:10.1146/annurev.es.25.110194.002303.
- 2. Abrams PA, Matsuda H (1996) Positive indirect effects between prey species that share predators. Ecology 77: 610-616. doi:10.2307/2265634.
- 3. Tack AJM, Gripenberg S, Roslin T (2011) Can we predict indirect interactions from quantitative food webs? - an experimental approach. J Anim Ecol 80: 108-118. doi:10.1111/j.1365-2656.2010.01744.x. PubMed: 20796204.
- 4. Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55: 433-440. doi:10.1007/s10144-013-0371-8.
- 5. Mouttet R, Bearez P, Thomas C, Desneux N (2011) Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions. PLOS ONE 6: e18840. doi:10.1371/journal.pone.0018840. PubMed: 21611161.
- 6. Mouttet R, Kaplan I, Bearez P, Amiens-Desneux E, Desneux N (2013) Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites. Oecologia. doi:10.1007/s00442-013-2716-6. PubMed: 23851986.
- 7. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47: 561-594. doi:10.1146/annurev.ento.47.091201.145240. PubMed: 11729085.
- 8. Desneux N, O’Neil RJ, Yoo HJS (2006) 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 35: 1342-1349. Available online at: doi:10.1603/0046-225X(2006)35[1342:SOPGOT]2.0.CO;2.
- 9. Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487: 362-365. doi:10.1038/nature11153. PubMed: 22722864.
- 10. Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25: 495-520. doi:10.1146/annurev.es.25.110194.002431.
- 11. Chaneton EJ, Bonsall MB (2000) Enemy-mediated apparent competition: empirical patterns and the evidence. Oikos 88: 380-394. doi:10.1034/j.1600-0706.2000.880217.x.
- 12. Eubanks MD, Denno RF (2000) Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species. Ecol Entomol 25: 140-146. doi:10.1046/j.1365-2311.2000.00243.x.
- 13. Fantinou A, Perdikis D, Labropoulos P, Maselou D (2009) Preference and consumption of Macrolophus pygmaeus preying on mixed instar assemblages of Myzus persicae. Biol Control 51: 76-80. doi:10.1016/j.biocontrol.2009.06.006.
- 14. Venzon M, Janssen A, Sabelis MW (2002) Prey preference and reproductive success of the generalist predator Orius laevigatus. Oikos 97: 116-124. doi:10.1034/j.1600-0706.2002.970112.x.
- 15. Desneux N, O’Neil RJ (2008) 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 98: 631-639. doi:10.1017/S0007485308006238. PubMed: 18845007.
- 16. Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37: 141-172. doi:10.1146/annurev.en.37.010192.001041.
- 17. Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol Monogr 39: 335-354. doi:10.2307/1942352.
- 18. Oaten A, Murdoch WW (1975) Switching, functional response, and stability in predator-prey systems. Am Nat 109: 299-318. doi:10.1086/282999.
- 19. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17: 170-176. doi:10.1016/S0169-5347(02)02495-3.
- 20. Li Y, Ke Z, Wang S, Smith GR, Liu X (2011) An exotic species is the favorite prey of a native enemy. PLOS ONE 6: e24299. doi:10.1371/journal.pone.0024299. PubMed: 21915306.
- 21. Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and Management of the Soybean Aphid in North America. Annu Rev Entomol 56: 375-399. doi:10.1146/annurev-ento-120709-144755. PubMed: 20868277.
- 22. Desneux N, Wajnberg E, Wyckhuys K, Burgio G, Arpaia S et al. (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83: 197-215. doi:10.1007/s10340-010-0321-6.
- 23. Desneux N, Luna M, Guillemaud T, Urbaneja A (2011) 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 84: 403-408. doi:10.1007/s10340-011-0398-6.
- 24. Qiu BL, Dang F, Li SJ, Ahmed M, Jin FL et al. (2011) Comparison of biological parameters between the invasive B biotype and a new defined Cv biotype of Bemisia tabaci (Hemiptera: Aleyradidae) in China. J Pest Sci 84: 419-427. doi:10.1007/s10340-011-0367-0.
- 25. McKenzie CL, Bethke JA, Byrne FJ, Chamberlin JR, Dennehy TJ et al. (2012) Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in North America after the Q invasion. J Econ Entomol 105: 753-766. doi:10.1603/EC11337. PubMed: 22812110.
- 26. Parrella G, Scassillo L, Giorgini M (2012) Evidence for a new genetic variant in the Bemisia tabaci species complex and the prevalence of the biotype Q in southern Italy. J Pest Sci 85: 227-238. doi:10.1007/s10340-012-0417-2.
- 27. Saleh D, Laarif A, Clouet C, Gauthier N (2012) Spatial and host-plant partitioning between coexisting Bemisia tabaci cryptic species in Tunisia. Population Ecol 54: 261-274. doi:10.1007/s10144-012-0303-z.
- 28. Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Protect 20: 709-723. doi:10.1016/S0261-2194(01)00108-9.
- 29. Jiao X, Xie W, Wang S, Wu Q, Zhou L et al. (2012) Host preference and nymph performance of B and Q putative species of Bemisia tabaci on three host plants. J Pest Sci 85: 423-430. doi:10.1007/s10340-012-0441-2.
- 30. Fauvel G, Malausa J, Kaspar B (1987) Laboratory studies on the main biological characteristics of Macrolophus caliginosus (Heteroptera: Miridae). Entomophaga 32: 529-543. doi:10.1007/BF02373522.
- 31. Enkegaard A, Brodsgaard HF, Hansen DL (2001) Macrolophus caliginosus: functional response to whiteflies and preference and switching capacity between whiteflies and spider mites. Entomol Exp Appl 101: 81-88. doi:10.1046/j.1570-7458.2001.00893.x.
- 32. Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnò J et al. (2013) 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. doi:10.1007/s10340-013-0531-9.
- 33. Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD et al. (2010) Predator-prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119: 610-621. doi:10.1111/j.1600-0706.2009.18039.x.
- 34. Perdikis D, Lykouressis D (2000) Effects of various items, host plants, and temperatures on the development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Biol Control 17: 55-60. doi:10.1006/bcon.1999.0774.
- 35. Perdikis DC, Lykouressis DP (2002) Life table and biological characteristics of Macrolophus pygmaeus when feeding on Myzus persicae and Trialeurodes vaporariorum. Entomol Exp Appl 102: 261-272. doi:10.1046/j.1570-7458.2002.00947.x.
- 36. Harwood JD, Yoo HJS, Greenstone MH, Rowley DL, O'Neil RJ (2009) Differential impact of adults and nymphs of a generalist predator on an exotic invasive pest demonstrated by molecular gut-content analysis. Biol Invasions 11: 895-903. doi:10.1007/s10530-008-9302-6.
- 37. Urbaneja A, Monton H, Molla O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133: 292-296. doi:10.1111/j.1439-0418.2008.01319.x.
- 38. Desneux N, Stary P, Delebecque CJ, Gariepy TD, Barta RJ et al. (2009) Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxyx koreanus; Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae). Ann Entomol Soc Am 102: 925-936. doi:10.1603/008.102.0603.
- 39. Simmons AM (1999) Nymphal survival and movement of crawlers of Bemisia argentifolii (Homoptera : Aleyrodidae) on leaf surfaces of selected vegetables. Environ Entomol 28: 212-216. PubMed: 11543187.
- 40. Chailleux A, Desneux N, Seguret J, Maignet P, Khanh HDT et al. (2012) Assessing European egg parasitoids as a mean of controlling the invasive south American tomato pinworm Tuta absoluta. PLOS ONE 7: e48068. doi:10.1371/journal.pone.0048068. PubMed: 23144727.
- 41. Manly B (1973) A linear model for frequency-dependent selection by predators. Researches on Population Ecol 14: 137-150. doi:10.1007/BF02518839.
- 42. Manly BFJ (1974) A model for certain types of selection experiments. Biometrics 30: 281-294. doi:10.2307/2529649.
- 43. Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17: 507-513. doi:10.1016/S0169-5347(02)02615-0.
- 44. Guershon M, Gerling D (1999) Predatory behavior of Delphastus pusillus in relation to the phenotypic plasticity of Bemisia tabaci nymphs. Entomol Exp Appl 92: 239-248. doi:10.1046/j.1570-7458.1999.00543.x.
- 45. Butler C, O'Neil R (2006) Defensive response of soybean aphid (Hemiptera : Aphididae) to predation by insidious flower bug (Hemiptera : Anthocoridae). Ann Entomol Soc Am 99: 317-320. Available online at: doi:10.1603/0013-8746(2006)099[0317:DROSAH]2.0.CO;2.
- 46. Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R et al. (2013) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest, Tuta absoluta. J Pest Sci 86: 533-541. doi:10.1007/s10340-013-0498-6.
- 47. Rosenheim JA, Wilhoit LR, Armer CA (1993) Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96: 439-449. doi:10.1007/BF00317517.
- 48. Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16: 945-956. doi:10.1093/beheco/ari075.
- 49. Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE (2009) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160: 387-398. doi:10.1007/s00442-009-1289-x. PubMed: 19219460.
- 50. Molla O, Alonso-Valiente M, Biondi A, Urbaneja A (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. Biol_Control. In press.
- 51. Johnson F, Short D, Castner J (1997) Sweetpotato/silverleaf whitefly life stages and damage. Entomology and Nematology Department SP 90. Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. Available: http://edis.ifas.ufl.edu/IN004.
- 52. Cabello T, Gallego J, Vila E, Soler A, del Pino M et al. (2009) Biological control of the South American tomato pinworm, Tuta absoluta (Lep.: Gelechiidae), with releases of Trichogramma achaeae (Hym.: Trichogrammatidae) in tomato greenhouses of Spain. IOBC/WPRS Bul 49: 225-230.
- 53. Murdoch WW, Briggs CJ, Nisbet RM (2003) Consumer resource dynamics. Princeton: Princeton University Press.
- 54. Kimbrell T, Holt R (2005) Individual behaviour, space and predator evolution promote persistence in a two-patch system with predator switching. Evol Ecol Res 7: 53-71.
- 55. Jaworski C, Bompard A, Béarez P, Desneux N (2011) Potential for apparent competition between endemic and invasive pests on tomato. 9ème Conférence Internationale sur les Ravageurs en Agriculture, 26 - 27 october 2011 – Montpellier SupAgro, France.
- 56. Kuusk AK, Ekbom B (2010) Lycosid spiders and alternative food: feeding behavior and implications for biological control. Biol Control 55: 20-26. doi:10.1016/j.biocontrol.2010.06.009.