Abstract
The limited availability of sugar sources (e.g., flowers) in greenhouses may affect biological pest control by parasitoid wasps. However, few studies have focused on feeding devices to provide parasitoids with sugar foods. We investigated the accessibility of a yellow-colored bottle-type feeding device to adult Cotesia vestalis (Halliday), a larval endoparasitoid of the diamondback moth Plutella xylostella (L.). All parasitoids died within four days in a room with no sugar source, whereas 66.7 % of individuals survived if a bottle-type feeding device providing honey solution was installed. We also investigated female longevity in response to different sugar solutions presented in a bottle-type feeding device. Honey and sugar mixtures (glucose and fructose) improved female longevity (38.4 and 39.2 days, respectively) much more than water (3.1 days), indicating these feeding devices containing sugar foods to be potentially useful for maintaining C. vestalis in greenhouses where natural food sources are limited.
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Introduction
Many parasitoid wasps depend on sugar-rich foods, such as (extra-) floral nectars and insect honeydews, for at least part of their diet (Wäckers 2001). Sugar foods affect the longevity, lifetime fecundity, host-searching behavior and parasitism of parasitoids (Röse et al. 2006; Bianchi and Wäckers 2008; Wäckers et al. 2008; Hirose et al. 2009). Some parasitoids visit sugar sources several times daily, due to their vulnerability to starvation (Siekmann et al. 2001; Azzouz et al. 2004; Winkler et al. 2005). However, sugar sources are often limited in greenhouses where no flowering plants are cultivated. The limited availability of sugar foods may thus deleteriously affect biological control by parasitoids (Takasu and Lewis 1993; Bianchi and Wäckers 2008).
The effectiveness of parasitoid wasps can be enhanced by spraying sugar solutions on crop plants (Jacob and Evans 1998; Wade et al. 2008) and by providing non-crop plants that produce (extra-) floral nectars (Lewis et al. 1998; Cortesero et al. 2000; Witting-Bissinger et al. 2008). Although these methods have been investigated for use in conservation biological control (Landis et al. 2000; Mills and Wajnberg 2008; Wade et al. 2008), their application might have its drawbacks. For example, sticky sugar solutions may stain the surfaces of the crop (Mitsunaga et al. 2012) and there are risks of causing plant disease on the sprayed crops (Ben Saad and Bishop 1976) and facilitating herbivory of the sugar-sprayed crop by pest insects that are attracted to the sugar (Winkler et al. 2005; Wäckers et al. 2007). Further, in greenhouses, planting non-crop plants decreases the cropping area available and may interfere with farm work (Mitsunaga et al. 2012). A possible solution to these problems is to supply sugar from artificial feeders. We have focused on feeding devices that mimic attractive flowers. The visual and olfactory cues of flowers can attract foraging parasitoids (Wäckers 1994; Kugimiya et al. 2010b). Such visual and olfactory preferences might be used to lure them to the feeding devices. Various types of feeding devices such as cups and bottles containing honey or other sugar solutions are empirically used to maintain parasitoid cultures in laboratories (Harvey et al. 2012). However, few studies have investigated artificial food supplementation as part of biological control.
The larval endoparasitoid Cotesia vestalis (Halliday) (Hymenoptera: Braconidae) is an important natural enemy of the diamondback moth Plutella xylostella (L.) (Lepidoptera: Yponomeutidae), a major pest of cruciferous vegetables in many countries (Talekar and Shelton 1993; Kawaguchi and Tanaka 1999; Furlong et al. 2013). C. vestalis does not show host-feeding behavior, and when supplied with sugar-rich foods such as floral nectars and honey, it show better survival and parasitic abilities than if denied sugar-containing foods (Mitsunaga et al. 2004; Kugimiya et al. 2010a, 2010b). Foraging C. vestalis individuals can use visual and olfactory cues to locate flowering plants (Kugimiya et al. 2010b). In regard to visual cues, C. vestalis innately prefer yellow over other colors such as red, orange or blue (Mitsunaga et al. 2012; Uefune et al. 2013). We have demonstrated that the placement of yellow sponges soaked with honey solution, hereinafter called “sponge-type feeding devices,” improved their rate of parasitism on P. xylostella-infested Brassica plants in greenhouses (Abe et al. 2007; Mitsunaga et al. 2012). However, the potential use of other types of feeding devices with honey or sugar solutions has hitherto not been tested experimentally.
The main purpose of this study was to evaluate the usefulness of "bottle-type feeding devices" for providing honey or other sugar solutions under laboratory conditions. We first investigated the survival rates of C. vestalis females in climate-controlled rooms in which yellow-colored, bottle-type or sponge-type feeding devices were installed to evaluate the accessibility of each feeding device. We then examined the influence of different sugar solutions on the survival ability of C. vestalis females in sealed plastic cases to seek out suitable food sources. Finally, we investigated their survival periods when accessing bottle-type feeding devices containing different food solutions in netted plastic cages to determine prototypes of feeding devices appropriate for use in greenhouses. In this paper, we show that yellow-colored, bottle-type feeding devices containing honey or sugar mixtures (glucose and fructose) are potentially the most useful for maintaining C. vestalis in greenhouses where natural food sources are limited.
Materials and methods
Plants and insects
Komatsuna plants (Brassica rapa, var. perviridis, cv. Rakuten) were cultivated in a greenhouse (23 ± 2 °C, 50 ± 10 RH and 16L:8D). Four plants were grown in commercial compost in a plastic pot (9 cm in diameter, 7 cm in depth) for 4–5 weeks and then used for both insect rearing and the experiments. Larvae and pupae of P. xylostella were collected from fields in Ayabe, Kyoto Prefecture, Japan, in 2001 and 2002, and mass-reared on komatsuna plants in a climate-controlled room (23 ± 1 °C, 60 ± 10 RH and 16L:8D). C. vestalis, originating from parasitized P. xylostella larvae in the same fields, was mass-reared on P. xylostella-infested komatsuna plants under the same conditions as their hosts. Virgin females within 4 h of emergence from their cocoons, individually maintained in glass vials, were used in this study, since there was no significant difference in longevity between virgin and mated females (Mitsunaga et al. 2006).
Feeding devices
Bottle-type feeding devices comprised a plastic bottle (diameter: 5 cm, height: 7 cm) with a plastic interior lid for storing sugar solutions, a capillary bundle of polypropylene fibers (diameter: 1.2 cm, length: 7 cm) for supplying the sugar solutions, and a yellow-colored plastic cap for attracting the parasitoids (Fig. 1a, b, c). Both of the interior lid and the yellow cap had a hole (diameter: 1.2 cm) to allow insertion of the capillary bundle into the bottle. Sponge-type feeding devices consisted of yellow polyurethane sponges (diameter: 9 cm, thickness: 2 cm) soaked with sugar solution and placed in laboratory glass dishes (diameter: 9 cm, depth: 1.8 cm, Fig. 1d).
Experiment 1: accessibility of the feeding devices to the parasitoids
To confirm parasitoid access to bottle-type feeding devices, survival experiments were conducted in a climate-controlled room (3.5 × 3.5 × 2.7 m) in which 25 komatsuna pots (four plants per pot) were arranged in a 5 × 5 grid pattern at 50-cm intervals (25 ± 1 °C, 50 ± 10 RH and 16L:8D). A bottle-type device containing 50 % (v/v) honey solution was placed on a yellow board (20 × 20 cm, 1 cm thick, citron yellow, SUMIPEX #250, Sumitomo Acryl Co., Ltd, Tokyo, Japan) installed at the center of the room. One adult female was introduced to the room and the status (dead or alive) of the same parasitoid was recorded daily for four days. If the living wasp was not found in each day, we judged the wasp to be dead and thus stopped the observation. The same experiments were carried out using a sponge-type device containing 50 % (v/v) honey solution placed on the yellow board and with no other feeding devices, as positive and negative control treatments respectively (Fig. 1d). Each treatment was repeated 12 times (females).
Experiment 2: influence of sugar foods on female longevity
To search for a suitable sugar source to prolong adult longevity, C. vestalis females were individually introduced into sealed plastic cases (8.2 cm in diameter, 2.4 cm in depth, V-2, AS ONE Corporation, Osaka, Japan) containing: (1) water, (2) 1 M glucose solution, (3) 1 M fructose solution, (4) a mixture of glucose and fructose (1 M each), or (5) 50 % (v/v) honey solution. Five 10-ml aliquots of water or food solution were placed on the bottom of each case. The cases were placed in an incubator (25 ± 1 °C, 50 ± 10 RH and 16L:8D) and examined once a day to investigate the survival period of each parasitoid. Thirty females were used for each treatment.
To search for a suitable concentration of sugar mixtures, we then conducted the same experiments using different concentrations of glucose and fructose (0.1, 0.25, 0.5 and 1 each), or water alone as a control. Thirty females were used in each experiment. Other conditions and procedures were the same as those describe above.
Experiment 3: effectiveness of bottle-type feeding devices
To assess the potential usefulness of bottle-type feeding devices for maintaining female parasitoids, 25 female wasps were introduced into a netted plastic cage (25 × 33 × 30 cm) containing a komatsuna pot (four plants per pot) and a bottle-type feeding device containing: (1) water, (2) a mixture of glucose and fructose (1 M each), or (3) 50 % (v/v) honey solution. Cages were maintained in a climate-controlled room (25 ± 1 °C, 50 ± 10 RH and 16L:8D). The number of dead parasitoids was recorded once daily to calculate the survival period for each treatment. Fifty females were tested in each experiment.
Statistical analysis
In experiment 1, the Kaplan–Meier survival analysis with log-rank test followed by the Bonferroni correction (P < 0.05/α = 0.016, α = 3 being the number for all combinations of the three treatments) was used to compare the survival probabilities of females depending on different feeding devices (for the details of statistical analyses, see, Sokal and Rohlf 1995; Meyhöfer and Hindayana 2000; Tang et al. 2014). In Experiments 2 and 3, we used one-way ANOVA followed by Tukey’s HSD test. The data for female longevity were log-transformed to fit the analyses. Each test was performed using JMP software package (version 10.0.2, SAS Institute Inc., Cary, NC, USA).
Results
Experiment 1: accessibility of feeding devices to the parasitoids
The survival rate of parasitoids in terms of the accessibility of feeding devices containing honey solutions showed a significant difference among the three treatments (χ 2 = 11.011; df = 2; P < 0.01; Fig. 2). All parasitoid females introduced were dead within four days in the climate-controlled room with no sugar source. In contrast, 66.7 % of the parasitoids were still alive four days after their release into the room in which a bottle-type feeding device was placed, and 50 % of the individuals with access to a sponge-type feeding device were alive after four days.
Experiment 2: influence of sugar foods on female longevity
Food condition significantly affected parasitoid survival. There was a significant difference in the parasitoid longevity among the five treatments (F = 375.880; df = 4, 145; P < 0.001; Fig. 3a). Adult females survived only an average of 3.6 days in sealed plastic cases when fed water alone. However, the provision of glucose significantly improved their survival ability (15.3 days). The effect of fructose (18.6 days) and honey (20.0 days) was significantly higher than that of glucose. The highest average value for longevity was obtained with a mixture of glucose and fructose (1 M each, 28.8 days). The effect of the sugar mixture was significantly higher than those of the other four treatments.
Blended concentrations of the sugars, i.e., mixtures of glucose and fructose, also affected female longevity (F = 1119.562; df = 4, 145; P < 0.001; Fig. 3b). Adult females survived an average of 30 days or longer in sealed plastic cases when offered high concentrations of sugar mixtures (0.5 M each: 30.8 days, 1 M each: 30.6 days). However, females survived only several days when offered low concentrations of sugars (0.1 M each: 5.0 days, 0.25 M each: 4.7 days) or water alone (3.6 days).
Experiment 3: effectiveness of bottle-type feeding device
Adult females survived an average of 3.1 days under caged conditions with no sugar source (Fig. 4). In contrast, parasitoids with access to bottle-type feeding devices containing honey solution survived 38.4 days, with the same results observed for devices containing a mixture of glucose and fructose (1 M each, 39.2 days). There was thus a significant difference among the three treatments as to survival period (F = 1859.832; df = 2, 147; P < 0.001).
Discussion
When considering feeding devices for parasitoids, the following two questions need to be addressed. The first is how efficiently parasitoids can find them in greenhouses. One idea for enhancing the accessibility of feeding devices is to use a flower-like color that is attractive to parasitoids. Starved C. vestalis females are attracted to Brassica flowers with bright yellow petals (Kugimiya et al. 2010b). The parasitoids can be lured to sponge-type feeding devices in greenhouses by utilizing their innate preference for the color yellow (Mitsunaga et al. 2012; Uefune et al. 2013). Our results indicate that the parasitoids were able to access yellow-colored, bottle-type feeding devices to a similar degree to yellow-colored, sponge-type devices (Fig. 2). Presumably, the parasitoids were not able to distinguish the subtle color difference between the two feeding devices and/or were equally attracted to either one, although their color preference can be modified by associative learning with foraging experience (Wäckers and Lewis 1994; Lucchetta et al. 2008).
The second issue that needs to be addressed is what sugar solutions are most suitable as artificial food supplements. The present investigation supports our previous study suggesting that honey is a suitable food for maintaining C. vestalis (Mitsunaga et al. 2004): adult females accessing honey solutions in bottle-type feeding devices survived much longer than those with water alone (38.4 vs. 3.1 days; Fig. 4). We also noted the suitability of mixtures of fructose and glucose (39.2 days: Fig. 4). These results do not contradict previous studies showing that fructose and glucose are the main components of most (extra-) floral nectars and many honeydews (Wäckers 2001) and that C. vestalis can exploit floral nectars and aphid honeydews as a suitable food source (Kugimiya et al. 2010a, 2010b). The fructose-glucose mixtures (0.5 and 1 M each) increased female lifespan by more than each of the sugar compounds, unless the concentrations of the sugar mixtures were low (0.1 and 0.25 M each) (Figs. 3a, b). Some reports show that combinations of sugars have a positive or even negative influence on parasitoid longevity, when compared with individual sugars (Wäckers 2001; Harvey et al. 2012). Further, increased longevity of other parasitoids fed with higher sugar concentrations has also been reported, such as C. rubecula (Halliday) (Siekmann et al. 2001) and Aphidius ervi (Halliday) (Hymenoptera: Braconidae) (Azzouz et al. 2004); longevity of A. ervi was attributed to the energetic value (carbohydrate concentration) of the sugar solutions rather than the quantity of the sugar solutions ingested (Azzouz et al. 2004). It is not clear which of these factors is more important for C. vestalis longevity, although sufficient amounts (50-ml aliquots) of sugar solutions were provided to parasitoids in the experiment. More research is needed to clarify the influence on C. vestalis longevity of other sugars or their mixtures at different concentrations.
Although this study showed the potential utility of bottle-type feeding devices for maintaining C. vestalis in greenhouses, there are three questions to be clarified. First, the relative influence of honey or other sugar solutions on their lifetime fecundity remains to be tested. For example, honey and glucose enhance the longevity of Gelis agilis Fabricius (Hymenoptera: Ichneumonidae), a hyperparasitoid of the primary parasitoid C. glomerata L., to similar degrees, whereas honey enhances the lifetime fecundity of G. agilis to a greater extent than glucose. The presence of proteins as well as sugars in honey may result in increased egg production (Harvey et al. 2012). However, honey and other sugars may enhance the lifetime fecundity to similar degrees in other endoparasitoids. Second, there is a need to evaluate the continuity of sugar foods provided by different types of feeding devices. For example, unlike sugar solutions in bottle-type feeding devices, honey solutions in sponge-type devices might be more likely to dry quickly, decay and grow mold in hot greenhouse environments. Third, it has not yet been clarified whether olfactory as well as visual cues of flowers can be used to attract parasitoids to feeding devices. Kugimiya et al. (2010b) have reported that starved C. vestalis females can find flowering plants by the aid of these cues. Addition of floral volatiles to feeding devices might be of use to lure them in greenhouses where yellow sticky traps are often set to catch flying pest insects.
Further studies should aim to explore the usefulness of yellow-colored feeding devices with sugar foods in biological pest control by C. vestalis and other parasitoids. Abe et al. (2007) reported that the release of five C. vestalis females resulted in the parasitization of approx. 90 % of 111 P. xylostella larvae on 2215 komatsuna plants in greenhouses in which several sponge-type feeding devices with honey solutions had been placed. Further, these feeding devices should be accessible by other parasitoid species, since yellow is a typical, attractive flower-color to parasitoids (Wäckers 1994) and because many parasitoids depend entirely or primarily on sugar-rich foods (Wäckers 2001). However, we should note the following two points in connection with the use of feeding devices. First, we need to evaluate the usefulness of the artificial feeding system for host-feeding parasitoids, as well as non host-feeding parasitoids, including C. vestalis. Provision of sugar foods might enhance the effectiveness of some species of host-feeding parasitoids (Harvey et al. 2012; Mills and Wajnberg 2008), although this may be less likely in other species that closely depend on host-derived foods (Wade et al. 2008). The second point to note is that supplying sugar using feeding devices and other methods (e.g., sugar spraying and the use of nectar-producing plants) involves the risk of facilitating herbivory by pest insects (Landis et al. 2000; Romeis et al. 2005; Winkler et al. 2009). In cruciferous pest insects, for instance, sucrose, glucose, and fructose can enhance the adult longevity of P. xylostella to similar degrees (Winkler et al. 2005). This is also true for the longevity and fecundity of the pea leafminer Chromatomyia horticola (Goureau) (Diptera: Agromyzidae) (Mitsunaga et al. 2006). On the other hand, it is known that parasitoids can utilize a range of sugars that are unsuitable for its herbivorous host (Wäckers 2001). Selecting the most suitable foods provided by feeding devices that can exclusively or primarily support parasitoids would contribute to the development of more efficient methods of conservation biological control.
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Acknowledgments
We thank Ms. Kimiko Kanbe, Ms. Yumiko Togashi and Ms. Yoshiko Ishimura for rearing the insects and growing the plants. This research was supported by the Bio-oriented Technology Research Advancement Institution and JSPS KAKENHI Grant Numbers (24780049 for SK, 19380188 and 22380038 for TS).
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Shimoda, T., Mitsunaga, T., Uefune, M. et al. A food-supply device for maintaining Cotesia vestalis, a larval parasitoid of the diamondback moth Plutella xylostella, in greenhouses. BioControl 59, 681–688 (2014). https://doi.org/10.1007/s10526-014-9611-x
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DOI: https://doi.org/10.1007/s10526-014-9611-x