Journal of Insect Physiology 47 (2001) 1077–1084 www.elsevier.com/locate/jinsphys A comparison of nectar- and honeydew sugars with respect to their utilization by the hymenopteran parasitoid Cotesia glomerata F.L. Wa¨ckers * Institute of Plant Sciences, Applied Entomology, Swiss Federal Institute of Technology (ETH), 8092 Zurich, Switzerland Received 10 October 2000; received in revised form 12 February 2001; accepted 19 February 2001 Abstract Fourteen naturally occurring sugars were individually tested with respect to their effect on Cotesia glomerata longevity. Parasitoids kept with solutions of either sucrose, glucose and fructose lived for Ͼ30 days. This constitutes a factor 15 increase in life span in comparison to control individuals kept with water only. Stachyose, mannose, melezitose, melibiose, maltose and erlose increased parasitoid longevity by a factor of 11.2–6.9. Solutions of galactose and trehalose had a marginal, but still significant effect. Lactose and raffinose did not raise parasitoid longevity, while rhamnose actually reduced parasitoid survival. In an additional experiment, the relationship between quantity of sugar consumption and longevity was established for all 14 sugars. To study the effect of an unsuitable sugar in sugar mixtures, a range of glucose:rhamnose mixtures was tested. Even at 20% of the sugar mixture rhamnose suppressed the nutritional benefit of the 80% glucose. The nutritional suitability of the sugars shows a positive correlation with the previously reported gustatory response towards the individual sugars. Patterns of sugar utilization are discussed with respect to hydrolytic enzymes and carbohydrate biochemical characteristics. Our findings for C. glomerata are compared to patterns of sugar utilization reported for other species. The comparison between C. glomerata and its host Pieris brassicae reveals that the parasitoid is capable of utilizing a range of sugars that are unsuitable to its herbivorous host. This specificity opens up opportunities to select food supplements for biological control programs that selectively target the antagonist, without concurrently enhancing herbivore fitness. 2001 Elsevier Science Ltd. All rights reserved. Keywords: Carbohydrate; Hymenoptera; Feeding; Enzymes 1. Introduction et al., 1996) extrafloral nectar (e.g., Bugg et al., 1989) and honeydew (Zoebelein, 1955). The sugar composition The majority of adult parasitoids depend entirely or of nectar and honeydew shows a broad variation both primarily on carbohydrates as an energy source (Jervis regarding the type of sugars present and the overall sugar et al., 1993). Both the parasitoid’s longevity and fec- concentration. Sucrose and its hexose components glu- undity are usually subject to energetic constraints cose and fructose are the most prevalent sugars in nectars (Leatemia et al., 1995), while the parasitoid’s behavior and honeydews (Baker and Baker, 1983; Kloft et al., can be strongly affected by its nutritional state as well 1985; Koptur, 1992). However, various other sugars can (Takasu and Lewis, 1995; Wa¨ckers, 1994). There is occur as well, sometimes in significant concentrations strong theoretical as well as empirical evidence that the (Table 1). availability of suitable sugar sources can play a key role Insect species can vary considerably with respect to in parasitoid host dynamics (Krivan and Sirot, 1997; the spectrum of nectar- and honeydew-sugars they can Wa¨ckers, unpublished data). utilize. Longevity studies indicate that distinct differ- The principle carbohydrate sources available to para- ences exist between insects in their ability to utilize sitoids are floral nectar (Idris and Grafius, 1995; Wa¨ckers particular sugars (Ferreira et al., 1998). Even though nectar or sugar supplements are increasingly rec- ommended as a tool to enhance parasitoid performance * Current address: NIOO CTO, P.O. Box 40, 6666 ZG Heteren, the (Jacob and Evans, 1998), little is known with regard to Netherlands. Tel.: +0031-26-479-1306; fax: +0031-26-472-3227. the suitability of individual carbohydrates as parasitoid E-mail address: [email protected] (F.L. Wa¨ckers). food sources. While a number of studies have quantified 0022-1910/01/$ - see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S0022-1910(01)00088-9 1078 F.L. Wa¨ckers / Journal of Insect Physiology 47 (2001) 1077–1084 Table 1 compare their longevity to that of a control group pro- a Natural (exogenous) sources for the sugars used in these experiments vided with water only. However, this approach fails to Source establish actual food consumption as it does not differen- tiate between lack of nutritional suitability and lack of Monosaccharides feeding stimulation. To account for this potential prob- Glucose Main sugar in: lem, a second experiment was conducted in which the —various (extra)floral nectars sugar consumption during a single feeding bout and sub- —honeydew Fructose Main sugar in: sequent survival of individual parasitoids was estab- —various (extra)floral nectars lished. —honeydew Galactose —(extra)floral nectar —honeydew 2. Materials and methods Mannose —traces in floral nectar and fruits Rhamnose —extra floral nectar Disaccharides 2.1. Insects Sucrose Main sugar in: —various (extra)floral nectars Cotesia glomerata were reared on Pieris brassicae fed —honeydew with Brussels sprouts plants [Brassicae oleracea (L.) Trehalose —honeydew (insect synthesized) = ° = Maltose —coccid honeydew var. Gemmifera]atT 21 C; RH 60%; 16L:8D. Two —floral nectar days after the parasitoid larvae had egressed from their Melibiose —floral nectar host, parasitoid coccoons were collected and transferred —eucalyptus exudate (manna) to a climate chamber (T=15°C; RH=95%; 16L:8D). Lactose —fruits of Achras sapota Upon emergence, groups of 30–40 parasitoids of both Trisaccharides Raffinose —primarily in honeydew (plant sexes were transferred to polypropylene cages derived and insect synthesized) (30×30×30 cm). Parasitoids were neither exposed to —some floral nectars food or water prior to the experiments. Water depri- Melezitose —primarily in honeydew (insect vation was required to assure some level of sugar uptake synthesized) even for those sugars that fail to stimulate feeding —rare in (extra)floral nectars Erlose —honeydew (Wa¨ckers, 1999). Tertrasaccharide Stachyose —honeydew 2.2. Longevity experiments: single sugars a Literature references for the sources of sugars mentioned in this One day following emergence, cohorts of 10 unfed C. table are available direct from the author if required. glomerata females were placed in plexiglas containers (7×3×14 cm) and offered three drops (10 µl each) of a the effect of the three more common nectar sugars 1M sugar solution. A control group was offered water (sucrose, fructose and glucose) on parasitoid longevity on a wet filter paper. The following sugars were tested: (Leatemia et al., 1995; Morales-Ramos et al., 1996; the monosaccharides glucose, fructose, galactose, man- McDougall, 1997), few have extended their assays to nose, and rhamnose, the disaccharides sucrose, trehalose, include additional carbohydrates. Zoebelein (1955) maltose, melibiose, and lactose the trisaccharides raf- included melezitose and dextrin in his longevity experi- finose, melezitose, and erlose, as well as the tetrasacch- ments with Microplectron uscipennis, while Ponnamma aride stachyose. Even though a number of these sugars and Kurian (1983) compared six sugars and mannitol do not elicit feeding behavior in food deprived C. glo- (a sugar alcohol) with respect to their effect on Bracon merata, they do not deter liquid uptake by water brevicornis longevity. deprived individuals (Wa¨ckers, 1999). Since no separate To obtain a more comprehensive overview on carbo- water source was provided in this experiment, parasit- hydrate utilization by the ecologically and economically oids could be expected to consume all sugar solutions important group of Hymenopteran parasitoids, I tested a irrespective of their feeding stimulatory properties. All range of 14 naturally occurring sugars (listed in Fig. 1) sugar solutions were renewed weekly through a reseal- with respect to their suitability as food sources for Cote- able hole in the container. This renewal schedule was sia glomerata (L.) (Hymenoptera: Braconidae). This based on HPLC analyses, showing microbial breakdown species represents the large group of parasitoids whose of sugars when solutions were exposed for longer per- adult nutrition is likely entirely restricted to carbohydrate iods. Due to the tendency of melezitose and raffinose to rich solutions, as it refrains from feeding on host haemo- crystallize, these two sugar solutions had to be renewed lymph or pollen (Wa¨ckers, personal observation). daily. The high humidity in the climate chamber and the The common practice in sugar suitability assays is to hygroscopic property of the other sugars prevented keep individuals with a particular sugar solution and their crystallization. F.L. Wa¨ckers / Journal of Insect Physiology 47 (2001) 1077–1084 1079 Fig. 1. Average longevity of C. glomerata females when provided with solutions of individual sugars. A total of 30 parasitoids were tested with each sugar. Different letters indicate significant differences (Fisher PLSD). Error bars represent standard deviations. Survival of the parasitoids was scored daily. A total ence. Parasitoids were transferred to a vial containing a of 30 parasitoids were tested with each sugar. Data were droplet (5 µl) of a 1M solution of an individual sugar.