Journal of Physiology 47 (2001) 1077–1084 www.elsevier.com/locate/jinsphys

A comparison of nectar- and honeydew 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 , and lived for Ͼ30 days. This constitutes a factor 15 increase in life span in comparison to control individuals kept with water only. , , , melibiose, and erlose increased parasitoid longevity by a factor of 11.2–6.9. Solutions of and had a marginal, but still significant effect. and raffinose did not raise parasitoid longevity, while actually reduced parasitoid survival. In an additional experiment, the relationship between quantity of 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 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 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 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 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 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 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 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 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. log10-transformed, and subsequently tested for nor- Upon contact with the sugar solution parasitoids were mality of distribution using a K–S Normality Test. As allowed to feed ad libitum. Those individuals that failed initial ANOVA statistics showed no container effect, this to show a feeding response were discarded from the test. factor was omitted from subsequent analyses. Transfor- Consumption (in percentage of the individual’s body med data were tested for the effect of sugar using weight) was determined by weighing the individual para- ANOVA analysis of variance. Differences between treat- sitoid on a precision scale (Mettler MT5; ±2 µg) both ments were tested using Fisher PLSD. immediately before and immediately after exposure to the solution. As a control an additional group of parasit- 2.3. Longevity experiments: rhamnose–glucose oids was given distilled water. Following the feeding, mixtures parasitoids were individually placed in a glass vial (4×2 cm), provided with water and transferred to a climate In a separate experiment parasitoids were provided chamber (T=15°C; RH=95%; 16L:8D). Survival of the with a series of sugar mixtures. The mixtures were com- parasitoids was scored daily. A total of 20 parasitoids posed of 1M solutions of the monosaccharides rhamnose was tested per sugar. For each sugar at least 10 parasit- and glucose in relative concentrations of 1:4, 2:3, 3:2, oids were included which had consumed 100 µg or more. and 4:1. Pure 1M rhamnose and glucose solutions were Degree of correlation was determined by linear tested as controls. Otherwise the methodology was ident- regression analysis (Statview). ical to the experiment described above.

2.4. Correlations between quantity of sugar 3. Results consumption and survival 3.1. Longevity experiments: individual sugars This experiment was added to determine whether the short life span achieved with some of the sugars is due The various sugars tested, differed considerably with to the parasitoid’s inability to utilize the sugars, or regard to their effect on parasitoid longevity (ANOVA, whether this poor performance simply reflects the lack df=14; F=33.4; PϽ0.0001). Parasitoids lived longest of feeding stimulation by these sugars. In this experi- when provided with one of the principal nectar sugars ment the quantity of sugar consumption during a single (glucose, fructose, or sucrose) (Fig. 1). In comparison to feeding bout was established and subsequently its effect the control individuals, these sugars increased the para- on parasitoid survival was determined. Since the lon- sitoid’s life span by a factor 15–16. A range of other gevity experiment showed that food deprived parasitoids sugars (erlose, maltose, melibiose, melezitose, mannose on average live a mere 2–3 days, I used food- and water- and stachyose) had a less distinct effect, increasing para- deprived parasitoids at 24–32 h following their emerg- sitoid longevity by a factor of 11.2–6.9. The effect of 1080 F.L. Wa¨ckers / Journal of Insect Physiology 47 (2001) 1077–1084 trehalose and galactose was marginal, but still signifi- cant. Lactose and raffinose did not significantly raise parasitoid longevity, while rhamnose significantly reduced the parasitoid’s life span. These data on the effect of sugar diet on parasitoid life span, can be plotted against the previously reported acceptance threshold for the individual sugars (Wa¨ckers, 1999) (Fig. 2). Making the (conservative) assumption that sugars which were not accepted at a two molar sol- ution have 2M as an acceptance threshold, this yields a strong correlation between the two parameters (Z-test; P=0.0002). The parasitoid’s gustatory response is most sensitive to those sugars that yield the strongest increase in parasitoid life span, while C. glomerata shows only Fig. 3. Average longevity of C. glomerata females when provided with different mixtures of 1M solutions of rhamnose and glucose. The a weak or no response to those sugars that have a lesser, relative concentrations tested were 1:4, 2:3, 3:2, and 4:1. Pure 1M or no impact on parasitoid survival. However, it has to rhamnose and glucose solutions were included as controls. Different be pointed out that this correlation is not absolute, since letters indicate significant differences (Fisher PLSD). Error bars rep- parasitoids were able to utilize some of the sugars (e.g., resent standard deviations. melibiose and mannose), to which they fail to show a specific feeding response. Trehalose, on the other hand, 3.3. Correlations between quantity of sugar represents a combination of low suitability and a relative consumption and survival sensitive gustatory response by C. glomerata. Of the 14 sugars tested, nine (sucrose, fructose, glu- 3.2. Longevity experiments: rhamnose–glucose cose, erlose, maltose, melibiose, melezitose, stachyose, mixtures and trehalose) showed a positive correlation between food consumption and longevity (Fig. 4). Rhamnose, lac- tose, galactose and raffinose showed no such correlation, Survival on pure glucose was similar to the results while the correlation for mannose was close to signifi- obtained with this sugar in the previous experiment. cance (P=0.06). Rhamnose, in mixtures with glucose, strongly reduced parasitoid longevity in comparison to the glucose-fed individuals (Fig. 3). Even at the lowest rhamnose con- 4. Discussion centration (20% rhamnose–80% glucose) longevity was almost halved. At 40%, rhamnose all but erased the 4.1. Longevity nutritional benefits of the suitable sugar. At the 60 and 80% rhamnose concentrations, the effect of the respect- The sugars tested show a marked variation with ive 40 and 20% glucose was completely suppressed. respect to their effect on parasitoid life span in the lon- gevity experiment (Fig. 1). While some sugars raised C. glomerata longevity by a factor 15, lactose and raffinose provided no significant benefit and rhamnose even reduced the parasitoid’s life span. The fact that rhamnose does not just act as an inert component was confirmed by the series of rhamnose–glucose mixtures, in which 20% rhamnose was sufficient to cut the parasitoid’s life span in half relative to the 100% glucose control. This finding emphasizes that nutritional effects of the individ- ual sugars in nectar or honeydew are not simply additive. Even relatively low concentrations of an unsuitable sugar can strongly diminish the suitability of the total sugar source. Similar findings have been reported for honeybees by Barker and Lehner (1974) who demonstrated that lac- tose, mannose, raffinose, melibiose, and galactose when Fig. 2. Average longevity data plotted against data on the gustatory acceptance threshold of C. glomerata for the 14 sugars tested. Accept- offered in equimolar mixtures with sucrose significantly ance threshold defined as the lowest molar concentration at which a increased mortality compared to fed sucrose only. sugar solution was accepted by food deprived parasitoids. The tolerance level for unsuitable sugars can be depen- F.L. Wa¨ckers / Journal of Insect Physiology 47 (2001) 1077–1084 1081

Fig. 4. Correlations between quantity of sugar consumption during a single sugar meal and subsequent survival by C. glomerata females. 1082 F.L. Wa¨ckers / Journal of Insect Physiology 47 (2001) 1077–1084 dent on the activity level of the insect. Bees fed lactose a far more pronounced effect on the parasitoid’s life and galactose in sucrose mixtures were able to excrete span. While some sugars increase the parasitoid’s life large amounts of the unsuitable sugars in the faeces dur- span by a factor 15, the maximum factor of increase in P. ing so-called cleansing flights, but failed to do so when brassicae is 3 (Romeis and Wa¨ckers, unpublished data). kept in confined conditions (Peng, 1981). This should Moreover, a range of sugars which are utilized by the caution us that negative effects found in experiments parasitoid, such as melezitose, maltose, melibiose pro- with caged individuals are not necessarily representative vide no nutritional benefittoP. brassicae (Romeis and for the free flying insect. Wa¨ckers, unpublished data). Previously it had been dem- The quantified feeding experiment (Fig. 4) confirmed onstrated that C. glomerata exhibits gustatory responses that the parasitoid is indeed unable to utilize lactose, to sugars which are not accepted by P. brassicae rhamnose and raffinose. Galactose and mannose, which (Wa¨ckers, 1999; Romeis and Wa¨ckers, 2000). This is had increased parasitoid life span in the survival studies, the first report to demonstrate that parasitoids and their did not reach significance levels in the correlation herbivorous hosts may also differ distinctly with respect experiment (0.36 and 0.06, respectively). C. glomerata’s to the range of sugars they can utilize. This specificity inability to utilize raffinose or lactose and its poor utiliz- has important implications for the use of natural or arti- ation of galactose corresponds with results reported for ficial food supplements in biological control programs, honeybees (Vogel, 1931; Maurizio, 1965; Barker and as it demonstrates that it is possible to choose food sup- Lehner, 1974; Peng, 1981). Considering the chemical plements that selectively promote the antagonist, without structure of these sugars, they all share the presence of concurrently enhancing herbivore fitness. a galactose unit. Melibiose and stachyose, however, rep- resent noticeable exceptions to this generalization, as 4.2. Correlation with taste data these galactosides were quite suitable as a parasitoid food source. This indicates that raffinose and lactose are When combining our data on sugar suitability with the unsuitable by themselves, and not as precursors of galac- previously reported gustatory response by C. glomerata tose. The relatively poor performance on trehalose, to these sugars we see a clear relationship between the which is the haemolymph sugar in insects, may explain two parameters (Fig. 2). Melibiose and mannose consti- why host feeding often only has a marginal impact on tute exceptions as they combine nutritional suitability parasitoid longevity (Jervis and Kidd, 1986). with a failure to elicit a feeding response. The opposite When comparing our results to those obtained from phenomenon, feeding stimulation by entirely unsuitable feeding experiments with other Hymenoptera it is notice- sugars, was not found among the sugars tested. Such able that C. glomerata is apparently able to utilize a erroneous stimulation has been reported in a number of number of sugars which have been reported to be unsuit- other insect species. Galactose stimulates feeding by able for other parasitoid species and/or honeybees. Mel- adults of the boll weevil Anthonomus grandis (Nettles ezitose, for instance, was reported to be unsuitable for and Burks, 1971), albeit it accumulates as galactitol in the parasitoid Microplectron uscipennis (Zoebelein, the insect’s haemolymph, rather than being metabolized 1955), while C. glomerata was quite capable of utilizing to energy. Dethier et al. (1956) report that the blowfly this sugar. Mannose raised the parasitoid’s life span by Phormia regina readily accepts and even a factor 6.9, even though it failed to prolong the life span though these sugars lack any nutritional value. Dethier of the parasitoid Bracon brevicornis (Ponnamma and (1968) reports that the blowfly even ingests fucose in Kurian, 1983), and causes 100% mortality in bees within preference to a highly nutritious sugar. 4 h following feeding (De la Fuente et al., 1986; Sols et al., 1960). The parasitoid’s utilization of melibiose 4.3. Sugar utilization was also remarkable, considering that this sugar has been classified as unsuitable for bees (Vogel, 1931; Barker Once ingested, the suitability of a given saccharide as and Lehner, 1974; Maurizio, 1965). The ability of C. an energy source, depends on its digestive , glomerata to utilize this sugar corresponds with findings absorption and metabolism. Oligo- and disaccharides reported for some Diptera (Hassett et al., 1950; van Han- typically need to be hydrolyzed into their constituent del, 1971). monosaccharides before they can be absorped through Species-specific patterns of sugar utilization can be the gutwall. For this purpose insects secrete digestive especially important when sugar sources are used in carbohydrases both in their salivary glands and in their agroecosystems to increase the effectiveness of predators midgut (Chippendale, 1978). The utilization pattern of or parasitoids (e.g., Hagen, 1986; Bugg et al., 1991; the disaccharides and by C. glomerata Canas and O’Neil, 1998). When we compare the parasit- indicates that at least two glucosidases are involved in oid C. glomerata and its herbivorous host Pieris bras- carbohydrate digestion. The fact that the parasitoid per- sicae with respect to their sugar utilization pattern, some formed well on a range of sugars with an α-glucosidic apparent differences emerge. For one, sugar feeding has bond (erlose, maltose, sucrose, melezitose and F.L. Wa¨ckers / Journal of Insect Physiology 47 (2001) 1077–1084 1083 stachyose) is evidence for the presence of α-glucosidase, compared to individuals fed sucrose, fructose, or glu- a common digestive enzyme (Chippendale, 1978). The cose. While this reduction was more pronounced (44– parasitoid’s relatively poor performance with trehalose, 47%) in the case of melezitose, parasitoids still survived also containing an α-glucosidic bond, represents an an average of 18.4 days on this sugar. C. glomerata fed obvious exception. However, this finding is in accord- trehalose or raffinose were more strongly affected. Tre- ance with the specific α-glucosidases reported in hone- halose reduced the parasitoid’s life span by 79%, while ybees, which show a high activity in hydrolyzing sucrose this figure was 88% in the case of raffinose. This low and maltose, without acting on trehalose (Huber and survival on honeydew specific sugars might be one fac- Mathison, 1976). The suitability of melibiose, a disac- tor explaining cases in which honeydew is less suitable charide containing an α-galactosidic bond, indicates the as a food source than nectar (Elliott et al., 1987; presence of α-galactosidase, an enzyme which has not Leius, 1961). been described in the honeybee (Peng, 1980; Gilliam et It has been generally accepted that al., 1988; Ferreira et al., 1998). The longevity data pro- synthesis helps the sapfeeder to reduce the high osmotic vide no evidence for the presence of β-galactosidase, pressure of the imbibed phloem sap to a level similar to since lactose did not increase parasitoid longevity. The the insect’s haemolymph (Kennedy and Fosbrooke, presence of β-glucosidase remains unresolved, due to the 1972; Wilkinson et al., 1997). The low nutritional suit- fact that disaccharides sugars with a β-glucosidic bond ability of insect synthesized sugars might be viewed as a (e.g., gentiobiose or ) were not included in the coincidental by-product of this osmoregulatory function. test. The relatively strong performance on stachyose [α- However, the low nutritional suitability of some honey- d-galactopyranosyl-(1→6)-α-d-galactopyranosyl-(1→6) dew might also reflect an actual evasive strategy -α-d-glucopyranoside-(2↔1)-β-d-fructofuranosyl] could allowing the sap feeder to reduce exploitation of honey- indicate the presence of β-fructofuranosidase. dew by parasitoids and non-mutualist predators (Wa¨ckers, 2000). 4.4. Consequences for nectar- and honeydew feeding

C. glomerata achieved the longest life span with those Acknowledgements sugars (sucrose, fructose and glucose) which are most commonly found in nectar and many honeydews. Com- bined with the fact that C. glomerata also shows the I would like to thank Professor R. Amado, A Michel most sensitive feeding response to these sugars and two anonymous reviewers for helpful suggestions. (Wa¨ckers, 1999), it can be concluded that the parasitoid S. Dorn provided the infrastructure. is well adjusted to dealing with the far majority of carbo- hydrate sources. Baker and Baker (1983) present evi- dence that insects visit nectar with a specific ratio of References sucrose to glucose and fructose, and they propose that insects actually select nectar on the basis of this ratio. Baker, H.G., Baker, I., 1983. Floral nectar sugar constituents in relation Even though we lack adequate preference studies in to pollinator type. In: Jones, C.E., Little, R.J. (Eds.), Handbook of parasitoids, our studies show that C. glomerata readily Experimental Pollination Biology. Van Nostrand Reinhold, New York, pp. 117–141. accepts all three sugars and survives equally well on Barker, R.J., Lehner, Y., 1974. Influence of diet on sugars found by them. This suggests that the nectar spectrum of this para- thin-layer chromatography in thoraces of honey bees (Apis sitoid is likely limited by nectar detectability (Wa¨ckers, mellifera). J. Exp. Zool. 188, 157–164. 1994; Wa¨ckers and Swaans, 1993) and accessibility Bugg, R.L., Ellis, R.T., Carlson, R.W., 1989. Ichneumonidae (Jervis, 1998; Wa¨ckers et al., 1996), rather than by its (Hymenoptera) using extrafloral nectar of faba (Vicia Faba L. Fabaceae) in Massachusetts. Biol. Agric. Hortic. 6, 107–114. sucrose to hexose ratio. Bugg, R.L., Wa¨ckers, F.L., Brunson, K.E., Dutcher, J.D., Phatak, S.C., Honeydew may include a range of additional oligo- 1991. Cool-season cover crops relay-intercropped with cantaloupe: saccharides. Many sap feeding insects synthesize com- influence on a generalist predator Geocoris punctipes (Hemiptera: plex sugars through the action of gut enzymes and sub- Lygaeidae). J. Econ. Entomol. 84, 408–416. sequently excrete these sugars in their honeydew Canas, L.A., O’Neil, R.J., 1998. Applications of sugar solutions to maize, and the impact of natural enemies on Fall Armyworm. Int. (Hendrix et al., 1992; MacVicker et al., 1990). Melezi- J. Pest Man. 44, 59–64. tose, erlose, raffinose, and trehalose are examples of Chippendale, G.M., 1978. The function of carbohydrates in insect life such insect synthesized sugars, which can dominate the processes. In: Rockstein, M. (Ed.), Biochemistry of Insects. Aca- honeydew sugar spectrum (Kloft et al., 1985). Out of the demic Press, New York, pp. 1–55. honeydew sugars included in this study, erlose was the De La Fuente, M., Penas, P.F., Sols, A., 1986. Mechanism of mannose toxicity. Biochem. Biophys. Res. Commun. 140, 51–55. most suitable as it clearly prolonged the parasitoid’s life Dethier, V.G., 1968. To each his taste. Bull. Entomol. Soc. Am. 14, span relative to control individuals. Nevertheless, lon- 10–14. gevity of erlose-fed parasitoids was 28–32% lower, as Dethier, V.G., Evans, D.R., Rhoades, M.V., 1956. Some factors con- 1084 F.L. Wa¨ckers / Journal of Insect Physiology 47 (2001) 1077–1084

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