The Journal of Experimental Biology
1692
© 2014. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2014) 217, 1692-1700 doi:10.1242/jeb.091843
ABSTRACT
We examined gustatory responses of the larval parasitoid Microplitis
croceipes to determine whether the adults discriminate among
common sugars, including fructose, glucose, maltose and sucrose,
found in plants. When given single sugar solutions of sucrose,
glucose, fructose and maltose at concentrations of 0.008–2.0 mol l
−1
,
the estimated concentrations at which 50% of wasps initiated feeding
ranged between 0.054 and 0.085 mol l
−1
for sucrose, glucose and
fructose, which was significantly lower than for maltose. Wasps
showed a strong decrease in feeding time for maltose or fructose
following a brief exposure to other sugars, suggesting that wasps can
distinguish maltose and fructose from the other sugars tested. The
higher acceptance threshold and short feeding time in the case of
maltose appears adaptive in light of the relatively poor nutritional
quality of the sugar in the longevity trial. The pronounced feeding
inhibition seen for fructose following exposure to other sugars is not
linked with lower nutritional performance. This feeding inhibition was
even seen in wasps that had fed on glucose at the lowest acceptance
threshold (0.031 mol l
−1
) and persisted for 24 h. This study is the first
to show feeding inhibition of otherwise phagostimulant sugars such
as maltose and fructose after gustatory stimulation on other sugars.
KEY WORDS: Feeding inhibition, Gustatory responses, Sugar
feeding
INTRODUCTION
There is a large variation in sugar composition among natural sugar
sources, such as nectar and honeydew (Percival, 1961; Kunkel and
Kloft, 1977; Baker and Baker, 1983; Nemec and Starý, 1990;
Wäckers, 2005). Floral nectars have been categorized according to
their nectar composition as sucrose-rich or hexose (glucose/fructose)-
rich (Baker and Baker, 1983), and insect groups often show a
tendency to visit nectars of a certain carbohydrate composition (Baker
and Baker, 1982). However, in many groups of nectar feeders, it
remains unclear whether the observed insect–flower associations are
directly driven by nectar sugar preferences, or whether this is based
on other factors, such as flower architecture (Jervis, 1998; Olson et
al., 2005; Wäckers and van Rijn, 2012).
Parasitoid feeding responses to different nectar and honeydew
sugars can vary widely; while several sugars fail to elicit any feeding
RESEARCH ARTICLE
1
Graduate School of Bioresources and Bioenvironmental Sciences, Kyushu
University, Fukuoka 812-8581, Japan.
2
Crop Protection and Management Unit,
USDA-ARS, Tifton, GA 31793-0748, USA.
3
Centre for Sustainable Agriculture,
Lancaster Environment Centre, Lancaster University, Bailrigg, Lancaster LA1 4YQ,
UK.
4
Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan.
*Present address: Nong Lam University, Ho Chi Minh City, Vietnam.
‡
Author for correspondence (takasu@brs.kyushu-u.ac.jp)
Received 5 June 2013; Accepted 22 January 2014
response in food-deprived parasitoids, other sugars stimulate feeding
at concentrations as low or lower than 0.016 mol l
−1
(Wäckers, 1999;
Beach et al., 2003). At equal concentrations, adult parasitoids
consume larger quantities of high-quality sugars such as glucose,
fructose and sucrose as compared with low-quality sugars (Wäckers,
2001; Beach et al., 2003; Williams and Roane, 2007). Because the
parasitoid feeding response is often correlated with the nutritional
suitability of the carbohydrates tested (Wäckers, 2001), the variation
of parasitoid feeding responses to different sugars could be
explained by optimal foraging theory, which predicts that foragers
should choose diet items to maximize their net energy intake or net
fitness benefits (Charnov, 1976; Stephens and Krebs, 1986; Sih and
Christensen, 2001). Parasitoids are known to adapt their preference
for hosts of different quality in accordance with their host encounter
rates and their own physiological states (van Alphen and Vet, 1986).
As natural sugar sources are vital for their survival and reproduction,
parasitoids can be expected to have a preference for high quality of
sugars and adapt their preference in accordance with feeding
experiences. While parasitoid gustatory responses to individual
sugars have been tested, the impact of prior experience and the
relative preference for individual sugars remains unknown.
The preference of nectar feeders for various nectar components
has been investigated in several vertebrates and invertebrates. The
methods used to assess such preferences vary among studies. The
most direct way to investigate the ability and propensity of an
animal to discriminate and select foods is to present it with two or
more types of food simultaneously, observe its behavior and/or
measure the quantity of food eaten (Dethier, 1976). These methods
require that the test organism shows repeated feeding bouts, and an
inclination to sample the food source. In the case of social
Hymenoptera, both of these conditions are met, as the foragers
continuously collect food to cover the needs of the entire colony.
This has facilitated the study of food preferences in ants and
honeybees. The tests used to determine feeding preferences in
honeybees typically assess the relative consumption in choice
experiments (Wykes, 1952; Waller, 1972; Inouye and Waller, 1984;
Alm et al., 1990). An alternative method makes use of the fact that
bees exhibit a typical ‘bee dance’ to recruit additional foragers (von
Frisch, 1934). As bees communicate food source quality through the
turning frequency, this parameter can also be used as an indicator of
how bees valuate a previously visited food source (Waller and
Bachman, 1981; Barron et al., 2009). In the case of ants, the relative
intensity with which scouts recruit nestmates to food alternatives is
also used as a method to establish preferences in choice
experiments. These studies typically count the number of ants
visiting the different food alternatives (Lanza and Krauss, 1984;
Lanza, 1988; Lanza et al., 1993; Völkl et al., 1999).
While these methods are effective in establishing preferences in
social Hymenoptera, they are unsuitable for the study of food
An acquired distaste: sugar discrimination by the larval parasitoid
Microplitis croceipes (Hymenoptera: Braconidae) is affected by
prior sugar exposure
J. K. Makatiani
1
, H. K. Le
1,
*, D. M. Olson
2
, F. L. Wäckers
3
and K. Takasu
4,‡