© 2004 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 110: 165 – 172, 2004 165
Blackwell Publishing, Ltd.
Influence of handling and conditioning protocol on
learning and memory of Microplitis croceipes
M. Tertuliano
1
, D.M. Olson
2
, G.C. Rains
1
& W.J. Lewis
2,
*
1
Department of Biological and Agricultural Engineering, University of Georgia, Tifton, GA 31793, USA;
2
USDA-ARS, PO
Box 748, Tifton, GA 31793, USA
Accepted: 4 November 2003
Key words: Microplitis croceipes, Hymenoptera, Braconidae, 3-octanone, training, reinforcement,
hunger state, memory
Abstract Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) learns odors in association with both
hosts and food. The food-associated ‘seeking’ behavior of M. croceipes was investigated under various
training protocols utilizing the conditioning odor, 3-octanone. We investigated the effects of odor
training, or its lack, training duration, training frequency, time elapsed after training, wasp hunger
state, and training reinforcement, on the food-seeking responses of M. croceipes females. We found
that odor-trained females show strong food seeking responses, whereas non-odor-trained females do
not respond to the odor, and that a single 10 s association with the odor whilst feeding on sugar water
subsequently conditioned the wasps to exhibiting significant responses to it. Increases in training
time to more than 10 s did not improve their responses. Repetition of the food–odor associations
increased a wasp’s recall, as well as its response over time, compared to a single exposure. Repeated
exposure to the learned odor in the absence of a food reward decreased the responses of less hungry
individuals. However, the level of response increased significantly following a single reinforcement
with the food–odor association. Understanding the factors that influence learning in parasitoids can
enhance our ability to predict their foraging behavior, and opens up avenues for the development of
effective biological detectors.
Introduction
Parasitic wasps detect and learn numerous chemical cues
associated with their host and food resources, and use them
in order to forage more effectively (Lewis & Martin, 1990;
Lewis et al., 1991; Zanen & Cardé, 1991). Recent studies of
the potential of wasps as biological detectors has also
indicated that Microplitis croceipes (Cresson) (Hymenoptera:
Braconidae), a specialist parasitoid of three highly poly-
phagous hosts species, can also detect and learn ‘foreign’
chemicals that are unlikely to have played a role as foraging
cues during their evolution (Wäckers et al., 2002; Olson
et al., 2003). This learning ability elicits specific behavioral
responses to cues associated with both long- (e.g., flight) and
short-range (e.g., area restricted search) foraging behaviors
(Olson et al., 2003). This species can also be trained to
simultaneously associate two different odors with food
and host rewards (Lewis & Takasu, 1990), or successively to
two different odors with the same reward (Takasu & Lewis,
1996), suggesting that they are able to store this informa-
tion for future use according to their specific resource
needs. Although the ability of these species to detect and
learn a wide variety of chemicals has been determined, we
still have very little information on the factors that affect
their acquisition and memory of learned experiences.
The optimal training protocol and age of females used
for flight responses of this species after food associated
conditioning were determined by Takasu & Lewis (1996);
responses peak 2–5 days after emergence and after five, 30 s
exposures to food and odor experience, which they remem-
ber for at least 2 days. Takasu & Lewis (1996) also showed
that female M. croceipes will cease to respond to learned
odors after several experiences with the odor without a
food reward, and that they will switch to a different odor
they had recently experienced as rewarding. However, the
effect of a state of hunger on responses over time, and the
factors which affect learning and memory of this species to
cues associated with the more short-range behavioral res-
ponses are not known. We chose a food-associated seeking
behavior of M. croceipes females, which is a modification of
‘area restricted search’ and other food-specific behaviors
Correspondence: W. Joe Lewis, USDA/ARS, PO Box 748, Tifton, GA
31793, USA. E-mail: wjl@tifton.uga.edu