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CHEMICALLY-MEDIATED ATTRACTION OF THREE PARASITOID
SPECIES TO MEALYBUG-INFESTED CASSAVA LEAVES
Catherine Bertschy, Ted C. J. Turlings,2 Anthony
C. Bellotti1
Institute of Plant Sciences
1Centro Internacional de Agricultura Tropical
2Current address: Institut de Zoologie
3To whom correspondences should be addressed
Abstract
We investigated whether cassava plants that are infested
by the cassava mealybug, Phenacoccus herreni (Pseudococcidae,
Sternorrhyncha), emit attractants for the encyrtid parasitoids
Aenasius vexans Kerrich, Apoanagyrus (Epidinocarsis) diversicornis
Howard, and Acerophagus coccois Smith. Bioassays with a Y-tube
olfactometer showed for all three species that female wasps were
most responsive and selective when they were 1.5 to 2.5 days old.
Females of these age groups were used to test their ability to
distinguish between the odor of plants with and without mealybugs.
The wasps were offered choices between infested cassava leaves
vs. healthy ones, infested leaves vs. clean air, and healthy leaves
vs. clean air. A. vexans and A. diversicornis were strongly attracted
to infested leaves and preferred these over healthy ones. In contrast,
A. coccois was significantly attracted to either healthy or infested
leaves, and did not distinguish between the two. The results suggest
that A. coccois, which has the broadest known host range of the
three, may be responsive only to general plant odors, while A.
vexans and A. diversicornis respond more specifically to odors
associated with mealybug infestation.
Key Words: Aenasius vexans, Apoanagyrus (Epidinocarsis)
diversicornis, Acerophagus coccois, cassava (Manihot esculenta),
host location, semiochemicals
Resumen
Se investigó si las plantas de yuca que son
infestadas por el piojo harinoso, Phenacoccus herreni (STERNORRHYNCHA:
Pseudococcidae), emiten sustancias atractivas para los parasitoides
Encyrtidae Aenasius vexans, Apoanagyrus (Epidinocarsis) diversicornis
y Acerophagus coccois. Ensayos con un tubo olfactómetro
en Y mostraron que las tres especies tienden a responder y seleccionar
más frecuentemente cuando tienen de 1.5 a 2.5 días
de edad. Las hembras de esta edad fueron usadas para determinar
su capacidad de distinguir entre el olor de plantas con y sin
piojos. Se ofreci˜ a las hembras olores de yuca infestadas
o limpias, hojas infestadas o aire puro y hojas limpias o aire
puro. A. vexans y A. diversicornis fueron atraídas fuertemente
por las hojas infestadas y presentaron preferencia por estas hojas
contra las hojas limpias. En contraste, A. coccois fue atraída
de manera significante por hojas limpias u hojas infestadas contra
aire, y no pudo dintinguir entre ambos olores. Los resultados
sugieren que A. coccois, que tiene el más alto rango de
huéspedes de los tres, puede responder sólo a los
olores generales de las plantas, mientras A. vexans y A. diversicornis
responden más especificamente a los olores asociados con
la presencia de los piojos harinosos.
Cassava mealybugs are among the most damaging pests
of cassava in South America and Africa (Vargas & Bellotti,
1984). The two most important species are Phenacoccus herreni
Cox & Williams and P. manihoti Matile-Ferrero (Sternorrhyncha:
Pseudococcidae), which both originate from South America (Cox
& Williams, 1981; Bellotti et al., 1984). P. herreni appeared
as a problem rather suddenly in Northeast Brazil in the mid 1970s
and was then reported from Colombia, Venezuela and Guyana (CIAT,
1984; 1987; 1988; 1990); it can cause root yield losses up to
80% (Bellotti et al., 1984; Bellotti, 1983). In Africa, the closely
related P. manihoti became a serious pest in most of the cassava
growing regions after its accidental introduction in the 1970s
(Matile-Ferrero, 1977; Herren & Neuenschwander, 1991). For
both pest species biological control programs have been developed.
The encyrtid parasitoid Apoanagyrus (Epidinocarsis) lopezi (De
Santis) was successfully released in African in the 1980s. It
established and now maintains the mealybug population at an acceptable
low-density in most regions (Herren & Neuenschwander, 1991;
CIAT, 1992). For the 5% of the African cassava fields where the
parasitoid has not been effective in controlling the mealybug
(Neuenschwander et al., 1991), alternative control agents were
investigated such as two strains of the coccinellid predator Hyperaspis
notata Mulsant (Stäubli Dreyer et al., 1997a; 1997b; 1997c).
Natural enemies of P. herreni have been systematically
collected for the control of the mealybug in South America, and
laboratory colonies of three encyrtid parasitoids were established
at CIAT (Centro International de Agricultura Tropical), in Cali,
Colombia. These parasitoids are Aenasius vexans Kerrich, Apoanagyrus
(Epidinocarsis) diversicornis Howard (asexual strain) and Acerophagus
coccois Smith (CIAT, 1982; 1983; 1990). Knowledge on the biology
of these insects is limited. Published information is mostly restricted
to CIAT reports (1982-1992).
At the beginning of this century, studies showed
that parasitic wasps use olfaction to locate hosts and that they
may first be attracted to the food that their hosts feed on (Picard
& Rabaud, 1914; Thorpe & Jones, 1937; Thorpe & Caudle,
1938). More recently, it was demonstrated that herbivore-damaged
plants can play a key role in attracting enemies of insect herbivores
(Dicke et al., 1990; Turlings et al., 1990; 1995; Vet & Dicke,
1992). For example, lima bean plants under spider mite attack
release specific volatiles that are attractive to predatory mites
(Dicke et al., 1990) and similar volatile compounds released by
caterpillar-infested maize plants are used by parasitoids to locate
caterpillars (Turlings et al., 1990).
Volatiles emitted by mealybug-infested plants are
also suspected to attract natural enemies of the mealybug (Nadel
& van Alphen, 1987). Changes in chemicals produced by the
cassava plant due to P. manihoti infestation have been reported
by Calatayud et al. (1994). Such changes could result in the emission
of volatiles and explain why A. lopezi and A. diversicornis (sexual
strain) are attracted by P. manihoti-infested cassava plants (Nadel
& van Alphen, 1987; van Alphen et al., 1990). The feeding
behavior of P. herreni is very similar to that of P. manihoti
(Castillo & Bellotti, 1990), and it can be expected that they
evoke similar reactions in the cassava plant. However, studies
with the asexual strain of A. diversicornis of South America by
Hofstee et al. (1993) showed no response by this parasitoid to
the odor of P. herreni-infested cassava plants (var. Odungbo).
A better understanding of the interactions between cassava plants,
mealybugs, and parasitoids requires more behavioral as well as
chemical studies.
In this paper, we report on olfactometer studies
with the three encyrtid parasitoids reared at CIAT, A. vexans,
A. diversicornis (asexual strain), and A. coccois. The studies
were conducted to determine whether these parasitoids are attracted
to odors that may emanate from cassava plants infested by P. herreni.
Materials and Methods
Plants
CMC40 cassava stakes (20 cm long) were planted every
week in pots and kept in a screened compartment, where they were
subjected to natural weather conditions at Palmira, Colombia,
though protected from rain. The plants were used in experiments
when they carried 10-30 leaves (approximately 6 weeks after planting).
Insects
The cassava mealybug, P. herreni was reared at CIAT
on potted cassava plants (var. CMC40). Every week 30-40 cm high
plants were infested with 15 mealybug ovisacs, as described by
van Driesche et al. (1987). The plants were separated in different
cages based on the age of the mealybugs they carried.
The parasitoids, A. vexans, A. diversicornis and
A. coccois were continuously reared at CIAT on mealybug-infested
cassava plants (var. Mcol 1505). The colonies of A. vexans and
A. coccois were initiated with insects collected in Venezuela
in 1990 and the colony of A. diversicornis with insects from Colombia
(1984). The colonies were maintained in a greenhouse at 35°C
and under natural light conditions.
The Olfactometer
A Y-tube olfactometer similar to the one first described
by Sabelis & van de Baan (1983) was used in our experiments
(Fig. 1). Two arms of a glass Y-shaped tube were connected to
glass chambers (6.5 cm diam.) in which odor sources could be placed.
Activated charcoal filtered air at a rate of 400 ml/min was pushed
into each glass chamber. To avoid visual distractions and to diffuse
the light, a wooden frame covered with white cloth was placed
around the Y-tube. A lamp (100 watt) was placed outside this visual
barrier opposite from the entrance where the insects were introduced.
As these parasitoids are attracted by light, the lamp helped to
induce the insects to walk upwind in the direction of the odor
sources. When a female reached the center of the Y-tube, where
the three arms met, she could choose one of the offered odors.
Odor Sources
Every week ovisac-infested cassava plants were transferred
into a greenhouse, where they were kept in nylon cages for three
weeks before being used for the Y-tube experiments. Control (healthy)
plants were transferred weekly from the screened compartment and
enclosed in a nylon screen cage in the same greenhouse as the
infested plants. Care was taken that no mealybugs came in contact
with healthy plants. To serve as an odor source, two leaves of
either infested or healthy plants were cut off and the cut ends
were wrapped in wet cotton wool. The leaves were carefully placed
in one of the odor chambers. The infested leaves that were selected
carried honeydew and sooty mold, as well as mealybugs and exuviae.
Experimental Procedure
On the day of each experiment, parasitoid females
were removed from their cage and kept in a glass jar (400 ml)
with some honey. The jar was placed in the air-conditioned chamber
(28-30°C) where the experiments would take place. The insects
were left one or two hours in their new environment to become
adjusted. Before each olfactometer test, female parasitoids were
allowed to parasitize a mealybug on a cassava leaf. An infested
cassava leaf was placed upside down in a petri dish and several
females were introduced and observed until they had parasitized,
or at least stung a mealybug. The parasitoids were given this
experience as it may increase their responsiveness to host-related
odors (Turlings et al., 1993; Vet et al., 1995, Steinberg et al.,
1992). The parasitoids were then captured in a gelatin capsule
and kept there for 10 to more than 60 minutes. Before each Y-tube
test, the gelatin capsule was opened and inserted at the base
of the Y-tube. Females were introduced and were observed individually
in the olfactometer and used only once. The odor sources were
reversed each time three wasps had been tested.
Evaluation of Choices
A stopwatch was started when the insect left the
gelatin capsule. The female was allowed 5 minutes to walk up the
no-choice-area (Fig. 1) to reach the center of the olfactometer,
which is the area where the three arms meet. If a female did not
reach this center within 5 minutes, she was counted as a “no-choice”.
For the other females, the observation was stopped 5 minutes after
they had made it to the center, or after they had reached the
end of one of the arms. Each arm, was divided into four zones
(Fig. 1), which measured 8, 6, 6, and 3 cm, respectively.
A female had to enter at least zone 2 (Fig. 1) to
be considered to have made a choice. A few females switched arms
after reaching zone 2. In those cases, females were considered
to choose the arm which they entered the furthest. For statistical
analyses, a chi-square test was applied, using the total number
of females that made a choice for a particular odor (a = 0.05).
Procedures and Results
The Effect of Wasp Age
It has been shown that the responsiveness to odors
may change when parasitoids get older (e.g. Thorpe & Caudle,
1938; Steinberg et al., 1992). To determine the optimal age of
our parasitoids for olfactometer bioassays, parasitoid females
of different ages were tested. Newly emerged wasps were isolated
daily at about noon and transferred to Plexiglas(r) cages in which
they were provided honey and water. The insects remained in the
cage until they had reached a certain age. Six different age classes
were tested, varying from 0.5 to 6.5 days after emergence. Each
wasp was given an oviposition experience, and then introduced
into the olfactometer, in which they had a choice between the
odors of infested and healthy cassava leaves.
Responsiveness, i.e. proportion of females that made
a choice, did not decrease with increasing age of females. Overall
it was high for A. diversicornis with an average of 73% and medium
to low for both A. vexans and A. coccois with an average of respectively
49 and 48% of the responding females.
Preference for an odor source changed in two of the
three species (Fig. 1-3). In A. vexans and A. diversicornis, the
preference for the odor of infested leaves over odor of healthy
leaves was age dependent and significant for young females only.
Of the younger (1.5-2.5d old) A. vexans females, 80% preferred
infested cassava leaf odors (c2 = 7.2, P < 0.01). The youngest
A. diversicornis (0.5-1.5d) showed the clearest preference (82.6%)
for the odor of infested leaves over the odor of healthy leaves
(c2 = 9.78, P < 0.005), but 17.4% of the females that made
a choice switched between arms before making a final decision.
The 1.5 to 2.5-day-old A. diversicornis switched arms much less
(3.8%), but exhibited a weaker preference for odors of infested
leaves (69.2%, c2 = 3.85, P < 0.05). The older wasps showed
no significant preference. All age classes of A. coccois did not
differentiate between infested and healthy plant odors. Like A.
diversicornis, A. coccois walked a lot in the olfactometer, often
switching between arms (26.3% of the choosing females).
The Role of Plant Odors
In a subsequent series of experiments we more specifically
determined the relative attractiveness of healthy and infested
cassava leaves. Based on the results of the previous experiments,
only females that were 1.5 to 2.5 days old were used. On a given
day three different pairs of odor sources were tested, namely
“Infested vs. Healthy”, “Infested vs. Blank”,
and “Healthy vs. Blank”. In the case of “Blank”,
one arm introduced clean air that had passed through an odor chamber
with just a piece of wet cotton wool. For each pair of odor sources,
4 to 6 insects per day were individually tested in the Y-tube.
Occasionally, another series of 6 insects per odor source was
tested the same day.
A. vexans females were significantly attracted to
infested cassava leaves compared to healthy ones or a blank (Fig.
5a). Healthy leaf odors were less attractive, since only 64.5%
of the females responded in the “Healthy vs. Blank”
test without showing a significant preference for one of the two
odor sources (c2 = 2.5, P > 0.05).
A. diversicornis females were significantly attracted
to infested and healthy cassava leaves when offered against a
blank. They also showed a significant preference for infested
cassava plant odors over healthy ones (c2 = 6.08, P < 0.025).
Only 51.7 to 58.3% of A. coccois females made a choice,
but these were significantly attracted by healthy and infested
plant odors when offered against a blank (c2 = 7.53, P < 0.01
and c2 = 11.65, P < 0.001). In the “Infested vs. Healthy”
test, the choosing females very often switched sides before going
up one arm, and they showed no significant preference for either
odor source (c2 = 0.26, P > 0.05) (Fig. 5c).
Discussion
The preference of female wasps to plant odors in
the olfactometer was age dependent for A. vexans and A. diversicornis.
The younger age classes of both these species significantly preferred
the odor of infested leaves, while older females showed no particular
preference. The preferences exhibited by young A. vexans and A.
diversicornis may have been due to the experience that the wasps
received with an infested leaf just before their introduction
into the olfactometer. During such an experience the females may
learn to respond to the odors that they encounter through a process
of association (Turlings et al., 1993; Vet et al., 1995), which
may be age dependent. Some parasitoids only learn as young adults
(Kester & Barbosa, 1991), which could explain why older wasps
did not make a distinction in our tests. It is possible that if
these older wasps had been given an experience at a younger age,
they would have shown a preference as well. In the subsequent
experiments only younger females were used.
For A. coccois, the lack of preference of females
of any age class may be due to the particular choice offered.
This species obviously did not distinguish between infested and
healthy cassava leaves. An alternative choice, such as between
plants and a blank might have revealed a similar age dependency
of the response as found for the two other species.
All three species distinguished between plant material
and clean air (blank). A. vexans showed only a marginal attraction
to healthy leaves, but was strongly attracted to infested leaves.
A. diversicornis was attracted to healthy leaves, but preferred
the odor of infested leaves. A. coccois was also attracted to
both healthy and infested leaves, but did not distinguish between
these two odor sources. These differences in response of the three
encyrtid parasitoids suggest that they may employ different foraging
strategies. A. vexans and A. diversicornis recognized odors that
are specifically associated with mealybug infestation. A. coccois,
on the other hand, appeared to respond only to general cassava
plant odors. It remains unknown if A. vexans and A. diversicornis
are attracted to odors emanating directly from the mealybugs or
if the infested plants emit the attractive odors.
In the petri dish, where females were experienced
by giving them the opportunity to walk over a cassava leaf and
sting a mealybug, A. vexans walked slower, but showed a more direct
orientation towards mealybugs. This slower, but directed searching
behavior was also observed in the olfactometer. A. vexans was
clearly attracted to the infested cassava plants, but not to the
odors of healthy plants. After it found a mealybug, this solitary
parasitoid needed only a few seconds to parasitize it. A. coccois
is gregarious and took up to an hour to parasitize a host. It
spent a lot of time walking rapidly around the petri dish and
had fewer encounters with mealybugs. Also in the olfactometer,
this species walked much faster and in more different directions
than the other species, particularly when the females were given
the choice between infested and healthy plant odors. This fast
moving species did not readily distinguish between the odors of
infested and healthy leaves.
The reported host preference of these parasitoids
may explain their behavior in the olfactometer to some extent.
A. vexans prefers P. herreni over a related species, Phenacoccus
gossypii (= madeirensis) (CIAT, 1990). It has been most frequently
recovered from P. herreni on cassava, but its host range does
include other Phenacoccus species on different plants (Noyes &
Ren, 1995). Pijls & van Alphen (1996) studied the specificity
of a sexual strain of A. diversicornis on cassava. It appears
to be specific to P. herreni and P. manihoti. An asexual strain
from Venezuela has been shown to prefer P. herreni over P. gossypii
(= madeirensis) (Van Driesche et al., 1987). A. coccois seems
to be the most polyphagous of the three. It parasitizes Pseudococcidae
species of different genus such as Oracella acuta (Homoptera:
Pseudococcidae) on loblolly pine (Pinus taeda L.) (Clarke et al.,
1990). On cassava plants, it parasitizes P. herreni and P. madeirensis
more or less equally (CIAT, 1990). As a generalist, A. coccois
may be more responsive to general plant odors, while the more
specialized wasps, A. vexans and A. diversicornis, may have adapted
to exploit odors that are specifically associated with the presence
of mealybugs on cassava.
It remains to be determined if cassava volatiles
play an important role in the specific attraction to infested
plants, or if the mealybug and its by-products emit odors that
are attractive. It is known that some herbivores induce reactions
in plants that make them highly attractive to some parasitic wasps
(Turlings et al., 1995). Nadel & van Alphen (1987) found evidence
that mealybug-infested cassava plants also release odors that
are attractive to the parasitoid A. lopezi. The odors probably
come from the plant itself, as the parasitoid was not attracted
by the mealybug and its by-products. Van Alphen et al. (1990)
also found an attraction to P. manihoti-infested cassava plants
by A. diversicornis. Unlike our results, the females were not
attracted by healthy cassava plants but showed a clear attraction
to uninfested leaves taken from a partially infested plant, which
suggests that the infested plant emits attractants. Little is
known about the exact source and identity of parasitoid attractants.
Our ongoing experiments aim to determine the exact role of the
cassava plant in the foraging success of the parasitoids in order
to consider and exploit this role in further control measures
against the cassava mealybug.
Acknowledgments
We thank Carlos „añez for maintaining
and rearing mealybugs and parasitoids; Jair López for his
collaboration in the preparation of the experiments. We also thank
Letizia Mattiacci and Lincoln Smith and three anonymous reviewers
for their critical comments on the manuscript. The project was
supported by a grant from the Swiss Center for International Agriculture,
ETH Zurich.
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Fig. 1. Diagram of the olfactometer set-up. Drawing
by Urs Lengwiler.
Fig. 2. Age dependency of response. Choices by A.
vexans females of different age classes between the odors of mealybug-infested
and healthy cassava leaves in a Y-tube olfactometer. In each bar
the actual number wasps that made a particular choice is given,
while the x-axis indicates the percentages of choosing wasps that
the numbers represent. To the right of the bars is the proportion
of females that made a choice for one of the two odors, as well
as the total number of females that were tested per age class.
Fig. 3. Age dependency of response. Choices by A.
diversicornis females of different age classes between the odors
of mealybug-infested and healthy cassava leaves in a Y-tube olfactometer.
In each bar the actual number wasps that made a particular choice
is given, while the x-axis indicates the percentages of choosing
wasps that the numbers represent. To the right of the bars is
the proportion of females that made a choice for one of the two
odors, as well as the total number of females that were tested
per age class.
Fig. 4. Age dependency of response. Choices by A.
coccois females of different age classes between the odors of
mealybug-infested and healthy cassava leaves in a Y-tube olfactometer.
In each bar the actual number wasps that made a particular choice
is given, while the x-axis indicates the percentages of choosing
wasps that the numbers represent. To the right of the bars is
the proportion of females that made a choice for one of the two
odors, as well as the total number of females that were tested
per age class.
Fig. 5. Responses of the three parasitoid species.
(A) A. vexans, (B) A. diversicornis and (C) A. coccois, in a Y-tube
olfactometer. The wasps were offered choices between the odors
of: clean air vs. healthy leaves, clean air vs. infested leaves,
and healthy leaves vs. infested leaves. In each bar the actual
number wasps that made a particular choice is given, while the
x-axis indicates the percentages of choosing wasps that the numbers
represent. Next to the bars the proportion is given of the females
that made a choice for one of the two odors, as well as the total
number of females that were tested per choice.
and Silvia Dorn3
Applied Entomology
ETH (Swiss Federal Institute of Technology)
CH-8092 Zurich, Switzerland
CIAT, Cali, Colombia
Université de Neuchâtel
CH-2007 Neuchâtel, Switzerland