BEHAVIOR

Oviposition Behavior of Stenoma catenifer (Lepidoptera: Elachistidae):

Chemical and Physical Stimuli and Diel Pattern of Egg Laying
DORI EDSON NAVA, JOSÉ ROBERTO POSTALI PARRA, GABRIELA INÉS DIEZ-RODRÍGUEZ,
AND JOSÉ MAURÍCIO SIMÕES BENTO

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Departamento de Entomologia, Fitopatologia e Zoologia Agrṍcola, Escola Superior de Agricultura “Luiz de Queiroz”,
Universidade de São Paulo, Piracicaba, São Paulo, 13418-900, Brazil

Ann. Entomol. Soc. Am. 98(3): 409Ð414 (2005)

ABSTRACT The inßuence of chemical and physical stimuli on the diel patterns of oviposition
behavior of the borer Stenoma catenifer Walsingham (Lepidoptera: Elachistidae) were investigated.
All experiments were conducted in the laboratory (25 ⫾ 2⬚C, 60 ⫾ 20% RH, photoperiod of 14:10 [L:D]
h) by using Þve pairs per cage (n ⫽ 5). To evaluate response to chemical stimulation, the cages were
lined internally with a paper towel containing different treatments: 1 and 2) avocado fruit of
ÔMargaridaÕ and ÔBredaÕ, 3) artiÞcial fruit, and 4) no fruit (natural or artiÞcial). Quilted paper towel,
nonquilted paper towel, and a smooth sheet of paper were used to evaluate response to the substrate.
The numbers of eggs in all treatments that included avocado fruit were statistically higher than the
others. Likewise, the numbers of eggs on quilted paper towel were statistically higher than on
nonquilted paper towel or on smooth paper. The peak egg-laying time in the laboratory occurred from
2000 to 2400 hours.

KEY WORDS Persea americana, Lepidoptera oviposition.

THE OVIPOSITION BEHAVIOR OF lepidopterans is a complex
process that follows a sequence of events. First, mated
females search for, orient to, and Þnd the host plant.
These events are difÞcult to evaluate in the laboratory
because they involve chemical cues governed by ol-
faction and by factors related to vision, such as shape,
size, and color of the substrate (Rausher 1979, Mihs-
feldt 1998). In a second step, now on the host, assess-
ment of the surface and its suitability for egg laying
takes place. Chemical and physical characteristics of
leaves, fruits, stem, and other plant parts can inßuence
the selection of an egg-laying site (Schultz 1988,
Thompson and Pellmyr 1991). At this stage, processes
involved in oviposition often can be determined under
laboratory conditions and in the greenhouse. At the
Þnal step, the acceptance or rejection of the oviposi-
tion site involves the central nervous system, which
processes the impulses emitted by sensilla located on
different parts of the body: tarsi, antennae, proboscis,
and ovipositor. In addition, the response does not
depend solely on characteristics of the plant but also
on the presence of insects, pheromones, age of fe-
males, and learning (Renwick and Chew 1994).
In lepidopterans, and particularly in moths, egg lay-
ing is done on pubescent or rough-surfaced sites that
allow better adhesion of the eggs to the substrate,
which protects the eggs from predators and parasitoids
(Callahan 1957, Nitao and Berenbaum 1988). Never-
theless, some microlepidopterans, such as Ethmia spp.
(Ethmiidae) (Peterson 1968) and Plutella maculipen-
nis (Curtis) (Plutellidae) (Gupta and Thorsteinson
1960), can use a polyvinyl plastic surface.
Despite the advances in laboratory insect rearing
techniques, especially on artiÞcial diet, obtaining eggs
is still one of the most difÞcult obstacles to overcome.
Therefore, knowledge of oviposition behavior under
natural conditions is necessary if techniques or meth-
ods that mimic natural conditions are to be used in the
laboratory. However, many lepidopterans lay their
eggs on substrates whose surfaces do not resemble the
natural host either chemically or physically. For ex-
ample, oviposition has been obtained on newspaper
for Spodoptera frugiperda (J.E. Smith) and Thyrinteina
arnobia (Stoll); on parafÞn wax-coated Þlter paper for
Anticarsia gemmatalis Hübner and Diatraea sacchara-
lis (F.); on ofÞce paper for Hedylepta indicata (F.)
(Parra 1999); on transparent plastic for Ecdytolopha
aurantiana (Lima) (Garcia 1998); and on transparent
plastic placed over green paper for Bonagota cranaodes
(Meyrick) (Parra et al. 1995), among others. For other
species, it is necessary to add plant parts that possibly
provide some chemical stimulus. Moreti and Parra
(1983) reported that Heliothis virescens (F.) (Noctu-
idae) requires cotton leaves in the cage for oviposi-
tion; otherwise, the number of eggs is dramatically
reduced. Mihsfeldt (1998) tested several treatments
consisting of paper, tomato leaf extract, and green
plastic for obtaining Tuta absoluta (Meyrick) eggs and
found that treatments associating an olfactory stimu-

0013-8746/05/0409Ð0414$04.00/0 䉷 2005 Entomological Society of America

410 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Fig. 1. Papers used as substrate for S. catenifer oviposition. (A) A SNOB two-ply quilted paper towel. (B) A SNOB two-ply
nonquilted paper towel. (C) A 75 g/m2 RIPAX white smooth sulÞte paper.
lus (tomato leaf extract) with a visual one (green
polyethylene) resulted in greater numbers of eggs.
Stenoma catenifer Walsingham is a native pest of the
Neotropical region; in Brazil, it has been reported to
occur in the main avocado (Persea americana Mill.)-
producing regions in the states of São Paulo, Minas
Gerais, Espṍrito Santo, and Paraná (Medina 1978). In
recent years, the presence of this pest has become a
limiting factor for the production of avocado fruits.
The damage is variable, and yield losses of up to 100%
are possible (Hohmann and Meneguim 1993). Control
is attained mainly with chemical products, but the
lack of insecticide application technologies, in addi-
tion to a lack of information about the bioecology of
the pest and grove management systems (e.g., row
spacing and pruning), contributes to low efÞciencies.
In recent years, the potential for biological control
by using parasitoids of the genera Trichogramma and
Trichogrammatoidea (Hohmann and Meneguim 1993,
Hohmann et al. 2003) has been demonstrated. Thus,
the objective of this work was to determine in the
laboratory whether the oviposition behavior of S.
catenifer is inßuenced by chemical (fruit) and physical
(paper) stimuli, and based on these results, to deter-
mine the egg-laying time, to obtain information for the
production of large quantities of eggs on a substrate
that could be handled easily for biological control
studies on this pest.
Materials and Methods
Experiments were conducted at the Insect Biology
Laboratory of Departamento de Entomologia, Fito-
patologia e Zoologia Agrṍcola of Escola Superior de
Agricultura “Luiz de Queiroz” (ESALQ), Univer-
sidade de São Paulo (USP), in Piracicaba-SP, Brazil.
The rearing rooms were maintained at 25 ⫾ 2⬚C,
60 ⫾ 20% RH, and a photoperiod of 14:10 (L:D) h.
S. catenifer Rearing. The insects were obtained by
collecting infested avocado fruit from orchards lo-
cated in the municipality of São Tomás de Aquino,
Minas Gerais, Brazil, 20⬚ 52⬘ 30⬙ S, 47⬚ 07⬘30⬙ W,
and 1000-m elevation. In the laboratory, the larvae
were removed from the fruit and reared on seeds
placed in transparent acrylic containers (10 by 10 by
8 cm) until pupation. Individual pupae were placed
under a plastic cup and arranged on a tray containing
Þlter paper, which was moistened daily. After emer-
gence, S. catenifer pairs were allowed to mate. Male
and female pupae were separated based on the shape
Vol. 98, no. 3
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of the end of the abdomen. The genital opening in
females lacks setae, forming the ovipore, whereas in
males no opening is visible because of the hair tufts.
Determination of Chemical Stimulus for Oviposi-
tion. To determine a possible chemical effect of the
avocado fruit on S. catenifer oviposition, Þve pairs with
females on the second day of oviposition were placed
in a cage consisting of a polyvinyl chloride (PVC) tube
(23.0 cm in height and 15.0 cm in diameter), supported
on the bottom side by a plastic container (Tupper-
ware-type, without a lid) measuring 18.0 cm in diam-
eter by 12.0 cm in height, and on top by a screened
plastic lid (0.02 cm2). These cages were lined inter-
nally with two-ply quilted paper towel (SNOB), and
the adults were fed 10% honey solution supplied to
the container by capillary action through a cotton roll
(2.5 by 0.3 cm). There were four treatments: 1) a cage
containing one avocado (ÔBredaÕ) fruit; 2) a cage con-
taining one avocado (ÔMargaridaÕ) fruit; 3) a cage
containing an artiÞcial fruit made of green plastic
material; and 4) a cage without fruit. Treatments were
repeated Þve times, and the numbers of eggs present
on the fruit and on the paper were evaluated after 24 h.
Determination of Physical Stimulus for Oviposi-
tion. In this experiment, the effect of different papers
on oviposition was tested (Fig. 1). Cages were set up
in a manner similar to the chemical stimulus experi-
ment, but three types of paper were used: 1) cage lined
with SNOB two-ply quilted paper towel; 2) cage lined
with SNOB two-ply nonquilted paper towel; and
3) cage lined with 75 g/m2 white smooth ofÞce paper
(sulÞte) (RIPAX). The nonquilted paper towel was
obtained by ironing the quilted paper towel with suc-
cessive pressings by using an electric iron adjusted to
160⬚C. One Breda avocado fruit and a container with
10% honey solution were placed inside the cages to
provide nourishment for the adults. Four replications
were conducted, and the numbers of eggs present on
the fruit and on the paper were evaluated after 24 h.
Five S. catenifer pairs, including females on the second
oviposition day, were placed in each cage.
Oviposition Time. Based on preliminary observa-
tions, it was determined that S. catenifer oviposits at
night. Therefore, the experiment was conducted from
1600 to 0600 hours. The previously described PVC
cage (Fig. 2A), containing Þve S. catenifer pairs, was
attached to an iron structure (Fig. 2B) with clasps
(Fig. 2C); the interior of the cage was lined with
SNOB two-ply quilted paper towel (Fig. 2D), and the
setting was placed on a laboratory bench (Fig. 2E).
May 2005 NAVA ET AL.: OVIPOSITION BEHAVIOR OF S. catenifer 411

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Fig. 2. Cage and iron structure used for S. catenifer oviposition time determination in the laboratory. (A) PVC cage.
(B) Iron structure. (C) Clasps for fastening the cage to the iron structure. (D) Cage internal lining consisting of quilted paper
tower. (E) Cage-supporting bench. (F) Paper towel for oviposition. (G) Avocado fruit suspended by a string. (H)
Avocado-suspending string. (I) Extension arm for attaching the string that suspends the fruit. (J) Screened plastic lid (0.02
mm2).

Eight overlapping paper towel sheets were stacked
between the bench and the base of the cage, corre-
sponding to one sheet for each 2-h interval (Fig. 2F).
One fruit was placed inside the cage at the center,
on paper towel sheets, without touching the sides
(Fig. 2G). The fruit was attached to a string (Fig. 2H)
that was tied to an arm hanging from the iron structure
(Fig. 2I). At evaluation time, the fruit was suspended
a few centimeters on the structureÕs arm, without
removing the screened plastic lid (0.02 mm2) (Fig. 2J).
The PVC cage was then moved a few millimeters
vertically to remove a paper towel sheet, correspond-
ing to the egg-laying time interval, while preventing
the adults from escaping. Later, the fruit was replaced
with another fruit through the upper part of the struc-
ture, by partially lifting the screened plastic lid.
Treatments consisted of 2-h egg-laying time inter-
vals, i.e., 1800 Ð2000 hours, 2000 Ð2200 hours, 2200 Ð
2400 hours, 2400 Ð 0200 hours, 0200 Ð 0400 hours, 0400 Ð
0600 hours, with six replicates during 2 d. Eggs on the
paper towel and on the fruit were counted 24 h after
their removal from the cage because by then the eggs
had become dark and more conspicuous.
Data Analysis. The experiments were conducted in
a completely randomized design. To determine a pos-
sible chemical stimulus for oviposition, the data for
number of eggs laid on the paper and on the fruit were
submitted to analysis of variance (ANOVA), and the
means were compared by the Tukey test (P ⱕ 0.05).
For determination of a possible physical stimulus, the
data were analyzed in a 3 by 2 factorial scheme, con-
sisting of the three types of paper (quilted, nonquilted,
and white sulÞte paper) and two oviposition sites
(fruit and paper). Results were submitted to ANOVA,
and the means were compared by the Tukey test (P ⱕ
0.05). For determination of oviposition time, the data
were submitted to a second degree polynomial re-
gression analysis.
412 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA
Table 1. Mean number (ⴞ SD) of S. catenifer eggs laid on fruit
and on paper added as lining to the oviposition cage, on avocado
fruit Margarida and Breda, and on artificial fruit, as well as on the
cage without fruit
No. eggs
Treatment
Fruit Paper
Margarida fruit ⫹ paper towel 110.85 ⫾ 22.36aB 321.10 ⫾ 60.29aA
Breda fruit ⫹ paper towel 87.51 ⫾ 19.03aB 362.72 ⫾ 66.28aA
ArtiÞcial fruit ⫹ paper towel 10.26 ⫾ 03.06b
(control)
No fruit ⫹ paper towel 08.06 ⫾ 02.55b
Means followed by the same lowercase letter in the column or
uppercase letter in the row do not differ among themselves by Tukey
test (P ⱕ 0.05).
Results and Discussion
Determination of Chemical Stimulus. S. catenifer
females required avocado fruit for oviposition (Table
1). The number of eggs laid on the fruit, both on
Margarida (110.85) and on Breda (87.51), was statis-
tically similar, representing 55.88 and 44.12%, respec-
tively (P ⫽ 0.00001). This preference also was ob-
served with respect to the number of eggs laid on
paper near the fruit when one avocado of Margarida
(321.10) or Breda (362.71) was included in the cage.
The number was signiÞcantly smaller (P ⫽ 0.00051) in
cages that either contained artiÞcial fruit (10.26) or
lacked fruit (8.06). This chemical stimulus for ovipo-
sition conferred by the substrate also was observed for
H. virescens. Placing cotton leaves in the upper part of
the cage increased oviposition on voile and on the
paper that lined the cage internally (Moreti and Parra
1983). According to Jackson et al. (1986), H. virescens
oviposition on tobacco leaves was inßuenced by
chemical substances of the terpene group. In other
species, such as Tuta absoluta (Meyrick) (Gelechi-
idae), the association of an olfactory (tomato leaf
extract) with a visual stimulus (green polyethylene)
stimulated more eggs to be deposited than on a “nat-
ural” oviposition substrate (tomato plant leaves)
(Mihsfeldt 1998).
Regardless of the presence of an avocado fruit, the
number of eggs laid on paper, in all treatments, was
signiÞcantly higher than the number laid on fruit (P ⫽
0.00001) (Table 1). This demonstrates that, in spite of
the chemical cue, females selected a speciÞc oviposi-
tion substrate. In this experiment, the quilted paper
towel was suitable for oviposition and was similar to
egg-laying sites under Þeld conditions, where eggs are
laid in crevices, on necrotic areas of the avocado fruit,
and on the pedicel of the fruit. In a Þeld study by
Hohmann et al. (2003), ⬎50% of the eggs were laid on
the pedicel.
Physical Stimulus Determination. The type of pa-
per placed in the cage inßuenced choice of oviposition
site (Table 2). The number of eggs laid on fruit was
higher when either smooth ofÞce (sulÞte) paper
(248) or nonquilted paper towel (184.75) was used as
cage lining, signiÞcantly differing from cages lined
with quilted paper towel (74) (P ⫽ 0.0212). This
probably is attributable to paper texture because the
Vol. 98, no. 3
Table 2. Mean number (ⴞ SD) of S. catenifer eggs laid on fruit
and on paper when the cage was lined with different types of paper
No. eggs
Treatment
Fruit Paper
Quilted paper towel ⫹ fruit 74.00 ⫾ 13.49bB 315.63 ⫾ 34.66aA
Nonquilted paper towel ⫹ 184.75 ⫾ 25.00aA 137.63 ⫾ 70.95bA
fruit
SulÞte paper ⫹ fruit 248.00 ⫾ 47.21aA 8.88 ⫾ 04.25cB
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Means followed by the same lowercase letter in the column or
uppercase letter in the row do not differ among themselves by Tukey
test (P ⱕ 0.05).
number of eggs laid on paper when the cage was lined
with quilted paper towel (315.63) was statistically
higher than the number laid in cages lined with non-
quilted paper (137.63) or sulÞte paper (8.88) (P ⫽
0.01578). Thus, it was observed that when a chemical
stimulus from the fruit is present and the egg-laying
substrate (paper) is unsuitable, oviposition occurs
preferably on the fruit. Conversely, when available the
quilted paper was the preferable substrate (315.63),
differing signiÞcantly from the number of eggs laid on
fruit (74) (Table 2). For the two-ply nonquilted paper
towel (without dimples), the numbers of eggs laid on
the fruit (184.75) and on paper (137.63) were statis-
tically similar. However, when cages lined with sulÞte
paper were used, egg laying was higher on the fruit
(248) than on paper (8.88) (P ⫽ 0.00001).
According to Ramaswamy (1988), physical stimuli
related to the oviposition substrate constitute an im-
portant tactile cue for lepidopteran females. However,
for S. catenifer, it was demonstrated that the physical
stimulus is related to the chemical stimulus (Table 1),
because no oviposition occurred on the quilted paper
towel without the presence of fruit. Controversy exists
with regard to the roles of physical versus chemical
stimuli in the tortricid Choristoneura fumiferana (Cle-
mens) (Tortricidae), a pest of conifers in North Amer-
ica. Renwick and Radke (1982) suggested that phys-
ical stimuli were more important than chemical stimuli
in relation to oviposition behavior, whereas Städler
(1974) concluded that chemical stimuli were more
important.
It was observed that a chemical stimulus is required
for S. catenifer oviposition in the laboratory, which is
provided by the avocado fruit. Notwithstanding, to
obtain a large amount of eggs on an easy-to-handle
substrate, it is necessary to line the cage with quilted
paper towel, for appropriate physical stimulus, which
provides protection for the eggs. Future research
should determine which chemical extracts from the
fruit stimulate oviposition so that after their synthesis,
they could be used instead of fruit.
Oviposition Time. The polynomial regression anal-
ysis for factor time indicated a signiÞcant quadratic
effect (P ⫽ 0.0013, F ⫽ 12.95476, R2 ⫽ 0.7513; y ⫽
16.86 ⫺ 3.72x ⫹ 0.18x2), where coefÞcients were dif-
ferent from zero by StudentÕs t-test (P ⱕ 0.05) (Fig. 3).
The point of maximum oviposition is 2200 Ð2400 hours
during which ⬇60% of all eggs are deposited, despite
that oviposition occurred during the entire scoto-
May 2005 NAVA ET AL.: OVIPOSITION BEHAVIOR OF S. catenifer
Fig. 3. Mean percentage of S. catenifer eggs laid at different times in the laboratory, with beginning of scotophase at 2000
hours and corresponding Þtting equation (25 ⫾ 2⬚C, 60 ⫾ 20% RH, and a photoperiod of 14:10 [L:D] h).
phase. Approximately 80% of the eggs were laid be-
tween 2000 and 2400 hours. This egg-laying behavior
is variable among Lepidoptera. Garcia (1998) ob-
served that Ecdytolopha aurantiana (Tortricidae) ovi-
posits during the day, and 16.12% of eggs were re-
corded from 0700 to 1900 hours. However, the greatest
egg-laying percentage was concentrated from 1900
to 2300 hours, when 78.96% of eggs were laid. For
S. catenifer, no oviposition was observed during the
day, and thus it can be said that its egg-laying habit is
crepuscular/nocturnal, because egg laying started at
1800 hours and ended at dawn by 0800 hours. Al-
though this study was conducted under laboratory
conditions, where transitions from day to night (pho-
tophase/scotophase) occurred in an abrupt manner,
this behavior may be similar to what occurs under Þeld
conditions.
Acknowledgments
We thank José Carlos Gonçalves (Café Total Company)
for funding this research and Coordenação de Aperfeiçoa-
mento do Ensino Superior (CapesÐCoordination for the De-
velopment of Higher Education Personnel) for granting a
doctoral scholarship.
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Received 6 July 2004; accepted 3 January 2005.
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