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 nis (Curtis) (Plutellidae) (Gupta and Thorsteinson
process that follows a sequence of events. First, mated 1960), can use a polyvinyl plastic surface.
females search for, orient to, and Þnd the host plant. Despite the advances in laboratory insect rearing
These events are difÞcult to evaluate in the laboratory techniques, especially on artiÞcial diet, obtaining eggs
because they involve chemical cues governed by ol- is still one of the most difÞcult obstacles to overcome.
faction and by factors related to vision, such as shape, Therefore, knowledge of oviposition behavior under
size, and color of the substrate (Rausher 1979, Mihs- natural conditions is necessary if techniques or meth-
feldt 1998). In a second step, now on the host, assess- ods that mimic natural conditions are to be used in the
ment of the surface and its suitability for egg laying laboratory. However, many lepidopterans lay their
takes place. Chemical and physical characteristics of eggs on substrates whose surfaces do not resemble the
leaves, fruits, stem, and other plant parts can inßuence natural host either chemically or physically. For ex-
the selection of an egg-laying site (Schultz 1988, ample, oviposition has been obtained on newspaper
Thompson and Pellmyr 1991). At this stage, processes for Spodoptera frugiperda (J.E. Smith) and Thyrinteina
involved in oviposition often can be determined under
arnobia (Stoll); on parafÞn wax-coated Þlter paper for
laboratory conditions and in the greenhouse. At the
Anticarsia gemmatalis Hübner and Diatraea sacchara-
Þnal step, the acceptance or rejection of the oviposi-
lis (F.); on ofÞce paper for Hedylepta indicata (F.)
tion site involves the central nervous system, which
processes the impulses emitted by sensilla located on (Parra 1999); on transparent plastic for Ecdytolopha
different parts of the body: tarsi, antennae, proboscis, aurantiana (Lima) (Garcia 1998); and on transparent
and ovipositor. In addition, the response does not plastic placed over green paper for Bonagota cranaodes
depend solely on characteristics of the plant but also (Meyrick) (Parra et al. 1995), among others. For other
on the presence of insects, pheromones, age of fe- species, it is necessary to add plant parts that possibly
males, and learning (Renwick and Chew 1994). provide some chemical stimulus. Moreti and Parra
In lepidopterans, and particularly in moths, egg lay- (1983) reported that Heliothis virescens (F.) (Noctu-
ing is done on pubescent or rough-surfaced sites that idae) requires cotton leaves in the cage for oviposi-
allow better adhesion of the eggs to the substrate, tion; otherwise, the number of eggs is dramatically
which protects the eggs from predators and parasitoids reduced. Mihsfeldt (1998) tested several treatments
(Callahan 1957, Nitao and Berenbaum 1988). Never- consisting of paper, tomato leaf extract, and green
theless, some microlepidopterans, such as Ethmia spp. plastic for obtaining Tuta absoluta (Meyrick) eggs and
(Ethmiidae) (Peterson 1968) and Plutella maculipen- 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 Vol. 98, no. 3

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.

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lus (tomato leaf extract) with a visual one (green of the end of the abdomen. The genital opening in
polyethylene) resulted in greater numbers of eggs. females lacks setae, forming the ovipore, whereas in
Stenoma catenifer Walsingham is a native pest of the males no opening is visible because of the hair tufts.
Neotropical region; in Brazil, it has been reported to Determination of Chemical Stimulus for Oviposi-
occur in the main avocado (Persea americana Mill.)- tion. To determine a possible chemical effect of the
producing regions in the states of São Paulo, Minas avocado fruit on S. catenifer oviposition, Þve pairs with
Gerais, Espṍrito Santo, and Paraná (Medina 1978). In females on the second day of oviposition were placed
recent years, the presence of this pest has become a in a cage consisting of a polyvinyl chloride (PVC) tube
limiting factor for the production of avocado fruits. (23.0 cm in height and 15.0 cm in diameter), supported
The damage is variable, and yield losses of up to 100% on the bottom side by a plastic container (Tupper-
are possible (Hohmann and Meneguim 1993). Control ware-type, without a lid) measuring 18.0 cm in diam-
is attained mainly with chemical products, but the eter by 12.0 cm in height, and on top by a screened
lack of insecticide application technologies, in addi- plastic lid (0.02 cm2). These cages were lined inter-
tion to a lack of information about the bioecology of nally with two-ply quilted paper towel (SNOB), and
the pest and grove management systems (e.g., row the adults were fed 10% honey solution supplied to
spacing and pruning), contributes to low efÞciencies. the container by capillary action through a cotton roll
In recent years, the potential for biological control (2.5 by 0.3 cm). There were four treatments: 1) a cage
by using parasitoids of the genera Trichogramma and containing one avocado (ÔBredaÕ) fruit; 2) a cage con-
Trichogrammatoidea (Hohmann and Meneguim 1993, taining one avocado (ÔMargaridaÕ) fruit; 3) a cage
Hohmann et al. 2003) has been demonstrated. Thus, containing an artiÞcial fruit made of green plastic
the objective of this work was to determine in the material; and 4) a cage without fruit. Treatments were
laboratory whether the oviposition behavior of S. repeated Þve times, and the numbers of eggs present
catenifer is inßuenced by chemical (fruit) and physical on the fruit and on the paper were evaluated after 24 h.
(paper) stimuli, and based on these results, to deter- Determination of Physical Stimulus for Oviposi-
mine the egg-laying time, to obtain information for the tion. In this experiment, the effect of different papers
production of large quantities of eggs on a substrate
on oviposition was tested (Fig. 1). Cages were set up
that could be handled easily for biological control
in a manner similar to the chemical stimulus experi-
studies on this pest.
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
Materials and Methods 3) cage lined with 75 g/m2 white smooth ofÞce paper
Experiments were conducted at the Insect Biology (sulÞte) (RIPAX). The nonquilted paper towel was
Laboratory of Departamento de Entomologia, Fito- obtained by ironing the quilted paper towel with suc-
patologia e Zoologia Agrṍcola of Escola Superior de cessive pressings by using an electric iron adjusted to
Agricultura “Luiz de Queiroz” (ESALQ), Univer- 160⬚C. One Breda avocado fruit and a container with
sidade de São Paulo (USP), in Piracicaba-SP, Brazil. 10% honey solution were placed inside the cages to
The rearing rooms were maintained at 25 ⫾ 2⬚C, provide nourishment for the adults. Four replications
60 ⫾ 20% RH, and a photoperiod of 14:10 (L:D) h. were conducted, and the numbers of eggs present on
S. catenifer Rearing. The insects were obtained by the fruit and on the paper were evaluated after 24 h.
collecting infested avocado fruit from orchards lo- Five S. catenifer pairs, including females on the second
cated in the municipality of São Tomás de Aquino, oviposition day, were placed in each cage.
Minas Gerais, Brazil, 20⬚ 52⬘ 30⬙ S, 47⬚ 07⬘30⬙ W, Oviposition Time. Based on preliminary observa-
and 1000-m elevation. In the laboratory, the larvae tions, it was determined that S. catenifer oviposits at
were removed from the fruit and reared on seeds night. Therefore, the experiment was conducted from
placed in transparent acrylic containers (10 by 10 by 1600 to 0600 hours. The previously described PVC
8 cm) until pupation. Individual pupae were placed cage (Fig. 2A), containing Þve S. catenifer pairs, was
under a plastic cup and arranged on a tray containing attached to an iron structure (Fig. 2B) with clasps
Þlter paper, which was moistened daily. After emer- (Fig. 2C); the interior of the cage was lined with
gence, S. catenifer pairs were allowed to mate. Male SNOB two-ply quilted paper towel (Fig. 2D), and the
and female pupae were separated based on the shape 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 0600 hours, with six replicates during 2 d. Eggs on the
between the bench and the base of the cage, corre- paper towel and on the fruit were counted 24 h after
sponding to one sheet for each 2-h interval (Fig. 2F). their removal from the cage because by then the eggs
One fruit was placed inside the cage at the center, had become dark and more conspicuous.
on paper towel sheets, without touching the sides Data Analysis. The experiments were conducted in
(Fig. 2G). The fruit was attached to a string (Fig. 2H) a completely randomized design. To determine a pos-
that was tied to an arm hanging from the iron structure sible chemical stimulus for oviposition, the data for
(Fig. 2I). At evaluation time, the fruit was suspended number of eggs laid on the paper and on the fruit were
a few centimeters on the structureÕs arm, without submitted to analysis of variance (ANOVA), and the
removing the screened plastic lid (0.02 mm2) (Fig. 2J). means were compared by the Tukey test (P ⱕ 0.05).
The PVC cage was then moved a few millimeters For determination of a possible physical stimulus, the
vertically to remove a paper towel sheet, correspond- data were analyzed in a 3 by 2 factorial scheme, con-
ing to the egg-laying time interval, while preventing sisting of the three types of paper (quilted, nonquilted,
the adults from escaping. Later, the fruit was replaced and white sulÞte paper) and two oviposition sites
with another fruit through the upper part of the struc- (fruit and paper). Results were submitted to ANOVA,
ture, by partially lifting the screened plastic lid. and the means were compared by the Tukey test (P ⱕ
Treatments consisted of 2-h egg-laying time inter- 0.05). For determination of oviposition time, the data
vals, i.e., 1800 Ð2000 hours, 2000 Ð2200 hours, 2200 Ð were submitted to a second degree polynomial re-
2400 hours, 2400 Ð 0200 hours, 0200 Ð 0400 hours, 0400 Ð gression analysis.
412 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 98, no. 3

Table 1. Mean number (ⴞ SD) of S. catenifer eggs laid on fruit Table 2. Mean number (ⴞ SD) of S. catenifer eggs laid on fruit
and on paper added as lining to the oviposition cage, on avocado and on paper when the cage was lined with different types of paper
fruit Margarida and Breda, and on artificial fruit, as well as on the
cage without fruit No. eggs
Treatment
Fruit Paper
No. eggs
Treatment Quilted paper towel ⫹ fruit 74.00 ⫾ 13.49bB 315.63 ⫾ 34.66aA
Fruit Paper
Nonquilted paper towel ⫹ 184.75 ⫾ 25.00aA 137.63 ⫾ 70.95bA
Margarida fruit ⫹ paper towel 110.85 ⫾ 22.36aB 321.10 ⫾ 60.29aA fruit
Breda fruit ⫹ paper towel 87.51 ⫾ 19.03aB 362.72 ⫾ 66.28aA SulÞte paper ⫹ fruit 248.00 ⫾ 47.21aA 8.88 ⫾ 04.25cB
ArtiÞcial fruit ⫹ paper towel 10.26 ⫾ 03.06b

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(control) Means followed by the same lowercase letter in the column or
No fruit ⫹ paper towel 08.06 ⫾ 02.55b uppercase letter in the row do not differ among themselves by Tukey
test (P ⱕ 0.05).
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-
Results and Discussion
quilted paper (137.63) or sulÞte paper (8.88) (P ⫽
Determination of Chemical Stimulus. S. catenifer 0.01578). Thus, it was observed that when a chemical
females required avocado fruit for oviposition (Table stimulus from the fruit is present and the egg-laying
1). The number of eggs laid on the fruit, both on substrate (paper) is unsuitable, oviposition occurs
Margarida (110.85) and on Breda (87.51), was statis- preferably on the fruit. Conversely, when available the
tically similar, representing 55.88 and 44.12%, respec- quilted paper was the preferable substrate (315.63),
tively (P ⫽ 0.00001). This preference also was ob- differing signiÞcantly from the number of eggs laid on
served with respect to the number of eggs laid on fruit (74) (Table 2). For the two-ply nonquilted paper
paper near the fruit when one avocado of Margarida towel (without dimples), the numbers of eggs laid on
(321.10) or Breda (362.71) was included in the cage. the fruit (184.75) and on paper (137.63) were statis-
The number was signiÞcantly smaller (P ⫽ 0.00051) in tically similar. However, when cages lined with sulÞte
cages that either contained artiÞcial fruit (10.26) or paper were used, egg laying was higher on the fruit
lacked fruit (8.06). This chemical stimulus for ovipo- (248) than on paper (8.88) (P ⫽ 0.00001).
sition conferred by the substrate also was observed for According to Ramaswamy (1988), physical stimuli
H. virescens. Placing cotton leaves in the upper part of related to the oviposition substrate constitute an im-
the cage increased oviposition on voile and on the portant tactile cue for lepidopteran females. However,
paper that lined the cage internally (Moreti and Parra for S. catenifer, it was demonstrated that the physical
1983). According to Jackson et al. (1986), H. virescens stimulus is related to the chemical stimulus (Table 1),
oviposition on tobacco leaves was inßuenced by because no oviposition occurred on the quilted paper
chemical substances of the terpene group. In other towel without the presence of fruit. Controversy exists
species, such as Tuta absoluta (Meyrick) (Gelechi- with regard to the roles of physical versus chemical
idae), the association of an olfactory (tomato leaf stimuli in the tortricid Choristoneura fumiferana (Cle-
extract) with a visual stimulus (green polyethylene) mens) (Tortricidae), a pest of conifers in North Amer-
stimulated more eggs to be deposited than on a “nat- ica. Renwick and Radke (1982) suggested that phys-
ural” oviposition substrate (tomato plant leaves) ical stimuli were more important than chemical stimuli
(Mihsfeldt 1998). in relation to oviposition behavior, whereas Städler
Regardless of the presence of an avocado fruit, the (1974) concluded that chemical stimuli were more
number of eggs laid on paper, in all treatments, was important.
signiÞcantly higher than the number laid on fruit (P ⫽ It was observed that a chemical stimulus is required
0.00001) (Table 1). This demonstrates that, in spite of for S. catenifer oviposition in the laboratory, which is
the chemical cue, females selected a speciÞc oviposi- provided by the avocado fruit. Notwithstanding, to
tion substrate. In this experiment, the quilted paper obtain a large amount of eggs on an easy-to-handle
towel was suitable for oviposition and was similar to substrate, it is necessary to line the cage with quilted
egg-laying sites under Þeld conditions, where eggs are paper towel, for appropriate physical stimulus, which
laid in crevices, on necrotic areas of the avocado fruit, provides protection for the eggs. Future research
and on the pedicel of the fruit. In a Þeld study by should determine which chemical extracts from the
Hohmann et al. (2003), ⬎50% of the eggs were laid on fruit stimulate oviposition so that after their synthesis,
the pedicel. they could be used instead of fruit.
Physical Stimulus Determination. The type of pa- Oviposition Time. The polynomial regression anal-
per placed in the cage inßuenced choice of oviposition ysis for factor time indicated a signiÞcant quadratic
site (Table 2). The number of eggs laid on fruit was effect (P ⫽ 0.0013, F ⫽ 12.95476, R2 ⫽ 0.7513; y ⫽
higher when either smooth ofÞce (sulÞte) paper 16.86 ⫺ 3.72x ⫹ 0.18x2), where coefÞcients were dif-
(248) or nonquilted paper towel (184.75) was used as ferent from zero by StudentÕs t-test (P ⱕ 0.05) (Fig. 3).
cage lining, signiÞcantly differing from cages lined The point of maximum oviposition is 2200 Ð2400 hours
with quilted paper towel (74) (P ⫽ 0.0212). This during which ⬇60% of all eggs are deposited, despite
probably is attributable to paper texture because the that oviposition occurred during the entire scoto-
May 2005 NAVA ET AL.: OVIPOSITION BEHAVIOR OF S. catenifer 413

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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- Hohmann, C. L., and A. M. Meneguim. 1993. Observações
tween 2000 and 2400 hours. This egg-laying behavior preliminares sobre a ocorrência da broca do abacate,
is variable among Lepidoptera. Garcia (1998) ob- Stenoma catenifer Wals. no estado do Paraná. Ann. Soc.
served that Ecdytolopha aurantiana (Tortricidae) ovi- Entomol. Bras. 22: 417Ð 419.
posits during the day, and 16.12% of eggs were re- Hohmann, C. L., A. M. Meneguim, E. A., Andrade,
T. C. Novaes, and C. Zandoná. 2003. The avocado fruit
corded from 0700 to 1900 hours. However, the greatest
borer Stenoma catenifer (Wals.) (Lepidoptera: Elachisti-
egg-laying percentage was concentrated from 1900 dae): egg and damage distribution and parasitism. Rev.
to 2300 hours, when 78.96% of eggs were laid. For Bras. Frutic. 23: 432Ð 435.
S. catenifer, no oviposition was observed during the Jackson, D. M., R. F. Severson, A. W. Johnson, and
day, and thus it can be said that its egg-laying habit is G. A. Herzog. 1986. Effects of cuticular duvane diterpe-
crepuscular/nocturnal, because egg laying started at nes from green tobacco leaves on tobacco budworm
1800 hours and ended at dawn by 0800 hours. Al- (Lepidoptera: Noctuidae) oviposition. J. Chem. Ecol. 12:
though this study was conducted under laboratory 1349 Ð1359.
conditions, where transitions from day to night (pho- Medina, J. C. 1978. Abacate: da cultura ao processamento e
tophase/scotophase) occurred in an abrupt manner, comercialização. Ital, Campinas, Brasil.
this behavior may be similar to what occurs under Þeld Mihsfeldt, L. H. 1998. Biologia e exigências térmicas de
Tuta absoluta (Meyriek, 1917) em dieta artiÞcial. Ph.D.
conditions.
dissertation, Escola Superior de Agricultura Luiz deq
Ueiroz, Universidade de São Paulo, Piracicaba, Brasil.
Acknowledgments Moreti, A. C., and J.R.P. Parra. 1983. Biologia comparada e
controle de qualidade de Heliothis virescens (Fabr., 1781)
We thank José Carlos Gonçalves (Café Total Company) (Lepidoptera: Noctuidae) em dietas naturais e artiÞcial.
for funding this research and Coordenação de Aperfeiçoa- Arq. Inst. Biol. 50: 7Ð15.
mento do Ensino Superior (CapesÐCoordination for the De- Nitao, J. K., and M. R. Berenbaum. 1988. Laboratory rearing
velopment of Higher Education Personnel) for granting a of the parsnip webworm, Depressaria pastinacella (Lep-
doctoral scholarship. idoptera: Oecophoridae). Ann. Entomol. Soc. Am. 81:
485Ð 487.
Parra, J.R.P., A. E. Eiras, M. L. Haddad, E. Vilela, and
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