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Studies on some aspects of the biology and ecology of Citrus butterfly Papilio demoleus (Papilionidae: Lepidoptera) on citrus in Vietnam

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The citrus butterfly Papilio demoleus L. (Papilionidae: Lepidoptera) is considered among the most important insect pests of citrus trees in Vietnam. Observations on the mean development times (in days) of various life stages of P. demoleus on Citrus sinensis (L.) were carried out under laboratory conditions. Our results show that the egg-hatching time and development period of P. demoleus immature stages decreased as temperature increased from 250 to 300C. The citrus butterfly had a life cycle of 35.50 days at 250C and 22.88 days at 300C. Eggs at 250, 26.50, 28.50 and 300C hatched in 3.55, 3.48, 3.08 and 2.06 days, respectively. This pest typically has five instars and duration of larval stage ranged from 11.50 days at 300C to 17.93 days at 250C. The average time of pupal stage was reduced from 12.46 days at 250C to 7.33 days at 300. Adult longevity of the pest on honey diets was about 2-5 days. The average reproduction rate per female on honey diet was low at 21.67 eggs. Leaf-feeding capacity of P. demoleus larvae on citrus leaves had a positive correlation with nymphal ages. The mean leaf quantity consumed by the fifth instar was highest (2.68±0.15g/day). Results of study on biological traits of P. demoleus would be valuable scientific evidence on building citrus butterfly management programs.
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Entomology
Journal!of!Tropical!Asian!
Lepcey&
Studies!on!some!aspects!of!the!biology!and!ecology!of!
Citrus!butterfly!Papilio'demoleus!(Papilionidae:!
Lepidoptera)!on!citrus!in!Vietnam
!
Hoang Gia Minh1*, Ho Thi Thu Giang2 and Ho Thi Quynh Trang3
1 Vietnam Academy of
Agricultural Sciences, Hanoi,
Vietnam
2 Entomology Department,
Faculty of Agronomy, Vietnam
National University of
Agriculture, Hanoi, Vietnam
3 Plant Quarantine Diagnostic
Center, Hanoi, Vietnam
*Correspondence:
hoanggia_minh85@yahoo.com
Received: 27 October 2014
Accepted: 2 December 2015
Geotags: Hanoi, Vietnam
[20.9371 N, 105.8419 E],
Northern Vietnam
[20°42'08.4"N 105°20'14.0"E]
Abstract!
The citrus butterfly
Papilio demoleus
L. (Papilionidae:
Lepidoptera) is considered among the most important insect pests
of citrus trees in Vietnam. Observations on the mean development
times (in days) of various life stages of
P. demoleus
on
Citrus sinensis
L. were carried out under laboratory conditions. Our results show
that the egg󵛁hatching time and development period of
P. demoleus
immature stages decreased as temperature increased from 250 to
300C. The citrus butterfly had a life cycle of 35.50 days at 250C and
22.88 days at 300C. Eggs at 250, 26.50, 28.50 and 300C hatched in 3.55,
3.48, 3.08 and 2.06 days, respectively. This pest typically has five
instars and duration of larval stage ranged from 11.50 days at 300C
to 17.93 days at 250C. The average time of pupal stage was reduced
from 12.46 days at 250C to 7.33 days at 300. Adult longevity of the
pest on honey diets was about 2󵛁5 days. The average reproduction
rate per female on honey diet was low at 21.67 eggs. Leaf󵛁feeding
capacity of
P. demoleus
larvae
on citrus leaves had a positive
correlation with nymphal ages. The mean leaf quantity consumed by
the fifth instar was highest (2.68±0.15g/day). Results of study on
biological traits of
P. demoleus
would be valuable scientific evidence
on building citrus butterfly management programs.
.
Keywords: caterpillar, fecundity, herbivory, life history, temperature
ISSN 2012 8746 |
04
(1): 20–27 | Published 30 December 2015 !!OPEN!
RESEARCH!ARTICLE!
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Introduction!
Papilio demoleus L. (Papilionidae: Lepidoptera), commonly known as citrus butterfly
(Figure 1), is found throughout tropical and subtropical areas of Southern and Southeast Asia
(Guerrero et al. 2004). This butterfly ranges widely and is an extremely successful invader.
Moreover, P. demoleus whose caterpillars are a serious insect pest feeding on citrus leaves and
blossoms, are a potential threat to citrus nursery stocks and other young citrus trees in Asia and
the Middle East (Lewis 2012; CABI 2013). In Vietnam, to date, this species is distributed widely
in many citrus production regions (NIPP, 1999). Globally, to develop improved strategies of
managing P. demoleus, numerous studies have been conducted in various localities to provide
valuable information on its biology (Singh & Gangwar 1989; Ramarethinam & Loganathan
2001) and ecology (Badawi 1981; Nandni et al. 2012) from subtropical to tropical regions. More
importantly, precise understanding of life-history parameters of insect pests is essential for
monitoring and studies of population dynamics. In Vietnam, however, knowledge of the
biology of this species is rarely known at both local and national scales. This research carried
out studies on the biology, food consumption of larvae and longevity of this insect under
laboratory conditions.
Methods!!
Experimental setup: P. demoleus pupae (Figure 1) were collected originally from citrus
orchards in Vietnam’s northern (20°42'08.4"N 105°20'14.0"E). Pupae were placed into plastic
vials (15cm in diameter and 25cm in height) until emergence. Each vial has a mesh lid for
ventilation. One-day-old adults were collected and mated after sexual identification. A young
citrus seedling with young shoot-tip leaves was put in net cages (50x50x50cm) with mated
adults for 2-day reproduction periods in order to obtain a cohort of eggs for the experiments.
At least 10 plants were used at each treatment condition. The eggs on leaves were marked and
observed daily using magnifiers to determine incubation time, development time of nymphal
stages and various other life cycle parameters of P. demoleus under different temperatures (n>10
at each treatment).
Fecundity: To determine fecundity of P. demoleus female adults, fifteen couples were
transferred individually into plastic vials covered with net lids (30cm in diameter and 35cm in
height). An artificial diet (honey 100%) was used as a food source for adults. The plastic vials
were checked daily to count mean numbers of eggs produced from the 1st day to the 5th day by
using magnifiers. Similarly, to investigate longevity of adults, five artificial diets (Distilled water,
honey 20%, 50%, pure honey and solution of sugar 50% and water) were designed. One P.
demoleus couple was transferred into a transparent plastic vial to measure mean longevity of P.
demoleus adults. Ten couples were designated on each diet.
Leaf-feeding capacity: To measure leaf-feeding capacity of age-specific larvae of P. demoleus,
ten larvae at different ages were placed individually into plastic vials with fresh young citrus
leaves. Leaf weight was measured (g) before and after feeding of larvae. Leaves were renewed
daily. Leaf-feeding capacity (g/day) of age-specific larvae was measured daily the difference in
the leaf weight.
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Figure 1. Lifecycle of The citrus butterfly Papilio demoleus: a. Female butterfly; b. Male butterfly; c. Egg; d.
1st instar larvae; e. 2nd instar larvae; f. 3rd instar larvae; g. 4th instar larvae; h. 5th instar larvae; i. Pupa. Scale
bars: a & b, 10 mm; ci, 5 mm.
Statistical Analysis: Statistical analysis was performed using SigmaPlot version 12.2. Means
were compared using Student-Newnan-Keuls method in one-way ANOVA to assess impact of
temperature on incubation period and development time of the immature stage of P. demoleus
and impact of artificial diets on adult longevity. Differences in probability level (P0.05) were
considered significant.
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Results!and!Discussion!!
Development time of eggs and immature stages of P. demoleus
The development periods of incubation and immature stage of P. demoleus on citrus
trees at various temperatures are summarized in Table 1. Our results indicated that the egg-
hatching time and development period of P. demoleus immature stages decreased as
temperature increased. All of the developmental stages of the species were affected by change
in temperature ranging from 250 to 300C (P<0.001). However, there were no significant
differences in incubation period at 250C and 26.50C (P=0.436). The larvae typically had five
stadia and total development time of nymphal stages varied at different temperatures (P<0.001).
The longest development duration of larvae was observed at 250C valuing 17.93 days, while the
shortest was 11.5 days at 300C. The development period of larval stage was about 4-5 times
longer than that of incubation time at all temperatures tested. Pupal period at 250C and 300C
was 12.46 days and 7.33 days, respectively.
Table 1. Mean (days±SE) development period of incubation and immature stage of Papilio demoleus L. on
citrus trees at various temperatures
Mean (days±SE) development duration of egg and immature stages
300C, 70%r.h.
28.50C, 77.2%r.h
26.50C, 86.5%r.h.
250C, 70%r.h.
2.60±0.10c (n=25)
3.08±0.14b (n=35)
3.48±0.15a (n=33)
3.55±0.20a (n=20)
1.70±0.12c (n=25)
2.31±0.08b (n=30)
2.61±0.13a (n=29)
2.78±0.17a (n=18)
1.96±0.13c (n=24)
2.19±0.08c (n=27)
2.56±0.12b (n=27)
2.94±0.13a (n=17)
1.61±0.12c (n=23)
2.29±0.09b (n=25)
2.64±0.12a (n=24)
3.00±0.16a (n=16)
2.60±0.13b (n=22)
2.70±0.11b (n=25)
3.42±0.10a (n=24)
3.57±0.14a (n=14)
3.60±0.13d (n=20)
4.08±0.11c (n=25)
4.91±0.14b (n=23)
5.43±0.17a (n=14)
11.50±0.27d (n=20)
13.60±0.25c (n=25)
16.17±0.35b (n=23)
17.93±0.32a (n=14)
7.33±0.37c (n=18)
7.39±0.28c (n=23)
10.68±0.39b (n=22)
12.46±0.45a (n=13)
Means followed by the different letter within a row are significantly different (Student-Newnan-Keuls test one-way ANOVA; P0.05)
Like other ectotherms, development of insect species is influenced by climatic
conditions, especially temperature (Bale et al. 2002). In this study, it could be suggested that
duration of P. demoleus development stages was significantly dependent on changes in
temperature under laboratory condition. Badawi (1981) reported that the longest and shortest
periods recorded were 6.1 and 3.1 days for the egg stage, 22.7 and 12.9 days for the larval stage
and 22.4 and 8.0 days for the pupal stages respectively, depending on temperature regimes
tested. The infestation of P. demoleus increased significantly with the increase in maximum
temperature (Chatterjee et al. 2000). The egg, larval, pupal and adult stages lasted 3.4 days, 13.1
days, 9.9 days and 1.5 days, respectively (Dang 2005). The total larval period of P. demoleus was
observed to be 17.98 ± 2.08 days. The pupal period was 11.57 ± 0.92 days (Nandni et al. 2012).
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We believe that differences in total development period of P. demoleus could be attributed to
differences in environmental factors, rearing methods or host plant quality.
Table 2. Mean (days±SE) pre-reproduction and generation time of P. demoleus L. on citrus trees at various
temperatures and relative humidity levels
Temperature and humidity
Pre-reproduction time
Generation time
n
Mean (days±SE)
n
Mean (days±SE)
300C, 70% r.h.
16
1.13±0.08c
13
22.88±0.48d
28.50C, 77.2% r.h
22
1.40±0.11c
20
25.40±0.44c
26.50C, 86.5% r.h.
20
1.47±0.11b
17
31.50±0.59b
250C, 70% r.h.
11
2.27±0.14a
11
35.50±0.73a
Means followed by the different letter within a column are significantly different (Student-Newnan-Keuls test one-way ANOVA; P0.05)
Life cycle of P. demoleus on citrus trees at different temperatures
The results of the experiments revealed that pre-oviposition and generation time of P.
demoleus were affected by temperature, which decreased following increase in temperature
(Table 2). The duration of pre-reproduction ranged from 1.13 days to 2.27 days at different
temperatures tested; however, no significant difference was found at 28.50 and 300C. The pre-
reproduction period in temperature 300C was about half that of in temperature 250C. Similarly,
mean generation time of P. demoleus was significantly longer at 250C with a value of 35.5 days
than at any other temperature regimes tested, ranging from 22.88 days at 300C, 25.4 days at
28.50C and 31.5 days at 26.50C.
Our findings were consistent with previous studies. For example, Rafi et al. (1996)
showed that pre-oviposition period was 1-2 days. Lewis (2012) reported that the average length
of a P. demoleus generation varied from 26 to 59 days, and this pest is capable of producing
multiple generations in a year depending on environmental variables, including temperature.
Dang (2005) also found that life cycle of P. demoleus was approximately 25–36 days, the average
being 29.5 days at 28.60C and 77.5% r.h. Similar results reported by Nandni et al. (2012) suggest
that average generation time of P. demoleus reared on citrus leaves was approximately 29.55 ±
3.06 days.
Fecundity and longevity of P. demoleus
In this study, the fecundity of P. demoleus reared on honey 100% was low, with
production an average of 21.67eggs/female (Table 3). The average egg production of a female
was highest (13.06 eggs/female) on the 2nd date after adult emergence. P. demoleus fecundity
decreased steadily on the 5th day with only 0.27 eggs/female. Our results were similar to an
earlier study by Dang (2005), who reported that reproduction capacity of P. demoleus was
observed to be very low, with only 22.9 eggs/female at temperature 28.40C and 75.2%r.h.
Similarly, Rafi et al. (1996) showed that the number of eggs produced by a single female of P.
demoleus ranged from 10 to 45 eggs, depending significantly on environmental variables and
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other biotic factors. However, reproduction values of P. demoleus on citrus leaves obtained by
Mishra and Pandey (1965) were higher than those on honey, ranging from 10 to 183
eggs/female. Also, on citrus plants in Southern Iran, Sharifi and Zarea (1970) found that a
female may lay up to 110 eggs. Our results find that, compared to many of insect pests belonging
to Lepidoptera family, the fecundity of P. demoleus was still low in despite of availability of food
sources. This is a reason why P. demoleus rarely become an epidemic species on citrus in
Vietnam.
Table 3. Fecundity of P. demoleus L. female adults reared on a 100% honey diet
Observation dates
(after adult emergence)
Number of eggs/female/day
Minimum
Maximum
Mean (eggs±SE)
1st day
3
12
5.86±0.86 (n=15)
2nd day
6
21
13.06±1.35 (n=15)
3rd day
0
5
1.80±0.44 (n=15)
4th day
0
2
1.00±0.23 (n=11)
5th day
0
1
0.27±0.14 (n=11)
Mean eggs/female
21.67±1.07
Table 4. Longevity of P. demoleus L. adults reared on different artificial diets (at 300C and 70%r.h.)
Artificial diets
n
Mean longevity of Papilio demoleus L. adults
Minimum
Maximum
Mean (±SE)
Disttiled water
10
1
2
1.10±0.18c
Honey 20%
10
2
4
3.23±0.26a
Honey 50%
10
2
5
3.50±0.42a
Pure honey
10
3
5
4.17±0.25a
Sugar 50 % + water solution
10
1
4
2.52±0.40b
Means followed by the different letter within a column are significantly different (Student-Newnan-Keuls test one-way ANOVA; P0.05)
In nature, adult female P. demoleus require a source of nutrition, provided by sources
such as pollen, nectar and honeydew or by host feeding, to promote longevity and facilitate egg
production. Longevity of the female adult is an important life table parameter to conserve
generation development and increase species population growth. In this study, longevity of P.
demoleus was examined on different diets of honey, sugar and water considered as natural food
source of the species (table 4). Results of statistical analysis revealed that differences in
concentration of honey in diets did not affect adult lifespan of P. demoleus (P>0.05). The mean
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adult longevity of the species was lowest (1.1 days) reared on distilled water, while this value
was 2.52 days on a diet of sugar solution. Maximum longevity of P. demoleus adults reared on
honey diets was about 5 days. A similar study by Dang (2005) showed that the longevity of
female adult was about 2-5 days on pure honey diet at 28.40C and 75.2%r.h. Additionally,
seasonal climatic condition may influence adult longevity of the pest. For example, Badawi
(1981) reported that adult longevity on citrus ranged from 4 to 6 days with an average of 5.1
days during spring. Similar report on mandarin plants carried out by Singh and Gangwar
(1989), mean lifespan of male and female adult was 5.1 days and 5.8 days, respectively.
Leaf-feeding capacity of P. demoleus larvae at different ages
Larvae of the citrus butterfly showed a different capacity of food consumption during
the larval instars. The mean leaf quantity consumption in gram was presented in Table 5. Leaf-
feeding capacity of P. demoleus larvae on citrus leaves had a positive correlation with nymphal
ages. Leave feeding activities of 4th and 5th larvae were rapid in comparison to other larval stages.
Our results are consistent with the results of Nandni et al. (2012) and Dang (2005).
Table 5. Mean leaf consumption of age-specific larvae
Age-specific larvae
Leaf consumption (g/day)
Minimum
Maximum
Mean (±SE)
1st larvae
0.008
0.34
0.13 ± 0.02e
2nd larvae
0.08
0.71
0.30 ± 0.02d
3rd larvae
0.16
1.22
0.63 ± 0.05c
4th larvae
0.26
3.43
1.19 ± 0.13b
5th larvae
0.66
4.56
2.68 ± 0.15a
Means followed by the different letter within a column are significantly different (Student-Newnan-Keuls test one-way ANOVA; P0.05)
Conclusion
Our results show that temperature is a key factor influencing the development of P. demoleus.
The egg-hatching time and development period of P. demoleus immature stages decreased as
temperature increased from 250 to 300C. Also, temperature plays an important role in the
decrease of populations in winter moths and in the relative abundance of P. demoleus in warm
months where mean generation time is shorter. Fourth and fifth larvae of P. demoleus showed
a high capacity of citrus leave consumption, compared to other instars. Moreover, adult
longevity of the species was short ranging from 2 to 5 days when rearing on honey diets. In term
of fecundity, the mean number of eggs laid by a P. demoleus female were low (21.67 eggs) in
despite of availability of food source and rearing condition. Due to low reproduction rate, P.
demoleus is less likely to damage severely on citrus plats in Vietnam. Results of study on
biological traits of P. demoleus would be valuable scientific evidence on building citrus butterfly
management programs.
!
!
!
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References!
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butterfly Papilio demoleus (Papilionidae: Lepidoptera) on citrus in Vietnam. Journal of Tropical Asian
Entomology 04 (1): 20 – 27
... erature, the incubation period was 4.812±0.403 days (represents 5.006% of the complete development cycle time). When temperature range between 27.67 0 and 30.53 0 C for warmer months, its incubation periods was 3.032±0.221 days (represents 10.337% of the complete development cycle time). The present observation is more or less similar with that of Hoang et. al. (2015) [11] findings. They found that the incubation period of P. demoleus was 2.60±0.10 days, 3.08±0.14 days, 3.48±0.15 days and 3.55±0.20 days at 30 0 C, 28.5 0 C, 26.5 0 C, and 25 0 C temperature respectively. Our findings were also consistent with Hoang et al (2015) [11] studies because of incubation periods increased with the decreased of ...
... The present observation is more or less similar with that of Hoang et. al. (2015) [11] findings. They found that the incubation period of P. demoleus was 2.60±0.10 ...
... days at 30 0 C, 28.5 0 C, 26.5 0 C, and 25 0 C temperature respectively. Our findings were also consistent with Hoang et al (2015) [11] studies because of incubation periods increased with the decreased of temperature and it becomes shorten with enhanced temperature. The larvae/caterpillar of P. demoleus typically had five instars and total larval development time (time elapsed between egg hatch and 5 th instar/final instar) significantly varied at different temperatures (P<0.05). ...
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Papilio. demoleus (L) is considered among the major insect pest of citrus cultivated areas in Bangladesh. In this study, we investigated the effect of winter months temperature (18.55 0 C to 25.37 0 C) and warmer months temperature (27.67 0 to 30.53 0 C) on development cycle and pupal coloration of P. demoleus. Results showed that development of the P. demoleus was slow at lower temperature and at the high temperature, developmental rate was fast. Towards the end of the November when temperature was 24.12 0 C, P. demoleus pupae entered into diapause and spent following months; December, January and middle of February in dormancy/diapause. Adults emerged at the end of February when temperature range was 25.5 0 C to 27 0 C with average 26.44 0 C, for this reason winter months pupal period was about six times longer than pupal period of warm months. We found that temperature had a significant effect on P. demoleus pupal coloration. Larvae maintained in winter environment had more brown pupae (76.19%) and less green pupae (9.53%), whereas more green pupae (65.38%) and less brown pupae (11.54%) were found when larvae maintained in warmer environment.
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Papilio demoleus L., a well-known citrus pest in the Old World, is documented from eastern Dominican Republic on the Caribbean island of Hispaniola. Resumen. Se registra la especie Papilio demoleus, una reconocido plaga de los citricos en el Mundo Viejo, para la Hispaniola Republica Dominicana.
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Life cycle of swallow tail butterfly, Papilio demoleus L. (Papilionidae: Lepidoptera) infesting the curry leaf, Murraya koenigii (L.) Sprengel was studied under the controlled laboratory condition. The results indicated about an average of 34.60 ± 8.15 days for the completion of one generation, i.e., egg to adult was recorded. Observations on the mean development times (in days) of various life stages such as egg incubation (5.67 ± 1.82), larval period (17.52 ± 3.45), pupal period (11.42 ± 2.94) and adult longevity (Female = 6.25 ± 1.28; Male = 3.40 ± 0.95) were also made and reported. The effectiveness of a neem oil based botanical pesticide - Nimbecidine (EC preparation with 0.03% azadirachtin) against swallow tail butterfly was also evaluated and reported.
Article
Papilio demoleus L. is considered among the most important pests of citrus trees in Saudi Arabia. Studies on the biology, food consumption of larvae and mortality rate of this insect were carried out under laboratory conditions. Five generations were reared during the period from mid October 1979 to end of June 1980. The longest and shortest periods recorded were 6.1 and 3.1 days for the egg stage, 22.7 and 12.9 days for the larval and 22.4 and 8.0 days for the pupal stages respectively. The insect seems to have about 8 generations a year in Riyadh region. During spring adult longevity ranged between 4 and 6 days with an average of 5.1 days.
Article
Papilio demoleus demoleus L. is an important pest of citrus plantations in southern Iran. The female deposits up to 110 eggs. The mean times required for incubation, larval, and pupal stages were 3.24, 18.25, and 11.7 days, respectively. The whole life cycle had a mean of 33.19 days, and the insect had 4 generations per year at Shiraz. The larva had 5 stadia and at the end of the 5th stadium there was a distinguishable prepupal stage which lasted 1–2 days. The effect of differences in sources of food on the life cycle was determined, using leaves from 6 species and 1 variety of citrus. It was found that overall duration of larval stages was statistically shortest on lemon, and then on sweet lime, while duration on mandarin orange was longest. Four other kinds of citrus did not induce significant differences in the duration of larval life. The kind of host plant had no effect on the length of pupal stage.
Herbivory in global climate change research: direct effects of rising temperature on insect herbivores
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Dang T. D. (2005) Morphological and Biological Characteristics of Swallow-tail (Papilio demoleus L.) (Papilionidae, Lepidoptera) on Citrus at Hanoi Agricultural University Area Journal of Science and Development vol. 2 (In Vietnamese with English abstract).
Lime swallowtail, chequered swallowtail, citrus swallowtail Papilio demoleus Linnaeus (Insecta: Lipidoptera: Papilionidae). Department of Entomology and Nematology; Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences
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Lewis D. S. (2012) Lime swallowtail, chequered swallowtail, citrus swallowtail Papilio demoleus Linnaeus (Insecta: Lipidoptera: Papilionidae). Department of Entomology and Nematology; Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL 32611.
Some observations on the biology of Papilio demoleus Linn (Papilionidae: Lepidoptera)
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Mishra S., & Pandey N. (1965) Some observations on the biology of Papilio demoleus Linn (Papilionidae: Lepidoptera). Labdev Journal of Science and Technology 3(2): 142-143.
Life cycle, population index and feeding activities of the lime butterfly, Papilio demoleus (Lepidoptera: Rhopalocera: Papilionidae)
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Nandni D., Raghuwanshi A., & Shrivastava V. K. (2012) Life cycle, population index and feeding activities of the lime butterfly, Papilio demoleus (Lepidoptera: Rhopalocera: Papilionidae). Trends in Biosciences 5(1): 31-34.