Download Some aspects of the biology of the lemon butterfly

Some aspects of the biology of the lemon butterfly Papilio
demodocus
Esper. (Lepidoptera; Papilionidae) and its
preference to three
citrus cultivars.
By
Ali Mukhtar Mohamed Abdallah
B.Sc. (Agric.) Honours
University of Khartoum, 2000
A thesis submitted to the University of Khartoum in partial
fulfillment of the requirements for the degree of
M.Sc. Crop Protection
Supervisor,
Prof. El Sayed El Bashir Mohamed
Department of Crop Protection
Faculty of Agriculture
University of Khartoum
December 2006
DEDICATION
To my family whose
love and pray
enlightened my way.
To those who gave
me care and love,
I dedicate this work.
ACKNOWLEDGEMENTS
Thanks to Almighty Allah who gave me patience to complete
this work. It is a pleasure to acknowledge with sincere thanks and
appreciation the continuous help and guidance of my supervisor Prof.
El Sayed Elbashir for his invaluable help throughout the preparation
of the thesis.
Thanks are also extended to Dr. Elwasila Guddoura, lecturer
at the Department of Crop Protection and to my brother Musab
Mukhtar who encouraged me to register for M.Sc.
Thanks are due to my friend Elhadi Mursal, for his help and
invaluable advice. I would like to thank the staff members of the Crop
Protection Department of the Faculty of Agriculture, U. of K.
Thanks are due to Sania Jobara, for her help and Fawzia
Shukartalla for typing this thesis.
LIST OF CONTENTS
Title
Page
Dedication………………………………………….………………………………………………………………………….……
i
Acknowledgements …………………………………………………………………………………………………….…
ii
List of Contents………………………………………………………………………………………………………………...
iii
List of Tables…………………………………………………………………………………………………………………….
vi
List of Figures…………………………………………………………………………………………………………………...
viii
List of Plates………………………………………………………………………………………………………………….......
ix
English Abstract ……………………………………………………………………………………………………………..
x
Arabic Abstract…………………………………………………………………………..…………………………………….
xi
CHAPTER ONE: INTRODUCTION…………………….…………..………………………………
1
CHAPTER TWO: LITERATURE REVIEW…………………………………………………
4
2.1. Classification of Papilio demodocus Esper. ..……………………………………
4
2.2. Morphology .……………………….………………………………………………………………………………..
5
2..2.1 The Egg……………………………………………………………………………………………………………….
5
2.2.2 The Larva…………………………………………………………………………………………………………....
6
2.2.3 The Pupa……………………………………………………………………………………………………………
7
2.2.4 Distinguished male and female features…………………………………………….
8
2.2.5 The Adult……………………………………………………………………………………………………………
8
2.3 Distribution and economic importance………………………………………………
9
2.4. Life history ..………………………………….……………………………………………………………………..
12
2.4.1 The egg stage…………………………………………………………………………………………………….
12
2.4.2 The larval stage.………………………..……………………………………………………………………..
13
2.4.3 The pre-pupal stage..………………………………………………………………………………………
15
2.4.4 The pupal stage………………………………………………………………………………………………..
15
2.4.5 Adult life span ………………………………………………………………………………………………….
16
2.5 Host plants ..………………………………..………………………………………………………………………..
16
2.6 Behavior…………………………………………………………………………………………………………………..
18
2.7 Natural enemies……………………………………………………………………………………………
20
2.7.1 Natural enemies of the egg…………………………………………………………………
20
2.7.2 Natural enemies of the larva……………………………………………………………...
21
2.7.3 Natural enemies of the pupa……………………………………………………………….
21
2.7.4 Entomopathogenic agents…………………………………………………………………………
22
2.8 Control of Papilio demodocus Esper.……………..……………………………………….
23
2.8.2 Chemical control……………………………………………………………………………………………
23
2.8.2.1 Insecticides……………………………………………………………………………………………………
23
2.8.3 Botanicals ………………………………………………………………………………………………………….
24
2.8.4 Mechanical control…………………………………………………………………………………………
24
CHAPTER THREE: MATERIALS AND METHODS……………..………….……
25
3.1. Site of the study..…………………………………………………………………………...………………………
25
3.2 Field survey .…………………………………………………………………….……………………………………
25
3.3 Rearing of Papilio demodocus Esper.………………………………………………………
26
3.4 Assessment of host preference.………………………………………………………………………
26
3.6 Morphological studies...…………………………………………………………………………………….
27
CHAPTER FOUR: RESULTS………………………………………………….…………………………
30
4.1 The biology ..…………………………………………….…………………………………………………………
30
4.1.1 Egg stage ..………………………………………………...…………………………………………………………
30
4.1.2 Larval stage ..……………………………...………………………………………………………………………
30
4.1.3 Pupal stage ..……………………………………….………………………………………………………………
30
4.1.4 Adult stage ..……………………………………..…………………………………………………………………
33
4.2 The morphology and description………………………………………………………………
33
4.2.1 The eggs.……………………………………………………………………………………………………………
33
4.2.2 The larval stage.…………………………………………………………………………………………………
33
4.2.3 The pupa ..……………………………………………………………………………………………………………
34
4.2.4 The adult………………………………………………………………………………………………………………
34
4.3 Food preference
……………………………………………………………...………………………………
38
CHAPTER FIVE: DISCUSSION AND CONCOLUSION……………………
41
REFERENCES…………………………………………………………………………….………………………………..…
47
APPENDICES
54
LIST OF TABLES
Table Title
Page
The duration of the different immature stages of Papilio
1
demodocus Esper. reared under laboratory conditions
31
(at 20 – 28 ºC and 44 - 63 R.H %.).
2
3
The development period of different stages of Papilio
demodocus Esper.
The body measurements of the different stages of
Papilio demodocus Esper.
32
36
LIST OF FIGURES
Fig.
Title
Page
1
Petri-dishes containing larvae and lemon leaves………………
28
2
Netted plants…………………………………………………………………………………………..
28
3
Adult rearing cage………………………………………………………………………………...
29
4
Equipment used in the experiment…………………………………………….
29
Damage caused by lemon butterfly fed on host plant for
5
3 days…………………………………………………………………………………………………………
39
Damage caused by lemon butterfly fed on host plant for
6
6 days………………………………………………………………………………………………………….
39
Damage caused by lemon butterfly fed on host plant for
7
9 days………………………………………………………………………………………………………….
40
LIST OF PLATES
Plate Title
Page
1.
The different stages in the life cycle of Papilio demodocus Esper.
37
2.
The nature of the damage caused by 5th larval instar.
40
ABSTRACT
The lemon butterfly Papilio demodocus Esper (Lepidoptera :
Papilionidae) also known as, citrus butterfly and orange dog butterfly
is a major pest of citrus trees and nurseries in the Sudan. Field surveys
were conducted during the course of this study at the nursery and the
Shambat Farm of the University of Khartoum while the labrotary
experiments were conducted at the Entomology laboratory of the
Department of Crop Protection of the Faculty of Agriculture,
University of Khartoum. The study aimed to investigate the biology
and morphology of the lemon buttterfly reared on leaves of lemon
plant, and to determine the degree of preference of
the lemon
butterfly to different citrus cultivars.
The development of the immature stages were followed under
laboratory conditions, (20-28°C and R.H. 44-63%). Egg incubation
period lasted for 4 to 5 days (average 4.2 ± 0.42). Larval duration
lasted for 17 to 19 days with an average of 17.7 ± 0.42 days. Pupal
period ranged from 8 to 9 days with an average of 8.2 ± 0.42 days.
The whole life cycle lasted for 29 to 32 days averaging 30.2 ± 1.032
days.
The egg is small round in shape, pale yellow but turns to dark
brown before hatching ; it shows a red mark on the top . The colour of
the first three larval instars ranged from black to dark brown and from
greenish to bright green for 4th and 5th instars respectively. The adult
is quite large in shape, dark brown with numerous pale yellow green
spots; the forewings are long and narrow, cream with green
longitudinal median wedges. Both sexes are alike but the female is
larger than the male in the size .
The results showed that, in the nurseries, the larvae of the
lemon butterfly preferred lemon to orange and the latter to grapefruit.
‫ﻤﻠﺨﺹ ﺍﻷﻁﺭﻭﺤﺔ‬
‫ﺘﻌﺘﺒﺭ ﺤﺸﺭﺓ ﺍﺒﻭﺩﻗﻴﻕ ﺍﻟﻤﻭﺍﻟﺢ ﺍﻟﺘﺎﺒﻌﺔ ﻟﺭﺘﺒﺔ ﺤﺭﺸﻔﻴﺔ ﺍﻻﺠﻨﺤﺔ ﻤﻥ ﺍﺨﻁﺭ ﺍﻻﻓﺎﺕ‬
‫ﻋﻠﻰ ﺍﻟﻤﻭﺍﻟﺢ ﻭﺒﺎﻻﺨﺹ ﻋﻠﻰ ﺍﻟﺸﺘﻭل‪ .‬ﺸﻤﻠﺕ ﺍﻟﺩﺭﺍﺴﺔ ﺍﻟﻤﺴﺢ ﺍﻟﺤﻘﻠﻲ ﻟﻤﺯﺭﻋﺔ ﺠﺎﻤﻌﺔ‬
‫ﺍﻟﺨﺭﻁﻭﻡ ﺒﺸﻤﺒﺎﺕ ﻭﺍﻟﺘﺠﺎﺭﺏ ﺍﻟﻤﻌﻤﻠﻴﺔ ﺒﻤﻌﻤل ﺍﻟﺤﺸﺭﺍﺕ ﺍﻟﺘﺎﺒﻊ ﻟﻘﺴﻡ ﻭﻗﺎﻴﺔ ﺍﻟﻤﺤﺎﺼﻴل‬
‫ﻭﺍﻟﻤﺸﺘل ﺒﻜﻠﻴﺔ ﺍﻟﺯﺭﺍﻋﺔ – ﺠﺎﻤﻌﺔ ﺍﻟﺨﺭﻁﻭﻡ ﺒﻐﺭﺽ ﺩﺭﺍﺴﺔ ﺩﻭﺭﺓ ﺍﻟﺤﻴﺎﺓ ﻭﺍﻟﺸﻜل ﺍﻟﻅﺎﻫﺭﻱ‬
‫ﻟﺤﺸﺭﺓ ﺍﺒﻭﺩﻗﻴﻕ ﺍﻟﻤﻭﺍﻟﺢ ‪ Papilio demodocus Esper.‬ﻭﺩﺭﺠﺔ ﺘﻔﻀﻴﻠﻬﺎ ﻟﺜﻼﺜﺔ ﺍﻨﻭﺍﻉ‬
‫ﻤﻥ ﺍﻟﻤﻭﺍﻟﺢ) ﻟﻴﻤﻭﻥ‪،‬ﺒﺭﺘﻘﺎل ﻭﻗﺭﻴﺏ ﻓﺭﻭﺕ(‪.‬‬
‫ﺘﻀﻤﻨﺕ ﺍﻟﺩﺭﺍﺴﺔ ﻤﺘﺎﺒﻌﺔ ﻟﺩﻭﺭﺓ ﺤﻴﺎﺓ ﺍﻟﺤﺸﺭﺓ ﺘﺤﺕ ﺍﻟﻅﺭﻭﻑ ﺍﻟﻤﻌﻤﻠﻴﺔ ﺤﻴﻥ‬
‫ﺘﺭﺍﻭﺤﺕ ﺩﺭﺠﺎﺕ ﺍﻟﺤﺭﺍﺭﺓ ﻤﺎ ﺒﻴﻥ ‪ 28-20‬ﺩﺭﺠﺔ ﻤﺌﻭﻴﺔ ﻭﺍﻟﺭﻁﻭﺒﺔ ﺍﻟﻨﺴﺒﻴﺔ ﻤﺎ ﺒﻴﻥ‪-44‬‬
‫‪.%63‬‬
‫ﺨﻼل ﺩﺭﺍﺴﺔ ﺩﻭﺭﺓ ﺤﻴﺎﺓ ﺍﻟﺤﺸﺭﺓ ﻭﺠﺩ ﺃﻥ ﻓﺘﺭﺓ ﺤﻀﺎﻨﺔ ﺍﻟﺒﻴﺽ ﺘﺘﺭﺍﻭﺡ ﻤﺎﺒﻴﻥ ‪4‬‬
‫ﺇﻟﻰ ‪ 5‬ﺃﻴﺎﻡ ﺒﻤﺘﻭﺴﻁ ‪ 4,20± 0,42‬ﻴﻭﻤﹰﺎ‪ .‬ﻭﺃﻥ ﻓﺘﺭﺓ ﻨﻤﻭ ﺍﻟﻁﻭﺭ ﺍﻟﻴﺭﻗﻲ ﻻﺒﻭﺩﻗﻴﻕ ﺍﻟﻤﻭﺍﻟﺢ‬
‫ﺘﺘﺭﺍﻭﺡ ﻤﺎﺒﻴﻥ ‪ 17‬ﺇﻟﻰ ‪ 19‬ﻴﻭﻡ ﺒﻤﺘﻭﺴﻁ ‪ 17,7± 0,42‬ﻴﻭﻤﹰﺎ ﻭﺍﻥ ﻓﺘﺭﺓ ﺘﻁﻭﺭ ﺍﻟﻌﺫﺭﺍﺀ‬
‫ﺘﺭﺍﻭﺤﺕ ﻤﺎ ﺒﻴﻥ ‪ 8‬ﺇﻟﻰ ‪ 9‬ﺃﻴﺎﻡ ﺒﻤﺘﻭﺴﻁ ‪ 8,2 ± 0,42‬ﻴﻭﻤ ﹰﺎ‪ .‬ﻭﺩﻭﺭﺓ ﺍﻟﺤﻴﺎﺓ ﺍﻟﻜﺎﻤﻠﺔ ﺘﺭﺍﻭﺤﺕ‬
‫ﻤﺎ ﺒﻴﻥ ‪ 29‬ﺇﻟﻰ ‪ 32‬ﻴﻭﻤﹰﺎ ﺒﻤﺘﻭﺴﻁ ‪ 30,2 ±1,032‬ﻴﻭﻤ ﹰﺎ‪.‬‬
‫ﻭﻤﻥ ﺨﻼل ﺩﺭﺍﺴﺔ ﺍﻟﺸﻜل ﺍﻟﻅﺎﻫﺭﻱ ﻟﻠﺤﺸﺭﺓ‪ ،‬ﺃﻭﻀﺤﺕ ﺍﻟﻨﺘﺎﺌﺞ ﺃﻥ ﺍﻟﺒﻴﻀﺔ ﺼﻐﻴﺭﺓ‬
‫ﻭﻜﺭﻭﻴﺔ ﺍﻟﺸﻜل‪،‬ﺼﻔﺭﺍﺀ ﺍﻟﻠﻭﻥ ﺘﺘﺤﻭل ﺍﻟﻰ ﺍﻟﻠﻭﻥ ﺍﻟﺒﻨﻰ ﻗﺒل ﺍﻟﻔﻘﺱ ﻤﻊ ﻭﺠﻭﺩﻋﻼﻤﺔ ﺤﻤﺭﺍﺀ‬
‫ﻓﻰ ﻗﻤﺘﻬﺎ‪ .‬ﺃﻤﺎ ﻟﻭﻥ ﻴﺭﻗﺔ ﺍﺒﻭﺩﻗﻴﻕ ﺍﻟﻤﻭﺍﻟﺢ ﻓﻴﺘﺭﺍﻭﺡ ﻤﺎ ﺒﻴﻥ ﺍﻻﺴﻭﺩ ﺇﻟﻰ ﺒﻨﻰ ﻏﺎﻤﻕ ﻤﻊ‬
‫ﻭﺠﻭﺩ ﺃﺸﻭﺍﻙ ﺒﻁﻨﻴﺔ ﻟﻼﻁﻭﺍﺭ ﺍﻟﺜﻼﺘﺔ ﺍﻻﻭﻟﻰ‪،‬ﻭﺍﻟﻠﻭﻥ ﺍﻟﻤﺨﻀﺭ ﺍﻟﻰ ﺍﻻﺨﻀﺭ ﻟﻼﻁﻭﺍﺭ ﺍﻟﺭﺍﺒﻊ‬
‫ﻭﺍﻟﺨﺎﻤﺱ‪.‬ﺍﻟﻌﺫﺭﺍﺀ ﺘﺸﺒﻪ ﺍﻟﺤﺸﺭﺓ ﺍﻟﻜﺎﻤﻠﺔ‪ ،‬ﺫﺍﺕ ﻟﻭﻥ ﺍﺨﻀﺭ ﺍﻟﻰ ﺒﻨﻰ‪ .‬ﺍﻟﻁﻭﺭ ﺍﻟﻜﺎﻤل ﻻﺒﻭﺩﻗﻴﻕ‬
‫ﺍﻟﻤﻭﺍﻟﺢ ﺠﻤﻴل ﺍﻟﺸﻜل ﻭﻜﺒﻴﺭ ﺍﻟﺤﺠﻡ ﻟﻭﻨﻪ ﺒﻨﻰ ﺩﺍﻜﻥ ﻤﻊ ﻭﺠﻭﺩ ﺒﻘﻊ ﺼﻔﺭﺍﺀ ﻤﺨﻀﺭﺓ ‪.‬‬
‫ﻫﻨﺎﻙ ﺸﺒﺔ ﻜﺒﻴﺭ ﺒﻴﻥ ﺍﻟﺫﻜﺭ ﻭﺍﻻﻨﺜﻰ ﺇﻻ ﺃﻥ ﺤﺠﻡ ﺍﻟﺫﻜﺭ ﺃﺼﻐﺭ ﻤﻥ ﺤﺠﻡ ﺍﻷﻨﺜﻰ‪.‬‬
‫ﺃﻅﻬﺭﺕ ﻨﺘﺎﺌﺞ ﺍﻟﺘﺠﺎﺭﺏ ﺍﻟﺘﻰ ﺃﺠﺭﻴﺕ ﻓﻰ ﺍﻟﻤﺸﺘل ﺃﻥ ﺍﻟﻴﺭﻗﺎﺕ ﺘﻔﻀل ﺃﻭﺭﺍﻕ‬
‫ﺍﻟﻠﻴﻤﻭﻥ ﺜﻡ ﺍﻟﺒﺭﺘﻘﺎل ﻭﺃﺨﻴﺭﺍ ﺍﻟﻘﺭﻴﺏ ﻓﺭﻭﺕ‪.‬‬
CHAPTER ONE
INTRODUCTION
The citrus swallowtail butterfly,(orange dog, chequered swallowtail,
lemon butterfly) (Papilio demodocus Esper.), belongs to the family Pipilionidae.
Its older name was Popilio demoleus Linnaeus (El Khidir, 1968 and Schmutterer,
1969). Papilio demodocus Esper is a major pest of citrus trees and nurseries in the
Sudan (Sania, 1992).
Papilio demodocus Esper is the common, large black and pale yellow
butterfly seen regularly in gardens in South Africa and also occurring in natural
vegetation. It occurs in open, often disturbed, habitat throughout Africa south of
the sahara, as well as in Cape Verde Islands, Madagascar and Mauritius (Ackery
et al., 1995).
In the Sudan, Papilio demodocus Esp. is distributed throughout the entire
country whenever sufficient citrus trees are found, especially in Equatoria and
along river vallies. During the rainy season it is more common than during the dry
season (Schmutterer, 1969). Wilson (1950) reported three species of Papilio,
other than P. demodocus, which attack citrus trees in northern and central Sudan
A powerful flying butterfly, which tends to fly 1-2 m above the
ground, like most of the swallowtail butterflies, it usually feeds on flowers while
on the wing, similar to hummingbirds. If disturbed before it is ready for flying,
such as early in the morning or while it is hardening it's wings after emerging
from the pupa, the butterfly will suddenly open the wings fully, exposing the two
pairs of eye-like spots on the hind wing. This response is very startling to
predatory birds. Some females feed like hummingbirds on the flowers of the
native verbine food plants, while busily laying eggs.
Citrus (Citrus spp. Rutaceae) cultivars infested by this pest include
orange, lemon, lime, mandarin, tangerine, grape fruit, and pomolo. Most of these
species of citrus are native to South East Asia. They are thorny, aromatic shrubs
or small trees with leathery evergreen leaves. The white or purple flowers are
usually very fragrant. They are cultivated from about 45°N to 35°S, between sealevel and l000 m, and are susceptible to frost unless a tree is dormant; they do not
grow well in the very humid tropics (Hills, 1981).
For many butterflies, an average temperature of 25-26°C, relative
humidity of 80-100% and daily rainfall of 50 mm were the most favourable
(Mathew, 2001). Peak activity period of P. demoleus L. is synchronized with the
emergence of new foliage (Narayanamma and Savithri, 2002). Yunus and Munir
(1972) concluded that the caterpillar preferred young nursery plants 1-2 feet high
and were capable of completely defoliating nursery groves.
In Sudan, the identity of the lemon butterfly infesting the important crop
plants (citrus species), the nature and magnitude of the damage it causes were
considered by few workers. Generally, the main factors which encourage
investigations of the lemon butterfly in Sudan may by summarized as follows:
Lack of information about the lemon butterfly, its biology, ecology, behaviour,
physiology, efficient methods of control and its natural enemies. Hence, the aim
of this investigation focuses on:
1. Study of the biology of Papilio demodocus Esper.
2. Determination of the degree its preference for three
main citrus cultivars grown in Sudan: (lemon, orange and
grape-fruit).
CHAPTER TWO
LITERATURE REVIEW
2.1 Classification
Kingdom
:
Animalia
Phylum
:
Arthropoda
Class
:
Insecta
Order
:
Lepidoptera
Family
:
Papilionidae
Genus
:
Papilio
Tribe
:
Papilionini
Species
:
demodocus demodocus Esper (1798)
Linnaeus, 1758
(= Papilio demoleus )
Common name : Citrus swallowtail, Christmas butterfly, lemon butterfly,
Orange dog.
Local Arabic name : ‘Abudagig el Mawalih’
According to Hancock (1983), a new classification of the Papilionidae,
based largely on a phylagenetic study of all species, is presented. The 33 genera
recognized are placed in 4 sub-families, one fossil and 17 new subgenera.
Considerable number of taxonomic changes are proposed, which included
splitting of the large genus Papilio into 6 genera and 8 subgenera, this affects a
considerable number of well-known and less well-known pest species. A total of
561 species is recognized, of which 4 are fossil.
2.2 Morphology
2.2.1 The Egg
The egg is large, pale yellow, nearly spherical about 1.5 mm, basally
flattened, smooth. If fertile, a small red mark or cross develops at the egg top. The
eggs are laid singly near the edges of the leaves of the food plant. Embryonic
development within the egg commences immediately after laying. The egg shell
is eaten by the newly emerging larvae, but most of the egg shells or larvae are
consumed by various tiny predators that suck out the contents of the egg (Grund,
2002). The egg is spherical but the surface attached to the plant is slightly
flattened. It is pale yellow when freshly laid, but the colour changes to brown and,
finally to black perior to hatching. The average diameter is slightly less than 1.00
mm (El Khidir, 1968 and Badawi, 1968). Schmutterer (1969) reported that the egg
is globular whitish at the beginning and turned to black towards the end of the
incubation period.
2.2.2 The larva
The young larval stage is brownish to blackish in colour except for the
yellowish anterior and posterior parts, and the white central parts. A fully-grown
larva is green with black or grey to brownish transverse and longitudinal stripes
(Schmutterer, 1969).
Grund (2002) reported that the larva passess through five larval instars;
initially, black coloured, with two subdorsal rows of short, bristly, fleshy spines.
The head is also black. Second, third and fourth instars are dark brown, shiny,
with the anterior, middle and posterior parts having broad transverse off-white
bands, giving the larva ‘a bird dropping’ camouflage pattern typical for the
swallowtail group of butterflies. The fleshy spines are less prominent and not as
bristly. They also acquire an additional row of paired fleshy spines on the thorax.
Head is brown, smooth, shining, with some short hairs. Fifth instar is 45 mm long,
green in colour with a lateral row and two pairs of subdorsal rows of orange or
pink spots edged black. The larva eats the egg shell after emergence, before
proceeding to scout the leaf surface. Later instars devour the entire leaf, from any
part of the plant.
2.2.3 The Pupa
The pupa is at first greenish-yellow then it turns brown. There is no
silken cocoon round the pupa, this is a naked pupa and typical of that of
butterflies. Externally the pupa is rather like the adult having well developed
wing pads, thoracic legs and antennae, enclosed in a thin cuticle (Depury, 1968).
The pupa is reasonably stout, rugose, about 30 mm long, the ventral part
containing the wing cases and the dorsal abdominal parts are bowed, anterior end
produced into a short pair of flattened projections, the thorax has prominent
projections dorsally and laterally, and there is an additional projection laterally
where the abdomen meets the wing case. There are also ridges laterally along the
thorax and again between the dorsal and lateral-abdominal projections. It is
attached to the thicker stems of the food plant, or to adjacent sticks and rocks. It
reclines from the vertical, and is attached by the posterior cremaster and a central
silken girdle (Grund, 2002).The colour of the pupal body is determined by a
hormone that produces brown coloration, known as the pupal cuticle melanizing
hormone (PC MH) which is secreted by the brain suboesophageal ganglion and
prothoracic ganglion (Br-SG-PG) complexes during the pharate pupal stage
(Yamanaka et al., 1999). Pupa is yellow or brown, fastened in upright position on
the tip of the abdomen with a gridle of silk round its thorax (Schmutterer, 1969).
2.2.4 Distinguishing Male and Female Features of The juvenile Stages
A search for external morphological characters that would facilitate the
sexing of P. demoleus L. in the larval and pupal stages showed that female larvae
have pairs of small triangular areas of transparent cuticle on each of the eighth and
ninth sternites, and that female pupae have a small narrow verticle furrow
extending over these two sternites. Male larvae and pupae can be distinguished
only by the absence of these characters (Sarivastara and Kumar, 1979).
2.2.5 The Adult
The butterfly has a wing span of 70-86 mm, forewing dark-grey or
blackish with numerous sulfur-yellow spots of different sizes. Hind wing has the
same ground colour as forewing, with a yellow transverse sub-median band, a
number of yellow spots and a colourful eye spot near the anterior and inner
margins. Abdomen blackish with longitudinal yellowish stripes (Schmutterer,
1969). A large tailless swallowtail that is mostly creamy yellow and black. Both
sexes are alike. In freshly emerged specimens, the cream yellow colour is almost
fluorescent, but this lovely brightness gradually changes into rusty orange with
age (Poorten, 2004).
The butterfly flies by day and females are often seen near the citrus trees
on which they lay their eggs, which are round and white and are laid singly on
leaves or stems, preferably near young succulent shoots (Depury, 1968). The
male and female adults look very much a like (Chua, 1978). The adult is quite
large and black with conspicuous bright yellow marking, and has two eye-spots
on each hind wing (El Khidir, 1968 and Badawi, 1968). The adult is a handsome
swallowtail butterfly often seen feeding on the nectar of various flowers. The
general colour is dark brown with numerous pale yellow markings (Hills, 1981).
The lemon butterfly is a large butterfly with a wing span about 9 cm (Depury,
1968).
2.3 Distribution and Economic Importance
The discovery of this butterfly in the West Indies may be of some
importance as this vagile butterfly species is an important citrus pest throughout
much of its Old World range, which is rapidly expanding (Badawi, 1981). In
India, Narayanamma et al., (2001) reported up to 83% defoliation of young grove
trees in Andra Pradesh, and Thakare and Borle (1974) reported an outbreak severe
enough to skeletonize an entire citrus garden. Individuals of P. demoleus are seen
throughout the year but their populations reach the peak before the onset of the
heavy monsoon rains (Poorten, 2004). In Qatar Papilio deomoleus L. was found
on cultivated citrus in gardens (Pittaway, 1980).
Divender and Gupta (2000) recorded Papilio demoleus (Papilio
demodocus) as a serious citrus pest in India where it is distributed country wide.
An identical infestation of the citrus dog (Papilio demoleus Linnaeus) increased
significantly with the increase in maximum temperature and relative humidity
(Chatterjee et al., 2000). P. demoleus larvae accept leaves of at least 19 citrus
species or varieties, but show some differences in consumption rates, development
time and mortality (Yunus and Munir, 1972).
Papilio spp. (P. demodocus Esp: (Africa), P. memon: (South and South
East Asia), P. thoat L: (Tropical America) and other species attack the leaves of
citrus trees (Schmutterer et al., 1977). The larvae prefer young nursery plants 1-2
feet high and are capable of completely defoliating nursery groves (Yunus and
Munir 1972; Thakare and Borle 1974; Singh 1993a; Matsumoto 1996, 2002;
Naryayanamma et al., 2001). Papilio demoleus L. occurs in Saudi Arabia,
Pakistan, India, South East Asia, South China, Taiwan, Australia, Pupua New
Guinea and West Iran (Hills, 1981).
Papilio demoleus L., is found throughout Southern Asia (Corbet and
Pendlebury, 1992), extending from Iran (Larsen, 1977) to India, and from the
Indo-Pacific (Van Wright and de Jong, 2003) to New Guinea and Australia
(Parsons, 1998; Braby, 2000), in parallel with the native or introduced range of its
principal host plants in the genus citrus (Rutaceae). Papilio demodocus Esp.
occurs in many countries in Africa, Asia and Australia where citrus is grown
(Schmutterer, 1969). Matsumoto (1996, 2002) reported the recent arrival of P.
demoleus into tropical regions such as the Dominican Republic, where favourable
climatic conditions and the preferred host plants prevail and where the population
of potential natural enemies is low. It could easily spread throughout the West
Indies and surrounding areas, including the United States where the impact could
be very high. P. demoleus is a successful invasive species, recently spreading
throughout an Old World island system very much like that in the Caribbean.
Beginning in the 1970s, this species invaded the islands of Java, Borneo,
Philippines and Sumarta, apparently facilitated by deforestation and the increased
availability of citrus groves. Ram-Pratap et al., (2000) documented the incidence
of P. demoleus on lime in Bundel Khan,India from July 1992 to July 1996 and
showed that maximum damage by this pest occurs from August to September. In
the Sudan, the lemon butterfly is distributed throughout the country, wherever
large enough population of citrus trees is found. But it is more common during the
rainy season, (July and August) (El Khidir, 1968). The different stages of the
caterpillars defoliate the trees and feed at the edges of either flush or hard leaves
(Hills, 1981).
2.4 Life History
2.4.1 The Egg Stage
The female settles on the host plant and, while still flapping its wings,
bends the abdomen downwards on to the leaf surface and lays an egg (Ackery et
al., 1995). Two eggs per leaf were noticed on the lower or upper surface of leaves
(El Khidir, 1968). Alturi et al., (2002) documented in India larval development
through to the adult stage using larvae reared on leaves of lemon (citrus limon
Burm) in the laboratory. They noted that eggs are laid singly, but may reach 8-10
eggs over 2-3 days, on the surface of young leaves and twigs. The eggs hatch in 45 days.
In the Sudan, the eggs were reported to be laid on the tender leaves and
very rarely on the twigs (Badawi, 1968 and Schmutterer, 1969). The eggs are laid
singly on flush leaves and hatch after about four days (Hill, 1981). The female
readily deposited eggs in response to methanolic extract of the Rutaceous plant
Toddalia asiatica (Nakayama et al., 2003). Egg development takes about 6 days
under warm conditions (Ackery et al., 1995). The incubation period of the eggs in
the Sudan ranged between 3 and 4 days under laboratory conditions (El Khidir,
1968), 4 and 5 days (Badawi, 1968 and Schmutterer, 1969). Farahbaksh and
Kashkooli (1978) reported that the female of P. demoleus L. laid 12-77 eggs, and
the eggs were laid singly on the lower surface of the young leaves. The egg
incubation period averaged 3.61 days, the shortest and longest periods recorded
for the egg stage were 3.1 and 6.1 days (Badawi, 1981).
2.4.2 The Larval Stage
The larva eats its way out of the egg and then consumes the remains of
the egg shell (Ackery et al., 1995). The young caterpillar hatches and feeds on a
citrus leaf (Depury, 1968). There are five larval instars; the first three are dark
brown with white markings which resemble bird droppings; the fourth and fifth
instars are pale green caterpillars with black, brown and grey markings. Fully
grown caterpillar is 5 cm or more long. The larval period lasts about 30 days
(Hills, 1981).
In the Sudan, the average duration of the different instars is: 3.5, 2.9, 4.1,
4.5 and 8.5 days for the first to fifth instars, respectively (El Khidir, 1968). The
duration of the fifth instars is 27-35 days (Atluri et al., 2002). In Saudi Arabia, the
larval stage took 18-32 days; optimum conditions for rearing of the different
stages were 30°C and 21% R.H. (Abu Yaman, 1973). The caterpillar moults
several times as it grows and at the last moult it changes colour completely and
becomes bright green with some black markings (Depury, 1968).
In Pakistan, the duration of 5 larval instars was 3,3,3,3 and 4 days
respectively (Rafi et al., 1989). Larvae take about a month to develop, reaching a
maximum size of about 45 mm (Ackery et al., 1995).
In Djahram area in Iran, the larval stage averaged 16.68 days in AprilSeptemper and 30.85 days in October (Farahbaksh, and Kashkooli, 1978). In
Saudi Arabia, the longest and shortest periods recorded for the larval stage were
22.7 and 12.9 days (Badawi, 1981).
2.4.3 The Pre-Pupal Stage
Badawi (1968) recorded that the pre- pupal stage took about one, two or three
days as exceptional.
2.4.4 The Pupal Stage
Alturi et al., (2002) documented that pupation took about 10-12 days.
Ackery et al., (1995) reported that when the caterpillar is fully grown, it spins a
mat of silk on a twig or leaf of the host plant to which it attaches the tip of its
abdomen. It pupates within 2 days, first spinning a griddle of silk to hold itself in
a slanting position.The pupal period lasts 2-3 weeks. Schmutterer (1969)
mentioned that the pupa is found on twigs. Certain pupae release the butterfly a
number of days after pupating (short term pupae), others after some weeks or
months (long term pupae). In winter, the life cycle takes about 1- 1.5 months in
central Sudan, in summer it is somewhat shorter. In irrigated areas and in
Southern Sudan the insect can be found the whole year round. The duration of the
pupal period decreased with an increase of temperature , ie averaged 8.0 days
during March and 11.87 days during November (Badawi, 1968).
2.4.5 Adult Life Span
In Sudan, the adult life span in the field is less than a week (Badawi,
1968). Elsewhere it takes about 7-12 days (Alturi et al., 2002). However, Asokan
(1997) recorded an adult longevity of 4-5 days and a total life cycle of 30-50 days.
The adult lived for an average of 6.21 days. According to Farahbakhsh and
Kashkooli (1978) the life cycle takes an average period of 34.5 days. In Saudi
Arabia an adult life span during spring ranged between 4 and 6 days with an
average of 5.1 days (Badawi, 1981). The citrus swallowtail passes through about
three generations during spring, summer and autumn with the winter period
usually spent as a hibernating pupa. One can, however, see the occasional adult
during winter (Ackery et al., 1995).
2.5 Host Plant
In July 1973, oviposition by Papilio demodocus Esp. on a small plant of
Euphorbia pilulifera (Litra) beside a citrus bush was reported in Kenya
(Sevastopulo, 1980). Mahesh et al., (2003) reported that lemon was the most
preferred and the most suitable food for the development of P. demolues. Deepak
et al., (1998) showed that females of P. demoleus preferred babchi (Psoralea
corylifolia) more than lemon for egg laying. Larval and pupal periods were longer
on babchi than on lemon and larvae took more time to complete their life cycle on
babchi than on lemon. Larvae consumed more lemon leaves compared with
babchi leaves.
The Larval food-hosts are Cullen(Psoralea) spp including C.
australasicum (tall verbine), C. cinereum (annual verbine), C. graveolens (native
lucerne), C. patens (native verbine), Psoralea pinnata (African scurf-pea)
(Leguminosae/ Papilionoideae). Larvae eat the softer green parts of the foodplant.
The larvae feed on Citrus spp (Grund 2002). Papilio demodocus has also been
found on Aegle marmelos. This note reports its occurrence on Psoralea
corylifolia, an important medical herb, in herbal gardens of the regional
Horticultural Research station at Jachhin Himachal Pradesh in India (Devender et
al., 2000). Yunus and Munir (1972) concluded that the caterpillar preferred young
nursery plants 1-2 feet high and were capable of completely defoliating nursery
groves.
Kroon (1999) reported the following host plants of Papilio demodocus
Esper:
•
Anacordiaceae: Psudospondias sp.
•
Apiaceae: Archangelica officinalis; Deverra burchelli,
Fennel Foeniculum vulgare, Blister bush Peucedanum
galbanum,
Peucedanum
gummiferum,
Piturathos
burchellii.
•
Rutaceae: Cape chestnut Calodendron capense, orange
and lemon trees Citrus spp., Clausena anisata (= C.
inaequalis), Fagara capensis, Oricia bachmannii, O.
swynnertoni, Teclea natalensis, Teclea swynnertonii,
Toddalia aculeate, Toddalia asiatica, Vepris lanceolata,
Zanthoxylum capense, Z. delagoense.
•
Sapidaceae: Hippobromus pauciflorus (= H. alata).
2.6 Behaviour
Observations of the occurrence of dark and light colour patterns in early
instar larvae of Papilio spp. in Florida suggested that they may have been selected
for disruptive coloration, or mimicry of bird or lizard dropping, depending upon
the size of the larval stage and relative occurrence of appropriate models in the
species habitat (Minno and Emmel, 1992).
The mature larvae which feed on shrubs and small trees of the family
Rutaceae, all of which feed and rest in the open on their food plants, are
described. These larvae possess distinctive false-face patterns on the caudal end
which are exposed to approaching predators moving up a stem or leaf petioles
(Minno and Emmel, 1992).
When a larva is disturbed by, for instance, a bird, it rears up and uses
blood pressure to squeeze out a forked, finger-like orange-coloured organ called
an osmetrium from just behind its head. Beside the visual impact of the organ, it
also has a strong smell which acts as a further repellent to the predator. The smell
is evidently caused by accumulation of substances from the oil glands in the
leaves of the host plant. It is thought that it is this osmetrium that gave rise to the
term orange for the caterpillar (Ackery et al., 1995). The eversible cervical gland
or osmetrium of the larva of P. demodocus Esp., was found to produce a secretion
containing isobutyric acid and 2-methyl butyric acid as well as small quantities of
methyl and ethyl esters of these acids. The secretion of final-instar larvae differed
from that of younger larvae (Burger et al., 1978). The 2nd, 3rd and 4th instars larvae
produced qualitatively similar secretions. Remarkable quantitative differences
were found between secretions of individual larvae. These variations could not be
correlated with the diet on which the larvae were fed, their sex, instar stage or
colour form. However, in a number of larvae, the 2 prongs of the osmetrium were
found to produce quantitatively different secretions (Burger et al., 1985).Young
caterpillars are protected by camouflage, their black, yellow and white colouration
making them like bird dropping (Clarke et al., 1963).
Saxena et al., (1975) showed that the larvae of P. demoleus L. were
attracted more to odours of citral, citronellal and citronellol, but slightly less to
geraniol and 1-limonene, and very low to hydroxyl-citronellal and geranyl acetate.
These chemicals (except the last) are the main odour constituents of the leaves of
the food-plant (citrus).
Beck et al., (1999) mentioned the attraction of adult butterflies to moist
soil and dirty places (a behaviour termed ‘mud-puddling’).
2.7 Natural Enemies
2.7.1 Natural Enemies of the Eggs
Eggs of Papilio demoleus collected from citrus trees in India were found
to be parasitized by Telenomus sp., Trichogramma sp. and Ooencyrtus papilionis
(a new record from this host in India). A single egg contained 3-7 adult of O.
papilionis, which lived for 5 days with a total development period of 11-13 days
(Jalali and Singh, 1990). In India Trichogramma shilionis Ishii., and the Scelionid
Telenomus sp. parasitize the eggs of Papilio demodocus (Thakare and Borle,
1974). Trichogramma brassicae parasitizes a number of non-target Lepidopteran
eggs belonging to different families (Babendreier et al., 2003). Eggs of P.
demodocus are parasitized by a small wasp Ooencyrtus spp. (Claasens and
Dickson, 1980).
2.7.2 Natural Enemies of Larvae
Vespa orientalis and unidentified species of praying mantids are reported
as predators of the citrus butterfly Papilio demoleus L. (Singh and Singh, 1998).
Distatrix papilionis is a potential braconid larval parasitoid of citrus butterflies
causing up to 73% parasitism in India (Mani and Krishnamoorthy, 2000). Thakare
and Borle (1974) published photographs of unidentified podisine predators
(Hemiptera: Pentatomidae: Asopinae), which along with some unidentified
dipteran parasitoids, are suggested to regulate local populations of P. demoleus.
Distatrix papilionis (Vireck) Hymenoptera: Braconidae is a potential braconoid
larval parasitoid of citrus butterflies causing up to 73% parasitism in India (Mani
and Kirshnamoorthy, 2000).
2.7.3 Natural Enemies of Pupae
Singh (1993a) reported apparent polymorphism in facultative pupal
diapause, and Badawi (1981) reported pupal mortality caused by application of
Bacillus infusion. Ackery et al., (1995) recorded pupae parasitized by the wasp
Pteromalus puparum (Hymenoptera: Pteromalidae).
2.7.4 Entomopathogenic agents
Acytoplasmic polyhedrosis virus was isolated from larvae of Papilio
demoleus from citrus orchards in Karnataka, India.Third instar larvae died 9-16
days after inoculation. In some cases the virus was associated with natural
parasitism by the braconid Apanteles Papilionis (Narayanan and Gopalakrishnan,
1987).
The butterfly Papilio demodocus was controlled with the DD 136 strain
of Neoaplectana carpocapsae in laboratory and field trials. At a dose of 600,000
nematodes/tree 63.33% kill of 3rd-instar larvae and 67.67% of 4th and 5th-instar
larvae were obtained (Srivastava, 1978).
Narayanan and Yayaraj (1975) reported laboratory tests in India the
effect of infecting larvae with Bacillus thuringiensis. He used 12 days old infected
larvae to measure the mean length, weight and total fat content. When moribund
(40-48 hrs after treatment) the values of these parameters were reduced by 47.8,
62.8 and 90.7%, respectively in comparison with healthy larvae.
2.8 Control of Papilio demodocus Esper.
2.8.1 Chemical control
2.8.1.1 Insecticides
Srivastava (1978) used the insecticides diazinon, monocrotophos and
dichlovovos at concentrations of 0.01 to 0.04% for the control P. demodocus.
Singh and Rao (1978) reported that
0.05% methyl-parathion, 0.05%
methamidophos and 0.06%. leptophos were the most effective and persistent
insecticides for the control of the larvae. Patil and Rajashekhargouda (1985)
reported Endosulfan 35 EC at 36ml/18 litres water was effective in controlling the
pest.
Siddappaji et al., (1977) documented the effectiveness of 14 insecticides
sprayed under laboratory conditions against eggs and larvae of Papilio spp. in
India. They found that methamidophos and quinalphos were the best and most
effective against both stages.
The efficiency of 5 insecticides: endosulfan, carbaryl, dichlorvos, HCH
and parathion were assessed in field trials against P. demoleus on mandarine, in
Jamma, India. All 5 insecticides were effective in reducing infestation, with
dichlorvos, carbaryl and parathion being the most effective (Singh and Kumar,
1986).
2.8.2 Botanicals
Solunk and Deshpande (1991) reported on the lemon butterfly P.
demoleus larvae when fed on citrus leaves dipped in aqueous extract of Ficus
religiosa,Parthenium hysterophonus, Azadirachta indica, Caliothropis gigantean
or Datura stramonium or untreated control. P. hyterophorus extract caused mean
mortality of 52.8% after 72 hrs. Ranjeet et al., (1996) reported on aqueous extract
of neem seed kernel at 0.5% which was tested for the control of P. demoleus, a
pest of the medicinal tree Aogle mormelos in Karnataka, India. Spraying seedlings
twice at an interval of 8 days was effective in providing protection against the
pest. Although low mortality (23.3%) was reported, the extract had strong
antifeedant and repellent effects and was effective as a moulting inhibitor.
2.8.3 Mechanical Control
Manual removal of eggs, larvae and pupae of Papilio demoleus effective in
nurseries and young citrus plantations (Doharey and Butani, 1985). Hand-picking
of caterpillar can be carried out in nurseries or in individual small citrus trees
(Schmutterer, 1969). Hand collection of caterpillar is often effective on small trees
(Hills, 1981).
CHAPTER THREE
MATERIALS AND METHODS
3.1 Site of the Study
The experiments were conducted at the Faculty of Agriculture, University
of Khartoum, Shambat, during 2005/2006. Shambat is located at the eastern bank
of the River Nile (Latitude 51 4 N and longitude 32 32 E.) Surveys were carried
out at the university and adjacent farms and laboratory experiments were
conducted both at a nursery and in the laboratory of the Department of Crop
Protection, Faculty of Agriculture.
3.2 Field Survey
Many farms where citrus trees are grown were randomly and periodically
surveyed. The purpose of these surveys was to record the infestation of Papilio
demodocus Esper., and to collect the different stages(eggs, larvae and pupae) for
further studies..
Laboratory studies focussed on the biology of Papilio demodocus Esper
and on its preference to three citrus cultivars (lemon, orange and grape fruit),
under laboratory and nursery conditions.
3.3 Rearing of Papilio demodocus Esper.
Leaves infested with eggs and larvae of Papilio demodocus Esper. were
collected from the farm, brought to the laboratory and examined to determine the
number and stages of the larvae. Larvae were transferred separately and placed in
Petri-dishes (9.0 cm in diameter) (Fig. 1), and supplied with fresh lemon leaves.
The leaves were daily renewed and faeces were discarded in order to keep the
Petri-dishes clean. The date of pupation and adult emergence were recorded. The
newly emerging adults were kept in rearing cages (62.15x45x45 cm), made of
wooden frames and covered by wire mesh. A muslin cloth sleeve was attached to
one side of the cage to facilitate cleaning, feeding and handling of insects within
the cage. Cotton rolls soaked in 10% sugar solution were provided in each cage as
food for the adult butterflies. Two fresh twigs of a lemon plant were kept in each
cage for oviposition and a branch of Lantana spp. was added to serve as a source
of nectar.
3.4 Assessment of host preference
Experiments were conducted at Shambat area in an orchard belonging to
the Faculty of Agriculture, University of Khartoum during 2005/2006.
Preference of Papilio demodocus Esper to three citrus cultivars (orange:
Citrus sienensis, lemon: Citrus limon, grapefruit: Citrus paradise) was
investigated in a nursery, where four second instar larvae of the lemon butterfly
were transferred to each netted plant (Fig 2). Plants free of larvae served as
control. Treatments were replicated three times and arranged in a completely
randomized block design. The degree of preference was determined by measuring
the total leaf area of each citrus cultivar consumed by the larvae.
3.5 Morphological Studies
The morphology of the different stages of Papilio demodocus Esper was
studied when freshly laid eggs were transferred into small Petri-dishes (5.5 cm in
diameter) and kept until they hatched. The external features, the morphometrics
and colours of the different stages were recorded. Some adult specimens were also
mounted on setting boards whereby different body parts were measured.
Fig (1) Petri-dishes containing larvae and fresh lemon leaves
Fig (2) Netted Plants
Fig (3) Adult rearing cage
Fig. (4) Equipment used in the laboratory experiments
CHAPTER FOUR
RESULTS
.4.1 The Biology
4.1.1 Egg stage
Females of Papilio demodocus Esper lay eggs at day time singly
or in small groups (between 2-3) on the lower and upper surfaces of
the citrus leaves. Eggs usually hatch during the day time after an
incubation period of 4.20 ±0.42 days (Table 1). The newly emerged
larvae eat the egg shells first and then search for other food sources.
4.1.2 Larval stage
The larval development period from egg hatching to the pupal
stage lasted for 17-19 days with a mean period of 17.8 ±0.79. Table 2
shows the duration of each larval stage.
4.1.3 Pupal stage
Table 2 shows the duration of the pupal period, which ranged
8-9 days, (mean 8.2±0.42 days). Before pupation the last larval instar
stopped feeding and attached its body to the upper side of the Petridish or to a branch of the food plant by means of a silk mat.
Table (1 ) The duration of the different immature stages of Papilio
demodocus Esper. reared under laboratory conditions (at 20-28°C
and 44-63% R.H).
Serial No.
of eggs
observed
Incubation
period (days)
Larval
period
(days)
Pupal
period
(days)
1
4
18
8
Total Life
cycle
(days)
30
2
4
17
9
30
3
5
19
8
32
4
4
18
8
30
5
4
17
8
29
6
4
17
8
29
7
5
17
9
31
8
4
18
8
30
9
4
19
8
31
10
4
18
8
30
Mean
4.2
17.8
8.2
30.2
Sd ±
± 0.42
± 0.79
± 0.42
±1.032
4.1.4 Adult stage
Table 2 shows the adult life span, which ranged 4-6 days, (mean 4.5 ±
0.42 days).Adults were always found outside the pupal cases in the morning,
indicating that emergence probably occurred during the night or at the early
hours of the morning. The total development period from egg to the adult
stage ranged from 29 to 32 days (mean 30.2 ± 1.03 days) (Table 1 ).
4.2 The Morphology and Description
4.2.1 The egg
The egg of Papilio demodocus Esper is round in shape and less than
1mm in diameter. The newly laid eggs are bright yellow in colour but they
become dark brown before hatching and show a red mark on the top (Plate
1“i”).
4.2.2 The larval instar
Papilio demodocus Esper. has five larval instars. The first larval
instar is black coloured with a white marking, with two subdorsal rows,
short bristly, fleshy spines and the head is also black, which resembles a
small bird-dropping (plate 1“ii”). The larvae range between 3 mm to 3.5 mm
in length, with a mean of 3.15 ± 0.24 mm (Table 3 ). Second instar (plate
1“ii”) and third instar (plate 1“ii”) are dark brown with white markings
giving the larva bird dropping camouflage patterns. A Larva ranges between
7.5 mm to 9 mm in length, with a mean of 8.15 ± 0.67 mm,15 mm to18 mm
in length, with a mean of 15.6 ± 0.97 mm for second and third instar
respectively (Table 3 ). Fourth instar (plate 1“ii”) and fifth instar larvae
(plate 1“ii”) are greenish to bright green in colour with some black markings
and the mature larvae become bright green in colour. The larvae range
between 24 mm to 25 mm in length, with a mean of 24.5 ± 0.53 mm. 45 mm
to 50 mm in length, with a mean of 47.5 ± 0.53 mm for fourth and fifth
instars respectively (Table 3).
4.2.3 The Pupae
The pupa is first greenish-brown and it changes to dark brown later.
The pupa is naked and typical of butterfly, and there is no silken cocoon
round the pupa. (Plate 1“iii”). The pupal measurements were 23 mm to 25
mm in length, with a mean 23.7± 0.87 mm.(Table 3 ).
4.2.4 The Adult
The adult of is a large-sized butterfly, forewings are long and narrow
with brown and cream chequers colour with blue eyes and red spots on the
hindwings. (Plate 1 “IV”). Wing-span is 80-90 mm, with a mean 85.00±0.47
mm. Total body length from 23 to 25 mm, with a mean 23.8± 0.91 and the
antenna was 15.00 mm long (Table 3).
There is no tail on the hind wing. Upper fore-wing is largely black
and outer wing margin with a series of irregular yellow spots in a discal
band.
4.3 Food preference
The degree of food preference is measured by the amount of the
consumed leaf area under nursary conditions using three citrus species
(Orange:Citrus sienensis, Lemon:Citrus limon, Grapefriut:Citrus paradise).
The results in (Fig 5) revealed that four larvae per plant during a
period of 3 days consumed 118.37,18.99,13.99 cm² of leaf area of lemon,
orange and grape fruit respectively. This showed that there was highly
significant differences among the citrus species. Lemon was the most
preferred host plant.
The results in (Fig 6) shows the amount of damage caused by four
larvae when kept on the plants for 6 days. The larvae consumed 283.65,
218.16, 125.185 cm² of leaf area of lemon, orange and grape fruit
respectively. There were no significant differences between the citrus
species with respect to the degree of damage when feeding continued for 6
days. However, the sizes of the leaf area consumed after 9 days were
373,295.26,210.18 cm² of lemon, orange and grape fruit respectively. The
degree of prefrence was highly significant among the citrus species and
lemon was the most preferred host plant (fig 7).
50
45
40
35
30
25
20
15
10
5
0
R1
R2
G
R3
O
L
Fig. (1). First reading
Fig (5) Damage caused by lemon butterfly fed o+n host plant for 3 days
120
100
80
60
40
20
0
R1
R2
G
R3
O
L
Fig. (2). Second reading
Fig (6) Damage caused by lemon butterfly fed on host plant for 6 days
140
120
100
80
60
40
20
0
R1
R2
G
R3
O
L
Fig. (3). Third reading
Fig (7) Damage caused by lemon butterfly fed on host plant for 9 days
Plate ( 2) Nature of damage caused by 5th larval instar
CHAPTER FIVE
DISCUSSION AND CONCLUSION
The lemon butterfly Papilio demodocus Esper. (Lepidoptera:
Papilionidae), is one of the major pests of citrus plants, especially in
nurseries and on young plants in orchards in Sudan (Sania, 1992).
In this study, Papilio demodocus Esper was found to have five larval
instars, a result confirming the findings of Elkhider (1968) who reported 5-6
instars. The egg incubation period lasted 4-5 days with a mean period of
4.20 ± 0.42 days. This result also agrees with the findings of Hills (1981),
Alturi et al., (1995), Badawi (1981) and Elkhider (1968) who reported an
incubation period in Sudan ranging between 3 and 4 days, but it differs from
that reported by Rajinder, et al. (1997) who obtained an incubation period
ranging from of 2.1 to 3.5 days.
The larval period ranged from 17-19 days with a mean duration of
17.8 ± 0.79 days. This is similar to the results of Farahbaksh et al., (1978)
and Rafi et al., (1989) who recorded a period of 16 days. On the other hand,
El-Khidir (1968) and Hills (1981) reported a larval period of 23-30 days,
which is totally different from the findings reported in this study.The prepupal period lasted for one day. This result supports the findings of Rajinder
et al., (1997), but it differs from that of Ackery et al., (1995) who reported a
pre-pupal period of 2 days.
The development period of the pupal stage ranged from 8 to 9 days
with a mean period of 8.2 ± 0.42 days. Comparable results were obtained by
Badawi (1968) for the shortest pupation period which lasted for 8 days. On
the other hand, Badawi reported a period of 22.4 days and Ackery et al.,
(1995) a period of up to 3 weeks for the longest pupation period.
The total duration of the life cycle of the lemon butterfly varies from
29 to 32 days with a mean duration of 30.2 ± 1.032 days. This is generally in
agreement with the findings of Rafi et al., (1989) and Schmutterer (1969),
but it differs from the results of Mahesh et al., (2002) who reported a period
of 30 to 45 days.
Adult longevity lasted for a period of 4-6 days which is different
from the 7 days reported by Rafi et al., (1989) for both males and females.
The egg is round in shape, bright yellow in colour but it turns dark
brown before hatching, and it is less than 1mm in diameter. These findings
agree with results of Elkhidir (1968) but are different from those of Sania
(1992) who reported that the egg of Papilio demodocus was over 1mm in
diameter. Rajinder et al., (1997) stated that the average length of the egg was
1.08 mm. These differences may be due to the weather condition and the
amount of food taken by the larva.
The average body length in the current study of 1st,2nd , 3rd, 4th and 5th
larval instar and pupa were 3.15 ± 0.24, 8.15 ± 0.67, 15.6 ± 0.95, 24.5 ±
0.53, 47.5 ± 3.54 and 23.9 ± 0.87 mm, respectively. This result is different
from that obtained by Rajinder et al., (1997) who reported the average sizes
of the 1st,2nd , 3rd, 4th and 5th instar and pupa as 2.89, 5.60, 7.50, 11.60, 26.5
and 28.86 mm, respectively.
The average size of the adult, wing-span and the antenna in the present
study were 23.8 , 85.00, and 15 mm, respectively. Other morphological
characters of the larval instars, pupae and adult are similar to the findings of
Grund (2002), Ackery et al., (1995), Hills (1981), Depury (1968) and
Schmutterer (1969).
The results show that the lemon butterfly preferred lemon more than
orange and that grapefruit was the least attractive cultivar. This result agrees
with the findings of Sania (1992) who found lemon more susceptible to
attack by the lemon butterfly than orange and grapefruit. Deepak et al.,
(1998) who reported a comparative study on the biology of
Papilio
demoleus on lemon Citrus limon and babchi Psoralea corylifolia showed
that larvae consumed more lemon leaves compared with babchi leaves,
Narayanamma and Savithri (2002) reported that fully grown larvae
consumed up to 92.34% of the leaf area of a two-year old sweet orange cv.
on the 13th day after release. At four larvae (second instar) per plant 52.5,
72.5 and 80.0% of the leaf area was consumed on the 5th, 10th and 13th day
after release on the plant respectively.
Saxena et al., (1975), showed that the larvae of P. demoleus L. were
attracted more to odours of citral, citronellal and citronellol, but slightly less
to geraniol and 1-limonene, and very low to hydroxyl-citronellal and geranyl
acetate. These chemicals (except the last) are the main odour constituents of
the leaves of the food-plant (citrus). Guenther (1949) reported that lemon
leaves have a higher citral content (the attractant to the larvae), while orange
and grape fruit leaves have lower content.
CONCLUSIONS
Infestation of citrus plants with Papilio demodocus Esper (the lemon
butterfly) is always synchronized with the flush of new foliage. This insect is
an important citrus pest throughout much of the citrus growing areas in the
old world. The lemon butterfly is rapidly colonizing new areas which
include Saudi Arabia, Pakistan, India, South East Asia, .China, Taiwan,
Parts of Australia, Pupua New Guinea and western Iran. In the Sudan
Papilio demodocus Esper is found everywhere, especially in Equatoria and
along the river Nile valley.
The present study was carried out at the laboratory and nursery of
the Department of Crop Protection during 2005/2006 in order to study the
biology, morphology of lemon butterfly, Papilio demodocus Esper. reared
on lemon leaves, and the food preference to three citrus speices
(Orange:Citrus sienensis, Lemon:Citrus limon, Grapefriut: Citrus paradise).
Labrotary investigations on the biology of the lemon butterfly
showed that the egg incubation period was 4.2 ± 0.42 days. There were five
larval instars with a mean duration of the larval period of 17.8±0.79 days.
The pupal period averaged
8.2 ± 0.42 days, with a total development
duration (life cycle) of 29 to 32 days; and a mean duration of 30.2 ± 1.03
days.
The morphological studies showed that the egg is small round in
shape with red mark on the top. The colour is bright yellow but it become
dark brown befor hatching. However, the larval colour ranged from black,
dark-brown, greenish and bright green. The pupa has naked shape, typical of
butterfly and there is no silken cocoon, the colour is brown. The adult is a
large-sized dark brown and cream chequer colour with blue eyes and red
spots on hind wings. and there is no tail on the hind wing.
Host plant preference tests showed that lemon was the most preferred
host followed by orange, and the least preferred host plant was grapefruit.
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APPENDIX
Appendix (1) Damage caused by the lemon butterfly fed on different
for 3 days
host plants
R1
R2
R3
Total
X
Grapefruit
4.87
3.62
5.5
13.99
4.66
Orange
8.81
2.93
7.25
18.99
6.33
Lemon
36.37
35.5
46.5
118.37
39.46
151.35
Total
Appendix (2) Damage caused by the lemon butterfly fed on different host plants for
6 days
R1
R2
R3
Total
X
Grapefruit
47.125
42.06
36
125.185
41.72
Orange
68.66
51
98.5
218.16
72.72
Lemon
83.66
85.83
114.16
283.65
94.55
Total
579.87
Appendix (3) Damage caused by the lemon butterfly fed on different host plants for
9 days
R1
R2
R3
Total
X
56.43
68
85.75
210.18
70.06
Orange
102
2.93
113
295.26
98.42
Lemon
126.08
35.5
124.16
373.9
124.63
Grapefruit
Total
879.34
ABBREVIATIONS WHICH APPEARED IN THE TEXT
C°
degree (s) Celsius centigrade.
Cm
centimeter (s).
Fig.
figure (s).
g
gram.
hrs.
hours.
mm
millimeter (s).
R.H
Relative humidity.
U.of K.
University of Khartoum.