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Analysis of the Territorial, Courtship and Coupling
Behavior of the Hemipterophagous Butterfly, Spalgis
epius (Westwood) (Lepidoptera: Lycaenidae)
Anegunda S. Dinesh &Melally G. Venkatesha
Revised: 7 May 2012 /Accepted: 21 May 2012 /
Published online: 31 May 2012
#Springer Science+Business Media, LLC 2012
Abstract In this study we examined the territorial, courtship and coupling behavior,
mating interruptions and influence of sunlight on mating behavior in Spalgis epius
(Westwood). We constructed an ethogram of territorial and courtship behavior, and
catalogued the sequence of behavioral acts associated with mating behavior. Mating
behavioral acts were divided into four repertoires i.e. pre-courtship, pre-coupling,
coupling and post-coupling behaviors. Totally 22 behavioral acts were recorded from
four repertoires. Tree canopy, canopy height and sunlight conditions are the important
factors that influence copulation in S. epius. The courtship activity led to successful
copulation in 71.9 % pairs. Incidence of different types of courtship and copula
interruptions in S. epius was also recorded.
Keywords Spalgis epius .territory .perching .courtship .mating .mealybugs
Introduction
Different butterfly species exhibit considerable diversity in the pattern of their mating
systems (Gilbert 1976; Wiklund 1977; Davies 1978). Generally males initiate sexual
behavior in several butterfly species and visually locate females (Magnus 1958;
Obara 1970; Hidaka and Yamashita 1975). Male butterflies adopt four main mate
locating strategies i.e. perching, patrolling, territorial defense, and lek assembly
(Shields 1967; Baker 1984; Scott 1974; Davies 1978; Rutowski 1991). Very little is
known about mate location sites and behavior in butterflies (Rutowski 1991). In
J Insect Behav (2013) 26:149–164
DOI 10.1007/s10905-012-9341-9
A. S. Dinesh :M. G. Venkatesha (*)
Insect Science Laboratory, Department of Zoology, Bangalore University, Bengaluru 560 056, India
e-mail: venkatmelally@gmail.com
perching butterflies initial approach is mainly based on visual stimuli particularly on
female movement and size, which is helpful to discriminate between same and
different species (Tinbergen 1941). Once a male butterfly locates a receptive conspe-
cific female, aerial or ground based courting behavior will follow depending on
species (Pinzari 2009). Investigations on mating behavior in many butterfly species
of different families including Lycaenidae have revealed that territorial behavior is
primarily a perching activity (Alcock 1983; Cordero and Soberon 1990; Fischer and
Fiedler 2001). A variety of courtship behavior has evolved in response to mate choice
by female butterflies to choose those males that show specific characteristics, which
enhance the reproductive success of females (Pinzari 2009). Studies on mating
behavior and copulation mechanisms are helpful to understand the evolution of
mating systems (Thornhill and Alcock 1983) and in Lepidoptera it is useful to
examine how ecological conditions curtail or promote sexual selection and the
evolution of different mating systems (Hughes et al. 2000). Moreover, to exploit
important entomophagous insects as biocontrol agents, knowledge of their mating
behavior is essential to plan an appropriate mass rearing program (van den Assem and
Povel 1973).
The apefly, Spalgis epius (Westwood) (Lepidoptera: Lycaenidae: Miletinae) has
been recorded as a predator of various species of mealybugs viz., Planococcus
virgatus (Cockerell), P. lilacinus (Cockerell), P. citri (Risso), Ferrisia virgata (Cock-
erell), Maconellicoccus hirsutus (Green) and Paracoccus marginatus Williams and
Granara de Willink (Hemiptera: Pseudococcidae); and scale insects Chloropulvinaria
polygonata (Cockerell.) (Hemiptera: Coccidae) and Dactylopius sp. (Hemiptera:
Dactylopiidae) (see Dinesh and Venkatesha 2011a). Moreover, S. epius has been
reported as a potential predator of P. citri, P. lilacinus and M. hirsutus in India
(Chacko et al. 1977; Gowda et al. 1996; Rahiman and Vijayalakshmi 1998; Venkatesha
and Shashikumar 2006). Dinesh and Venkatesha (2011a,b) have reported that S.
epius can be used as a major biocontrol agent of M. hirsutus and P. citri.
Spalgis epius occurs in India, Bangladesh, Burma, Sri Lanka, Philippines, Java,
Thailand and Krakatau Island (Indonesia) (see Dinesh and Venkatesha 2011a). The
morphology, life history and feeding potential of S. epius has been studied (De
Niceville 1890; Aitken 1894;Bingham1907; Vinod Kumar et al. 2006,2008a;
Dinesh et al. 2010; Thangamalar et al. 2010; Dinesh and Venkatesha 2011a,b).
Observations on the activities of S. epius and its interaction with ants have been made
in the field (Venkatesha et al. 2004; Venkatesha 2005; Vinod Kumar et al. 2008b).
Venkatesha and Dinesh (2011) developed the first mass rearing method for S. epius.
Very little is known about the courtship and mating behavior of S. epius (Dinesh et
al. 2010; Venkatesha and Dinesh 2011). Moreover, no information on the mating
behavior of any other carnivorous lycaenid species is available. Hence, we made
observations on the territorial, courtship and mating activities of S. epius both in
captivity and field. In this paper we present a detailed ethogram of mating behavior
including courtship and copula interruptions and influence of sunlight on mating in S.
epius. This study provides the first clear knowledge about the mating behavior of a
hemipterophagous butterfly species and it is useful for investigations on the biology
and rearing of other economically important carnivorous lycaenid species. Besides,
this study also helps to broaden our knowledge about mating behavioral patterns in
phytophagous and carnivorous lycaenids.
150 J Insect Behav (2013) 26:149–164
Materials and Methods
The study was carried out in the Bangalore University campus, Bengaluru, India
(Latitude 12° 58′N, longitude 77° 35′E, elevation 921 masl).
Lab Rearing of S. epius
To rear S. epius in the laboratory, its prey P. c i t r i was cultured on pumpkins
(Cucurbita maxima Duchesne) following the method of Serrano and Lapointe
(2002). Spalgis epius was reared on the mealybug infested pumpkins at 28 ± 1°C
and 65±5 % relative humidity as described by Dinesh et al. (2010). Spalgis epius
adults reared in the laboratory were utilized for conducting studies on courtship
behavior. Freshly eclosed adults were fed with water in the laboratory to enhance
their longevity (Dinesh et al. 2010).
The Ethogram of Mating Behavior
To make an ethogram of mating behavior of S. epius, observations were made in an
outdoor nylon tent cage (6 m length×6 m width× 10 m height) placed over a tree
(≈9 m height) in the field as followed by Venkatesha and Dinesh (2011). As S. epius
adults are known to mate a day after their pupal eclosion (Dinesh et al. 2010), for
each observation five to ten pairs of 1 day old S. epius adults reared in the laboratory
were released into the cage at 0700 h and their territorial, courtship and mating
behavior was observed during their active period (i.e. 0800–1700 h) till their death.
Based on the focal-animal observation method (Altmann 1974) behavioral acts and
duration of each act of males and females directly involved in mating were recorded
and described the sequences of acts. The sequence of mating behavior was described
using all-occurrences sampling method (Altmann 1974). Altogether randomly select-
ed 135 pairs were released into the cage for observations on courtship behavior. Close
observations on every courtship event in the cage was made from a plank platform
(6 m height), which was set up adjacent to the tree canopy as followed by Venkatesha
and Dinesh (2011). In addition to visual observations a video camera (Sony HDR-
XR150E, 25× optical zoom lens) was set up to record all details of focal-animal
courtship activities. Later, video and visual recordings were critically analyzed and
noted every details of courtship behavior. Duration of territorial and courtship flights
was recorded using a stop watch (Model-EC8071). To differentiate between male and
female butterflies during courtship observations, ventral side of both forewings of
males and females were marked with black and red marker ink (Reynolds, India ink),
respectively, before releasing them into the mating cage. Moreover, males and
females of S. epius can be differentiated based on shape of forewings (Dinesh et al.
2010). To distinguish different territorial males of S. epius during courtship observa-
tions, forewings of males were marked with black marker ink at selected spots.
Identity of resident or intruder males in a territory was confirmed by using a
binocular (Nikon 12x50) or zoom in picture of video recording based on the
position of ink markings on the forewing. Daytime ambient temperature within
the tree canopy in the cage was recorded by a digital thermometer (Temp.Tec:
Ao9Q32).
J Insect Behav (2013) 26:149–164 151
Mating Interruptions
The occurrence of courtship and copula interruptions in captivity was recorded.
Courtship Behavior in the Field
Five to ten pairs of 1 day old S. epius adults reared in the laboratory were released
each observation period on bushes/trees in the field and recorded their courtship
behavior. Totally 50 pairs were released in the field. In addition, observations were
made on courtship behavior of the field population of S. epius in a mealybug (P.
marginatus) infested papaya (Carica papaya L.) field in Bengaluru, where a high
incidence of S. epius was noticed.
Influence of Time and Daylight on Mating
To assess the peak mating time and successful mating under different daylight
conditions i.e., bright/diffused sunlight and overcast sky, five pairs of 1 day old S.
epius were released into the cage for 5 days under each of the above conditions. The
copulation time and number of pairs copulated under different daylight conditions
were recorded.
Data Analysis
To test the difference in the number of pairs copulating at different timings of the day
under different daylight conditions, one-way ANOVA was conducted and significant
difference was determined utilizing Tukey HSD test at P≤5 % (SPSS Inc. 2008).
Results
The Ethogram of Mating Behavior in Captivity
Male and female butterflies of S. epius were active 1 day after their pupal eclosion.
Behavioral acts associated with mating behavior in S. epius were divided into four
repertoires i.e. pre-courtship, pre-coupling, coupling and post-coupling behaviors.
The number of behavioral acts recorded under each repertoire was 6, 6, 5 and 5,
respectively (Table 1). Of the total 22 behavioral acts, 13 and two were performed
exclusively of male and female, respectively, and seven acts common to both sexes.
The male initiated entire process of mating through perching and marking in the tree
canopy at 6–9 m (Mean±SE: 7.5 ± 0.9) height from the ground and established a
territory (Fig. 1). A single territorial male marked 11.2±3.4 perch points in the
territory; distance between perch points was ≈20–25 cm. Spalgis epius males per-
formed territorial flights between 1100 and 1400 h. Males exhibited intense pre-
courtship flight activity in the canopy interspersed with short periods of basking.
Males spent most of their time in establishing territory, chasing intruder males and
courting females. Sometimes, a few S. epius males established territories simulta-
neously and strictly maintained a neutral space of 0.5–2 m between territories. In an
152 J Insect Behav (2013) 26:149–164
Table 1 Description of ethogram for behavioral acts involved in the territorial, courtship and mating of
Spalgis epius
Behavioral act Sex Description
Pre-courtship
Territory marking Male The male marks a territory in a tree canopy by dragging his
abdominal tip on the foliages of proximal end of the twigs.
Perching Male The male perches at some fixed points in a horizontal plane≈
within the radius of one meter (Fig. 1).
Inspection Male The male occasionally makes spontaneous short flights in a limited
range within the 2–3 m radius around the perch points in absence
of any conspecific individuals and frequently changes perch spots
within the marked territorial area.
Basking Male During perching activity the territorial male basks for
2–3 min by horizontally spreading both wings (Fig. 2a).
Chasing an intruder
by straight flight
Male Short flight wherein the territorial male chases a conspecific
intruder male in the territory in a horizontal plane without
any contest (Fig. 1).
Chasing an intruder
by circling flight
Male Long flight wherein the territorial male rushes towards a
conspecific intruder male in the territory and engages in an
ascending circling flight up to 1–1.5 m height from the
territory with 4-6 repeat bouts (Fig. 1).
Pre-coupling
Territorial flight Female The flying female enters the territory or the female sitting
in the territory starts flying (Fig. 2b).
Flight pursuit Male The territorial male engages in courtship flight almost immediately
after a flying female enters the territory (Fig. 2c).
Initiation of courtship
flight
Male The pair initiates courtship flight in a horizontal plane
above the tree branches and then fly through the canopy.
Female
Courtship flight Male During the courtship flight the male follows closely at ≈12–18 cm
behind, but slightly above the steadily flying female (Fig. 2d).
Female
Tracking Male The male follows the female constantly without losing the track till
the end of courtship flights.
Alighting on vegetation Male First the female alights suddenly on the foliage and soon after the
male alights at a distance of 4–8 cm behind the female (Fig. 2e).
Female
Coupling
Crawling Male The alighted male walks alongside the stationary female.
Abdomen raising Female The alighted female raises her abdomen.
Parallel position Male The male passes alongside until the couple in close parallel head to
head position (Fig. 2f).
Abdominal bending Male The male quickly bends his abdominal tip to establish contact with
the genitalia of the female (Fig. 2g).
Coupling Male The male pushes its bent abdominal tip against the raised
female genitalia and interlocks.
Post-coupling
Couple rotation Male After genital coupling the male moves laterally until both sexes face
opposite direction.
Couple abdomen raising Male Abdomens of the pair are held in slightly raised position
with their wings dorsally folded and heads pointing
downward all through the copulation (Fig. 2h).
Female
J Insect Behav (2013) 26:149–164 153
ascending circular territorial flight between residents and conspecific intruder males
(N015), resident males won and intruders were chased away. But, in short flight an
intruder male was chased away without contest (Table 1).
The sequence of successful courtship activities observed in S. epius is pre-
sented in Fig. 2. An active male attracted a virgin female within 23.8±7.8 min after
establishing a territory. The pair alighted after 1–4 rounds of courtship flights at an
interval of ≈4–5 min; each courtship flight last for about a minute. Sometimes pairs
made one or more alighting attempts before final settling. During courtship flight
males were very persistent and ceasing their activity only after females alighted.
Various courtship events and their duration in S. epius are presented in Fig. 3.
Duration of overall flight activity (i.e. perching and territorial activity, chasing an
intruder male, and courtship flight) of males was longer than that of females (see
Fig. 3).
In the final stage of courtship (N0104), 93.3 % (097) of S. epius males that
alighted behind females crawled to the left side of the females, then bent their
Table 1 (continued)
Behavioral act Sex Description
Pair in copula Male The coupled pair stays motionless and copulation lasts for
55.7± 9.6 min.
Female
Flight Male Only in the instance of any disturbances by predators (i.e.
ants or spiders)/strong wind the pair flies in copula to different
place in the canopy. If it rains the mating pair moves underside
the leaf without interrupting the copulation (n06).
Female
Copula termination Female Copulation terminated by slight movement of the female, thus
copula unplugs. Generally the separated pair remains in the
mating place for 15–20 min. If it is an ending stage of the day’s
activity then they stay in the mating place for 30–45 min.
Male
Fig. 1 Territorial activity of Spalgis epius male butterfly. Dark grey: medium to thick canopy, Light grey:
thin canopy, White: space in the canopy, Dashed circle: territorial area, Crosses: perch points in the
territory. Straight line: straight flight in chasing of an intruder, Curved line: ascending circling flights
between resident and intruder males
154 J Insect Behav (2013) 26:149–164
abdominal tip to the right and established contact with the female genitalia (Fig. 2f,
g). Only seven out of 104 males moved to the right of the females and in two of these
cases the males had trouble in establishing genital contact and the female ended flying
away. However, one of the two males in the second attempt quickly alighted on the
left side of the female and able to mate by bending its abdominal tip to its right side.
After genital coupling the male turns laterally until the pair reaches the tail-to-tail
position with slightly raised abdomens and dorsally folded wings (Fig. 2h). Coupling
is the longest phase of mating activity (see Fig. 3) and is characterized by the great
immobility of the couple at the mating site. Copulations constantly took place in the
canopy in the diffused sun shining area. Always copulation terminated by slight
movement of females. Totally 71.9 % (N0135) of pairs successfully copulated in
captivity.
All the time S. epius pairs initiated courtship strictly inside the territory (N0104),
but 36.5 % of copulations took place within an own territory, 46.2 % in a neutral
space between territories, 5.8 % in a general area and 11.5 % in others territory.
Whenever a courting pair landed directly in others territory and copulated immedi-
ately, the resident male never disturbed the copulating pair. But, in two instances after
the pair detached, a resident male tried to court the mated female, which was strictly
unreceptive.
Fig. 2 Sequence of acts of successful courtship and mating in Spalgis epius.aperching male in the
territory, bresting female in the tree canopy, cflying female in the territory, dcourtship flight of a pair, e
courted pair alighting on the vegetation, fcrawling male in parallel position with the courted female, g
copula joining (dorsal view), and hpair in copula
J Insect Behav (2013) 26:149–164 155
Courtship Interruptions
A total of 128 courtship interruptions were recorded in S. epius in captive mating.
Wherein mainly five types of interruptions were observed: 1) multiple males courting
a single female- 33.6 % mating interruptions were because of multiple males trying to
court a single female. When many males were active in the cage they marked their
territory in close proximity to each other within the confined area. Soon after a female
entered the territory she was courted by the territorial male. Whenever the courting
pair got into others territory and continued their courtship flight, the resident male
suddenly followed the courting pair and when the courting female alighted on the
foliage, two competing males attempted to copulate the female, which flew away
under such circumstances. Any time a single female was courted by more than one
male, the courtship led to unsuccessful copulation. Although at times multiple males
courted a single female, 3.9 % of males that courted continuously without losing the
track of the female till the end led to successful copulation; 2) the male fails to locate
the female- 28.1 % of males courted the females till the end of the courtship flight and
finally when the receptive female quickly alighted on the foliage the courting male
was unable to locate the female; 3) losing the track of females- 18.0 % of courting
males lost the track of erratically flying females during courtship flight in the tree
canopy; 4) strong wind- strong wind disturbed the courtship flights and 7.0 % of
couples were unsuccessful in mating; and 5) obstacle- 13.3 % of courtship flights
Fig. 3 Courtship and mating behaviors showing various events and their duration in Spalgis epius. tt: tail
to tail
156 J Insect Behav (2013) 26:149–164
were interrupted when courting couples had hit the wall of the mating cage and lost
courtship momentum.
Copula Interruption
After the successful union of 103 pairs of S. epius, only 5.8 % (06) of copula
interruptions were observed. In which 2.9 % pairs detached from their copula within
two minutes after copulation. In 1.9 % of courtship flights, both male and female
butterflies alighted on a leaf and then the male with difficulty made contact with the
unnaturally raised female genitalia, but the female detached from him and flew away.
In 1.0 % of copulations, 12 min after union the female began dragging the male
behind her and even she made small flights while dragging him. When the male was
still motionless, the female began twisting her body while dragging and in the process
the male was hanging in copula, and finally the pair got detached.
Courtship and Mating Behavior in the Field
When S. epius pairs were released in the field, they flew short distances and sat on the
tree foliages. Generally we could not track all the field released S. epius adults as they
flew away and lost in the sylvan. Hence, courtship and mating was observed only in
six pairs of the 50 pairs released on different days in the field. Although courting pairs
of S. epius were observed many times in the papaya field, mating was observed only
in four pairs on different days. The territorial, courtship and mating behavior of the
field released S. epius adults or in the natural population of S. epius in the papaya
field was similar to that observed in the captivity. But, the territory height range was
6–15 m from the ground in the field. Moreover, the ascending circling flight between
resident and intruder males was ≈4–6 m height from the territory.
Influence of Time and Sunlight on Mating
Under bright sunlight, the maximum number of pairs copulated between 11.00 and
12.00 h, though it was not significantly different from that mated between 10.00 and
11.00 h (Tukey HSD test: P00.115). However, these were significantly higher than
those (F
3, 16
017.939; P<0.05) mated during 12.00–13.00 and 13.00–14.00 h
(Fig. 4). In diffused sunlight, the pairs never mated between 10.00 and 11.00 h.
But, more pairs mated between 12.00 and 13.00 h than between 11.00 and 12.00 and ,
13.00 and 14.00 h and it was significantly different (F
3, 16
021.030; P<0.05).
Similarly, the pairs never mated between 10.00 and 11.00 h under overcast sky.
Although the pairs mated in subsequent hours, a few pairs mated between 11.00 and
12.00 h and, it was significantly lower than the pairs mated between 12.00 and 13.00
and 13.00 and 14.00 h (F
3, 16
07.704; P<0.05). Overall, the maximum numbers of
pairs mated under bright sunlight, but it was not significantly different from that
mated under diffused sunlight. However, number of pairs mated under bright/diffused
light was significantly higher than that mated under overcast sky (F
2, 57
08.453; P<
0.05) (Fig. 5). Spalgis epius mated in the temperature range of 26–34°C under bright/
diffused daylight in the cage. But, whenever temperature increased above 36°C in the
hot season, S. epius very rarely mated in the cage.
J Insect Behav (2013) 26:149–164 157
Discussion
Spalgis epius males performed more behavioral acts than females (see Table 1). In most
butterfly species it is the male who actively seeks mates, and females are less active
Fig. 4 Influence of sunlight on
Spalgis epius mating during dif-
ferent hours of the day. abright
sunlight, bdiffused sunlight, c
overcast sky. Values are mean±
SE; Bars with different letters
indicate the significant difference
between the hours within the
same daylight condition at P<
0.05 (one way ANOVA –Tukey
HSD test)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
Bright Diffused Overcast
Sunli
g
ht condition
Mean number of copulation
aa
b
Fig. 5 Influence of different sunlight conditions on Spalgis epius mating. Values are mean±SE; Bars with
different letters indicate the significant difference between different lighting condition at P<0.05 (one way
ANOVA –Tukey HSD test)
158 J Insect Behav (2013) 26:149–164
than males (Scott 1972; Rutowski 1984). The pre-courtship behavior of S. epius (i.e.
territorial marking and perching at fixed points) is similar to other phytophagous
lycaenids viz., Atlides halesus (Cramer) (Alcock 1983), Callophrys xami (Reakirt)
(Cordero 1993), Favonius taxila Bremer (Takeuchi and Imafuku 2005a), and Chrys-
ozephyrus smaragdinus Bremer (Takeuchi and Imafuku 2005b). The spontaneous
flight of S. epius territorial male in the territory may provide inspection of the territory
as reported in Lycaena hippothoe (Linnaeus) (Fischer and Fiedler 2001), F. taxila
(Takeuchi and Imafuku 2005a), and C. smaragdinus (Takeuchi and Imafuku 2005b).
More number of S. epius butterflies was able to mate in the cage. It may be because of
butterflies that adopt perching in the territories are known to have higher mating
success than patrolling ones (Wickman 1986).
Generally in butterfly species with more number of males than females perform
perching, territorial defense and lek assembly activities (Ehrlich 1984). However, in S.
epius though males perform perching and territorial defense, their number is always
lower than that of females (Vinod Kumar et al. 2006; Dinesh et al. 2010). Basking
behavior observed in S. epius territorial males during territorial flights is also reported
in other lycaenids e.g., Incisalia iroides (Boisduval) (Powell 1968), C. smaragdinus
(Takeuchi and Imafuku 2005b) and F. taxila (Takeuchi and Imafuku 2005a). Basking
behavior of territorial male butterflies is to regulate their body temperature as they
require high thoracic temperature in order to perform flight activities (Clench 1966;
Pivnick and Mcneil 1986). Moreover, Stutt and Willmer (1998) reported that resi-
dents can achieve a higher body temperature by basking in a territory, which enhances
their physical condition, and are therefore more likely to win a contest with an
intruder. Similar behavior was observed in S. epius. Likewise, resident males of
Pararge aegeria (Linnaeus) are almost always known to win (Davies 1978; Wickman
and Wiklund 1983). Takeuchi and Honda (2009) reported that real fighting ability is
correlated with ownership status. Furthermore, as butterflies are ectotherms, owners
win because they are able to rise their body temperature to optimum levels by basking
in a territory, whereas intruder males are not (Stutt and Willmer 1998). The two types
of chasing flights between territorial and intruder males of S. epius are also observed
in a lycaenid Eumaeus toxea Godart (Martinez-Lendech et al. 2007). The circling
ascending flight between resident and intruder males of S. epius is similar to that of A.
halesus (Alcock 1983), Strymon melinus Hübner (Alcock and O’Neill 1986), C. xami
(Cordero 1993) and C. smaragdinus (Takeuchi and Imafuku 2005b). The circling
flights of territorial and intruder males of S. epius were initiated within a territory, and
invariably terminated outside the territory as observed with L. hippothoe (Fischer and
Fiedler 2001) and F. taxila (Takeuchi and Imafuku 2005a). Contest between individ-
ual males for mating opportunities is a widespread phenomenon and constitutes an
important factor of Darwin’s(1871) theory of sexual selection. Spalgis epius territo-
rial males maintained neutral spaces between territories as observed in various
butterfly species (Knapton 1985).
The initiation of courtship flight followed by approaching only a flying female by
a territorial male including entire courtship behavior in S. epius is similar to that of C.
xami (Cordero 1993)andC. smaragdinus (Takeuchi and Imafuku 2005b). This
indicates that visual signal plays an important role in S. epius courtship behavior as
observed in several species of butterflies (Lutz 2002; Jiggins et al. 2004; Oliver et al.
2009). Therefore, when a courting pair of S. epius gets into others territory the
J Insect Behav (2013) 26:149–164 159
resident male joins the courting pair. But, if a courting pair lands directly in others
territory and copulate immediately, the resident male never disturbs the pair in copula.
However, we are not sure whether only visual signal or male pheromone or both are
involved in attraction of a female to the male territory in S. epius. The alighting and
copulating behavior of S. epius is similar to that of C. xami (Cordero 1993) and C.
smaragdinus (Takeuchi and Imafuku 2005b). The successful copulation of S. epius
males by bending abdominal tip to their right side is not reported so far in any other
species. Furthermore, it is not known why an S. epius male struggles to bend its
abdominal tip to the left when it rarely crawls to the right side of the female. As far as
we know our description of genital coupling behavior of males from the right or left
side of the female in S. epius is the first record of occurrence of this type of behavior
in any species of lycaenids in particular and other butterfly families in general. This
behavior seems to be crucial for the copulatory success of S. epius males because
when a male struggles to establish genital contact from the right side of the female,
she flies away.
As S. epius is a shy butterfly and hide in bushes (Venkatesha et al. 2004), its
courtship and mating activities are not commonly observed in the field. However, our
observations on the mating behavior of S. epius in the field have revealed that it is
almost similar to that in the confined condition. As we could observe courtship
activity in a few individual pairs of S. epius in the field, information on neutral
spaces including several other courtship events could not be recorded. The courtship
and mating activity of S. epius in the field may purely depends on the availability of
hemipteran host insects as the predator pupates on the hemipteran infested
bushes/trees and this short lived species (Dinesh et al. 2010) may mate in the
same place. However, if the host infestation in the field is on the very small bushes,
S. epius adults may fly to a different place to find a tree canopy as they mate at a
moderate height from the ground level. In phytophagous butterflies conditions like
the occurrence of larval host plants, temperature and heat, adult nectar resources, and
geography will increase the density of individuals and enhance encounter rates
between sexes (Dennis and Shreeve 1988). The same may be true in hemipteropha-
gous S. epius.
Several courtship interruptions in S. epius were because of multiple males courted
a single female in the cage. Whenever more numbers of S. epius pairs were present in
the cage the incidence of competition among males was more in a restricted space.
However, this condition was not observed in natural condition. When swift alighting
of a receptive S. epius female on the leaf coincided with a flying intruder male diverts
the concentration of the courting male that is unable to track the female. Strong wind
or some physical obstacles interrupted the courtship in S. epius as observed with C.
xami (Cordero 1993). Copulation of S. epius in the partly sun shining area in the
canopy may prevent harmful overheating or attack of visually oriented predators as
reported in the butterfly Dryas iulia alcionea F. (Mega and de Araujo 2010). In case
of disturbance from rain or predators, it is always females of S. epius in copula that
drag males to some other safe location.
Some pairs of S. epius separated within a few minutes after interlocking as
reported by Cordero (1993)inC. xami. Generally copula interruption occurs quickly
owing to rapid assessment of mate quality as physical separation may be difficult if
copulation is prolonged (Wickman 1985). Furthermore, copula interruptions in C.
160 J Insect Behav (2013) 26:149–164
xami were due to mate choice after mating began (Cordero 1993). Females or males
may be able to evaluate their mating partners after copulation begins and decide to
interrupt it within a few minutes (Eberhard 1985,1994; Eberhard and Cordero 1995;
Cordero 1995).
The high incidence of mating under bright sunlight in butterflies is because of their
ability to absorb heat from the sunlight through their wings (Watt 1968) and the behavior
of ectothermic insects is constrained by ambient thermal conditions (Heinrich 1996).
Sunlight is crucial for flight behavior in butterflies since the performance of thoracic
flight muscle is dependent on the thoracic temperature, which in turn depends on the
ambient thermal conditions (Watt 1969; Kammer 1970; Rawlins 1980). Hence, under
bright/diffused sunlight S. epius males were active and marked the territory, under-
took territorial flights as well as chasing flights with intruder males and located active
females and had more copulations. Hence, the delayed mating activity in S. epius
under diffused and overcast conditions may be due to prolonged exposure to light to
rise their body temperature for courtship activities. Most pairs of S. epius mated under
bright/diffused sunlight than under overcast sky as observed in the lycaenid butterfly
Heodes virgaureae (L.) (Douwes 1976). However, S. epius pairs rarely mated under
rising temperature during summer period. This could be one of the reasons for low
population of S. epius during summer months as reported by Venkatesha and Sha-
shikumar (2006) and Vinod Kumar et al. (2006). Initiation of copulation separation
by S. epius females suggests that the duration of sperm transfer is determined by the
female as noticed in C. xami (Cordero 1993) and in some other species of butterflies
(Scott 1972) and several species of moths (Phelan and Baker 1990). However, in
several species of butterflies, it is males that determine the end of copulation
(Wickman 1985).
Much work is still to be done to explain the role of visual and chemical
signaling in courtship activity and male coupling behavior in S. epius. Yet, we
hope our study provides the first detail ethogram of the territorial, courtship and
mating behavior of a hemipterophagous butterfly. It is evident that under captivity S.
epius adults should be provided primarily a tree canopy for perching and territorial
activities, then a wide space, more height from the ground level and bright light for
successful mating. Although a number of mating behavioral acts in S. epius are
similar to those of some phytophagous lycaenids, the importance of vital conditions
i.e. tree canopy, canopy height from the ground level, space and daylight conditions
essential for mating in S. epius is not reported in other species. In the field, S. epius
mate location is mainly dependent on the availability of resources i.e. density of
hemipteran infestation, occurrence of tree canopy, and bright daylight. This vital
information can be utilized in mass rearing of S. epius in captivity as well as its
conservation in the field to exploit the predator as a major biocontrol agent for
mealybugs and other hemipteran pests. Furthermore, this investigation may be useful
to induce mating in captivity for rearing of any carnivorous and phytophagous
lycaenids.
Acknowledgements The second author acknowledges the financial assistance [F. No.33-344/2007 (SR)]
from the University Grants Commission (UGC), New Delhi, India to carry out the above work. The first
author is grateful to the Council of Scientific and Industrial Research (CSIR), New Delhi, for the award of
Senior Research Fellowship.
J Insect Behav (2013) 26:149–164 161
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