Journal of
Threatened Taxa | www.threatenedtaxa.org | 26 August 2018 | 10(9): 12203–12209
Breeding behaviour of the Coromandel Damselfly Ceriagrion
coromandelianum (Fabricius) (Zygoptera:
Coenagrionidae) in central India: copulation
Nilesh R. Thaokar
1, Payal R. Verma
2 & Raymond J. Andrew 3
1,2,3 Centre for Higher Learning and Research in
Zoology, Hislop College, Civil lines, Nagpur,
Maharashtra 440001, India
1nilesh.thavkar@gmail.com, 2payalrverma@gmail.com,
3rajuandrew@yahoo.com (corresponding author)
doi: https://doi.org/10.11609/jott.3529.10.9.12203-12209
Editor: K.A.
Subramanian, Zoological Survey of India, Chennai, India. Date
of publication: 26 August 2018 (online & print)
Manuscript details: Ms
# 3529 | Received 31 May 2017 | Final received 13 July 2018 | Finally accepted
20 July 2018
Citation: Thaokar, N.R., P.R. Verma & R. J. Andrew (2018). Breeding
behaviour of the Coromandel Damselfly Ceriagrion
coromandelianum (Fabricius)
(Zygoptera: Coenagrionidae)
in central India: copulation.. Journal
of Threatened Taxa 10(9): 12203–12209; https://doi.org/10.11609/jott.3529.10.912203-12209
Copyright: © Thaokar et al. 2018.
Creative Commons Attribution 4.0 International License.
JoTT allows unrestricted use of this article in any
medium, reproduction and distribution by providing adequate credit to the
authors and the source of publication.
Funding: Self-funded.
Competing interests: The authors declare no competing interests.
Author
Details: Dr.
R.J. Andrew has been studying various
physiological, morphological, ethological and ecological aspects of dragonflies
of central India for the last 30 years and has more than 90 research papers to
his credit. He serves as the Director of the P.G. Dept. of Zoology, and Vice
Principal, Hislop College, Nagpur. He has published
two books on Odonates and has organized one
International, two South Asian, five National and two State level Symposia. Dr. Payal R. Verma is actively engaged in Research in the area of
Odonatology. She has completed her PhD from Rashtrasant Tukadoji Maharaj Nagpur University, and currently is an Adhoc lecturer at the Post Graduate Department of Zoology.
She has published 11 papers in national and two papers in international
journals. Dr. Nilesh
R. Thaokar completed his PhD from Nagpur
University and is presently teaching at the Post Graduate Department of Zoology
as an Adhoc lecturer. He has published 10 papers in
national and two papers in international journals.
Authors
Contribution: Nilesh R. Thaokar and Payal R. Verma contributed in field work and documentation of the oviposition
behaviour.
Raymond J. Andrew set up the project and evaluated the findings.
Acknowledgements: We thank the Principal Dr. Ms.
D.R. Christian and Management of Hislop College,
Nagpur for providing us laboratory facilities.
Abstract: The Coromandel Damselfly Ceriagrion coromandelianum can be easily identified because of its bright yellow abdomen,
greenish thorax and eyes. In females,
the abdomen is darker with light brown colouration
extending to dark brown towards the terminal end. The documentation of the reproductive behaviour of Ceriagrion
coromandelianum was carried out at the botanical
garden of Hislop College, Nagpur, India. The males of C. coromandelianum
arrive early in the morning by 07:00hr at the ovipositing
site. They belong to “sit and wait” type
of mate-location. While perched and
waiting for the female to arrive they at times exhibit abdominal bobbing, and oviposition posture.
The territorial area of male C. coromandelianum
is very small, within a range of about 45cm around his perch. There is no precopulatory
courtship display and the male move toward the arriving receptive female and
directly tries to form a tandem link.
The other males of the group follow the pair. The tandem pair flies towards the safety of
the surrounding vegetation to copulate. Before copulation, the male fills his
penis vesicle with sperm material by the process of “intra male sperm
translocation” which lasts for 30±8 seconds.
The female curves her abdomen ventrally forward so that her gonopore which
is located between the eighth and ninth sternite
comes to lie before the secondary copulatory
apparatus of the male and forms a strong genital link, to form the copulatory wheel.
The copulation duration can be long (34–55 min) or short (12–15
min). Two stages of copulation depending
upon the pumping movement of the couple can be differentiated. During the first stage, the male rhythmically
and forcefully depresses and stretches the first two abdominal segments,
vigorously pumping the penis inside the female vagina which
accounts for 72% of the copulation duration.
The second stage starts with rapid short thrusting movement
which are not forceful but exhibit shallow movements of the first two
abdominal segment of the male. The
tandem pairs after copulation may directly move for oviposition
or settle around the surrounding foliage and exhibit “post-copulatory
resting” (PCR) behaviour. It is noted that 23.3% females immediately
commence oviposition, 53.4% exhibit brief, while
23.3% display prolonged PCR behaviour.
Keywords: Intra male sperm
translocation, mate-location, post-copulatory
resting.
INTRODUCTION
In Odonata, the mating system has the following components—encounter,
recognition, copulation, sperm transfer and oviposition. The encounter for a majority of odonates is near the oviposition
site and is therefore the water body (Waage
1984). Encounter leads to territoriality
and aggressive interaction between males. Recognition of sex and species is
based predominantly on visual signals (Mokrushov
& Frantsevich 1976). In many odonates
the phenomena of male courtship follows recognition during which the female can
exhibit “refusal display” to unwelcome approaches by male. Courtship leads to pre-copulatory
tandem formation where the male grasps the female’s thorax and head with his
anal appendages. Intra-male sperm
translocation generally occurs during tandem and is followed by copulation. Copulation is achieved by the “wheel”
formation where the female’s genital aperture is secured to the male’s
secondary genitalia. Copulation in Odonata is unique among pterygote
insects since the primary genitalia of the two sexes do not meet during sperm
transfer (Carle 1982; Matsuda 1976).
Sperm competition occurs widely among insects and the discovery that the
odonate penis both inseminates the female and
displaces rival sperm (Waage 1986) has indeed proved
to be an invaluable aid in interpreting odonate
reproductive behaviour (Corbet 1999). Sperm competition as found in Odonata benefits the female by reducing their energy
expenditure, lowering risk of harassment from conspecific males and predators,
survival of genetic diversity of progeny and fertility backup.
MATERIAL AND
METHOD
The
documentation of the reproductive behaviour of Ceriagrion
coromandelianum was carried out at the botanical
garden of Hislop College, Nagpur, (21.1660N
& 79.0330E) where small underground cement tubs are used to grow
macrophytes.
The garden houses aquatic plants in a large circular tub surrounded by
six smaller circular tubs followed by a row of three rectangular cement
containers. These tubs contain free floating Nymphaea nouchali, Lemna paucicostata and submerged Hydrilla
verticillata.
The tubs are surrounded by grasses and bushes of
flowering plants (Mussaenda laxa, Chrozophora sp., Catharanthus roseus, Phyllanthus amarus, Ageratum conyzoides, Bougainvillea sp.) (Images 1 a,b). Post-noon this area is in shadow of the
college building. Adult C. coromandelianum are found almost all round the year
breeding in these water-bodies.
To
study the reproductive behaviour of C. coromandelianum,
field observations were carried out mostly during the months of August to
November and March to May from 2008–2013.
These observations were carried out in the morning and/or afternoon and
the reproductive behaviour was documented, noted and/or photographed,
videotaped while the duration of different behaviour was timed with a stop-watch.
RESULTS
On a
typical breeding day, the males of C. coromandelianum
arrive early in the morning by 7am and move between the bushes and grasses
around the ovipositing site (water tubs). Within an hour, they can be spotted perched
all around the bushes surrounding the water-body. The male belong to “sit and wait” type of
mate-location. They occupy a base perch which is about 10–60 cm above the ground and not more
than 120cm away from the water tubs. The
base perch is commonly a floating/emerging water plant or any other object on
water or shrubs and grasses bordering the water-body. While perched and waiting for the female to
arrive, they at times exhibit two peculiar behaviors. The first is “abdominal bobbing” when a wave
of motion passes from the first to the last abdominal segment while the second
is copying the “oviposition posture of the female”
when the male bends the abdomen down along the fourth-fifth segment (Image 2 a,b).
Territoriality
The territorial area is determined by the range of distance beyond which
the resident territorial male does not respond to an intruder. The territorial area of male C. coromandelianum is very small. It gets disturbed only if an intruder comes
within a range of about 45cm near his perch.
Many a times, two to three males can be seen perched within a vicinity
of 120cm.
Whenever
an intruder (conspecific or heterospecific male or
any other insect) enters his territory, the resident male flies behind the
intruder, follows it up to around 600cm and chasing it away. The male returns to his territory either at
the same base perch or a few inches around it.
If the intruder persists in his territory, then the resident male moves
to a new perch about 70–120 cm away but returns as soon as the intruder
leaves. If the intruder (generally a
conspecific male) is persistent, he chases the resident male away from the ovipositing site into the surrounding bushes. The male later moves to a new location around
the water-body. The territorial male
also undertakes small patrolling flights.
This flight is of not more than 500cm from his perch. The female arrives
from 07:30hr onwards (upto noon) when most of the
male have demarcated their territory.
Precopulatory behaviour
The
males move toward the arriving receptive female when she is at a distance of
70cm from the water body. The males follow the female and directly try to form
a tandem link. This link is also formed
when the female has entered the oviposition site and
is settled on a low lying bush. There is no precopulatory
courtship display. It is a common site to find 2–3 males following a female to
form a link. Although there is no
visible fight amongst the males, the quickest male holds the female just below
the head with his anal appendages and forms the tandem linkage. The other males of the group follow the pair
but do not try to physically dislodge the male.
Once the link is formed, the remaining males may follow the pair keeping
a distance of 6–12 cm. The tandem pair
moves away from the water-body and flies towards the safety of the surrounding
vegetation where they form the copulatory wheel. Before forming the copulatory
wheel, the male charges his penis with sperm material by the process of “intra
male sperm translocation”.
Intra male sperm translocation
The
male transfers the sperm material from the sperm sac which is
located in the ninth abdominal segment to the penis of the secondary copulatory apparatus located on the second abdominal
segment. The male gonopore
and paired coxites of the primary genitalia located
on ninth abdominal sternum and penis vesicle of the secondary copulatory apparatus play a key role during this process of
intra male sperm translocation (IMST).
During this translocation, the position of the male is precarious, since
it has to grip the substrate with his legs, hold the female with his terminal
anal appendages and curve and bend the abdomen to bring the gonopore
in contact with the penis vesicle with the female suspended vertically. The female hangs passively with folded wings
and the abdomen is either straight or slightly curved inwards. IMST in C. coromandelianum
lasts for 30+8 seconds (N=28). During
this translocation, the male’s gonopore pumps sperm
material in the penis vesicle which acts as a sperm
reservoir during copulation.
Copulatory wheel
After
IMST, the female curves the abdomen ventrally forward so that her gonopore which
is located between the eighth and ninth sternite
comes to lie before the secondary copulatory
apparatus of the male and forms a strong genital link, in the form of a copulatory wheel.
The wheel is always formed when the male is holding a supporting
substrate and never in flight.
Copulation takes place within 5m around the oviposition
site and not more than 500cm above ground level. Copulation lasts for 29.3±4 m (N=10, Max - 55
min: Min - 12 min, SD - 14.93).
Copulation
Copulation
of C. coromandelianum is initiated when the
male starts pumping the penis inside the female’s vagina. Two types of pumping movement can be
differentiated (which can be observed from a distance) by recording the
variation in the periodic movements of the first two abdominal segments of the
male, the change in the shape of the copulatory wheel
and the pressure exerted on the head of the female by the anal appendages of
the male.
During
the first stage, i.e., stage I, the male rhythmically and forcefully depresses
and stretches the first two abdominal segments, vigorously pumping the penis
inside the female genitalia. At this
stage, there is a rapid and energetic movement of the male’s abdomen
which in turn exerts heavy pressure on the females head held by the anal
appendages. The female’s head generally
wobbles with every thrusting movement.
This movement is interspaced with very short (<14 seconds) resting
periods when there is no movement of the abdomen. This stage lasts for 21.5±3 min (N = 10, Max
- 34 min: Min- 8
min, SD - 9.62) and covers 72% of the copulation duration.
The
Stage II starts with rapid short thrusting movement which are
not forceful as found in Stage I.
Along with the rhythmic but shallow movements of the first two abdominal
segment of the male, the third abdominal segment too exhibits periodic
synchronised movements. The abdomen of male exhibit angular bending along the fourth-
seventh abdominal segment. The
frequency of movements decrease until all movements stop and the couple is
immobile. This is
followed by the breaking of the copulatory wheel,
when the female extricates her genitalia from the secondary copulatory
apparatus of the male. This stage lasts
for 8.3±2 min (N = 10, Max - 21 min: Min. - 1 min, SD - 6.36). The duration of Stage I is always greater
than Stage II (Image 3a–d; Table 1; Fig. 1).
The copulation duration can be long (34–55
min) or short (12–15 min) distinctly divided into division. The long copulation which clocks between 55 to 34 minutes and short
copulation which completes between 15 to 12 minutes (Fig. 2)
Post copulatory resting behaviour
The
tandem pairs after copulation may directly move for oviposition
or settle around the surrounding foliage and exhibit “post-copulatory
resting” (PCR) behavior (Image 4 a,b,c). After
monitoring and timing the PCR behavior of 30 pairs,
it is found that PCR can be divided into three types. In Type-1, the pair directly moves for oviposition immediately after copulation. In Type-2, the PCR is brief (208±90 sec) and
in Type-3 the PCR is prolonged (619±11 sec).
Post copulation, 23.3% females immediately commence
oviposition, 53.4% exhibit brief, while 23.3% display
prolonged PCR behavior (Table 2, Fig. 3).
DISCUSSION
Habitat
selection based on the oviposition site is practiced
by females and by males of many species of Odonata
for which the oviposition site, that is mostly a
water-body, forms the focus for reproductive activity (Corbet
1999). The choice of
such sites mostly depend upon the plant community present in and around
the water-body and therefore a link between the odonate
and composition and structure of vegetation is evident in most odonates (Buchwald 1991).
Ceriagrion coromandelianum
is one of the most common damselflies from the Indian sub-continent found
around banks of large and small perennial and weedy ponds and lakes and small
garden tanks or any shallow water body with profuse growth of vegetation with
floating and/or submerged vegetation (Fraser 1933; Andrew et al. 2008). C. coromandelianum
is found breeding year around in the small tanks and tubs of the college
botanical garden used for the propagation of aquatic macrophytes
(Nymphaea nouchali,
Hydrilla verticillata,
Lemna paucicostata). These plants are used as substrate for egg
deposition by this endophytic species. In a few odonate
species, copulation occurs away from the oviposition
site during roosting and foraging (Fincke 1987;
Miller 1987a).
In Odonata, territoriality is functionally related to site
attachment and aggressive behaviour to protect the territory. The area defended by a territorial male in Odonata varies from 1800m (Hemianax
papuensis) to 0.2m (Copera
marginipes) (Furtado 1974; Rowe 1987). Prasad (1990) and Sharma (2009) observed that
the male of C. coromandelianum selects a small
oval/circular territory (40–80 cm radius) and defends this area against any
intrusion by other males by abdominal raising display (threat display) but Srivastava & Babu (1985)
found lack of territoriality in this species.
In the present investigation, it is found that the territoriality area
of C. coromandelianum is small (Max -
45cm radius) but not a single case of threat display was
detected. The “sit and wait” type search mode behaviour of male as found in C.
coromandelianum is also found in the damselfly Ceriagrion melanurum
(Mizuta 1988) Enallagma nigridorsum
(Samway 1994) and the gomphid,
Onychogomphus forcipatus
unguiculatus (Miller & Miller 1985). The male odonate
may seize the female while she is flying or perched and often while she is ovipositing. C. coromandelianum always seize
the female in flight and never when she is perched or ovipositing. Pantala flavescens executes tandem formation and wheel
formation always in flight followed by oviposition
(R.J. Andrew pers. obs. 2010–2017), while some odonates
form the wheel in air and then perch to complete copulation (Sakagami et al. 1974; Miller & Miller 1989). In C. coromandelianum
wheel formation is achieved in perched condition. According to Corbet
(1999) long bodied odonates will always perch for
copulation.
Copulation
in most zygopteran species is divided into two to
three stages. The first stage, i.e.
Stage I can cover upto 95% of the total duration (Nososticta kalumburu
Thompson, 1990) while in C. coromandelianum it
covers 72%. In Enallagma
cyathigerum the Stage II and Stage III is brief
whereas in C. coromandelianum the Stage II and
Stage III cannot be differentiated as reported in many other zygopterans (Cordero & Miller 1992; Tajima &
Watanabe 2014). During Stage I the penis
removes the pre-deposited sperm of previous mating from the sperm storage organ
of the female and during Stage II the now empty sperm storage organs are
inseminated (Waage 1982, 1984, 1986, 1988; Miller 1987a,b; Corbet
1999; Andrew 2001; Cordero-Rivera et al. 2004; Cordoba-Aguilar 2010; Tajima
& Watanabe 2014). During the present
investigation it is found that in C. coromandelianum
the copulation duration is divided into short copulation
which completes between 12–15 minutes and long copulation of 34–55
minutes. The probable reason for this
variation is the condition of female.
While copulating with virgin females and/or females with a smaller
amount of sperm in their storage organs the male needs less time to displace
sperm and therefore the Stage I gets over quickly which reduces the copulation
duration.
In Odonata,
more than 50 species exhibit post copulatory resting
(PCR) behaviour, which in damselflies can fluctuate
from 01 (Calopteryx maculata
Meek & Herman, 1990) to 180 minutes (Argia
vivida, Conrad & Pritchard 1988). Srivastava & Babu (1985) reported that PCR by C. coromandelianum
is for 50–60 seconds followed by post copulatory
flights in tandem for 54–90 minutes; such short post copulatory
flights were not recorded in the present study.
Prasad (1990) and Sharma (2009) observed that PCR occurs for about six
minutes in this species. In the present
study it is found that C. coromandelianum PCR
is clearly differentiated into two categories, the brief PCR ranges from
136–253 seconds while the prolonged one from 577–652 seconds. Disturbance during copulation, temperature
and sunlight are few factors that may increase the duration of PCR, but in the
present study no specific relationship between these factors and the duration
of PCR is noticed. As postulated by
Miller & Miller (1989) “sperm handling” appears to be the only feasible
reason for PCR in C. coromandelianum. Perhaps it implies that there is variation in
the PCR of virgin and non-virgin females or maybe, long copulation leads to
prolonged PCR as found in Orthetrum caledonicum (Alcock 1988).
Table 1. Duration (in minutes) of
copulation observed in 10 pairs of Ceriagrion
coromandelianum.
|
1 |
2 |
3 |
4 |
5 |
6 |
7 |
8 |
9 |
10 |
Total |
Mean |
SD |
SE |
Stage I |
34 |
34 |
25 |
25 |
27 |
22 |
12 |
12 |
13 |
8 |
215 |
21.5 |
9.62 |
3.21 |
Stage II |
21 |
7 |
15 |
10 |
8 |
12 |
3 |
2 |
1 |
4 |
83 |
8.3 |
6.36 |
2.12 |
Total |
55 |
41 |
40 |
37 |
36 |
34 |
15 |
14 |
14 |
12 |
298 |
29.3 |
14.93 |
4.97 |
Table 2. Ceriagrion coromandelianum post copulation. Duration (in
seconds) of post copulatory
resting behavior.
Sno |
PCR |
Sno |
PCR |
Sno |
PCR |
1 |
0 |
11 |
184 |
21 |
249 |
2 |
0 |
12 |
185 |
22 |
253 |
3 |
0 |
13 |
187 |
23 |
253 |
4 |
0 |
14 |
196 |
24 |
577 |
5 |
0 |
15 |
208 |
25 |
590 |
6 |
0 |
16 |
221 |
26 |
602 |
7 |
34 |
17 |
226 |
27 |
628 |
8 |
136 |
18 |
229 |
28 |
632 |
9 |
152 |
19 |
232 |
29 |
650 |
10 |
174 |
20 |
244 |
30 |
652 |
REFERENCES
Alcock, J. (1988). The mating system of Orthetrum
caledonicum (Brauer),
with special reference to variation in copulation duration (Anisoptera:
Libellulidae). Odonatologica 17: 1–8.
Andrew, R.J.
(2001). Evidence of sperm
displacement in Ischnura aurora.
Odonatologica 30: 435-439.
Andrew, R.J., K.A.
Subramanian & A.D. Tiple (2008). A Handbook of Common Odonates
of Central India. Published by the South Asian Council of Odonatology (SACO), India for the 18th
International Symposium of Odonatology, 54pp.
Buchwald, R.
(1991). Libellenfunna und vegetation - eine Zwischenbilanz biozonologicher Forschung. Verhandlungen der Gesellschaft für
Ökology 2: 45–62.
Carle, F.L. (1982). Evolution of the odonate
copulatory process. Odonatologica 11: 271–286.
Corbet, P.S. (1999). Dragonflies - Behaviour
and Ecology of Dragonflies. Harley Books (B.H. Hsrley and A. Harley Ltd.), Great Horkesley,
England, 829pp.
Conrad, K.F. &
G. Pritchard (1988). The reproductive behavior of Argia vivida Hagen:
an example of a female-control mating system (Zygoptera:
Coenagrionidae). Odonatologica 17: 179–185.
Cordoba-Aguilar, A. (2010). Seasonal variation in genital and body size, sperm displacement
ability, female mating rate and male harassment in two calopterygid
damselflies (Odonata: Calopterygidae).
Biological Journal of the Linnean
Society 6: 815–829.
Cordero-Rivera, A. & P.L. Miller (1992). Sperm transfer, displacement and
precedence in Ischnura graellsii
(Odonata: Coenagrionidae). Behavioral Ecology and Sociobiology 30: 261–267.
Cordero-Rivera, A., J.A. Andres, A. Cordoba & C. Utzeri (2004). Postmating sexual selection: allopathic evolution of sperm
competition mechanisms and genital morphology in calopterygid
damselflies (Insecta: Odonata).
Evolution 58: 349–359.
Fincke, O.M. (1987). Female monogamy in the damselfly Ischnura
verticalis Say (Zygoptera:
Coenagrionidae). Odonatologica 16: 129–143.
Fraser, F.C.
(1933). The Fauna of British India
- Odonata - Vol. 1. Taylor & Francis, London, 423pp.
Furtado, J.I.
(1974). The reproductive behavior of Copera marginipes (Rambur) and C. vitata acutimargo (Kruger) (Zygoptera:
Platycnemididae). Odonatologica 3: 167–177.
Matsuda, R. (1976). Morphology and Evolution of
the Insect Abdomen. Pergamon Press, Oxford, 534pp.
Meek, S.B. & T.B. Herman (1990). A comparison of the reproductive behaviours of three Calopteryx
species (Odonata: Calopterygidae)
in Nova Scotia. Canadian Journal of Zoology 68:
10–16.
Miller, P.L.
(1987a). An examination of the
prolonged copulations of Ischnura elegans (Vander Linden) (Zygoptera:
Coenagrionidae). Odonatologica 16:
37–56.
Miller, P.L.
(1987b). Sperm competition in Ischnura elegans (Vander
Linden) (Zygoptera: Coenagrionidae).
Odonatologica 16: 201–207.
Miller, P.L & A.K. Miller (1989). Post-copulatory
‘resting’ in Orthetrum coerulescens
(Fabricius) and some other Libellulidae:
time for ‘sperm handling’? (Anisoptera). Odonatologica 18: 33-41.
Miller, A.K. & P.L. Miller (1985). Flight style, sexual identity and male
interactions in a nonterritorial dragonfly Onychogomphus forcipatus
unguiculatus (Van der Lindane)
(Odonata: Gomphidae).
The Entomoiogist’s Monthly
Magazine 121: 127–132.
Mizuta, K. (1988). Adult ecology of Ceriagrion
melanurum Selys, and C.
nipponicum Asahina (Zygoptera: Coenagrionidae) 1.
Diurnal variations in the reproductive behaviour.
Odonatologica 17: 195–204.
Mokrushov, P.A. & L.I. Frantsevich
(1976). Visual stimuli in behavior of
dragonflies. III. Choice of settling place in Erythromma
najas. Vestnik
Zoologii (Kiev). 4: 20–24.
Prasad, M. (1990). Reproductive behaviour of Ceriagrion coromandelianum
(Fabricius) and Pseudoagrion
rubriceps Selys ((Zygoptera: Coenagrionidae). Annals of Entomology 8: 35–58.
Rowe, R.J. (1987). The Dragonflies of
New Zealand. Auckland University Press, 260pp.
Sakagami, S.F., H. Ubukata, M. Iga & M.J. Toda
(1974). Observations on the behavior of some Odonata in the Bonin Islands, with considerations on the
evolution of reproductive behavior in Libellulidae. Journal of the
Faculty of Sciences, Hokkaido University, Series 6, Zoology 19: 722–757.
Samway, M.J. (1994). Insect Conservation
Biology. Chapman and Hall, London, 358pp.
Sharma, G. (2009). Life history
reproductive and behaviour of Ceriagrion coromandelianum (Fabricius) (Odonata: Insecta). Annals of Forestry 17: 298–310.
Srivastava, B.K. &
B.S. Babu (1985). Reproductive behaviour
of Ceriagrion coromandelianum
(Fabricius) (Zygoptera: Coenagrionidae). Proceedings of the First Indian
Symposium of Odonatology 209–216.
Tajima, Y. & M. Watanabe (2014). Seasonal variation of
genital morphology and sperm removal in damselfly Ischnura
asiatica (Brauer) (Zygoptera: Coenagrionidae).
Odonatologica 43: 213–226.
Thompson, D.J. (1990). On the biology of the
damselfly Nososticta kalumburu
Watson & Theischinger (Zygoptera:
Protoneuridae). Biological
Journal of the Linnean Society 40: 347–356.
Waage, J.K. (1982). Sperm displacement by
male Lestes vigilax
Hagen (Zygoptera: Lestidae).
Odonatologica 11: 201–209.
Waage, J.K. (1984). Sperm competition and
the evolution of Odonate mating systems, pp. 251–290.
In: Smith, R.L. (ed.) Sperm Competition and the Evolution of Animal Mating
Systems. Academic Press, New York, 710pp.
Waage, J.K. (1986). Evidence of widespread
sperm displacement ability amongst Zygoptera and the
means for predicting its presence. Biological
Journal of the Linnean Society 28: 285–300.
Waage, J.K. (1988). Reproductive behaviour
of the damselfly Calopteryx dimidiata Burmeister (Zygoptera: Calopterygidae).
Odonatologica 17: 365–378.