Journal of Threatened Taxa | www.threatenedtaxa.org | 26 March 2018 | 10(3): 11443–11449

Breeding behaviour of the Coromandel Marsh Dart Damselfly (Zygoptera: Coenagrionidae: Ceriagrion coromandelianum (Fabricius)) in central India

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)

Abstract: Ceriagrion coromandelianum (Fabricius) is one of the most common damselflies in the Indian subcontinent. It flies among bushes and breeds in stagnant pools, small garden tanks, tubs and ornamental cement ponds containing submerged and/or floating vegetation. The oviposition behaviour of C. coromandelianum was observed at the botanical garden of Hislop College, Nagpur, India, where small underground cement tubs are utilized to grow macrophytes. C. coromandelianum displays a refined hierarchy of preferences for oviposition and chooses floating leaves of Nymphaea nouchali (69%) over Lemna paucicostata (23%) and submerged Hydrilla verticillata (8%). In an uninterrupted oviposition bout, the female deposits 283 eggs in 16 rows (N=5) on the under surface of the N. nouchali leaf. The tiny leaves of L. paucicostata holds 7.8 eggs in 4.8 rows (N=10). In H. verticillata, the internode region of the stem can house 25.4 eggs (N=10). One or two eggs are also found neatly inserted in the thin leaf base of H. verticillata. Decaying plant material is never used for oviposition. The present investigation also clearly demonstrates that the choice of oviposition substrate not only depends upon the presence of aquatic species in the water body but also on the spatial location of the oviposition site.

Keywords: Egg, endophytic, Hydrilla verticillata, Lemna paucicostata, Nymphaea nouchali, Nagpur, oviposition

doi: http://doi.org/10.11609/jott.3537.10.3.11443-11449

Editor: K.A. Subramanian, Zoological Survey of India, Chennai, India. Date of publication: 26 March 2018 (online & print)

Manuscript details: Ms # 3537 | Received 03 June 2017 | Final received 08 March 2018 | Finally accepted 13 March t2018

Citation: Thaokar, N..R., P.R. Verma & R.J. Andrew (2018). Breeding behaviour of the Coromandel Marsh Dart Damselfly (Zygoptera: Coenagrionidae: Ceriagrion coromandelianum (Fabricius)) in central India. Journal of Threatened Taxa 10(3): 11443–11449; http://doi.org/10.11609/jott.3537.10.3.11443-11449

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, A merit topper in MSc, completed his MPhil, and Ph.D., from Nagpur University using dragonfly as his research subject. He has been studying various physiological, morphological, ethological and ecological aspects of dragonflies of Central India since last 30 years and has more than 90 research papers to his credit. Presently, he is the Patron of the South Asian Council of Odonatology and is serving 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. In 2002 he was awarded the “Outstanding teachers Award” where as in 2016, he was awarded the “Best Researcher “by the RTM Nagpur University. 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. She is teaching as an Adhoc lecturer at the Post Graduate Department of Zoology. She has published 11 papers in National & two papers in International journals, and attended several conferences, seminar and workshops. 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 & two papers in International journals, and attended several conferences, seminar and workshops.

Author Contribution: NRT and PRV contributed in field work and documentation of the oviposition behaviour. RJA 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.

INTRODUCTION

Habitat selection for oviposition is a vital and complex behavior undertaken by odonates, after the termination of copulation. Oviposition takes place either in water (aquatic), on floating plant material (epiphytic), or inside plant tissue (endophytic). For damselflies, choice of ovipositing material primarily depends upon “the initial preference” which is a suitable place both, for landing and easy deposition of egg in the plant tissue (Waage 1987; Martens 1992, 1993, 1994, 1996, 2001). Highly stenotopic species oviposit in one or very few species of plant while eurytopic species may exhibit distinct preferences and oviposit in a wide variety of plants (Martens 1996). Some odonate species of temperate regions show preferences in selecting plant species or even parts/region of plants for oviposition (Martens 1992; Wildermuth 1993; Grunert 1995).

Previously we found that the Coromandel Marsh Dart Damselfly Ceriagrion coromandelianum (Fabricius, 1798) selects specific laminar region of the leaf of water lily, Nymphaea nouchali f. for oviposition and also reported the existence of a direct co-relation between the choice of leaf lamina region and the day of oviposition (Andrew et al. 2011a). In this damselfly, we also studied and evaluated the process of contact guarding oviposition with reference to the male in sentinel position (Andrew et al. 2011b). In continuation with the study of the reproductive biology of this species, the present paper describes the oviposition of Ceriagrion coromandelianum with reference to choice, insertion and deposition of egg in the aquatic plants Nymphaea nouchali Burm, f., Hydrilla verticillata (L.f.) Royde and Lemna paucicostata Hegelm. 6746.

MATERIAL AND METHODS

Site: The observation and collection for the present work was carried out at the botanical garden of Hislop College, Nagpur, (21.16⁰N & 79.03⁰E) where small underground cement tubs/tanks are used to grow macrophytes (Image 1). There is a large circular tub (diameter 105cm) surrounded by six smaller circular tubs (diameter 42cm), followed by a row of three rectangular cement containers (84cm x 47cm). Height of the tubs varies between two to three feet. Two rectangular tubs contain floating L. paucicostata and submerged H. verticillata while the small circular tubs contain H. verticillata. The single large circular tub contains floating N. nouchali, small patches of L. paucicostata and submerged H. verticillata (Image 2). The bottom of the tubs comprise mud, debris and decaying leaves. C. coromandelianum is found ovipositing in these tanks all around the year (except from December to February). The plant material were collected after the female had completed egg deposition and taken to the laboratory for investigation under stereoscope binocular microscope.

RESULTS

Ceriagrion coromandelianum is one of the most common damselflies in the Indian subconti-nent. The male is bright yellow with olivaceous and pale greenish yellow eyes. The females are initially as bright as the males but with maturity turn dull yellow to light brown. The intensity of dullness increases with maturity. It flies among bushes and breeds in stagnant pools and small garden tanks, tubs and ornamental cement ponds containing floating and/or submerged vegetation. Females visit the waters only for reproduction but the males can be spotted at all times around the shrubs near the ovipositing site.

For oviposition, the tandem pair of C. coromandelianum flies towards the tubs and alights on a floating substrate (N. nouchali, H. verticillata, L. paucicostata). The female starts probing the underside with the ovipositor located at the terminal tip of the abdomen. Initially, the female evaluates the under-surface of the substrate by feeling and testing the plant material with the stylus of her ovipositor. If she finds that the substrate is not suitable for oviposition, she repositions herself by moving a few inches along the rim of the leaf lamina (in case of N. nouchali) or relocates to a different site, not more than 5cm (in case of H. verticillata and L. paucicostata) away. Once settled, she begins to perforate the plant tissue with her saber shaped sharp ovipositor valvules and starts laying eggs in it. The female never uses decaying plant material for oviposition.

Experiments were conducted by placing plastic leaf models of Nymphaea in a plastic water tub to understand the behaviour of oviposition. The tandem pair readily settled on the plastic leaf and the female started probing the under-surface of the artificial leaf with the ovipositor, but after hectic probing (168 Sec, Max-225; Min.- 15, N=5), the tandem pair left the site (Image 2). To understand the order of preference for oviposition substrate by C. coromandelianum the data of 20 days (when maximum number of oviposition was noticed) was evaluated. C. coromandelianum displays a refined hierarchy of preference for oviposition substrate and chooses floating leaves of N. nouchali (69%) over L. paucicostata (23%) and submerged H. verticillata (8%) (Table 1, Fig. 1).

Table 1. Ceriagrion coromandelianum - number of ovipositing females on different plants over 20 days.

Days	N. nouchali	L. paucicostata	H. verticillata
1	4	1	0
2	7	3	1
3	5	3	2
4	6	2	0
5	6	0	0
6	8	0	0
7	5	0	0
8	4	4	1
9	6	4	2
10	4	2	0
11	4	2	1
12	9	3	1
13	3	3	2
14	3	2	1
15	5	0	0
16	6	1	0
17	3	2	0
18	3	1	0
19	5	0	0
20	3	1	1
TOTAL	99	34	12
%	69	23	8
Mean	4.95	1.7	0.6
SD	2.06	1.41	0.75
SE	0.38	0.30	0.16

Oviposition in Nymphaea nouchali

Leaves of Nymphaea nouchali form a perfect landing site for C. coromandelianum and provide a large surface area for oviposition (Image 3). In an uninterrupted oviposition bout, the female deposits 288 eggs (Max 322; Min 243; N=5) in 19 rows along the undersurface of the leaf (Image 3). The eggs are mostly arranged in slightly concentric rows and the distance between two eggs is about 689.4±26.5 µm (Max 1230µm; Min 230µm; N=100). The distance between two rows is 2.4±0.3 mm (Max 3.32mm; Min 1.6mm; N=5). Graphic representation by plotting the trend line of second order polynomial shows that maximum number of eggs are laid in the middle row (Table 2, Fig. 2).

Oviposition in Lemna paucicostata

The puncture mark of the ovipositor of C. coromandelianum can be easily observed on the reddish-brown undersurface of L. paucicostata (Image 4). Carefully peeling the leaf under the microscope reveals that the tiny leaf of L. paucicostata holds 37.8 eggs in 4.8 rows (Max 47; Min 30; N=10) (Table 3). The distance between two eggs is 182±20.6 µm and the distance between the two rows is 1610±70 µm (Max 1800µm; Min 1610µm; N=20). The statistical analysis of the data by plotting the trend line of second order polynomial reveals that the maximum numbers of eggs are laid in the middle rows (Fig. 3).

Oviposition in Hydrilla verticillata

In H. verticillata, the internode region of the stem is used for oviposition. Each internode region can house 25.4 eggs of C. coromandelianum (Max 33; Min 14; N=10) (Table 4). The eggs are arranged mostly in two to four longitudinal rows. There is a gap of 71.6±12.7 µm between the eggs. The rows are at a distance of 847.6±52 µm (Max 980µm; Min 670µm). Sometimes oblique or overlapping rows of eggs are also found in the internode region. Rarely, one or two eggs are found neatly inserted in the very thin leaf base of the plant (Image 5).

At times, the female sitting on N. nouchali dips the abdomen in water and the ovipositor encounters the underlying H. verticillata. She ensures the suitability of H. verticillata plant by probing it with the ovipositor and starts depositing eggs in it. This has been tested by deliberately placing or removing H. verticillata below N. nouchali during oviposition. If H. verticillata is removed, the female explores the surrounding areas with the ovipositor without moving from her position and begins ovipositing in N. nouchali, and, if H. verticillata is placed between the ovipositor and N. nouchali leaf, the female easily switches and starts ovipositing in H. verticillata.

After a complete duration of oviposition, the female dislodges herself from the tandem and flies away into the surrounding shrubs or darts away up to a different site. At times, the tandem couple exhibits the ritual of ‘water-touching’ after completing oviposition, i.e., the pair in tandem flies over the water body, and then the female dips her abdominal tip in the water and then the pair flies away among the surrounding bushes. The male is reluctant to leave the female and tries to either re-copulate or force her to re-oviposit by leading her back to water. Sometimes, the female releases herself from the male after resting in tandem for 2–7 minutes. The released female is at times followed by other males but she quickly darts away from the ovipositing site.

Table 2. Ceriagrion coromandelianum - row wise number of eggs deposited in one bout of oviposition on the leaf of Nymphaea nouchali.

Row	Ovipositing female
	1st	2nd	3rd	4th	5th	Total
1	10	14	7	8	7	46
2	11	27	16	10	12	76
3	15	25	25	22	26	113
4	18	42	14	13	15	102
5	9	38	34	11	14	106
6	17	19	7	10	7	60
7	11	30	16	16	15	88
8	13	8	25	17	18	81
9	18	10	14	33	34	109
10	13	24	34	34	38	143
11	14	7	10	7	43	81
12	17	12	42	14	23	108
13	15	15	26	12	21	89
14	21	6	18	39	-	84
15	17	-	12	26	-	55
16	11	-	7	18	-	36
17	7	-	4	19	-	30
18	6	-	8	17	-	31
19	-	-	3	-	-	3
Total	243	277	322	326	273	1441
%	16.9	19.3	22.3	22.6	18.9	100
SD	4.12	11.5	11.18	9.34	11.45	35.46
SE	0.97	2.71	2.63	2.20	2.70	3.36

Table 3. Number of eggs deposited by Ceriagrion coromandelianum in the leaves of Lemna paucicostata.

Leaf	Row						Total	%
	1	2	3	4	5	6
1	3	6	7	7	4	3	30	08
2	9	7	11	7	2	-	36	9.5
3	3	3	11	10	7	-	34	09
4	5	8	14	13	7	-	47	12.4
5	3	9	7	13	9	-	41	10.8
6	4	5	8	8	11	-	36	9.5
7	3	5	12	13	7	-	40	10.6
8	8	11	12	7	-	-	38	10
9	7	8	12	9	-	-	36	9.5
10	8	14	6	11	-	-	39	10.3
Total							377	100

Discussion

In Ceriagrion coromandelianum, the selection of the landing site for oviposition is visual. This was demonstrated by the experiment of using plastic models of Nymphaea leaves as site for oviposition, where the female readily alighted on the artificial leaf and started to feel the under-surface of this leaf for oviposition. Since the plastic was harder (than aquatic vegetation) the female could not penetrate the ovipositor and lay eggs. Once the female dips the abdomen inside water, it is the ovipositor which determines the choice of the insertion site, which can either be the landing substrate (N. nouchali), or the underlying H. verticillata as demonstrated in the experiment of removing or placing H. verticillata below the landing substance.

Matushkina & Gorb (2007) found that coenagrionids and platycnemidid damselflies predominantly choose tissues of Nymphaeaceae for oviposition, while lestids mostly laid eggs in coastal plants. Lestes temporalis and Chalcolestes spp. oviposit into woody branches of trees and bushes. Aeshna viridis used leaves of Stratiotes aloides while Coenagrion mercuriale, mostly used the aquatic Berula erecta (Matushkina & Gorb 2002). Matushkina & Lambret (2011) observed that before inserting her ovipositor in the plant, the damselfly Lestes macrostigma, touches the plant tissue six times before ovipositing. These touches may provide information leading to a choice of insertion site. The damselfly Platycnemis pennipes oviposit in at least 25 species of plants but while ovipositing into the flowering stem of Nuphar lutea, it also exhibits similar hierarchy of preferences in which the age of stems, colour, size and association with a floating leaf are taken into consideration (Martens 1996; Corbet 1999).

In India, Srivastava & Babu (1985) found that C. coromandelianum prefers the aquatic plant Salvinia over Azolla and never oviposits in Spirodela polyrhiza, Trapa natans, Eichhornia crassipes, Lemna microphylla and Nelumbo sp. or dead or decaying leaves at Sagar, Madhya Pradesh. Prasad (1990) found that it oviposits in all aquatic plants at Kolkata, West Bengal while Sharma (2009) reported that it prefers H. verticillata and Polygonum barbatum over other aquatic plants at Hoshiarpur, Punjab. In the present study we have noticeably demonstrated the C. coromandelianum displays a refined hierarchy of preferences for oviposition and chooses floating leaves of N. nouchali over L. paucicostata and submerged H. verticillata. The present investigation clearly demonstrates that the choice of oviposition substrate not only depends upon the presence of aquatic species in the water body but also on the spatial location of the oviposition site.

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