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First report on mass reproductive swarming of a polychaete worm,

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DOI: 10.5376/ijms.2015.05.0003

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 International Journal of Marine Science 2015, Vol.5, No.3, 1-7
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Research Report Open Access

First report on mass reproductive swarming of a polychaete worm, Dendronereis
aestuarina (Annelida, Nereididae) Southern 1921, from a freshwater environment
in the south west coast of India
P.R. Jayachandran, M.P. Prabhakaran, C.V. Asha, Akhilesh Vijay, S. Bijoy Nandan
Department of Marine Biology, Microbiology & Biochemistry, School of Marine Sciences, Cochin University of Science & Technology, Cochin-16, India
Corresponding author email: bijoynandan@yahoo.co.in
International Journal of Marine Science, 2015, Vol.5, No.3 doi: 10.5376/ijms.2015.05.0003
Received: 25 Oct., 2014
Accepted: 23 Nov., 2014
Published: 05 Jan., 2015
Copyright © 2015 Jayachandran et al., This is an open access article published under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:
Jayachandran et al., 2015, First report on mass reproductive swarming of a polychaete worm, Dendronereis aestuarina (Annelida, Nereididae) Southern 1921,
from a freshwater environment in the south west coast of India, International Journal of Marine Science, Vol.5, No.3 1-7 (doi: 10.5376/ijms.2015.05.0003)

Abstract In the present study we report the occurrence of red coloured mass reproductive swarms of Dendronereis aestuarina from
Periyar River of the south west coast of India. It was observed in the freshwater zone of the river during the evening hours of August
31st, 2010. Reproductive swarming behaviour of D. aestuarina has been first reported by Southern, 1921 from brackishwater
environment in the Gangetic delta, however present study reports first time from absolutely freshwater environment. The density of
swarmed polychaete was ~14800 indls. m-2 with the average length of 86 ±16 mm. Male worms were dominated in the 60 specimens
analyzed and the sex ratio was 3:1 (M/F). The average diameter of eggs collected from polychaete body was 0.33 ± 0.08 mm.
Swarming was extended for two days; after successful mating and spawning they were died.
Keywords Dendronereis aestuarina; Reproductive swarming; Periyar River; Cochin estuary; Kodungallure - Azhikode estuary

Introduction aquatic environment and energy flow through

The polychaetes worms are generally found living in
all marine environments, some floating freely near the
surface or the bottom (pelagic fauna), some others, as
part of the benthic fauna, burrowing in the mud, sand
and rocks of seashores down to abyssal depths and
they can even colonize non marine habitats, such as
freshwater and others aquatic systems (Southern 1921,
Fauvel 1953, Nyman et al. 1995, Hutchings 1998,
Bakken and Wilson 2005). Over 10,000 species have
been described to date, belonging to 83 recognized
families, and various estimates have been made to the
total polychaete fauna ranging from 25,000 to 30,000
(Snelgrove 1997, Rouse and Pleijel 2001). They
exhibit considerable variations in recruitment both in
time and space, which is then often reflected in adult
distribution. The families and genera of polychaetes
have wide distributions while, normally, species have
discrete distributions (Hutchings 1998, Ajmal Khan
and Murugesan 2005). A quantitatively enhanced
population indicates that input of organic matter
stimulates benthic productivity (Ansari et al. 1986).
They are involved in demineralization and recycling
processing of organic and inorganic matters in the
1
different food chains (Nair et al. 1984). The breeding
and spawning of polychaetes are induced by various
biotic and abiotic factors such as temperature,
endogenous and lunar timing, while swarming is
controlled by daytime, tide, environmental and
endocrine factors like pheromones (Gaston and Hall
2000, Andries 2001). Temperature is assumed to be
one of the most important external factors
synchronizing maturation and spawning in marine
invertebrates (Tsuji and Hill 1983, Hardege et al. 1990,
Fong and Pearse 1992, Ajmal Khan 2006, Lawrence
and Soame 2009).
The Nereididae (Blainville, 1818) is among the most
diverse of polychaete families, comprising over 540
species and 43 genera (Beesley et al. 2000). They are
most common in shallow marine habitats, but the
Nereididae are the ones that have been more
commonly found in freshwater environments
compared to other polychaete families (Bakken and
Wilson 2005). The variety of Nereididae species being
commercially harvested for fish bait and used as test
organisms in research related to physiology,
endocrinology and the environment (Nithart 2000,
 International Journal of Marine Science 2015, Vol.5, No.3, 1-7
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Bakken and Wilson 2005). These organisms are
important in the form of diet for many fishes and
invertebrates (Gottfried Pillai 1965, Chan 2009, Bijoy
Nandan et al. 2012, Jayachandran et al. 2013). Some
species commonly live in large numbers in the
intertidal zone of estuarine and brackish waters,
normally in sediments of medium to high organic
content (Bent 1967).
Nereididae species exhibit a wide range of
reproductive modes, including external brooding,
viviparity and hermaphroditism (Dorresteijn and
Westheide 1999). Most species undergo morphological
and physiological modifications when they become
sexually mature, suiting many of them for a brief
pelagic existence and improving the chances that
sexual partners will find each other (Chatelain et al.
2008). All Nereididae polychaetes have a semelparous
life cycle; they reproduce once in a lifetime and die
soon after spawning (Dorresteijn and Westheide 1999).
The reproductive swarming of the Nereididae to the
surface waters of marine and estuarine environments
is a well-known phenomenon (Tampi 1958, Read
1974). A conspicuous breeding behaviour, swarming
(mass aggregation of sexually matured adults for
spawning in the surface water), with or without typical
metamorphosis to the pelagic epitokal (heteronereis)
form, is known in many Nereididae species (Hanafiah
et al. 2006). Metamorphosis of the immature worm
into a special reproductive form is known as epitoky
(Chatelain et al. 2008). This is the formation of
pelagic, reproductive individuals, known as epitokes,
from benthic non-reproductive individuals, or atokes.
The production of epitokes usually occurs
synchronously in an entire population, correlated with
lunar and tidal cycles (Rouse and Pleijel 2001) .
Swarming epitokes can be very conspicuous due to
the sheer numbers of worms, especially if they are
bioluminescent (Schulze and Timm 2012). These
types of reproductive strategies enabled them to build
up large populations over very short time periods
(Hutchings 1998).
Polychaetes are commonly found in Indian estuaries,
among 152 species recorded, 119 species from east
coast, 10 species from west coast and 23 species were
recorded from both east and west coasts. Many
investigations were carried out on the abundance and
distribution of polychaetes in the estuarine environments
2
of the south west coast of India (Ramachandra et al.
1984, Sarala Devi et al. 1991a, Prabhu et al. 1993,
Sheeba 2000, Feebarani 2009). Among the 34
estuaries of the south west coast of India, the largest
number of polychaetes species (19) were recorded in
the Cochin estuary (Ajmal Khan and Murugesan
2005). However, there were no previous reports on
reproductive swarming of Dendronereis aestuarina
Southern, 1921 in the estuarine and riverine conditions of
the south west coast of India. The present study is the
first report on mass reproductive swarming of D.
aestuarina on purely freshwater environment and second
report on mass reproductive swarming.
1 Materials and Methods
The swarming of Dendronereis aestuarina occurred in
the riverbank (Aluva Manapuram) (Figure 1) of
Periyar River (10°6'N, 76°21'E), south west coast of
India. At this point, the river bifurcates into the
Marthandavarma and the Mangalapuzha branches.
The Mangalapuzha branch joins Chalakkudy river and
empties into the Lakshadweep sea at Munambam, and
the Marthandavarma branch flows southwards,
through the Udhyogamandal area and joins the Cochin
backwater system at Varapuzha (Government of
Kerala 2009). The tidal cycle in these estuaries was
semidiurnal with microtidal range (0-2m); tidal
influence extended to approximately 25km landward.
The study area is located ~33 km landward from
mouth of Cochin estuary; not under tidal influence.
The average rainfall in the study area was 310 cm/year
and characterized by a totally freshwater environment
during the monsoon, post monsoon and summer season
Figure 1 Location (O) of Dendronereis aestuarina swarming
observed in the Periyar River (Aluva Manapuram)
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(Revichandran and Abraham 1998, Government of
Kerala 2009, Jayachandran and Bijoy Nandan 2012,
Jayachandran et al. 2012b). The present swarming
occurred in the first quarter of the moon; however, the
study area is not under tidal influence.
[NTU- Nephelometric Turbidity Units]). However,
dissolved oxygen content in the water column was
quite low (2.9 ml L-1) and pH slightly acidic in nature
(6.5).

The swarms occurred in the first quarter moon (7 days

after full moon). The swarmed individuals were
observed in the submerged concrete blocks (<10 cm
depth) in the lake shore. Density of swarmed
specimens was estimated using a quadrat (0.25m2)
with 15 cm height, which prevented the escape of
organisms during sampling. Polychaetes were
collected during the sunset hours of August 31st, 2010
and preserved in 4% buffered formalin. Collected
samples were brought to the laboratory and sorted out.
The abundance of polychaetes was expressed in
numbers per square meter (Holme and Mc Intyre
1971). The samples were identified using standard Figure 2 Unfertilized eggs collected from swarmed
references (Southern 1921, Fauvel 1953, Kaushal and Dendronereis aestuarina
Binford 1999, Avnimelech et al. 2001, Bakken and
Wilson 2005, Gravely 2005). Surface water
(duplicates) was collected in 125 ml DO bottle for
dissolved oxygen measurements and the rest of the
parameters such as temperature, salinity and pH were
analyzed by a Systronics water analyzer (Eaton et al.
2005).

2 Results
Dendronereis aestuarina were assembled as a thick
and profuse swarm on a submerged concrete platform
located in the land-water interface at a depth of <10cm.
Following careful identification, it was found that the
swarms were constituted of only a single species: D.
aestuarina. Examined live individuals were reddish
brown mature worms; all female worms carrying
unfertilized eggs (Figure 2). Six random samples were
taken using a standard quadrat and we measured the
average density (Figure 3 a&b) of swarmed
polychaetes (14800 indls. m-2) and mean length (86 ±
16mm). Sex ratio [number of males (M) / number of
females (F)] of swarm was 3:1 among 60 specimens
analyzed. The eggs collected from the polychaetes
were 0.33 ± 0.08 mm in diameter; they were spawned
in firm, irregular gelatinoid masses. Water quality
parameters such as water temperature, salinity, pH and
dissolved oxygen were measured during the sample
collection. Temperature in the water column was
27.6°C. Turbidity showed moderately low value (5.7
3
Figure 3 (a) Microphotograph of Dendronereis aestuarina
Southern, 1921(b) Red colored reproductive swarm of D.
aestuarina, August 31st, 2010 (Photo taken at sunset, 5.30pm)
at Periyar River, India
SYSTEMATICS
Order Phyllodocida Dales, 1962
Family Nereididae, Blainville, 1818
Genus Dendronereis Peters, 1854
Dendronereis aestuarina Southern, 1921
Dendronereis aestuarina Southern, 1921 pl. XX,
Figure 4A-N, text-figs. 9a-h
Dendronereis aestuarina is an annulated worm,
endowed with locomotive bristles or setae. Papillae
present on oral ring of pharynx. First three pairs of
branchiae pectinate and the rest bipinnate. Anterior
neuropodia with 10-12 lobes and an inferior ligule.
 International Journal of Marine Science 2015, Vol.5, No.3, 1-7
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Figure 4 (a) Diagram of dorsal cirri bearing lateral pinnate gills
(40 X), (b) Microphotograph of 18th left foot of Dendronereis
aestuarina bearing lateral pinnate gills (front view)
Dorsal cirri bearing the lateral pinnate gills, which
commence at the 14th-15th foot. In the males, the
dorsal cirrus of the heteronereized segments bear a
series of wart-like protuberances on the ventral surface
while in the females examined these cirri were smooth.
COLOUR: Throughout their life the body is reddish
brown, the colour being probably due to the blood,
and the gills and dorsal vessels are bright red. The
body in front of the gills is much darker, and appears
to be coloured with reddish brown pigment.
DISTRIBUTION: D. aestuarina is widely distributed
along the Indian coast. It has been reported from both
east coast [Chilka Lake (Southern 1921, Kaushal and
Binford 1999), Kakinada Bay (Vijayakumar et al.
1991), mangroves of Tamil Nadu coast (Rouse and
Pleijel 2001)] & west coast of Indian [Cochin estuary
(Sarala Devi et al. 1991b), Periyar River (present
study), Nethravathi estuary (Jepsen et al. 1997),
Talapady River (Dorresteijn and Westheide 1999),
Ratnagiri coast (Westheide 2004), Mandovi – Zuari
estuary (Nimi 2003)].
4
TYPE LOCALITY: Brackish water environment of
Chilka Lake
REMARKS: There were four species described under
the genus Dendronereis. They are Dendronereis
aestuarina Southern, 1921; Dendronereis arborifera
Peters, 1854; Dendronereis dayi Misra (Endemic to
West Bengal, India), 1999 and Dendronereis
pinnaticirris Grube, 1878.
D. aestuarina was described by Southern (1921) from
nineteen specimens of this species, collected from
brackish water on November 27th, 1911, by Mr. S. G.
Platts in the Sunderbans, a district in the Gangetic
Delta and sent by him to the Indian Museum. The type
specimen is 160 mm long, and consists of 160
setigerous segments. It is a female full of immature
ova (Southern 1921, Gottfried Pillai 1965, Sunil
Kumar 2003, Chan 2009). In the lower reaches of
Periyar River such as Kodungallure-Azhikode estuary
and Cochin estuary, the dominant polychaetes were
Dendronereis aestuarina, Dendronereides zululandica,
Prionospio polybranchiata and Heteromastus
filiformis (Pillai 1977, Sarala Devi and Venugopal
1989, Sarala Devi et al. 1991b, Sarala Devi et al. 1992,
Sheeba 2000, Pillai 2001, Feebarani 2009).
Researches on the polychaetes in this region are
mainly concentrated on taxonomy and distribution.
3 Discussion
Nereididae is a group of polychaete worms that is
relatively well known for having been first mentioned
in pre-Linnaean writing. This family is one of the
most diverse polychaete families in the world and the
most diverse species in the Indian Ocean region. In the
present study, we report the occurrence of red
coloured mass reproductive swarming of Nereididae
polychaete D. aestuarina from the purely freshwater
environment of Periyar River in the south west
coast of India. There were no previous reports on
swarming phenomena of this species except on
species description reports of D. aestuarina from
brackish water environment of Chilka Lake by
Southern (1921).
Environmental cues control or synchronize the
breeding of many marine invertebrates. Of these,
photoperiod, temperature, endogenous and lunar
timing have been shown to moderate reproduction
either individually or in combination. In addition, they
 International Journal of Marine Science 2015, Vol.5, No.3, 1-7
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may act directly or, in the case of photoperiod, set
circannual clock mechanisms. However, swarming is
controlled by daytime, tide, weather conditions and
sex pheromones (Hardege et al. 1990, Fong and
Pearse 1992, Andries 2001). Among marine
invertebrate species, reproduction requires the
synchronous spawning of neighboring individuals in a
population. The fact that, in some species, entire
populations can spawn abruptly, sometimes within a
few days, suggests that spawning is coordinated by
external environmental factors. Among the
environmental variables, temperature and day length
may interfere with the reproductive cycle without
even triggering the spawning period (Andries 2001).
Field studies have clearly shown that, in this case,
swarming and spawning are often correlated with
particular phases of the lunar cycle. However,
temperature may interfere with lunar timing, so
swarming may occur at different times of the lunar
cycle in order to enhance breeding success at higher
water temperatures. The spawning of polychaete
worms generally appeared at midnight as recorded by
earlier reports (Tampi 1963). They appeared in small
numbers usually an hour or two before midnight and
were mingled with spawning swarms. It may be said,
in general, that more intense swarming occurs usually
between the full moon and last quarter (Tampi 1963).
In the present observation, more intense swarming
occurred in the first quarter.
Swarming of marine worms has been associated with
the lunar phase (Woodworth 1907, Lillie and Just
1913, Guberlet 1933). Conversely, according to
Hardege et al. (1990) swarming was more correlated
with temperature than lunar phase. As mentioned
above, if, in some cases, environmental factors
provide the information necessary for the observed
synchronization, these factors alone do not seem
sufficient to synchronize the reproduction of marine
polychaetes. This is particularly the case in epitokous
Nereididae, whose reproduction requires exact spatial
and temporal synchronization, leading to the
formation of swarms in which partners recognize each
other by means of chemical signals. Many of the
Nereididae species undergo drastic behavioural,
morphological and physiological changes during their
sexual maturation (epitoky) (Chatelain et al. 2008).
This metamorphosis prepares benthic worms for a
5
brief pelagic existence devoted to mating and, after
spawning, individuals of both the sexes die.
In the Nereis (Neanthes) virens of family Nereididae,
the gravid males leave their burrows and swarm
before spawning and releasing gametes in the sea
while the females apparently spawn in their burrows,
minimizing predation and avoiding adverse
environmental conditions that males encounter.
However, D. aestuarina worms first come to the
nuptial party where they are scattered as individuals.
The isolated small heteronereis females with ripen
eggs suddenly appear from below and rise to the
immediate surface, swimming a few moments there in
spirals and loops. Males continue unabated in
numbers and vigor as the females appear a little later
to join the dance, a dance which seemingly is a climax
that marks the end of their lives. This swimming in
increasingly small circles while emitting genital
products called nuptial dance (Zeeck et al. 1996 ).
This swimming behavior limits the dispersion of
gametes and ensures their release in close proximity to
one another and, consequently, a good fertilization
rate. In mature worms, the behavioral sequence
leading to and including the nuptial dance suggests
that different chemical signals are implicated; these
are, successively, a mate-recognition pheromone
(MRP), an egg-release pheromone (ERP), and a
sperm-release pheromone (SRP). The Nereid coelomic
fluid contains sex pheromones that not only induce
prolonged electrical activity in the central nervous
system of epitokous individuals of the opposite sex,
but also elicit the nuptial dance (Zeeck et al. 1996).
In the present study, swarming occurred on the
concrete steps submerged in the riverbank, where
hundreds of people come to perform the last rites for
their ancestors. The gathering of a large human
population has brought huge amounts of organic
matter that might have favoured polychaete swarming.
D. aestuarina has been recorded in high abundance
from polluted parts of the estuaries around
metropolitan areas (Sheeba 2000, Ajmal Khan and
Murugesan 2005, Feebarani 2009). The present study
area was a purely freshwater environment with
moderately low dissolved oxygen level (2.9 ml L-1)
and slightly acidic (pH 6.5). Water temperature was
27.6°C with low turbidity (5.7 NTU). The observation
that epitokous Nereididae species show significantly
 International Journal of Marine Science 2015, Vol.5, No.3, 1-7
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higher oxygen consumption compared to atokous
worms is consistent with the hypothesis of increased
respiratory capacity during the period of increased
muscular activity when the worms are swarming
(Chatelain et al. 2008). Observed decrease in
dissolved oxygen level in the area could be due to
increased oxygen consumption of these swarming
epitokes. Swarming extended for two days, and then
mating and spawned worms ended up their lives with
mass mortality.
Acknowledgement
The authors are thankful to the Head, of the Department,
Department of Marine Biology, Microbiology and
Biochemistry, Cochin University of Science and Technology
for providing the necessary facilities.
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