Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 January 2024 | 16(1): 24529–24534
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8684.16.1.24529-24534
#8684 | Received 12 August 2023 | Final received 31 December 2023 |
Finally accepted 06 January 2024
Observations on the courtship behaviour of Deocata Pipefish Microphis deocata
(Hamilton, 1822) (Actinopterygii: Syngnathiformes: Syngnathidae) in an aquarium
Anu Saikia
1, Jayanta Kumar Nath 2 &
Dandadhar Sarma 3
1,2,3 Department of Zoology, Gauhati University, Jalukbari,
Guwahati, Assam 781014, India.
1 anusaikia1994@gmail.com, 2 jayantanath459@gmail.com,
3 sarma_dandadhar@yahoo.com (corresponding author)
Editor: Ingrid Ahnesjö,
Uppsala University, Uppsala, Sweden. Date of publication: 26 January
2024 (online & print)
Citation: Saikia, A., J.K. Nath & D. Sarma
(2024).
Observations on the courtship behaviour of Deocata
Pipefish Microphis deocata
(Hamilton, 1822) (Actinopterygii: Syngnathiformes: Syngnathidae) in an aquarium. Journal of Threatened Taxa 16(1): 24529–24534. https://doi.org/10.11609/jott.8684.16.1.24529-24534
Copyright: © Saikia et al. 2024. Creative Commons Attribution 4.0 International
License. JoTT
allows unrestricted use, reproduction, and distribution of this article in any
medium by providing adequate credit to the author(s) and the source of
publication.
Funding: This study was funded by the ICAR-National Bureau of Fish Genetic Resources (ICAR-NBFGR), Lucknow (Project code: G./NE/2015).
Competing interests: The authors declare no competing interests.
Author details: Anu Saikia, a
research scholar in the Department of Zoology, Gauhati University, is currently engaged in studying the breeding biology of M. Deocata, along with other small indigenous fish species. Jayanta Kumar Nath, a research scholar in the Department of Zoology, Gauhati University, concurrently working as an assistant professor at the Department of Zoology, Suren Das College, Hajo. His research focuses on the breeding biology of indigenous fish species. Prof. Dandadhar Sarma, is a professor in the Department of Zoology and coordinator of the Aquaculture and Biodiversity Center, Gauhati University, Assam. He has received numerous research grants in recognition of his significant contributions and discoveries in his research domains. His expertise is reflected in a substantial number of publications in both national and international journals.
Author contributions: The experiment was planned and critically examined by AS and DS; the methodologies were carried out by AS and JKN; the manuscript was prepared by AS and JKN; the final editing was done by DS. All authors reviewed and approved the final version of the manuscript.
Acknowledgements: The authors express gratitude to
the NFDB, Hyderabad, and the University Grants Commission (UGC), New Delhi, for
their technical assistance and support through SAP (DRS-Phase III).
Additionally, the local fishermen are acknowledged for their valuable
assistance during the fieldwork.
Abstract: The Deocata
Pipefish Microphis deocata,
is the sole freshwater syngnathid found in the
Himalayan range. This species is categorised as ‘Near
Threatened’ by the IUCN Red List and is also listed as a Schedule I species
under the Wildlife Protection Act of 1972. This species is highly sought after
in the ornamental fish trade due to its attractive colouration
and uniqueness. The courtship behaviour of M. deocata consists of three distinct phases (initial
courtship, spawning, and swaying) characterized by substantial behavioural alterations. M. deocata
is a species where the action of females is more visible for commencing
courting and strengthening at later phases. The females exhibit skin fold
ornamentation to signal their readiness to spawn mature eggs. The first
courtship phase is characterised by female quivering
along with head pointing by both sexes and often tail entangling. As a sign of
embracing the male often overlies upon the female. In the second phase, the
female transfers her eggs onto the male incubating ventral surface with an
upside-down body posture. During the final phase, the male forms his body into
a contracting wave and lastly settles down in the bottom of the tank.
Keywords: Conservation, captive breeding,
male pregnancy, sex-role reversal, spawning.
INTRODUCTION
Although the family Syngnathidae largely consists of a marine taxon that
includes seahorses, pipefishes, and seadragons, there
are a few pipefishes of the genus Dorichthys
and Microphis that inhabit freshwater habitat
(Dawson 1979, 1984). These species often exhibit a unique pre-copulation
nuptial dance in the water column (Gudger 1905) and
paternal care where male investment in offspring typically is in the form of
embryo incubation, aeration, protection, and provisioning (Ridley 1978; Wilson
et al. 2001; Stölting & Wilson 2007; Kvarnemo et al. 2011). In the Broadnosed
Pipefish Syngnathus typhle,
males possess a brood pouch that enables efficient nursing of offspring (Kvarnemo et al. 2011). In contrast, Nerophis
ophidion lacks such a brood pouch (Berglund et
al. 1986). Predominant competition for mates in females is more pronounced in
species where the male potential reproductive rate is lower than that of
females (Vincent et al. 1992). Moreover, among species the male shows a
variation in the degree of structural and physiological specialization of
parental care (Herald 1959; Vincent et al. 1992; Wilson et al. 2001). Within
this family the operation of sexual selection (Trivers
1972; Thornhill & Gwynne 1986) can work on either of the sex (Shuker & Kvarnemo 2021), by the process of competition for mating or
differential mate choice (Trivers 1972; Shuker & Kvarnemo 2021). If males compete among themselves for
females, then the sexual selection pressure will be primarily on males, whereas
predominant female competition results in sexually selected traits and
ornaments in females (Vincent et al. 1992). However, in the conventional
courtship pattern of the animal kingdom, where males are typically more
competitive, females may invest a greater portion of their energy towards
offspring than males (Trivers 1972; Masonjones 1996).
In
this article, we present data on the courtship and spawning of M. deocata. Some brief notes on several aspects of syngnathid behaviour are also
presented, to allow comparisons with M. deocata’s specific reproductive behaviour patterns. As this species is the only threatened
freshwater syngnathid from Himalayan range therefore
it should be our prime concern to save this species and their natural
populations. Its conservation is much more crucial as by protecting this
species, the habitat and rest of the fish communities will also get protected
(Vincent et al. 2011a). In addition, this species has got a huge market demand
in the ornamental fish business because of its uniqueness (Vincent et al.
2011b). Overexploitation and habitat destruction have resulted in a significant
loss of wild stocks. Acquiring an understanding of courtship behaviour will improve our knowledge of their reproductive
ecologies, and how to protect them in nature, but it can also enable captive
propagation, thereby reducing pressure on wild stocks.
METHODS
The present study was approved by
the Institutional Animal Ethical Committee of Gauhati
University, Assam (Reference ID: IAEC/PER/2019/PP-IAEC/2018-034). Microphis deocata
occurs mainly in rivers, streams and lakes (Menon 1999) and was found in rivers
of northern Bengal and Bihar. Afterwards, reported from the foothills of
eastern Himalaya, below Darjeeling (Hora 1921; Menon 1974), Brahmaputra
drainage in Assam (Sehgal 1956; Sen & Choudhury 1977; Sen 1980) and
Arunachal Pradesh (Sen 2000). The species has been categorized as ‘Near
Threatened’ in the IUCN Red list of Threatened Species due to habitat
destruction and overexploitation. The body is elongated and sub-cylindrical with
a protruding snout. The sexes are dimorphic. Males are mainly brownish, with a
dark lateral stripe on the snout and above the operculum (Dawson 1984). Adult
females show distinctive Y-shaped markings on the lower half side of the trunk.
During the breeding season, females extend their abdomen from their body axis
with vibrant colour pattern whereas males show a
continuous distinct white dotted line in its dorsal surface (Image 1) (A. Saikia, pers. obs. 29 August 2020).
About 105 adult individuals (Average
total length±S.D: Male—113±3 mm; Female—141±3 mm)
were kept for 12 months in three tanks approximately 90 l, depth—365.76 mm with
sand and rock bottom, planted with Vallisneria
sp. and Hydrilla sp. sponge and under-gravel filters were provided
for the recirculating water. Fishes were kept in the sex ratio of 1:2 (Male:
Female). The male produces 7–8 broods over a span of a year, with a brooding
period of 25±2 days. The fish were collected as by-catch from local fishermen
using scoop nets (mesh size: 1.0–2.0 mm) in January 2020 from the Manas River (Brahmaputra drainage), Assam, India.
Thermostats (RS 300 W, 220–240 V) were fitted and maintained at 26°C and the
diet consisted of Artemia nauplii or copepods/rotifers. The aquaria were
illuminated with T5 tubes (24W) maintaining a 14L/10D cycle. More than 200 h of
ad libitum observations were made at random intervals, with about 1–2 h of
videotape recordings and the main stages of the courtship rituals were measured
and described. In total, we observed eight pairs of courting fish. To give the
fish time to get used to the observers, observations were made after a week or
two.
RESULTS
Gravid females began to show
pre-spawning displays, especially in the morning hours (0430–0600 h ), by constantly inflating the ventral skin folds. It
consists of a Y-shaped alternate banding pattern (Image 1). The ornament
(contrasted bands) is presented throughout the entire courtship process that
lasts for 1–2 h. Before the onset of courtship, there is an increase in basal activity
of females accompanied by restless parallel movements with other females
horizontally. A clearly distinct 1 mm extended ovipositor and contrasted colouration in the trunk region was visible (Image 1).
Whereas, in males, the dorsal portion is singly lined with a discontinuous
dotted pattern extending from anterior to posterior region,
and has a swollen pouch fold. The spawning events of M. deocata consisted of three distinct phases marked by
prominent behavioural changes and can be summarized
as follows:
In the first phase, continuous
quivering by females is observed. However, males were seen to dilate the
opening of their pouch, inflating the pouch to balloon-like proportions. Both
male and female swam side by side and the male often touched the female’s belly
with his head; the male and female exhibited head-pointing and their tails were
often tangled together. The male often overlies upon the female as a sign of
embracing the female. After approximately 2 h, the male and female began to
swim towards the water’s surface. This phase lasts for a long time as males
have a low degree of mating propensity or due to interruptions brought about by
other females. The interfering females attempted to place their bodies between
those of the mating pair (four at a time in one observation). Males that were
ready to receive the eggs moved their folds apart and approached the female,
manifesting their readiness. (Figure 1a–c)
The mating pair steadily rose in
the water column (up to 38 cm) before the actual spawning event. On approaching
a male, the female starts to rotate her prehensile tail (4 rotations). Further,
the female grasps the tail of the male, swirls it up, and immediately in an
upside- down body posture relaxes its abdomen and lay the eggs facing the anterior
region of the pouch within 1‒2 s of the time period. During egg transfer, the
male and female were usually suspended horizontally in the water column. The
attempt for the egg-transfer process was usually repeated thrice at each swim
towards the surface and it lasted one to three days during which the male was
successful to receive the egg (Figure 1d).
The male continued to swim in the
water column while bending his body into a contracting wave, while the female
started swimming in an orderly directed way right after the egg transfer. The
male maintains this posture for 6–8 s then swims back and repeats the movement.
Perhaps, this behaviour was responsible for the
packing of the eggs in the posterior end of the marsupium. Despite the fact
that sperm ejaculation was not clearly visible, fertilization possibly takes
place inside the marsupium right after egg transfer (Kvarnemo
& Simmons 2004). After this stage, the male progressively sank to the
substratum and remained there immobile, occasionally adopting an S-shaped
stance, like other pipefish species (Fiedler 1954) (Figure 1e)
DISCUSSION
Before mating, the increase in
activity of the female is more pronounced similar to as observed in Syngnathus abaster (Silva
et al. 2006) that usually initiated displays, mainly consisting of vertical
swimming movements indicating shallow intertidal habitats also reported in Corythoichthys intestinalis (Gronell 1984), Nerophis
ophidion (L.) (Fiedler 1954). However, it
contradicts what is reported for N. lumbriciformes
where there is a reduction in vertical and swimming movements as they thrive in
intertidal zones to avoid strong wave action (Monteiro et al. 2002). In
contrast, M. deocata shows horizontal parallel
movement signifying shallow river and stream habitats, similar as observed in M.
aculeatus (Christie 2022). Courtship display shown by female of M.
deocata occurs early in the morning and lasts for
about 4.30–6 h. This is in contrast to S. abster (Silva
et al. 2006) where courtship occurs throughout the day.
Many pipefishes are known to
intertwine their bodies like twisted rope during courtship in C.
intestinalis (Gronell, 1984) and N. lumbriciformes (Monteiro, 2002), but the distinct “S”
shape curves exhibited here by M. deocata are
similar to as observed in M. aculeatus and other species such as S. floridae and S. abaster
(Breder & Rosen 1966; Gudger
1905; Silva et al. 2006). Male M. deocata
exhibits a preference for larger-bodied females with greater ornamentation,
resembling the characteristics observed in N. ophidion
(Rosenqvist 1990) and S. typhle
(Berglund et al. 1997; Berglund & Rosenqvist
2003, 2009). After completion of courtship, the body of the male will be in a
bending structure, which indicates that the male has just received the egg.
This kind of behavioural adaptation of males strongly
signifies that it takes one batch of eggs from a single female at a particular
time. During our study, one of the pair pouches was empty before mating but
became full after mating. Further investigation is needed on brooding males
receiving eggs from one or multiple females.
Afterwards, when the pouch is
full, that male will be unavailable for mating with other females in the group.
Females are the courting sex and show more intense changes in colour patterns during reproduction than males, as also
reported in N. lumbriciformes, N. ophidion and S. typhle
(Monteiro 2002; Berglund & Rosenqvist 2003). As
in N. ophidion (Rosenqvist
1990), S. typhle (Berglund & Rosenqvist 2009), S. abaster (Silva
et al. 2006), and M. deocata an overtly
interactions among females suggests the female-female competition for mates
resulting dominance one over another which occurs mainly through sexual signalling, having a more contrasted colouration
in the trunk with more inflation tendency. They can be considered sex role
reversed (Vincent et al. 1992) as predominantly females are much more active
than males and female-female competition is seen for matings,
similar as observed in M. deocata.
The incidence of disturbances
during the initial stage of the courting ritual appears to be another common
occurrence. Females were seen approaching the courting couple and starting to
aggressively flicker or just following the pair in a parallel motion, a behaviour that might be seen as a sort of competitiveness
(Matsumoto & Yanagisawa 2001). Strangely, the invading female frequently
had trouble mating with the courting male. The prolonged courting display,
however, appeared to come to a halt as a result of these disruptive females’
far greater effectiveness in diverting the other female’s attention. Similar
observations have been described in Corythoichthys
haematopterus (Bleeker) (Matsumoto &
Yanagisawa 2001), Syngnathus schlegeli Kaup (Watanabe et
al. 2000) N. lumbriciformis (Monteiro et al.
2002) and M. deocata, indicating that the
struggle for mates, which differs widely throughout the syngnathid
taxa, is highly influenced by female-female interactions (Berglund & Rosenqvist 2003). However, an experiment carried out by Rosenqvist (1990) on Nerophis
ophidion showed a female-dominance effect in
order of the size of the skin fold of females. Similarly, the exhibition of
female-dominance cannot be denied in M. deocata
because the successful deposition of eggs was recorded in all males of the
present study despite the maintenance of 1 male: 2 female sex ratio. As females of M. deocata
exhibit an ornament, i.e., the colourful belly, and
distension of the belly amplifies this ornament, there is always a greater
tendency of males’ choice to select a female having the largest skin fold
during courtship and subsequent mating.
In conclusion, the present study
provides insights of the breeding behaviour of M. deocata in captivity, i.e., in aquarium. Being the only
threatened freshwater syngnathid of northeastern
India, information shared here will aid in the formulation of effective captive
breeding and rearing protocols along with proper identification of broodstock and their basic requirements in captivity. The
information shared here aims to assist freshwater pipefish breeders worldwide
and restore the population of this threatened species in the wild.
For
images - - click here for full PDF
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