Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 August 2021 | 13(9): 19263–19273
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.7164.13.9.19263-19273
#7164 | Received 06 February 2021 | Final
received 22 July 2021 | Finally accepted 05 August 2021
On the reproductive biology of
the invasive Armoured Sailfin Catfish Pterygoplicthys
pardalis (Castelnau,
1855) (Siluriformes: Loricariidae)
from the natural drainages in Thiruvananthapuram, India
Smrithy Raj 1, Suvarna S.
Devi 2, Amrutha Joy 3 & A. Biju Kumar 4
1–4 Department of Aquatic Biology
& Fisheries, University of Kerala, Thiruvananthapuram, Kerala 695581,
India.
1 smrithyaqb@gmail.com, 2 suvarnaraja1995@gmail.com,
3 amrithajoyj2@gmail.com,
4 bijukumar@keralauniversity.ac.in (corresponding
author)
Abstract: The present paper deals with the
breeding biology of the invasive fish Pterygoplicthys
pardalis from the natural drainages of
Thiruvananthapuram, Kerala. The specimens were collected from Amayizhanchan Thodu,
a natural drainage running through the heart of the city. A total of 145 males
and 142 females were collected from January to December 2018. The sex ratio was
determined monthly as the percentage of males to females (M: F). Monthly mean
gonadosomatic index (GSI) values were compared using R stat, and GSI was
plotted monthly to identify the spawning seasons. The gonads were examined and
different stages of maturity were noted using standard methods. The length at
first maturity was also found out. The fish exhibit courtship behaviour and the eggs are deposited in burrows and also
along the crevices in the granite walls; the burrows are guarded by the male
fish till the young ones are hatched out. The sex ratio showed an average mean
value of 1.04: 1 and showed no significant departure. The size at first maturity
was 23.9 cm standard length. The ova diameter studies show the presence of ripe
ovaries throughout the year, with peaks during March and April and between
August and September and in December, indicating the fish is a batch spawner. The absolute fecundity ranges from 923 to 14,777
eggs, and the relative fecundity ranges 0.0142–0.0015. Regression analysis
showed a significant relationship (P <0.001) between absolute fecundity and
the total length, the total body weight, and ovary weight. The strong breeding behaviour, the presence of accessory respiratory organs,
the absence of natural enemies and parental care makes Pterygoplichthys
pardalis a successful invader in the natural
drainage. More biological studies are needed for the successful eradication of
the species from the invaded ecosystem.
Keywords: Breeding biology, breeding
behaviour, fecundity, invasive alien species,
invasion biology.
Editor: Anonymity requested. Date of publication: 26 August 2021 (online &
print)
Citation: Raj, S., S.S. Devi, A. Joy & A.B. Kumar (2021). On the reproductive
biology of the invasive Armoured Sailfin Catfish Pterygoplicthys
pardalis (Castelnau,
1855) (Siluriformes: Loricariidae)
from the natural drainages in Thiruvananthapuram, India. Journal of Threatened Taxa 13(9): 19263–19273. https://doi.org/10.11609/jott.7164.13.9.19263-19273
Copyright: © Raj et al. 2021. 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 research was funded by the Directorate of Environment and Climate Change, Government of Kerala, India.
Competing interests: The authors declare no competing interests.
Author details: Smrithy
Raj (SR) is a PhD candidate in the Department of Aquatic Biology &
Fisheries, University of Kerala. He works on invasive fishes, invasion biology
and taxonomy of freshwater crabs. Suvarna Devi (SD) works as guest faculty in
the Department of Aquatic Biology & Fisheries, University of Kerala and she
is specialised in fish biology and taxonomy of
brachyuran crabs. Amrutha Joy (AJ) is an M.Phil. student in the Department of
Aquatic Biology & Fisheries, University of Kerala. Biju Kumar (ABK) is the
professor and head in the Department of Aquatic Biology & Fisheries,
University of Kerala. His research interests include taxonomy of aquatic
organisms, invasion biology, fisheries management and conservation policies.
Author contributions: SR—field work, data collection,
photography, drafting manuscript, revisions at different stages. SD—methodology
design, data analysis and interpretation, write up, review, revisions at
different stages. AJ—data collection, practical biology studies, writing of
preliminary draft.
ABK—conceptualization, funding acquisition, photography, manuscript
review, editing.
Acknowledgements: The authors thank the Directorate
of Environment and Climate Change, Government of Kerala, for the financial
support of the project on aquatic exotic species in Kerala. We are grateful to
Madhu Vellayani, the fisherman who was our close
companion and helped us in fish collection in all field surveys. We thank the
support of Mr Mosab Ali Mohamed Ali Al-zahaby for his help in the regression analyses. SR is funded for his PhD programme
by the Rajiv Gandhi National Fellowship (RGNF), Government of India
INTRODUCTION
Reproductive biology is one of
the key features considered for the invasion biology studies of fish (Feiner et al. 2012; Gutkowsky
& Fox 2012; Zahorska et al. 2013; Horkova & Kovac 2015). The suckermouth armoured catfishes of the family Loricariidae,
especially the genus Pterygoplichthys T.N.
Gill, native to inland water bodies of South America, is an emerging invasive
fish globally (Orfinger & Goodding
2018), also, one of the most popular and commonly traded aquarium fish in India
(Knight 2010). The sailfin armoured catfish species
recorded from the natural water bodies of India include P. anisitsi, P. disjunctivus, P.
multiradiatus, P. pardalis,
and possible hybrids (Sinha et al. 2010; Singh 2014; Kumar et al. 2015; Soundararajan et al. 2015; Sandilyan
et al. 2016; Hussan et al. 2018).
The high invasiveness shown by
this species is primarily because of its unique biological features, which
include the ability to survive in water with varying levels of flow regimes
(Nico & Martin 2001; Welcomme & Vidthayanom 2003; Chavez et al. 2006; Nico et al. 2012),
temperature and dissolved oxygen using accessory respiration with diverticula
of the gastrointestinal tract (Armbruster 1998; da Cruz et al. 2013), and pH
(Mendoza et al. 2009; Parente et al. 2017), a
broad range of diet (German et al. 2010) and the absence of natural predators
(Nico & Martin 2001; Gibbs et al. 2008), which enable them to survive in
the invaded ecosystems. They are
salt-tolerant and survive well in brackish water regions (Mendoza et al. 2009;
Kumar et al. 2018). They also have efficient reproductive strategies, including
parental care and deter predation by possessing bony plates that cover their
body (Hoover et al. 2004; Liang et al. 2005; Wei et al. 2017). One such extreme
measure of parental care is exhibited by the male members of the genus Pterygoplichthys. It is the burrows
they dig out on the river banks, and the female will lay eggs that are guarded
by males (Nico et al. 2009; Alamdin & Jumawan 2016). Thus, site selection for spawning, nest
building and caring of eggs and the young ones are a complex set of
reproductive behaviour among loricariids (Covain & Fisch-Muller 2007).
The reproductive traits of Pterygoplichthys spp such
as size at maturity, spawning, sex-ratio, ova diameter, fecundity and
reproductive plasticity are studied to have a better knowledge on the
reproductive dynamics (Jumawan and Herrera, 2014;
Gibbs et al., 2017) which is a prerequisite for the management measures of an
invasive species (Hoover et al., 2005; Kopp et al. 2009). The reproductive
patterns of P. disjunctivus from Florida were
extensively analysed by Gibbs et al. (2017) for 10
years. In contrast, studies on the particular aspects of reproduction have been
published by Rueda-Jasso et al. (2013), Jumawa &
Herrera (2014) on P. disjunctivus from Mexico
and Philippines, Samat et al. (2016) on P. pardalis from Malaysian waters, and Cook-Hildreth et
al. (2016) from Texas waters. Wei et al. (2017) studied the maturity of Pterygoplichthys spp., a hybrid from China and
reported self-sustaining populations in the drainages of the area.
The negative impacts caused by
Pterygoplichthys spp. in the invaded ecosystems,
include siltation problems, bank erosion in rivers and streams, competition
with native species for food and space, consumption of the eggs of native and
threatened species, displacement of vegetation and disturbance to the breeding
grounds of native fish and economic losses to the fishermen including damage to
the fishing gears, are reported earlier by many researchers (see Bunkley-Williams et al. 1994; Hoover et al. 2004; Chavez et
al. 2006; Wakida-Kusunoki et al. 2007; Hossain et al.
2008; Cook-Hildreth 2009; Krishnakumar et al. 2009;
Mendoza et al. 2009; Nico et al. 2009; Capps & Flecker
2013).
The reproductive parameters of
oviparous fish outside their natural range will supplement the evidence to
comprehend their establishment in the invaded ecosystems (Samat
et al. 2016). Such studies, especially on reproductive biology, are required to
better understand the natural history and reproductive plasticity, which are
necessary tools for effectively managing this emergent invasive species.
Despite the increasing numbers of publications regarding the invasion range
extension of Pterygoplichthys spp. in
various biogeographic regions, a knowledge gap on the reproductive biology of
this invasive fish persists in India. Hence to address this significant gap, we
investigated the reproductive biology of invasive loricariid fish Pterygoplicthys pardalis
with a description of their breeding behaviour in
natural streams.
MATERIALS
AND METHODS
Collection Site and Sampling
The fishes for the study were
collected from Amayizhanchan Thodu,
(8.484711 – 8.5662930N; 76.933348 – 76.9499820E), a
natural drainage of 3.4 km2 in Thiruvananthapuram city, Kerala
(Figure 1; Image 1). A total of 145 males and 142 females were collected
fortnightly from January to December 2018 using a cast net, 5-m long and 3.8-cm
mesh size. The fishes were dissected, but before that, they were kept for four
hours in a deep freezer. The sex ratio was determined monthly as the percentage
of males to females (M: F). The burrow structure was captured with a digital
camera, and its width, diameter, depth, the maximum height of entrance, shape of
the tunnel, condition of the burrow, and occupancy of burrows were noted (Image
2).
Measurements of total length (TL,
cm), standard length (SL), total weight (TW, g) and gonad weight (GW, g) were
taken for male and female specimens. Total length and standard length were
measured to the nearest 0.1 cm, and weight to the nearest gram 0.1 g using a
digital balance. Gonadosomatic index (GSI) was calculated as GSI = [(gonad
weight)/(total weight of fish)] × 100 (Vazzoler,
1996). Monthly mean GSI values were compared using R stat, and GSI was plotted
monthly to identify the spawning seasons.
The fishes were dissected to
remove their gonads. Stages of maturity were determined following (Mazzoni & Caramaschi 1997)
and ova diameter observations. The number of fishes in various stages include:
immature (16), maturing (33), ripe (45), regressing spent (18), and recovering
spent (30). Ovaries were excised, weighed to the nearest gram, and preserved in
10 per cent formalin for later assessment. Spawning type was designated
according to the stage of the ripe and spent ovaries. Testis was characterized
using a visual-based macro scale of maturity based on testicular size, colour, and swelling (Lowerre-Barbieri
et al. 2011).
The length at first maturity (L50)
was defined as the total length, where 50% of all individuals are predicted to
be adults (Vazzoler 1996). For ova diameter studies,
the diameter of maturing and mature eggs (Vitellogenic
oocytes) was measured to the nearest 0.01 mm with digital calipers and from the
photos taken using Leica stereo zoom dissecting microscope.
To evaluate the absolute
fecundity (AF), ripe ovaries which are in late-maturing stages to ripe ones
(mid to late vitellogenic phase- Patiño
& Sullivan 2002) were taken for the studies, and 100 mg sub-samples of eggs
from the anterior, middle, and posterior regions were weighed and counted under
a binocular stereo microscope. The counted eggs were averaged and extrapolated
for the entire ovaries using the formula: F= nG/g
where F is the fecundity, n is the number of eggs in the sub-sample, G, ovary
weight and g the subsample weight. The
number and size of eggs were determined under a binocular dissecting
microscope. The gonadal cycle also has been estimated based on macroscopic
observation, and five stages have been described (Araújo et al. 1998; Duarte
& Araújo 2002). To evaluate the relative fecundity (RF), the absolute
fecundity is divided by the total weight of the fish (Bagenal
1978). The relationship between relative fecundity (RF) and the variables total
body length (TL), the total fish weight (FW), and ovary weight (OW) were
estimated.
RESULTS
Breeding behaviour
Pterygoplichthys pardalis that invaded the natural
drainages in Thiruvananthapuram city (Images 1A–C) excavate burrows for
breeding <https://www.youtube.com/watch?v=h5VZ-SVw7Wc>. Our observations
reveal that the male fish excavate burrows (Image 2A, B) before spawning for
laying eggs.
The burrows (older/used) above
the water level are small and triangular to circular, measuring 10–20 cm in
diameter. In contrast, those below water are larger without definite shape,
measuring 30–50 cm in width. The horizontal burrows are 120–140 cm deep, with
the slope extending downwards into the bank. Courtship behaviour
was exhibited in the form of circular movements near the burrows (Images 2C–E),
by rubbing their bodies with the flashing of water, and in a few cases,
multiple males take part in the process, and the eggs are guarded till the
young ones emerge from the nest (Image 2F).
It was also observed that this
species also selects crevices in the granite walls of the stream to deposit
eggs, which may be one of the reasons for their higher rate of survival in the
drainages of Thiruvananthapuram city in Kerala.
Sex ratio
A total of 145 males and 142
females of P. pardalis collected from the
study site showed sex ratio (M: F) of an average mean value of 1.04: 1. The
ratio was tested by chi-square analysis for differences from hypothetical ratio
1: 1, which showed no significant departure.
Stages of the reproductive cycle
Females (N=
142) ranging from SL 17.2 cm (TL 24.4 mm) to 45.6 cm (TL 58.4 mm) were
considered for ascertaining reproductive stages. Mature ovaries exhibited
asymmetry, whereas immature ones were symmetrical. It was observed that the
larger the size of the individual, the greater would be the occupancy of the
ripe ovary in the abdominal cavity and vice versa. Based on macroscopic and
microscopic examination (Table 1) and ova diameter studies, five developmental
stages of gonads (immature, maturing, ripe, regressing spent, and recovering
spent) were identified in female fish (Table 1, Image 3 A–D, 4 A–F). In males,
three maturity stages were identified: immature, maturing and mature, depending
upon the colour and size of testes (Image 5 A–F).
The
macroscopic and ova diameter studies showed P. pardalis
has an intermittent spawning period with ripe ovaries throughout the year,
maximum during March and April. Immature stages were noticed from May onwards,
followed by maturing ones from June to November with a peak in July. The ripe
ovaries were present in all months except February, with a maximum during March
and April. Accordingly, the spent ovaries (regressive and recovering ones) and
immature stages were noticed in the subsequent months, which mean the fish
spawns during the rains (as summer rains occur during May). The second set of a
large number of ripe ovaries was visible in August and December, with
regressing and recovering spent in September and January, respectively showing
the extended spawning season for the fish.
Length at
first maturity
The minimum
length to attain sexual maturity with vitellogenic
oocytes was noticed in females at a standard length of 23.9 cm. The length at
which 50% of the fish gets matured is at 36.56 cm (Figure 3).
Fecundity
To
understand the absolute fecundity (AF), the ovary (left lobe) of ripe fishes
were dissected, and the ripe ova were fully counted and extrapolated.
The absolute fecundity of fish ranges from 923 (TL 393 mm; SL 294 mm) to 14,777
eggs (TL 516 mm; SL 414mm), and the relative fecundity ranges from 0.0142 (TL
459 mm) to 0.0015 (TL 393 mm). In mature fish, both the ovaries (left and right
lobe) showed a clear asymmetry inside the abdominal cavity (Image 4A).
Gonado-Somatic
index and ova diameter
The GSI of
females showed three peaks, with the first one in March–April, the second in
August–September and a third in December, which indicates an extended batch
spawning nature of the fish (Figure 4). Similar to GSI, three peaks could also
be observed with regard to the mean ova diameter, confirming an extended
spawning season for P. pardalis (Figure 5).
The maximum ova diameter obtained in the present study was 3.75 mm. While
comparing ova diameter frequencies corresponding to different maturity stages,
maximum oocyte diameter (mean) was noticed in the ripe stage (Figure 6).
Regression analysis
Regression analysis showed a
significant relationship (P <0.001) between absolute fecundity and the total
length, the total body weight and ovary weight (Figures 7–9). As the total
length, total body weight, and ovary weight of fish increases, the fecundity
does not increase correspondingly due to lesser ‘b’ value (2.0482, 0.8214,
0.6944).
DISCUSSION
Although the suckermouth armoured catfish of the genus Pterygoplichthys
is an emerging global invader, the details of its invasion biology are also
being studied from its extended invasion ranges (Orfinger
& Goodding 2018), the unique breeding behaviour of Pterygoplichthys
spp. by excavating burrows in river banks have been documented from Florida
(Nico et al. 2009), Mexico (Lienart et al. 2013) and
the Philippines (Almadin & Jumawan
2016). Similar breeding behaviour was also observed
in the present study. The females use the burrows dug by the males to deposit
eggs and are guarded by the males till the young ones emerge from the nest;
similar behaviour was also noted by Mazzoni et al. (2002), Power (2003), and Liang et al.
(2005), which establish that the males of this fish exhibit parental care by
building nests, protecting eggs and as well as the juveniles. Lienart et al. (2013) observed egg clutches frequently
inside active nests, and such observation was not observed in the present
study. The present study observes that Pterygoplichthys
pardalis use the crevices in the granite wall for
breeding, which was the first record of breeding behaviour
of the species in the Indian water bodies. The benefit of additional natural
space also compounded the reproductive behaviour of
the fish enhanced its invasive nature in the invaded ecosystem. The sex ratio
(M: F) of P. pardalis showed an average mean
value of 1.04: 1, indicating no bias, showing an equal representation of both
sexes in the population.
The current study on the
macroscopic and the ova diameter clearly showed different reproductive
strategies, showing an extended spawning period with ripe ovaries throughout
the year, mostly during March, April, August, and December. Spent ovaries
(regressive and recovering ones) and immature stages were noticed in the
subsequent months. Such reproductive plasticity was also reported for P. disjunctivus by Gibbs et al. (2017) from Volusia Blue
Spring for a decade. The peak breeding season reported in P. pardalis by Wakida-Kusunoki,
& Amador-del Angel (2011) was from June to September. GSI and ova diameter
also showed the same results, which coincided with these months. Fish with ripe gonads were obtained
throughout our study period except for February, which is consistent with the
studies of Rueda-Jasso et al. (2013) for P. disjunctivus
from Mexico. In the ripe ovaries itself, we came across oocytes with different
diameters, consisting of several immature and maturing ova at the same time,
which proves the fish as a determinate batch spawner.
Similar to other congeners, P. pardalis also
spawn in batches (Suzuki et al. 2000; Duarte & Araujo 2002). Studies on P.
disjunctivus from the Philippines by Jumawan & Herrera (2014) also support this view. Batch
spawning in P. pardalis and its congeners like
Loricariichthys platymetopon,
Loricariichthys sp., and Loricaria sp. (Suzuki et al. 2000), and Hypostomus affinis
(Duarte & Araujo 2002) have been reported, where the mature ovaries are
seen along with immature and maturing ones with pre-vitellogenic
eggs. All Loricariids do not spawn in batches, as Hypostomus
ternetzi, Megalancistrus
aculeatus, and Rhinelepis aspera are
total spawners (Suzuki et al. 2000).
Changes in climatic events could
disrupt the reproductive process in fishes (Yoneda
& Wright 2005; Pankhurst & Munday 2011).
Stable water temperature in tropical rivers is considered best instead of
fluctuating waters in subtropical rivers and a shift in temperature could
confine the spawning period as well (Samat et al.
2016). According to Humphries et al. (1999), flooding is likely the dominant factor
in the breeding behaviour of fish. Pterygoplichthys may be adapted to take advantage of
flooding by initiating reproduction before or at the time of the flood, which
allows fry to feed and grow within inundated floodplain habitats (Kramer 1978;
Humphries et al. 1999; Lienart et al. 2013). Based on
the results of this work, it may be presumed that P. pardalis
inhabiting the natural drainages without noticeable temperature variations is a
batch spawner and temperature may not be an important
limiting factor for spawning of fish that live in a habitat with stable or less
fluctuating water temperature. The population assessment of P. pardalis from natural drainages of Thiruvananthapuram
indicated rapid growth, high-performance index and continuous recruitment,
which resulted in their successful invasion (Raj et al. 2020). Maximum
reproductive activity of P. disjunctivus and L.
multiradiatus were reported from July to
September (Liang et al. 2005; Rueda-Jasso et al. 2013).
The size at first maturity of P.
pardalis in our study was 23.9 cm standard length
(TL 33.5 cm). The minimum size at sexual maturity with highly vitellogenic ova in P. disjunctivus
was reported as 26.7 cm SL onwards by Jumawan
& Herrera (2014) from the Philippines. The case of precocious maturation
was also reported in smaller females during the peak spawning time. A report of
sexual maturity in P. disjunctivus by Gibbs et
al. (2008) was of 300 mm SL. The length at which 50% of fish gets mature is
36.56 cm. Gonadal development of male
and females in the present study also corroborates with the observations of
researchers from other parts of the world.
Absolute fecundity of fish ranges
from 923 to 14,777 in the present study, and the fecundity reported for P. pardalis from Malaysian waters ranged between 1,297 and
18,791 (Samat et al. 2016). A linear relationship is
also exhibited between fecundity and TL, TW, and GW of the fish (Bagenal 1978; Mazzoni & Caramaschi 1995; Duarte & Aroujo
2002). The highest degree of correlation was exhibited in the present study
between fecundity and the total length of the fish (r= 0.7445).
The maximum ova diameter obtained
in the present study was 3.75 mm, which was in accordance with the ova diameter
of 3.3 mm for P. pardalis by Samat et al. (2016), 3.8 mm and 3.6 mm obtained for P. disjunctivus by Gibbs et al. (2008) and Jumawan & Herrera (2014) respectively. The largest mean
ova diameter was 2.327 for ripe ova, as the ova samples contain vitellogenic oocytes of different sizes from the anterior,
middle and posterior regions.
A clear case of asymmetry in the
ripe ovary with the left lobe larger than the right in the abdominal cavity was
observed in the present study. Similar asymmetry in the mature ovary was also
observed in P. disjunctivus (Gibbs et al.
2008). This asymmetry may be due to the large area occupied by the intestine
and the bulk of fat in the abdominal cavity as reported by Rounsefell
(1957) in three female salmonids species.
There are no predators for P. pardalis in the natural drainages where they have
established. This, coupled with the availability of plenty of detritus in the
polluted drainages as food, provide them with a competitive edge over
indigenous species, better reproductive strategies, including the ability to
breed in burrows along the stream banks and crevices in the granite walls,
accessory respiratory organs, batch spawning abilities and parental care
assisted P. pardalis to colonize the system
successfully. The population assessment of P. pardalis
from the same habitat indicated that rapid growth, high growth performance
index, and continuous recruitment are the reasons for their successful
invasion, and targeting the young individuals would help in controlling the
population of the invasive fish (Raj et al. 2020). We recommend more research
on the invasion biology of invasive P. pardalis,
incorporating long-term studies to fully understand the long-term strategies
for their establishment and plasticity in the reproductive behaviour.
Table 1. Macroscopic and
microscopic characteristics of ovarian maturity in Pterygoplichthys
pardalis.
|
Stages of maturity |
Macroscopic and microscopic features |
|
1. Immature |
Tiny ovaries, ranging 11.08–32.5mm,
SL mostly less than 33.4 cm occupying only a tiny percentage of the body
cavity. Ovary thin transparent to light pink, no visible oocytes |
|
2. Maturing |
Size of the ovary ranges
between 33–59.36 mm with tiny granules to less yolky oocytes with SL around
35 cm, colour opaque to pale yellow |
|
3. Ripe |
Highly vascularised,
thin-walled large asymmetrical ovaries occupying mostly half of the body
cavity, brightly orange coloured fully yolked
oocytes, size (1.88–2.81 mm) |
|
4. Regressing spent |
Large flaccid thick-walled
ovaries usually with very few or no vitellogenic
oocytes, vascularisation still visible but less, thick brush-like fimbriae
projects from the ovarian wall into the lumen. |
|
5. Recovering spent |
Ovaries purple to dark pink
with thick inner ovarian walls with slight vascularisation with small oocytes
of different diameters, absence of ripe oocytes |
For
figures & images - - click here
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