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First report of the hybrid blood parrot cichlid from a rice agroecosystem in Seberang Perai Tengah, Penang, Peninsular Malaysia, with notes on syntopic Midas cichlid, Amphilophus citrinellus (Günther, 1864)

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BioInvasions Records (2020) Volume 9, Issue 3: 588–598
Aqmal-Naser and Ahmad (2020), BioInvasions Records 9(3): 588–598, https://doi.org/10.3391/bir.2020.9.3.15 588
CORRECTED PROOF
Rapid Communication
First report of the hybrid blood parrot cichlid from a rice agroecosystem in
Seberang Perai Tengah, Penang, Peninsular Malaysia, with notes on syntopic
Midas cichlid, Amphilophus citrinellus (Günther, 1864)
M. Aqmal-Naser1 and Amirrudin B. Ahmad1,2,*
1Faculty of Science and Marine Environment, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia
2Institute of Tropical Biodiversity and Sustainable Development, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia
*Corresponding author
E-mail: amirrudin@umt.edu.my
Abstract
The blood parrot cichlid, an artificial fish hybrid, was recorded for the first time in
a rice agroecosystem based on specimen collected in Seberang Perai Tengah, Penang,
Peninsular Malaysia. A potential parental species of this hybrid fish, the Midas cichlid
(Amphilophus citrinellus) was also recorded from this agroecosystem. There was
no evidence of self-sustaining populations of this hybrid fish in the agroecosystem.
Nevertheless, their presence increased the risk of food and space competition with
native species (e.g., Pristolepis fasciata), as well as the spread of disease such as
pneumocystectomy.
Key words: Midas cichlid, alien species, aquarium dumping, ornamental fish,
Cichlidae
Introduction
Ornamental fish keeping is a very popular hobby around the world. Due to
their various striking patterns, colours and behaviours, ornamental fish
have become among the most sought after animals in the world. Some
hobbyists also breed fishes through hybridisation in order to obtain
desirable traits. However, lack of knowledge of the correct ethical practices
has led to the dumping of non-indigenous fish species in the environment
(Gertzen et al. 2008). The ornamental fish industry is reported to contribute
to more than 30% of invasive species translocations throughout the world
(Padilla and Williams 2004). For example, pet abandonment has become
the major cause of the introduction of non-indigenous fish species in the
water bodies in Singapore (Ng and Tan 2010) and Japan (Ishikawa and
Tachihara 2014).
The family Cichlidae is one of the most diverse freshwater fish taxa, and
it is very important in the aquaculture and ornamental fish industry (Pullin
1991). For example, Oreochromis niloticus (Linnaeus, 1758) and Oreochromis
mossambicus (Peters, 1852) are the two major non-native species used for
Citation: Aqmal-Naser M, Ahmad AB
(2020) First report of the hybrid blood
p
arrot cichlid from a rice agroecosystem in
Seberang Perai Tengah, Penang, Peninsula
r
Malaysia, with notes on syntopic Midas
cichlid, Amphilophus citrinellus (Günther,
1864). BioInvasions Records 9(3): 588–
598, https://doi.org/10.3391/bir.2020.9.3.15
Received: 8 April 2019
Accepted: 26 March 2020
Published: 21 May 2020
Handling editor: Darren Yeo
Thematic editor: Michal Janáč
Copyright: © Aqmal-Naser and Ahmad
This is an open access article distributed under terms
of the Creative Commons Attribution License
(Attribution 4.0 International - CC BY 4.0).
OPEN ACCESS.
Hybrid cichlid in rice agroecosystem
Aqmal-Naser and Ahmad (2020), BioInvasions Records 9(3): 588–598, https://doi.org/10.3391/bir.2020.9.3.15 589
aquaculture in Malaysia (Rahim et al. 2013). These species are highly
resistant and adaptable to habitat alterations as they reside diverse trophic
levels, which also greatly reduces the cost of rearing them at large scale
(Pullin 1991). A study by Aqmal-Naser and Ahmad (2018a) in a rice field
in Seberang Perai Tengah, Penang, recorded Oreochromis niloticus which
was common throughout the paddy planting season. After 50 years of
introduction, Oreochromis spp. have now established breeding populations
in nearly all water bodies in Peninsular Malaysia (Rahim et al. 2013). The
latter study recorded another additional species from the family Cichlidae,
which was Midas cichlid, Amphilophus citrinellus (Günther, 1864) (Aqmal-
Naser and Ahmad 2018b). Native to Costa Rica and Nicaragua, this species
has been introduced and established in the Asian region, including also
Taiwan and Singapore. Amphilophus citrinellus has a very bright orange
colour morph that has also been reported to be used in the hybridisation
programme with another cichlid, Vieja melanura (Günther, 1862), which
has very colourful pigmentation on the body, to produce the blood parrot
hybrid (Li et al. 2018). Some of the hybrid offspring are found to be
impaired due to deformities (e.g., narrow mouth and damaged swim bladder
which will distort the feeding and swimming of the fishes) related to
inbreeding (Noga et al. 1981; Mair 1992; Tave 1999) and genetic inheritance
(Russell 2003; Stelkens et al. 2015), and even surgical removal of the caudal
fin of the hybrid fish to produce the heart-shaped fish. Apart from that, the
external colouration is a vital criterion in selection of ornamental fishes
where the retail price is closely linked to attractive and auspicious
colouration (Gouveia et al. 2003). The selection process is carried out on
those impaired individuals with undesirable traits in terms of colourations
and shapes, which are often discarded into natural water bodies.
To date, there is no evidence of Amphilophus citrinellus and its hybrid
being able to breed naturally and establish a viable population in the wild
in Peninsular Malaysia. In general, there are no published materials on the
record of Amphilophus citrinellus in Peninsular Malaysia except in Penang
(Aqmal-Naser and Ahmad 2018b). However, based on the information
gathered from the Malaysian Facebook angling group (https://www.
facebook.com/groups/kelabjoranFB) and Malaysian Freshwater Fish
group (https://www.facebook.com/groups/158073811005000/), Amphilophus
citrinellus is usually caught from man-made lakes (Figure 1) in urban areas
(e.g., Selangor and Putrajaya), although no hybrid blood parrot cichlids
were recorded. The presence of Amphilophus citrinellus could increase the
risk of food and space competition with native fish species (Barlow 1983;
McKaye and Barlow 1976), as well as spread fish disease such as
pneumocystectomy (Lewbart et al. 1995). In this study, we aim to provide
more information regarding the introduced Amphilophus citrinellus and its
artificial hybrid, and highlight the emerging problems from the rising numbers
Hybrid cichlid in rice agroecosystem
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Figure 1. Amphilophus citrinellus which was caught from a man-made recreational lake in
Putrajaya, Kuala Lumpur and kept in an aquarium (A); the fish was also caught from an
unspecified locality in Peninsular Malaysia (B). Source: A – Mohd Iskandar Recondzilla and
B – Jenglot Mata Biru Rich.
of the introduced alien species. We investigated the presence of these
cichlids in the rice field environment throughout the paddy planting
season from June 2018 until March 2019 in Seberang Perai Tengah,
Penang, Malaysia.
Materials and methods
Fishes were collected from a rice field ecosystem (i.e. rice agroecosystem)
in Seberang Perai Tengah, Penang (Figure 2), by cast net and scoop net
from various habitats (Figure 3) in the rice field where the water persists
thoroughout the year. The collected specimens were photographed, preserved
Hybrid cichlid in rice agroecosystem
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Figure 2. Map of the state of Penang (A) located in the Peninsular Malaysia. The black shaded
area (B) shows Seberang Perai Tengah where the study area is located. Red triangles show the
distribution of Amphilophus citrinellus collected in the study area (C). CR: concretised river,
SD: storm drain, R: river.
Figure 3. Habitats of Amphilophus citrinellus in the rice agroecosystem. A: river, B: concretised
river, C and D: storm drain. Blood parrot cichlid was collected from the storm drain.
Photograph by M. Aqmal-Naser.
in 10% formalin solution and later transferred to 75% ethanol and
deposited in Universiti Malaysia Terengganu Zoological Collection
(UMTZC). Standard length (SL) was measured from the tip of the upper
jaw to the base of caudal fin using dial calipers. A set of eight selected meristic
Hybrid cichlid in rice agroecosystem
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Table 1. Comparison of selected meristic counts between Amphilophus citrinellus, Vieja melanura, and blood parrot fish from
literature and specimens collected in this study. Numbers in parentheses indicate the average values. NHM: Natural History
Museum, London, UK.
Species Amphilophus citrinellus Vieja
melanura Blood
Parrot Amphilophus
citrinellus
Author Günther et al.
(1905)
Astorqui
(1972)
Barlow &
Munsey (1976)
Villa
(1976)
Stauffer &
McKaye (2002)
McMahan
et al. (2011) This study
Origin Lake
Nicaragua
Lake
Nicaragua
Lake
Nicaragua
Type
specimen
(NHM)
Syntypes
(NHM)
Type
locality
(Laguna de
Petén)
Penang
n 3 17 30 2 3 85 1 25 mode
Dorsal spine 16–17 16–17 16–17 16–17 16–17 16–18 16 15–17 (16)
Dorsal fin rays 11–12 10–12 10–13 12 11–12 11–12 13 11–12 (12)
Anal spine 7 6–8 7 7 3 5–7 7 5–7 (7)
Anal fin rays 8–9 8–9 7–9 8–9 8–9 7–9 11 8–9 (9)
Pectoral fin rays 14–15 15 15 13–16 14 14–15 (14)
Pelvic fin rays 5 5 5 5 5 (5)
Caudal fin rays 16 16 16–18 (16)
Lateral line scales 31–33 30–34 28–31 31–34 30–31 30 30–32 (30)
Figure 4. Blood parrot fish with undesirable (for ornamental fish trade) colour and form,
46.0 mm SL specimen. Coll: M. Aqmal-Naser, 22 June 2018. Photograph by M. Aqmal-Naser.
characters were identified and counted; dorsal spine, dorsal spine rays, anal
spine, anal spine rays, pectoral fin rays, pelvic fin rays, caudal fin rays and
lateral line scales, following Stauffer and McKaye (2002). Data were taken
on the left side of specimens (n = 26) by the first author to reduce bias. A
simple comparison of selected meristic counts between blood parrot fish,
Vieja melanura and Amphilophus citrinellus from literature and from
specimens collected in this study were made to further validate the
identitiy of Amphilophus citrinellus collected in this study (Table 1).
Results
From this survey, we collected a hybrid cichlid fish, commonly known as
blood parrot (Figure 4). Liew et al. (2012) stated that the hybrid is most
likely produced through hybridization between two cichlid species,
Amphilophus citrinellus and Vieja melanura. We also collected an introduced
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Figure 5. Amphilophus citrinellus, SL 72.0 mm (A), 63.0 mm (B), 52.0 mm (C), 55.0 mm (D), 64.0 mm (E), 54.0 mm (F),
56.0 mm (G), 65.0 mm (H), 70.0 mm (I), 64.0 mm (J), 64.0 mm (K), 42.0 mm (L), 52.0 mm (M), 44.0 mm (N), 44.0 mm (O),
64.0 mm (P), 54.0 mm (Q), 72.0 mm (R), 68.0 mm (S), 62.0 mm (T). coll: M. Aqmal-Naser, June 2018 until March 2019.
Photograph by M. Aqmal-Naser.
species, Amphilophus citrinellus (Figure 5), commonly known in the
aquarium fish trade as Midas cichlid with various phenotypes. However,
no specimen of Vieja melanura was obtained during the survey.
Blood parrot hybrid
Material examined: One specimen (UMTZC 8001) from stagnant water in
a storm drain, in rice field, Seberang Perai Tengah, Penang, coll: M. Aqmal-
Naser, 22 June 2018.
Diagnostic characters: The specimen was identified as blood parrot based
on following characteristics: 13 dorsal fin rays, 11 anal fin rays, truncated
body shape with thick foreback, beak-shaped mouth that cannot be fully
closed, which is different from a typical Amphilophus citrinellus that
possess 12 dorsal fin rays, 9 anal fin rays, compressed body with steeper
Hybrid cichlid in rice agroecosystem
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forehead and fleshy lip. The hybrid also usually has oddly shaped and
variations of iris – either oval or round. Some of the juveniles have dark
stripes, but these eventually fade away within the first four months as they
grow (Fishlore 2018). The tail might be cut off to produce a heart shape
body (thus it is also called as heart parrot).
Amphilophus citrinellus
Material examined: 25 ex. (UMTZC 8002; 25) from stagnant water in a
storm drain, in rice field, Seberang Perai Tengah, Penang, coll: M. Aqmal-
Naser, June 2018 until March 2019.
Diagnostic characters: This species has great variation in colouration and
morphology, thus its identification can be more complicated compared to
other species (Barlow 1976; Tan 2014). According to Barlow (1976),
Amphilophus citrinellus has a steeper anterior head profile, deeper body
and thinner upper and lower lips compared to the nearest species,
Amphilophus labiatus (Günther, 1864). In Malaysia, the identification
becomes easier as there are not many species that look similar to
Amphilophus citrinellus, especially those with orange colouration. The
barred morph of Amphilophus citrinellus could be distinguished from the
Mayan cichlid (Mayaheros urophthalmus), another introduced cichlid in
Peninsular Malaysia, by having a smaller ocellus with no white ring at the
caudal peduncle (Tan 2014). None of the individuals collected bear the
characteristics of Mayaheros urophthalmus or Amphilophus labiatus.
Discussion
From the survey, we recorded one species of cichlid, Amphilophus
citrinellus and its hybrid the blood parrot cichlid (Amphilophus citrinellus
× Vieja melanura). We collected several medium size individuals (42 mm
to 72 mm SL) of Amphilophus citrinellus in this study. This would indicate
that the species could thrive well in a rice field ecosystem. The cichlid were
collected from several localities (Figure 2); however, we did not collect any
small fish (juveniles) of Amphilophus citrinellus; thus we believe the fish
has not established a breeding population in this rice field ecosystem. All
Amphilophus citrinellus collected in this study are of similar size, suggesting
that these could have been a single cohort released simultaneously. We also
surveyed local aquarium shops, but did not find any Amphilophus citrinellus
or its hybrid on sale. To compare, Amphilophus citrinellus has already
established breeding populations in Singapore, with breeding pits and size
classes from juveniles to egg brooding adults detected (size ranging from
10 mm to 236 mm total length), with the species being most abundant in
man-made urban stormwater ponds (Kwik et al. 2013).
The specimen of blood parrot cichlid collected might be an escapee or
abandoned fish related to aquarium dumping. The caudal part was not
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removed and it lacked the bright orange colour that is preferable in the
trade. The blood parrot fish that have some deformities or undesirable
traits (body shape and colors) are more prone to be dumped or discarded
into the wild. The male blood parrot is known to be sterile; however, the
female blood parrot has been reported to have the ability to breed with
other cichlids (Fishlore 2018; Sharpe 2018). Some physical deformities may
also prevent these fish from establishing viable populations and surviving
in natural water bodies (Liew et al. 2012). The presence of Amphilophus
citrinellus in this ecosystem could facilitate the hybridization process with
other cichlids in this rice field. The degree of existing hybridization
between Amphilophus citrinellus and other cichlids in this study area could
be underestimated, because the hybrid populations are hard to detect
without genetic approaches (Smith et al. 2003; Magalhães et al. 2015; Meier
et al. 2017) as the family Cichlidae has shown wide intra- and inter-specific
morphological and behavioural diversity (Seehausen 2006).
Based on information gathered from social media (Facebook angling group,
https://www.facebook.com/groups/kelabjoranFB), cichlids have become
extremely widespread and established across Peninsular Malaysia. Ng and
Tan (2010) reported that cichlids are ubiquitous in Singapore, especially in
estuarine and artificial freshwater systems, with Amphilophus citrinellus
having established in almost all types of man-made habitats including
reservoirs, mud ponds and concretized waterways (Ng and Tan 2010; Kwik
et al. 2013; Tan 2014). Detailed knowledge on the exact distribution of
Amphilophus citrinellus throughout Peninsular Malaysia is, however, still
undetermined. The cichlid is usually recorded in abandoned mining pools
and recreational lakes within the urban area where they are caught
alongside other introduced cichlids including Parachromis managuensis
(jaguar cichlid) and flower horn (another artificial hybrid cichlid) (Figure 6).
In the Seberang Perai Tengah agroecosytem, Amphilophus citrinellus was
found only in the major waterways which are the river, concretised river and
storm drain. The slow-flowing to stagnant water and substratum in those
habitats is similar with the native habitat of Amphilophus citrinellus in Lake
Nicaragua, which has stagnant water and a muddy bottom (Barlow 1976).
In general, the ability of the introduced species to exploit different
niches could be one of the reasons it may outnumber native species;
however, the ecological effects are often hard to estimate and quantify
(Trexler et al. 2000). Hassall (2014) suggested Amphilophus citrinellus
could have a major impact on the fish assemblage of artificial habitats in
Singapore. Unfortunately, the true ecological impact of the cichlid
introduction on native species in natural habitats remains understudied.
Possible impacts due to the existence of cichlids in rice field ecosystems on
indigenous species populations include competition for natural resources
(food and space) and the spread of parasites and diseases (Corfield et al.
2007). Both Amphilophus citrinellus and the hybrid are reported to be highly
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Figure 6. Amphilophus citrinellus (A) caught alongside with other cichlids, Parachromis
managuensis (jaguar cichlid) (B) and flower horn (C). Source: Fitri Mohd Noor.
aggressive (McKaye and Barlow 1976; Magalhães et al. 2017). In addition,
captive cichlids have shown increased levels of aggressiveness due to
competition (Oldfield 2011). Native species which share the same habitat
with Amphilophus citrinellus in this agroecosystem are Clarias macrocephalus,
Pristolepis fasciata, and several smaller species, such as Rasbora trilineata,
Oryzias javanicus and Lepidocephalichthys hasselti (Aqmal-Naser and Ahmad
2018a, b). In this rice agoroecosystem, Amphilophus citrinellus also co-exist
with other introduced species such as Trichopodus pectoralis, Oreochromis
niloticus and Barbonymus gonionotus (Aqmal-Naser and Ahmad 2018a, b).
Since Amphilophus citrinellus is omnivorous and consumes a variety of
food, including algae, insects and small fishes (Barlow 1976), fish larvae
and small-sized species in this ecosystem are prone to the predation threats
posed by Amphilophus citrinellus.
Conclusion
The existence of the Amphilophus citrinellus and the associated hybrid in
the Seberang Perai Tengah rice agroecosystem provide a clear signal that
artificial environments with high degrees of disturbance are not a major
obstacle for introduced species to thrive. Dumping of introduced aquarium
fish species, one of the major vectors of biological invasion of the aquatic
environment, must be monitored. Public awareness may be the only
efficient approach to reduce the spread of introduced species in Malaysian
Hybrid cichlid in rice agroecosystem
Aqmal-Naser and Ahmad (2020), BioInvasions Records 9(3): 588–598, https://doi.org/10.3391/bir.2020.9.3.15 597
waters as ornamental fish keeping hobby starting to grow and flourish
among Malaysian. At the moment, little has been done to increase
awareness among local hobbyists, but continuous awareness programmes
through social and mass media could spark awareness of the threats caused
by alien introduced species toward native ecosystems.
Acknowledgements
We thank Universiti Malaysia Terengganu for all the facilities and equipment used in the study.
We thank Dr. Tan Heok Hui, Dr. Low Bi Wei and Associate Professor Dr. Darren Yeo Chong
Jinn for their comments and suggestions to improve the manuscript. We thank Mr. Lim Teow
Yeong for identifying some of the fish species and sharing information regarding the subject.
Amirul, Amirah, Aisha and Azira are gratefully acknowledged for their assistance in the field.
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... Tabla I. Caracteres merísticos seleccionados de ejemplares de Amphilophus citrinellus colectados en la presa de Hatillo, comparados con los encontrados por Stauffer y Mckaye (2002) A. citrinellus o cíclido de Midas (conocido en el mercado de acuarios como parrot fish o cichlid midas fish), es una especie de cíclido nativa de lagos y cráteres volcánicos inundados de Nicaragua y Costa Rica (Stauffer y McKaye, 2002). Este organismo es altamente utilizado en el comercio de mascotas por sus atractivos colores (Arias, 2011) y se ha utilizado en hibridación con otras especies de acuario (Li et al., 2018;Aqmal-Naser y Ahmad, 2020). ...
... El complejo A. citrinellus (híbridos y variedades de acuarios), se ha reportado como invasor en diferentes partes del mundo, por ejemplo, Brasil, Malasia, Filipinas y con poblaciones establecidas en Estados Unidos, Puerto Rico y Hawái donde aún no se conocen sus efectos sobre el medio ambiente (Magalhães et al., 2017;Poniente et al., 2019;Aqmal-Naser y Ahmad, 2020;Nico y Neilson, 2021). En República Dominicana se reporta el comercio de esta especie desde el 2009 a través del mercado de acuarios y mascotas (Mateo y Balbuena, 2011). ...
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