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Aquatic Invasions (2012) Volume 7, Issue 4: xxx–xxx
© 2012 The Author(s). Journal compilation © 2012 REABIC
Open Access
521
Research Article CORRECTED PROOF
Alien invasion in Wallace’s Dreamponds: records of the hybridogenic
“flowerhorn” cichlid in Lake Matano, with an annotated checklist
of fish species introduced to the Malili Lakes system in Sulawesi
Fabian Herder1, Ulrich K. Schliewen2, Matthias F. Geiger1, Renny K. Hadiaty3, Suzanne M. Gray4,
Jeffrey S. McKinnon5, Ryan P. Walter6 and Jobst Pfaender1
1 Sektion Ichthyologie, Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany
2 Department of Ichthyology, Bavarian State Collection of Zoology (ZSM), Münchhausenstr. 21, D-81247 München, Germany
3 Ichthyology Laboratory, Division of Zoology, Research Center for Biology, Indonesian Institute of Sciences (LIPI), Jl. Raya Bogor Km 46,
Cibinong 16911, Indonesia
4 Department of Biology, McGill University, 1205 Docteur Penfield Ave., Montreal, Quebec H3A 1B1, Canada
5 Department of Biology and North Carolina Center for Biodiversity, Howell Science Complex N108, East Carolina University, Greenville,
NC 27858-4353, USA
6 Great Lakes Institute for Environmental Research, University of Windsor, 401 Sunset Ave, Windsor, ON N9B 3P4, Canada
E-mail: f.herder.zfmk@uni-bonn.de (FH), jobst.pfaender.zfmk@uni-bonn.de (JP), matthias.f.geiger@t-online.de (MFG),
Schliewen@zsm.mwn.de (UKS), rani_hadiaty@yahoo.com (RKH), gray.suzanne@gmail.com (SMG) , mckinnonj@ecu.edu (JSM),
rdubsy@gmail.com (RPW)
*Corresponding author
Received: 9 February 2012 / Accepted: 6 October 2012 / Published online: 22 October 2012
Abstract
Invasive fish species can have major impacts on freshwater faunas, particularly in isolated systems harbouring adaptive animal radiations.
Here, we report on the occurrence and recent rapid expansion of the hybridogenic “flowerhorn” cichlid in ancient Lake Matano, the
hydrological head of the Malili Lakes system in Central Sulawesi, Indonesia. We show that flowerhorns rapidly dispersed along the lake’s
shoreline, inhabited most of the southern inshore habitats in 2010, and were present all around the lake in mid-2012. In addition, we present
stomach content and observational data supporting the hypothesis that this cichlid threatens the local fauna through both predation and
competition. We discuss 13 additional alien fish species recorded in the Malili Lakes drainage since 2000, including the recent, first record of
the invasive sailfin catfish Pterygoplichthys pardalis for Sulawesi, highlighting the multitude of artificial introductions of foreign fish
species into these unique and highly isolated freshwater systems. We conclude that alien fish species pose both serious and diverse threats to
the fauna of the Malili Lakes system – an ecosystem of high socio-economic importance and an exceptional natural laboratory for study of
evolution, referred to as “Wallace’s Dreamponds”. Finally, we provide recommendations for minimizing future alien species introductions.
Key words: invasive species; ancient lakes; adaptive radiation; biodiversity hotspot; conservation; flowerhorn cichlid; Pterygoplichthys
Introduction
The introduction of alien fish species into
freshwater ecosystems can have profound
consequences, including loss of species
diversity, extinction of endemic species,
distortion of food web function, and changes to
ecosystem productivity (Barel et al. 1985; Rahel
2000, 2002; Vitule et al. 2009; Gozlan et al.
2010; Hoffmann et al. 2010; Zambrano et al.
2010). However, not all species introductions
lead to the establishment of permanent
populations or even invasions (Gurevitch and
Padilla 2004; Gozlan 2009), as populations of
invaders may collapse under certain conditions
(Cooling et al. 2011). Isolated ecosystems
harbouring adaptive radiations are particularly
vulnerable to the establishment of invasive
species, and in some cases have been seriously
affected by the resulting impacts (Vitousek 1988;
Cox and Elmqvist 2000; Sax et al. 2002; Strecker
2006; Sax and Gaines 2008).
There are several potential impacts of foreign
fishes to native freshwater ecosystems,
especially in evolving radiations (Strecker 2006).
Piscivorous or omnivorous species can be a
direct threat to smaller fish species, juveniles,
fry, or eggs. Invertebrate species of evolving
species flocks, such as shrimps and gastropods
(K von Rintelen et al. 2010; T von Rintelen et al.
F. Herder et al.
522
2010) are likely affected by fish predation.
Introduced fish might also out-compete native
species by exploiting limited resources (e.g.,
food or spawning sites). Finally, introduced
fishes can act as vectors for diseases and
parasites (Kottelat 1990; Strecker 2006; Nico et
al. 2007; Vitule et al. 2009). Examples, such as
the Nile perch (Lates niloticus) introduction in
Lake Victoria about half a century ago (Barel et
al. 1985), have highlighted the potentially
devastating impact invasive species can inflict
on evolving species flocks. In that case, Nile
perch introduction contributed to the decline of
the native fish stocks, including the loss of
hundreds of haplochromine cichlid species, with
massive impacts to the whole ecosystem (Ogutu-
Ohwayo 1990; Witte et al. 1992), and serves to
date as the textbook example for negative
ecological and economical impacts of alien fish
species invasion (Lowe et al. 2000).
The ancient Malili Lakes system in Central
Sulawesi (Indonesia) harbours endemic radia-
tions of various freshwater organisms, including
fishes, molluscs, shrimps and crabs (reviewed in
von Rintelen et al. 2012 and Vaillant et al.
2011). In the last decade, these species flocks of
“Wallace’s Dreamponds” (Herder et al. 2006a)
have been used as valuable model systems for
testing hypotheses on the adaptive character of
intralacustrine radiations (von Rintelen et al.
2004, 2010; Herder et al. 2006a, 2008; Pfaender
et al. 2010, 2011), on gene flow among evolving
species (Herder et al. 2008; Schwarzer et al.
2008; Walter et al. 2009a, 2011), on behavioural
specialization and filial cannibalism (Gray et al.
2007, 2008a; Cerwenka et al. 2012), on the
evolution of male colour polymorphisms (Gray
et al. 2008b; Walter et al. 2009b), and on
geographic modes of speciation, including
mechanisms of ecological speciation in sympatry
(Herder et al. 2008; Pfaender et al. 2011; Walter
et al. 2011).
Most of the lacustrine organisms of the Malili
Lakes system are endemic to one or a few of the
lakes (von Rintelen et al. 2012). The endemism
is a result of the zoogeographic isolation of
Sulawesi from the nearby Sunda shelf with its
rich Southeast Asian fauna (Whitten et al. 2002),
the isolation of the Malili Lakes from other
freshwaters of the island (Brooks 1950), and due
to natural barriers between the lakes (Schwarzer
et al. 2008; Walter et al. 2011). With respect to
the freshwater fishes of the Malili Lakes
drainage, research has largely focused on the
adaptive radiation of sailfin silversides
(Atheriniformes: Telmatherinidae): small,
colourful relatives of Australian and New
Guinean rainbow fishes (Melanotaeniidae) (see
Herder et al. 2006b for a taxonomic checklist,
and Herder and Schliewen 2010 for a review on
evolutionary studies). However, the native
ichthyofauna also comprises small endemic
species flocks of ricefish (Adrianichthyidae),
gobies (Gobiidae), endemic species of halfbeaks
(Zenarchopteridae), and at least one eel species
(Anguillidae) (Kottelat et al. 1993). Descriptions
of fish species new to science continue to
emerge, including taxa from a variety of
different fish families (e.g. Kottelat 1990, 1991;
Larson 2001; Herder and Chapuis 2010;
Huylebrouck et al. 2012), showing that the
aquatic faunal diversity of the area is still not
completely explored.
Sulawesi’s freshwater biodiversity is facing
manifold threats. In the Malili Lakes area, major
threats come from surface nickel mining
operations, including one of the largest mines in
the world, currently extending principally
between Lakes Matano and Mahalona. Impacts
from mining include various direct (land use and
transformation destroying stream and river
habitats; mine effluents; erection of dams for
power supply) and indirect (increased logging
and urbanization, with related pollution; loss of
swamp and forest habitats; land use at the lake’s
shoreline) consequences for aquatic habitats and
their endemic species assemblages. In addition,
commercial fisheries, especially nocturnal light
fishing in Lake Towuti, put pressure on native
lake fish stocks (Parenti and Soeroto 2004).
Introduction of alien fish species adds another
component to the disruption of the natural
ecosystem.
The main sources of non-native and
potentially invasive fish species in the Malili
Lakes include: stockings intended for developing
local fisheries; fishes that escape from
aquaculture ponds or enclosures; and release of
ornamental fishes from ponds or pet aquaria
(Wittenberg and Cock 2001; Parenti and Soeroto
2004; Keller and Lodge 2007). Even by the early
1990s, Kottelat reported as many as 10
confirmed or likely introduced fish species from
Lake Matano alone (Kottelat 1989, 1991), and
successive workers have confirmed and added
additional records of alien fish species in the
area (Hadiaty and Wirjoatmodjo 2002; Hadiaty
et al. 2004). In lakes Poso and Lindu in Central
Sulawesi, exotic fish species likely contributed
to the threat imposed on those endemic fish
Malili Lakes alien fishes
523
communities, including species extinctions
(Kottelat 1990, 1992; Kottelat et al. 1993;
Whitten et al. 2002). Unfortunately, much of the
public is unaware that the Malili Lakes habitat is
a unique freshwater biodiversity “hotspot” and
that its existence is threatened. Moreover, studies
estimating the impact of species introductions on
the ecosystem are lacking.
Here, we provide records of alien fish species
in the Malili Lakes area, including the recent,
rapid spread of a cichlid (family Cichlidae) in
Lake Matano, known in the ornamental fish trade
by various names, mainly flowerhorn, Luohan or
Kirin cichlid (Nico et al. 2007; Ng and Tan
2010). Flowerhorns constitute a man-made
hybrid complex, reportedly composed of parental
species of the neotropical cichlid genera
“Cichlasoma”, Amphilophus and Paraneetroplus
(Vieja) (Nico et al. 2007; Ng and Tan 2010;
McMahan et al. 2010). Flowerhorns are named
for their distinctive head shape and vivid
colours, and have become popular aquarium fish
over the last decade. Recently, cichlid hybrids
originating from aquarium flowerhorn stocks
have been reported as invasive aliens in several
Asian countries (Nico et al. 2007; Knight 2010;
Ng and Tan 2010). We confirmed that flower-
horns have established proliferating populations
in Lake Matano, and also document that this
invasive hybrid has rapidly spread along the
lake’s coast defending new territories and
feeding on the local endemic fauna, including
fishes. Our data clearly demonstrate that this is a
successful invasion and a serious threat to the
lake’s biodiversity. In addition, we present
updates and records of 13 other alien fish species
recorded since 2000 during field work in the
Malili Lakes watershed; however, none of the
other alien fish species so far approaches the
rapid increase of population density and speed of
flowerhorn dispersal observed in Lake Matano.
Material and methods
Study area
The tropical Malili Lakes consist of three main
lakes, interconnected by small rivers, and two
small satellite lakes connected by peripheral
streams (Figure 1a). Lake Matano (Figure 1b) is
the hydrological head of the system (Brooks
1950). It is the eighth deepest lake in the world
(590 m deep), and unique among the tropical
ancient lakes due to its very low productivity and
correspondingly crystal clear waters (Crowe et
al. 2008a, 2008b). Lake Matano’s effluent is the
high-gradient River Petea that flows to Lake
Mahalona. From there, the flow continues more
gently to the largest water body of the system,
Lake Towuti, which drains to the sea.
Field work
Alien fish species were recorded between 2000
and 2012 in various field campaigns (November
2000, October to December 2002, January and
February 2003, January to May 2004, October to
December 2004, November 2006, January 2007,
June to August 2010, September 2012). Field
work focused mostly on Lake Matano, covering
sites around the lake’s shoreline, but also
included sampling in lakes Towuti, Mahalona,
Lontoa and Masapi, as well as most of the
permanent streams and rivers of the system.
Sampling and visual surveys were conducted
using SCUBA- and snorkelling-aided gillnetting
(6 and 8-mm mesh size), a DEKA 3000 portable
electrofishing device, cast netting, dip netting,
beach seining, angling, observations by
snorkelling and SCUBA diving, and underwater
video recording. Catches of local fishermen were
incorporated if clearly related to a specific
locality.
Abundances and distribution of flowerhorns
within Lake Matano were recorded during focal
investigations from June to August 2010 at 134
sampling locations distributed equally around the
lake’s shoreline (see Figure 1b for sampling lo-
cations). This approach covered different habitat
types with varying substrates, up to 13 m depth.
Abundances were estimated by a single observer
(J.P.) based on 5 minutes of standardized snorke-
lling observation in the following categories:
absence (no single individual observed); low
abundance (<10 individuals observed), medium
abundance (<20 individuals observed); and high
abundance (records exceeding 20 individuals). In
2012, this approach was repeated in a brief
follow-up survey, at a few selected sites mainly
near the northern shore.
Material and species determination
Collected voucher specimens were sedated and
euthanized in chlorobutanol (1,1,1-trichloro-2-
methyl-2-propanol), then preserved either in
70% ethanol or in 4% formalin, and later
transferred to 70% ethanol for storage. To deter-
mine diet we examined the stomach contents of
F. Herder et al.
524
Figure 1. (a) Map of the Malili Lakes system (including associated streams), Central Sulawesi (Indonesia), showing location records for 13
non-native fish species from 2000 to 2012. (b) Map of Lake Matano showing sites where flowerhorn cichlid were captured or observed in
2010 and 2012, based on 134 sampling locations covering the shoreline at 500 m intervals in 2010 and nine locations re-visited in 2012.
Maps by T. von Rintelen, modified (with permission).
Malili Lakes alien fishes
525
15 flowerhorn cichlid specimens from five
sampling locations. Food items between the
oesophagus and pylorus were embedded in
Gelvatol (Polyvenylalcohol) or stored in 70%
ethanol. Food items were identified to the lowest
feasible taxonomic level, and their relative
volumetric proportion was estimated for each
specimen (see Herder and Freyhof 2006 for
details).
Voucher specimens of the flowerhorn cichlid
and most of the other alien fish species recorded
are stored in the collections of Research Centre
for Biology, the Indonesian Institute of Sciences
(LIPI, formerly the Museum Zoologicum
Bogoriense – MZB 21239-21246), Cibinong,
Indonesia, and Zoologisches Forschungsmuseum
Alexander Koenig, Bonn (ZFMK 48849-48852;
ZFMK 48854-48859; ZFMK 48865-48871;
ZFMK 48874-48875). Alien fish species, with
the exception of the flowerhorn, Colossoma sp.,
and Pseudotropheus (Melanochromis)
cyaneorhabdos were determined following
Kottelat et al. (1993). Assignment of walking
catfish specimens to Clarias batrachus remains
tentative (thus: C. cf. batrachus), and positive
identification will not be possible until clariid
systematics and taxonomy are resolved (see Ng
and Kottelat 2008). The determination of the
suckermouth armored catfish as Pterygoplichthys
pardalis follows Page and Robins (2006); the
key character is the colouration, including a
pattern of unconnected dark spots on a light
background on the underside.
Identification of the swamp eel, Ophisternon
cf. bengalense, was based on obvious external
characters: fin reduction, absence of pectoral and
pelvic fins, characteristic habitus of the head
with small, fused ventral gill opening; and was
later confirmed by voucher specimen
examination (ZFMK 48851). Abbreviations used:
TL - total length, from snout to distal tip of
caudal fin; SL - standard length, from snout to
end of hypural plate.
Results
Records, observations and stomach content
analyses of the flowerhorn cichlid in Lake Matano
Specimens of the invasive cichlid were
determined to be flowerhorns, following Nico et
al. (2007) and Ng and Tan (2010). Breeding
pairs and numerous juveniles were first recorded
in June 2010 at the southern shore of Lake
Matano (western Soroako: Salonsa Beach).
Flowerhorns were subsequently recorded at 38 of
the 134 sampled sites visited in 2010, all along
the lake’s southern shore (Figure 1b). The
species occured in mostly medium to high
abundances along the shoreline area from
-2,46701667; +121,23238333 to -2,53843333;
+121,41291667 (Figure 1b). Within this
distribution, flowerhorns were rarely observed in
soft-bottom bays, likely indicative of a less-
preferred macrohabitat. However, soft-bottom
habitats do not represent barriers to flowerhorns,
as its 2010 range included several predominantly
muddy or sandy shoreline habitats (compare the
detailed habitat map in T. von Rintelen et al.
2010). In September 2012, flowerhorns were also
recorded at all five locations visited at the
northern shoreline, and were also present at the
lake’s outlet to River Petea (D. Haffner, pers.
comm.).
Flowerhorns were not recorded during earlier
field campaigns (see Material and Methods);
however, they were observed in two local
aquarium pet shops of Soroako, the main city at
Lake Matano in 2004 and 2006 (F.H., pers. obs.).
Both shops held various alien fish species, with
one of the shops located directly above a small
channel (a former stream) draining directly to
Lake Matano, just a few dozen meters from the
present-day harbour. In 2010, we found this part
of the town restructured, with the shop gone,
including all fishes. We also recorded adult
flowerhorns in a small park pond in Salonsa, the
western part of Soroako (J.P. and F. H., pers.
obs.).
In Lake Matano, flowerhorns were found from
the shoreline out to >13 m depth. Territories of
adults were associated mostly with hard substrate
such as rock or coarse gravel, which they
aggressively defend. All stages of reproduction
were observed, including clutches of eggs
deposited on the surface of stones within
territories, clouds of juveniles of various sizes
guarded by parental fish, and schools of
immature individuals found mostly in the
shallow lake habitats.
One immature specimen (about 7 cm total
length) was observed feeding on eggs of the
endemic goby Glossogobius matanensis, a
species that deposit their eggs on rocks (F.H.,
pers. obs.; see Figure 3). The cichlid seemed to
ignore the guarding male goby (which was
approximately three times the cichlid’s body
length), and fed for at least 10 minutes on the
F. Herder et al.
526
Figure 2. Lateral view of an adult
flowerhorn cichlid (approx. 15 cm
SL) taken from Lake Matano on June
16, 2010. The fish was photographed
in the field immediately after capture.
Figure 3. A flowerhorn cichlid feeding
on eggs of the endemic goby
Glossogobius matanensis in Lake
Matano. The clutch consisted of
numerous small, yellowish eggs (yellow
arrow) deposited on a rock in approx.
0.8 m depth, guarded by the male goby
(black arrow).
eggs, without significant interruption. The
feeding disturbance also attracted another egg-
eating fish (sailfin silversides, Telmatherina
sarasinorum; see Figure 3); and ultimately the
entire clutch was destroyed. We also captured an
adult flowerhorn and adult sailfin silverside
(Telmatherina antoniae “small”; see Herder et
al. 2006b for a species overview). When placed
together in a bucket, the flowerhorn immediately
attacked and consumed the smaller silverside.
Stomach content analyses of 15 individuals
show that flowerhorns in Lake Matano prey on
endemic fauna, including atyid shrimps, a
gecarcinucid crab, and hydrobioid gastropods
(Figure 4). One stomach contained fish remains,
most likely a fish of the genus Telmatherina. The
record of a gecarcinucid crab is based on a single
leg, of approx. 20 mm length, found in the
stomach of one flowerhorn, which suggested the
fish ingested only part of a larger crab specimen.
Records of other alien fish species in the Malili
Lakes drainage
Besides the invasive flowerhorn, 13 additional
alien fish species have been recorded by the
Malili Lakes alien fishes
527
Figure 4. Stomach
contents (in percent) of 15
flowerhorn cichlid taken
from different sites in
Lake Matano. Values on
the x-axis are standard
length (cm) of each
individual fish. Molluscs
(hydrobioid gastropods)
are the most prominent
content in flowerhorn
stomachs, but shrimps,
fish and their eggs, crabs,
and insects are also
represented in the diet
spectrum
Table 1. Frequency distribution of fin spines, lateral bars and the midline blotch of 15 flowerhorn cichlids (same individuals as used for
stomach content analyses).
Number of anal-fin spines Number of dorsal-fin spines
7 8 Mean SD 16 17 18 Mean SD
n=13 11 2 7.15 0.1 3 8 2 16.92 0.18
Number of lateral bars Midline blotch on 4th bar
7 8 Mean SD Present Absent
12 1 7.08 0.08 13 0
authors in the Malili Lakes drainage since 2000
(Appendix 1). These included members of the
families Anabantidae (1 sp.): Anabas testudineus
(Bloch, 1792); Aplocheilidae (1 sp.): Aplocheilus
panchax (Hamilton, 1822); Channidae (1 sp.):
Channa striata (Bloch, 1797); Cichlidae (2 sp.):
Oreochromis mossambicus; Pseudotropheus
cyaneorhabdos (Bowers & Stauffer, 1997)
(Maingano population) - see Konings & Stauffer
(2012) for generic classification); Clariidae (1
sp.): Clarias cf. batrachus (Linnaeus, 1758);
Cyprinidae (1 sp.): Cyprinus carpio (Linnaeus,
1758); Loricariidae (1 sp.): Pterygoplichthys
pardalis (Castelnau, 1855); Osphronemidae (2
sp.): Trichopodus (Trichogaster) pectoralis
(Regan, 1910); Trichopodus (Trichogaster)
trichopterus (Pallas, 1770); Poecilidae (1 sp.):
Poecilia reticulata (Peters, 1859); Serrasalmidae
(1 sp.): Colossoma macropomum (Cuvier, 1816);
and, Synbranchidae (1 sp.): Ophisternon cf.
bengalense McClelland, 1844.
Many of the alien species records were found
to be associated with sites strongly affected by
human activity, especially around the towns of
Soroako (Lake Matano) and Timampu (Lake
Towuti). All alien species recorded were present
in Lake Matano, followed by eight species in
Lake Towuti and two in Lake Mahalona. The
snakehead Channa striata was the only
introduced species found in Lake Masapi, where
it is extremely abundant. Six non-native species
were present in streams and rivers. Two species
(Channa striata, Clarias cf. batrachus) are
comparatively large predators and pose a
potential threat, even for adult native fish and
crustaceans.
Throughout the period of study, we frequently
observed juvenile Channa striata packed live per
dozen in plastic bags at local markets for
stocking purposes, reflecting the potential for
introduction into the wild. Ponds and ditches
stocked with C. striata were found in the
flooding area of River Petea (outlet Lake
Matano) and close to several streams draining
into the lakes (Figure 1; F. Herder, pers. obs.).
Specimens of all size classes were observed in
all lakes, most of them in areas close to human
settlements. Extremely high population density
F. Herder et al.
528
was observed in Lake Masapi: according to local
people this is the result of direct stocking. Even
a small and very remote lake in the hills north of
Lake Matano, far from the closest human
settlement, was found to contain many C. striata,
most likely introduced by local loggers. Like C.
striata, juveniles of the walking catfish Clarias
cf. batrachus are widely available for stocking
purposes in Sulawesi, and live adults marketed
as popular food fish. The same applies to the
climbing perch Anabas testudineus, likely
introduced to Lakes Matano, Mahalona and
Towuti, and present also in surrounding streams.
The swamp eel Ophisternon cf. bengalense was
not abundant at any of the field locations visited,
but present down to 20 m depth in Lakes Matano
and Towuti, a notable finding for an air-
breathing species.
A single specimen of the sailfin catfish
Pterygoplichthys pardalis (Figure 1a) was
captured in 2 Sept. 2012 at south-western Lake
Matano, in a habitat characterized by mud and
rocks at 14 m deep (A. Indermaur, pers. comm.).
This site is located few hundred meters from
some forsaken aquaculture cage facilities; the
fish was about 40 cm long and in very good
condition.
Tilapia of the genus Oreochromis were
commonly observed in small aquaculture ponds
of the region, often connected to natural streams.
Shoals of Oreochromis and their sand bowers
(“breeding craters”), are common in Lake
Matano and present at different depths.
Likewise, catches of tilapia marketed at
Timampu originated, according to local
fishermen, from Lake Towuti. Tilapia are also
frequently available at the local fish market of
Soroako (Lake Matano). However, many of the
Oreochromis observed within Lake Matano
appeared to be in poor condition, judging from
their disproportionally large head size and
emaciated bodies.
There are indications for infections of
indigenous fishes with fungi: Oryzias matanensis
and Telmatherina and Glossogobius species in
Lake Matano, as well as Tominanga in Lake
Towuti. These infections are uncommon in the
Malili Lakes, and are largely associated with the
occurrence of introduced fish species near the
large towns of Timampu and Soroako, but also in
remote areas where (forsaken) fish cages or
aquaculture ponds are present (e.g. at Lake
Matano, S2 28.458, E121 15.570). In Lake
Mahalona, introduced Anabas carried fish louse
(Argulus sp.), a non-indigenous fish ectoparasite.
Discussion
Introduction, dispersal and potential impact
of flowerhorns in Lake Matano
The introduction of flowerhorns into Lake
Matano is likely of very recent origin. This
hybrid was not observed during intensive field
sampling campaigns conducted prior to 2010.
Therefore, it appears that the initial introduction
does not date further back than approximately
2005. The most likely sources are possible
releases during the closing of local aquarium pet
shops, or by local aquarists. Based on the
assumption that only a single or a few releases
took place, most likely in the Soroako area, and
the 2010, approx. 21 km distribution area along
the lake’s southern coastline, we estimated that
the rate of expansion of this cichlid along the
coast has been about 6 km of shoreline per year.
Given roughly constant rates of dispersal, we
expected the two invasion fronts to meet at the
lake’s northern shore around 2013. Flowerhorns
were, however, even faster. In September 2012,
they were present at each single location visited,
including several sites at the lake’s northern
shore. All of these sites harboured mixed
populations of immature and mature
flowerhorns, including several brooding pairs,
indicating that population expansion is still in
progress.
Natural habitat heterogeneity in the lake
appeared at first glance to possibly decelerate the
cichlid’s dispersal, as most specimens were
observed associated with rocky habitats. The
2010 distribution roughly corresponded to the
borders of predominantly soft-bottom areas in
the west and east of the lake; however, the soft-
bottom bay at the town area of Soroako did not
prevent dispersal, and the 2012 distribution
demonstrated that soft-bottom habitats do not
form a barrier for these fishes in Lake Matano.
In addition, the wide array of habitats
successfully used by flowerhorns in Lake
Matano and elsewhere (Knight 2010; Ng and Tan
2010) raises the question if the River Petea
constitutes an effective downstream barrier
preventing cichlid dispersal to the lower lakes,
and rivers and streams in the Malili lakes system.
Stomach content data and observational
records are consistent with an expected
omnivorous diet, similar to that of related
cichlids (Nico et al. 2007). Although the diet of
only a few specimens (n = 15) were examined,
representatives of all major animal radiations
Malili Lakes alien fishes
529
native to Lake Matano were found to be preyed
upon by flowerhorns, including gastropods,
shrimps, crabs, and fishes. Admittedly, cichlid
predation is likely affecting different members of
the native species flocks unequally. In the case
of the hydrobioid gastropods, only some of the
shells were crushed, a pattern also observed in
stomach content samples of the endemic sailfin
silversides (Pfaender et al. 2010) and likely a
result of the gastropod’s minute size. In
summary, stomach content data and field
observations support the notion that the
flowerhorn cichlid is a highly opportunistic
predator, which is consistent with published
records from other cases in Asia where
flowerhorns or the closely related “Cichlasoma”
urophthalmus are invasive (Nico et al. 2007;
Knight 2010). In addition, competitive
interactions with nearly all of the highly
specialized endemic lake fish species (Pfaender
et al. 2010, 2011) appear likely.
Given the apparent preference of flowerhorns
for hard substrate, such as rock or coarse gravel,
native species inhabiting such habitats are likely
most susceptible to predation by this invasive
fish. Fish species most likely to be affected are
those brooding on open rocks, such as
Glossogobius gobies, and those specialized on
foraging in rocky or gravel habitats, such as
Telmatherina sp. “elongated” or T. sp. “thicklip”
(Herder et al. 2006b). In contrast, native species
that inhabit habitats less preferred by
flowerhorns, predominantly soft substrate
habitats or even open waters, are likely less
affected such as sailfin silversides of the
“roundfin” clade, especially the highly abundant
Telmatherina antoniae “small”. The implications
for the lake’s ecosystem, including its
invertebrate radiations, remain to be studied in
detail.
Records of other alien fish species
in the Malili Lakes drainage
Most of the alien fish species recorded in the
Malili Lakes system are commercially valuable
and popular food fishes. Their introduction
appears related to intentional stocking, or to
escapees from aquaculture ponds or enclosures.
Anabas testudineus, Channa striata, Clarias cf.
batrachus, and the gouramis Trichopodus
pectoralis and Trichopodus trichopterus are air-
breathing species with exceptional tolerance of
transport conditions, and consequently are
transported, marketed and introduced throughout
Southeast Asia (Kottelat et al. 1993; Berra 2007
and references therein). Their native
distributions are considered to be restricted to
Asia west of Wallace’s line, and therefore those
populations found in Sulawesi are considered
introduced (Kottelat et al. 1993; Berra 2007).
Anabas, Channa and Clarias are moreover
known for their resistance against droughts and
their ability to disperse even across short
stretches of land (Dutta and Munshi 1985;
Kottelat et al. 1993). Anabas testudineus (as A.
scandens) and Channa striata (as Ophiocephalus
striatus) had been reported for Lakes Matano,
Towuti and Poso nearly one hundred years ago
by Weber (1913), supporting the hypothesis of
introduction by early settlers (Larson and
Kottelat 1992).
In contrast to the rather small and omnivorous
Anabas and Trichopodus, Channa striata and
Clarias cf. batrachus are comparatively large
predators, and potentially pose a serious direct
threat to indigenous fish, crustaceans, and even
amphibians. Kottelat (1990) discussed the strong
population decline in Lake Poso’s (Central
Sulawesi) species flock of ricefishes in
association with (among other factors) the
introduction of alien fish, including Channa and
Clarias. However, in the Malili Lakes, we found
Channa mostly in shallow habitats characterized
by dense vegetation or wood, or among large
boulders, suggesting that their impact might be
restricted to species inhabiting these habitats.
We also did not find indications of a noteworthy
increase in Channa population densities within
Lake Matano over the last decade, indicating that
Channa might - at least currently - not pose a
major threat in this lake. Likewise, records of the
walking catfish, Clarias cf. batrachus, in Lake
Matano are comparatively rare so far, but
specimens were also observed in depths
exceeding 5 m, suggesting that a broad range of
lake species might be affected by this nocturnal
predator.
Like Channa and Anabas, the snakeskin
gourami Trichopodus pectoralis as well as the
three spot gourami Trichopodus trichopterus
typically inhabit shallow habitats with dense
vegetation, such as rice field ditches, where
these fish feed on small invertebrates. This
habitat type occurs in the Malili Lakes region
predominantly near towns or villages, reflecting
increased nutrient levels. Trichopodus pectoralis
was observed exclusively in such habitats,
possibly due to repeated introductions from
ponds or rice fields. The closely related T.
F. Herder et al.
530
trichopterus was reported earlier by Kottelat
(1989) from Lake Matano, but actual records are
restricted to one site in Lake Matano and two
sites in Lake Towuti (Figure 1a). The record in
Lake Matano is a shallow, polluted beach site
with unusual macrophyte growth, where it co-
occurs with abundant T. pectoralis, Anabas
testudineus and Oreochromis mossambicus. The
two sites in Lake Towuti appeared however not
visibly disturbed.
Swamp eels like Monopterus and Ophisternon
are also able to breathe atmospheric air, are
commonly marketed live, and occur widespread
in local aquaculture (Kottelat et al. 1993; Berra
2007). Information on swamp eels in Sulawesi is
scarce (T. Roberts, pers. comm.), and their
taxonomy needs to be updated (Allen et al.
2002). Here, we follow T. Roberts (pers. comm),
Berra (2007) and Allen et al. (2002) in
tentatively assigning the Ophisternon found in
the Malili Lakes to O. bengalense, a taxon
distributed from the Indo-Malaysian region to
New Guinea (Berra 2007). We follow Kottelat
(1991) and Whitten et al. (2002) by assuming
that swamp eels are likely not native to the
Malili Lakes drainage, but introduced for
aquaculture purposes; however, further
investigations are required to test this
assumption.
The common carp, Cyprinus carpio, and the
Mozambique tilapia, Oreochromis mossambicus,
are not air-breathers, but nevertheless
extraordinarily resistant to hypoxic conditions.
As valuable food fish, both species have been
used extensively for aquaculture purposes
throughout Asia, including programs for
increasing fisheries productivity by stocking in
natural waters; neither is native to Southeast
Asia (Berra 2007). According to the local district
governor, tens of thousands of C. carpio have
been stocked regularly in Lake Towuti. These
stockings explain sightings in Lake Towuti,
some kilo-metres away from Timampu, as well
as the pre-sence of fresh adult individuals in fish
markets in Timampu and Soroako. Cyprinus
carpio has also been recorded in Lake Matano, is
known to change the habitat by digging up the
sediment, and may pose a direct threat to eggs
and fry of indigenous fish species. Moreover,
common carp can be assumed to feed on native
invertebrates, aufwuchs and plants. However,
and contrary to its invasive potential
demonstrated elsewhere (e.g., Koehn 2004),
there are as yet no indications for successful
reproduction of C. carpio in the lakes, and there
are also no signs of dispersal to the other lakes
or streams.
Tilapias (e.g., Oreochromis niloticus, and
various hybrids) were widely introduced
throughout tropical freshwaters as a potential
human food source. As such, they have become a
major pest in freshwaters throughout the tropics
(Lowe et al. 2000), with significant impacts on
evolving species flocks (Canonico et al. 2005;
Strecker 2006). Oreochromis mossambicus feed
mainly on plant matter (Allen et al. 2002), and,
in contrast to C. carpio, have been observed
breeding within the Malili Lakes (F. H. and
S.M.G., pers. obs. 2002, 2003, 2004). Coupled
with substantial resistance against hypoxia and
high temperatures, the species’ parental care and
low habitat stenotopy explain the globally
invasive character of this valuable food fish
(Allen et al. 2002; Berra 2007). Interestingly,
many of the O. mossambicus observed in Lake
Matano, at different sites and over several years,
were in poor condition, possibly indicating
resource limitation for these species in this
ultraoligotrophic lake (Haffner et al. 2001;
Crowe et al. 2008a; Vaillant et al. 2011).
However, this does not apply to all specimens
recorded, and was also not observed in Lake
Towuti. Moreover, the situation might change
with increasing nutrition in the lake’s ecosystem,
in addition to contemporary evolution triggering
local adaptation of introduced fishes (Lee 2002).
The blackfin pacu Colossoma macropomum
from South America is another non-indigenous
food fish species introduced to Asian waters,
including parts of China, Taiwan, Singapore,
Bangladesh, the Philippines and Indonesia (FAO
Fisheries and Aquaculture Department Database;
10-2011). Weighing up to 30 kg, it is mainly
herbivorous, generally feeding on fruits, seeds,
and leaves. The Pacu is known as very resistant
to diseases, but not much information is
available regarding its impact on native faunas.
The present record of a single specimen caught
in Lake Matano dates back to 2000 (see also
Parenti and Soeroto 2004).
The sailfin or suckermouth armored catfish
Pterygoplichthys pardalis from the Amazon
basin is the most recent exotic fish species
discovered in Lake Matano. At least three
species of the genus are invasive in Southeast
Asia, including Taiwan, Thailand, Vietnam, the
Philippines, Singapore, Malaysia, Java and
Sumatra (Page and Robins 2006; Levin et al.
2008). Local people reported that sailfin catfish
have also been caught elsewhere in Lake Matano
Malili Lakes alien fishes
531
in the recent past, suggesting that the species is
spreading in the lake. This record adds Sulawesi
to this list of countries or islands affected by
invasive Pterygoplichthys; we expect that the
species might also disperse downstream to Lakes
Mahalona and Towuti. Ecological and economic
effects reported from invasive sailfin catfish
elsewhere comprise environmental degradation
and ecological disruption, including degradation
of banks and siltation problems in reservoirs and
streams caused by burrowing and tunnelling
behaviour, competing with native species for
food resources, and additional unexpected
interactions such as attaching and grazing on the
bodies of other aquatic animals (Nico and Martin
2001; Page and Robins 2006; Levin et al. 2008;
Nico et al. 2009). Competition for limited
resources might be critical for some of the
endemic animals in the ultraoligotrophic and
potentially resource-limited (Vaillant et al. 2011)
Malili Lakes ecosystem; siltation may pose
additional threats especially to the highly
adapted invertebrate fauna (von Rintelen et al.
2012).
The guppy Poecilia reticulata and the blue
panchax A. panchax have both been widely
introduced for mosquito control, and are also
used as aquarium pets (Berra 2007). Aplocheilus
panchax is native to parts of Sulawesi, but we
tentatively assume that it is not native to the
study area. This species is tolerant of increased
salinity (Lim and Ng 1990), and may have
crossed Wallace’s line naturally (Parenti and
Louie 1998; Whitten et al. 2002; Berra 2007).
Nevertheless, A. panchax has mostly been
observed at sites in the Malili Lakes modified by
human activity, mainly polluted swamps or
inshore habitats close to major settlements.
Guppies are widely available in the local
aquarium trade in Sulawesi and the Malili Lakes
region, and present in urban ditches and streams
draining to Lake Matano. The species is not
especially effective in controlling mosquito
numbers, at least on a broad scale, but it has had
marked negative impacts on native fishes and
certain invertebrates (see Kottelat et al. 1993 for
comments).
Introductions of both Pseudotropheus
cyaneorhabdos, a species endemic to East
African Lake Malawi (Maingano population),
and flowerhorns, likely resulted from release of
pet specimens. The record of P. cyaneorhabdos
is based on a single observation (by S.G. and
J.S.M in Feb. 2004). The fish was caught and
removed from the lake.
Prospects and recommendations
The number of alien fish species recorded for the
Malili Lakes system is almost certainly
incomplete. There are likely many unreported
cases of other species that have either failed to
become established or others that are present but
remain undetected. Nevertheless, the diversity of
alien fish species recorded shows that there is a
huge likelihood for harmful introductions into
this unique and naturally isolated lake system.
However, most of these introductions have, in
line with expectations derived from theory and
other fish invasions (Britton et al. 2011), so far
not resulted in massive invasions, and one of the
species recorded by earlier investigators has
apparently not established stable populations
(Appendix 1). Nevertheless, presence of
obviously stable populations of alien predators in
the lakes, such as snakehead or walking catfish,
warrants careful monitoring.
The present case of the flowerhorn cichlid
invasion demonstrates the speed at which a
successfully invading species can establish
across a lake, and our data highlight its threat to
the native fauna. Attempts at population control
through targeted harvesting unfortunately appear
neither realistic nor promising given the
flowerhorn’s high fecundity in this very sensitive
aquatic environment (Zipkin et al. 2009). The
challenge remaining is to monitor its impact
carefully, with an emphasis on preventing the
colonization of the other Malili Lakes. Well-
studied species invasions, such as the Nile perch
disaster in Lake Victoria, or the direct and
indirect impacts of alien fish on the Cyprinodon
species flock in Yucatan (Mexico) (Strecker
2006), have shown the destructive potential
arising from such introductions.
Endemic fishes of the Malili Lakes also likely
suffer from diseases and parasites introduced
with alien fishes. So far, observed infections
related to alien fish vectors are restricted to a
few cases, but fish diseases and parasites can
spread rapidly and have seriously affected other
species flocks (e.g. Strecker 2006), including
lake radiations in Central Sulawesi (Kottelat
1990; Whitten et al. 2002).
To date, we cannot fully assess the impacts of
the flowerhorn invasion, neither for the
environment with its endemic species flocks, nor
for the people exploiting it. The fishes of the
Malili Lakes are traditionally used for
subsistence fisheries (Haryani 2006), which are,
however, of limited capacity due to the
F. Herder et al.
532
ultraoligotrophic character of the lakes (Haffner
et al. 2001). Nevertheless, the stocks of the
large, predatory Glossogobius gobies, the most
valuable indigenous food fishes of Lake Matano,
are likely among those species most affected by
the flowerhorns due to the gobies’ spawning
sites on open, hard substrate (Figure 3). In line
with this expectation, non-quantitative
observations by the first author in September
2012 revealed extremely low abundances of
Glossogobius at all sites visited, an observation
standing in stark contrast to their abundances
observed in 2002, 2004, 2006 and 2008). Of
similar economic importance, stocks of the
colourful endemic Caridina shrimps exported as
aquarium pets will also likely suffer from cichlid
predation.
The majority of native species in the Malili
Lakes drainage face many threats, primarily due
to habitat loss and pollution. Because many are
endemic to very restricted geographic ranges and
few in number, these species are especially
vulnerable (von Rintelen et al. 2012). The
introduction of more and more invasive fishes to
the Malili Lakes exacerbates the existing threats
to native organisms. Actions to prevent further
species introductions are urgently needed, a
seemingly simple step towards developing
sustainable use of these unique lakes. Authorities
and agencies should be aware that production of
exotic freshwater fish species poses a very high
risk for species loss by introducing invaders in
this hotspot of freshwater biodiversity. For the
long-term maintenance of the Malili Lakes
ecosystem and its endemic species radiations, we
strongly recommend prohibition of stocking,
culture of exotic fish species in fish cages, and
other releases of freshwater organisms into
natural waters of the lakes’ drainage. We also
recommend accompanying programs raising
local awareness of the endemic fauna, and the
creation of a regular monitoring program, tasked
with providing the baseline data for future
control and management.
Acknowledgements
We thank the Indonesian Institute of Sciences (LIPI) and
Kementerian Riset dan Teknologi Republik Indonesia (RISTEK)
for the permits to conduct research in Indonesia. PT. INCO / PT.
VALE Indonesia Tbk., provided outstanding logistic support in
Sulawesi. Fieldwork benefited from logistic support in Indonesia
by T. von Rintelen. For invaluable assistance in the field we thank
A.F. Cerwenka, S. Chapuis, J. Frommen, J. Herder, M.
Milanovic, A.W. Nolte, J. Schwarzer and F. Tantu. We are
grateful to T. Lepel for identifying the Pseudotropheus species,
and to T. Roberts for determining the Ophisternon. A. Indermaur
and W. Salzburger caught Pterygoplichthys in L. Matano; D.
Haffner reported flowerhorn occurrence at L. Matano’s outlet. We
acknowledge T. von Rintelen for providing access to digitized
maps. Fieldwork was funded by several research grants (to U. K.
Schliewen: DFG SCHL 567/2-1, 2, 3; to F. Herder: DFG HE
5707/2-1; to J.S. McKinnon NSF RUI 9981638; ARCBC 2001-
2003 to S. Wirjoatmodjo). Three anonymous referees helped to
improve the manuscript.
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Malili Lakes alien fishes
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Appendix 1. List of alien fish species reported from the Malili Lakes drainage, including their English and Indonesian common
names, their native distribution and their most recent record.
Family Species English name Indonesian name Native
distribution
Latest
record
Anabantidae Anabas testudineus (Bloch, 1792) climbing perch Betok, Puyu, Oseng from India to
Taiwan, SE Asia this study
Aplocheilidae Aplocheilus panchax (Hamilton,
1822)
tinhead, blue
panchax Kepala Timah India, SE Asia this study
Channidae Channa striata (Bloch, 1797) chevron snakehead Gabus, Ikan Salo India, China, SE
Asia this study
Channidae Channa lucius (Cuvier, 1831) forest snakehead Runtuk Sundaland,
Indochina
Kottelat
(1989, 1991)
Cichlidae artificial hybrid flowerhorn cichlid Lou Han Neotropics this study
Cichlidae Oreochromis mossambicus (Peters,
1852) Mozambique tilapia Mujair, Tilapia Africa this study
Cichlidae Pseudotropheus cyaneorhabdos
(Bowers & Stauffer, 1997) Maingano cichlid not available East Africa: L.
Malawi this study
Clariidae Clarias batrachus (Linnaeus,
1758) walking catfish Lele
India, Indochina,
Sundaland,
Philippines
this study
Cyprinidae Cyprinus carpio (Linnaeus, 1758) common carp Mas, Karpers
Central Asia,
Japan, widely
distributed
this study
Loricariidae Pterygoplichthys cf. pardalis sailfin catfish Bertulan Sejati
South America
(Amazon River
basin)
this study
Osphronemidae Trichopodus (Trichogaster)
pectoralis Regan, 1910 snakeskin gourami Sepat Siam, Janggo Thailand this study
Osphronemidae Trichopodus (Trichogaster)
trichopterus Pallas, 1770 three spot gourami Sepat Sundaland,
Indochina this study
Poecilidae Poecilia reticulata Peters, 1859 guppy Seribu
Northern South
America this study
Synbranchidae Ophisternon cf. bengalense
McClelland, 1844 swamp eel Belut
Indo-Malaysian
region to New
Guinea
this study
Serrasalmidae Colossoma macropomum (Cuvier,
1816) blackfin pacu Ikan bawal hitam South America this study
