Risk and benefit assessment of alien fish species of the aquaculture and aquarium trade into India

16 Pages·2011·0.61 MB·English

ReviewsinAquaculture(2011)3,3–18 doi:10.1111/j.1753-5131.2010.01039.x
Risk and benefit assessment of alien fish species of the
aquaculture and aquarium trade into India
Atul K. Singh and Wazir S. Lakra
NationalBureauofFishGeneticResources,Lucknow,UttarPradesh,India
Correspondence Abstract
AtulK.Singh,NationalBureauofFishGenetic
Resources,CanalRingRoadPODilkusha, There has been an increasing demand for alien fish species in India. However,
Lucknow-226002,UttarPradesh,India. environmental, socioeconomic and biodiversity issues are important consider-
Email:[email protected] ations when regulating the unauthorized culture and spread of alien species.
Information collected in the present review revealed the presence of over 300
Received19January2010;accepted alien species imported intentionally or illegally; 291 ornamental species, 31
19November2010.
aquaculture species and two larvicidal fishes. Field data demonstrated the wide-
spread occurrence of some of the world’s worst invasive species, for example,
Cyprinus carpio, Oreochromis niloticus, Aristichthys nobilis, Pygocentrus nattereri
and Pterygoplichthys spp., in inland waters; other species are emerging as a
threat to aquatic biodiversity. The benefits and risks of alien species were analy-
sed and the impact was quantified using a simple developed ‘Fish Invasiveness
Screening Test’ (FIST). Our information suggests that alien species, despite
possessing some attractive culture characteristics, generally reduce the availabil-
ity of local species and establish in natural water bodies becoming invasive and
consequently adversely affecting fish biodiversity and aquatic ecosystems. In
light of the adverse ecological impacts of alien species, we developed strategic
regulations and quarantine procedures and advised aquaculturists to strictly
follow them to contain potential and plausible menaces.
Keywords: alienspecies,culture,impactassessment,invasiveness,risks,unauthorizedculture.
global aquaculture production (De Silva et al. 2009). Over
Introduction
the past decade, alien finfish species have accounted for
India is endowed with a rich aquatic biodiversity of over over 12.2% of total cultured finfish production and the
2319 finfish species, which includes 838 freshwater, 113 proportion is as much as 35% when China is excluded
brackish water and 1368 marine fishes (Kapoor et al. (De Silva et al. 2006, 2009).
2002; Lakra et al. 2009). As these captive fishery resources Alien fish species are non-native or exotic fishes that
are stagnating or declining, advancement in the aquacul- occur outside their natural ranges and have dispersal
ture sector has been taking place to provide nutritional potential. Alien fish species have been brought into India
security. Thus, aquaculture is becoming increasingly intentionally or otherwise for the purposes of aquacul-
important in developing countries, particularly as it can ture, aquarium trade, therapeutic value, research and bio-
provide an affordable source of food and a nutritional logical control (Singh & Lakra 2006; Lakra et al. 2008). In
diet to rural poor (Delgado et al. 2003). To augment fish addition, to alien aquaculture species, over one billion
production, a number of alien fishes have been intro- ornamental fish comprising more than 4000 freshwater
duced for aquaculture purposes throughout the world and 1400 marine species are also traded internationally
(De Silva et al. 2006, 2009) and such occurrences are each year, making it one of the most important compo-
common even today (Naylor et al. 2001; Lakra et al. nents of the global fish trade (Whittington & Chong
2008; Turchini & De Silva 2008). The mean yearly cul- 2007; European Commission 2008). In India, hundreds
tured alien freshwater finfish production from 2000 to of alien ornamental species form part of the aquarium
2004 amounted to 3.6 million tonnes or 16% of the trade (Lakra et al. 2008). The role of alien species in
ª2011BlackwellPublishingAsiaPtyLtd 3
A.K.SinghandW.S.Lakra
aquaculture and the ornamental trade has not yet been and two species of larvicidal fish used for malaria control.
properly addressed in India. The collected and generated information on the historical
Inland aquatic biodiversity offers several potential cul- perspective of deliberate or illegal introductions are
tivable species for aquaculture development and also for presented in Table 1.
aquarium purposes (Ghosh et al. 2003; Lakra et al.
2009). There have been incessant efforts to diversify
Food fishes
aquaculture through alien fish species in India in recent
years; total fish production has grown nearly 12-fold in The historical information on alien fish species and the
the past five decades and stands at 6.9 million tonnes, of purpose as well as the places where they were originally
which 3.2 million tonnes is from the inland sector (Kat- introduced to were generated from secondary sources and
iha et al. 2005). Over the past two decades, many alien also through field studies and interaction with aquacul-
fish species have been clandestinely brought into India turists, scientists and state fishery officials. The informa-
by private aquaculturists, entrepreneurs and aqua-indus- tion compiled on the historical perspective of alien
trialists for immediate gains. Such unauthorized activities species in India is summarized and presented in Table 1.
are causing indiscriminate spreading of alien species, Trout was the first alien fish introduced back in 1863
with potentially adverse ecological consequences (Singh by the British for angling purposes. Rainbow trout,
& Lakra 2006; Lakra et al. 2008). The use of aquatic Oncorhynchus mykiss (Waulbaum 1792), and brown trout,
alien species in aquaculture and in the ornamental fish Salmo trutta fario (Linnaeus 1758), were two important
trade is of increasing occurrence because of the social aquaculture species in upland waters, although other alien
and economic importance of the fishery and aquaculture species of trout were brought into the country. Atlantic
(Ross et al. 2008; De Silva et al. 2009). The unregulated salmon, S. salar (Linnaeus 1758), was available in the
transboundary movement of aquatic alien species into trout hatcheries of Kashmir in 1960, but failed to estab-
India in recent times has invited serious attention from lish. In the cold Himalayan region, brown trout is now so
scientists and policy makers (Singh & Lakra 2006; Lakra well established in Jammu and Kashmir State that the
et al. 2008). In this review, we have endeavoured to col- State is credited with some of the best trout streams in
lect scientific information on alien species in India and Asia. Some streams in Himachal Pradesh are known for
to assess the pros and cons of such introductions. At rainbow trout (O. mykiss) and several kilometres of the
present, the status of alien fishes involved in aquaculture tributaries of the Beas River are frequented by anglers
and in the aquarium trade in India is not available. and support a lucrative recreational fishery. More
Whatever information on alien fish species exists, in recently, these species have been re-established in the
India, it is scattered and available only in the form of states of Uttarakhand, Arunachal Pradesh and in the
so-called ‘grey’ sources (i.e. reports, popular science Nilgiris in Tamil Nadu. Over the past decade, the devel-
magazines and newspapers). We have attempted to gen- opment of infrastructure (hatcheries and farms) and
erate and synthesize information in order to update the human capacity coupled with the establishment of feed
status of alien fish species. Effort has also been made to mills has given a new thrust to the commercial produc-
document the historical perspective of the unauthorised tion of trout (Vass & Raina 2002). Recently brook trout,
culture of alien fish species under aquaculture and the Salvelinus fontinalis (Mitchill 1814), has also been adopted
aquarium trade and to examine the spread of such alien for aquaculture in the Himachal Pradesh and Jammu and
species in different aquatic environments throughout Kashmir states.
India. This paper is a review of the outcomes of our Tilapia, Oreochromis mossambicus (Peters), was first
efforts over the past 10 years to generate field data on introduced into pond ecosystems in 1952 and thereafter
alien fish species in India and to assess their potential stocked in several reservoirs of south India for production
impacts, in terms of both benefits and risks. This infor- enhancement (Sugunan 1995). Oreochromis mossambicus
mation will provide a scientific basis for evaluations of is abundantly found in almost all reservoirs of Tamil
the entry of a particular alien species into the country, Nadu, Kerala, Andhra Pradesh and in some reservoirs in
restricting the spread of potentially invasive species and Karnataka (Sugunan 1995; Lakra et al. 2008). This species
building up regulatory mechanisms to deal with safe is now found in almost every environment from Punjab
aquaculture activities. to Assam and in the north-east through the Indo–Ganget-
ic plains to down south. In India, four species of tilapia,
O. mossambicus, Oreochromis niloticus, Oreochromis urol-
Historical perspective
epis and Tilapia zilli are available. The first two species
We collected information on more than 300 alien fish O. mossambicus and O. niloticus are predominantly avail-
species; 291 ornamental fishes, 31 aquaculture species able in the country.
ReviewsinAquaculture(2011)3,3–18
4 ª2011BlackwellPublishingAsiaPtyLtd
RisksandbenefitsofalienspeciesinIndia
Table1 Historicalperspectivesandstatusofalienfishspecies(reasonforintroduction,yearandsourceandfromwhere)inIndianaquaculture
Species Reason Year⁄source From Presentstatus
(commonname)
SalmotruttafarioL. Forplantingin 1863,England;1908, Nilgiris(TamilNadu(TN)), Cultivatedandbredin
(Browntrout) reservoirsand Japan HarwaninKashmir(J&K), mostofthehillstates.
lakes Kerala Naturalizedpopulation
existsinuplandrivers,
streamsandlakes
SalmolevensisPickens -do-(cid:2) 1863,England Nilgiris(TN) Limitedoccurrence
(Leventrout) mostlyinTNandJ&K
Onchorhynchus -do- 1909,SriLanka, -do- Widelycultivatedand
mykissWalbaum Germany, bredinmostofthehill
(Rainbowtrout) NewZealand states.Somearefound
inthewild
Salmogairdneri -do- 1867,Europe;1940, Nilgiris(TN),Kashmir, Limitedoccurrence
irideusRanae Englandand Kerala
(Steelheadtrout) SriLanka
Salmogairdneri -do- 1941,England Kerala Limitedoccurrence
shastaRanae
(Steelheadtrout)
Salvelinusfontinalis -do- 1959,2007,Canada -do- Aquacultureofthis
Mitchill1814 speciesisnowpracticed
(Brooktrout) inHimachalPradesh
Salvelinusnamaykush Forplantingin 1968,Japan Nilgiris(TN) Limitedoccurrence
Walbaum1972 reservoirsand
(Splaketrout) lakes
Onchorhynchusnerka -do- 1968,1970,Canada -do- Limitedoccurrence
Walbaum(Sockeye
salmon)
SalmosalarLinnaeus -do- 1968,NorthAmerica Kashmir Limitedoccurrence
(Atlanticsalmon)
CarassiuscarassiusL. Gamefishery 1974,England Nilgiriwaters(TN) Presentatmost
(Goldencarp⁄crusian freshwaterfarms.Some
carp) arealsoavailablein
naturalwaters
CarassiusauratusL. -do- 1974,England OotylakeandNilgiri -do-
(Goldcarp) waters(TN)
TincatincaL.(Tench) -do- 1870,England -do- Presentinthestatesof
TN,Kanataka,HP,J&K
andUttarakhand
Osphronemus -do- 1856,Java Kolkata,WestBengal Presentatmost
gouramiLacepede (WB) freshwaterfarms.Some
(Gourami) areavailableinnatural
waters
Puntiusgonionotus -do- 1972,Indonesia WestBengaland CulturedmostlyinWB,
Bleeker1850 Orissa OrissaandAndaman
(Tawes) andNicobarandare
availableinnatural
waters
Oreochromis -do- 1952,SriLanka; WestBengal, Naturalpopulationofthe
mossambicusPeters 1962,SriLanka (Mandapam,TN) culturedspeciesexistsin
(Mozambiquetilapia) (JaisamundLake) riversandreservoirs
Rajasthan
Oreochromisurolepis Aquaculture Notknown Coastalwatersof Underaquaculturein
urolepisNorman, AndamanandNicobar AndamanandNicobar
1922(wamitilapia)
ReviewsinAquaculture(2011)3,3–18
ª2011BlackwellPublishingAsiaPtyLtd 5
A.K.SinghandW.S.Lakra
Table1 (Continued)
Species Reason Year⁄source From Presentstatus
(commonname)
Cyprinuscarpio Aquaculture 1939,SriLanka; Cuttack Widelycultivated.Itis
communisL. 1957,Bangkok availableinrivers,lakes
(commoncarp) andreservoirs
Cyprinuscarpio -do- 1939,SriLanka; Nilgiris,TN Underaquacultureinhill
specularisLacepede 1957,Bangkok statesandareavailable
(Mirrorcarp) innaturalwaters
CyprinuscarpioBloch -do- 1939,SriLanka; Cuttack,Orissa Underaquacultureinhill
(Leathercarp) 1957,Bangkok statesandareavailable
innaturalwaters
Ctenopharyngodon -do- 1959,Japan, Cuttack,Orissa Widelyculturedandare
idellaVal. HongKong availableinnatural
(Grasscarp) waters
Hypophthalmichthys -do- 1959,Japan, -do- Widelyculturedand
molitrixVal. HongKong someareavailablein
(Silvercarp) naturalwaters
(cid:2)‘-do-’asmentionedinabovecolumn.
Three varieties of the Prussian (German) strain of
Ornamental fishes
common carp, namely the scale carp (Cyprinus carpio
communis), the mirror carp (C. carpio specularis) and The ornamental fish trade in India is dominated by alien
the leather carp (C. carpio nudus) were introduced from fish varieties, such as goldfish, angel, guppy, swordtail,
Ceylon (Sri Lanka) in 1939. Several high altitude ponds oscar, platy, gourami, arowana, piranha, pacu, koi carp
and lakes were stocked with these species in the 1950s. and sucker mouth catfish; these varieties were introduced
Later, in 1957, a Bangkok strain of the common carp and from different parts of the world, but mainly from Asia.
the Chinese silver carp, Hypophthalmichthys molitrix Most of these species are freshwater species, although
(Val.), were brought into the country with the objectives marine aquarium fishes have become popular in recent
of broadening the species spectrum in aquaculture years. However, there are no records or information
and increasing yields through better utilisation of vacant available documenting the timing and⁄or source of these
trophic niches. Of the alien carps, the common carp imported species. The information collected revealed that
(C. carpio var communis) is now widely cultured all over more than 200 alien aquarium fish species are now bred
the country in ponds and is deliberately stocked in lakes in different parts of the country (Ghosh et al. 2003; Lakra
and reservoirs to enhance productivity. Fish are now et al. 2008), mostly in indoor small cement cisterns or
found in several rivers including the Yamuna and the earthen ponds and tanks for supply to the domestic mar-
Ganga (Singh et al. 2010a,b). kets or even for export purposes. The most commonly
Both silver carp (H. molitrix) and grass carp (Cteno- cultivated aquarium species are goldfish (Carassius aura-
pharyngodon idella) were introduced in 1959 for a specific tus and C. carassius), gourami (Trichogaster spp.), koi
purpose and have led to the development of a high yield- carp (Cyprinus carpio), sutchi catfish (Pangasianodon
ing technology, ‘Composite Fish Culture’, after several hypophthalmus), red-bellied pacu (Piaractus brachypomus),
years of experimentation. The grass carp (C. idella) was Piranha (Pygocentrus nattereri), sucker mouth catfish
introduced in 1959, mainly to control weeds in natural (Pterygoplichthys spp.), guppy (Poecilia reticulata) and
water bodies. It is an important species used in ‘compos- Oscar (Astronotus ocellatus). These species are flooding in
ite fish culture’ and is widely cultured throughout India, markets and pet shops.
including in the hill states. Silver barb, Puntius gonionotus
(Bleeker), alternatively known as Barbonymus gonionotus
Larvicidal fishes
is an important species in many south-east Asian coun-
tries (Alam et al. 2004). This species was introduced into The most commonly occurring larvicidal fishes in India
India in 1972 from Indonesia with a view to control are Poecilia reticulata (Peters) and Gambusia affinis (Baird
aquatic weeds (Das et al. 1994). It is mainly cultivated in & Girard). These species were introduced in 1908 and
the West Bengal, Orissa, and Andaman and Nicobar 1928, respectively, to contain mosquito larvae in confined
states. waters. However, the insecticidal value of these species is
ReviewsinAquaculture(2011)3,3–18
6 ª2011BlackwellPublishingAsiaPtyLtd
RisksandbenefitsofalienspeciesinIndia
not well established. These species now occur in several hypophthalmus, Aistichthys nobilis, Oreochromis niloticus
natural aquatic environments in India. and Piaractus brachypomus, have been surreptitiously
smuggled into India and are being cultivated (Table 2).
These unauthorized introductions have achieved popular-
Unauthorized or illegal fish introductions
ity in aquaculture and in the aquarium trade. Some of
Our neighbours, Bangladesh and Nepal, culture a number these alien fish species were widely distributed across
of alien species (Barua et al. 2001; Gurung 2005). Many several states⁄union territories, for example, African cat-
alien species, such as Clarias gariepinus, Pangasianodon fish (C. gariepinus), bighead (A. nobilis) and Nile tilapia
Table2 Illegal and unauthorised culture of alien fish species (reasons for introduction, year and source, and place of original introduction)
inIndia
Species Reason Year⁄source Place Presentstatus Remarks
(commonname)
Oreochromisniloticus Aquaculture Possibly1987 TamilNadu, Commercialculture Governmentconsidered
L.(Niletilapia) fromThailand WestBengal, productionin itsregulatedculture
andIsrael Rajasthan AndhraPradesh. owingtoincreased
Naturalpopulation demand.Adverse
existsinriversand impactperceived
reservoirs
TilapiazilliGervais, Aquaticweed 1986Thailand IndiraGandhi Presentinfreshwater Impactnotperceived,
1848(Redbelly controlin Canal, farmsinadditionto butintroductionwas
tilapia) irrigation Rajasthan theIndiraGandhi unnecessary
systems CanalinRajasthan
Aristichthysnobils Aquaculture 1980Possibly WestBengal Widelycultivatedand Abannedspeciesin
Richard.(Bighead) Bangladesh somearepresentin aquaculture.Significant
andNepal naturalwaters adverseimpact
perceived
Ictaluruspunctatus -do-(cid:2) 1990 Thanjavur(TN) Limitedoccurrence Unauthorizedtrialswere
Rafinesque,1818 WestBengal notsuccessful
(Channelcatfish)
Clariasgariepinus -do- Possibly1994 WestBengal Widelyculturedand Abannedspeciesin
Burch.1822(African somearepresent aquaculture.Significant
catfish) innaturalwaters adverseimpact
perceived
Pangasianodon Aquacultureand Possibly1997 WestBengal Culturedmostlyin Someadverseecological
hypophthalmus aquarium coastalstates. impactperceived.
Sauvage purpose Somearepresent However,government
(Sutchicatfish) innaturalwaters considereditsregulated
culture
Mylopharyngodon Aquacultureand Possibly2005 24(cid:2)NParganas Presentmainlyin Limitedcultureand
piceusRichardson molluskcontrol fromBangladesh ofWestBengal WestBengaland impactnotperceived
(Blackcarp) havenowspread
throughoutnorth
India
Myliopharyngodon Aquaculture Possibly2005 24(cid:2)NParganas Limitedoccurrence Limitedcultureand
idellaRichardson fromBangladesh ofWestBengal impactnotperceived
(Mudcarp)
Piaractusbrachypomus Aquacultureand Possiblyin2004 WestBengal Large-scalebreeding Usedforboththe
Cuvier1818(Pacu) aquarium fromBangladesh inWestBengal aquacultureand
purpose anddistributed aquariumtrade
inAP,Kerala,
north-eastern
region.
Litopaeneusvannamai Aquaculture 2001Probably AndhraPradesh, Underaquaculture Governmenthasnow
Boone1931 fromThailand TamilNadu mostlyin considereditsculture
(Whitelegshrimp) AndhraPradesh underbio-security
(cid:2)‘-do-’asmentionedinabovecolumn.
ReviewsinAquaculture(2011)3,3–18
ª2011BlackwellPublishingAsiaPtyLtd 7
A.K.SinghandW.S.Lakra
(O. niloticus), whereas others were localized in specific of the opinion that this shrimp species has huge potential
regions (e.g. sutchi catfish and red-bellied pacu). Bighead for culture because of great demand in international
carp, a popular aquaculture species in India, was possibly markets. The Indian Government has allowed a small
introduced in 1987 from Bangladesh. It spread quickly number of farmers to culture this shrimp species using
and presently this alien species exists in most areas of specific pathogen free (SPF) stock. Culture and breeding
freshwater aquaculture. Among the catfishes, the African of red-bellied pacu (P. brachypomus) was clandestinely
catfish (C. gariepinus) was clandestinely introduced into started in the state of West Bengal in 2001 and has
the state of West Bengal possibly during 1994 and quickly becomepopular (Lakraet al.2008;Chatterjee& Mazumdar
spread throughout the country, including into cold 2009), particularly in the states of Andhra Pradesh, Kerala,
regions as well as coastal areas. It is largely cultured in Maharashtra and Orissa, and in some areas of the north.
the states of West Bengal and Andhra Pradesh. However,
seed production is mainly practiced in the state of West
Risk assessment
Bengal. Although its culture is unauthorized, these fishes
have become popular among aquaculturists in the coun- Risk assessment of alien fish is one of the core elements
try. Hybrid catfish (C. gariepinus · C. macrocephalus) are for protecting fish biodiversity and food safety today. The
a fast growing variety and hybrid seed is being produced benefits and risks of alien fish species in India have been
in hatcheries in Bangladesh (Baruah et al. 1999; Khan assessed for ecological functions, within which they are
et al. 2000) and then smuggled into the bordering north- embedded. A science-based simple risk assessment proto-
eastern States, Assam and West Bengal and as far as colnamedhereasthe‘InvasivenessScreeningTest’(FIST),
Bihar, forming the basis of a flourishing trade in India. which includes screening of potential biological features
Hybrid catfish are more popular in Punjab and Haryana, such as growth, culture level, history of establishment,
owing to their fast growth. Hybrid catfish are very breeding in the wild, phenotypic plasticity (tolerance to a
inexpensive to feed because recycled chicken and slaugh- range of salinities and temperatures), ability to live off a
terhouse wastes are generally used. Another catfish, wide range of food types, competition with local species,
P. hypophthalmus, has also become popular in aquacul- diseases, dispersal ability (propagule pressure) (Table 3)
ture, particularly in West Bengal and Andhra Pradesh. and other characteristics attributable to invasiveness
This species has also been found in other coastal states (Kolar & Lodge 2001; Kolar & Lodge 2002; Ricciardi &
including Kerala and is used both for aquaculture and Kipp 2008), was used in the present evaluation. The
aquarium keeping; thus, it has spread throughout the cumulative value percentage (CV %) for each screening
country. In India, there was also a trial by Hindustan criteriawasstatisticallyanalysedusingStatistixVersion8.1
Lever to culture the American channel catfish Ictalu- software (Informer Technologies Inc) and a ranking for
rus punctatus (Molur & Walker 1998). This company each criteria was determined based on the CV %. The fre-
imported seed directly from the USA and began cultur- quency distribution percentage value (FD %; +++) of
ing. However, the trial failed to produce the desired screened criteria for each species was calculated. The risk
results. Red tilapia (O. niloticus) was first introduced into level for the assessed species was classified on the basis of
West Bengal and became a popular species in sewage-fed thevaluecalculated forFD%.SpecieswithFD%valuesof
fisheries. Later, Vorion Chemicals brought the species to +++ for overall screened criteria (i.e. above 50%) were
Chennai and cultured it using distillery wastes and classified as high-risk species, species between 30 and 50%
claimed high production of over 50 tonnes ha)1 (Singh & were classified as medium-risk species, and species below
Lakra 2006). However, the project collapsed. Now some 30% were classified as low-risk species (Table 3). The
aquaculturists are demanding the importation of O. nil- potential biological characters of the alien species that
oticus for culture purposes and the Indian Government were attributable to invasiveness were assessed through an
has permitted importation by a couple of entrepreneurs analysis of dietary intake and environmental tolerance and
in Andhra Pradesh. The introduction of Tilapia zilli was also from the history of establishment success (Kolar &
for weed control in the Indira Gandhi Canal in Rajasthan. Lodge 2001; Kolar & Lodge 2002). A lack of data isgener-
This introduction was unnecessary as many locally avail- ally a constraint in risk assessment. Therefore, we also
able weed-controlling species, such as Puntius pulchellus consulted the Database of Introduced Aquatic Species
or even grass carp, were present in the country. An alien (DIAS) (http://www.fao.org/figis/servlet/static?dom=root&
shrimp species, Litopenaeus vennamei (Boon 1931), has xml=introsp_s.xml), a Food and Agriculture Organization
also recently been incorporated into brackish-water (FAO)databaseontheintroductionofaquaticspecies(DIAS
aquaculture, possibly in 2001 (Lakra et al. 2008). Many 2004), Fish Base (http⁄⁄:http://www.fishbase.org), Global
farmers started culturing this alien shrimp species, partic- Invasive Species Database (GISD) (http://www.issg.org/
ularly in Andhra Pradesh and Tamil Nadu. Farmers are database/welcome) and the database on National Biological
ReviewsinAquaculture(2011)3,3–18
8 ª2011BlackwellPublishingAsiaPtyLtd
RisksandbenefitsofalienspeciesinIndia
Table3 Invasivenessscreeningtest(FIST)ofalienfishspeciestodeterminetherisklevel
Invasiveness Speciesinvasivenessassessment Rankingof
screeningcriteria thescreened
criteriabased
1§ 2§ 3(cid:2) 4§ 5(cid:2) 6(cid:2) 7(cid:3) 8§ 9(cid:2) 10(cid:2) 11§ 12§ 13§ CV% onCV%
Culturelevel +++ +++ ++ +++ ++ ++ ++ + ++ ++ +++ +++ +++ 36.4 4
Growth +++ +++ +++ ++ +++ +++ +++ ++ +++ ++ +++ +++ + 63.6 7
Propagulepressure +++ +++ +++ +++ +++ +++ ++ + +++ ++ +++ +++ +++ 81.8 9
(transportation)
Historyofestablishment + +++ + +++ +++ ++ +++ +++ + – ++ ++ +++ 72.7 8
Abilitytoliveoffawide +++ ++ +++ ++ ++ ++ +++ ++ ++ ++ +++ +++ +++ 18.2 2
rangeoffood
Tolerancetotemperature +++ +++ + +++ ++ +++ ++ +++ ++ +++ +++ ++ +++ 100.0 11
Tolerancetosalinity +++ + ++ ++ + + +++ ++ ++ +++ +++ +++ ++ 90.9 10
Tolerancetodissolvedoxygen +++ ++ ++ ++ + + ++ +++ + ++ +++ +++ +++ 54.5 6
Abilitytobreedinthewild + ++ + +++ ++ ++ +++ +++ + + ++ +++ +++ 9.1 1
Competitionwithlocalspecies +++ +++ ++ +++ ++ + +++ +++ ++ ++ +++ +++ +++ 27.3 3
Diseases + ++ +++ + + + + + + ++ + ++ + 45.5 5
Frequencydistribution% 72.7 54.5 45.5 54.5 27.3 27.3 45.5 54.5 27.3 27.3 72.7 72.7 72.7 – –
(FD%)for+++
1, Clariasgariepinus; 2, Aristichthysnobilis; 3, Pangasianodonhypophthalmus; 4, Cyprinuscarpio; 5, Hypophthalmichthysmolitrix; 6, Ctenophar-
yngodonidella; 7, Oreochromisniloticus; 8, O.mossambicus; 9, Piaractusbrachypomus; 10, Litopenaeusvennamei; 11, Pygocentrusnattereri;
12,Pterygoplichthysspp.;13,Poeciliareticulata);CV%,cumulativevalue%;+,low;++,moderate;+++,high.
(cid:2)SpecieswithanFD%for+++below30areconsideredtobelow-riskspecies.
(cid:3)SpecieswithanFD%for+++between30and50areconsideredtobemoderate-riskspecies.
§SpecieswithanFD%valuefor+++above50areconsideredtobehigh-riskspecies.
TheassessedPterygoplichthysspp.werePterygoplichthysperdalisandPterygoplichthysdisjuntivus.
Information Infrastructures in the USA (http://www.
Impact of alien food fishes
invasivespecies.nbii.gov)duringtheriskassessmentprocess.
The risk assessment process covered two major compo- An impact assessment of alien fish species was conducted
nents: ‘probability of establishment’ (i.e. the invasion of for the Yamuna, Ganga and Periyar Rivers, backwaters of
an alien species) and ‘consequence of establishment’ (i.e. Kerala, Jaiselmer Lake (Rajasthan), Ramgarh Lake (Uttar
the impact of alien species). The invasion process was sig- Pradesh) and Kolleru Lake (Andhra Pradesh). The ecolog-
nificantly facilitated by propagule pressure and environ- ical impact of Oreochromis mossambicus, O. niloticus, Pan-
mental factors (e.g. temperature and salinity). The main gasianodon hypophthalmus, Litopenaeus vannamei, Clarias
predictor of establishment for various aquatic alien spe- gariepinus, Cyprinus carpio, Hypophthalmichthys molitrix,
cies depended on propagule pressure, which was the Ctenopharyngodon idella, Aristichthys nobilis and some
number or frequency of alien species released (Fausch ornamental fish species such as Piaractus brachypomus,
et al. 2009) and depended on human interest in any alien Pterygoplichthys spp. and Pygocentrus nattereri, which
species. Hence, unauthorised culture of alien species by commonly occur in culture and breeding, was conducted
public aquaculturists has been burgeoning in recent years. following the risk assessment protocols and approaches. It
Alien species once established often quickly spread is noteworthy that the invasiveness and impacts of some
depending on environmental factors such as temperature alien species are fully apparent within a short timeframe
and salinity (Moyle & Light 1996; Bomford et al. 2010). (within 2 years) in some cases (e.g. African catfish and
Invasive species are alien fishes that can colonize through Piranha), whereas for other species it can take decades
naturally breeding populations or have the potential to (e.g. common carp) (Strayer et al. 2006; Arthur et al.
establish. Such invasive species are mostly capable of 2010; Singh et al. 2010a). We present the overall impacts
causing adverse ecological impacts, although in some of various species below.
cases they do not; for example, there are hardly any Impact assessments of tilapia have shown that it can
reports on the adverse ecological impacts of gold fish make up a substantial part (up to 25%) of the catch in
(C. auratus) and freshwater jellyfish (Craspedacusta sower- many reservoirs of Kerala, resulting in stunting, poor
byi), although these species are known to be invasive growth or even elimination of some indigenous species,
worldwide (Ricciardi & Cohen 2007; Valery et al. 2008). such as the Gangetic carps, Puntius dubius and Labeo
ReviewsinAquaculture(2011)3,3–18
ª2011BlackwellPublishingAsiaPtyLtd 9
A.K.SinghandW.S.Lakra
kontius, in the southern region of the country (Lakra s) 2500
t5eot00all.ges2ys0e0atr8h))a1.nTinh1em0g0arngoywywtehaart)oe1fr CbcohodamniepossaricnehdaTnaowmsitiwhlaNstahrdeeustrwuicshtueeandl ch (tonne 2000 2031 1785 1532
at 1500
tilapia were present. Its prolific breeding habit and paren- c
e
tal care help it to multiply every 3 weeks, causing space ag 1000
er 753
overlap with local species, particularly carps. Tilapia now v
a
form part of the fish fauna in the Godavari, Krishna, al 500
u
n
Cauvery, Yamuna and Ganga Rivers (Lakra et al. 2008). n
A 0
Tilapia and Indian economic local species share a com- 2004 2009
mon food niche, the success of one in competition with
the other can be determined by the ability of this fish to Figure1 Increased occurrence of alien species in the Ganga River
(2004and2009).( )Exotics;( )local.
breed and propagate. Given the propensity of tilapia for
auto-stocking, indigenous species that breed in the eco-
system have to struggle to coexist with tilapia. Released Pradesh. Increased populations of carp in natural water
tilapias as a result of anthropogenic activities tend to bodies have negatively impacted on catches of the local
establish in waters that have deteriorated or in quasi- mahseer species Tor putitora, snow-trout Schizothorax
natural water bodies such as reservoirs, rivers and irriga- richardsonii and some other species, such as carps and
tion systems. The ecological consequences of the invasion catfishes, in different ecosystems (Petr 1999; Singh &
of tilapias and their establishment in such waters bodies Lakra 2006; Lakra et al. 2008). Its over population has
can be serious (Canonico et al. 2005; Lakra et al. 2008). been found to critically reduce the endemic fish species
An interesting example of tilapia invasion was noted from Osteobrama belangiri from Loktak Lake (Manipur) (Singh
Jaisalmund Lake in Rajasthan, where it out-competed & Lakra 2006). It has recently invaded the Ganga River
many local species and resulted in a phenomenal reduc- System after 50 years of existence in pond aquaculture
tion in the average weight of Indian major carps (Lakra (Fausch et al. 2009; Singh et al. 2010a). At present both
et al. 2008). Tilapia was introduced into this lake during C. carpio and O. niloticus have been found to dominate
1988 and started appearing in commercial catches in commercial catches in the Ganga River (Singh et al.
1990. Since 1998 it has constituted more than 90% of the 2010a). Catches of local fishes, particularly Indian major
catch (Lakra et al. 2008). Despite this, the growing popu- carpsand someothers, have declined by 72%at Allahabad
larity of Nile tilapia in aquaculture for food production and Varanasi, whereas the catch of alien fishes (mainly
has attracted some aquaculturists in India who are willing C. carpio and O. niloticus) increased 237.1% in 2009
to culture it mainly for export purposes; it is not in high (Fig. 1). This increasing trend in the catch of alien fishes
demand domestically. Oreochromis niloticus is cultured was noticed from 2004 onwards. A similar phenomenon
in relatively poor quality waters, in sewage-fed ponds in was found in the Yamuna River, where commercial
West Bengal or under commercial culture operations in catches were dominated by the presence of alien fishes,
Andhra Pradesh. Recent efforts to culture Genetically particularly C. carpio, Oreochromis spp. (both O. niloticus
Improved Farmed Tilapia (GIFT) tilapia introduced to and O. mossambicus) and also some C. gariepinus at most
Central Institute of Freshwater Aquaculture (CIFA), sampling stations (Singh et al. 2010b).
Bhubaneswar, and study its performance and prospects Occurrences of common carp, tilapia and African
have not provided any recommendation on its culture catfish in the Yamuna River have been mapped for an
and propagation. approximately 900-km-long river stretch using a Geo-
The common carp (Cyprinus carpio) is a very popular graphical Information System (GIS) tool for the period
fish in aquaculture and has considerably added to the 2003 and 2008 (Fig. 2). Cyprinus carpio, Oreochromis mos-
total yield from pond culture. However, its pond-breed- sambicus and O. niloticus were found to colonize naturally
ing habit upsets the population balance leading to severe breeding populations in this river and the presence of all
competition for food and space, resulting in the produc- reproductive stages was confirmed in our studies. Some
tion of small-sized individuals. Three varieties of common of the river stretches of the Yamuna were full of tilapia
carp (scale carp, leather carp and mirror carp) have only and hardly any other local fish species were caught
formed naturalized populations in rivers, lakes and reser- (Singh et al. 2010b).
voirs (Lakra et al. 2008; Singh et al. 2010a). The naturally Both silver carp (Hypophthalmichthys molitrix) and
bred mirror carp and leather carp have not only been grass carp (Ctenopharyngodon idella) have increased
observed in upland waters, but have also been observed farmer yields and, although not commensurate with their
approximately 200 km downstream in the plains of Uttar income, are still a welcome addition so long as the
ReviewsinAquaculture(2011)3,3–18
10 ª2011BlackwellPublishingAsiaPtyLtd
RisksandbenefitsofalienspeciesinIndia
77°0'0"E 78°0'0"E 79°0'0"E 80°0'0"E 81°0'0"E 82°0'0"E 83°0'0"E 84°0'0"E 85°0'0"E
30°0'0"N Sanaranpur N 30°0'0"N
Y W E
aMuzaffarnagar
m
u
29°0'0"N na Meerut S 29°0'0"N
Ghaziabad
BulandShahar
28°0'0"N 28°0'0"N
Mathura
Firozabad
27°0'0"N Agra Chambal Yamuna Basin 27°0'0"N
YamunaEtawah Ganga Basin
Jalaun
26°0'0"N Benva Fatehpur 26°0'0"N
n
JhansiDhasa Hameerpur KenBanda Allahabad
25°0'0"N 25°0'0"N
Lalitpur
24°0'0"N 24°0'0"N
0 190 380 760km
77°0'0"E 78°0'0"E 79°0'0"E 80°0'0"E 81°0'0"E 82°0'0"E 83°0'0"E 84°0'0"E 85°0'0"E
Figure2 Mapping of the occurrences of alien fish species in the Yamuna River using a Geographical Information System tool. ( ) No data;
( )Cyprinuscarpio,Clariasgariepinus,Oreachromisspp.;( )Cyprinuscarpio,Oreachromisspp.
proportions of the different species are maintained as ture by 24.6%, whereas growth of Catla catla was reduced
suggested to avoid competition with indigenous species by 17.0%. The specific growth rate (% day)1) of C. catla
(Jena et al. 2002). However, in an interesting example, a was also affected and it was less than that of A. nobilis in
few specimens of silver carp escaped into the Gobindsagar the same environment and on the same diet. One major
Reservoir (Himachal Pradesh) during transportation and reason for such an adverse impact could be the indiscrim-
this species has now become the most dominant fishery inate and irregular stockings of bighead in established
in the reservoir, accounting for over 80% of the total composite culture farms. Both C. catla and A. nobilis were
catch (Singh & Lakra 2006; Lakra et al. 2008). The abun- found to occupy the same ecological niche and they had
dant population of silver carp in the Govindsagar Reser- similar feeding habits in the wild. Bighead have the
voir (Himachal Pradesh) and similarly in the Kulgarhi potential to hybridize with C. catla and silver carp
Reservoir (Madhya Pradesh) has changed the trophic (H. molitrix) under farm conditions (Lakra et al. 2006,
structure significantly (Singh & Lakra 2006; Lakra et al. 2008). Its hybrid with silver carp (H. molitrix) is very
2008). These alien carps have further established in many common at many farms (Mia et al. 2005; Singh & Lakra
rivers. Available data suggest that this species possesses 2006). In our field studies, we recorded the occurrence of
invasive characters, such as good survival, growth and 23.6% hybrid stocks of A. nobilis and H. molitrix in cul-
competition with local fishes and is able to establish ture farms. An F hybrid between bighead A. nobilis and
1
breeding populations in the wild. In a field study of 18 silver carp H. molitrix showed beneficial properties in
grow-out farms in a cluster, Aristichthys nobilis negatively terms of growth, food conversion and disease resistance.
impacted the overall average pond production in polycul- However, further uncontrolled hybridization in later
ReviewsinAquaculture(2011)3,3–18
ª2011BlackwellPublishingAsiaPtyLtd 11
A.K.SinghandW.S.Lakra
generations might result in the loss of the acquired bene- fish breedinthewild.Geneintrogression hasalreadybeen
ficial traits (Mia et al. 2005). Invasion of A. nobilis into reported in the local species C. macrocephalus in Thailand
several rivers, reservoirs and lakes has been shown to as a result of escapee C.gariepinus (Na-Nakornet al.2004;
adversely affect the local fishes because it is a voracious Senananetal.2004).Its spread in different aquatic ecosys-
feeder and depends mostly on naturally available plank- tems has negatively impacted on the existence of local
tonic food on which many local fishes thrive (Lakra et al. magur C. batrachus, in addition to other native species.
2008; Sampson et al. 2009). Invasive impacts of this spe- Africancatfishareeasytocultureandseed is readily avail-
cies have also been reported from some countries where able throughout the year. In Western ghat, a biodiversity-
bighead carp (A. nobilis) are reported to form established rich hotspot, farmers culture C. gariepinus over the
natural populations causing adverse ecological conditions endemicyellowcatfish(Horabagrusbrachysoma),whichhas
(Taylor et al. 2005; Sampson et al. 2009). now critically declined (Lakra et al. 2008). African catfish
Aquaculture of Puntius gonionotus is commonly prac- grow fast, culture management is easy and farmers prefer
ticedinWestBengal,OrissaandalsoinAndmanandNic- it to local species. African catfishhave been shown to pos-
obar.Thisspecieshasbeenincorporatedintopondculture sess attractive culture characteristics, such as fast growth
systems and its growth ranges from 200 to 500 g year)1 in (approximately 600 g in 6 months), and acceptability of
differentareas.However,alackofinformationonitscom- cheap feed, such as slaughterhouse and chicken waste.
patibility, growth performance and interaction with local This species is disease resistant and easy to breed. At the
speciesofculturehasbeenamajorlimitationinriskassess- same time it also possesses some characters attributable to
ment. A recent study on the compatibility of silver barb invasiveness, such as survival in different agro-climatic
with other local species used in polyculture reported that conditions,superiorgrowthoverlocalspecies,carnivorous
silver barb had a higher level of competition with Labeo and aggressive behaviour, acceptability of a wide range of
rohitathanC. catla.However,thisspeciesmaybeapoten- feed, including live fish and other aquatic animals, and
tialcandidatespeciesofaquacultureandisapreferredfish attaining maturity in different water bodies. A critically
speciesinpaddy-cum-fishculture(Jenaet al.2007). declining bird, the Moorhen Gallinula chloropus, was
In India, monoculture of African catfish (Clarias garie- recently found in the gut of a 67-cm-long fish caught
pinus) has shown a wide range in growth when integrated from the Bharatpur bird sanctuary in Rajasthan (Anoop
with slaughter house and chicken wastes and improvised et al. 2009). Low culture management practice, tolerance
feed with 40% protein (Singh & Mishra 2001), and pro- of a harsh environment, acceptability of a variety of feed,
duction under monoculture was estimated to range from including slaughterhouse wastes, and fast growth mean
a few kg to over 20 t ha)1 year)1 at different farms (Singh that farmers have begun to culture it in small pits and
& Lakra 2006; Lakra et al. 2008). There was a loss to the cement cisterns as well as in large ponds and reservoirs.
carps in the range of 78.2–86.3% when C. gariepinus was However, this obnoxious predator has become far more
cultured under polyculture with carps (Baruah et al. 1999; inimicaltoindigenousspeciesasithasnowgainedunsolic-
Lakra et al. 2008). An average growth of 1.63 mm day)1 ited entry into mighty rivers, such as the Ganga, Yamuna,
was observed in managed grow-out ponds. This species Sutlej and Godavari, which are the pride of India for their
was found to possess a highly carnivorous feeding habit precious and specific gene pool (Kapoor et al. 2002; Lakra
on live fish, insects, snails, earthworms, plankton, plants et al. 2009). The threat of C. gariepinus and its invasion
and fruits and also rotting flesh. African catfish (C. gari- intoariverinSouthBrazilhavealsobeenreported(Vitule
epinus)exist infishponds, lakes, streams and other natural et al. 2006). Considering the threats posed by African cat-
waterbodies, including river stretches both deep and shal- fish, the Ministry of Agriculture, Government of India,
low. This species tolerates harsh environmental conditions ordered killing of this alien catfish en masse and has
and is distributed over a wide range of temperatures (12– imposed a ban on its culture. However, it is still bred and
36 ± 1(cid:2)C) and salinities (<14 p.p.t.), which is why it is culturedeventodayindifferentpartsofthecountry.
widespread throughout the country. It occurs in coastal Aquaculture of Pangasianodon hopophthalmus has been
areas, freshwater ponds, tanks, lakes, reservoirs, aquatic booming in recent years in the coastal states. This species
bodies of foot-hills in cool environments and even in shows fast growth and can be farmed intensively, thus
some rivers, such as the Godavari, Yamuna, Gomti and attracting aquaculturists. In cases of polyculture with
the Ganga Rivers, with different pristine diversity (Lakra carps it has been shown to harm other local culture spe-
et al. 2008, 2009). African catfish culture has occurred cies. Intensive monoculture of P. hypophthalmus was
in all areas where local C. batrachus naturally exist. found to be associated with heavy disease infestation.
Clarias gariepinus has the potential to hybridize with local Some diseases, particularly haemorrhagic septicaemia,
C. batrachus (Rahman et al. 1995; Sahoo et al. 2003), sug- bacillary diseases, Flavobacterium columnarae and Tricho-
gesting the possibility of genetic pollution when escapee dina, that have been found at a number of farms are a
ReviewsinAquaculture(2011)3,3–18
12 ª2011BlackwellPublishingAsiaPtyLtd