Current State of Knowledge on Invasive and Alien Fauna of Nepal

This study produced a comprehensive list of introduced fauna of Nepal. Of the sixty four species of alien fauna reported, there were seven species of mammals with forty improved breeds of cow, buffalo, goat, sheep and pig, six species of birds with eight breeds of chicken and duck, nineteen species of fish, twenty two species of arthropods including one species of freshwater prawn and twenty one species of insects, nine species of molluscs and one species of platyhelminths. Among reported alien species Achatina fulica, Capra hircus, Clarius batrachus, Cyprinus carpio, Gambusia affinis, Oncorynchus mykiss, Oreochromis mossambicus, Oryctolagus cuniculus, Platydemus manokwari, and Sus scrofa are considered the worst species of the world and listed in ‘100 of the World’s Worst Invasive Alien Species’. The impacts of all these serious animals in Nepal are still to be studied but some problematic species of agricultural pests, freshwater habitat as well as livestock breeds are discussed in this paper.


INTRODUCTION
Several terminologies have been used for alien species such as exotic species, introduced species, non-native species, non-indigenous species and invasive species.The Convention on Biological Diversity (CBD) defines alien species as "species, subspecies or lower taxon, introduced outside its natural past or present distribution; includes any part, gametes, seeds, eggs, or propagules of such species that might survive and subsequently reproduce" (https://www.cbd.int/invasive/terms.shtml).Similarly, IUCN defines alien invasive species as "an alien species which becomes established in natural or semi-natural ecosystems or habitat, is an agent of change, and threatens native biological diversity" (http://www.iucn.org).Not all alien species are invasive; alien species that establish in natural and semi-natural systems and cause negative impacts on those ecosystems, native species and their habitat are classified as Invasive Alien Species (IAS).The impacts of IAS are widely recognized as one of the major factors for biodiversity loss; mechanisms of impact include competition with, and predation on native species, hybridization with native species, changes in ecosystem processes, habitat modification and an increase of pests and diseases (Vitousek et al. 1996, Ruiz et al. 1997, Mack et al. 2000, Crooks 2002, Bruno et al. 2005, Rodriguez 2006), often resulting in a significant loss of native species, decline in ecosystem services and subsequent socio-economic impacts (Pimental et al. 2001, Hulme 2003).
IAS are represented in all major taxonomic groups, such as micro-organisms, fungi, plants, invertebrates, fish, amphibians, reptiles, birds and mammals (Lowe et al. 2000).IAS are introduced by human agencies either accidentally (with trading goods) or intentionally and also in the form of commodities such as livestock, pets, nursery stock, and produce from agriculture and forestry or contaminants (McNeely et al. 2001).
In Nepal, alien fauna have been poorly investigated and relatively neglected in comparison to alien plant species.Budha (2013) produced the first preliminary documentation on alien and invasive alien fauna of Nepal and provided information on twenty seven alien animal species, however, many more species need to be included to produce a more comprehensive list of alien animal species of Nepal and their impact studies are still lacking.This is the first attempt to update baseline information on alien and invasive fauna of Nepal (excluding zoo animals) which also addresses Aichi Target 9 that aims "By 2020, invasive alien species and pathways are identified and prioritized, priority species are controlled or eradicated and measures are in place to manage pathways to prevent their introduction and establishment."The list of alien/ invasive mammals, birds, fish, insects, molluscs and helminthes of Nepal and their impacts will be useful for policy makers, conservationists, educationalists, researchers and students.

MATERIALS AND METHODS
This work was primarily based on field observations, as well as the best available published information.A comprehensive literature review was undertaken to collect data on known alien and IAS in Nepal.Native ranges of species were verified and the year of introduction/first report in Nepal, for each species was documented where data was available.The list of known alien and IAS animal species and their impacts on biodiversity, food security and human health are also discussed.

RESULTS
This study reported sixty four species of alien fauna of Nepal for the first time.These have been grouped into mammals (livestock/feral), birds (including poultry birds, such as chicken, ducks, turkeys, large flightless birds and common pet parakeets), fish, freshwater prawns, insects (primarily agricultural pests and biocontrol agents viz.parasitoids, predators) and one species of flatworm.All introduced animal species are discussed separately in groups, and the complete list is given in Annex 1.

Introduced Insects and Freshwater Prawns
Twenty species of arthropods, including Macrobrachium rosenbergii (giant freshwater prawn) and twenty one species of insects are listed.Among the insects there are eight species of Diptera belonging to two families Agromyzidae and Tephritidae), five species of Homoptera belonging to four families Aphididae (2 species), one species of each family Diaspididae, Margarodidae, Psyllidae; one species of Coleoptera belonging to Chrysomelidae, four species of Hymenoptera belonging to the family Barconidae (2 species), Encytridae (1species) and Apidae (1 species) and two species of Lepidoptera belonging to one species of each family Bombycidae and Gelechiidae (see Annex 1).

Introduced Flatworm
Only one species of flatworm Platydemus manokwari has been reported in Nepal, which is a predator of snails and slugs and considered as one of the worst invasive species worldwide.

DISCUSSION
The status of many introduced alien species has still been overlooked in Nepal.The increasing trend of introducing animals for commercial purposes without an impact analysis has had negative impacts on the local environment and native species.
The raising of livestock is a fundamental component of the Nepalese rural farming system that provides resources for cultivating farmland, as well wool, meat and milk.It has been the second major economic activity which has substantially contributed to household incomes.Out of around 35 percent national GDP contributed by agriculture sector (MOAD 2011/12) livestock products shares 13 percent (Thakuri 2012).Livestock development was initiated in the beginning of the 1950s in Nepal (Shrestha & Pradhan 1995), however the first introduction of Jersey cows dates back to Jung Bahadur Rana regime, who imported the Jersey cows from the UK in the 1850s (www.nlbc.gov.np).Livestock development always remains the government's priority to increase national production.The importing of new animals and bird species has increased over the last few decades viz.introduction of alpaca, ostrich and emu for commercial farming purposes.With increasing livestock business, problem of livestock diseases has also increased significantly.Thousands of outbreaks of Foot and Mouth Disease (FMD), Pests des Petits in Ruminants (PPR), Classical Swine Fever (CSF), have been observed throughout the country (Thakuri 2012).
Feral animals have also created human-wildlife conflict in several places in Nepal.Feral pig Sus scrofa, which was nominated as among 100 of the 'World's Worst' invaders (www.issg.org)was introduced to Nepal in the 1970s by King Mahendra Bir Bikram Shah as a gift from Russia (Chalise 2013).Although, there are no official records available of the exact date of import of this species, it could have been reared in the Royal palace before the King's death in 1972 and later released into the natural forest of the Shivapuri area in the 1980s (HMG/N 1995).According to Chalise (2013) the introduced species has spread in hills from east to west, however, it is a matter of investigation as to whether the introduced wild boar is restricted within Shivapuri area or has spread to other parts of the country.
Fisheries and aquaculture is another priority sector to the government of Nepal to boost fish production.The fisheries sector contributed about one percent in national GDP and three percent in AGDP with a growth rate of over six percent (Mishra & Upadhyaya 2011).Many introduced species viz.salmon, carp, cichlid, tilapia, catfish and aquarium fish have been commercially exploited in different parts of the country in ponds, natural lakes, reservoirs and cold water river streams.The exact number of exotic fish species in Nepal varies according to different authors ranging from eight to eleven species (Shrestha 1994, 2013, Sharma 2008), however, the list of most of the aquarium species has not yet been updated.This paper identified nineteen species of introduced fish species.
Among the insects, the two most commercial species Bombyx mori and Apis mellifera are well established in Nepal.Based on the definition and impact on native bee A. cerana, the European honey bee A. mellifera is considered as an invasive species.

Impacts of Invasive Species
There are many examples of impacts due to IAS across the world, such as evolutionary impacts by altering the evolutionary pathway of native species by competitive exclusion (Mooney & Cleland 2001), niche displacement (Race 1982, Kenward & Holm 1993), hybridization, introgression (Rhymer & Simberloff 1996), predation, and ultimately extinction (Clavero & Garcia-Berthou 2005).But the impact analysis of introduced fauna of many species in Nepal has not yet been fully investigated.
Most of the species intentionally introduced for commercial purposes are livestock and fishery.But impact due to these species has already been noticed in Nepal.The local breed of cow in the far west Nepal, Achhame, is considered as an endangered endemic breed due to its rapidly decreasing population (Mahato & Gorkhali 2011).The lulu cow, which is a local breed from eastern Nepal has been replaced by the Siri breeds (Shah 2010).The introgression of exotic genes into livestock breeds through crossbreeding programmes may lose the genetic polymorphism/diversity of the breeds which may ultimately lead to the extinction of the breeds (Mahato & Gorkhali 2011).Outbreaks of diseases is another serious problem due to such introductions (Thakuri 2012).
The impacts of feral pigs S. scrofa across the globe are discussed in the Global Invasive Species Database (http:// www.issg.org).In Nepal, the introduced S. scrofa is the most problematic wild animal in Nagarjun-Shivapuri National Park, causing human-wildlife conflict.The author observed evidence that the pigs were consuming snails viz.Bensonies spp., Oxytesta spp.and Cyclophorus spp. in the Park and found reduced populations of these snails in the area.
It was reported that there has been a forty two percent reduction of native fish in Begnash lake, Pokhara after the introduction of bighead carp, silver carp and grass carp (Swar & Gurung 1988) and increasing and decreasing trends of production of introduced fish and native fish respectively in Phewa lake (Husen 2014).More than seven species have vanished from Indrasarobar (Swar 1992) and only two native fish species Neolissocheilus hexagonolepis and Nazirator chelynoides remain (Saud & Shrestha 2007).The invasive tilapia fish in Yamuna river eat detritus, filamentous and cellular algae, zooplankton, fish and insects.It has spread to Godavari, Krishna, Cauveri, Yamuna and Ganga river in India (Ganie et al. 2013).Rainbow trout, one of'100 of the World's Worst Invasive Species' (Lowe et al. 2000) has been introduced to 87 countries worldwide (Welcomme 1992) as commercial table and game fish.Rainbow and brown trout have negative impacts on local biodiversity in established areas (Kitano 2004).These two species have been successfully established in rivers and streams in Japan and India (Himachal Pradesh, NW India) (http:// hpfisheries.gov.in).They have caused native fish species to change their foraging habitats by reducing prey species by seventy five percent (Fausch et al. 1997, Nakano et al.1999).In Nepal, they are highly prioritized species for commercial purposes (Gurung 2008) but they are voracious predators and feed on natural aquatic fauna if released into natural water bodies.Budha (2013) noted comparatively rapid growth of unintentionally released rainbow trout in the natural cold streams than in the fish farm in Rasuwa, Nepal.C. batrachus, an air breathing catfish, native to SE Asia (Indonesia), is also one of the 'world's worst invasive species' and has been introduced to several parts of the world, including Nepal.Another catfish is C. garipenius, which is native to Africa is also commercially farmed in Nepal.It has been reported in the natural river system in eastern Nepal, tributaries of Tamor river (Sharma 1999).
The insect pest species cause major problems in agricultural productivity by reducing significant loss of yield, for example the PTM causes thirty to eighty five percent losses of stored potato and the standing crop (Joshi 1989, Lal 1998, Chandla & Verma 1998, Chandel & Chandla 2005), often reached complete loss during heavy infestation if control measures are not applied (NPRP 2004/05, SSMP 2008).L. huidobrensis is a serious pest for the floriculture and vegetable crop industries, where leaf-miner damage directly affects the marketable portion.Many other species emerged as serious problems in agriculture viz. the San José Scale Q. perniciosus, the Leucaena Psyllid and H. cubana.Introduction of A. mellifera in Asia has encountered a number of problems, such as the inter-species transmission of bee pests and diseases (Ahmad et al. 2004), robbing and displacing the native bee A. cerana (Verma 1992).
The giant African snail is another species included in '100 of the world's worst invasive alien species' list.A single pair of snails were released in Calcutta by a British malacologist, William Henry Benson in 1847 (Naggs 1997) and spread to the entire continent.It was likely introduced to Nepal during the 1930s-1940s in eastern Nepal (Budha & Naggs 2008, Raut 1999) and is now established in all Tarai districts of Nepal, including several hill districts, such as Kaski, Parbat, Baglung, Gulmi, Syangjha, Palpa, Surkhet, Chitwan, Dhading, Myagdi and Dang.It is a serious pest of crops, vegetables and fruits in most of the established areas.The rate of spread has been very rapid and it has been considered that one of the main causes of its dispersal in Nepal is due to its attractive shell (Budha & Naggs 2008).
The terrestrial flatworm P. manokwari is another invasive species; feeding upon native snails and earthworms in its introduced range.Terrestrial molluscs are the principal prey in the field (Justine et al. 2014).Author has recently been reported it from Langtang National Park and Nagarjun-Shivapuri National Park (unpublished data).It is still not known how it has been introduced into these areas.

CONCLUSION
Altogether sixty four alien species have been reported in this paper, including twenty one species of insects, which includes commercial insects, pests and biocontrol agents (predator, parasitoid, defoliator, gall insect), one freshwater prawn, one species of flatworm, nineteen species of fish, six species of birds, and seven species of mammals including one feral pig.Out of all reported alien species ten are among the world's worst IAS.Impact studies of most of the invasive species is severely lacking, however, negative impacts on crop yields and native fauna have been documented for some species.