Alien species recorded in the United Arab Emirates: an initial list of terrestrial and freshwater species

Acknowledgements: We would like to thank the H.E. Razan Al Mubarak, Secretary General of EAD for supporting this important work. Thanks to Dr. Piero Genovesi, Chair, Invasive Species Specialist Group (ISSG) for providing valuable input and comments. Abstract: Little is documented on the alien terrestrial and freshwater species in the United Arab Emirates. To address this, an assessment of terrestrial and freshwater alien species was conducted using various techniques such as a questionnaire, fieldwork data, networking with relevant people, and a detailed literature review. The results of the initial assessment show that there are 146 alien species recorded in the following seven major taxonomic groups: invertebrates 49 species, freshwater fish five species, amphibian one species, reptiles six species, birds 71 species, mammals six species and plants eight species. To inform decision makers a full list of the 146 species identified in this assessment is presented.


INTRODUCTION
The United Arab Emirates (UAE) is a federation of seven emirates: Abu Dhabi, Dubai, Sharjah, Ajman, Umm Al Quwain, Ras Al Khaimah and Fujairah that altogether cover an area of approximately 89,000km 2 (which includes offshore islands). The UAE is located in the northern part of the Arabian Peninsula and is bordered to the west and south by Saudi Arabia, Oman to the east and the Arabian Gulf to the north. UAE's climate can be described as hot and dry throughout most of the year, and according to the UNEP classification of dry lands is regarded as hyper arid (Middleton & Thomas 1997). The UAE is a unique case in that its harsh hyper arid climate itself poses a challenge for the survival and establishment of alien species, which are found to be limited mainly to degraded and transformed (e.g., urban) habitats.
Consequently, a project was initiated by the Environment Agency ABU DHABI (EAD) to conduct an assessment of terrestrial and freshwater alien species within the UAE. This was considered an initial step to document the types of species that are nonnative to the UAE and which may pose a high risk to the natural ecosystem if they become established. A sub-regional workshop for western Asia and northern Africa to address alien species and to achieve the Aichi Biodiversity Target 9 (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 http://www.cbd.int/sp/targets/) was held in the UAE in February 2013. This workshop was organized by the Ministry of Environment and Water (which has a federal level mandate covering all seven emirates) to start addressing the issues of invasive alien species (IAS) at a sub-regional level. Within a regulatory framework, management of alien species is required as the UAE is a signatory to the Convention on Biological Diversity (CBD) as per Article 8-In situ Conservation, Part H-Prevent the introduction of, control or eradicate those alien species, which threaten ecosystems, habitats, or species (https://www.cbd.int/idb/2009/about/cbd/). Hence, this paper presents an initial list of known terrestrial and freshwater alien species in the UAE, with the aim to present this knowledge in one list so that any future efforts can be based upon this baseline list shown in Appendix 1. population), means of introduction (known or inferred), year first recorded, possible impacts to environment and control methods (if known); -Section 3: species geographical information, including the native range of a species, UAE recorded distribution, particular Emirate and GPS location (if known); and -Section 4: miscellaneous information such as literature reference(s), website addresses, references and notes.
We received a 30% response to the questionnaires, which is a good response rate for mail and email surveys (see Shough & Yates 2002;Brennan & Charbonneau 2009). As is typical with mail-out/email surveys, not all fields were completed in many instances (e.g., Trenouth et al. 2012). Particular fields that were commonly omitted included the year of introduction, on which very little information was received.

Confiscated species database and terrestrial baseline surveys
A review of EAD's environmental databases to pinpoint further records of alien species was conducted. EAD, which conducts wildlife assessment and monitoring activities, has databases on species distribution mainly native species but occasionally alien species are also recorded. EAD is also the UAE CITES Scientific Authority agency for the UAE at the Federal level and it therefore maintains records of CITES species confiscations within the UAE. The CITES confiscations include occasional records of non-native species which have been collected in the wild such as Ball Pythons Python regius (P. Soorae, pers. obs. 2004). The CITES confiscation records provided some useful data on species collected from the wild which are mainly escapees. Therefore, these two datasets also added to the initial alien species list developed through the questionnaire and literature review. All the species identified through these various methods are illustrated in Appendix A (supplemental material).

RESULTS
A total of 146 alien species were recorded in seven major taxonomic groups as shown in Table 1. The highest number of alien species were birds recorded at 49%, followed by invertebrates at 34%, plants and reptiles and amphibians both at 5%, mammals at 4% and freshwater fish at 3% as shown in Table 1.

Invertebrates Invasion trends & introduction pathways:
The main reports of invertebrate alien species are from the 1990s (one in 1980s) with the majority having an unknown date of first introduction. Almost a third (32%) of the alien species records are listed as 'accidental introductions' with the remainder of 68% having an 'unknown' pathway/vector. There are various terrestrial alien species such as ants, spiders, weevils, slugs and snails that have been recorded within the UAE. The majority of these species, and those that have become naturalized, are mainly found in urbanized and disturbed habitats (Collingwood et al. 1997). The tropical Fire Ant Solenopsis geminata is a Central American endemic and was first recorded from Arabia in the Dubai Emirate, UAE. This species is an aggressive predator and can have a very negative impact on the ecology, by altering the local fauna through both predation and competition for food (Balfour 2003). The presence of Australian Red-back Spiders Latrodectus hasselti has also been recorded from Dubai Emirate (Balfour 2003). In the year 2010, a Red-back Spider collected in Abu Dhabi, has been confirmed as Latrodectus erythromelas by a collaborative study done by the EAD (Saji & Al Dhaheri 2010) (Image 1). These spiders are reported from domestic gardens and further research is required to understand whether these spiders are able to survive within UAE's natural habitat.
The Red Palm Weevil Rhynchophorus ferrugineus is another alien species that is an important insect pest of date palms in the UAE and has widespread distribution in tropical Asia (Murphy & Briscoe 1999). The excessive use Image 1. Red-back Spider Latrodectus erythromelas of insecticides may limit the activity of natural enemies in plantations and thereby the red palm weevil has had a devastating impact in the countries of the Middle East (Murphy & Briscoe 1999). Non-native mollusk species have been recorded such as the southern Flat Coil Snail Polygyra cereolus, a native of Florida, USA, which is present in pest proportions in some lawns and garden environments. The Garden Slug Laevicaulis alte is found in regularly watered landscaped areas and cultivated sites within the UAE and these snails may compete for food with native snails. They are often imported with their nests to the UAE, in agricultural products such as soil, potted plants and compost (Feulner & Green 2003). A number of other non-native pest species have been recorded from imported foodstuffs, fruits and vegetables in the UAE (see Appendix 1).

Freshwater fish
Invasion trends & introduction pathways: Freshwater fish have been recorded since the year 2000 and all listed as 'accidental introductions'. Freshwater ecosystems in the UAE are limited to seasonal rivers in mountainous areas known as 'wadis', and in dams that collect water during the rainy season. A majority of these are located in the northern part of the country. Different Tilapias Oreochromis spp. have been recorded in some wadis and also in dams and other freshwater bodies. In Wadi Wurayah, Fujairah Emirate, the Mozambique Tilapia Oreochromis mossambicus and mainly tropical aquarium fish such as Armored Catfish Plecostomus sp., Shark Catfish Pangasianodon hypopthalmus and Common Carp Cyprinus carpio have been recorded (Smart-Beadsmore et al. 2008;Tourenq et al. 2011). Tilapias have also been recorded in Al Ain City in wadis and other water bodies (Soorae, pers. obs.) (Image 2). Mollies Poecilia spp. are established in irrigation ditches at Ruwayyah outside Dubai City in Dubai Emirate (Feulner 2005).

Amphibians & Reptiles
Invasion trends & introduction pathways: Like the freshwater fish, amphibians and reptiles have only been recorded since the year 2000 onwards with the majority noted between the years 2000 and 2009. A total of 72% of these alien species have been categorized as 'escape from captivity', with 14% as 'accidental introductions' and 14% as having 'unknown' pathways.
In general, amphibians and reptiles do not pose a major threat, as most of the records so far have been of individuals that have escaped from captivity. The Green Toad Bufo viridis, collected in Abu Dhabi City in 2006 (Soorae, pers. obs. 2006) was an obvious released pet or one that had escaped from captivity. Freshwater turtle species can pose a threat in freshwater ecosystems such as the record of a Red-eared Slider Trachemys scripta elegans from Wadi Wurayah, Fujairah Emirate (Tourenq & Shuriqi 2010). A Leopard Tortoise Stigmochelys pardalis was recorded from Bul Sayeef Island, Abu Dhabi Emirate during a routine biodiversity survey in 2008, which was most likely an abandoned pet that was left on this island (P. Soorae, pers. obs. 2008) (Image 3).

Birds
Invasion trends & introduction pathways: The majority of alien bird species records have been between the years 1980 and 2009. Two species have been recorded from 2010 to present. The main pathways are 'accidental introductions' (41%), followed by 'escape from captivity' (34%) and 25% as 'unknown'. The most common alien bird species in the UAE is the Common Mynah Acridotheres tristis and Indian House Crow Corvus splendens. The Ring-necked Parakeet Psittacula krameri (Image 4) and White-eared Bulbul Pycnonotus leucotis are also naturalized within the UAE and seen commonly in urbanized areas (Khan 1993 mecranensis is another widespread species and there is some controversy on whether it was naturally occurring in parts of the Arabian peninsula or whether it is an introduced species as its native range is described as Afghanistan and Iran. This species has nevertheless spread widely in the UAE with greening of roadways and spread of farms, gardens and urban areas . The majority of these avian species are usually found in urban and disturbed habitats. Although Indian House Crows occur in small numbers at the moment, over the years a noticeable increase in the frequency of sighting has been reported, mostly in areas close to human habitation and along the coastal strip (Ryall & Meier 2008). Several thousand house crows are present on Delma Island in the Arabian Gulf but have not fortunately spread to other nearby uninhabited islands that are used by seabirds for breeding. This could be due to the absence of human habitation and roosting trees. In the future with some islands undergoing development, the likelihood of their range extension cannot be ruled out as many offshore islands in the UAE host breeding colonies of several seabird species, many of them regionally and internationally important (Javed 2008).

Mammals Invasion trends & introduction pathways:
Only one out of the six mammal species has a known date of first introduction in 1999 and the other five are unknown. The main pathways are 50% accidental introductions and 50% escape from captivity. The main mammalian alien species is the feral cat Felis domesticus, feral dog Canis familiaris and rodents such as the Black Rat Rattus rattus, Brown Rat Rattus norvegicus and House Mouse Mus musculus. All of these alien species are common in transformed and degraded habitats. These are species that easily spread via anthropogenic activities and are also disease vectors (Shoukry 2001) and very efficient predators of native biodiversity Javed 2008;Javed et al. 2012).
With a worldwide distribution, the Brown Rat is commonly found in towns of the Arabian Peninsula (Harrison & Bates 1991). The House Mouse is found as a commensal species in towns and settlements throughout the UAE. As human settlements expand into previously unsettled areas, new habitat is 'created' for House Mice. Consequently, the population is thought to be expanding its geographic range and increasing in absolute numbers. This species is also found on islands of the Arabian Gulf, such as Zirku and Arzanah, Abu Dhabi Emirate where it constitutes a threat to seabird species of conservation concern (Drew et al. 2003;Javed et al. 2004). In 2014, House Mice were also recorded from Marawah Island, Abu Dhabi Emirate (P. Soorae, pers. obs. 2014). Feral cats and feral dogs have been recorded in some high biodiversity areas via camera traps and these have had a negative effect on biodiversity (P. Soorae, pers. obs. 2015). Feral cats predate on ground nesting birds feeding on eggs and chicks. The native Gordon's Wild Cat Felis silvestris gordoni is threatened by genetic pollution due to interbreeding with feral domestic cats (Aspinall et al. 2005).

Plants Invasion trends & introduction pathways:
The records of alien plant species are from the year 2000 to present and 50% are categorized as unknown pathway, 25% each as accidental introduction and escape from cultivation. One of the main invasive alien plant species in the UAE is the Mesquite Tree Prosopis juliflora, which Image 3. Leopard tortoise Stigmochelys pardalis Image 4. Ring-necked Parakeet Psittacula krameri is introduced from Central America and has spread quite extensively within the UAE. It has also colonized the many wadi environments, which have higher moisture availability, compared to the more true desert environments (El-Keblawy & Rawai 2007;Tourenq & Shuriqi 2010). The Sea-purslane Sesuvium portulacastrum, which is native to Africa, Asia, Australia, North and South America, and the Goat Creeper Ipomoea pes-caprae that is native to South America, have become naturalized in the UAE. These are low risk species widely used for landscaping in coastal areas or where soil salinity is high (S. Sakkir, pers. obs. 2012). The common invasive grass is the Fountain Grass Pennisetum setaceum, which is a native of northern Africa, has been introduced into the UAE as an ornamental grass for its attractive inflorescence and is highly invasive with long-lived wind dispersed seeds making its control extremely difficult. It has been observed in wadis on Jebel Hafeet (S. Sakkir, pers. obs. 2014).

DISCUSSION
On an ecosystem basis (terrestrial versus freshwater) the majority of alien species were recorded from terrestrial environments (95%), and freshwater aquatic species comprised 5% of records (freshwater fish, crocodile, amphibian and aquatic turtle). The majority of alien species have been observed in urban and semiurban habitats and those that have been disturbed by anthropogenic activities. The hyper-arid climate in the UAE ensures that alien species find it extremely difficult to get established in more wild, pristine areas as these are very challenging environments and are mainly inhabited by native species that have become highly adapted to living in these extreme conditions.
The more vulnerable are the freshwater wadi ecosystems in which the UAE's three main native fish species and two species of regionally endemic toads are vulnerable to introduced species such as Tilapia, tropical aquarium fish, aquatic turtles and the amphibian chytridiomycosis fungus that has decimated amphibian populations worldwide (Soorae et al. 2012). This is a priority area for raising public awareness to prevent unintentional releases in these freshwater wadi systems. The main threat on native fish species would be predation, disease introduction and competition for resources. The very low numbers of fish species can be severely impacted by any freshwater alien species becoming established in these fragile ecosystems.
In conclusion this survey has highlighted the terrestrial and freshwater alien species of the UAE and this information will be useful for biodiversity conservation and management within the UAE. It would also be useful in the future to extend such a project to cover the marine environment given the high volume of international shipping in the UAE and the associated threat of alien species introduction through ballast water discharges.
Author Details: Pritpal Soorae is Unit Head of the Terrestrial Assessment & Monitoring unit and works mainly on reptiles, amphibians, alien species and wildlife trade issues. Salim Javed is Manager of the Terrestrial Assessment & Conservation section and his interests lie mainly in avian ecology and telemetry studies. Shaikha Al Dhaheri is Executive Director of the Terrestrial Marine & Biodiversity Sector and has worked on species conservation and ecology as part of her MSc and PhD. Majid Al Qassimi is Director of the Terrestrial Biodiversity Department and is a veterinarian by training and who oversees the large ungulate ex-situ and reintroduction programs. Maher Kabshawi is Unit Head of the Threatened Species and Habitat unit and whose main interest lies in desert plants. Anitha Saji is an entomologist by training and has worked extensively on UAE invertebrates and besides finding new species to science has a wasp named after her. Shahid Khan is an ornithologist who works on avian projects within the Terrestrial Assessment & Monitoring unit. Sabitha Sakkir is a botanist who oversees the botanical side of the Terrestrial Assessment & Monitoring unit and has considerable experience in UAE's desert vegetation and in conducting large-scale ecosystem surveys. Rashid Al Zaabi whose main interest lies in mammalogy, coordinates the mammalian assessment and monitoring activities of the Terrestrial Assessment & Monitoring unit. Shakeel Ahmed is an ornithologist who works both on avian ecology and mammal monitoring and assessment. He also oversees the camera-trapping program. Junid N. Shah holds a PhD in Wildlife Sciences and is an ornithologist by training and has done extensive wild bird monitoring within the UAE and also involved in various biodiversity surveys within Abu Dhabi Emirate. Ahmed Ali has recently joined the Terrestrial Assessment & Monitoring unit and besides working on herpetology is an authority on using drones and other modern technologies for wildlife monitoring and assessment.