Invasive Acacia mearnsii De Wilde in Kunming , Yunnan Province , China : a new biogeographic distribution that Threatens Airport Safety

Acacia mearnsii De Wilde is on the top 100 of the world’s most invasive alien species and has successfully invaded many areas around the world. However, its distribution and expansion is seldom reported in China. This study for the first time conducted a survey on the new distribution of A. mearnsii at the Kunming Changshui Airport (Yunnan Province, China), through monitoring on population characteristics (number, density, height and ground diameter) and spatial distribution (spread distance). Our survey results show that A. mearnsii has spread rapidly across the airport. This study discusses three factors of environmental factors, human disturbance and weed characteristics behind this successful invasion. The species invasion has a strong potential to change the local vegetation structure, enhances the probability of bird strikes at the airport, and is vulnerable to invade new biogeographic regions if it is not controlled. Currently, eradication combined with mechanical control is considered to be the best option for control. Our study helps improve awareness about the potential risk of A. mearnsii invasion in other airports around China and the world.


Introduction
Invasive plant species are increasingly threatening biodiversity and ecosystem functioning around the world.They are often referred to as naturalized alien (exotic or non-native) plants that establish and maintain their population by self-reproduction and self-diffusion at considerable distances from the parent plants, and have become harmful species, to some extent, or have had a negative influence on humans (Lamarque et al. 2011;Pyšek et al. 2004;Richardson et al. 2000).These species are characterized by easy establishment, fast growth and high propagule pressure (Dodet and Collet 2012).
Acacia mearnsii De Wilde (black wattle) is native to Australia, and is listed as being among ''100 of the world's worst invasive alien species" by the World Conservation Union (Lowe et al. 2000;Luque et al. 2014).The species has already been disseminated globally for more than 150 years owing to its multiple uses (e.g., leather, resins, fuel, paper, medical applications, etc.) (Castro-Dièz et al. 2011;Richardson et al. 2011).The Global Invasive Species Database (GISD) reported the species has become an invasive problem in France, India, Israel, Italy, New Zealand, Portugal, Reunion, South Africa, Spain, Uganda and United States.Its invasiveness threatens the native environment by competing with indigenous vegetation, replacing grass populations, and reducing native biodiversity, which causes large economic losses to these regions (http://www.issg.org/database).
In the 1950s, A. mearnsii was first introduced into China for afforestation and commercial forestry (Fu 2005;Griffin et al. 2011).However, after that, the expansion of this species was seldom reported in China.In recent years, a few studies reported that 10 provinces in China have already recorded A. mearnsii (including Yunnan Province) (Cai et al. 2009;Feng et al. 2010;Fu 2005;Ke et al. 2010;Li et al. 2007).However, there is not sufficient evidence to show A. mearnsii has turned into an invasive species in these provinces.
At the Kunming Changshui international airport (here after referred to as Changshui airport), Yunnan, China, we discovered that A. mearnsii populations have appeared by self-renewal in recent years.The trees attract many birds to rest on them, which increases the opportunities for bird strike at the airport (Gallagher et al. 2011;Gibson et al. 2011;Li 2014;Li et al. 2011;Xu et al. 2011).We undertook an A. mearnsii invasion survey, which is the first time in China that a detailed monitoring investigation of this species has been performed.The aims of this study were thus to determine: (1) could A. mearnsii become an invasive species in China, especially in areas with similar climates (such as Kunming); (2) what are the potential risks of A. mearnsii invasion at the airport where bird strike prevention measures are needed to ensure flight safety; (3) which effective management options can be adopted for the treatment of A. mearnsii invasion?

Acacia mearnsii
Acacia mearnsii belongs to the Mimosaceae (affiliated to the Leguminosae), and is a heliophile, evergreen, nitrogen fixing, fast growing tree species.A detailed description is provided by De Wit et al. (2001) and Sherry (1971).The species grows in disturbed, mesic habitats and thrives in a range of climates, including warm temperate dry climates and moist tropical climates (http://www.issg.org/database).Duke (1983) reported that it can tolerate an annual precipitation of between 660-2280 mm, an annual mean temperature of 14.7-27.8°C, and a pH of 5.0-7.2.The GISD says that it does not grow well on very dry or poor soils, however, Crous et al. (2012) reported that it is highly drought-tolerant, able to withstand low minimum water potentials, and can utilize a large proportion of soil water.

Study area
Changshui airport is located in the north-eastern part of Kunming (the capital city of Yunnan Province) (Fig. 1a, b).It is the fourth largest airport in China.It handles 20 million passengers each year and has 275 routes to 134 cities, such as Beijing, Shanghai, Singapore and Paris.The total area of Changshui airport is 22.97 km 2 , its functional units are composed of an airport terminal, two runways (East and West), grass-planting area and the planning area (area for future development) (Fig. 1c).The grass-planting area of the airport was established in 2012 where grassy herbaceous plants (mainly graminoid) are cultivated.The airport is surrounded by farmland, secondary forest and villages.It is located in a subtropical semi-humid monsoon climate zone, with an average temperature of 15 °C and an average precipitation of 1035 mm.The climate features are quite similar to the original habitats of A. mearnsii in Australia (Duke 1983;Fu 2005;Gao and Ren 1989; http://www.issg.org/database).

Survey method
The pilot survey in early 2013 showed that A. mearnsii seedlings mostly had appeared in the grass-planting area near two gutterways and the planning area within the airport.Considering flight safety, the airport authority approved the use of the grass area around the west gutterway as our sample area.In this context, we conducted 12 surveys, twice a month, in the sample area from June 2013 to November 2013.Two line transects along the gutterway (6.2 km long, see Fig. 1c) in west grass-planting area were established.Quadrat plots (5 × 5 m) were used as the secondary unit for surveys, with a 100 m interval between each plot.The number, height and ground diameter of A. mearnsii were recorded in each plot.The dispersal rate was also estimated by measuring the diffusion distance of new seedlings of A. mearnsii along two transects during the survey period.

Invasion of A. mearnsii
The A. mearnsii populations first appeared in the south side of the west gutterway in May 2013 and spread slowly.In the following months when rainfall became abundant (i.e., July and August), the spread of A. mearnsii increased rapidly and most of them formed into relatively dense populations.They then also appeared in the north side of the west gutterway in August.Fig. 2 shows the extent of A. mearnsii invasion within the grassplanting area near the west gutterway.In the south side of gutterway, there were 400 m of A. mearnsii populations through the initial measurement in June.The diffusion rate was fastest in August, and the distance increased up to 1100 m with 400 m of these new seedlings.The diffusion continued to the west of the gutterway with 200, 300 and 200 m, respectively, from September to November.During the whole study period, the black wattle seedlings had totally spread to 1800 m with an average rate of 300 m per month.In the north side of gutterway, the new population distribution of A. mearnsii with 200 m was measured in August, and spread with 150 m to both ends of the gutterway in September.The last increase with 100 m in east side of the gutterway was found in October.August it reached the highest density peak.The average density of A. mearnsii was 1-3 plants/m 2 .In the denser areas, it was up to 10 plants/m 2 , and the area had begun to resemble a wood.Fig. 3(c) shows the average sample heights were 19-47 cm.Most of the trees in the survey area were over 1 m high and the maximum height of A. mearnsii was up to 1.35 m in August.Fig. 3(d) reflects the mean diameter (ground diameter) of A. mearnsii, which ranges from 2.2 cm to 3.56 cm, and some seedlings increased their diameter more than 10 cm.

Local invasion rate
Our investigation clearly demonstrates a successful invasion of A. mearnsii in the grassplanting area near the west gutterway at Changshui airport.The invasions have also appeared in other sites of the airport, such as in the grass-planting area near east gutterway and in the planning area of the airport.The data also show that the black wattle had an extraordinary pace of expansion at the survey area, which was reflected in the diffusion distance and in the population characteristics.The population overall diffused to 1800 m in the south side of the gutterway from June to November and 450 m in the north side of the gutterway from August to November.Population features (such as number, density, height and ground diameter) showed that the species had a very high growth rate.They increased dramatically in June and reached the peak in August, then decreased after 3 months, which exactly corresponds to the pattern of local rainfall.It should be note that these increased growths are partially flatted or slowed down by human disturbance.In order to prevent bird strikes, the frequent pruning works are practiced by airport staff and they clean up the larger and higher plants artificially at the airport, including many A. mearnsii seedlings in our survey area.However, despite this pruning, A. mearnsii populations still showed a rapid diffusion over the grass-planting area near the gutterway of the airport.With such a trend, A. mearnsii would become woodland in the near future and the whole grass-planting area of airport would be threatened.

Possible factors affecting invasion success
Explanations for A. mearnsii invasions have received attention in some studies (Dodet and Collet 2012;Donaldson et al. 2014;Lamarque et al. 2011;Low 2012).We identify a number of factors that are possible for the successful invasion by A. mearnsii at the Changshui airport, and group them into environmental factors, human disturbance and weed characteristics.Dodet and Collet (2012) highlighted that invasion may become effective only when environmental conditions allow the species to express their potential for invasion.In this case study, the land claimed as the airport were villages, farmland and planted forests (including planted black wattle forests) prior to the con-struction of the airport in 2007, which probably resulted in extensive A. mearnsii seed banks that were spread and concentrated in the grass-planting area and in the planning area.Secondly, the species is highly adapted to the habitat because it has similar climate conditions to its natural habitat, which leads to high growth performance and an ability to become the dominant population.Thirdly, the on-going flight activities can take more seeds of A. mearnsii into the airport environment, either by flight flows or human/plane attachments.Meanwhile, interference by construction activities enhances invasion ability of A. mearnsii, because it can help break seed dormancy underground.Finally, the weedy characteristics are also key drivers of invasive success (Gibson et al. 2011;Low 2012), such as long-lasting inflorescences, a variety of dispersal pathways, the ability to re-sprout and germinate in abundance following disturbance, and high growth rates.All result in the emergence of a large number of tree seedlings after environmental adaptation in grass-planting area at the airport.However, uncertainty still remains as to the relative importance of environmental factors and species traits when determining the propensity of A. mearnsii at the Changshui airport to become invasive, and this needs to be further studied.

Risk assessment and management implications
Acacia mearnsii grows quickly and spreads rapidly in our study area.The species can radically change local vegetation structure, such as converting grass-planting area into woodland, or even forest (if there are no control measures) with this single dominant species.In addition, woodland or forest could enhance bird abundance and increase the probability of bird strike events (Li et al. 2010;Liao et al. 2012;Sandström et al. 2006;Tilghman 1987;Xu et al. 2011), which have been upgraded to an "A" class air disaster risk by the FAI (Federation Aeronautique Internationale).The detailed study of bird abundance for Changshui airport in 2013 showed there were 34 bird species often stay on or around the A. mearnsii trees, including Passer montanus, Carduelis ambigua, Alauda gulgula, Motacilla alba, and Ardeola bacchus (Bird Strike Prevention Office of Kunming Changshui International Airport 2013; Li 2014).In this context, invasions by A. mearnsii species will pose a potential threat to bird strikes at the airport.
The whole grass environment at the airport is vulnerable to invasion by the current population of black wattle if it is not controlled, and the populations will continue to spread or invade new biogeographic regions.Therefore precautionary risk assessment and adaptive management towards this species in the study area should be undertaken so that the negative impact and harm can be limited.At the airport, the A. mearnsii populations are in the early stages of invasion, and appropriate mix of available management methods should be employed to maximize their effect.So eradication combined with mechanical control is an effective option at current stage (van Wilgen and Richardson 2014).This is helped by the fact that the tree populations are localized and the trees themselves are kept in small.For the stages when trees grow up, mechanical control before flowering and seed maturity should be adopted to eliminate their further dispersal.Finaly, promoting education and awareness of the dangers of A. mearnsii invasion is also needed to prevent further expansion of this species in the region (van Wilgen and Richardson 2014).

Conclusions
This study has shown that A. mearnsii has successfully invaded areas inside Changshui airport.The populations continue to spread at a rapid rate, and may invade new areas and change local ecosystem.Furthermore, the rapid distribution of A. mearnsii poses an increased threat to airport flights.These results imply that eradication, combined with an education program, need to be proposed.The rapid invasion of A. mearnsii at the study area highlights the potential risks to other airports in tropical and warm temperate areas of China or around the world.We therefore suggest detailed monitoring and assessment of A. mearnsii species should be carried out in these regions.

Figure 1 .
Figure 1.Location map (a, b) and the main functional units of the Changshui airport (c).
Population characteristics of A. mearnsii Plot-average data are shown in Fig. 3. Fig. 3(a) shows the average number of A. mearnsii species each month during the survey period.The population number reached a maximum in August, and the average number of trees per plot was 37 and the maximum number was 268.Fig. 3(b) shows the average sample density.Similarly, In

Figure 2 .
Figure 2. The distribution of A. mearnsii in the grass-planting area near the west gutterway at Changshui airport (June-November 2013).

Figure 3 .
Figure 3.The population characteristics of A. mearnsii on mean population number (a), mean population density (b), mean population height (c) and mean population ground diameter (d) for plots in the west transect sampling area at Changshui airport.