Effect of Varying Alternanthera Philoxeroides (Alligator Weed) Cover on the Macrophyte Species Diversity of Pond Ecosystems: a Quadrat–Based Study

Aquatic Invasions (2014) Volume 9, Issue 3: 343–355 doi: http://dx.doi.org/10.3391/ai.2014.9.3.09 Open Access

Proceedings of the 18th International Conference on Aquatic Invasive Species (April 21–25, 2013, Niagara Falls, Canada)

Research Article

Effect of varying Alternanthera philoxeroides (alligator weed) cover on the macrophyte species diversity of pond ecosystems: a quadrat–based study

Anindita Chatterjee* and Anjana Dewanji Agricultural and Ecological Research Unit, Biological Sciences Division, Indian Statistical Institute, Kolkata – 700108, India E-mail: [email protected] (AC), [email protected] (AD) *Corresponding author

Received: 30 October 2013 / Accepted: 3 February 2014 / Published online: 17 February 2014 Handling editor: Vadim Panov

Abstract

This year-long study, covering three main seasons of India, focused on enumerating the effect of varying cover of Alternanthera philoxeroides (alligator weed) on the associated macrophyte species diversity of the littoral region of natural pond ecosystem. A total of 192 quadrats were randomly placed in the littoral region of 12 similar ponds containing varying degrees of A. philoxeroides infestation to estimate A. philoxeroides ‘cover (%)’ and number of associated macrophyte species in each quadrat. Overall, 20 associated macrophyte species, including 16 aquatic/ littoral-associated, 2 non-aquatic species, and grasses and sedges, were found to be present. A. philoxeroides infestation was categorized into 4 cover grades (Grade I-IV) from lowest (no/negligible: <10% cover) to highest (>60% cover). For each season, significant differences in the total number of associated macrophyte species across the 4 A. philoxeroides cover grades were found. A Poisson-regression model showed that for each season, even when the effect of other invasive species was adjusted, the number of associated native macrophyte species in a quadrat decreases significantly with increase in A. philoxeroides cover. A comparison of the quadrat communities between the lowest grade (Grade I) and highest grade (Grade IV) of A. philoxeroides infestation showed a significant reduction of species richness, diversity and evenness from the lowest to the highest infestation grades. Again, Mann-Whitney U tests further revealed that the number of native macrophyte species was significantly lower at highest (Grade IV) A. philoxeroides infestation than that at lowest infestation (Grade I). The presence of multiple invaders in A. philoxeroides infested aquatic ecosystems is also reported, indicating probable facilitative interactions between A. philoxeroides and other invasive species. The socio-economic valuation of some important native plants, which were found to be significantly reduced at high infestation levels of A. philoxeroides, has also been highlighted. Key words: aquatic ecosystems, ponds, quadrat, macrophytes, native biodiversity, invasive species, invasion impacts

Introduction modifications (Vitousek et al. 1997) and worldwide increase in trade and transport (Lockwood The introduction and spread of non-native species 1999) are the leading causes of creation of invasive has become a global ecological and conservation species on a global scale. crisis as invasive organisms are increasingly Aquatic macrophytes are key components of altering terrestrial and aquatic communities world- aquatic and wetland ecosystems (Rejmánková wide, causing catastrophes for the native ecosystems 2011) playing a pivotal role in the ecosystem, (McNeely 2001), leading to biodiversity loss like oxygenation of water (Caraco et al. 2006), (Powell et al. 2011) and local extinction of native productivity and nutrient retention (Engelhardt species (Butchart et al. 2010). Invasive species and Ritchie 2001), providing shelter and refuge may inflict harmful ecological and economic and food (Wetzel 2001) for aquatic macro- impacts upon ecosystems in non native regions invertebrates and other animals. Native aquatic (Pimentel et al. 2005). They can lead towards macrophytes not only form an important source ecosystem degradation and impairment of ecosystem of food and medicine but also provide livelihood services worldwide (Pysek and Richardson 2010), for many marginalised people and are essential thereby inducing high conservation concerns to society (Ghosh 2005). Although freshwater (Wilcove et al. 1998). Direct consequences of recent ecosystems cover approximately 0.01% of the anthropogenic activities like environmental earth’s water, they contain about 6% of all

343 A. Chatterjee and A. Dewanji described species (Dudgeon et al. 2006), have (Erwin et al. 2013; Masoodi et al. 2013) and ponds the highest extinction rates (Jenkins 2003) and (Clements et al. 2011). Assessments of the impacts are under extreme pressure (Michelan et al. of individual invasive species on the native 2010). The problem is compounded by aquatic aquatic ecosystems are also scarce (Oreska and invasive species, which are known to have dramatic Aldridge 2011) and much work remains to be effects where they become introduced and done (Vilà et al. 2010) especially in the invaded established (Homans and Smith 2013) causing huge ecosystems of the tropics and subtropics. changes in many ecosystems worldwide and This study aimed to investigate the impact of profoundly altering native communities and A. philoxeroides invasion on the associated macro- ecosystems (Gurevitch and Padilla 2004). The full phyte diversity of littoral zones of natural pond impact of invasive aquatic species can only be ecosystems. Ideally the experimental design for such evaluated when its effect on human well-being, a case-control study should have included different such as the number of people affected and the pond ecosystems with and without A. philoxeroides magnitude of its impact on their lives (Pejchar invasion for measurement of the plant community and Mooney 2004) are also accounted. Loss of richness. But most of the ponds in our area already native biodiversity not only threatens the produ- contained A. philoxeroides. Thus, this study was ctivity and sustainability of ecosystems (Tilman restricted to an ‘impact-only’ analysis of A. et al. 1996), but also has significant socio- philoxeroides infestation on the floristic composition economic and environmental impacts, especially of aquatic/littoral macrophytes. We hypothesised in developing, over-populated countries of Asia and that there would be a negative impact of increasing Africa (Juffe-Bignoli et al. 2012). A. philoxeroides abundance, measured as cover Alternanthera philoxeroides (Martius) Griseb percentage, on the overall associated macrophyte (Amaranthaceae), commonly known as ‘alligator diversity of any pond ecosystem, across the 3 weed’, is an invasive perennial wetland herb main seasons of India. Specifically, the effect of originating from the Parana River region of South no/negligible and very high A. philoxeroides America (Maddox 1968). Cross-continental infestation on the associated native macrophyte transport primarily by ships’ ballast water until diversity was studied. The study also presents a the turn of the 20th century (Gunasekera and detailed floristic account of some native aquatic/ Bonilla 2001) and deliberate and accidental littoral macrophytes of India along with their inter-catchment dispersals by humans in present socio-ecological value, and tries to enumerate the times (Sainty et al. 1998), are considered to be effect of A. philoxeroides infestation on the the primary pathways of its global spread. growth of these plants, and in turn, highlight A. philoxeroides fulfils most criteria of Baker’s some socio-economic implications of such invasion (1974) ideal weed characteristics and is regarded as of pond ecosystems in the developing world. one of the worst weeds of the world because of its invasiveness, potential for spread, high tolerance Materials and methods to environmental fluctuations and a wide range of adaptive potential (Chatterjee and Dewanji 2012) Study area and duration and has detrimental economic and environmental The study was conducted in a highly populated impacts. Once established, it is extremely hard to suburban locality (Baranagar) in the northern control and eradication is very expensive (Sainty part of Greater Kolkata Metropolitan area. After et al. 1998). In spite of the recognition of surveying a large number of ponds within a A. philoxeroides as a problematic invasive plant radius of 10 kms, 12 ponds, which were homo- (Wang et al. 2008), field-based studies about the genous in terms of average water-quality (pH: ecological consequences of this species have 6.5 – 8.5; Conductivity < 1000 µS/cm; Turbidity been relatively few. A. philoxeroides invasion < 10 NTU; Total Phosphorus < 5 mg/L; Total have been associated with altered soil decomposition Kjeldahl Nitrogen < 10 mg/L; Dissolved Oxygen > dynamics and composition of soil microorganisms 5 mg/L) and other anthropogenic influences, (Bassett et al. 2011) and allelopathic inhibition were selected for the study with the primary of water blooms (Zuo et al. 2012). A majority of ascertainment such that varying degrees of A. the studies report the presence of A. philoxeroides philoxeroides cover were represented in the in different ecosystems (Chatterjee and Dewanji selected sample of the ponds. Due to logistic 2010; Masoodi and Khan 2012) and model its problems in obtaining suitable ponds as controls spread in different aquatic ecosystems like lakes as mentioned before, a case-control study could

344 Impact of A. philoxeroides on macrophyte diversity not be designed. Instead, the primary focus of they were given a score of 2, while the less this research was directed to an “impact only” commonly used ones were given a score of 1. study where the severity of varying degree of Plants with fodder and ‘other’ miscellaneous use A. philoxeroides on associated macrophyte richness were both scored as 1. Additionally, four local sub- in the littoral zones were explored. urban markets of Kolkata were surveyed to check The study was conducted over a period of 1 the market availability of the plants as per their year (2009–2010), covering all the three major socio-economic utility. When plants were available, seasons of India, viz.: summer (March – June), subjective scoring was done under two heads, monsoon (July – October) and winter (November namely ‘Market Supply’ - where daily supply –February). The mean seasonal average tempera- was scored as 1.0, supply at intervals of 3–4 days tures were 31.33 ± 1.81ºC, 29.94 ± 1.46ºC and was scored as 0.5, while a supply of once a week 21.89 ± 3.63ºC respectively while the total was given a score of 0.25; and ‘Abundance in rainfall varied considerably between seasons shops’ – where presence in most shops were scored (398.2 mm in summer, 866.9 mm during the 1 against 0.5, when available in only a few monsoon and 21.1 mm in winter). Meteorological specialized shops. data for the duration of the study was obtained from the Regional Meteorological Centre, Kolkata, Statistical analysis Indian Meteorological Department, Ministry of Earth Sciences, Government of India. The basic sampling unit for the purpose of all analysis was chosen to be the quadrat, which Sampling protocol resulted in a larger number of observations (n = 16 quadrats × 12 ponds = 192 quadrats per The standard procedure of visual estimation by season) compared to a pond-based study, providing the quadrat method (Jaccard 1901) was employed the flexibility of more reliable inferences. Each to record cover percent of A. philoxeroides as quadrat was considered to be a representative well as to estimate the macrophyte biodiversity area of the littoral zone of the aquatic ecosystem, (alpha diversity) within and near the littoral region and they were classified into 4 infestation grades of pond ecosystems. Following standardization, the on the basis of A. philoxeroides cover. Figure 1 quadrat size was fixed at 1 sq. meter while the (A–D) presents the four cover groups of minimum number of quadrats was found to be 11 A. philoxeroides namely, ‘No/Negligible infestation’ for each of the ponds. To increase efficiency of (Grade I: 0–10% cover); ‘Low–Medium infestation’ estimation, 16 1m2 quadrats were randomly (Grade II: 10–30% cover); ‘Medium–High placed in littoral zones of each pond per season. infestation’ (Grade III: 30–60% cover) and In each quadrat, the percentage area covered by ‘Extremely High infestation’ (Grade IV: 60–100% A. philoxeroides was recorded as its cover (%) cover). In order to evaluate the simultaneous effects and the associated macrophyte species present of sampling seasons and study ponds on the therein were noted in order to check for number of associated macrophyte species, a two- differences between A. philoxeroides cover and way analysis with suitable modifications to the number of associated macrophyte species. standard ANOVA was carried out, since the Identification of all macrophytes up to the species- variable of interest (associated macrophyte species) level were done (Prain 1903; Cook 1996), except does not follow a normal distribution. Thus, for the families ‘Poaceae’ and ‘Cyperaceae’, instead of using the usual F-distributions, the which were considered as single units, referred empirical p-values corresponding to ANOVA to as ‘Grasses’ and ‘Sedges’ respectively. statistics based on permutations were computed In order to highlight the socio-economic utility to analyse the data. This statistical test verified value of the native species with respect to that of the effect (if any) of the different study ponds on A. philoxeroides, a subjective valuation scoring the number of associated macrophyte species, so of these plants were done. Four categories of that the quadrat-wise study could be justified. usage value were defined, primarily based on The species accumulation curves computed for literature reviews, and scored under food, fodder, each of the 3 seasons were similar and revealed medicine and others (eg. aquaculture, fish feed, the adequacy of using 192 quadrats per season; ornamental etc.). Further under food value, staple the results for monsoon season is presented in vegetables were given a score of 2, while vegetable Figure 2. supplements were scored as 1. Similarly when plants The Kruskal-Wallis H test was used to analyse were popularly used as traditional medicines, the differences in overall cover (%) of

345 A. Chatterjee and A. Dewanji

Figure 1. Quadrats depicting the four infestation grades of Alternanthera philoxeroides based on its cover (%). A: No/Negligible infestation (Grade I: 0–10% cover); B: Low-Medium infestation (Grade II: 10-30% cover); C: Medium-High infestation (Grade III: 30–60% cover); D: Extremely high infestation (Grade IV: 60–100% cover) (Photographs by Anindita Chatterjee).

A. philoxeroides between 3 seasons. Again, for each

sampling season, the Kruskal-Wallis H test was used to analyse whether the number of associated macrophyte species differed significantly across the four cover (%) groups or infestation grades of A. philoxeroides. The Mann-Whitney U test was used to evaluate the pair-wise differences for number of associated macrophyte species between the lowest (Grade I) and highest (Grade IV) infestation grades of A. philoxeroides. To evaluate the effect of A. philoxeroides cover on native macrophyte diversity, a modified Poisson-regression model was used, given by: Y|X,Z ~ Poisson (e α+βX+γZ) where Y = the number of native associated macrophyte species in the quadrat; X = the actual density of Alternanthera philoxeroides as cover % in the quadrat; Z = the number of other invasive macrophyte species in the quadrat. Figure 2. The species accumulation curve for 192 quadrats for We incorporated in the model, the number of monsoon season. other invasive macrophyte species in the quadrat (Z) as it could be a potential confounder in the association between the actual density (cover %) of A. philoxeroides (X) and the number of native

346 Impact of A. philoxeroides on macrophyte diversity macrophyte species (Y). This statistical test corrected for the effect of ‘other invasive species’ and gave the results as the exclusive effect of A. philoxeroides cover on native macrophyte diversity in the quadrats. For each season, the Simpson’s Diversity Index (D) (Simpson 1949), based on the species presence/absence data, was used to estimate the species diversity for the lowest and highest infestation grades of A. philoxeroides, as given by the formula: 1 Figure 3. Distribution of the cover percentage (%) of Alternan- where S = the Species Richness (i.e. total number thera philoxeroides for each of the three sampling seasons (N= 192 quadrats/season). of species in that group); n = the total number of times the i-th species is present combining all the quadrats of that infestation grade; N = the total z = -6.918, p < 0.0001), although no significant number of individuals (i.e. total count of the difference between summer and winter (p = number of times each species is present combining 0.458) was observed. all the quadrats of that infestation grade). Similarly, for estimation of the corresponding Macrophyte species present during the study evenness of these 2 groups, an evenness measure (E1/D), was calculated and termed as ‘Simpson’s The species list of plants present in the quadrats Evenness Index’ (Kent 2012). This was obtained in association with A. philoxeroides in this study by dividing the reciprocal form of the Simpson’s has been enumerated according to their functional Diversity Index (1/D) by the number of species groups (Vis et al. 2003) and other details in Table in the sample (S), as given by the formula: 1. A total of 20 associated macrophyte species, covering 4 ‘aquatic functional classes’, viz. 1⁄ ‘submerged’ (3) (Ceratophyllum demersum, Ottelia ⁄ alismoides and Vallisneria spiralis), ‘free- floating’ (4) (Eichhornia crassipes, Lemna aequi- The Microsoft excel, IBM-SPSS (ver. 16) and noctialis, Spirodela polyrhiza and Pistia stratiotes), R–language (R Core Team (2013) http://www.R- ‘rooted-floating’ (4) (Nymphaea pubescens, project.org/) was used for statistical evaluation Ipomoea aquatic, Ludwigia adscendens and of the data. Nymphoides hydrophylla) and ‘emergent or littoral- associated’ (5) (Colocasia esculenta, Commelina Results benghalensis, Enhydra fluctuans, Marsilea Seasonal distribution of A. philoxeroides cover (%) minuta and Polygonum glabrum), along with grasses and sedges and 2 other non-aquatic plants The seasonal distribution pattern of A. philoxeroides (Rumex dentatus and Mikania micrantha), were cover (%) pooled across all 192 quadrats per found to be present. The plants were mostly season, is shown in Figure 3. The box plots show perennials, and apart from Eichhornia crassipes, that the mean cover (%) of A. philoxeroides was Pistia stratiotes and Mikania micrantha, which higher during monsoon (34.72%), followed by have been identified as invasive plants, the rest summer (26.79%), while it was lowest during were all native species. winter (16.95%). The Kruskal-Wallis H tests revealed significant difference of their mean Macrophyte diversity along infestation grades rank for monsoon (352.81), summer (267.39) and of A. philoxeroides winter (245.31): chi-square (2, N=192) = 45.269, p < 0.001. Monsoon had a significantly higher ANOVA results of the simultaneous effects of mean cover (%) than both summer (U = 13582.5, sampling seasons and study ponds on the number z = -4.485, p < 0.0001) and winter (U = 10934.5, of associated species revealed neither significant

347 A. Chatterjee and A. Dewanji

Table 1. The associated macrophyte species and their observed frequency (%) of occurrence across the quadrats (2009–2010).

General Provenance S.No. Associated Macrophyte Species Family# Common Name# Duration* Habit* (in India)*

Submerged** Perennial in Ceratophyllum demersum L. Ceratophyllaceae Coontail Forb/ Herb Native 1 tropics Perennial in Ottelia alismoides (L.) Pers. Hydrocharitacece Duck lettuce Forb/ Herb Native 2 tropics Perennial in Vallisneria spiralis L. Hydrocharitaceae Eelgrass; Tapegrass Forb/ Herb Native 3 tropics

Free-floating** Eichhornia crassipes (Mart.) Solms- Pontederiaceae Water hyacinth Forb/ Herb Perennial Invasive 4 Laubach

5 Lemna aequinoctialis Welwitsch Lemnaceae Lesser duckweed Forb/ Herb Perennial Native

6 Pistia stratiotes L. Araceae Water lettuce Forb/ Herb Perennial Invasive

7 Spirodela polyrhiza (L.) Schleid. Araceae Greater duckweed Forb/ Herb Perennial Native

Rooted-floating leaf/stem**

8 Nymphaea pubescens Willd. Nymphaeceae Water lily Forb/ Herb Perennial Native

9 Ipomoea aquatica Forssk. Convolvulaceae Water spinach Forb/ Herb Perennial Native

10 Ludwigia adscendens (L.) H. Hara Onagraceae Primrose willow Forb/ Herb Perennial Native

11 Nymphoides hydrophylla (Lour.) O. Kuntze Menyanthaceae Floating heart Forb/ Herb Perennial Native

Emergent / Littoral-associated**

12 Colocasia esculenta (L.) Schott Araceae Arum; Elephant Ear Forb/ Herb Perennial Native

Annual / 13 Commelina benghalensis L. Commelinaceae Bengal dayflower Forb/ Herb Native Perennial

14 Enhydra fluctuans Loureiro Asteraceae Water cress Forb/ Herb Perennial Native

15 Marsilea minuta L. Marsileaceae Dwarf Water Clove Forb/ Herb Perennial Native

Denseflower Annual / 16 Polygonum glabrum Willd. Polygonaceae Forb/ Herb Native knotweed Perennial

Others** Annual/ Rumex dentatus L. Polygonaceae Toothed dock Forb/ Herb Native 17 Biennial

18 Mikania micrantha H. B. Kunth. Asteraceae Mile-a-minute Vine Perennial Invasive

19 ‘Cyperaceae’ Cyperaceae Sedges - - Native

20 ‘Graminae’ Poaceae Grasses - - Native

#Plant identification & common name sources: Prain (1903), Cook (1996), Ghosh (2005) *Plant general habit/provenance/status sources: http://plants.usda.gov/; http://www.issg.org/; http://www.iucnredlist.org/; http://www.invasive speciesinfo.gov/ **Functional grouping: based on Vis et al. (2003)

pond effect (p-value = 0.1604) nor significant four infestation grades of A. philoxeroides. A season-effect (p-value = 0.4484) on them, justifying general decreasing trend in number of associated the season-wise pooling of the quadrat data to macrophyte species was evident from grade I to estimate the effect of infestation of A. philoxeroides grade IV of A. philoxeroides infestation for each on the number of associated macrophyte species. sampling season. Significant differences across Table 2 presents the associated macrophyte species the four infestation grades of A. philoxeroides seasonal presence/absence check-list, across the were also revealed by the Kruskal-Wallis H tests:

348 Impact of A. philoxeroides on macrophyte diversity

Table 2. Seasonal presence of associated macrophyte species across the four ‘Infestation Grades’ of Alternanthera philoxeroides for three sampling seasons.

‘Infestation Grades’ of A. philoxeroides## Associated Macrophytes 1 2 3 4 1 2 3 4 1 2 3 4

Provenance Species Name Winter Summer Monsoon

Ceratophyllum demersum - - - - + - + - + + + - Ottelia alismoides - - - - + + - - - - + - Vallisneria spiralis + - - - + - + - + - + + Lemna aequinoctialis + + + + + + + + + + + + Spirodela polyrhiza + + + + + + + + + + + + Nymphaea pubescens + - - - - - + - + - - - Ipomoea aquatic + + + + + + + + + + + + Ludwigia adscendens + + + + + + - + + + - + Nymphoides hydrophylla ------+ - + - - - Colocasia esculenta + + + + + + + + + + + + Commelina benghalensis + + + - + + + + + + + - Enhydra fluctuans + + ------+ + + - Native (true) species Marsilea minuta + - - - + + + - + + - - Polygonum glabrum - - - + + + - - + - - - Rumex dentatus + + - - + + + + - - - - Cyperaceae# + + + - + + + - + + - + Graminae# + + + + + + + + + + + + Eichhornia crassipes + + + + + + + + + + + + Pistia stratiotes + + + + + + - + + + + - Species

Invasive Invasive Mikania micrantha + + + + + + + + + + + + Total no. of species (group-wise) 16 13 11 10 17 15 15 11 18 14 13 10 Chi-Square Value (Kruskal-Wallis H test) 11.007 10.002 54.433 p – value (significant at: *0.05 level; ** 0.01 level) 0.012 * 0.019 * < 0.001 ** ##1 = No/Negligible Infestation, 2 = Low-Medium Infestation, 3 = Medium-High Infestation, 4 = Extremely High Infestation;#Functional group has been designated as ‘species’ here; (+) = Species Present, (-) = Species Absent.

chi-square (3, N=192) = 11.007, p = 0.012 (winter); summer: 0.440, monsoon: 0.645). The evenness chi-square (3, N=192) = 10.002, p=0.019 (summer); index (E1/D) which ranges from 0 (all biomass in chi-square (3, N=192) = 54.433, p = <0.001 one species) to 1 (>1 species present in equal (monsoon). Among the 9 individual species that abundance), with lower values indicating larger were present in 10 or more (>80%) of the 12 differences in abundance between species (Mulder categorical classes (3 season × 4 infestation grade) et al. 2004), showed that at highest grade of of A. philoxeroides infestation grades, 3 were infestation, evenness was lower (winter: 0.208, other invasive species (Eichhornia sp., Pistia sp. summer: 0.189, monsoon: 0.141) when compared and Mikania sp.), thereby showing the consistent with the corresponding evenness at Grade I (winter: presence of multiple invader species in aquatic 0.240, summer: 0.307, monsoon: 0.259). The results ecosystems. also showed that maximum reduction of species The overall species richness (S), Simpson’s richness was during the monsoon (42%), followed diversity index (D) and evenness index (E1/D) by winter (35%) and summer (33%) from Grade between the lowest (Grade I) and highest (Grade I to Grade IV. IV) infestation grade of A. philoxeroides were For each season, the exclusive effect of calculated and presented in Table 3. For each A. philoxeroides infestation impact on the associated season, species diversity (D) was higher at Grade macrophyte species richness, after adjusting for I (winter: 0.245, summer: 0.181, monsoon: 0.203) the number of other invasive species in that quadrat, than the diversity of Grade IV (winter: 0.438, was checked using the Poisson-regression model.

349 A. Chatterjee and A. Dewanji

Figure 4. Overall frequency of occurrence (%) of native associated macrophytes across the lowest (Grade – I) and highest (Grade – IV) of Alternanthera philoxeroides infestation.

The results of these tests revealed that the Nymphoides sp. and Marselia sp.) were completely number of native macrophyte species in a quadrat eliminated at Grade IV of A. philoxeroides decreased significantly with the increase in A. infestation. philoxeroides cover (monsoon: p<0.001; winter: We identified the overall socio-economic p=0.014; summer: p=0.009), thereby indicating importance of some aquatic/littoral native associated the negative effect of A. philoxeroides density on macrophytes found in this study, including a associated native species in littoral regions of the subjective scoring of their sociological valuation aquatic ecosystems. Additionally, the Mann- and market availability, and compared it with Whitney U test also revealed a significant decrease A. philoxeroides (Table 4). It was noted that 10 in number of native associated macrophytes out of these 12 native plants were used as across the lowest (Grade I) and the highest vegetables or food supplements (Colocasia sp., (Grade IV) of A. philoxeroides infestation for Enhydra sp., Ipomoea sp., Ludwigia sp., Marsilea each season: U = 481.0, z = -3.744, p < 0.001 sp., Nymphaea sp., Nymphoides sp. and Ottelia (winter); U=1566.0, z = -2.305, p = 0.021 (summer); sp., Polygonum sp., Vallisneria sp.). All these U=175.5, z=-7.453, p < 0.001 (monsoon). The mean plants, except for Vallisneria sp., were also used ranks of maximum number of native macrophyte as traditional medicines. Ipomoea sp., which had species for Grade I were 74.02, 76.80 and 67.58; a high sociological usage score, was also the while the mean ranks for Group IV were 37.29, most popular native aquatic plant, having daily 59.65 and 24.89 for the seasons winter, summer market turnover and wide-spread availability, and monsoon respectively. The frequency of followed by Colocasia sp. and Nymphaea sp. overall quadrat-wise occurrence (%) of 12 true- Again while Nymphoides sp. had a high socio- aquatic native associated macrophytes across the logical usage score; it was less popular in the lowest (Grade I) and highest (Grade IV) infestation market when compared to plants like Enhydra grades, represented in Figure 4, shows that the sp., Marselia sp. and Ludwigia sp. Although A. occurrence of all these native macrophytes were philoxeroides had some sociological use value at impacted at higher infestation (Grade IV) of par with some native plants (Ceratophyllum sp., A. philoxeroides. The presence of dominant co- Ottelia sp., Vallisneria sp. Commelina sp. and occurring native species like Ipomoea sp. (from Polygonum sp.), but unlike these natives, all of 42.3% to 34.0%), Commelina sp. (from 21.1% to which were marginally popular in the market, 6.2%) and Colocasia sp. (from 12.7% to 10.3%) none of the markets surveyed during the study were considerably reduced, while 50% of these sold A. philoxeroides on a commercial basis, 12 native associated macrophytes (Ceratophyllum indicating the low popularity of A. philoxeroides sp., Otelia sp., Nymphaea sp., Enhydra sp., in the sub-urban markets; and hence emphasizing

350 Impact of A. philoxeroides on macrophyte diversity the higher importance of these native plants over plants between the lowest (no/negligible) and A. philoxeroides in the society. highest infestation grades of A. philoxeroides. We found negative impacts of A. philoxeroides Discussion cover on the total associated macrophyte diversity in littoral zones of aquatic ecosystems, A. philoxeroides, although perennial in the tropics though due to the lack of controlled/experimental and semi-tropics, exhibited low covers during study plots, it was not possible for us to conclude the winter months. The monsoon season, with if the diversity of associated macrophyte species ambient temperature nearing 30°C and high were directly affected by higher cover of seasonal rainfall (>850.0 mm), provided the most A. philoxeroides or if it was due to some other favourable environmental conditions for the factors. Some of the characteristics of invasive luxuriant growth of A. philoxeroides, which was plants which are responsible for their strong evident by the significantly higher overall cover impact on native plant communities are vigorous (%) of A. philoxeroides during this season. Good growth, dense rhizomatous structures, homogenous rainfall and temperatures around 30°C have been strands and high cover (Hejda et al. 2009), all of reported to be conducive for optimum shoot which are satisfied by A. philoxeroides. Aquatic emergence and growth (Sainty et al. 1998; Shen A. philoxeroides has rapid growth and reproduction et al. 2005) as well as peak plant height and (Chatterjee and Dewanji 2012), high biomass maximum biomass (Liu et al. 2004) of A. philo- accumulation potential (Zuo et al. 2012) and xeroides. forms dense mats of entangled stems (Dugdale et Overall 18 aquatic/littoral macrophytes, along al. 2010), some attributes which might help with grasses and sedges, were found in A. philoxeroides to pose serious threat to native association with A. philoxeroides in the quadrats, plant diversity (Julien et al. 1995) by limiting the of which 3 were other invasive plant species. growth of other associated species in its close Gradual decrease in total number of associated vicinity. Zuo et al. (2012) found a lower number species (species richness) was observed from the of companion plants alongside A. philoxeroides lowest to highest infestation grades of under aquatic conditions when compared with its A. philoxeroides, for each season. When comparing terrestrial ecotype, while Jin Cheng and Qiang between the community structures of the quadrats (2006) also reported a gradual decrease in the belonging to the lowest (no/negligible) and highest species composition and diversity of the community infestation grades of A. philoxeroides, for all 3 with increasing dominance of A. philoxeroides. seasons, reduction of both species diversity and Bassett et al. (2012) also reported a strong evenness were revealed at the higher infestation competitive interaction between native vegetation grades of A. philoxeroides. More than 30% and A. philoxeroides in the littoral region of a reduction in species richness was observed in the New Zealand lake, while acknowledging certain quadrats belonging to highest infestation grades similar limitations of a field-based study. Further when compared with that of the species richness replicated research comparing uninvaded aquatic of the no/negligible ones. Of the two components ecosystems with invaded ones; or greenhouse of species diversity, richness and evenness and/or field based experimental studies manipulating (Magurran 1988), the focus of invasive species competition, would be essential for exact elucidation impacts has been primarily on richness (Levine et of the extent of A. philoxeroides impact on al. 2003). Hulme and Bremner (2006) also reported different plant communities. that the presence of the invasive riparian plant The most commonly occurring macrophyte Impatiens glandulifera resulted in more than a functional group was the ‘free-floating’ one, 25% reduction in alpha diversity. Similar decrease consisting of Eichhornia sp., Lemna sp., Spirodela in species richness, diversity and evenness, at sp and Pistia sp.; large growths of which are also higher cover of some invasive species were also known to adversely affect freshwater ecosystems reported by Hejda et al. (2009). During this study, (Scheffer et al. 2003). The consistent presence of a significant negative impact of A. philoxeroides other invasive macrophytes like Eichhornia sp., cover on associated native macrophyte richness Pistia sp. and Mikania sp. across the different was evident for all 3 seasons, even after adjusting infestation grades of A. philoxeroides found in for the influence of other invasive species. The this study provides an ecologically important present study also found a highly significant indication about the increasing presence of multiple reduction in total number of associated native invaders in aquatic ecosystems and suggest avenues

351 A. Chatterjee and A. Dewanji

Table 3. Comparison of species richness (=number of species in sample S), species diversity (=Simpson’s Diversity Index D), and evenness (=Simpson’s Evenness Index (E1/D)) of A. philoxeroides infestation Grades I (cover 0–10%) and IV (cover 60–100%) across the 3 seasons.

Winter Summer Monsoon Diversity Measures Grade I Grade IV Grade I Grade IV Grade I Grade IV Species Richness (S) 17 11 18 12 19 11 Simpson’s Diversity Index (D) * 0.245 0.438 0.181 0.440 0.203 0.645

Simpson’s Evenness Index (E1/D) ** 0.240 0.208 0.307 0.189 0.259 0.141

*as index value (D) increases, diversity decreases ** lower the index value (E1/D), larger is the differences in abundance between species (Mulder et al. 2004)

Table 4. Socio-economic usage and their preliminary subjective valuation depicting the importance of some native plants and Alternanthera philoxeroides.

aSociological Usage (Scores)** bMarket Availability (Scores)** # Abun- Species Usage of specific plant parts Medi- Market Others Total dance in Food Fodder cine Supply a Total shops b Ceratophyllum 1. Whole Plant (Fish food2,3, Aquarium - 1 1 1 3 0.25 0.5 0.75 demersum Plant3, Traditional Medicine4) 1. Young stems, leaves & petioles Ottelia 3 alismoides (Vegetable ) 2 - 1 - 3 - - - 2. Leaves (Traditional Medicine3) Vallisneria 1. Whole Plant (Aquarium Plant4, Fish food2) 1 1 - 1 3 0.25 0.5 0.75 spiralis 2. Young Leaves (Vegetable supplement2) 1. Flower (Aesthetic & market value3) Nymphaea 2. Flowers, petioles & rhizomes (Traditional 2 - 2 1 5 1.0 0.5 1.5 pubescens Medicine5) 3. Peduncles (Vegetables6) Commelina 1. Leaves & twigs (Fodder4) - 1 2 - 3 0.25 0.5 0.75 benghalensis 2. Leaf extract (Traditional Medicine4) 1. Young leaves & stem (Vegetables4,5, Enhydra 3 fluctuans Fodder ) 2 1 2 - 5 0.5 0.5 1.0 2. Leaves extract (Traditional Medicine4) Ipomoea 1. Leaves & stem (Vegetable4 , Fodder4, 2 1 2 - 5 1.0 1.0 2.0 aquatica Traditional Medicine4) Ludwigia 1. Stem & leaves (Vegetable supplements3, 1 - 2 - 3 0.5 0.5 1.0 adscendens Traditional Medicine3,4) 1. Leaves & seeds (Medicinal properties3, Nymphoides Ornamental3) 1 - 2 1 4 0.25 0.5 0.75 hydrophylla 3. Tender leaves & stem (Vegetable supplements4) 1. Rhizomes, stem, petioles & leaves Colocasia 5 esculenta (Vegetables ) 2 - 2 - 4 1.0 1.0 2.0 2. Corm & leaves (Medicinal properties1,5) Marsilea 1. Leaves & sprouts (Vegetable3) 2 - 2 - 4 0.5 0.5 1.0 minuta 2. Leaves & root (Medicinal properties6) 1. Young shoots & leaves (Vegetable Polygonum supplements4) 1 1 1 - 3 0.25 0.5 0.75 glabrum 2. Leaves & twigs (Fodder3, Medicinal properties6) 1. Leaves & twigs (Fodder3) Alternanthera 3 philoxeroides 2. Young leaves (Vegetable supplements , 1 1 1 - 3 - - - Medicine2)

# References: Brown and Valiere (2004)1; Cook (1996)2; Ghosh (2005)3; Panda and Mishra (2011)4; Patil and Ageely (2011)5; Swapna et al. (2011)6; **Scores = Subjective valuation based on preliminary market survey: aSociological Usage: (Food, Medicine: vegetable/highly popular = 2, vegetable supplements/less popular = 1; Fodder, Others = 1); Data not available = (-) bMarket Availability: Market Supply: (1=Daily, 0.5=at 3–4 days’ interval, 0.25=weekly); Abundance in shops: (1.0 = all vegetable shops; 0.5 = specialized shops).

352 Impact of A. philoxeroides on macrophyte diversity of future research on facilitative interactions Acknowledgements between invasive species. Ricciardi (2001) reported that some invaders can alter habitat conditions in The authors want to thank Indian Statistical Institute (ISI) for favour of other invaders, creating a positive funding of this research; Prof. Saurabh Ghosh, Human Genetics Unit, ISI for their statistical guidance; Dr. Snigdha Chakrabarti, feedback system and leading to accumulation of Economics Research Unit, ISI for guidance on market-survey and other non-indigenous/introduced species. Positive socio-economic valuation scoring of the macrophytes; Mr. facilitative interactions between A. philoxeroides Hemanth Kulkarni, Bayesian and Interdisciplinary Research Unit, and other invasives like Eichhornia crassipes ISI for help in R-programming; Mr. Sourav Sengupta, Mr. Sandip Chatterjee and Mr. Susant Mahankur, AERU, ISI for technical and Pistia stratiotes have also been recently assistance in the field; and two anonymous reviewers for their reported (Wundrow et al. 2012). valuable comments and suggestions on the earlier drafts of this Aquatic and wetland plants are important manuscript, which greatly improved the manuscript. sources of food, fodder, biomass and building material for human societies (Bornette and References Puijalon 2011). Since people in South-East Asia spend as high as 72% of their income on food Baker HG (1974) The Evolution of Weeds. Annual Review of Ecology and Systematics 5: 1–24, http://dx.doi.org/10.1146/ alone (FAO 2011), importance of the aquatic annurev.es.05.110174.000245 plants as cheap and quality sources of vegetables Bassett I, Paynter Q, Beggs JR (2011) Invasive Alternanthera in Asian diet is huge (Peter 2013). Wetland philoxeroides (alligator weed) associated with increased plants as sources of traditional medicine provide fungivore dominance in Coleoptera on decomposing leaf litter. Biological Invasions 13: 1377–1385, http://dx.doi.org/ health services to about 80% of the world’s 10.1007/s10530-010-9896-3 population, which further highlights their socio- Bassett I, Paynter Q, Hankin R, Beggs JR (2012) Characterising economical importance (Panda and Misra 2011). alligator weed (Alternanthera philoxeroides; Amaranthaceae) invasion at a northern New Zealand lake. New Zealand An additional impact of A. philoxeroides, which Journal of Ecology 36(2): 216–222 has not been widely demonstrated previously, is Bornette G, Puijalon S (2011) Response of aquatic plants to that A. philoxeroides reduces the availability of abiotic factors: a review. Aquatic Sciences 73: 1–14, many plants useful for humans. Thus, as http://dx.doi.org/10.1007/s00027-010-0162-7 Brown AC, Valiere A (2004) The medicinal uses of poi. Nutrition highlighted in this study, replacement of native in Clinical Care 7(2): 69–74 aquatic/wetland plants, which are sources of Butchart SHM, Walpole M, Collen B, Strien VA, Scharlemann cheap and popular food and medicinal sources, JPW, Almond REA, et al. (2010) Global Biodiversity: due to high infestation of A. philoxeroides, a Indicators of Recent Declines. Science 328: 1164–1168, http://dx.doi.org/10.1126/science.1187512 less-popular food source in itself, is a huge cause Caraco N, Cole J, Findlay S, Wigand C (2006) Vascular plants as of concern in terms of socio-economic sustainability engineers of oxygen in aquatic systems. BioScience 56(3): of highly populated, developing countries of the 219–225, http://dx.doi.org/10.1641/0006-3568(2006)056[0219:VPA EOO]2.0.CO;2 world (Juffe-Bignoli et al. 2012). Chatterjee A, Dewanji A (2010) Global climate change and biotic Reports on quantitative assessment of impacts invasion: A case study of a wetland plant species. 2nd of A. philoxeroides invasion on native vegetation International conference on Environmental Management, are mostly from temperate countries where the Jawaharlal Nehru Technological University, Hyderabad, India, B. S. Publications, pp 270–277 plant is naturally controlled during the winter Chatterjee A, Dewanji A (2012) Peroxidase as a metric of stress season due to snow (Liu and Yu 2009). It is tolerance and invasive potential of alligator weed surprising that such studies from sub-tropical and (Alternanthera philoxeroides) growing in aquatic habitats. tropical areas are severely lacking, considering Management of Biological Invasions 3: 65–76, http://dx.doi.org/10.3391/mbi.2012.3.2.01 its perennial growth in those regions and its Clements D, Dugdale TM, Hunt TD (2011) Growth of aquatic status as one of the worst weeds of the world alligator weed (Alternanthera philoxeroides) over 5 years in (Chatterjee and Dewanji 2012). However, accepting south-east Australia. Aquatic Invasions 6: 77–82, http://dx.doi.org/10.3391/ai.2011.6.1.09 the limitations of an ‘impact-only’ field-based Cook CDK (1996) Aquatic and wetland plants of India: A observational study conducted post-invasion, this reference book and identification manual for the vascular study provides an insight into the floral plants found in permanent or seasonal fresh water in the associations of A. philoxeroides in this region subcontinent of India south of the Himalayas. Oxford, Oxford University Press, 385 pp and together with its potential to displace a large Dudgeon D, Arthington AH, Gessner MO, Kawabata ZI, Knowler number of native flora at high infestation levels, DJ, Leveque C (2006) Freshwater biodiversity: importance, it also highlights the socio-economic value of threats, status and conservation challenges. Biological these plants, which is an unique feature to Reviews 81: 163–182, http://dx.doi.org/10.1017/S1464793105006950 Dugdale TM, Clements C, Hunt TD, Butler KL (2010) Alligator- tropical regions. weed produces viable stem fragments in reponse to herbicide treatment. Journal of Aquatic Plant Management 48: 84–91

353 A. Chatterjee and A. Dewanji

Engelhardt KAM, Ritchie ME (2001) Effects of macrophyte Maddox DM (1968) Bionomics of an alligatorweed flea beetle, species richness on wetland ecosystem functioning and Agasicles sp., in Argentina. Annals of the Entomological services. Nature 411: 687–689, http://dx.doi.org/10.1038/35079573 Society of America 61: 1299–1305 Erwin S, Huckaba A, He KS, McCarthy M (2013) Matrix analysis Magurran AE (1988) Ecological Diversity and its Measurement. to model the invasion of alligatorweed (Alternanthera Princeton University Press/Croom Helm, London, 179 pp philoxeroides) on Kentucky lakes. Journal of Plant Ecology Masoodi A, Khan FA (2012) Invasion of alligator weed 6(2): 150–157, http://dx.doi.org/10.1093/jpe/rts024 (Alternanthera philoxeroides) in Wular Lake, Kashmir, India. FAO (2011) The state of food insecurity in the world. Office of Aquatic Invasions 7: 143–146, http://dx.doi.org/10.3391/ai.2012. knowledge exchange, research and extension, Food and 7.1.016 Agricultural Organization of the United Nations, Rome, Italy Masoodi A, Sengupta A, Khan FA, Sharma GP (2013) Predicting Ghosh SK (2005) Illustrated aquatic and wetland plants in the spread of alligator weed (Alternanthera philoxeroides) in harmony with mankind. Kolkata, India, Standard Literature, Wular lake, India: A mathematical approach. Ecological 225 pp Modelling 263: 119–125, http://dx.doi.org/10.1016/j.ecolmodel. Gunasekera L, Bonilla J (2001) Alligator weed: tasty vegetable in 2013.04.021 Australian backyards? Journal of Aquatic Plant Management McNeely J (2001) Invasive species: a costly catastrophe for native 39: 17–20 biodiversity. Land Use and Water Resources Research 1(2): Gurevitch J, Padilla DK (2004) Are invasive species a major 1–10 cause of extinctions? Trends in Ecology & Evolution 19(9): Michelan TS, Thomaz SM, Mormul RP, Carvalho P (2010) 470–474, http://dx.doi.org/10.1016/j.tree.2004.07.005 Effects of an exotic invasive macrophyte (tropical Hejda M, Pysek P, Jarosik V (2009) Impact of invasive plant on signalgrass) on native plant community composition, species the species richness, diversity and composition of invaded richness and functional diversity. Freshwater Biology 55: communities. Journal of Ecology 97: 393–403, 1315–1326, http://dx.doi.org/10.1111/j.1365-2427.2009.02355.x http://dx.doi.org/10.1111/j.1365-2745.2009.01480.x Mulder CPH, Bazeley-White E, Dimitrakopoulos PG, Hector A, Homans FR, Smith DJ (2013) Evaluating management options for Scherer-Lorenzen M, Schmid B (2004) Species evenness and aquatic invasive species: concepts and methods. Biological productivity in experimental plant communities. Oikos 107: Invasions 15: 7–16, http://dx.doi.org/10.1007/s10530-011-0134-4 50–63, http://dx.doi.org/10.1111/j.0030-1299.2004.13110.x Hulme PE, Bremner ET (2006) Assessing the impact of Impatiens Oreska MPJ, Aldridge DC (2011) Estimating the ﬁnancial costs glandulifera on riparian habitats: partitioning diversity of freshwater invasive species in Great Britain: A standar- components following species removal. Journal of Applied dized approach to invasive species costing. Biological Inva- Ecology 43: 43–50, http://dx.doi.org/10.1111/j.1365-2664.2005. sions 13: 305–319, http://dx.doi.org/10.1007/s10530-010-9807-7 01102.x Panda A, Misra MK (2011) Ethnomedicinal survey of some Jaccard P (1901) Étude comparative de la distribution florale dans wetland plants of South Orissa and their conservation. Indian une portion des Alpes et des Jura. Bulletin de la Société Journal of Traditional Knowledge 10(2): 296–303 Vaudoise des Sciences Naturelles 37: 547–579 Patil B, Ageely H (2011) Antihepatotoxic activity of Colocasia Jenkins M (2003) Prospects for Biodiversity. Science 302: 1175– esculenta leaf juice. International Journal of Advanced 1177, http://dx.doi.org/10.1126/science.1088666 Biotechnology & Research 2(2): 296–304 Julien MH, Skarratt B, Maywald GF (1995) Potential Pejchar L, Mooney HA (2004) Invasive species, ecosystem geographical distribution of alligator weed and its biological services and human well-being. Trends in Ecology & control by Agasicles hygrophila. Journal of Aquatic Plant Evolution 4: 497–504, http://dx.doi.org/10.1016/j.tree.2009.03.016 Management 33: 55–60 Peter KV (2013) Potential of aquatic vegetables in the Asian diet. JinCheng L, Qiang Sheng Q (2006) Influence of Alternanthera In: Holmer R, Linwattana G, Nath P, Keatinge JDH (eds), philoxeroides on the species composition and diversity of Proceedings of the Regional Symposium on High Value weed community in spring in Nanjing. Journal of Plant Vegetables in Southeast Asia: Production, Supply and Ecology 30(4): 585–592 Demand (SEAVEG2012). January 24-26, 2012, Chiang Mai, Juffe-Bignoli D, Rhazi L, Grillas P (2012) The socio-economic Thailand, AVRDC - The World Vegetable Center, value of aquatic plants. In: Juffe-Bignoli D, Darwall WRT Publication No. 12–758. AVRDC - The World Vegetable (eds), Assessment of the socio-economic value of freshwater Center, Taiwan, pp 210–215 species for the northern African region. IUCN IV, pp 41–65 Pimentel D, Zuniga R, Morrison D (2005) Update on the Kent M (2012) Vegetation description and Data Analysis: A environmental and economic costs associated with alien- Practical Approach, 2nd edn. Wiley-Blackwell, UK, 414 pp invasive species in the United States. Ecological Economics Levine JM, Vilà M, D’Antonio CM, Dukes JS, Grigulis K, 52: 273–288, http://dx.doi.org/10.1016/j.ecolecon.2004.10.002 Lavorel S (2003) Mechanisms underlying the impacts of Powell KI, Chase JM, Knight TM (2011) A synthesis of plant exotic plant invasions. Proceedings of the Royal Society invasion effects on biodiversity across spatial scales. London B 270: 775–781, http://dx.doi.org/10.1098/rspb.2003.2327 American Journal of Botany 98: 539–548, http://dx.doi.org/ Liu C, Wua G, Yua D, Wanga D, Xia S (2004) Seasonal Changes 10.3732/ajb.1000402 in Height, Biomass and Biomass Allocation of Two Exotic Prain D (1903) Bengal Plants. Calcutta, India, Botanical Survey Aquatic Plants in a Shallow Eutrophic Lake. Journal of of India, 1319 pp Freshwater Ecology 19(1): 41–45, http://dx.doi.org/10.1080/ Pysek P, Richardson DM (2010) Invasive Species, Environmental 02705060.2004.9664510 Change and Management, and Health. Annual Review of Liu C, Yu D (2009) The bud and root sprouting capacity of Environment and Resources 35: 25–55, http://dx.doi.org/ 10.1146/annurev-environ-033009-095548 Alternanthera philoxeroides after over-wintering on Rejmánková E (2011) The role of macrophytes in wetland sediments of a drained canal. Hydrobiologia 623(1): 251– ecosystems. Journal of Ecology and Field Biology 34(4): 256, http://dx.doi.org/10.1007/s10750-008-9693-5 333–345, http://dx.doi.org/10.5141/JEFB.2011.044 Lockwood JL (1999) Using Taxonomy to Predict Success among Ricciardi A (2001) Facilitative interactions among aquatic Introduced Avifauna: Relative Importance of Transport and invaders: is an “invasional meltdown” occurring in the Great Establishment. Conservation Biology 13(3): 560–567, Lakes? Canadian Journal of Fisheries and Aquatic Sciences http://dx.doi.org/10.1046/j.1523-1739.1999.98155.x 58: 2513–2525, http://dx.doi.org/10.1139/f01-178

354 Impact of A. philoxeroides on macrophyte diversity

Sainty G, McCorkelle G, Julien M (1998) Control and spread of Wang N, Yu F-H, Li P-X, He W-M, Liu F-H, Liu J-M (2008) Alligator Weed Alternanthera philoxeroides (Mart.) Griseb., Clonal integration affects growth, photosynthetic efﬁciency in Australia: lessons for other regions. Wetlands Ecology and and biomass allocation, but not the competitive ability, of the Management 5:195–201, http://dx.doi.org/10.1023/A:1008248921849 alien invasive Alternanthera philoxeroides under severe Scheffer M, Szabo SN, Gragnani A, Nes van EH, Rinaldi S, stress. Annals of Botany 101: 671–678, http://dx.doi.org/10.10 Kautsky N, Norberg J, Roijackers RMM, Franken RJM 93/aob/mcn005 (2003) Floating plant dominance as a stable state. Wetzel RG (2001) Limnology Lakes and River Ecosystems, Proceedings of the National Academy of Sciences 100(7): Elsevier, 1006 pp 4040–4045 Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Shen J, Shen M, Wang X, Lu Y (2005) Effect of environmental Quantifying Threats to Imperiled Species in the United factors on shoot emergence and vegetative growth of States. Science 48(8): 607–615 alligatorweed (Alternanthera philoxeroides). Weed Science Wundrow EJ, Carrillo J, Gabler CA, Horn KC, Siemann E (2012) 53(4): 471–478, http://dx.doi.org/10.1614/WS-04-198R Facilitation and competition among invasive plants: A field Simpson EH (1949) Measurement of diversity. Nature 163: 688, experiment with alligatorweed and water hyacinth. Plos ONE http://dx.doi.org/10.1038/163688a0 7(10): e48444, http://dx.doi.org/10.1371/journal.pone.0048444 Swapna MM, Prakashkumar R, Anoop KP, Manju CN, Rajith NP Zuo S, Ma Y, Shinobu I (2012) Differences in ecological (2011) A review on the medicinal and edible aspects of and allelopathic traits among Alternanthera philo- aquatic and wetland plants of India. Journal of Medicinal xeroides populations. Weed Biology and Management Plants Research 5(33): 7163–7176 12: 123–130, http://dx.doi.org/10.1111/j.1445-6664.2012.00443.x Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influences by biodiversity in grassland ecosystems. List of Databases Nature 379: 718–720, http://dx.doi.org/10.1038/379718a0 Vilà M, Basnou C, Pysek P, Josefsson M, Genovesi P, Gollasch Global Invasive Species Database (GISD), Invasive Species S, Nentwig W, Olenin S, Roques A, Roy D, Hulme PH Specialist Group (ISSG), International Union for (2010) How well do we understand the impacts of alien Conservation of Nature (IUCN). http://www.issg.org/ database species on ecosystem services? A pan-European, cross-taxa (Accessed on 15 September 2013) assessment. Frontiers in Ecology and the Environment 8(3): IUCN (2013) International Union for Conservation of Nature, 135–144, http://dx.doi.org/10.1890/080083 IUCN Red List of Threatened Species. Version 2013.2. Vis C, Hudon C, Carignan R (2003) An evaluation of approaches http://www.iucnredlist.org (Accessed on 27 January 2014) used to determine the distribution and biomass of emergent National Invasive Species Information Center (NISIC): Gateway and submerged aquatic macrophytes over large spatial scales. to invasive species information; covering Federal, State, Aquatic Botany 77(3): 187–201, http://dx.doi.org/10.1016/S0304- local, and international sources, United States Department of 3770(03)00105-0 Agriculture (USDA). http://www.invasivespeciesinfo.gov Vitousek PM, D’antonio CM, Loope LL, Rejmánek M, (Accessed on 15 October 2013) Westbrooks R (1997) Introduced species: a significant Natural Resources Conservation Services (NRCS), The Plant component of human-caused global change. New Zealand Database, United States Department of Agriculture (USDA). Journal of Ecology 21(1): 1–16 http://plants.usda.gov (Accessed on 01 October 2013)

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