Biodivers Conserv (2008) 173181ndash3194DOI 101007s10531-008-9419-z

ORIGINAL PAPER

Operational characterization of alien invasive Xoraand its management implications

Anzar A Khuroo middot Zafar Reshi middot Irfan Rashid middotG H Dar middot Zafar S Khan

Received 15 January 2008 Accepted 26 June 2008 Published online 16 July 2008copy Springer Science+Business Media BV 2008

Abstract A continuing lack of consensus on the operational characterisation of alieninvasive species (AIS) in invasion biology has hampered the integration of researchresults generated worldwide This impedes our progress in devising sound managementstrategies to stem the tide of biological invasions In this regard we here use the neutralterminology model of Colautti and MacIsaac (Divers Distrib 10135ndash141 2004) (CMmodel) for the characterization of alien invasive Xora of the Kashmir Himalaya Indiaand more emphatically expound the utility of such a stage-based operational frameworkin the management of plant invasions Out of the total of 436 alien invasive plant speciesrecorded in the region the number of species belonging to invasion stages II III IVaIVb and V was 119 107 56 77 and 77 species respectively In terms of relative propor-tion of species belonging to the diVerent invasion stages trees dominated the Stage-V(3125) followed by aquatics subshrubs biennial herbs perennial herbs annual herbsand shrubs in descending order Based on the results obtained in the present investiga-tion and in an attempt to link the characterisation of AIS with the management of plantinvasions we here propose a hierarchical management framework based on predictionprevention prescription and public awareness While the present study focuses on plantsonly the proposed management framework can be operationally used across diVerenttaxonomic groups and within varied ecosystems with potentially immense managementimplications

Keywords Biological invasions middot Alien invasive species middot Abundance middot Distribution middot Management strategies

Electronic supplementary material The online version of this article (doi101007s10531-008-9419-z) contains supplementary material which is available to authorized users

A A Khuroo middot Z Reshi (amp) middot I Rashid middot G H Dar middot Z S KhanDepartment of Botany University of Kashmir Srinagar 190006 J amp K Indiae-mail zreshiyahoocom

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3182 Biodivers Conserv (2008) 173181ndash3194

Introduction

The discipline of invasion biology has rapidly emerged as an area of intense research activ-ity with an increasing number of hypotheses (Hierro et al 2005 Inderjit et al 2005) syn-theses (Drake et al 1989 Pysek et al 1995 Williamson 1996 Mack et al 2000 Perringset al 2000 Mooney et al 2005 Cadotte et al 2006) and management practices (Prestonet al 2000 McNeely et al 2001 Wittenberg and Cock 2001 Ruiz and Carlton 2003) Sucha focus has been mainly triggered by mounting evidence of environmental and economiclosses inXicted by the alien invasive species (AIS) on native ecosystems worldwide(Pimentel et al 2005) The insights gained from theoretical as well as empirical studies per-taining to various facets of invasion biology pervade both natural and social sciences witha pressing priority for conservation of biodiversity environmental management and sus-tainable development at the sub-national national and international levels (Sanderlundet al 1999)

In spite of these heightened scientiWc insights and growing public awareness about theincreasing threats of biological invasions (Devine 1998 Kaiser 1999 Moore 2000 Raghuet al 2006) lack of consensus among scientists working in diVerent regions of the worldabout the operational deWnition of the fundamental unit of study ie alien invasive speciesis hampering progress in this Weld Invasion ecology has witnessed several debates in thesearch for a universally acceptable and workable deWnition of the term lsquoinvasive speciesrsquo(Thompson et al 1995 Gould 1998 Slobodkin 2001 Davis and Thompson 2001 2002Davis et al 2001 Daehler 2001 Rejmanek et al 2002 Brown and Sax 2004 2005 Casseyet al 2005 Larson 2005) In this pursuit a plethora of terms and deWnitions have been pro-posed that capture the amorphous concept of biological invasion (Williamson 1996 Davisand Thompson 2000 Richardson et al 2000 Pysek et al 2004) but none of these haveproved to be of universal acceptability On each proposal the opposite schools of thoughthave forcefully put forward their point of view often pinpointing an Achillesrsquo heel in eachothersrsquo argument On revisiting the literature of ecological science it becomes undoubtedlyapparent that adoption of terminologies and deWnitions for the conceptualization of scien-tiWc processes or phenomena has resulted in much debate (Tansley 1935 Peters 1991Grimm and Wissel 1997 Pickett and Cadenasso 2002) These scientiWc debates moreoften disagreements are crucial to the progressive evolution of every scientiWc disciplineincluding invasion ecology (Wallington and Moore 2005) However when debates simplyrevolve round semantics the discourses may create more confusion than consensus Veryoften such a semantic split spawns polarization among the scientiWc community and mayipso facto prove detrimental to the progress of a scientiWc discipline in particular and pub-lic policy formulation in general In the Weld of invasion ecology too a recurrent lack ofconsensus on the operational categorization of lsquoinvasive speciesrsquo has impeded progresstowards a fruitful integration of information generated worldwide (SimberloV et al 2005)and hampered collaboration for eVective management of biological invasions (Puth andPost 2005) In this din of criticism and counter-criticism the war against biological inva-sions one of the major drivers of global environmental change has been hampered (Vito-usek et al 1996 Hulme 2003 2006)

In an attempt to forge a broad-based consensus amongst disparate viewpoints Colauttiand MacIsaac (2004) proposed a neutral terminology to deWne lsquoinvasiversquo species TheColautti and MacIsaac model (hereafter referred to as CM model) scrupulously tried toblend together all the previous contributions by developing a hierarchical stage-basedframework of invasion which in essence mirrored the series of steps involved in the actualprocess of biological invasion Theoretical aspects of this model have been thoroughly

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Biodivers Conserv (2008) 173181ndash3194 3183

discussed particularly its promising application in the management of biological invasions(Colautti 2005) The model is still at an early stage of development as little progress hasbeen made in evaluating its applicability in the characterization of alien invasive speciesRecently Lawes et al (2006) have meticulously used the CM model along with two otherpreviously proposed models (Richardson et al 2000 Davis and Thompson 2000) for char-acterization of alien invasive plant species in the Burdekin Catchment Australia spreadover an area of 1700 km While this study evaluated the operational success of these threepublished frameworks for the classiWcation of alien plant species in their study area itfailed to explicitly integrate and make compatible the characterization of alien invasivespecies with the management practices used to address the problem Also the study wasconducted within a relatively small riparian ecosystem so only 66 species could be identi-Wed and characterized In comparison the present study was undertaken at a relatively largeand multi-ecosystem scale and hence resulted in characterization of a large number of alieninvasive plant species Furthermore the study pursued the speciWc objectives of (a) evalu-ation of the applicability of CM model in the characterization of AIS (b) managementimplications of stage-based characterization of AIS and (c) the likely future challenges thatthe CM model shall have to convincingly address for its broad-based applicability in char-acterization and management of biological invasions

Study area

The study area included the Kashmir Himalayan region which is nestled within the north-western folds of the recently designated Global Biodiversity Hotspot of the Himalayas(Mittermeier et al 2005) The region sometimes referred to as lsquoSwitzerland of Asiarsquo liesbetween 32deg 20 to 34deg 50 North latitude and 73deg 55 to 75deg 35 East longitude coveringan area of about 15948 km2 with nearly 64 of mountainous area (Husain 2002) Topo-graphically it includes a deep elliptical bowl-shaped valley bound by the Pir Panjal rangeof Lesser Himalaya in the south and south-west and the Zanskar range of the GreaterHimalaya in the north and north-east The climate of the study area displays a well-markedseasonality akin to inner continental parts of the temperate latitudes The study area expe-riences maximum day temperature of 33degC during summer and a minimum of iexcl5degC duringwinter The region receives an annual precipitation of about 1050 mm mostly in the formof snow during winter months Altitudinal gradient varies from 1600 m (amsl) at Srinagarcity to that of highest peak of lsquoKolahoirsquo glacier at an altitude of 5420 m (amsl) among itssurrounding mountains Owing to this wide altitudinal gradient and varied edapho-climaticand physiographic features the region harbours wide array of habitats including freshwaterlakes wetlands springs ponds swamps marshes streams rivers Xood plains terracedtablelands (lsquoKarewasrsquo) wastelands montane slopes rock outcrops permanent glaciersetc which support equally diverse vegetation types including cultivated pastures and cropWelds plantation stands orchards deciduous scrubs evergreen coniferous forests subal-pine and alpine meadows etc Being situated at the intersection of the Eurasian and Palaeo-tropical bio-realms the region represents just 215 of the total land area of the entireHimalayas but contributes about 2000 (20) plant species to the total Himalayan plantdiversity (Dar et al 2002)

During the ancient past the region was an important stopping point for the trade cara-vans travelling along the erstwhile Silk route starting from Far-East Asia passing throughthe Central Asia to reach the Mediterranean coast and vice versa (Kachroo 1995) Sojournsof European colonists (who ruled Indian sub-continent from mid-eighteenth century to

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3184 Biodivers Conserv (2008) 173181ndash3194

mid-twentieth century) religious missionaries and foreign tourists to Kashmir is anotherreason of intentional and unintentional introduction of alien plants particularly of Euro-pean origin (Khuroo et al 2007) These introduced European Xoristic elements got natural-ized in Kashmir presumably because of considerable climate matching between these tworegions Such historically human-abetted alien plant introductions along with increasinganthropogenic pressures in the recent past due to burgeoning human population unbridledurbanization habitat loss and degradation and eco-unfriendly development activities haveaided in the spread of AIS throughout this Himalayan region Our previous study (Khurooet al 2007) has revealed that a high percentage of alien plants was intentionally introducedas ornamentals Furthermore being mostly mountainous the region provides one of theideal systems to study plant invasions among the biologically diverse but ecologically sen-sitive montane areas (Becker et al 2005) of the developing world

Materials and methods

The present paper is based on our on-going work on alien plant invasions in the IndianKashmir Himalaya and also on our previous study that enabled us to document a compre-hensive database of 571 alien plant species in this region (Khuroo et al 2007) For the pres-ent investigation we deliberately excluded lsquocultivated speciesrsquo ie those alien plantspecies which are under cultivation for a long period of time but have not escaped into thewild in this region Primarily building upon this updated database the present investigationcharacterizes the alien plant species in the study area according to their current stage ofinvasion as expounded in the CM model (Colautti and MacIsaac 2004) excluding theStages 0 and 1 which represent the potential alien invaders (or their propagules) as resi-dents in the nativedonor regions and transport vectors respectively Though theoreticallyuseful practically it is diYcult to identify and characterize alien species at these two stagesof invasion Hence in the present study categorization of AIS in the region commencesfrom the actual process of invasion when the alien species are released to become intro-duced in their non-native range (Stage II) followed by categorization of species in thestages represented by species having the potential to become established (Stage III) Subse-quently the established species may either become widespread but occasional (Stage IVa)or localized but abundant (Stage IVb) Finally those species which were both widespreadand abundant throughout this region were assigned to Stage V In a slight departure fromthe CM model for operational Xexibility without losing objectivity we have intentionallyused the term lsquooccasionalrsquo instead of lsquorarersquo because the latter term has become commoncurrency in the characterization of threatened species

In the present study widespread and localized refer to the extent of spatial spread of par-ticular alien invasive plant species in the Kashmir Himalayan region and for this the fre-quency percentage (FP) across sites in this region has been used Accordingly the AISoccurring in more than 50 of sites were considered as widespread and those with less than50 occurrence in sites were recognized as localized Similarly abundant and occasionalAIS were categorized on the basis of their percentage cover within the sites Accordinglythe AIS showing more than 50 of cover percentage (CP) were regarded as abundant andthose with greater than 10 CP were considered as occasional (Table 1) The descriptorssuch as widespread localized abundant and occasional have been used at the scale ofwhole landscape of the Kashmir Himalayan region which encompasses a range of aquaticand terrestrial ecosystems as detailed above Standard quadrat sizes of 1 5 and 10 m forherbs shrubs and trees respectively were used for estimating the frequency and cover of

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Biodivers Conserv (2008) 173181ndash3194 3185

the alien species We followed Stewart (1972) for plant nomenclature classiWcation andcircumscription of plant species under the families and genera

Results and discussion

The present investigation resulted in identiWcation of 436 plant species distributed among270 genera and 73 families (See Supplementary material Appendix I Table 2) Number ofspecies belonging to diVerent growth forms in the descending order is as follows annualherbs (164) gt perennial herbs (139) gt aquatics (47) gt biennial herbs (27) gt trees(16) gt shrubs (15) gt subshrubs (13) gt climbers (7) gt lianas (6) gt parasitic herbs (2) Num-ber of alien species included in the invasion stages of II III IVa IVb and V is 119 107 5677 and 77 species respectively Relative proportion of the alien species within these Wverecognized stages of invasion in the region is 2729 2454 1283 1767 and 1767respectively (Table 2) Annual herbs with 27 species contribute highest number of speciesto the Stage-V followed closely by perennial herbs with 23 species Aquatic herbs bien-nial herbs subshrubs shrubs and trees belonging to this category are represented by 13 53 1 and 5 species respectively None of the climbers lianas or parasitic herbs is suY-ciently widespread and dominant in the region to qualify for inclusion in Stage V Compar-ison of the relative proportion of species belonging to diVerent invasion stages (Table 2)revealed some interesting patterns For example trees dominate Stage V (3125) fol-lowed by aquatics subshrubs biennial herbs perennial herbs annual herbs and shrubs withrelative proportion of 2766 2308 1852 1655 1646 and 667 respectively The rela-tively higher proportion of trees at the Stage V of invasion may probably be due to inten-tional introduction of trees for aVorestationplantation purposes with full support of thestate governmental agencies The higher proportion of aquatics at the Stage V may bepartly because of water being an eYcient vector for dispersal and also due to the weakerbarriers to establishment and spread in aquatic ecosystems (Galatowitsch 2004) In thesame way within the 77 species recognized at Stage IVb the annual and perennial herbslead with 27 and 26 species respectively but shrubs and trees with relative proportion of40 and 25 respectively are dominantly represented This stage does not include any

Table 1 The stages of invasion recognized after CM model with their description and criterion used for char-acterization of alien invasive Xora in the Kashmir Himalaya

Frequency percentage (FP) is a measure of occurrence across sites while cover percentage (CP) is a measureof abundance within sites

Stage of invasion

Description Our criterion

Stage 0 Potential AIS (or their propagules) in their native range(s) Not appliedStage I Potential AIS (or their propagules) in the transport vector(s) Not appliedStage II AIS (or their propagules) released and introduced into

their non-native range(s)lt10 FP amp lt10 CP

Stage III AIS that reproduce and establish their populations in the non-native range(s)

lt20 FP amp lt10 CP

Stage IVa AIS become widespread in distribution but form populations with limited number of individuals

gt50 FP amp gt10 CP

Stage IVb AIS remain localized in distribution but form abundant populations

lt50 FP amp gt50 CP

Stage V AIS become widespread in distribution and form abundant populations

gt50 FP amp gt50 CP

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3186 Biodivers Conserv (2008) 173181ndash3194

climbers lianas or parasitic herbs It is pertinent to mention here that the woody plantssuch as trees and shrubs have been also reported to be common invaders at the global scale(Weber 2003 Pysek 2004)

The contrasting patterns between absolute number of species and relative proportion ofspecies belonging to diVerent growth forms in the alien Xora of the Kashmir Himalaya arediscernible at other stages of invasion (IVa III and II) as well Perusal of the results per-taining to species distribution belonging to these stages of invasion reveal some importantWndings such as (a) no subshrub shrub tree or parasitic herb has reached Stage IVa ofinvasion (b) for each of the recognized growth forms the major proportion of species areat Stage III particularly the aquatics with a percentage of 4255 (c) in terms of relative pro-portion climbers lianas and parasitic herbs have more than half of their representatives atStage II and (d) annual herbs show signiWcantly higher representation of species at StageII not only in terms of number but also in terms of relative proportion

In distinction to previous models (Richardson et al 2000 Kolar and Lodge 2001) theCM model recognizes three discrete stages (Stages IVa IVb V) for characterization ofinvasive plant species after their establishment Such species categorization makes opera-tional sense of what is practically observed in the natural landscape of our study area andexpectedly elsewhere in the world To bring home this point we here exemplify the case ofthree Asteraceous alien plant species in our region namely Cichorium intybus Centaureaiberica and Anthemis cotula In our previous study (Khuroo et al 2007) we had character-ized these three as lsquoinvasiversquo species (sensu Pysek et al 2004) notwithstanding signiWcantdiVerences in the nature and magnitude of their invasion For example individuals ofCichorium intybus are widely distributed among diverse habitats throughout the KashmirHimalayan region but rarely form abundant populations and occur as occasional individu-als Conversely Centaurea iberica forms abundant populations but is largely localized to afew habitats only Conversely Anthemis cotula is widespread across many habitats all overthe region and characteristically forms abundant populations In addition to these three spe-cies numerous examples of other alien species in the region display diVerences in theirspatial spread and population abundances Though such species could be categorized aslsquoinvasivesrsquo (sensu Pysek et al 2004) they need to be further categorized in a manner thatmirrors the diVerences in their abundance and spatial distribution in the region Thus thedistinction of three stages (Stages IVa IVb and V) in the CM model is highly suitable forranking such invasive species that vary in their spatial spread and local abundance Whilst

Table 2 Distribution of alien plant species of various growth forms belonging to diVerent stages of invasionin the Kashmir Himalaya (within parenthesis is given the relative proportion of species)

Growth form

Stage II Stage III Stage IVa Stage IVb Stage V Total

A 58 (3537) 29 (1768) 23 (1403) 27 (1646) 27 (1646) 164 (3761)P 35 (2518) 33 (2374) 22 (1583) 26 (1871) 23 (1655) 139 (3188)Aq 4 (851) 20 (4255) 3 (638) 7 (1489) 13 (2766) 47 (1078)B 3 (1111) 8 (2963) 6 (2222) 5 (1852) 5 (1852) 27 (619)T 4 (2500) 3 (1875) 0 (00) 4 (250) 5 (3125) 16 (367)S 4 (2667) 4 (2667) 0 (00) 6 (4000) 1 (667) 15 (344)Ss 3 (2308) 5 (3846) 0 (00) 2 (1538) 3 (2308) 13 (298)C 4 (5714) 2 (2857) 1 (1428) 0 (00) 0 (00) 7 (160)L 3 (5000) 2 (3333) 1 (1667) 0 (00) 0 (00) 6 (138)Ps 1 (5000) 1 (5000) 0 (00) 0 (00) 0 (00) 2 (046)Total 119 (2729) 107 (2454) 56 (1283) 77 (1767) 77 (1767) 436

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3186 Biodivers Conserv (2008) 173181ndash3194

climbers lianas or parasitic herbs It is pertinent to mention here that the woody plantssuch as trees and shrubs have been also reported to be common invaders at the global scale(Weber 2003 Pysek 2004)

The contrasting patterns between absolute number of species and relative proportion ofspecies belonging to diVerent growth forms in the alien Xora of the Kashmir Himalaya arediscernible at other stages of invasion (IVa III and II) as well Perusal of the results per-taining to species distribution belonging to these stages of invasion reveal some importantWndings such as (a) no subshrub shrub tree or parasitic herb has reached Stage IVa ofinvasion (b) for each of the recognized growth forms the major proportion of species areat Stage III particularly the aquatics with a percentage of 4255 (c) in terms of relative pro-portion climbers lianas and parasitic herbs have more than half of their representatives atStage II and (d) annual herbs show signiWcantly higher representation of species at StageII not only in terms of number but also in terms of relative proportion

In distinction to previous models (Richardson et al 2000 Kolar and Lodge 2001) theCM model recognizes three discrete stages (Stages IVa IVb V) for characterization ofinvasive plant species after their establishment Such species categorization makes opera-tional sense of what is practically observed in the natural landscape of our study area andexpectedly elsewhere in the world To bring home this point we here exemplify the case ofthree Asteraceous alien plant species in our region namely Cichorium intybus Centaureaiberica and Anthemis cotula In our previous study (Khuroo et al 2007) we had character-ized these three as lsquoinvasiversquo species (sensu Pysek et al 2004) notwithstanding signiWcantdiVerences in the nature and magnitude of their invasion For example individuals ofCichorium intybus are widely distributed among diverse habitats throughout the KashmirHimalayan region but rarely form abundant populations and occur as occasional individu-als Conversely Centaurea iberica forms abundant populations but is largely localized to afew habitats only Conversely Anthemis cotula is widespread across many habitats all overthe region and characteristically forms abundant populations In addition to these three spe-cies numerous examples of other alien species in the region display diVerences in theirspatial spread and population abundances Though such species could be categorized aslsquoinvasivesrsquo (sensu Pysek et al 2004) they need to be further categorized in a manner thatmirrors the diVerences in their abundance and spatial distribution in the region Thus thedistinction of three stages (Stages IVa IVb and V) in the CM model is highly suitable forranking such invasive species that vary in their spatial spread and local abundance Whilst

Table 2 Distribution of alien plant species of various growth forms belonging to diVerent stages of invasionin the Kashmir Himalaya (within parenthesis is given the relative proportion of species)

Growth form

Stage II Stage III Stage IVa Stage IVb Stage V Total

A 58 (3537) 29 (1768) 23 (1403) 27 (1646) 27 (1646) 164 (3761)P 35 (2518) 33 (2374) 22 (1583) 26 (1871) 23 (1655) 139 (3188)Aq 4 (851) 20 (4255) 3 (638) 7 (1489) 13 (2766) 47 (1078)B 3 (1111) 8 (2963) 6 (2222) 5 (1852) 5 (1852) 27 (619)T 4 (2500) 3 (1875) 0 (00) 4 (250) 5 (3125) 16 (367)S 4 (2667) 4 (2667) 0 (00) 6 (4000) 1 (667) 15 (344)Ss 3 (2308) 5 (3846) 0 (00) 2 (1538) 3 (2308) 13 (298)C 4 (5714) 2 (2857) 1 (1428) 0 (00) 0 (00) 7 (160)L 3 (5000) 2 (3333) 1 (1667) 0 (00) 0 (00) 6 (138)Ps 1 (5000) 1 (5000) 0 (00) 0 (00) 0 (00) 2 (046)Total 119 (2729) 107 (2454) 56 (1283) 77 (1767) 77 (1767) 436

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Biodivers Conserv (2008) 173181ndash3194 3187

capturing the actual invasion status of the alien species in the Weld the CM model as it isbased on operationally objective criteria helps to a great extent in achieving universaluniformity in the characterization of alien invasive species This important feature of theCM model is amply demonstrated by the present study

Linking AIS characterization with their management

Most of the comparative studies on alien invasive biota since being based on divergenthypotheses and unequal study units are fraught with non-reproducibility among the organ-isms as well as across diVerent spatio-temporal scales This has proved to be an intractableimpediment in the development of an eVective management strategy against biologicalinvasions Also it is for this reason that a meaningful organization and synthesis ofknowledge with a Xexible inter-operational compatibility across taxa and regions isincreasingly recognized as one of the formidable challenges in invasion ecology (Meyersonand Mooney 2007) Against this backdrop the CM model as evaluated in the present studyhas practical relevance in the sound systematic sustainable and successful management ofbiological invasion

By laying emphasis on the population abundance and geographical spread of AIS deter-mined by the biotic and abiotic Wlters along the continuum of invasion process the modelhas the advantage of linking the science of invasion ecology with its management andthereby oVers an integrated approach for applying a more holistic management strategy Inaddition to its role in explicating the general patterns and processes involved in biologicalinvasion such an approach of characterization of alien biota can not only implicate thealready established invasive species that warrant immediate action but also would paveway for identiWcation of potential AIS which though not of immediate environmental andeconomic concern in the aVected region merit a vigilant monitoring Through the recogni-tion of a cascade of stages comprising the process of invasion the use of CM model allowsconsideration of the entire range of alien biota which permits development and implemen-tation of a cost-eVective management strategy with a long-term planning and monitoringapproach at the ecosystem and landscape scale (Williamson 2006) The inclusion and char-acterization of stages prior to widespread occurrence and abundance of AIS are of pivotalimportance in the development of workable early warning and quick response protocolsThis enables formulation and implementation of an eVective management strategy againstthe most troublesome groups of AIS without losing sight of those alien species which arecurrently at the initial stages of invasion As the species move up the ladder of invasionstages management options become limited as eradication is often diYcult if not impossi-ble in case of established AIS (Hulme 2006) Furthermore from an economic perspectivethe CM model also provides rational criteria for identifying priority alien species needingimmediate attention and thus enables eYcient allocation of often scarce Wnancialresources Such broad management implications of the model assume signiWcance in viewof the non-uniform and imprecise usage of terms in the discipline of invasion biology

A proposal for lsquo4Prsquo management framework against biological invasions

Perusal of literature pertaining to management of biological invasions reveals that someterms are used interchangeably limiting their practicality in the eVective management ofbiological invasions (Table 3) For instance the quarantine screening and early detection

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3188 Biodivers Conserv (2008) 173181ndash3194

protocols make practical sense at the level of prediction of alien invasions rather than atthe prevention and prescription level Similarly eradication containment and control mea-sures are prescriptive tools and have little relevance at the level of prediction In an attemptto bring order to this management maze the present study proposes an operational frame-work for the management of biological invasions Based on insights gained from the pres-ent investigation we have mainly focused our eVorts to make management a broad-basedstrategy with precise and on-target management toolsprotocols that are relevant to a partic-ular stage(s) of invasion Taking a cue from the successful lsquo4Prsquo (product place price andpromotion) marketing mantra in business management (McCarthy and Perrault 1993) wehere suggest a management mix of 4Ps namely prediction prevention prescription andpublic awareness to stem the tide of biological invasions This management frameworkhowever can be successfully implemented only when the entire alien invasive biota of aregion is characterized in terms of their current stage of invasion (sensu CM model) Asdone in the present study characterization of entire alien invasive Xora by applying the CMmodel practically helps in the hierarchical coupling of species at a particular stage of inva-sion with an appropriate management option In spite of our personal research expertise onthe plants the applicability of this management framework can be evaluated in other taxo-nomic groups too

Prediction the Wrst line of defence

As an eVective Wrst line of defence prediction of AIS has to be made robust and precise(Kolar and Lodge 2001) so that a stringent quarantine regime is established Also a need isfelt to not only speciWcally predict the negative consequences of an alien species but also toestimate the probability of such negative impacts At present most workers advocate thelsquoguilty until proven innocentrsquo approach Furthermore intentional and unintentional intro-ductions present diVerent challenges and consequently need to be addressed diVerently(SimberloV et al 2005) For instance it is not so diYcult to restrict the deliberate introduc-tion of alien species that have caused more harm than good in regions where they were

Table 3 A summary of the management strategies with available tools and protocols relevant at diVerentstages of invasion sensu CM model

Management strategy Management protocols and tools Stage(s) of invasion

Prediction Quarantine screening at entry points I II amp IIIEvaluation of source biotaClimate matching assessmentPrecautionEarly detection

Prevention Risk analysis III amp IVbEarly warning systemRapid response and actionEradication exclusion

Prescription Containment control elimination mitigation adaptation

IVa IVb amp V

Public awareness Informed policy decisions eVectivemonitoring regimes public educationand awareness campaigns prioritization eVorts restoration plans

I II III IVa IVb amp V

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Biodivers Conserv (2008) 173181ndash3194 3189

previously introduced Conversely those alien species that are inadvertently introduced arediYcult to deal with as these species hitchhike on people or on commercial products orcryptically use the pathways that people utilize for diVerent purposes (roads highways bal-last water) Since it is not possible to prevent and restrict all unintentional introductions theoption left is to identify rank and interrupt the vectors and pathways so that such introduc-tions are predicted at the earliest stage of invasion and then immediately prevented (Ruizand Carlton 2003) To make it a reality global coordination and networking for informa-tion sharing regarding the worldrsquos worst invasives and other potential invaders assumesurgency (SimberloV et al 2005)

Prevention an ounce of prevention is better than a dollar of cure

In view of the limited capacity of the screening models to accurately predict AIS particu-larly unintentional species introductions it is very likely that one or more alien species mayescape detection and get introduced into the non-native range Even if its negative impactsare not well characterized the individuals of such species upon their detection need to beprevented from becoming established (Wittenberg and Cock 2001) Although this soundsuncomplicated in practice such rapid response is far from rapid because of the constraintsthat beset identifying the target species and occasional occurrence of alien species duringthe initial stages of invasion (Stage II amp III) However development of cutting-edge remotesensing technologies such as hyperspectral imagery at 2-m spatial resolution couldcontribute to major advances in invasive species management (Lass et al 2005) Aerialphotography can even be used to detect individuals as well as the population structure ofalien invasive plants (Mullerova et al 2005) Hence at a coarse scale extent of geographi-cal spread and population abundance can be eVectively mapped by employing the geo-spa-tial modelling techniques For example such an approach can provide unprecedentedopportunities for monitoring of those alien invasive plant species that have tree and shrubgrowth forms Nonetheless for the cryptic small scattered or highly mobile speciesremote sensing may have limitations and the only option is ground-based Weld surveys

Preventive measures can be successful only when we are able to accurately predict theinvasions assess the risks involved sound the early warning bells initiate rapid response tothe threats and launch immediate eradication of potential alien invasive species Experiencehas shown that eradication which involves complete removal of AIS can work only forsmaller areas Also eradication should not do more harm than good (Myers et al 2000) Asis evident from the present study prevention can be meaningful and a realistic goal if kick-started against the alien species at the Stages III and IVb It is diYcult to prevent those alienspecies which have advanced to Stage IVa of invasion cascade because they occur widelythroughout the region although less abundantly

Prescription even if prevention fails still it is never too late to cure

When the AIS spread throughout the landscape the only management option left is to curethe problem Prescription can involve containment and control measures that ultimatelyaim at mitigation of the harmful impacts While as the containment measures aim at mini-mizing the spread of alien invasives from the Stage III onwards the control measuresattempt to obtain long-term reduction in the population size at a lsquobenignrsquo level (Table 3)SimberloV (2002) recognized four main methods namely physical and mechanical control

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3190 Biodivers Conserv (2008) 173181ndash3194

chemical control biological control and ecosystem management for addressing alieninvasions Recently Hulme (2006) has grouped these prescriptive methods into threemutually inclusive approaches in order to keep an alien invasive species at reasonablylower levels

Public awareness linking science to society

Meeting the challenge of established invasive species and future introductions of AIS requirespublic education research policy development and enforcement The most critical gap is inthe areas of policy development and enforcement which need to be supported by forcefulpublic awareness and educational campaigns Public awareness of the ecological economicand health risks from AIS is essential to successful implementation of policy and enforce-ment especially because until the past decade or so conservation biologists resource manag-ers foresters and others were often complacent about introduced alien species

Notwithstanding the serious economic and environmental damages caused by AIS(Pimentel et al 2005) the survey conducted by Colton and Alpert (1998) revealed thateven among relatively well-educated public visitors to botanical gardens and museumsonly a minority supported greater eVorts to control invasive plants Their survey alsoshowed limited familiarity with the concept of biological invasion or the related conceptof biodiversity Such lack of awareness among the policy planners and general public isstill prevalent particularly in developing countries Although several countries havepromulgated legislation intended to discourage the movement of crop pests very few haveany overall legal authority for dealing speciWcally and eVectively with the problem ofbiological invasions Even the agreements that focus speciWcally on ecological problemshave generally given biological invasions short shrift Although the Millennium Ecosys-tem Assessment (MEA) and COP 6 of the CBD urge all member states to pay particularattention to the prevention of the harmful impacts of AIS more ambitious activities areneeded to halt the unprecedented increase in the transport of alien species to non-nativeranges

The dismal policy framework for management of AIS in developing countries isbecause the study of biological invasion even today is an obscure and rather fracturedenterprise and it is diYcult to locate critical information or relevant expertise Thus a data-base that consolidates existing information with a free public access on the World WideWeb is much needed The database could stimulate the production of new media to encour-age additional research and synthesis and help in dissemination of information and aware-ness about biological invasions among the policy makers public and private decisionmakers land managers educators and local community leaders

Future challenges

The suitability of applying the CM model to the characterization of alien invasive plantswas undertaken in the present study For more broad-based applications this model needsto be applied to alien species belonging to other taxonomic groups such as mammalsinsects ants or microorganisms Even within the same taxonomic group (for instance vas-cular plants) invasive species of diVerent growth forms (eg herbs shrubs trees) have var-iable impacts on biotic interactions and community dynamics and consequently there is aneed to have globally acceptable quantitative standards to account for growth form

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Biodivers Conserv (2008) 173181ndash3194 3191

diVerences when assigning the species to a particular invasion stage Moreover a wholebiota-centric approach rather than the prevalent single alien species-centric approach needsto be followed if we have to make any appreciable progress in eVective management ofbiotic invasions Furthermore we believe that the suggested framework for management ofbiological invasions including four fundamental lsquoarsenals of invasion combat strategyrsquocan catalyze the formulation of objective protocols and on-target tools for an eVectivemodus operandi against the alien invasive species

Notwithstanding its claim of being more objective than previous models those using theCM model must make some subjective decisions for its operational utility In sciencedespite its emphasis on achieving objectivity subjectivity cannot be entirely eliminatedbut instead can be minimized (Stern 2005 Noss 2007) For instance although the presentstudy has recognized diVerent stages a clear-cut demarcation line between each stage ofinvasion is not discernible Because the diVerent stages of biological invasions represent acontinuum it is never possible to disentangle the diVerent stages in a strict objective senseFor this reason the quantitative criteria used for characterizing terms such as widespreadand localized for denoting the extent of geographical spread and abundant and occasionalfor the populational dominance have been used with reference to the Kashmir HimalayaAlso such an explication is important in view of the critical importance of the scale formeaningful comparison of ecological studies easier replication and better interpretation ofthe results generated across the taxa and within the ecosystems With such caveats in mindwe believe that tangible progress in the management of AIS entails upon the adoption ofexpansive notions of objectivity rather than strict empiricist version and espousal of aninteractive activity in which multiple forms of reasoning and evidence together withcritical discussion take place among a diverse scientiWc community (Wallington and Moore2005) so as to arrive at meaningful conclusions in respect of the management of biologicalinvasions

Conclusions

The present study establishes that the CM model provides a holistic framework by suc-cessfully merging together the concepts of both species invasiveness and communityinvasibility with a cross-linkage of probable vectors and possible Wlters As investigatedin the present study the model is plausible practicable promising and progressive way-forward towards universal standardization of terminology for deWning the alien invasivespecies in the dimensions of both time and space By presenting a mechanistic explana-tion the model oVers an improved understanding of biological invasions and makes possi-ble robust generalizations and sound conclusions Looking ahead we believe that testingthe applicability of this model in the characterization of alien invasive biota among a vari-ety of taxonomic groups and growth forms and across diverse ecosystems and ecoregionscould engender speciWc problems but the resultant follow-up research is likely to lead topossible solutions Such an exercise will hopefully improve the model and make it morewidely useful radically improving our ability in systematic management of biologicalinvasions

Acknowledgements We are greatly thankful to Drs Robert I Colautti Philip E Hulme and Curtis CDaehler for their valuable comments on the earlier versions of manuscript Authors are thankful to HeadDepartment of Botany University of Kashmir Srinagar J amp K India for providing necessary facilities dur-ing the course of this study We are also grateful to our colleagues working in the Weld of invasion biologyfor their helpful comments and fruitful discussion

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3192 Biodivers Conserv (2008) 173181ndash3194

References

Becker T Dietz H Billeter R Buschmann H Edwards PJ (2005) Altitudinal distribution of alien plant speciesin the Swiss Alps Perspect Plant Ecol Evol Syst 7173ndash183

Brown JH Sax DF (2004) An essay on some topics concerning invasive species Aust Ecol 29530ndash536Brown JH Sax DF (2005) Biological invasions and scientiWc objectivity Reply to Cassey et al (2005) Aust

Ecol 30481ndash483Cadotte MW McMahon SM Fukami T (eds) (2006) Conceptual ecology and invasions biology reciprocal

approaches to nature Springer Verlag BerlinCassey P Blackburn TM Duncan RP Chown SL (2005) Concerning invasive species reply to Brown and

Sax Aust Ecol 30475ndash480Colautti RI (2005) In search of an operational lexicon for biological invasion In Inderjit (ed) Invasive plants

ecological and agricultural aspects Birkhausar Verlag Basal Switzerland pp 1ndash15Colautti RI MacIsaac HI (2004) A neutral terminology to deWne lsquoinvasiversquo species Divers Distrib 10135ndash141

doi101111j1366-9516200400061xColton TF Alpert P (1998) Lack of public awareness of biological invasions by plants J Nat Areas 18262ndash266Daehler CC (2001) Two ways to be an invader but one is more suitable for ecology ESA Bull 82101ndash102Dar GH Bhagat RC Khan MA (2002) Biodiversity of the Kashmir Himalaya Valley Book House Srinagar IndiaDavis MA Thompson K (2000) Eight ways to be a colonizer two ways to be an invader a proposed nomen-

clature scheme for invasion ecology ESA Bull 81226ndash230Davis MA Thompson K (2001) Invasion terminology should ecologists deWne their terms diVerently than

others No not if we want to be of any help ESA Bull 82206Davis MA Thompson K (2002) lsquoNewcomersrsquo invade the Weld of invasion ecology question the Weldrsquos future

ESA Bull 83196ndash197Davis MA Thompson K Grime JP (2001) Charles S Elton and the dissociation of invasion ecology from the

rest of ecology Divers Distrib 797ndash102 doi101046j1472-4642200100099xDevine R (1998) Alien invasions Americarsquos battle with non-native animals and plants National Geographic

Press Washington DC USADrake JA Mooney HA di Castri F Groves RH Kruger FJ Rejmanek M et al (eds) (1989) Biological invasions

a global perspective Wiley New YorkGalatowitsch S (2004) Invasive aquatic species of Europe Divers Distrib 10313ndash314 doi101111j1366-

9516200400098xGould SJ (1998) An evolutionary perspective on strengths fallacies and confusions in the concept of native

plants Arnoldia 5811ndash19Grimm V Wissel C (1997) Babel or the ecological stability discussions an inventory and analysis of termi-

nology and a guide for avoiding confusion Oecologia 109323ndash334 doi101007s004420050090Hierro JL Maron JL Callaway RM (2005) A biogeographical approach to plant invasions the importance of

studying exotics in their introduced and native range J Ecol 935ndash15 doi101111j0022-0477200400953x

Hulme PE (2003) Biological invasions winning the science battles but losing the conservation wars Oryx37178ndash193 doi101017S003060530300036X

Hulme PE (2006) Beyond control wider implications for the management of biological invasions J ApplEcol 43835ndash847 doi101111j1365-2664200601227x

Husain M (2002) Geography of Jammu and Kashmir Rajesh Publications New Delhi IndiaInderjit Cadotte MW Colautti RI (2005) The ecology of biological invasions past present and future In

Inderjit (ed) Invasive plants ecological and agricultural aspects Birkhausar Verlag Basal Switzerlandpp 19ndash43

Kachroo P (1995) Central Asia and Kashmir Himalaya-Archaeobotany and Floristics ScientiWc PublishersJodhpur India

Kaiser J (1999) Stemming the tide of invading species Science 2851836ndash1841 doi101126science28554351836

Khuroo AA Rashid I Reshi Z Dar GH Wafai BA (2007) The alien Xora of Kashmir Himalaya Biol Invasions9269ndash292 doi101007s10530-006-9032-6

Kolar CS Lodge DM (2001) Progress in invasion biology predicting invaders Trends Ecol Evol 16199ndash204doi101016S0169-5347(01)02101-2

Larson DL (2005) Native weeds and exotic plants relationships to disturbance in mixed-grass prairie PlantEcol 169317ndash333 doi101023A1026046810307

Lass LW Prather TS Glenn NF Weber KT Mundt JT Pettingill J (2005) A review of remote sensing of invasiveweeds and examples of the early detection of spotted knapweed (Centaurea maculosa) and babysbreath(Gypsophila paniculata) with a hyperspectral sensor Weed Sci 53242ndash251 doi101614WS-04-044R2

1 C

Biodivers Conserv (2008) 173181ndash3194 3193

Lawes RA Murphy HT Grice AC (2006) Comparing agglomerative clustering and three weed classiWcationframeworks to assess the invasiveness of alien species across spatial scales Divers Distrib 12633ndash644doi101111j1472-4642200600291x

Mack RN SimberloV D Lonsdale WM Evans H Clout M Bazzaz FA (2000) Biotic invasions causesepidemiology global consequences and control Ecol Appl 10689ndash710 doi1018901051-0761(2000)010[0689BICEGC]20CO2

McCarthy EJ Perrault WD (1993) Basic marketing a global managerial approach Richard D Irwin USABurr Ridge IL

McNeely JA Mooney HA Neville LE Schei PJ Waage JK (eds) (2001) Global strategy on invasive alienspecies IUCN Gland

Meyerson LA Mooney HA (2007) Invasive alien species in an era of globalization Front Ecol Environ5199ndash208 doi1018901540-9295(2007)5[199IASIAE]20CO2

Mittermeier RA Gil PR HoVmann M Pilgrim J Brooks T Mittermeier CG Lamoreux J Da Fonseca GAB(2005) Hotspots revised Earthrsquos biologically richest and most threatened terrestrial ecoregions Conser-vation International (httpwwwbiodiversityhotspotsorg)

Mooney HA Mack RN McNeely JA Neville LE Schei PJ Waage JK (2005) Invasive alien species a newsynthesis Island Press Washington DC

Moore PD (2000) Alien Invaders Nature 403492ndash493 doi10103835000686Mullerova J Pysek P Jarosik V Pergl J (2005) Aerial photographs as a tool for assessing the regional dynam-

ics of the invasive plant species Heracleum mantegazzianum J Appl Ecol 421042ndash1053 doi101111j1365-2664200501092x

Myers JH SimberloV D Kuris AM Carey JR (2000) Eradication revisited dealing with non-indigenousspecies Trends Ecol Evol 15316ndash320 doi101016S0169-5347(00)01914-5

Noss RF (2007) Values are good thing in conservation biology Conserv Biol 2118ndash20 doi101111j1523-1739200600637x

Perrings C Williamson M Dalmazzone S (eds) (2000) The economics of biological invasion Edward ElgarCheltenham UK

Peters RH (1991) A critique for ecology Cambridge University Press CambridgePickett STA Cadenasso ML (2002) The ecosystem as a multidimensional concept meaning model and

metaphor Ecosystems (N Y Print) 51ndash10 doi101007s10021-001-0051-yPimentel D Zuniga R Morrison D (2005) Update on the environmental and economic costs associated with

alien-invasive species in the United States Ecol Econ 52273ndash288 doi101016jecolecon200407013Preston G Brown G van Wyk E (eds) (2000) Best management practices for preventing and controlling inva-

sive alien species The Working for Water Programme Cape Town South AfricaPuth LM Post DM (2005) Studying invasion have we missed the boat Ecol Lett 8715ndash721 doi101111

j1461-0248200500774xPysek P (2004) The most complete global overview of invasive species in natural areas Divers Distrib

10505ndash507 doi101111j1366-9516200400128xPysek P Prach K Rejmanek M Wade M (eds) (1995) Plant invasions general aspects and special problems

SPB Academic Publishing Amsterdam NLPysek P Richardson DM Rejmanek M Webster GL Williamson M Kirschner J (2004) Alien plants in check-

lists and Xora towards better communication between taxonomists and ecologists Taxon 53131ndash143doi1023074135498

Raghu S Anderson RC Daehler CC Davis AS Wiedenmann RN SimberloV D et al (2006) Adding biofuelsto the invasive species Wre Science 3131742 doi101126science1129313

Rejmanek M Richardson DM Barbour MG Crawley MJ Hrusa GF Moyle PB et al (2002) Biological inva-sions politics and the discontinuity of ecological terminology ESA Bull 83131ndash133

Richardson DM Pysek P Rejmanek M Barbour MG Panetta FD West CJ (2000) Naturalization and invasionof alien plants concepts and deWnitions Divers Distrib 693ndash107 doi101046j1472-4642200000083x

Ruiz G Carlton JT (eds) (2003) Invasive species vectors and management strategies Island Press WashingtonSanderlund O Schei P Viken A (eds) (1999) Invasive species and biodiversity management Kluwer DordrechtSimberloV D (2002) Managing established populations of alien species In Claudi R Nantel P Muckle-JeVs

E (eds) Alien invaders in Canadarsquos waters wetlands and forests Natural Resources Ottawa CanadaSimberloV D Parker IM Windle PN (2005) Introduced species policy management and future research

needs Front Ecol Environ 3(1)12ndash20Slobodkin LB (2001) The good the bad and the reiWed Evol Ecol Res 31ndash13Stern PC (2005) Deliberative methods for understanding environmental systems Bioscience 55976ndash982

doi1016410006-3568(2005)055[0976DMFUES]20CO2Stewart RR (1972) An annotated catalogue of the vascular plants of West Pakistan and Kashmir Fakhri Press

Karachi Pakistan

1 C

3194 Biodivers Conserv (2008) 173181ndash3194

Tansley AG (1935) The use and abuse of vegetational concepts and terms Ecology 16284ndash307 doi1023071930070

Thompson K Hodgson JG Rich TCG (1995) Native and alien invasive plants more of the same Ecography18390ndash402 doi101111j1600-05871995tb00142x

Vitousek PM DrsquoAntonio CM Loop LL Westbrooks R (1996) Biological invasions as global environmentalchange Am Sci 84468ndash478

Wallington TJ Moore SA (2005) Ecology values and objectivity advancing the debate Bioscience 55873ndash878doi1016410006-3568(2005)055[0873EVAOAT]20CO2

Weber E (2003) Invasive plant species of the world a reference guide to environmental weeds CABIPublishing Wallingford

Williamson M (1996) Biological invasions Chapman amp Hall LondonWilliamson M (2006) Explaining and predicting the success of invading species at diVerent stages of invasion

Biol Invasions 81561ndash1568 doi101007s10530-005-5849-7Wittenberg R Cock MJW (eds) (2001) Invasive alien species a toolkit for best prevention and management

practices CAB International Publishing Wallingford UK

1 C