Weerl Re.seareti. 1986, Volume 26. .151-364

Characteristics distinguishing invasive weeds withinEchium (Bugloss)

F, FORCELLA. J. T. WOOD ANDS. P. DILLON * North Central Soil ResearchLaboratory, USDA-ARS. Morris MN 56267.U.S.A., and *CSIRO-Austratia Divisions ofMathematics and Statistics, and Ptant Industry,Canberra ACT 260]

Accepted 28 February 1986

Summary: Resume: Zusammenfassung

Plant quarantine agencies attempt to regulate thecontinuing worldwide problem of spread of alienplants, but systems of plant quarantine have notbeen based entirely on objective criteria. Com-parative epidemiological research of known alienweeds may provide such criteria and therebyimprove the success of plant quarantine. For thisreason biogeographical and ecophysiologicaldata were gathered and analyzed for Echium(Boraginaceae), especially for the three differen-tially distributed and weedy species in Australia:E. itaticum L. (rare), E. vutgare L. (uncommon).and B. ptantagineum L. (common). Such dataincluded the following: native distributions inEurasia and North Africa, historical spread inAustralia, seed germination, vegetative growthand propensity to flower. Quantitative plantcharacteristics which distinguish weedy species ofEehium from their innocuous counterparts, andwhose values could most easily be determined byplant quarantine officials, are the breadth ofnative distribution and rapidity of seed germina-tion. Although these results were derived fromonly a few temperate taxa, they may apply inprinciple to many species.

Caraeteres distinctifs des mauvaises herbes enva-hissantes dans le genre Echium

Des agences de mise en quarantaine de vegetauxs'attachent a controler le probleme permanent a

travers le monde de la propagation des vegetauxetrangers: cependant, les systemes de quarantainen'ont pas ete etablis exclusivement sur des criteresobjectifs. Des etudes d'epidemiologie compara-tives pour des adventiees etrangeres connuespeuvent fournir de tels criteres et ainsi accroitre lesucces dc la mise en quarantaine des vegetaux.Pour cette raison. des donnces biogeographiqueset ecophysiologiques ont ete regroupees et analy-sces pour le genre Echium (Boraginacee). enparticulier pour trois especes de mauvaises herbesdifferemment reparties en Australie: E. itaticumL. (rare), E. vutgare L. (peu repandu), E. ptantagi-neum L, (eommun). Parmi ces donnees. on trou-vait les suivantes: repartition originelle en Eurasieet en Afrique du Nord, historique de la propaga-tion en Australie. germination des semences,croissance vegetative et propension a fleurir. Lescaracteristiques quantifiables qui permettraientde distinguer les especes nuisibles d'Echium deleurs equivalents inoffensifs et dont les valeurspourraient tres aisement etre determinees par lesorganismes officiels responsables des quaran-taines sont: Pampleur de la distribution d'origineet la rapidite de la germination des semences. Bienque ces resultats proviennent de seulement quel-ques taxons. ils peuvent ctre appliques, en prin-cipe. a de nombreuses especes.

Merkmale zur Definition schadticher Arten in derGattung Echium (Natterkopf)

Pflanzenquarantaneamter versuchen das welt-weite Problem der Ausbreitung von eingeschlep-pten Pflanzen zu kontrollieren; die Quarantan-evorschriften sind jedoeh nicht vollig auf objektiverfassbare Kriterien abgestutzt. Vergleichendeepidemiologische Erforschung von Adventiv-pflanzen kann derartige Kriterien liefern unddamit den Nutzeffekt von Quarantanemassnah-men verbessern. Zu diesem Zweck wurden fur dieGattung Eehium (Boraginaceen) biogeogra-phische und okophysiologische Daten gesammeltund analysiert; es wurden dabei speziell die drei inAustralien als Unkrater geltendcn und verschie-

352 F. Foreetta, J. T. Wood and S. P. Ditton

den verbreiteten Arten E. itaticum L. (selten).E. vutgare L. (gelegentilich vorkommend) und E.ptantagineum L. (haufig) untersucht. Der Daten-katalog enthielt Angaben uber: die ursprunglicheVerbreitung in Eurasien und N-Afrika. Ges-chichte der Ausbreitung in Australien. Samenkei-mung, vegetatives Waehstum und Bluhbereits-chaft. Der Ausdehnungsbereich derursprunglichen Vorkommen und die Geschwin-digkeit der Samenkeimung sind quantitativerfassbare. durch Quarantanebcamte leicht zubewertende, Kriterien zur Unterscheidung zwi-schen unschadliehen und als Unkrauter schadli-chen Eehium-XrX.cn. Obwoh! diese Ergebnisse nurvon relativ wenigen, unter tempcrierten Be-dingungen vorkommenden, taxonomischcn Ein-heiten abgeleitet worden sind. mogen sie imPrinzip fur viele Arten Gultigkeit haben.

Introduction

Most countries are hosts to increasing numbers ofalien plants [e.g.. Australia (Specht, 1981)|, butonly some of these new introductions are likely tobecome serious weeds (Forcella & Harvey, 1983),How will potentially serious weeds be identified?This is an important question, because only theseplants should merit expensive research and con-trol programmes. Weed epidemiology is a subjectwhich embraces this problem through determina-tions of (1) probabilities of plant introduction,establishment and further spread, and (2) modesof transport of species with high probabilities offurther spread. If successful, weed epidemiologywould facilitate development of quarantine andcontrol technologies prior to arrival and spreadof potentially troublesome species.

For solutions to the outstanding problems ofplant quarantine, basic principles of weed epi-demiology must be developed and/or refined.Some tentative principles include: (1) species withvery broad native distributions have higher pro-babilities of introduction than those with narrownative distributions (Forcella & Wood. 1984). (2)at least some taxonomic sets of serious weeds tendto originate from the same small group of coun-tries (Forcella & Wood, 1984). (3) aliens intro-duced at multiple sites are apt to spread at rateshigher than those with fewer sites of introduction(Auld & Coote. 1980). and (4) species with highinitial rates of spread within a region typicallybecome the region's most troublesome weeds(Forcella. 1985).

Several plant traits have been presumed todistinguish potentially troublesome alien speciesfrom innocuous plants (Baker. 1965), Some ofthese may not be practical for use by plantquarantine officials, whereas others are valueless.For example, genetic diversity, although muchdiscussed in the past (see Baker, 1974). has notbeen found to be associated with the ability of aplant or animal to spread widely (Moran &Marshall. 1978: Myers & Sabath. 1981; Jain,1983: Forcella & Wood, i 984). In contrast, rapidseed germination is an easily determined trait andone which appears to characterize widespreadnoxious weeds. Narrowly distributed speeiesexhibit relatively slow germination. This differ-ence in rapidity of seed germination betweenserious and minor weeds occurs both within agenus[e.g. A'afl?/j/«m(Martin»S:Carnahan, 1983)Jand among genera (Forcella. 1985). A great dealof further research will be necessary for successfulprediction of whether one plant species has thepotential to be a serious weed whilst another doesnot. and for reconciliation of which plant traitsare most useful for screening hitherto unfamiliarpiant species. Towards this end we have com-pared the epidemiology of three closely relatedalien plants in Australia.

Three herbaceous species of the genus EchiumL. occur in Australia (Piggin. 1977), E. ptantagi-neum L., an annual or occassional biennial, hasnaturalized so well that it is perhaps one of themost common and characteristic plants of largesections of southern Australia. F. vutgare L., abiennial and occassional annual, is not wide-spread, but restricted to cool and moist sectors ofsoutheastern Australia, Lastly E. ttalicum L, is avery rare, short-lived perennial (Piggin, 1977).What has allowed sueh differential infestation?Have the two restricted species had too little timeto spread to their physiological limits, or are theyincapable of thriving in areas other than wherethey currently grow? We attempt to answer thesequestions below, and we use our answers to helpbuild a conceptual model of successful andunsuccessful alien plants, especially in temperateenvironments.

Seemingly similar comparative work eon-ducted by Baker and his students (see Baker 1974and references therein) has provided much valu-able theoretical insight into differential migrationof species of several taxa. However, these studieswere rather qualitative, at least in their publishedforms, and the migrations they discussed often

Characteristics of invasive weeds 353

referred to those which occurred in the Pleisto-cene, If tomorrow's plant quarantine decisionsare to be rigourous, then more quantitativeevidence will be necessary on the epidemiologyand ecology of today's alien weeds.

Methods

A select group of variables bearing on the biogeo-graphy and ecology of Echium was analysed.These variables included distributions of thespecies in their native continents as well asAustralia and characteristics of seed germination.vegetative growth and flowering, especially inrelation to temperature and/or photoperiod.Other variables whieh were not examined may beas important as those which were. The measuredecophysiological variables were derived fromplants whose seeds originated from a singlepopulation for each speeies. We recognize thatsuch narrow genetic bases restrict our ability toextrapolate. Nevertheless, as will become clear.results for E. plantagineum closely match thoseavailable in the literature for widely disparatepopulations of this species. Additionally, ourinterspecific differences were often so large thatintraspecific variability was considered unimpor-tant.

Native distributions

Eurasian and North African countries, or prov-inces within large countries, in which any ofthe 17species of European Eehium are known to occurwere recorded from the following sources: Davis(1978). Freinbrun-Dothan (1978). Gibbs (1972),Jahandiez & Maire (1934), Klotz (1960), Post(1933). Qaiser (1979), Quezel & Santa (1963),Riedl (1967) and Tackholm (1974), A presence/absence matrix of species/countries was con-tructed and subjected to correspondence analysis(Hill. 1973), whieh compared multivariately therelationships among species according to theirdistributions, and relationships among countriesaccording to their inhabitant species. First andseeond principal components of resultant analy-ses for species and countries were superimposedupon one another. This allowed better visualiza-tion of association of species with particularcountries (Foreella & Wood 1984),

Australian distributions

Rates of collection of Echium herbarium speci-mens through time {cf Lacey. 1957; Auld et al.,1982/83) were calculated using label informationfrom Piggin (1977), In addition, we determinedlatitude and longitude of each specimen collec-tion site and its appropriate 1 by 1-5 referencemap grid (Anon,. 1975; Scott& Kenneally. 1981).Distribution maps using these grids were thengenerated by computer (Chippendale & Wolf.1980) for each decade from 1831 to 1977.Although the resulting time-series distributionmaps may not represent ranges of plants accu-rately, they do refleet true distributions as pre-cisely as is possible. In any event, in the analyseswhich follow it is only the relative extent ofdistributions among both time periods and spe-cies which is important. We feel that herbariumspecimens are adequate for this purpose.

Seed germination

Seeds of E. italicum were collected east of Cor-owa. New South Wales (NSW), in January 1982.Rarity of this species at the collection site andelsewhere resulted in only 118 seeds being avail-able for experimentation. Abundant seeds of E.vutgare were collected in May 1981 betweenBredbo and Cooma. NSW. Near Wagga Wagga.NSW, quantities of E. ptantigineum were gath-ered in February 1982. All seeds were stored onlaboratory shelves until used in September 1982and January 1983. Storage duration should havebeen sufficient for all after-ripening processes tooecur (£•/, Ballard, 1970; Piggin. 1976).

E.xperiment I. Stored seeds of eaeh speeies wereweighed in three groups of 20 seeds each. Subse-quently, seeds were germinated in petri dishes inthree environmental chambers with day/nighttemperatures of 28 720 . 23/15" and 18710,Each chamber received 8 h of natural daylightsupplemented with 4 h of incandescent light (60//E m"- s"'). Radicle emergence was monitoreddaily. Three replicates of 25 seeds each werepossible for E. ptantigineum and E. vutgare, butonly a single petri dish containing 36 seeds couldbe examined in each chamber for E. italicum.

Experiment 2. Ten petri dishes, each with 25 seedsof both E. plantigineum and F. vutgare. werealigned on a temperature gradient bar with aconstant temperature gradient ranging from 2'"' to

354 F. Forcelta, J. T. Wood and S. P. Dillon

32 \ Seeds were illuminated continuously withfluorescent light (100/JE m"^s"')- Radicle emer-gence was monitored daily in three replicates ofeach dish.

Subsequently, we received a sample of F.;7fl/;Vum seeds collected in September 1983 by J. F.Vayssieres at Lae du Salagou, Heiault, France. InNovember, germination of these seeds was exam-ined as above, except that the temperature gra-dient ranged from 10''-40^. We recognize that thegenetie base of this seed population may differfrom Australian material.

Vegetative growth

One- to 3-day-old seedlings were transplantedinto pots (10 cm diameter, 20 cm deep) filled withperlite and sand (1:1). Pots were placed in one ofnine environmental chambers, each programmedfor one of nine combinations of day/night tem-perature and photoperiod: 28'/20\ 2 3 / 1 5 \ 18 /10% 16 h, 12 hand 8 h. Photoperiods consisted of8 hr of natural daylight supplemented by anappropriate period of incandescent light (60 /JEm"^ S"'). Plants were watered twice daily, oncewith Hoagland's solution and once with water.Established plants were thinned to one per pot.

At weekly intervals from 3-6 weeks aftertransplantation four pots in each chamber ofboth E. plantagineum and E. vulgare were har-vested. Leaf areas of these plants were deter-mined. Roots were washed free of soil and bothroots and shoots were oven-dried and weighed.For £. italicum silhouettes of intact leaves of fourplants from each chamber were constructed andtheir areas determined.

Flowering

Four or more plants of each species were main-tained in the chambers from January 1983 untilflowers were noticed, or until April for vegetativeplants. At this time vegetative plants were repot-ted (30 cm diameter pots); half of these pots wereplaced in a greenhouse (25'/10') and theremainder in a coldframe. Later, half the cold-frame pots were transferred to the greenhouse.Plants were watered and fertilized as needed.Flowering responses were noted.

Results

Native distribution

The three herbaceous species of Echium whieh

were introduced to Australia have the mostwidespread native distributions ofthe 17 speciesanalysed, occurring in 29, 27 and 34 countries orregions (£. italicum. E. vulgare and E. plantagi-neum. respectively). Species not known in Austra-lia occur in an average of 6-4 ( ± 5 4) countries.This average is significantly (/*<001) smallerthan that ofthe 'Australian' species in parametricor nonparametric statistical comparisons.Among the "non-Australian" species £. russicumhas the widest distribution (19 regions), but isrestricted mostly to eastern Eurasia. E. parviftora,the next most wide-ranging species (13 regions),has a range seemingly similar to F. plantagineumbut is more closely associated with the shores ofthe Mediterranean Sea.

Biogeographie relationships among Echiumspp, are shown in Figure 1. Species characteristicofthe Iberian Peninsula (E. albieans. E. boissierii,E. tusitanicum and £, rosutatum) form a discretecluster. Nearby, but less distinct, is a north centralMediterranean group which includes E. asperi-num, E. creticum and E. sabulieola, and a westernMediterranean pair composed of F.Jlavum and £.tuberculatum. A strictly circum-Mediterraneangroup Is comprised of E. arenarium, E. angustifo-tium and F. parviflora. Both F. italicum and E.ptantagineum are very closely linked to this lattergroup, but the first speeies ranges more widely tothe south and east, while the second extendsfarther north. E. vulgare is a northern plant,which is unknown south ofthe Mediterranea Sea;its northern limit is about 50 N latitude.

In Figure I both Iberia and northern Europestand alone, because of higb and low Echiumdiversity, respectively. Interestingly, central Euro-pean Mediterranean regions are more closelyallied with North Africa than either is to Iberia.

Australian distributions

Currently, E. italieum has a disjunct distributionin Australia (Fig. 2), occurring in southeasternSouth Australia (Adelaide to Mount Gambier)and the border of north central Victoria andadjacent south central NSW. Additionally, therate of spread of this species has been and is stillthe lowest of the three Australian species (Fig.5a). More widespread is E. vulgare (Figure 3).Although restricted to cool/humid portions ofsoutheastern Australia, it ean be prominent alongthe Great Dividing Range of NSW and Victoria,as well as in Tasmania. This speeies appears to

Characteristics of invasive weeds 355

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Fig. 1 Correspondence analysis of Echium spp. (numbers) and North African andEurasian regions (letters) in which they are native. The first and second components ofIhe analysis correspond to geographic gradients from south to north and wesi lo east,respectively. The three species occurring in Australia are represented by bold andenlarged numbers and connected by dotled lines. Regions characterizing variousspecies are proximal lo such species in the graph.

Appendix 1. Abbreviations for countries and regions shown in Fig. I: AB Albania,AO. Algeria, AU Austria, BA Balaeras Islands. BE Belgium. BL Baltic Islands. BRBritain. BU. Bulgaria, CM Crimea, CO Corsica. CR Central Russia, CT Crete, CZCzechoslavakia. DE Denmark. EG Egypt. ER Eastern Russia, ET European Turkey,FI Finland, FR France. GE Germany, GR Greece. HO Holland. HU Hungary. IDIreland. IR Iraq. IT Italy. JU Jugoslavia. LB Lebanon. LY Libya. MO Morocco. NONorway. NR Northern Russia. PO Poland, PR Portugal, RO Romania. SA Sardinia,SD Sweden. SI Sicily. SP Spain, SW Switzerland, SY Syria, TR Anatolian Turkey. TUTunisia, and WR Western Russia.

Numbers representing species shown in Fig. I: (1) Echium atbieans, (2) E.anguslifolium\ (3) E. arenarium; (4) E. asperinum; (5) E. hoisserii, lusitanicum andro.sutaium: (6) E. creticum: (7) E.fiavum; (8) E. humile\ (9) E. iiaticum\ (10) £.pan'iftora\{[]) E. ptaniagineum,{\2) E. russicum,{]'i) E. sat'uticola;t]4) E. iubercutaium,andi]5)E. vutgare.

have reached the limits of its potential distribu-tion in Australia, as it has only spread very slowlyinto new areas over the past half century (Fig. 5a).Those districts into which the plant has spreadduring this time invariably occur within thegeneral pre-existing distribution of the species. Incontrast, £. ptantagineum has been collected fromthroughout Australia, except the very arid por-tions of Western Australia and latitudes < I6'S(Fig. 4). Although controversial (Kloot. 1982),the history of spread of E. plantigineum appearsto have started as four or more isolated 'infes-tation points' by 1900, with later movement as

migrating fronts from these points, and, finally,amalgamation ofthe spreading fronts. Unlike E.italicum and E. vulgare, E. plantagineum hascontinued to increase its known distributionrapidly (15 districts year ' ) - with many recentcollections being made in areas previously devoidof the plant, e.g.. Western Australia and theNorthern Territory (Figs 4, 5).

Australian eolleclions

Herbarium specimens of Echium increased atrates similar to numbers of districts occupied

356 F. Forcella. J. T. Wood and S. P. Dillon

Echium italicum

I90I-I9I0 1931-1950

rx

V •

1911-1920 1951-1977

X

, -,.........

V

1921-1930

rxX

%

Fig. 2 See Fig. 4 for details.

(Fig. 5). However, numbers of new collections perdecade (COL) was not correlated with numbers ofnew districts per decade (DIS) occupied, especiallyfor the less common species. For example, regres-sion analyses of COL with DIS revealed R^ values of002, 0 70 and 0 03 for E. italicum, E. plantagi-neum and E. vulgare, respectively. Lack of corre-spondence of COL with DIS stemmed from dispro-portionate collection efforts after a species

reached its 'final' distribution, e.g., E. vulgarefrom 1960-1977.

An index of collection intensity (INT) can bederived by dividing numbers of specimen collec-tions by numbers of districts occupied for anytime period. By 1977 INT values were 3-1,4-7 and3 3 for £. italicum, E. planlagineum and E.vulgare, respectively. Thus, INT was greater inwidespread species than in narrowly distributed

Characteristics of invasive weeds 357

Echium vuigara

-1900 1941-1960

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1901-1920 1961-1977

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Fig. 3 Sec Fig. 4 for details.

Species. Furthermore, regressions of INT with DISrevealed that INT increased with time for indi-vidual species, with the rate of increase being 13and 1 2 times greater for E. ptantagineum than forE. italicum and E. vulgare, respectively.

Germination

Experiment 1. Weights of viable seeds for the

three species were 7-5, 3 9 and 3-4 mg seed '(I.s.d.= l 3 mg [/'<001]) for E. italicum, E.plantagineum and E. vutgare, respectively. Timeto achieve more than 50% germination was lessfor F. ptantagineum (1-2 days) than E. vulgare (3 -7 days) or E. italicum f'9-10 days). However,maximum germination percentage was lower forthe former than the latter species (65,75 and 85%,respectively), despite all seeds appearing to have

358 F. Forcella. J. T. Wood and S. P. Dillon

Echium ptantagintum

1831-1900 1941-1960

X

1901-1920 1961-1977

1921-1940

Figs 2-4 Spread of Echium italicum, E. vutgare and E. piantagineum, respectively, as represented by allherbarium specimens available in 1977 (Piggin, 1977). Each 1° by l'5° block represenls a mappingdistrict in which at least one herbarium specimen was collected.

fully developed embryos.Germination rate index (Maguire, 1962),

which integrates extent with speed of germina-tion, was highest for E. plantagineum at eachtemperature regime (Table 1), with E. vulgareintermediate and E. italieum lowest. Indices forall species were greatest at the high temperatureregime; no germination of E. itaiicum occurred at

lower temperatures nor ofE. vulgare at the lowesttemperature.

Experiment 2. From Day 1 to Day 14 the range oftemperatures over which E. ptantagineum wasable to germinate was about two and three timesas great as that of E. vulgare and E. italieum,respectively (Fig. 6). At low temperatures (< 17'')

Characteristics of invasive weeds 359

300 -

g 200-

100

1840 I860 1880 1900 1920 1940 I960

Time (years)

1980

Fig. 5 Rales of spread (A) and rates of specimen collection (B)of E. ilaticum (solid circle), E. vutgare (open circle) and E.planlagineum (square). Districts are 1 by I 5 ((. 115 km by136 km) as used by the Australian Grid Syslein. Dala derivedfrom Piggin (1977), Fig. 5A adapted from Forcella & Harvey(1983).

Table I Germination rate index {sensu Maguirie, 1962), whichintegrates germination percentage and rate into a single value,forihree species of fi'cAiufn at three temperature regimes. Valueswilh no superscripts in common differ significantly ( / '<0 05).£. iialicum was nol included in the stalistical analysis

Tempera lure regime

species 28720° 23715-' 18 10

E. planlagineumE. rutgari'E. ilaticum

(rale index)7'5''4.!''20

17"00

up to 45% of E. plantagineum seeds germinated,whereas only very few seeds of the other speciesdid so. At higher temperatures both E. plantagi-neum and F. vutgare germinated well, with E.ptantagineum doing so significantly ( / '<005)more rapidly by Day 3 (Fig. 6). E. itaticumgerminated well, albeit slowly, only within therelatively narrow and high temperature band of33"-36^, where maximum germination was 26%.Thus, the relative response to temperature ofthese French seeds was similar to those fromAustralia {cf Experiment I).

In both experiments germination behaviour ofour seed accessions was simitar to that of popula-

tions originating elsewhere (for E. planlagineumsec Ballard, 1970; Piggin, 1976; Trumble, 1937;for E. vulgare see Cross, 1931; Mitchell, 1926; nocomparisons available for E. italicum).

Vegetative growth

Leaf area. For E. plantagineum leaf area wascorrelated with temperature, but daylength didnot affect this species (Fig. 7). Under eachtreatment, leaf area of E. ptantagineum wasconsistently and significantly ( P < 0 0 ! ) greaterthan that ofthe other species.

Leaf area of E. vulgare was not affected bydaylength, but it was altered significantly bytemperature and the interaction of temperatureand harvest date. Low temperature retarded leafarea expansion; initially, high temperature pro-moted it, but by the last two harvest dates leafarea at the intermediate temperature regime wasequal to or greater than that at high temperature.F. vutgare commonly had the smallest leafarea ofthe three species.

Long days, especially at high temperature,significantly promoted leaf area expansion of E.itatieum. Effects of temperature varied with time,but by the final harvest, leafarea was correlatedwith temperature (Fig, 7), Leafarea ofthis specieswas considerably less than that of E. ptantagi-neum. and usually equal to or greater than that ofE. vutgare, except at low temperature.

Results for leafarea were analysed on the basisof days after transplantation of 1- or 2-day-oldseedlings. If 'days after sowing' had been used,differences would have been magnified for E.ptantagineum in comparison with other species,and reduced at high and increased at low tem-perature between E. italicum and E. vulgare.

Shoot and root weights. Analyses of variancerevealed that both shoot and root dry weightsgenerally responded to environmental conditionsin the same manner as leafarea. These traits willnot, therefore, be elaborated further, except tonote that shoot:root ratios were consistentlygreater in F. plantagineum (overall mean, 51)t h a n in e i t h e r E. italicum {3-2) or E. vutgare (41).

Flowering

E. plantigineum produced flowers in eight of ninetemperature/photoperiod combinations (Table2). Flowering oecurred at progressively younger

360 F. Forcetla. J. T. Wood and S. P. Ditton

ages, to a minimum of 80 days, as daylengthincreased and temperature decreased. Of theother species, only one plant of E. vulgare pro-duced flowers in the environmental chambers(18710', 16 h).

All E. italicum plants placed in a coidframe inwinter (July) and returned later to a heatedgreenhouse (August) flowered within 30 days.Plants left in the coldframe produced flowers byNovember. Plants placed directly in the green-house without an intervening cold treatment didnot flower. For E. vutgare, only plants remainingin coldframes throughout the winter producedflowers in spring (November).

Discussion

The alien herbaceous species of Echium in Austra-lia all have very wide native distributions. Thistrait, together with the presumed ornamentaland/or medicinal values of each species (Bonnier,1912), may have increased the probabilities of

their seeds being transported to Australia. Asimilar relationship has been observed for alienthistles (Forcella & Wood, 1984) and clovers(Morley & Katznelson, 1965) in Australia. Inter-estingly, two countries, Albania and Yugoslavia,which characterize native distributions of alienthistles and clovers, are also associated withnative ranges of invasive species of Echium.

Many species ot Echium unknown in Australiamay be distributed too narrowly in their nativeranges to have had high probabilities of transportto other regions. However, some of these species,namely F. parviflorum and E. russicum. havebiogeographie characteristics which somewhatresemble those of invasive Echium spp., implyingthat these plants may be potential alien weeds.

Plant colonization in Australia, as determinedfrom herbarium specimens, appears to havestarted with multiple infestation points {cf Kloot,1982). These points for Fehium were frequentlynot near {i.e., within 1 ''fX-S'' latitude/longitude) oflarge cities and/or established herbaria. Thisimplies that plant collectors neither favoured nor

6 0 -

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Fig. 6 Seed germinaiion percentage off. ;>/(7/7(flg/rti'i/m| A). E. r^/gur('(B)and £. ilaticum {C) o\er a range of constant lemperaturesandat five times after sowing. Each value is the mean of ihree replicates.

Characteristics of invasive weeds 361

disfavoured rural or urban areas, and it alleviatessome concern in using herbarium specimens asdata sources.

From multiple infestation points Fehium spp.spread as migrating fronts with varying degrees ofrapidity. For E. plantagineutn these migratingfronts coalesced into large ranges in which theplant was more or less evenly distributed geo-graphically. It was during the time of multiplemigrating fronts that this species spread exponen-tially in its distribution. This suggests Ihat if aspecies spreads from only one or two infestationpoints, its rate of spread would be lower than if itwas first introduced at several locations (Auld &Coole, 1980), as seems to be true in the diiferen-tial spread of Echium spp. (Figs 2-4). The greaternumber of initial infestation points for E. ptanta-gineum may have been due to its ornamentalvalue (K loot. 1982) and that its seeds are found ina much wider variety of transported productsthan the other species (Anon.. 1941, 1955, 1975:Low. 1969, 1978; Thomas et at.. 1984).

Relative to E. ptantagineum. distributions of £".itatieum and E. vutgare have stabilized. Thus

other factors must have interacted with originalnumbers of infestation points in determiningranges of the species in Australia. Potentiallyadaptive ecological traits of these plants arediscussed below.

Numbers of herbarium specimens appear to beuseful for documenting the historical spread of aspecies (Auld et at.. 1982/83: Lacey. 1957). buttend to be inaeeuratc in determining whether aspecies is still spreading. Numbers of occupiedcounties, districts or map grids ofsome kind mustbe employed to detect reeent movement of alienweeds.

Number of herbarium colleetions per unit areaappears to be a useful index of eollection inten-sity, and perhaps commoness. at least withinEchium. For example, collection intensity is I 4and 1-5 times greater for E. plantagineum than forF. vutgare and E. itaticum. respectively. Thiseorresponds to recent findings that the mostwidespread animals are also the most loeallyabundant species (Hanski, 1981; Boek& Ricklefs.1983; Brown. 1983).

Once an alien piant has been introduced il must

4 5 6

Time {weeks)

25715° - —-28720°

Hg. 7 Increase of leaf areas under ihrec photnperiods and three lempcriilurc regimes for E.piantagineum (\),E. iiaiicum (B) «nd E. vutgare (C) as a funciion of lime after transplanting of I -und 2-day-old seedlings. Noie differing scales of leal area for each iilihe species. Six-week values;il 12 hand \ii\i\ctv E.iuigareM 2.1 ,15 arc missing. All values represent means of four repliL-aies.

362 F. Forcetla. J. T. Wood and S. P. Ditton

Table 2 Age of F.chwm pianiagineum planls at iriitialion ofanlhesis as aflected by nine cum hi na I ions of Icmperaturo andphotiiperiod. Onh ii single plani flowered in ihe 2H 20 . 12 hIreaimenl (240 days afier gcniim:iiu>nl. and no plarils Howeredunder N h at the same temperature. Leasi sijinilicanl iliHcrence(A'<0fl5) over all irealments is 25 days

Tempeniiure regime

Phoiopcriod

(hours)S

1216

28 /20'

X

>24(l11)1

23 /15

(diivs)201IW100

1 8 / 1 0

179136

m

respond to the physical environment in ways thatpromote its survival. Survival will depend uponphysical hardiness and biological competitive-ness. Opportune seed germination, vigorousvegetative growth and prolific seed production,all under both stressful and benign physicalconditions, would seem to be requisite traits.How well are these traits reflected in the threedifferentially distributed species of Fehium inAustralia?

The physical environment has eonsiderableand differential clTeets on these Fehium species.The species which germinate over relatively nar-row and somewhat high ranges of temperature,and which germinate slowly, are restricted indistribution. In contrast, F. ptantagineum seedgermination is rapid, like that of other wide-spread noxious weeds (Martin & Carnahan, 1983;Forcella. 1985), and it also occurs over a widerange of temperatures. Responses of Eehium spp.are similar to differenees found in eommon andless common weeds of other genera (Cumming,1959: Dillon & Forcella. 1984). Additionally, therelatively high germination of £. ptantagineum attemperatures between 10-20 would be favour-able for establishment in Mediterranean-like en-vironments, where soil temperatures in autumn{when the growing season begins) are within thisrange (Storrier. 1965).

Vegetative growth of E. ptantigineum wasalways greater than that of other species ofEchium. It wasmonotonieally related to tempera-tures, but otherwise unresponsive to temperature/daylength combinations. Growth of less eommonspecies of Echium was regulated more rigorouslyby environmental variables. High rates of leafarea expansion under a variety of conditionswould be important for an estabishing alien weedin competition with neighbouring plants. Its

value in interspecific competition has been notedby Jennings & Aquino (1968), Hofstra & Stien-stra (1977) and Slatyer (1970).

Despite differenees in habit, a trait which is nota reliable indicator of invasiveness (Foreella,1985), all tested speeies of Echium were able toflower and set seed within one year after seedgermination in experimental settings. However,differences were pronounced in the degree ofenvironmental rcguhition of anthesis among thespecies. The highly invasive species floweredunder nearly any temperature/photoperiod com-bination (Ballard & Grant Lipp, 1970). In con-trast, the less common species required distinctvernalization and long photoperiods. require-ments which would constrain their distributionsin Australia and elsewhere.

Some of our conclusions are apt to be ques-tioned, because analyses were based on seedsderived from single populations. However, thepopulation genetics of the most important spe-eies, E. ptantagineum. justifies such narrow sam-pling, at least for some analyses. For example.Wood & Degabriele (1985) have shown thatattributable genetic variability is 3'5, 56 and 5-5times greater within populations than betweenpopulations for relevant traits such as leaf area,dry weight and age at flowering, respectively.Thus, the substantial genetic variability for thesetraits within single populations may often encom-pass inter-population differenees.

For praetieal eharaeterization of an unknownalien as either a potentially noxious weed or aninnocuous waif, the range of its native distribu-tion eoupled with the rapidity and extent of seedgermination appear to be the most useful traitsexamined in our studies. Thus speeies whosestatus as weeds are unknown, but which havewide native ranges and whose seeds exhibit highgermination rate indices are prime suspects aspotentially troublesome pests. Although suehconclusions were derived from analyses of weedsin Mediterranean Australia, other studies implythat the principle may hold for weeds of differentregions (Cumming. 1959; Foreella, 1985; Foreeila& Wood. 1984; Martin & Carnahan, 1983). Otherplant traits, such as ability to produce large leafareas quickly and propensity to flower under anarray of environmental conditions, also charac-terize troublesome weeds. However, such traitscould not be documented by plant quarantineoflieials as easily as native distribution and germi-nation rate.

Characteristics of invasive weeds 363

Ackno w ledgments

We thank R. Amor, J. Burdon, J. Carnahan, R.Downes. A. M. Gill, R. H. Groves. P. Kioot, R.Pullen and editorial staff of this journal forhelpful eomments on initial versions ofthis paper.L. Wolf provided his mapping program. Staff ofthe CSIRO Phytotron skillfully nurtured ourplants on a daily basis. Data collection occurredduring the first author's tenure with the Divisionof Plant Industry, CSIRO-Australia.

(Received 23 July 1985)

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