Can species traits be used to predict marine macroalgal introductions?

Cecilia D. Nyberg* & Inger WallentinusDepartment of Marine Ecology, Marine Botany, Goteborg University, Box 461, SE 405 30 Goteborg,Sweden; *Author for correspondence (e-mail: cecilia.nyberg@marbot.gu.se; fax: +46-31-7732727)

Received 17 July 2003; accepted in revised form 18 February 2004

Key words: distribution, ecological impact, establishment, Europe, introduced, invasive, macroalgae,marine, NIS (non-indigenous species), species traits

Abstract

Species traits which facilitate introduction and predominance have been quantitatively ranked usinginterval arithmetic to search for common patterns among 113 marine macroalgae introduced in Europe.Three main categories were used: dispersal, establishment and ecological impact. These were further sub-divided into more specific categories, a total of 13. Introduced species were compared with the samenumber of native species randomized from the same families as the introduced. Invasive species (i.e. spe-cies having a negative ecological or economical impact) were also compared with non-invasive introduc-tions, separately for the three algal groups. In many categories, as well as when adding all species, theintroduced species ranked more hazardous than the native species and the invasive species ranked higherthan the non-invasive ones. The ranking within the three main categories differed, reflecting differentstrategies between the species within the three algal groups. When all categories (excluding salinity andtemperature) were summed, the top five risk species, all invasive, were, in descending order, Codiumfragile spp. tomentosoides, Caulerpa taxifolia, Undaria pinnatifida, Asparagopsis armata and Grateloupiadoryphora, while Sargassum muticum ranked eight and Caulerpa racemosa ten. Fifteen of the twenty-sixspecies listed as invasive were among the twenty highest ranked.

Introduction

Introduction of species into new environmentshas been occurring for a long time but today’sfast transportation possibilities have increasedthe chance of survival of unintentional and inten-tional introductions. Further, the breakage ofnatural boundaries through construction ofcanals and artificial waterways also contributesto the increased spread of marine organisms.Humans profoundly facilitate dispersal of marinespecies through discharge of ballast water, foul-ing communities on ships’ hulls, intentionalintroductions of species for aquaculture andaquaria trade, and unintentional introductionson or in such organisms as well as algae used as

transportation material around shellfish and livebaits (Minchin and Gollasch 2002; Wallentinus2002 and references therein).

When introduced, only a small number of alienspecies will survive in the new area and becomeestablished and even fewer will cause disturbance,but once a species has been established it will bevery hard or impossible to eradicate (e.g. Critch-ley et al. 1986; Bax et al. 2001; Squair et al.2003). Therefore it would be valuable if it werepossible to predict which species would become arisk. One way of doing this is to search for com-mon patterns of features that can increase thelikelihood of a successful invasion. Severalattempts to find such patterns have been madein, for example, terrestrial plants (Williamson

Biological Invasions (2005) 7: 265–279 � Springer 2005

and Fitter 1996; Kolar and Lodge 2001; Prinzinget al. 2002), marine algae in the Mediterranean(Boudouresque and Verlaque 2002) and in theNorth Sea (Maggs and Stegenga 1999). Wewanted to evaluate this on a larger assemblage ofmacroalgae introduced into Europe and thereforeapplied quantitative ranking of species traits thatfacilitate dispersal and establishment of intro-duced species as well as their ecological impact.In addition, we wanted to test if a quantitativearrangement of species traits could be used as atool for risk assessment for intentional introduc-tions or when establishing risk species lists.

Materials and methods

Species traits for 113 introduced marine macroal-gae, 77 red (R), 26 brown (B) and 10 green algae(G) in Europe (Boudouresque and Verlaque2002; Ribera Siguan 2002; Wallentinus 2002),have been collected from a wide source of litera-ture (available on www.aqualiens.tmbl.gu.se).For a list of species, see Appendix 1. The datafor all species are too voluminous to be pub-lished, but can be provided by the authors.

Three main categories were used: dispersal,establishment and ecological impact. These werefurther subdivided into more specific categories(see Tables 1–3). The algal groups were kept sepa-rate despite the uneven numbers of speciesincluded, since different algal groups may havespecific characters we did not wish to lose. Foreach category, introduced species were comparedwith native species (Anonymous 2000). The nativespecies were randomized from the same families(23 families from Rhodophyta, 12 from Phaeophy-

ceae and six from Chlorophyta) as the introduced,since some traits (e.g. secondary metabolites andsize) may differ widely between families. Someintroduced species also occur in the list of natives,but only when they are indeed native in some partof Europe, while introduced in others. Also, inva-sive (18R, 4B, 4G in seven, four and two families,respectively) and non-invasive introductions (59R,22B, 6G) were compared for each category. Wedefined invasive algae as an introduced species thatis ecologically and/or economically harmful (Bou-douresque and Verlaque 2002).

Interval arithmetic

Interval arithmetic is a method for evaluatingcalculations over sets of numbers contained inintervals. An interval denoted [a, b], with a lessthan b, is the set of all real numbers between theupper and lower boundaries including the end-points. Adding intervals [a, b] +� � �+ [e, f] givesus a new interval [g, h] where g is a +� � �+ eand h is b +� � �+ f. In this study the speciestraits were quantitatively ranked by using thistechnique (K. Hayes, personal communication)for the different categories. For each category ascale from 0 to 1, divided into ten intervals wasused (0 being the least risk and 1 the highest).An interval was obtained for each alga some-where between 0 and 1 depending on the specifictrait they possessed. These were finally summa-rized for each group of algae (R, B and G) andfor each category, and the average value formaximum and minimum was plotted as a bar (ameasure of uncertainty, not comparable to nor-mal statistical standard deviation). Where infor-mation was not available an ‘educated guess’ was

Table 1. Dispersal–categories and intervals.

Dispersal 0–0.1 0.1–0.2 0.2–0.3 0.3–0.4 0.4–0.5 0.5–0.6 0.6–0.7 0.7–0.8 0.8–0.9 0.9–1.0

1. Distribution

(regions)

1 or 25 2 or 24 3 or 23 4 or 22 5 or 21 6 or 20 7 or 19 8 or 18 9 or 17 10 to 16

2. Probability

of being

transported

>10 cm

no other

character

<10 cm

no other

character

Microsco

-pic stage

in life

cycle

Often

looslying

/drifting

Vegetative

propagules

or

fragments

Large

bouyancy

or ‘hooks’

Cultivated

or sold in

aquaria

trade

Growing

on

artificial

substrates

Growing

on

oysters

and

mussels

Growing

on ships

and plat-

forms

3. Survival

time

out of water

<1 h 1–6 h 6–12 h 12–24 h 24–36 h 1.5–3 days 4–6 days 1–2 weeks 2–4 weeks >1 month

266

Table

2.Establishment–categories

andintervals.

Establishment

0–0.1

0.1–0.2

0.2–0.3

0.3–0.4

0.4–0.5

0.5–0.6

0.6–0.7

0.7–0.8

0.8–0.9

0.9–1.0

4.Salinity(range)

£33–6

7–10

11–14

15–18

19–22

23–26

27–30

31–34

‡35

5.Tem

perature

(range)

(�C)

£56–8

9–11

12–14

15–17

18–20

21–23

24–26

27–29

‡30

6.Tolerance

to

pollutants

Only

in

cleanand

clearwater

Verypoor

inslight

pollution

Survive

andgrow

inslight

pollution

Very

poor

growth

in

moderate

pollution

Surviveand

grow

in

moderate

pollution

Verypoor

inhigh,

medium

good

inmoderate

pollution

Some

growth

inhighand

goodin

moderate

pollution

Tolerantto

highdegree

ofpollution

Some

increase

at

highdegree

ofpollution

Mass

development

athigh

degreeof

pollution

7.Reproductive

mode

Dioec.

gamet.

fertileonly

short

period

Dioec.

gamet.fer-

tile

long/

manyperi-

ods

Monoic.

gamet.

notself-

fertileandonly

forshort

per-

iod

Monoic.

gamet.

notself-

fertile

long/

many

periods

Monoic.

gameto-

phyte,

self-fertile

Largepart

ofthallus

fertileshort

period

Largepart

ofthallus

fertilelong/

many

periods

Asexual

spores

Vegetative

propagulae

Fragmenta-

tion

8.Growth

strategies,

surface

:volume

S-strat.

low

s:v

S-strat.med-

ium

s:v

S-strat.high

s:v

C-strat.

low

s:v

C-strategy

medium

s:v

C-strategyhigh

s:v

C-strategy

andR-

strategy

R-strat.low

s:v

R-strategy

medium

s:v

R-strategy

highs:v

9.Grazingand

defense

mechanisms

Much

preferred

andgrazed

bymany,

‘no’toxins

Some

grazers

but

hugeim

pact

Somegrazer

withmedium

impact

Onestage

crust

or

micro-

scopic

Regenerate

orsm

all

fragments

cangrow

Thalluscalcar-

eousortough

morphology

Some

chem

ical

defense

and

often

grazed

withsome

impact

Much

chem

ical

defense

and

somegra-

zer,

small

impact

Several

toxinsand

few

specia-

list

grazers

‘Never’

grazed

severaltox-

ins

orcombined

strategies

267

made and the interval was extended. We alsosummed all categories (excluding salinity andtemperature) to determine the species constitutingthe highest overall risk.

Categories

DispersalThe main category ‘dispersal’ was divided intothree subcategories: (1) Geographical distributionwas based on division of the oceans into 25 bio-geographical regions according to Luning (1990),except for the Mediterranean, which here wastreated as a separate area. A species was assumedto have maximum dispersal potential if it isfound in 10–16 regions, if occurring in more orless, the risk was reduced proportionally. If aspecies occurs in few regions the possibility ofbeing distributed is low and if it occurs in manyregions the risk of being introduced is reducedbecause it is already present in most areas. Dis-tribution data were mainly collected from Algae-base (Guiry and Nic Dhonncha 2003). (2) Thecategory probability of being transported includesthe species’ use in cultivation and aquaria trade,and their capacity to float, attach with hooksand grow on live molluscs and artificial substrate.(3) The survival time out of water reflects theduration out of water that a species can survive,ranging from less than an hour to more than onemonth. Few literature data regarding dehydra-tion were available and these were mostly notcomparable with each other. Estimates were thusbased on morphology and depth range and justin some few cases could the survival time out ofwater be obtained from literature. Species with athick thallus, mucus production or growing inthe littoral zone scored high.

EstablishmentThe main category ‘establishment’ was dividedinto six subcategories: (4) Salinity defines the sur-vival range from geographical areas with salinityranges of £3 to ‡35 (with intervals of 4). (5)Temperature survival range spans from areaswith ranges of £5 to ‡30 �C (with 3 �C intervals).The temperature range that each species has beendenoted is assigned from the region were it isfound (temperatures below zero are notincluded). The ultimate would be to base thisT

able

3.Ecologicalim

pact–categories

andintervals.

Impact

type

0–0.1

0.1–0.2

0.2–0.3

0.3–0.4

0.4–0.5

0.5–0.6

0.6–0.7

0.7–0.8

0.8–0.9

0.9–1.0

10.Size

<1cm

1–5cm

6–10cm

10–20cm

20–30cm

30–50cm

50–75cm

75–100cm

1–2m

>2m

11.Morphology

Verysm

all

£1cm

Only

as

crusts

Lobed

and

thick

Flatand

thin,sm

all

holdfast

Quitethin

filaments,

medium

or

little

branched

orsm

all

tufts

Coarse,

medium

or

little

branched

orthick

andflat

Much

branched,

nolarge

holdfast,

<0.5

m

vertic.

or

horiz.

Dense

turf

ofmuch

branched

quitethin

filaments

(sedim

ent

traps)

Coarseand

bushyor

withlarge

holdfasts,

>0.5

m

vertic.

or

horiz.

Often

mat-form

ing

andloose

-lying

12.Habitat

effect

Sparse

Less

common,

narrow

depth

interval

Less

common,

largedepth

interval

Common

epiphyticor

epilithic

restricted

depth

interval

Common

epiphyticor

epilithic,

largedepth

interval

Dense

cover

epiphyticor

epilithic,

restricted

depth

interval

Dense

cover

onmany

substrates,

restricted

depth

interval

Dense

cover

epiphyticor

epilithic

largedepth

interval

Dense

cover

onmany

substrates,

largedepth

interval

Supress

other

species

13.Lifespan

1–2

weeks

2–4weeks

1–2

months

2–4

months

4–6months

6–9months

9—

12months

1–2years

3–5years

>5years

268

category solemnly on experiments but few studieshave been made for our set of species (and inthese cases we have included these results). (6)Tolerance to pollutants describes the species’ sur-vival in clean to polluted water, including massdevelopment in eutrophicated water. (7) Repro-ductive mode includes the species’ reproductiveperiod and the different ways in which they canreproduce, e.g. sexually, by parthenogenesis, veg-etative propagules and fragmentation (scored inthe highest interval). (8) Growth strategies com-prise three types of strategies (S: stress tolerant,C: competitive and R: ruderal strategy) and theratio between the surface : volume of the thallus.When only part of the thallus is perennial thespecies was assigned a combined C–R strategy(Farnham 1997). (9) Grazing and defense mecha-nisms are composed of occurrence of toxins, thestructure of the thallus, including gland cells, andthe extent of grazing. For many species informa-tion about toxins and grazing was not availableand has been estimated.

Ecological impactThe main category ‘ecological impact’ was dividedinto four subcategories. (10) Size spans from lessthan 1 cm to more than 2 m. The largest size inany stage was considered. (11) Morphology is theshape of the alga, for example, crust-forming, thedegree of branching and development of loose-lying mats. (12) Habitat effects include abun-dance, the expansion in the water column andpossibility to suppress other species. (13) The cat-egory life span encompasses the temporal occur-rence from ephemerals to long-lived perennials.

Results

Dispersal

Category 1: For the brown and green algae andall species summed, the geographical distributionof introduced species pose a higher risk thannatives, while there is hardly any difference forthe red algae (Figures 1a and 4a). Comparinginvasive and non-invasive species we can see ahigher risk in the geographical distribution of theformer in all algal groups (Figure 1b) as well asfor all species summed (Figure 4b). Category 2:

Many of the introduced species ranked high inthe category for probability of being transported,since they grow on oysters, are used in aquacul-ture, in aquaria trade or can grow on artificialsubstrate (including ships’ hulls), while nativesseldom do (Figures 1a and 4a). The results forthe invasive vs non-invasive species, on the otherhand, showed different patterns. Invasive brownand red algae are more likely transported thantheir non-invasive correspondents, while onaverage invasive green algae are less likely

Figure 1. (a) Dispersal of all introduced species vs native spe-

cies; (1) geographical distribution, (2) probability of being

transported and (3) survival time out of water. Introduced

algae (It): (m) red, (j) brown and (d) green. Native algae

(Na): (n) red, (h) brown and (s) green. The bars show the

average maximum and minimum values of the intervals.

(b) Dispersal of invasive species vs non-invasive species: (1)

geographical distribution, (2) probability of being transported

and (3) survival time out of water. Invasive algae (Iv): (m)

red, (j) brown and (d) green. Non-invasive algae (No): (n)

red, (h) brown and (s) green. The bars show the average

maximum and minimum values of the intervals.

269

transported than their non-invasive correspon-dents (Figure 1b). However, summed over allspecies (Figure 4b) there was a higher risk withinvasive species, due to the low number ofgreens. Category 3: The many estimates used forthe comparison of the survival time out of waterdid not reveal any different patterns (Figures 1a,b and 4a, b).

Adding all categories of dispersal, introducedspecies presented a higher risk than native (Fig-ure 5a) and invasive species a higher risk thannon-invasive (Figure 5b). The introduced greenand brown algae had a risk of being dispersedmore easily than the red algae (Figure 5a).

Establishment

Category 4: The comparison of salinity tolerancerevealed different patterns for the different algalgroups (Figure 2b). There was no difference inrisk between invasive and non-invasive red algae.Brown invasive species clearly survive a broadersalinity range than the non-invasive species whilea trend for the opposite was seen for the greenalgae. Salinity ranges for the native species couldnot be estimated. Summing all species gave no dif-ference between invasive and non-invasive due tothe high number of red algae (Figure 4b). Cate-gory 5: The introduced green algae tolerate abroader temperature range than native, while noclear pattern was observed for the other groups,nor for invasive vs non-invasive species (Figures2a, b and 4b). Summing all species there was atrend for slightly larger temperature tolerancesamong introduced species compared with native(Figure 4a). Category 6: The tolerance to pollu-tants showed marginally lower risks for the nativespecies compared with introduced, which growwell in a moderate to high degree of pollution(Figure 2a), also when summing all species(Figure 4a). No clear pattern was seen whencomparing invasive species with non-invasive spe-cies (Figures 2b and 4b). Category 7: In generalthere seemed to be a slight trend with introducedspecies reproducing more often asexually thannative ones (Figures 2a and 4a), although manynative red and green algae also have that ability.Invasive red algae reproduce more often asexuallythan the non-invasive ones while the brownnon-invasive algae reproduce more often asexually

than the invasive ones. Only a slight differencewas seen for the green algae (Figure 2b). Summedover all species the invasives posed a slightlyhigher risk (Figure 4b) due to the high number ofred algae. Category 8: Many species are R-strate-gists with high surface : volume ratios. Only forintroduced red algae vs native could aslightly higher risk be seen in growth strategies(Figure 2a), mirrored also in the summed species(Figure 4a). For the others no obvious patterncould be seen. Category 9: The importance ofdefense mechanisms and secondary metabolitesamong introduced species has been highlighted inprevious papers (Maggs and Stegenga 1999;Boudouresque and Verlaque 2002). Our resultsshowed that this does not apply to all introducedspecies, which ranked about the same as nativeones (Figures 2a and 4a). Comparisons of invasivevs non-invasive species revealed that invasive redand green algae are clearly more resistant tograzing than the non-invasive ones (Figure 2b)which was also mirrored in the summed species(Figure 4b).

Figure 5 shows the sum of four categories underestablishment. We excluded salinity and tempera-ture which highly depend on geographical attri-butes, to see if there were any patterns among theother traits. Introduced species then representedslightly higher risks than native (Figure 5a) andinvasive than non-invasive, albeit small for thebrown algae (Figure 5b). The introduced greenalgae had a risk of establishing more easily, butthere was only a small difference between theintroduced red and brown algae (Figure 5a).

Ecological impact

Category 10: Introduced green algae are largerthan the native species, thus with a risk of higherimpact, while red and brown algae showed noclear difference between introduced and nativespecies (Figure 3a). For all species summed therewas a trend of a slightly higher impact by size ofintroduced species (Figure 4a). The invasivebrown and green algae are larger than the non-invasive species but no real difference can be seenfor red algae (Figure 3b), most of them beingquite small. Summing all species the risk ofimpact was slightly higher for invasive thannon-invasive species (Figure 4b). Category 11:

270

No obvious difference in morphology wasnoticed between any of the groups of introducedalgae vs native ones (Figure 3a), nor when spe-cies were summed (Figure 4a). Red and browninvasive species showed higher risks vs non-inva-sive species, while no difference was seen for thegreen algae (Figure 3b). Several invasive red spe-cies form dense turfs or mats, while the tiny orcompact species lowered the value for the non-invasive browns. Summing all species showed asomewhat higher risk of environmental impactby morphology of invasive species (Figure 4b).Category 12: A clear pattern could be seen forthe comparisons of the habitat effects, with

higher risks of impact of both introduced vsnative species (Figure 3a) as well as invasive vsnon-invasive ones (Figure 3b). This was alsoclearly seen when adding the species (Figure 4a,b). Several introduced species develop a densecover, suppress other species or grow on manydifferent substrates. Category 13: No patterncould be seen in comparisons of their life span(Figures 3a, b and 4a, b).

Summing the categories under ecologicalimpact revealed that invasive species in all algalgroups constituted clearly higher risks than non-invasive ones (Figure 5b). There was also aclearly higher risk of introduced green algae vs

Figure 2. (a) Establishment of all introduced species vs native

species: (4) salinity, (5) temperature, (6) tolerance to pollu-

tants, (7) reproductive mode, (8) growth strategies and (9)

grazing and defense mechanisms. For symbols and abbrevia-

tions, see Figure 1a. (b) Establishment of invasive species vs

non-invasive species: (4) salinity, (5) temperature, (6) tolerance

to pollutants and (7) reproductive mode, (8) growth strategies

and (9) grazing and defense mechanisms. For symbols and

abbreviations, see Figure 1b.

Figure 3. (a) Ecological impact of all introduced species vs

native species: (10) size, (11) morphology, (12) habitat effects

and (13) life span. For symbols and abbreviations, see Fig-

ure 1a. (b) Ecological impact of invasive species vs non-inva-

sive species: (10) size, (11) morphology, (12) habitat effects

and (13) life span. For symbols and abbreviations, see

Figure 1b.

271

native ones, but hardly any difference for intro-duced red and brown vs native algae (Figure 5a).The introduced green algae had the highestimpact and the introduced red algae the lowest(Figure 5a).

Total scores

Based on all categories except salinity and tem-perature, eight red, four brown and four greenalgae in each main category were identified as themost hazardous introductions (Table 4). Theranking within the three main categories differed,reflecting different strategies between the specieswithin the three algal groups. This ranking wasnot made for the randomized native species, sincethe most risky donor species must be searchedamong all native species. The top five most haz-ardous species when summarizing the 11 catego-ries (excluding salinity and temperature) were (in

descending order) Codium fragile spp. tomentoso-ides, Caulerpa taxifolia, Undaria pinnatifida, As-paragopsis armata and Grateloupia doryphora, allinvasive, while Sargassum muticum ranked eight,Caulerpa racemosa ten and Antithamnion pectina-tum 13. Fifteen of the twenty-six species listed asinvasive were among the twenty highest ranked.On average for all these categories, all introducedalgae had higher scores than the correspondinggroup of native species (Appendix 1).

Discussion

The use of interval arithmetic for quantifyingspecies traits is an easy approach to obtain a

Figure 4. (a) Summarization of all species for each category:

introduced (r) and native ()). (b) Summarization of all spe-

cies for each category: Invasive (r) and non-invasive ()).Figure 5. (a) Summarization of all categories in each main

category (excluding salinity and temperature in the main cate-

gory establishment). For symbols and abbreviations, see Fig-

ure 1a. (b) Summarization of all categories in each main

category (excluding salinity and temperature in the main cate-

gory establishment). For symbols and abbreviations, see

Figure 1b.

272

value for comparing different species or groupsand it allowed us to incorporate different levelsof uncertainties (Hayes et al. 2003). When reli-able literature data were available, only the high-est interval in the category was scored. The maintype of uncertainties in our analysis were associ-ated with the lack of available information whichmade it necessary for us to use ‘educatedguesses’, however, this was compensated for witha broader interval. It was especially hard to findecological data for all our comparisons. It wouldbe beneficial for invasion studies if more scien-tists writing about species taxonomy and distri-

bution also included ecological data, at least ontemperature and salinity of the area.

A few species traits have been used in differentmain categories. In the case of fragmentation/vegetative propagules, we consider these charac-ters a very high risk when establishing a popula-tion. Sakai et al. (2001) found that one of thetraits that promote the success of an invasive spe-cies is the possibility to reproduce both sexuallyand asexually. However, we also see such traitsas a medium risk in the probability of dispersal,since only fragments need to spread. Maximumsize was used directly when comparing the risk of

Table 4. The most hazardous algae in Europe and their score. Names in bold are invasive species and bold italics highly invasive

species.

Dispersal (3 categories) Score Establishment (excluding salinity

and temperature, 4 categories)

Score

Caulacanthus ustulatus 0.73 Asparagopsis armatac 0.91

Grateloupia doryphora 0.72 Antithamnion pectinatum 0.86

Pikea californica 0.72 Acrothamnion preissii 0.85

Antithamnionella spirographidis 0.67 Antithamnion amphigeneum 0.85

Symphyocladia marchantioides 0.67 Antithamnionella elegans 0.85

Asparagopsis armatac 0.65 Antithamnionella spirographidis 0.85

Bonnemaisonia hamifera 0.65 Antithamnionella ternifolia 0.85

Dasya baillouviana 0.65 Hypnea valentiae 0.81

Undaria pinnatifidac 0.95 Pilayella littoralis 0.81

Colpomenia perigrina 0.77 Desmarestia viridis 0.78

Sphaerotrichia divaricata 0.77 Ectocarpus siliculosus 0.71

Leathesia difformis 0.75 Endarachne binghamiae 0.71

Codium fragile spp. tomentosoides 0.72 Caulerpa taxifoliaa 0.88

Caulerpa racemosaa 0.63 Codium fragile spp. tomentosoides 0.83

Monostroma obscurum 0.60 Caulerpa scalpelliformis 0.78

Caulerpa taxifoliaa 0.55 Codium fragile spp. scandinavicum 0.76

Ecological impact (4 categories) Score All categories (excl. salinity and

temperature, 11 categories)

Score

Grateloupia doryphora 0.81 Asparagopsis armatac 0.74

Grateloupia filicina var. luxurians 0.74 Grateloupia doryphora 0.73

Mastocarpus stellatusex 0.70 Dasya baillouviana 0.72

Polysiphonia harveyi 0.69 Antithamnion pectinatum 0.70

Dasya baillouviana 0.69 Antithamnionella spirographidis 0.69

Chrysymenia wrightii 0.69 Antithamnionella ternifolia 0.68

Polysiphonia fucoides 0.69 Agardhiella subulata 0.68

Womersleyella setacea 0.68 Acrothamnion preissii 0.67

Macrocystis pyriferaex 0.93 Undaria pinnatifidac 0.75

Sargassum muticum 0.89 Pilayella littoralis 0.73

Undaria pinnatifidac 0.86 Sargassum muticum 0.71

Laminaria japonicac 0.84 Ectocarpus siliculosus 0.70

Caulerpa taxifoliaa 0.81 Codium fragile spp. tomentosoides 0.79

Codium fragile spp. tomentosoides 0.81 Caulerpa taxifoliaa 0.76

Monostroma obscurum 0.75 Monostroma obscurum 0.71

Caulerpa racemosaa 0.71 Caulerpa racemosaa 0.70aSpecies used in aquaria trade.cCultivated species.exSpecies used in field experiments.

273

the ecological impact, but the lowest interval wasalso used in the category ‘morphology’, since itdid not seem meaningful to discuss the impact ofmorphology for plants not exceeding 1 cm. Inthe probability of dispersal, possessing micro-scopical stages were ranked slightly higher thanhaving large stages only, since microscopic stagesmay grow in very small crevices, etc., but thesame species may score the highest risk of eco-logical impact of size (e.g. kelp species).

The category intervals used were obviously notcompletely objective because we defined inadvance the specific traits which make it easierfor a species to be spread, get established andhave an effect on the ecology. This was, however,necessary to develop a designated quantitativeapproach which hopefully can be used for futurerisk assessments and we evaluated each speciesindividually, independent of being invasive ornot.

When comparing introduced and native specieswe used the same number of taxa. However, theother comparisons (between red, brown andgreen algae as well as invasive and non-invasivespecies) were not based on the same number oftaxa. Because we chose to base this study on allintroduced macroalgae in Europe we could notget an even number of red, brown and greenalgal species, unless we reduced all groups to theminimum level. This, however, would have meantthat much information was lost. Thus a greenalga scoring a high or low risk meant morefor the average of that group than a red algadid. Furthermore, most green algae belonged tojust two families (Caulerpaceae and Codiaceae).Also the comparison of invasive and non-inva-sive brown and red algae is prone to such dis-crepancies. However, the scores for theindividual species and their ranking are notaffected by this.

There were several interesting trends of speciestraits in our study that are important for intro-duced species in comparison to native. The larg-est differences in risk were the higherprobabilities of being transported, the largerimpact on the habitat, their geographical distri-bution, and when all species were combined alsotolerance to pollutants. There were no differencesin life span, grazing or survival time out of waterof introduced vs native species. We were expect-

ing a broader tolerance range for dehydration,salinity, temperature, and grazing and defensemechanisms for introduced species. The reasonfor our expectations is that the ability to survivedehydration for a longer time could be necessaryto survive transportation in fishnets, aroundanchors on deck or as packing material. Also abroad tolerance range for salinity, temperatureand pollutants as well as grazing facilitates thesurvival in new areas, even though the conditionsmay not be the same as in their original area. Awide environmental tolerance, meaning a toler-ance to the stresses of environmental fluctuationsand extremes, promotes the success of introducedspecies (Boudouresque and Verlaque 2002). Theonly category meeting our expectations was thetolerance to pollutants which is advantageous forthe establishment in contaminated harbors or ineutrophicated areas. The reason we did not getthe expected results for dehydration and salinitymight be due to the lack of data. The salinityranges may be underestimated, since literaturedoes not always state estuarine occurrence.Defense mechanisms have in earlier studiesshown to be important (Maggs and Stegenga1999; Boudouresque and Verlaque 2002). Oneexplanation why we did not see the same clearpattern probably is that a larger number of spe-cies was used by us, including also non-invasivespecies. However, we found differences betweeninvasive and non-invasive red and green algae.Another important trait that many introducedspecies have that facilitate both dispersal andestablishment is the ability to grow on a widevariety of substrates, from sand to artificial sur-faces, as well as on live molluscs. This characteris also of importance for the habitat effects.

Dividing introduced species into invasive andnon-invasive we can see that important charac-ters of the invasive species are their large impacton the habitat through development of a densecover, suppression of other species and their dis-tribution in a large depth range. The invasivespecies also have a higher risk in their geographi-cal distribution, more grazing resistance and asomewhat higher impact through a larger sizeand their morphology. No pattern is noticed forthe categories survival time out of water, toler-ance to temperature, salinity and pollutants, norgrowth strategies or life span.

274

The main categories we have chosen do notinclude all categories of interest to compare. Wealso wanted to include survival time in darknesswhich is crucial for survival in the northern partsof Europe and also for the survival in ballastwater tanks. Dispersal of pathogens and parasitesis also of great importance. A new species thatbrings pathogens into an area may have a verystrong effect on the native species. Another viewis discussed in three recent studies. These sug-gested that species are more likely to becomeinvasive when they are released from their naturalenemies such as parasites (Clay 2003; Torchinet al. 2003) or pathogens (Mitchell and Power2003). The reason we did not include the catego-ries for darkness and pathogens and parasites arethat we found very little information for most spe-cies, and they were almost impossible to estimate.Another character which probably is important,but more difficult to quantify, is the matching oftemperature and day length, where a mismatchoften leads to loss of fertility (e.g. Breeman et al.1988; Guiry and Dawes 1992), but the speciesmay still survive through vegetative reproduction.

No risks of economic impact were calculatedby us. Such criteria may largely depend on theactivities in the receiving area and few such dataare available for others than highly invasive spe-cies. It is likely that species having a high risk ofecological impact also have a negative impact oneconomy, at least indirectly, as have speciesgrowing on artificial substrates and shellfish.

The difficulty with this study was the lack ofecological information and especially experimen-tal data for survival time out of water and effectsof grazers, but also experiments on factors suchas salinity, temperature and response to pollu-tants (including nutrient enrichment) are oftenlacking. We chose not to include temperatureand salinity when calculating the total averagescore and ranking, to have a more general pic-ture of species traits of importance for introduc-tions. However, in a regional to local perspectivesalinity and temperature tolerances are highlyimportant for survival. This especially concernsthe Baltic and Kattegat coasts, but may also gov-ern survival in many estuaries, lagoons and har-bor areas.

Summing the categories (Table 4) gave us 16species that turned out most hazardous, for each

main category as well as totally. For example,the totally highest ranked red alga Asparagopsisarmata was not among the eight red algae withthe highest ecological impact, while invasive redalgae such as Mastocarpus stellatus and Womers-leyella setacea only were among the eight worstred algae in this main category, but not in thetwo others. Caulacanthus ustulatus is thought tobe very easily dispersed but because it scoredlower risks in getting established and has a verylow ecological impact it did not reveal to be oneof the most risky species when summarizing allthe categories. In contrast the green algae, Caul-erpa taxifolia and Codium fragile ssp. tomentoso-ides ranked as first or second most risky speciesin all categories. In general large species or thosedominating or suppressing other species were themost risky ones in the main category ‘Impact’.The red algae had a lower average score than theother groups due to the many tiny species amongthe introductions. In the main category ‘Estab-lishment’ the highest risks were with fast-growingR-strategists, often having grazing defense andasexual reproduction. This accentuates the needto include all the three main categories whenevaluating the risk of a species’ possibility toestablish and become invasive.

Our purpose was not to use the results todescribe the average traits of an introduced or aninvasive species, but to see if the categories andintervals we proposed gave ranks that seemedplausible, and would place most of the invasivespecies high in the ranking, which most of themdid. Thus if a species will score high in many ofthe categories listed here, and also has salinityand temperature survival ranges that encompassthat of the geographical area of interest, such aspecies may pose a high risk of becoming inva-sive there. If this setup is used to test the risk ofa species being intentionally released in an area,then the main category ‘Dispersal’ might beexcluded. Our setup may also be used to rankthe most risky donor species.

The reason not all known invasive speciesranked high in this study is that different featureshave been compared in earlier studies and in thisstudy. In earlier studies usually only a fewaspects were regarded but in this study severalaspects were examined. We are aware of that areader trying to sum the overall score for a

275

specific species may end up with a different num-ber than we did. However, our main purpose wasnot to get fix risk values for the species involvedbut to look for patterns in species traits and howrisks may be quantitatively assessed. We hopethat combined expert knowledge may be used torefine the tabular setup we have used for devel-opment of future risk assessments.

Acknowledgements

We thank Keith Hayes CRIMP, CSIRO, Austra-lia, for his ideas and support on how to useinterval arithmetic and Frank Linares and MalinWerner for their technical support. We are alsomuch obliged to the Swedish EPA for financingthe AquAliens project.

Appendix 1. Introduced macroalgae in Europe and randomized native European species from the same families as the introduced.

The score for each species is the average for all categories excluding temperature and salinity. Names in bold refer to invasive spe-

cies, bold italics represent highly invasive species

Family Introduced species Score Native species Score

77 red algae

Bangiaceae Porphyra yezoensisc 0.60 Porphyra miniata 0.49

Phragmonemataceae Goniotrichiopsis sublittoralis 0.37 Neevea repens 0.40

Achrochaetiaceae Acrochaetium balticum 0.39 Acrochaetium corymbiferum 0.41

Achrochaetiaceae Acrochaetium cf. codicolum 0.47 Acrochaetium microscopicum 0.40

Rhodophysemataceae Rhodophysema georgei 0.44 Rhodophysema elegans 0.46

Liagoraceae Ganonema farinosum 0.48 Liagora tetrasporifera 0.42

Gracilariaceae Gracilaria multipartita 0.40 Gracilaria dura 0.53

Bonnemaisoniaceae Asparagopsis armatac 0.75 Asparagopsis taxiformis 0.61

Bonnemaisoniaceae Asparagopsis taxiformis 0.61 Bonnemaisonia asparagoides 0.44

Bonnemaisoniaceae Bonnemaisonia hamifera 0.65 Bonnemaisonia clavata 0.40

Dumontiaceae Pikea californica 0.56 Dudresnaya verticillata 0.42

Halymeniaceae Grateloupia doryphora 0.73 Cryptonemia tunaeformis 0.46

Halymeniaceae Grateloupia filicina var. luxurians 0.60 Grateloupia cuneifolia 0.35

Halymeniaceae Grateloupia lanceolata 0.55 Grateloupia proteus 0.42

Halymeniaceae Grateloupia cf. turuturu 0.54 Halymenia dichotoma 0.31

Halymeniaceae Prionitis patens 0.51 Halymenia floridana 0.39

Corallinaceae Lithophyllum yessoense 0.52 Pneophyllum subplanum 0.18

Caulacanthaceae Caulacanthus ustulatus 0.56 Caulacanthus ustulatus 0.56

Gigartinaceae Chondrus giganteus 0.45 Chondracanthus teedei 0.55

Hypneaceae Hypnea cornuta 0.55 Hypnea arbuscula 0.45

Hypneaceae Hypnea esperi 0.51 Hypnea coccinea 0.44

Hypneaceae Hypnea spinella 0.57 Hypnea flagelliformis 0.49

Hypneaceae Hypnea valentiae 0.62 Hypneocolax stellaris 0.31

Nemastomataceae Predaea huismanii 0.45 Predaea pusilla 0.44

Phyllophoraceae Mastocarpus stellatusex 0.58 Mastocarpus stellatus

ex 0.58

Phyllophoraceae Ahnfeltiopsis flabelliformis 0.52 Gymnogongrus patens 0.41

Areschougiaceae Agardhiella subulata 0.68 Meristotheca decumbens* 0.27

Areschougiaceae Sarconema filiforme 0.46 Rhabdonia decumbens* 0.27

Areschougiaceae Sarconema scinaioides 0.40 Sarcodiotheca divaricata 0.43

Areschougiaceae Solieria chordalis 0.49 Solieria chordalis 0.49

Areschougiaceae Solieria filiformis 0.59 Turnerella pennyi 0.50

Plocamiaceae Plocamium secundatum 0.45 Plocamium raphelisianum 0.38

Lomentariaceae Lomentaria hakodatensis 0.55 Lomentaria baileyana 0.57

Rhodymeniaceae Botryocladia madagascariensis 0.45 Botryocladia chiajeana 0.33

Rhodymeniaceae Chrysymenia wrightii 0.60 Chrysymenia ventricosa 0.40

Ceramiaceae Acrothamnion preissii 0.67 Aglaothamnion gallicum 0.34

Ceramiaceae Aglaothamnion feldmanniae 0.53 Aglaothamnion sepositum 0.50

Ceramiaceae Aglaothamnion halliae 0.52 Anotrichium barbatum 0.31

Ceramiaceae Anotrichium furcellatum 0.60 Antithamnion cruciatum 0.51

Ceramiaceae Antithamnion amphigeneum 0.53 Balliella cladoderma 0.40

Ceramiaceae Antithamnion densum 0.47 Bornetia secundiflora 0.44

276

Appendix 1. Continued

Family Introduced species Score Native species Score

77 red algae

Ceramiaceae Antithamnion diminuatum 0.48 Callithamnion tetricum 0.45

Ceramiaceae Antithamnion pectinatum 0.70 Ceramium circinatum 0.53

Ceramiaceae Antithamnionella elegans 0.50 Ceramium codii 0.55

Ceramiaceae Antithamnionella sublittoralis 0.38 Ceramium diaphanum 0.57

Ceramiaceae Antithamnionella spirographidis 0.69 Ceramium secundatum 0.54

Ceramiaceae Antithamnionella ternifolia 0.68 Diplothamnion jolyi 0.30

Ceramiaceae Ceramium bisporum 0.33 Dohrniella neapolitana 0.40

Ceramiaceae Ceramium strobiliforme 0.32 Griffithsia phyllamphora 0.35

Ceramiaceae Grallatoria reptans 0.30 Ptilocladiopsis horrida 0.39

Ceramiaceae Griffithsia corallinoides 0.60 Ptilota serrata 0.35

Ceramiaceae Gymnophycus hapsiphorus 0.50 Seirospora interrupta 0.50

Ceramiaceae Pleonosporium caribaeum 0.57 Spermothamnion repens 0.57

Ceramiaceae Scageliopsis patens 0.50 Wrangelia penicillata 0.50

Dasyaceae Dasya baillouviana 0.72 Dasya baillouviana 0.72

Dasyaceae Dasya sessilis 0.58 Eupogodon planus 0.44

Dasyaceae Heterosiphonia japonica 0.64 Heterosiphonia crispella 0.49

Delesseriaceae Apoglossum gregarium 0.32 Erythroglossum balearicum 0.32

Delesseriaceae Platysiphonia caribaea 0.36 Nitophyllum flabellatum 0.33

Rhodomelaceae Acanthophora nayadiformis 0.61 Aphanocladia stichidiosa 0.39

Rhodomelaceae Chondria coerulescens 0.46 Chondria capillaris 0.43

Rhodomelaceae Chondria curvilineata 0.33 Chondria curvilineata 0.33

Rhodomelaceae Chondria polyrhiza 0.46 Chondria oppositiclada 0.51

Rhodomelaceae Chondria pygmaea 0.36 Chondrophycus papillosus 0.57

Rhodomelaceae Herposiphonia parca 0.45 Ctenosiphonia hypnoides 0.36

Rhodomelaceae Laurencia brongniartii 0.52 Laurencia brongniartii 0.52

Rhodomelaceae Laurencia okamurae 0.54 Laurencia obtusa 0.66

Rhodomelaceae Lophocladia lallemandii 0.48 Laurencia viridis 0.38

Rhodomelaceae Polysiphonia fucoides 0.62 Osmundaria volubilis 0.40

Rhodomelaceae Polysiphonia harveyi 0.67 Osmundea pelagosae 0.48

Rhodomelaceae Polysiphonia morrowii 0.63 Osmundea pinnatifida 0.44

Rhodomelaceae Polysiphonia paniculata 0.43 Polysiphonia arctica 0.50

Rhodomelaceae Polysiphonia senticulosa 0.62 Polysiphonia atlantica 0.66

Rhodomelaceae Pterosiphonia pinnulata 0.54 Polysiphonia polyspora 0.40

Rhodomelaceae Pterosiphonia tanakae 0.43 Polysiphonia rhunensis 0.45

Rhodomelaceae Symphyocladia marchantioides 0.54 Pterosiphonia ardreana 0.38

Rhodomelaceae Womersleyella setacea 0.63 Symphyocladia marchantioides 0.54

Average 0.53 0.44

26 Brown algae

Ectocarpaceae Ectocarpus siliculosus 0.70 Feldmannia lebelii 0.31

Acinetosporaceae Pilayella littoralis 0.73 Pilayella littoralis 0.73

Dictyotaceae Padina boergesenii 0.42 Dictyopteris divaricata 0.41

Dictyotaceae Stypopodium schimperi 0.50 Taonia atomaria 0.44

Chordariaceae Acrothrix gracilis 0.59 Acrothrix gracilis 0.59

Chordariaceae Asperococcus scaber 0.33 Asperococcus scaber 0.33

Chordariaceae Cladosiphon zosterae 0.52 Clathrodiscus mandouli 0.32

Chordariaceae Corynophlaea umbellata 0.34 Corynophlaea cystophorae 0.41

Chordariaceae Halothrix lumbricalis 0.48 Corynophlaea flaccida 0.32

Chordariaceae Leathesia difformis 0.55 Herponema solitarium 0.30

Chordariaceae Leathesia verruculiformis 0.36 Leptonematella fasciculata 0.45

Chordariaceae Punctaria tenuissima 0.50 Microcoryne ocellata 0.35

Chordariaceae Sphaerotrichia divaricata 0.62 Saundersella simplex 0.44

Scytosiphonaceae Colpomenia peregrina 0.62 Colpomenia sinuosa 0.53

Scytosiphonaceae Endarachne binghamiae 0.60 Compsonema saxicolum 0.43

Scytosiphonaceae Scytosiphon dotyi 0.52 Petalonia zosterifolia 0.56

Desmarestiaceae Desmarestia viridis 0.70 Desmarestia aculeata 0.55

277

Note added in proof

The introduced red alga here called Grateloupiadoryphora has, according to Gavio and Fredrique(2002), been identified as the Japanese speciesGrateloupia turuturu.

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Family Introduced species Score Native species Score

26 Brown algae

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