A weed risk assessment model for use as a biosecurity tool evaluating plant introductions

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Journal of Environmental Management (1999) 57, 239–251
Article No. jema.1999.0297, available online at http://www.idealibrary.com on

A weed risk assessment model for use
as a biosecurity tool evaluating plant
introductions
P. C. Pheloung†‡ , P. A. Williams§* , S. R. Halloy¶

New plant taxa from around the world continue to be imported into Australia and New Zealand. Many of
these taxa have the potential to become agricultural or environmental weeds and this risk needs to be
assessed before allowing their entry. A weed risk assessment system is described that uses information
on a taxon’s current weed status in other parts of the world, climate and environmental preferences, and
biological attributes. The system is designed to be operated by quarantine personnel via a user-friendly
computer interface.
   The model was tested against experts’ scores for weediness for 370 taxa present in Australia, representing
both weeds and useful taxa from agriculture, the environment, and other sectors. The model was judged on
its ability to correctly ‘reject’ weeds, ‘accept’ non-weeds, and generate a low proportion of taxa which could
not be decisively categorised, termed ‘evaluate’. More than 70% of the taxa were rejected or accepted. All
taxa classified as serious weeds, and most minor weeds, were rejected or required further evaluation, while
only 7% of non-weeds were rejected. The model was modified to New Zealand conditions and evaluated
against the opinions of several groups of experts and against economic measures. The model produced a
weediness score very similar to the mean of the experts scores. The latter were highly variable: agriculturalists
tended to accept known weeds, conservationists tended to reject most adventive taxa, and only botanists
produced scores similar to the model. The model scores also tended to be independent of economic value
as measured in this study. The model could be adapted for use as a screening tool in any region of the world.
 1999 Academic Press

Keywords: Australia, New Zealand, weed risk assessment, plant introductions, biosecurity,
quarantine, computer model.

Introduction                                              potential (reviewed by Mack, 1996), but bor-
                                                          der authorities urgently need an objective,
                                                                                                                    Ł Corresponding author
                                                          credible, and publicly acceptable risk assess-
Weeds have major impacts on economies and                 ment system to predict the weediness, or                  † Agriculture Western
natural environments world wide, including                invasive potential, of the thousands of poten-            Australia, 3 Baron-Hay Crt,
                                                                                                                    South Perth WA 6151,
Australia (Groves, 1986) and New Zealand                  tial new entries.                                         Australia
(Williams and Timmins, 1990). Many of these                  There have been several symposia (e.g.
weeds have been purposely introduced as                   Drake et al., 1989) and a growing research                ‡ Present address:
                                                                                                                    Australian Quarantine
potential new crops, ornamentals, or as novel-            literature on invasive plant taxa, but until              Inspection Service, GPO
ties (Esler, 1988; Lonsdale, 1994). To counter            recently there was considerable pessimism                 Box 858, Canberra,
the threat to agriculture or the environment              that potentially invasive species could be                ACT 2601, Australia

from new plant taxa, regulatory authori-                  identified (Crawley, 1987). However, progress             § Landcare Research,
ties have a statutory responsibility to ensure            has recently been made in identifying the                 Private Bag 6, Nelson,
that all plant taxa proposed to be imported,              key characteristics of potential weeds in                 New Zealand

which are not already prohibited and are not              Australia (Noble, 1988; Scott and Panetta,                ¶ Crop and Food, Private
already established, be evaluated for their               1993), New Zealand (Esler et al., 1993),                  Bag, Mosgiel, New
potential to damage the productive capac-                 South Africa (Richardson et al., 1990),                   Zealand

ity or environment of these countries. There              Britain (Williamson and Fitter, 1996), and                Received 27 August 1998;
are many approaches to predicting weed                    north America (Mack 1996; Reichard and                    accepted 23 April 1999

0301–4797/99/120239C13 $30.00/0                                                                                        1999 Academic Press
240   P. C. Pheloung et al.

                       Hamilton, 1997), or within closely related         authority that satisfies many of these crite-
                       groups of taxa including herbs (Forcella et al.,   ria: the Weed Risk Assessment model (WRA).
                       1986; Williamson, 1993) or woody seed plants       We then report on a test of the applicabil-
                       (Rejmanek and Richardson, 1996). Predic-           ity of a slightly altered version of the model
                       tions from a non-experimental approach are         that incorporates environmental differences
                       most accurate if they are based on informa-        between Australia and New Zealand: the
                       tion that includes the biology of the invad-       New Zealand Weed Risk Assessment Model
                       ing species, the bioclimatic features of the       (New Zealand WRA). In testing the New
                       recipient and source regions, and the evo-         Zealand WRA we examine the sources of
                       lutionary history of both (e.g. Richardson         expert bias that are inherent in the con-
                       et al., 1990). A synthesis of this informa-        cept of weediness (Perrins et al., 1992) and
                       tion can lead to general conceptual models of      demonstrate that the model minimises these
                       plant invasiveness (Rejmanek, 1995) which          difficulties.
                       in turn can be applied to screening procedures        The model could be used to investigate
                       such as decision trees to categorise poten-        the nature of weediness, but here we simply
                       tial plant imports (Panetta, 1993; Tucker and      describe how it works and the steps we took
                       Richardson, 1995; Reichard, 1996; Reichard         to ensure it would function as a publicly
                                                                          acceptable screening tool.
                       and Hamilton, 1997). Regulatory authorities
                       responsible for biosecurity need a tool that
                       synthesizes much of this disparate and some-       Methods and results
                       times theoretical information. One approach
                       is a computer based spreadsheet model pro-         Producing the WRA
                       ducing a score for weediness, which can then
                       be converted to an entry recommendation for        The basis of the WRA is the answers to
                       a specified taxon.                                 49 questions (Appendix 1) based on the main
                          An acceptable biosecurity assessment sys-       attributes and impacts of weeds. These are
                       tem should satisfy a number of requirements        combined into a scoring system which in
                       (Hazard, 1988; Panetta, 1993). It should be        the absence of any evidence to the contrary,
                       calibrated and validated against a large num-      gives an equal weight to nearly all questions
                       ber of taxa already present in the recipient       (Appendix 2). These cover a range of weedy
                       country and representing the full spectrum of      attributes in order to screen for taxa that are
                       taxa likely to be encountered as imports into      likely to become weeds of the environment
                       that country. It must effectively discriminate     and/or agriculture. The questions are divided
                                                                          into three sections producing identifiable
                       between weeds and non-weeds, such that the
                                                                          scores that contribute to the total score
                       majority of weeds are not accepted, non-
                                                                          (Appendix 2).
                       weeds are not rejected, and the proportion
                                                                             Biogeography (section A) encompasses
                       of taxa requiring further evaluation is kept
                                                                          the documented distribution, climate
                       to a minimum. As international trade agree-
                                                                          preferences, history of cultivation, and
                       ments require that prohibited taxa should
                                                                          weediness of a plant taxon elsewhere in the
                       fit the definition of a quarantine pest before     world, i.e. apart from the proposed recipient
                       they can be excluded by quarantine regula-         country. Weediness elsewhere is a good
                       tions (Anon., 1994, 1995; Walton and Parnell,      predictor of a taxon becoming a weed in new
                       1996), the system must be based on explicit        areas with similar environmental conditions
                       assumptions and scientific principles so that      (Forcella and Wood, 1984; Panetta and
                       the country cannot be accused of applying          Mitchell, 1991a,b). The question concerning
                       unjustified non-tariff trade barriers. Ideally     the history of cultivation recognises the
                       the system should be capable of identifying        important human component of propagule
                       which land use system the taxon is likely to       pressure (Richardson et al., 1994; Williamson
                       invade, to assist in an economic evaluation        and Fitter, 1996), but such data are obviously
                       of its potential impacts. Finally, the sys-        never available for the proposed new
                       tem must be cost effective to the prospective      country. The global distribution and climate
                       importer and the border control authority.         preferences, where these are available, are
                          Here, we first describe a model designed        used to predict a potential distribution in the
                       specifically for the Australian quarantine         recipient country.
A weed risk assessment model   241

   Undesirable attributes (section B) are char-      A benchmark against which to compare the
acteristics such as toxic fruits and unpalat-      model is problematic because there are no
ibility, or invasive behaviour, such as a          absolute values for weediness of individual
climbing or smothering growth habit, or the        taxa (Perrins et al., 1992). However, those
ability to survive in dense shade.                 familiar with a taxon in a country can offer a
   Biology/ecology (section C) are the attri-      meaningful opinion on the actual or potential
butes that enable a taxon to reproduce,            weediness of the taxon in that country,
spread, and persist (Noble, 1988), such as         against which to compare the score from the
whether the plant is wind dispersed or animal      model. (The sources of bias in this procedure
dispersed, and whether the seeds would             are examined in evaluating the New Zealand
survive passage through an animal’s gut.           WRA.) A further 12 scientists therefore
   Availability of information is often very       defined the weed status or usefulness of taxa
limited for new species which can restrain         they were familiar with. Taxa were given a
the utility of screening systems. To ensure        rank of 0, 1 or 2 and this was used to classify
that at least some questions were answered         them as non-weeds, minor weeds, and serious
for each section, the WRA system requires          weeds, respectively. The mean score was used
the answers to two questions in section A,         to assess the performance of the WRA model;
two in section B, and six in section C before it   again, potential bias is examined in testing
will give an evaluation and recommendation.        the New Zealand WRA.
The recommendation can be compared with
the number of questions answered as an
indication of its reliability, which obviously     Results of the WRA
improves as more questions are answered.
   Answers to the questions provide a poten-       The majority of the 370 taxa (81%) are
tial total score ranging from 14 (benign           perceived as weeds in some context, but
taxa) to 29 (maximum weediness) for each           less than half are considered serious weeds.
taxon. The total score is partitioned between      Useful taxa (63%) including both weeds
answers to questions considered to relate pri-     (45%) and non-weeds (18%), and non-useful
marily to agriculture, to the environment, or      taxa (37%) were included in the sam-
common to both (Appendix 1). The total scores      ple. Weeds from all sectors—agriculture,
are converted to one of the three possible rec-    environment, horticulture, garden and ser-
ommendations by two critical score settings.       vice areas—were well represented (data not
The lower critical score, 0, separates accept-     shown).
able taxa from those requiring evaluation,            The cumulative frequency distributions of
and the higher critical score, 6, separates        WRA scores, for each of the survey classifica-
taxa requiring evaluation from those that          tions (Figure 1), were used to investigate the
should be rejected. Evaluation could mean          effect of different pairs of critical scores on
either obtaining more data and re-running          the distribution of WRA recommendations.
the model, or undertaking further investiga-       The range of scores for non-weeds overlaps
tions such as field trials (Mack, 1996).           the range for serious weeds, so it is impos-
   To provide data for defining these score        sible to define any set of critical scores that
settings, six Australian scientists in a range     reject all serious weeds while accepting all
of the fields ran the model to assess the          non-weeds. However, it is possible to ensure
weed potential of taxa they were familiar          that none of the serious weeds are accepted by
with, ranging from non-weedy beneficial taxa       setting the accept score at 0 or less. Similarly,
to serious weeds. In addition, all taxa that       less than 10% of non-weeds will be rejected if
have a noxious status in Australia were            the reject score is greater than 6. This would
assessed using the information provided by         mean that 29% of the taxa assessed in this
Parsons and Cuthbertson (1992). Assessors          study would fall between these extremes and
treated each taxon as if it had not yet            require evaluation. Lowering the minimum
arrived in Australia, such that serious weeds,     reject score to 6 would reduce this proportion
for example, were assessed purely on their         to 22% but increase the proportion of rejected
weed status outside Australia. The taxa were       non-weeds to 15%, which is less desirable,
classified as agricultural or environmental        since some of these are regarded as useful
weeds.                                             (Figure 1). Consequently, the critical scores,
242   P. C. Pheloung et al.

                                Proportion of species scoring the amount shown or less (%)
                                                                                             100

                                                                                             80

                                                                                             60      Accept                                                  Reject

                                                                                             40

                                                                                             20

                                                                                              0
                                                                                              –15   –10           –5       0           5       10       15       20       25     30
                                                                                                                               Weed risk assessment score

                       Figure 1. Cumulative frequency of taxa receiving a particular WRA score or less for each survey
                       classification. Survey categories: ( M ), serious weeds (139); ( ž ), minor weeds (147); (  ), non-weeds
                       (84); (      ), all plants (370).

                       0 and 6, were used to convert the WRA scores                                                                         Table 2. Correlations of the agriculture and
                       into the recommendations–‘accept’, ‘evaluate’                                                                        environment components of the WRA score
                                                                                                                                            and the total WRA score, with the experts
                       and ‘reject’. These settings recommended all                                                                         classification of taxa as weeds of agriculture
                       serious weeds and most minor weeds (84%)                                                                             or environment. All P
A weed risk assessment model   243

‘a range of soil conditions’ because infertile        The WRA database contains replicate
soils are not as extensive in New Zealand. As       scores from the six independent Australian
anticipated, several questions that remained        experts. These were used to estimate the vari-
the same needed to be answered differently          ance of the model scores, on the assumption
for Australia and New Zealand; e.g. in              that a similar degree of variability would be
Australia there are many parrots which              found in the scores from experts using the
destroy seeds, and so certain new plants            New Zealand WRA model.
are more likely to have natural enemies in            Next, 13 New Zealand experts, 12 of whom
Australia than in New Zealand. None of              were not involved with the model, classified
the modified questions required alterations         many of the same 291 taxa into the categories
to the scoring system, so that the outcome          of non-weed, minor weed, and major weed.
scores were directly comparable. The outcome        The categories were not defined, and neither
of these changes was the New Zealand                were the taxa classified as environmental or
WRA model.                                          agricultural weeds as in Australia. However,
                                                    respondents were asked not to consider
                                                    economic value, i.e. we were interested only in
                                                    their opinion as to whether taxa were weeds
Testing the New Zealand WRA                         in any land-use system. This classification
                                                    was transformed into the numbers 0, 0Ð5 and
We assessed the ability of the model to iden-       1Ð0, respectively. The experts were classified
tify weeds of a range of land use systems when      by one of us (P.A.W.) as botanists (seven),
used in a country for which it was not origi-       agriculturalists (three), and conservationists
nally designed, in this instance New Zealand.       (three). This classification was unknown to
   We also tested the New Zealand WRA—in            them, to avoid any conscious bias. This
a manner that was equally relevant to               allowed an evaluation of speciality bias with
WRA—by asking whether it was better than            respect to classification, and how it affected
an expert’s opinion? ‘Better’ we define as          variation. Each expert reviewed between
efficacy, ease of use, and cost of use but only     twenty-seven and 291 taxa, with most doing
efficacy was tested, i.e. the capability to score   between 140 and 250 taxa. Two hundred and
correctly with respect to the benchmark, and        seventy-four taxa were classified by more
with a low variation when used by several           than one expert.
individuals.                                          Finally, 195 taxa for which data were avail-
   We tested whether the New Zealand WRA            able were scored for relative economic value,
was more biased by economic or environ-             based on the average of three evaluations.
mental considerations than the collective           (1) The area of the taxon cultivated from
opinion, as represented by an average score,        1842 to 1991 was obtained from New Zealand
of a group of experts representing a wide           statistics as processed by Halloy (1994). The
range of interests. This potentially large ele-     logarithm of this area was standardised to a
ment of subjectivity was tested with a series       range of 0 to 1. (2) An estimate of an eco-
of cross-checks on variation and bias using         nomic value of any type was scored as 0 to 5
three data sets referred to the same taxa.          by one of us (S.R.H.) then standardised 0 to 1.
   Firstly, the New Zealand WRA model was           (3) Taxa were scored according to their pres-
run on 198 taxa used in testing the WRA             ence or absence in the New Zealand Nursery
model that are also present in New Zealand          Register 1995/1996, on the assumption that
(the majority of which are adventive), plus         a listing represents value as an ornamental
any additional noxious plants in New Zealand        but not as a major economic plant. Scores
(Esler et al., 1993). Responses to the model        were 1 if the taxon was present, 0Ð5 if only
questions for the resulting 291 taxa were           the genus was present but with probability of
made by one of us (P.A.W) as if they were not       the taxon being present, 0 if the genus was
yet in New Zealand, using the international         absent. This value was standardised 0 to 0Ð2.
literature, floras, and databases. The scores         The data were divided into five classes, and
of 14 to 29 for each taxon were standardised        the taxon score outcomes for New Zealand
from 0 to 1 for comparison with the other data      WRA and the experts were compared within
sets, using the thresholds: accept
244   P. C. Pheloung et al.

                       WRA within each economic class is expressed              ‘evaluate’ category of the three expert groups,
                       as percentages.                                          as against 21% for the model, shows that
                         Lastly, the total scores for the WRA and               all expert groups have a tendency to either
                       New Zealand WRA models derived in the two                accept or reject a larger proportion of taxa
                       countries were compared for the 198 taxa                 than the model (Table 3).
                       common to both.                                             There are differences in recommendations
                                                                                between the New Zealand WRA model and
                                                                                the average experts’ evaluation (Figure 2).
                       Results of testing the New Zealand
                                                                                Sixty-four percent of taxa did not change,
                       WRA                                                      and overall 93% of taxa either rejected
                                                                                by the model or requiring evaluation were
                       The combined scores and their variability
                                                                                also not accepted by the experts. Only 4%
                       show a strong similarity between the scores
                                                                                of taxa that were accepted by the model
                       from the New Zealand WRA model (0Ð538)
                                                                                were rejected by the expert averages. Two
                       and the mean scores for the 13 experts
                                                                                differences between the New Zealand WRA
                       (0Ð545), and for the deviations, and the dis-
                                                                                outcomes and the expert outcomes (Figure 2)
                       tributions (Table 3). When converted to out-
                                                                                require examination.
                       comes the results are again very similar. That
                       the higher proportion of taxa rejected by both              (1) A greater permissiveness in the model
                       the New Zealand WRA model and the experts                as compared with the experts could allow
                       score (mean 62Ð0%) is higher than might be               introduction of weeds if the model alone were
                       expected from a random selection of taxa                 used as a screening tool. Eight percent of
                       partly reflects the addition of all the noxious          taxa were accepted by the model but classed
                       weeds of New Zealand to the database.                    as ‘reject’ or ‘evaluate’ by the expert averages.
                          Replicate answers to the New Zealand                  Taxa accepted by the model but rejected by
                       WRA model are less variable (CV 8Ð2%)                    experts include: Chasmanthe floribunda (Sal-
                       than the mean expert scores (CV 58Ð7%)                   isb.) N. E. Brown, Echium candicans L., Era-
                       (Table 3). The high variation in taxon scores            grostis tef Trott and Scabiosa atropurpurea
                       is explained by the variability among the                L. Taxa rated as ‘evaluate’ include Betula
                       individual respondents, even within expert               pendula Roth, Festuca rubra L., Gliricidia
                       groups. Agriculturalists gave the lowest                 sepium (Jacq.) Walp and Lathyrus ochrus L.
                       scores for weediness (0Ð438), conservationists           These taxa have several features in common.
                       the highest (0Ð673). Conservationists’ scores            They received a low number of responses
                       were also less variable than those of the                (two or three), their expert score variation
                       other groups (19Ð5% cf. 31Ð3% and 33Ð8%).                was high (data not presented), and most had
                       The outcome is that conservationists tend to             model scores on or near the thresholds. It
                       reject most taxa while agronomists accept a              is significant that no taxon with an average
                       higher proportion. The 5–6% of taxa in the               expert score of major weed was accepted by

                       Table 3. Comparisons of scores from NZWRA and the expert groups: (a) the average of all taxa scored and
                       the variation; (b) the average level of variability of scores for individual taxa from NZWRA and the experts for
                       taxa with two or more scores; (c) the outcomes for all taxa expressed as a rounded percentage

                                                   NZ Model         Mean         Botanists      Agriculturalists     Conservationists
                                                                    expert

                       (a) All taxa scores
                            N                       291            291           288                251                  291
                            Mean                      0Ð538          0Ð545         0Ð520              0Ð438                0Ð673
                            SD taxa score             0Ð204          0Ð238         0Ð307              0Ð311                0Ð258
                       (b) Individual taxa
                            N                       291            291           208                181                  224
                            Mean SD of score          0Ð041          0Ð231         0Ð115              0Ð099                0Ð087
                            CV % of score             8Ð2           58Ð7          31Ð3               33Ð8                 19Ð5
                       (c) All taxa outcomes
                            Accept                   16             17             25                35                     7
                            Evaluate                 21             20              5                 6                     4
                            Reject                   63             63             70                59                    89
A weed risk assessment model   245

                                                       80

                                                       70

                  Proportion of model outcomes which
                    differed from experts outcomes
                                                       60

                                                       50

                                                       40

                                                       30

                                                       20

                                                       10

                                                       0
                                Expert:                     No change   Evaluate   Reject    Accept    Reject   Accept   Evaluate
                                Model:                                        Accept             Evaluate            Reject

Figure 2. A comparison of the outcomes from the NZWRA model vs. the outcomes from the expert groups,
expressed as a percentage of the total outcomes for each group. , agriculturalists (251); , botanists
(288); , conservationists (291); , all (291).

the New Zealand WRA model, nor any taxon                                                       Scoring by the model and by the experts
rated as a noxious plant in New Zealand.                                                    varied according to the economic value of
   (2) A greater severity of assessment by the                                              the taxon (Figure 3). The mean expert score
model than by the experts could result in                                                   showed very little bias, with only a slight
benign taxa being rejected. The model was                                                   tendency to accept more taxa (16Ð7%) of
more cautious than the experts in 19% of                                                    intermediate economic value (
246   P. C. Pheloung et al.

                                                                                    80

                                         Difference in accepted vs. rejected (%)
                                                                                    60

                                                                                    40

                                                                                    20

                                                                                    0

                                                                                   –20

                                                                                   –40

                                                                                   –60
                                                                                         0
A weed risk assessment model   247

availability of experts may be limiting, but       Zealand context Agrostis stolonifera L., Lupi-
any smaller number of experts—especially if        nus polyphyllus and Pinus contorta. Where
they were from one interest group—would            a taxon may have significant economic ben-
be likely to give a biased answer with             efits, a further evaluation of its weediness
respect to a particular sector (Perrins et al.,    potential may include experimental stud-
1992).                                             ies (Williamson, 1993; Scott and Panetta,
   The bias displayed by different groups of       1993). Economic value should be scored in
experts differs between the two countries for      a transparently separate exercise and bal-
which we have information. Conservation-           anced against weediness in appropriate risk
ists in Britain, for example, are less inclined    assessment evaluations (Walton and Parnell,
than the average to consider a taxon to be         1996).
a weed (Perrins et al., 1992; Williamson,             We conclude that the weed risk assess-
1993), presumably because many weeds have          ment model with explicit scoring of biolog-
redeeming features such as colourful flow-         ical, ecological, and geographical attributes
ers. In contrast, New Zealand conservation-        is a useful biosecurity tool for detecting
ists are inclined to consider such taxa as         potentially invasive weeds in many areas of
weeds. Those with botanical training distin-       the world.
guish clearly between the native and alien
floras, often to the exclusion of the latter
in the compilation and collection of botani-
                                                   Acknowledgement
cal data (Raven and Engelhorn, 1971). The
interplay between these two floras is a major      This work is a largely collaborative effort to
issue on oceanic islands (Simberloff, 1995)        gather and process information on several hun-
                                                   dred plant taxa. Mark Boersma, Richard Carter,
such as New Zealand, and all alien taxa are        David Cooke, Roger Cousens, Jon Dodd, Bryan
considered weeds to the extent that they           Hacker, Surrey Jacobs, Mark Lonsdale, Michael
are perceived to impact on native ecosys-          Mulvaney, Dane Panetta, Tom Parnell, Bruce Pen-
tems, irrespective of any redeeming features       gelly, Darren Phillips, Rod Randall and Craig
                                                   Walton all contributed to the development of
(Williams and Timmins, 1990). The situation        the model. Thanks also to the anonymous New
could well be different, yet unpredictable, in     Zealand experts.
other countries. In Argentina and Chile for          The Australian Quarantine and Inspection
example, some wild adventive taxa have an          Service (AQIS) provided funding for resources
                                                   and technical assistance in Australia and the
economic value because of their potential to
                                                   Ministry of Agriculture and Fisheries in New
provide food for poor people (E. Rapoport, per-    Zealand. Final preparation of the paper was
sonal communication to P.A.W.), and there is       funded by the Foundation for Research, Science
less inclination to consider them to be weeds.     and Technology in New Zealand under contract
In contrast to these differing judgments, the      (No. 9625).
model would be less influenced by the eco-
nomic value of a taxon than any group of
experts.                                           References
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A weed risk assessment model   249

Appendix 1
250   P. C. Pheloung et al.
A weed risk assessment model   251

Appendix 2
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