Research Article |
Corresponding author: Kelsey C. Brock ( kcbrock@hawaii.edu ) Academic editor: John Ross Wilson
© 2020 Kelsey C. Brock, Curtis C. Daehler.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Brock KC, Daehler CC (2020) Applying an invasion and risk framework to track non-native island floras: a case study of challenges and solutions in Hawai‘i. In: Wilson JR, Bacher S, Daehler CC, Groom QJ, Kumschick S, Lockwood JL, Robinson TB, Zengeya TA, Richardson DM. NeoBiota 62: 55-79. https://doi.org/10.3897/neobiota.62.52764
|
Islands are plant invasion hotspots, with some having more non-native than native species. Many plants are recent arrivals, leading to concerns that their full spread and impacts are not yet realised. Given that islands host extraordinary numbers of endemic and threatened species, schemes are urgently needed to track the complex, species-rich but data-poor scenarios typical of islands. This study applies the unified framework by
Biodiversity monitoring, flora, invasion framework, invasion tracking, invasive plants, naturalisation, species checklist, weed risk assessment
Oceanic islands have long been considered highly invasible, hosting higher ratios of native to non-native richness per area than climatically comparable mainland regions (
Uncertainty of impacts from numerous naturalised species, especially on remote islands with unique endemic taxa, severely complicates management strategies. Conservation decision-making is often based on the precautionary principle, a central concept which proposes that actions taken to prevent known negative consequences should also be applied to scenarios where negative consequences are possible, but uncertain (
Given that non-native species are frequently established on islands and that their behaviour over time is uncertain, two approaches are needed to provide the basis for evaluating current and future impacts: 1) tracking non-native species along the introduction-naturalisation-invasion continuum and 2) predicting the likelihood of naturalisation and invasion when field data are sparse or temporally limited (
Nearly three decades’ worth of work to characterise the invasion process worldwide and across taxa has culminated in a unified framework proposed by
The Hawaiian archipelago is an excellent model to assess methods for invasion tracking and prediction as > 55% of the total terrestrial vascular flora is comprised of naturalised species (
In this study, we assess the viability of applying the unified framework proposed by
The Bishop Museum’s checklist of naturalised plants (
We additionally reviewed naturalisation reports and herbarium specimen labels, supplementing the checklist by
For each island, we summed the number of species in each of the following two categories: “naturalised” (including pre-European introductions by Polynesians) and “questionably naturalised” for the remaining species that could not be clearly categorised after considering available data and criteria in the unified framework. We then attempted to align species in these two groups, as well as non-naturalised cultivated species in Hawai‘i, with the unified framework categories. We highlighted specific examples of challenges encountered when applying the unified framework across a flora and assessed whether it is valuable for improving non-native plant species tracking and management in Hawai‘i and elsewhere. Subsequently, we constructed a modified categorisation scheme that accommodates the data deficiencies found in Hawai‘i’s non-native flora.
To determine whether the Hawai‘i-Pacific WRA score or components of that score might be useful for inferring the status of “questionably naturalised” species, we examined the distribution of WRA scores amongst known naturalised species versus non-naturalised cultivated species. We also assessed the correlation between WRA score and number of islands where a species is known to be naturalised. The WRA scores were additionally separated into components related to likelihood of spread and potential consequences of impact, creating two independent scores for each species, following
We conducted statistical analyses with the Python library SciPy 1.0 (
Cultivated species
More than 7,300 cultivated species have been reported in Hawai‘i, although data describing the circumstances of their containment are often lacking so that they cannot be finely categorised according to the unified framework. Thus, plants that are cultivated in Hawai‘i but are not naturalised were roughly aligned to the lumped categories B1 (in captivity or quarantine) and B2 (in cultivation; Fig.
Alignment of
Questionably naturalised species
We considered 180 species to be “questionably naturalised” at the state-wide level, amounting to 342 per-island introductions being classified in this checklist category. Based on our review of Hawai‘i’s records and recommended terminology for conceptualising plant invasions (
Remnants from cultivation may arise when homesteads or forestry plots are no longer maintained, making it difficult to determine whether a species is a C1 (outside of cultivation, but not reproducing) or a mature individual of a naturalised population, especially if no historical planting data exist. An example of C1 species that may appear as naturalised in the field without prior knowledge of their planting history includes approximately 30 species of Ficus that were planted on forest reserves without the introduction of their specific pollinator wasp (
Although we currently lack data to distinguish recently introduced invaders from the rest of the “questionably naturalised” group on the checklist, we were conceptually unable to determine to which framework category these species would belong, even if they could be identified. Recently-introduced species do not appear to belong to category C3, as they do not yet form self-sustaining populations with multiple generations, but nor do they align with category C2, for which self-sustaining populations will never be formed.
Naturalised species
Of the 1,668 species in our checklist of plants growing outside of cultivation, 1,473 are considered naturalised in Hawai‘i. However, these species are not uniformly naturalised across all islands, with no island containing naturalised populations of all these species. Considering each naturalisation event separately per island, we counted 4,970 instances by summing the number of naturalisations from all islands. The checklist does not provide information on dispersal and formation of new populations, as needed to distinguish between the last four categories of the unified framework and, thus, the “naturalised” category aligns broadly with C3–E (Fig.
The Hawai‘i-Pacific WRA dataset included 828 non-naturalised and 712 naturalised species after questionably naturalised and recently-introduced non-naturalised species were removed (Fig.
Distribution of non-naturalised (yellow) and naturalised (purple) scores based on WRA (left) and likelihood-only scoring (right). Dotted lines represent the lower quartile, median and upper quartile while thick solid red lines represent the scoring threshold used by the Hawai‘i-Pacific WRA for designating species as high risk (> 6) and low risk (< 1). Dots represent scores for “Questionably Naturalised” species; grey = possibly extirpated, black = recently observed.
Only 11% of the 436 species with WRA scores less than 1 are naturalised in Hawai‘i, which is the upper threshold score used by the Hawai‘i-Pacific WRA to designate species as “Low Risk” (Fig.
The WRA score and likelihood-only score were significantly positively correlated with the number of islands on which a plant has naturalised (p < 0.001 for both). The trend was weak in both cases, although we observed a more positive correlation for the standard WRA score than the likelihood-only score (Kendall’s τb = 0.27 versus 0.14, respectively; Fig.
Sixty-three of the 180 “questionably naturalised” species state-wide have been assessed by the Hawai‘i-Pacific WRA (Table
Based on the aforementioned relationship between WRA scores and naturalisation, we find that 11 species have scores < 1 and therefore 89% of these are expected to not naturalise (Fig.
Species in the “Questionably Naturalised” checklist category alongside their likely status category derived from WRA scores and time since last observation.
Family | Species Name | WRA score | WRA rating | Likely Status* |
---|---|---|---|---|
Fabaceae | Lespedeza cuneata (Dum. Cours.) G.Don | 17 | High Risk | Extirpated |
Apiaceae | Eryngium foetidum L. | 15 | High Risk | Naturalised-Unspecified |
Asteraceae | Tithonia rotundifolia (Mill.) S.F.Blake | 15 | High Risk | Naturalised-Unspecified |
Menispermaceae | Stephania japonica (Thunb.) Miers | 13 | High Risk | Naturalised-Unspecified |
Tamaricaceae | Tamarix aphylla (L.) H.Karst. | 13 | High Risk | Naturalised-Unspecified |
Cannabaceae | Cannabis sativa subsp. indica (Lam.) E.Small & Conquist | 12 | High Risk | Naturalised-Unspecified |
Bromeliaceae | Tillandsia usneoides (L.) L. | 12 | High Risk | Naturalised-Unspecified |
Asparagaceae | Asparagus falcatus L. | 11 | High Risk | Naturalised-Unspecified |
Poaceae | Lamarckia aurea (L.) Moench | 11 | High Risk | Naturalised-Unspecified |
Poaceae | Panicum virgatum L. | 11 | High Risk | Extirpated |
Acanthaceae | Barleria lupulina Lindl. | 10 | High Risk | Naturalised-Unspecified |
Begoniaceae | Begonia nelumbiifolia Schltdl & Cham. | 10 | High Risk | Naturalised-Unspecified |
Combretaceae | Quisqualis indica L. | 10 | High Risk | Naturalised-Unspecified |
Urticaceae | Laportea aestuans (L.) Chew | 10 | High Risk | Naturalised-Unspecified |
Sapindaceae | Allophylus cobbe (L.) Raeusch. | 9 | High Risk | Naturalised-Unspecified |
Iridaceae | Sisyrinchium rosulatum E.P.Bicknell | 9 | High Risk | Extirpated |
Orchidaceae | Vanilla planifolia Jacks. | 9 | High Risk | Naturalised-Unspecified |
Rhamnaceae | Ziziphus mauritiana Lam. | 9 | High Risk | Naturalised-Unspecified |
Fabaceae | Acacia retinodes Schltdl. | 8 | High Risk | Naturalised-Unspecified |
Apocynaceae | Allamanda schottii Pohl | 8 | High Risk | Naturalised-Unspecified |
Primulaceae | Ardisia virens Kurz | 8 | High Risk | Naturalised-Unspecified |
Poaceae | Echinochloa esculenta (A.Braun) H.Scholz | 8 | High Risk | Extirpated |
Vitaceae | Tetrastigma voinieranum (Baltet) Pierre ex Gagnep. | 8 | High Risk | Naturalised-Unspecified |
Fabaceae | Acacia robusta Burch. subsp. clavigera (E.Mey.) Brenan | 7 | High Risk | Naturalised-Unspecified |
Bromeliaceae | Aechmea bracteata (Sw.) Griseb. | 7 | High Risk | Naturalised-Unspecified |
Primulaceae | Ardisia sieboldii Miq. | 7 | High Risk | Naturalised-Unspecified |
Scrophulariaceae | Buddleja paniculata Wall. | 7 | High Risk | Naturalised-Unspecified |
Poaceae | Cenchrus elegans (Hassk.) Veldk. | 7 | High Risk | Naturalised-Unspecified |
Poaceae | Melinis nerviglumis (Franch.) Zizka | 7 | High Risk | Naturalised-Unspecified |
Marcgraviaceae | Norantea guianensis (Aubl.) | 7 | High Risk | Naturalised-Unspecified |
Pinaceae | Pinus pinaster Aiton | 7 | High Risk | Naturalised-Unspecified |
Apocynaceae | Acokanthera schimperi (A.DC.) Schweinf. | 6 | Evaluate | Data Deficient |
Polygonaceae | Homalocladium platycladum (F.Muell.) L.H.Bailey | 6 | Evaluate | Data Deficient |
Fabaceae | Platymiscium stipulare Benth. | 6 | Evaluate | Data Deficient |
Lamiaceae | Clerodendrum myricoides (Hochst.) Vatke | 6 | High Risk | Data Deficient |
Bignoniaceae | Markhamia lutea (Benth.) K.Schum. | 5 | High Risk | Data Deficient |
Plantaginaceae | Maurandya antirrhiniflora Humb. & Bonpl. ex Willd. | 5 | Evaluate | Extirpated |
Aizoaceae | Mesembryanthemum cordifolium L.f. | 5 | Low Risk | Data Deficient |
Fabaceae | Parkia timoriana (DC.) Merr. | 5 | Evaluate | Data Deficient |
Asteraceae | Coreopsis tinctoria Nutt. | 4.5 | High Risk | Extirpated |
Euphorbiaceae | Synadenium grantii Hook.f. | 4 | Low Risk | Data Deficient |
Cactaceae | Peniocereus hirschtianus (K.Schum.) D.R.Hunt | 4 | Evaluate | Data Deficient |
Bignoniaceae | Radermachera sinica (Hance) Hemsl. | 4 | Evaluate | Data Deficient |
Moraceae | Antiaris toxicaria Lesch. | 3 | Evaluate | Data Deficient |
Annonaceae | Cananga odorata (Lam.) Hook.f & Thoms | 3 | Low Risk | Data Deficient |
Euphorbiaceae | Euphorbia albomarginata Torr. & A.Gray | 3 | Low Risk | Extirpated |
Pinaceae | Pinus jeffreyi A.Murray bis | 3 | Evaluate | Data Deficient |
Solanaceae | Solandra maxima (Sessé & Moç.) P.S.Green | 3 | Evaluate | Data Deficient |
Moraceae | Ficus pumila L. | 2 | Low Risk | Data Deficient |
Fabaceae | Sesbania grandiflora L. Pers. | 2 | Low Risk | Data Deficient |
Myrtaceae | Eucalyptus pulchella Desf. | 1 | Evaluate | Data Deficient |
Plantaginaceae | Linaria purpurea (L.) Mill. | 1 | High Risk | Extirpated |
Anacardiaceae | Anacardium occidentale L. | 0 | Low Risk | Not Self-Sustaining |
Araliaceae |
Plerandra elegantissima (Veitch ex Mast.) Lowry, G.M.Plunkett & Frodin |
0 | Low Risk | Not Self-Sustaining |
Podocarpaceae | Afrocarpus mannii (Hook.f.) C.N.Page | -1 | Low Risk | Not Self-Sustaining |
Marantaceae | Calathea zebrina (Hort. ex Bosse) | -1 | Low Risk | Not Self-Sustaining |
Boraginaceae | Cordia sebestena L. | -1 | Low Risk | Not Self-Sustaining |
Fabaceae | Delonix regia (Bojer ex Hook.) Raf.) | -1 | Low Risk | Not Self-Sustaining |
Ebenaceae | Diospyros blancoi A.DC. | -1 | Low Risk | Not Self-Sustaining |
Myrtaceae | Melaleuca styphelioides (Sol. ex Gaertn.) Sm. | -2 | Low Risk | Not Self-Sustaining |
Apocynaceae | Beaumontia multiflora Teijsm. & Binn. | -4 | Low Risk | Not Self-Sustaining |
Magnoliaceae | Magnolia champaca (L.) Baill. ex Pierre | -5 | Low Risk | Not Self-Sustaining |
Malvaceae | Pachira aquatica Aubl. | -6 | Low Risk | Not Self-Sustaining |
Our whole-flora analysis identified 342 cases where naturalisation status is currently uncertain, emphasising the need for effective tracking of non-native populations in the Hawaiian Islands. Hawai‘i’s current checklist (
Practical adaptation of the unified framework requiring minimal additional data collection beyond species checklists.
Categories as per |
Proposed Status Tracking Categories | Category Description | |
---|---|---|---|
A – Not transported beyond limits of native range. | Not Present | No history of introduction, or if previously introduced (e.g. for cultivation or forestry), it was never found outside of cultivation and is no longer present. | |
Not Included | No Longer Present * | Establishment Failure | Previously found outside of cultivation at one time, but was purposefully or naturally removed before self-sustaining populations formed (naturalisation). |
Extirpated | Previously forming self-sustaining populations (naturalised) at one time, but no longer existing through purposeful (eradication) or natural means. | ||
B1 (captive) – Individuals transported beyond limits of native range, and in captivity or quarantine (i.e. individuals provided with conditions suitable for them, but explicit measures of containment are in place). | Contained / Cultivated | Existing in cultivation or somehow contained. Includes accidental soil contaminants that are contained within pots or aquaria alongside purposefully cultivated species. | |
B2 (cultivated) – Individuals transported beyond limits of native range and in cultivation (i.e. individuals provided with conditions suitable for them, but explicit measures to prevent dispersal are limited at best). | |||
B3 (released) – Individuals transported beyond limits of native range, and directly released into novel environment. | Not Included | N/A | |
C0 (failing) – Individuals released into the wild (i.e. outside of captivity or cultivation) in location where introduced, but incapable of surviving for a significant period. | Re-appropriated into “Establishment Failure” Above | ||
C1 (casual) – Individuals surviving in the wild (i.e. outside of captivity or cultivation) in location where introduced, no reproduction. | Not Self-Sustaining | Plants surviving outside of cultivation with sufficient evidence suggesting that offspring, if produced, do not contribute to a self-sustaining population. | |
C2 (reproducing) – Individuals surviving in the wild in location where introduced, reproduction occurring, but population not self-sustaining. | |||
Not Included | Potentially Naturalising | Plants apparently surviving and reproducing outside of cultivation, but insufficient time has passed to determine if a self-replacing population exists. | |
C3 (established) – Individuals surviving in the wild in location where introduced, reproduction occurring and population self-sustaining. | Naturalised-Unspecified* | Naturalised Where Introduced | Plants that form self-sustaining populations without human intervention (e.g. cultivation), but have not dispersed a significant distance from their point of introduction. |
D1 (colonising) – Self-sustaining population in the wild, with individuals surviving a significant distance from the original point of introduction. | |||
D2 (invasive) – Self-sustaining population in the wild, with individuals surviving and reproducing a significant distance from the original point of introduction. | Naturalised Beyond Introduction Site | Plants that form self-sustaining populations without human intervention (e.g. cultivation) and have dispersed and established a significant distance from their point of introduction. | |
E (widespread invasive) – Fully invasive species, with individuals dispersing, surviving and reproducing at multiple sites across a greater or lesser spectrum of habitats and extent of occurrence. |
The largest obstacle that arose when aligning the species checklist to the unified framework is that the “questionably naturalised” category contains species on fundamentally different trajectories, from species that have actually died out to those that will very soon become widespread invaders (Fig.
Hawai‘i’s checklist is not unique in having questionable status categories (
Our data show that the WRA can be a useful tool for predicting naturalisation, with scores obtained from the standard WRA scoring method being more able to distinguish naturalised from non-naturalised species than scores from the likelihood questions only (Fig.
Given that WRA scores appear to be more useful than scores derived from the likelihood questions only, the scoring thresholds currently in use to assess risk of weediness by the Hawai‘i-Pacific WRA (> 6 = “High Risk”, < 1 = “Low Risk”) may be sufficient for predicting the likely status of data deficient “questionably naturalised” species (Table
By applying the Hawai‘i-Pacific WRA thresholds to “questionably naturalised” species (and accepting their associated error rates), we would infer that the 11 species (~20%) with scores less than 1 are unlikely to naturalise and instead belong to the C1 or C2 categories, while 27 (49%) species with scores greater than 6 would likely belong to, or eventually belong to, the C3 category or higher (Table
Similar to other inventories that reference the unified framework when categorising the status of non-native species (
When naming our proposed status categories in Table
We combine B1 (measures of containment in place) and B2 (containment limited) into a single category “Contained/Cultivated” because, although information about circumstances preventing dispersal can be informative for management, acquiring this data for an entire flora is difficult. Additionally, plants cultivated under strict containment measures are likely to be far less common than those with limited (or no) attempt to prevent dispersal. We include “Not Self-Sustaining” (aligning to C1–C2) and “Potentially Naturalising”, with the latter referring to recently-introduced species that appear to be in the process of naturalising (but have not yet done so), which is not included as a category in the unified framework. The adoption of the latter category provides a list of species in need of careful monitoring and alerts invasive species managers to eradication possibilities without indicating that naturalisation has occurred.
Describing the phase of naturalisation for entire floras provides a unique challenge because distribution data may be insufficient to determine whether individuals are dispersing, surviving and reproducing at locations beyond introduction sites for numerous species (
For the purposes of tracking regional floras, the A category (not transported outside native range) should be adapted to include likely invaders that have not yet arrived in the region of interest, identified via horizon scanning or risk assessment tools. Moreover, the unified framework does not categorise species that were once present in a region and are now absent, but describes the invasion continuum as a unidirectional process, with multiple avenues for invasion failure, making it unclear how species can go backwards in status. Thus, additional categories would be useful for species that were once growing outside of cultivation, but are now absent, with possible sub-categorisation according to whether a species disappeared before (C0–C2) or after naturalisation (≥ C3) if data are available (Table
We found that, although categories B3 (directly released outside of cultivation) and C0 (the same as B3 but no survival) are useful for conceptualising barriers to invasion success, they are not practically applicable as status categories (Table
Classification schemes used in species checklists, such as the three categories used in Hawai‘i’s checklist, may be converted to our system using typically available information while accommodating more detailed population data when available. To account for uncertainty when assigning categories, we suggest that low, medium and high confidence levels be attached to each status, with guidance available in Suppl. material
Assigning species’ statuses along the introduction-naturalisation-invasion continuum is an important first step for developing a biodiversity informatics (rather than species-specific) approach to managing invasions and monitoring status changes over time. Changes in spatial extent and population size could further accompany our proposed status tracking system to strengthen assessments of both impacts and control feasibility. For instance, species that are just beginning to naturalise would be categorised as “Potentially Naturalising”, a status potentially assumed to be eradicable, but feasibility may be complicated by the presence of numerous introduction sites. Future efforts towards this goal could refer to frameworks categorising commonness and changes in population size (
Our analyses allude to possible uses of the WRA beyond the novel use we describe here, as well as its original goal of identifying potential weeds. High scoring species that have failed to naturalise are priorities for monitoring and prevention (particularly multi-island introductions) and could be compared with similarly-scored species that have naturalised, possibly identifying important traits or conditions inhibiting species otherwise prone to invade. Conversely, investigating low scoring species that have naturalised could reveal possible sources of error during prediction, suggesting location-specific contexts that promote invasion (e.g. remote island ecosystems with low native diversity). While we show that WRAs can help assign naturalised statuses for data-deficient species, future studies could investigate avenues for inferring other positions along the introduction-naturalisation-invasion continuum (Suppl. material
Our attempt to apply the unified framework by
We thank reviewers Wayne Dawson, Nicol Fuentes and Annie Simpson whose comments helped improve this manuscript, as well as John Wilson for his useful suggestions during the editorial process and comments arising from a workshop on ‘Frameworks used in Invasion Science’ hosted by the DSI-NRF Centre of Excellence for Invasion Biology in Stellenbosch, South Africa, 11–13 November 2019, that was supported by the National Research Foundation of South Africa and Stellenbosch University. Additionally, we are indebted to Clyde Imada for his careful curation of Hawai‘i’s naturalised plant checklist and for sharing his thoughts on a tracking system and to Chuck Chimera for his guidance on the Hawai‘i-Pacific Weed Risk Assessment.
We thank the Hawai‘i Invasive Species Council for providing the funding support to conduct this work.
Guidance on the status confidence rating and adapting a regional checklist to track invasion statuses
Data type: table and figure