Research Article |
Corresponding author: Llewellyn C. Foxcroft ( llewellyn.foxcroft@sanparks.org ) Academic editor: Brad Murray
© 2019 Llewellyn C. Foxcroft, Dian Spear, Nicola J. van Wilgen, Melodie A. McGeoch.
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:
Foxcroft LC, Spear D, van Wilgen NJ, McGeoch MA (2019) Assessing the association between pathways of alien plant invaders and their impacts in protected areas. NeoBiota 43: 1-25. https://doi.org/10.3897/neobiota.43.29644
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Protected areas face mounting pressures, including invasion by alien plant species. Scientifically sound information is required to advise invasive species management strategies, where early detection and rapid response is particularly important. One approach to this is to determine: (i) the relative importance of pathways of invasion by which a species is introduced, (ii) the range of likely impacts associated with each species, and (iii) the relationship between pathways and impacts, to assess the relative threats posed by different pathways of alien species introductions. This assessment was performed on 139 alien plants that are invasive across the South African National Parks (19 national parks, covering ~39,000 km2), and based on available literature and expert opinion, known to have negative ecological impacts. For each species the likelihood of being introduced by each of eight pathways, and of having negative impacts in each of 13 identified impact categories, was assessed. The similarity of impact and pathway types between species was assessed using the Jaccard index and cladograms. Differences in the prevalence of impacts and pathways and relationships between these were assessed using a Chi-squared contingency and Generalised Linear Model. Nearly 80% of the species are ornamental plants and about 60% are also dispersed by rivers, highlighting the importance of managing ornamental species and surveillance along rivers in preventing future invasions. As to the impacts, ~95% of the species compete directly with native species and 70% change the physical structure of the environment. The majority of species exert multiple impacts, with 70% of species assessed having five or more impacts. There was a significant positive relationship between the number of pathways via which a species can be introduced into an area and the number of potential impacts they can have. This suggests that species using multiple pathways reach a wider range of suitable habitats, increasing the potential for different kinds of impacts over a wider area.
Global change, Invasive alien plants, Management, Non-native species, Ornamental plants, State of knowledge assessment
Protected areas represent some of the last opportunities to retain intact or at least relatively naturally functioning ecosystems with a near full complement of biological diversity (e.g.
As with all conservation practices, the control of alien plant invasions requires scientifically sound information to advise policy strategies and management approaches (
Early detection, rapid response and eradication are regarded as the first line of defence in proactively managing alien plant invasions, and are considered wholly feasible in the protected area context (
Although conceptual frameworks for prioritisation based on potential impacts are evolving (e.g. Kumschick et al. 2012,
We used a combined assessment of the impacts that an invasive species can have and the potential pathways of invasion, to develop an approach to determine species of highest concern and inform management strategies. To do this we assessed 139 alien plants across the South African National Parks estate that are considered to be transformer or potential transformer species (i.e. the most invasive species) and determined: (i) the relative importance of pathways of invasion by which a species is introduced, (ii) the range of likely impacts associated with each species, and (iii) the relationship between pathways and impacts, to assess the relative threats posed by different pathways of alien species introductions in different parks and biomes.
We used South African National Parks (SANParks) as a model system as it has 752 alien plant species recorded across 19 national parks (
Transformer species were defined as the “subset of invasive plant species that change the character, condition, form, or nature of ecosystems over a substantial area relative to the extent of that ecosystem” (
This selection process resulted in a list of 139 alien plants regarded as transformer species (see Suppl. material
The potential pathways of introduction and impacts that alien plant species may have in national parks in South Africa were determined by the authors as a group, using literature (for example
Pathway | Interpretation |
---|---|
Rivers | Unintentional: The species is introduced by rivers (e.g. seeds that float downstream into the park). |
Roads, paths, trails, tracks | Roads, paths, trails, tracks facilitate movement of the species. |
Contaminated construction material, equipment, and soils | Unintentional: The species (seeds or small plants) is spread in construction material (e.g. building sand, crushed stone, gravel, bricks, timber, thatch), equipment (pumps) and soil (excluding material on transport vehicles like bulldozers or trucks). |
Ornamental plants | The species is deliberately introduced as an ornamental plant by staff living in a park, or in landscaping in tourist facilities. Former farmsteads or abandoned structures incorporated into new parks may have ornamental plants associated with them. |
Agriculture | The species is deliberately introduced for agriculture (small scale for staff or tourist use), or was the previous landuse in areas which now, or in the future, may be incorporated into new parks. |
Clothing | Unintentional: The species is introduced on human clothing (normally seeds). |
Food or produce | Unintentional: The species is introduced along with food substances brought into the park for staff, tourists, pets and animals. Note for intentional food imports the category “Agriculture” should be used. |
Animal dispersed | Unintentional: The species is spread by animals (e.g. seed burs that get transported in animals’ coats, birds and baboons eating fruit). |
Higher category | Heading/ Impact | Interpretation |
---|---|---|
Impact on ecosystem processes and system-wide parameters | Fire properties | The species alters fire frequency, intensity or timing (of the fire regime). |
If species only occurs in forest, it is unlikely to impact on fire, because fire is not part of the system (No). | ||
If the species is only ruderal, it is not likely to impact on fire (No). | ||
Geomorphology | The species affects erosion, sedimentation processes or geo-engineers soil structure or geomorphological processes. | |
Hydrological regimes | The species affects run-off and other hydrological process like flow rate, the frequency of flood events or timing and seasonality of water flow – or could change the “pattern” – physical water course. | |
Nutrient/Mineral dynamics | The species alters the nutrient or mineral content of its environment (soil or water). This includes eutrophication. This can be marked yes in addition to the column “pH, salinity, alkalinity”. | |
Light | The species affects the amount of light filtering to layers below it (in water or sub-canopy). | |
Yes – based on the habitat the species invades, and the structure of the plant, it is likely to affect the amount of light that reaches the layer directly below it. | ||
Unknown – it is unclear from the species structure and habitat whether light is affected. | ||
No – light not affected (e.g. species low growing terrestrial species). | ||
pH, salinity, alkalinity | The species affects the pH, salinity or alkalinity of the medium in/on which it occurs. This can be marked yes in addition to the column “Nutrient/Mineral dynamics”. | |
Yes – species where this has been recorded. | ||
Unknown - alleopathic species have the potential to alter pH. | ||
No – no evidence of altering pH and unlikely to do so because of life-form (e.g. vine) or other traits. | ||
Impact on community structure | Physical structure | The species adds (or removes) a new layer to the community (e.g. tree in shrub-land, aquatic plants where no plants previously covered the water). |
Impact on community composition | Facilitation | The species facilitates the invasion of other aliens. |
Yes – must directly facilitate the invasion or dispersal of another alien species (e.g. by providing food for the species). | ||
Alteration of successional process | This species alters successional processes in areas where low level disturbance is common (e.g. flood plains). Also includes species that change the disturbance regime (e.g. creation of gaps or disturbed areas). | |
Impact on individual indigenous species | Competition | The species competes with native species. |
Hybridization | The species can hybridise with related native species. | |
Poison / allelopathy / stinging | The species may poison, sting or have allelopathic effects on other species. | |
Species interactions | Disruption of ecological interactions | The species disrupts native ecological interactions (including any mutualisms (e.g. seed dispersal), predator prey interactions, pollination, herbivory or other trophic interactions). |
Interactions include: | ||
Disruption of native seed (or fruit) dispersal due to provision of alternate food source. | ||
Effects on plant herbivore interactions by displacing food sources (e.g. unpalatable grass), breeding sites and habitat (e.g. of birds, fish and crocodiles) transformed until the species can no longer use a river. | ||
Alteration of food webs (e.g. trophic cascade). | ||
Species that only restrict movement without demonstrating disruption of an interaction were excluded. |
For each species the likelihood of being introduced by each of the eight pathways, and of having negative impacts in each of the 13 impact categories, was assessed using three primary local resources (
Three options were used to describe whether a species has the potential to result in an impact described by each of the 13 categories: (i) Yes – the species has been documented to impact in this way or there is other evidence, including authors’ specialist judgement, that the species will do so. (ii) No – the species does not impact in this manner or the impact is very unlikely and has never been documented for this species. (iii) Unknown – there is too little information to make a confident decision as to whether the species may impact in this manner, but this is not implausible given the biology of its taxonomic group. To be conservative, unknown records were treated as ‘No’ records for some analyses (detailed below). For pathways of entry, all pathways for each species could confidently be scored as ‘Yes’ or ‘No’ (i.e. no species/pathway combination was scored as ‘Unknown’). In addition to the impact and pathway data we also recorded family, life-form, park invaded (
Species were divided among authors and scored for pathways and impacts. Thereafter, a subset of species was randomly selected by category to check for consistency within, and between, categories and authors. Categories where inconsistencies were identified were systematically verified by the group for all species individually, specifically comparing entries within and between categories. The data were also checked by grouping species based on their similarity (Jaccard index) of impacts, particularly the number of impacts shared. Species that appeared to be outliers were then further examined to ensure data consistency.
Distribution of species across life-forms, families, parks, biomes, pathways and impact categories
Species were counted across life-forms, families, pathways and impact categories, to determine the status of transformer species in SANParks. For this analysis, the afore-mentioned data were transformed to binary as follows: Yes – 1, No – 0, Unknown – 0.
To determine the importance of each variable we tested for significant differences between the numbers of species counted within each category. The data were expanded into unique combinations across each category, resulting in a total of 32,718 records. The variables for impacts were maintained as Yes–No–Unknown, from which combinations including Unknown records were then excluded from the analyses. Analyses were run in R 3.0.2 (R Development Core Team 2010), using the base stats library and the chi-squared contingency table and goodness-of-fit tests.
Relationship between impact and biome, park and pathway type
A Generalised Linear Model with quasi-poisson error distribution was used to examine the relationships between the count of numbers of impacts per species, with the number of pathways by which it can invade the biomes and parks in which it occurs. The analysis was performed on all 139 species, using the glm function in R to determine the relationship of the number of impact types with the number of biomes, parks and pathways per species.
Similarity in species clusters by pathways and impacts
We assessed the occurrence of groups of species with similar pathways of introduction or similar impacts to identify groups for which particular management strategies might be effective. A statistical test for non-independence of columns, using a Spearman’s rank order correlation matrix was performed in R. The variables were weighted as follows for impacts and pathways: Yes – 1, No – 0, Unknown – 0.
Spearman rank correlations were conducted between all variables to exclude strongly correlated variables (rs > 0.60). None of the pathway variables were highly correlated (See Suppl. material
A binary species by impact matrix, and species by pathway matrix, was constructed and the Jaccard’s index calculated in Estimate S 7.51 (
The transformer plant species present in parks represent 43 families, with the three most represented families being Fabaceae (20% of all the taxa assessed), Myrtaceae (9%) and Cactaceae (8%), and all other families contributing 5% or less. There were significant differences among life forms of transformer species (χ² = 118.7626, df = 8, P < 0.001; Table
Differences in numbers of transformer plant species per impact category, pathway, biome, park and life-form. (Chi-square test results for individual models), (See Figures
Number of: | Chi-square | df | Significance |
---|---|---|---|
Species per impact category | 346.92 | 12 | P < 0.001 |
Number of species per pathway type | 193.61 | 7 | P < 0.001 |
Number of species per biome | 155.71 | 7 | P < 0.001 |
Number of species per park | 372.38 | 18 | P < 0.001 |
Number of life forms per species | 118.7626 | 8 | P < 0.001 |
There were significant differences in the number of transformer species per biome (χ² = 155.7173, df = 7, P < 0.001; Table
We found a significant difference in the numbers of species within each pathway category (χ² = 193.6135, df = 7, P < 0.001; Table
Percentage life forms and total percent species per pathway. Columns show the percent of each life form per pathway type, with the total number of species per pathway above each column. For example, 35% of the species that can be introduced as ornamental plants are trees, and trees make up 45% of the species that can be spread by rivers. Black dots show the total percent of species per pathway type. For example, 78% of the total species can be introduced as ornamental plants, 63% as rivers and 48% by animals.
For impacts, there is a significant difference in the numbers of species within each impact category (χ² = 346.9231, df = 12, P < 0.0001; Table
Percentage life forms and total percent species per impact category. Columns show the percent of life forms per each impact category, with the total number of species per impact category above each column. For example 37% of the species in the competition category are trees and 39% of the species that can impact through changes to physical structure are trees. The black dots show the percent of species in each impact category of the total species list. For example, 96% of the species could impact through direct competition, while 73% could impact through changing the physical structure.
There was no relationship between the number of impact types per species and the number of biomes (P = 0.331) or parks in which the species occurred (P = 0.131) (Table
The relationship between number of impact types per species and number of biomes invaded, parks invaded and pathways per species. (General linear model with quassi-Poisson link function).
Term | Coefficient Estimate | Std. Error | t- value | Significance |
---|---|---|---|---|
(Intercept) | 1.113 | 0.120 | 9.237 | P < 0.001 |
Number of biomes per species | -0.049 | 0.050 | -0.975 | 0.331 |
Number of parks per species | 0.040 | 0.026 | 1.520 | 0.131 |
Number of pathway types per species | 0.154 | 0.029 | 5.239 | P < 0.001 |
The pathway cluster analysis separated the species into three main groups and four sub-groups (Figure
Cladogram of plant introduction pathways, based on similarities of pathways. Mean number and type of pathways have been calculated per clade (Groups a–c). Sub-groups d include 25 species (Mean: 4.5 pathways/species; 100% contaminants; 92% rivers; 84% roads; 80% ornamentals) e include 20 species (Mean: 2.9 pathways/species; 100% roads; 85% ornamentals) f include 29 species (Mean: 2.5 pathways/species; 96% ornamentals; 90% animals) g include 48 species (Mean: 2.1 pathways/species; 91% ornamentals). The vertical black bars indicate clustering of species, whereas all other species are scattered across the groups h Acacia podalyriifolia, A. baileyana, A. elata, A. implexa, A. longifolia i Pinus pinaster, P. radiata, P. roxburghii, P. taeda, P. halepensis, P. patula.
In the cluster analysis of impact categories, three main groups were observed (Figure
Cladogram of plant impacts, based on similarities of impact types. Mean number and type of impacts have been calculated per clade (Groups a–c). Sub-groups include d 24 species (Mean: 3 impacts/species; 100% competition; physical structure 100%) e 11 species (Mean: 4.6 impacts/species; 100% competition; physical structure 100%; 82% hydrological) f 32 species (Mean: 7.9 impacts/species; competition, physical structure, light, hydrology, fire >90%) g 22 species (Mean: 6.4 impacts/species; competition, physical structure, light, hydrology >90%). The vertical black bars indicate clustering of species, whereas all other species are scattered across the groups h Cereus jamacaru, Echinopsis spachiana, Opuntia aurantiaca, O. ficus-indica, O. humifusa, Cylindropuntia imbricata, C. fulgida, Opuntia stricta i Eucalyptus cladocalyx, E. lehmannii, E. sideroxylon, E. camaldulensis, E. diversicolor j Pinus radiata, P. roxburghii, P. taeda, P. halepensis, P. patula, P. canariensis, P. pinaster k Acacia dealbata, A. mearnsii, A. melanoxylon, A. paradoxa, A. podalyriifolia, A. pycnantha, A. saligna, A. baileyana, A. cyclops, A. decurrens, A. elata, A. implexa, A. longifolia.
In contrast to the cladogram for pathways, there were four instances where related species clustered together based on the similarities of their impacts. All four Opuntia and two Cylindropuntia species (group h; Figure
The two most important pathways of invasion identified for transformer species into national parks included use as ornamental species and rivers. An additional two pathways appear to play a role as vectors, although to a lesser extent, including dispersal by animals and along roads, paths, tracks and trails. The results from the analyses all point to the high likelihood that many of the species currently in SANParks (~80%) were introduced for ornamentation. This can be illustrated in two parks, Kruger and Table Mountain. Kruger has a long history of plant introductions and the control of ornamental plants was first recommended in 1935 (
Rivers have been widely acknowledged as key dispersal vectors for invasion (
Although animals are widely considered to be major dispersers of invasive plants (e.g.
In contrast with work done in a number of studies (e.g.
Assessing the transformer species richness per park and biome provides some insights into the potential invasibility of an area. For example, Kruger includes about 350 alien plant species, which is about 100 alien plant species more than in Table Mountain (~240) (
Additional support for prioritising pathways may be gained from associations or shared traits of species that clustered together, while for some groups it is clear that prioritising one or even a few pathways will not be enough to curb spread and integrated approaches will be required. For example, all Acacia species share four of the eight pathways, with five of the 13 species sharing exactly the same pathways. These clusters together with the large body of work on Acacia (
That nearly all transformer species compete directly with native species is not an entirely unexpected result. More importantly, however, a large proportion (~70%) of the species showed the potential to impact in at least four additional ways. This most frequently included impacts such as altering hydrological regimes, changing light properties of invaded habitats, changing the physical structure of invaded areas, fire properties and succession. At a higher level in our categorisation these impacts were included as community structure, community composition and ecosystem level processes. These combined impacts can lead to cascading effects which are less easy, if at all possible, to reengineer (
Four of the most represented naturalised genera globally were recorded in our list (
By assessing each species against the eight pathway and 13 impact categories, we aimed to determine a relative risk profile for each species that could assist in determining the threat that the species posed to a protected area. The significant relationship between pathways and impacts indicates that the more pathways a species can use to disperse, the higher the likelihood that the species will become problematic.
For protected areas in our study, a species introduced by multiple pathways can be expected to be distributed over a larger area and should be given a higher priority. For example, when spreading along rivers, riparian vegetation may be displaced, causing substantial changes to the geomorphology, vegetation and community structure and composition (
Managers need reliable evidence on which to base their decisions about the location and nature of the species to be prioritised for management. These decisions often have substantial financial commitments with long-term ramifications. The ability to forecast which species, and the number or kinds of impacts they may have, can support decision making for different contexts. The correlation between the number of pathways and impacts per species highlights species of concern due to their ability to reach different habitats more widely. Implementing measures to curtail invasions along pathways that can be managed by implementing suitable policies (e.g. ornamental plants), or structured monitoring (e.g. along roadsides, trails and tracks), and combined with intensive surveillance (e.g. along rivers), will be important for a large proportion of the species.
This research was funded by the South African National Parks Park Development Funds and The Andrew W. Mellon Foundation as part of the Global Environmental Change Programme and the DST-NRF Centre for Invasion Biology, Stellenbosch University. LCF thanks South African National Parks, the DST-NRF Centre of Excellence (CIB) for Invasion Biology and Stellenbosch University, and the National Research Foundation of South Africa (project numbers IFR2010041400019 and IFR160215158271) for support. DS acknowledges the National Research Foundation for support through an Innovation Postdoctoral Research bursary. We thank Sandra MacFadyen for statistical assistance and Petr Pyšek for comments on the manuscript. We also thank the editor and reviewers for helpful comments on the manuscript.
Data for species and their pathways and impacts per category
Data type: species data
Assessing the association between pathways of alien plant invaders and their impacts in protected area
Data type: measurement