Discussion Paper |
Corresponding author: Mark R. McNeill ( mark.mcneill@agresearch.co.nz ) Academic editor: Curtis Daehler
© 2019 Sarah Mansfield, Mark R. McNeill, Lee T. Aalders, Nigel L. Bell, John M. Kean, Barbara I.P. Barratt, Kirsty Boyd-Wilson, David A.J. Teulon.
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:
Mansfield S, McNeill MR, Aalders LT, Bell NL, Kean JM, Barratt BIP, Boyd-Wilson K, Teulon DAJ (2019) The value of sentinel plants for risk assessment and surveillance to support biosecurity. NeoBiota 48: 1-24. https://doi.org/10.3897/neobiota.48.34205
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Effective surveillance for early detection of invasive alien species in natural ecosystems, or on valued plants found in modified areas, could prevent potentially devastating and costly impacts (whether environmental, economic or cultural) of new invasions on the invaded country. Surveillance technologies are often constrained by a range of factors. Determining which species present a significant risk before they reach the border is an effective strategy to minimize the possibility of invasion and/or the impact of invasion. Surveillance of sentinel plants provides an important tool to strengthen biosecurity programs assisting with i) detecting and identifying insect pests, nematodes and plant diseases that could potentially invade uncolonized countries, and ii) developing pest risk analysis profiles to eliminate or mitigate the risk of arrival. This review examines some of the challenges and opportunities provided by sentinel plant research and discusses the factors that could affect the success of their use for biosecurity risk assessment and surveillance in the New Zealand context.
Plant biosecurity, expatriate plant sentinels, IPSN, insects, plant pathogens, nematodes, pest surveillance, pest risk analysis
Global mass transportation of trade and humans is a significant driver for movement of biota into new regions and ecosystems. Some of these biota thrive in the new environments and become invasive aliens. A key aim of invasion science is to predict which species will become invasive before an invasion occurs. Accurate prediction of potential invasiveness of an organism supports the risk assessment of that organism and the development of effective, targeted biosecurity measures, including surveillance, against it. In practice, the first invasion of a new species is frequently unanticipated because the invader is not a recognized pest in its country of origin (
Since the concept was formally proposed as a means of identifying the potential risk of invasive species offshore (
The simplest definition of a sentinel plant is “a plant that is monitored for the presence of species that have the potential to cause damage”. Examples of damaging species include herbivorous insects, plant parasitic nematodes and plant pathogens, and these will hereafter be referred to collectively as “pests”. Sentinel plants may be broadly classified into two types depending on the primary reason for monitoring, i.e. to identify new pest species of risk to determine their distribution (sentinel plants for risk assessment) or to detect pest species of risk (sentinel plants for surveillance) (Figure
Different types of sentinel plants. Risk Assessment: monitoring expatriate plant A (outside its native range), can give information on exotic pests (pest X) associated with plant B that might attack Plant A should pest X become established in the home range of plant A. In this case, plant A acts as a sentinel plant for risk assessment. Sentinel plants may be in situ within existing botanic gardens and arboreta or planned plantings to record colonization and impacts. Risk assessment sites can be in the native range of plant B or regions outside plant B’s native range where pest X is invasive. Surveillance: monitoring plant A and/or plant B in the native range of plant A may give information on the arrival and spread of pest X into that area. In this case, plants A and B act as sentinel plants for surveillance. Surveillance sites may be in native habitats for plant A or at likely points of entry for pest X.
The purpose of sentinel plants for risk assessment is to detect new host associations of particular valued plants with pests with which they have not co-evolved. To do so, we monitor valued plants that have been grown outside their natural home range, i.e. expatriate plants (
Examples of sentinel plant research for risk assessment and surveillance including use of in situ plants and planned plantings.
Sentinel type | Sentinel location | Target plants | Target pests | Outcome | Reference |
Risk, in situ | Ventnor Botanic Garden, Isle of Wight | New Zealand species | Nematodes | New association found between root nematode and rare endemic species |
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Risk, in situ | Siberian arboreta and cities | European and Eurasian woody broadleaved species | Fungal pathogens | 29 new fungus-host plant associations detected, some with significant damage |
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Risk, in situ | Southern California | 39 New Zealand perennial species | Homalodisca vitripennis, Xylella fastidiosa | 28 species tested positive for X. fastidiosa; 26 out of 102 individual plants showed H. vitripennis activity |
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Risk, in situ | Christchurch | 62 exotic conifers | Exotic aphids | 13 new aphid-plant associations detected |
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Risk, planned | Riverside, California | 12 Australian tree species | H. vitripennis | 8 species supported at least one life stage; 5 species supported adults, nymphs and eggs |
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Risk, planned | Beijing and Fuyang | European trees: 5 broadleaves, 2 conifers | Foliage-feeding insects | > 100 morphospecies including larvae of at least 6 species detected on trees |
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Risk, planned | Fuyang | 3 Quercus species | Fungal pathogens | Four taxa associated with disease symptoms identified |
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Risk, planned | Beijing and Fuyang | 5 ornamental woody plants from Asia | Insects | > 90 new insect-plant associations detected |
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Surveillance, in situ | Palm House, Kew Gardens | 181 species | Scirtothrips dorsalis | 73 species had S. dorsalis adults, 44 species also had juveniles |
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Surveillance, in situ | New Zealand wide | Various native and exotic spp. | Exotic pests | 22 exotic species detected 2013–2018 |
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An example of this is New Zealand native plants growing in botanic gardens or arboreta in other countries which provide the opportunity to identify species utilizing those plants and which could become pests if they established themselves in New Zealand (
While established expatriate sentinel plants can be used for monitoring (
The concept of growing plant species in exotic environments to detect known associate pests of those plant species, or similarly native species in their home range has been described as “ex-patria” and “in-patria” plantings respectively (
Invasion pathways into New Zealand in relation to the invasive species’ country of origin. In a primary invasion, an invader may enter New Zealand directly from its native range, while in a secondary invasion pathway, the pest colonizes one (or more) countries outside its native range through bridgehead invasion, before reaching New Zealand.
Sentinel plants used for surveillance assume that a risk of pest invasion has been identified and possible entry and dispersal pathways determined. In this case, surveillance sites can be selected based on proximity to trade and tourism entry points, climate matching and other relevant criteria such as potential host-plant associations, historical interception records and logistics of accessing sites. Once the risk of a new host association has been identified, then sentinel plants for surveillance may be used to detect arrival or range expansion of particular pests (Table
An obvious application of sentinel plants for surveillance is for detecting the invasion of new species into an area. For example, New Zealand’s Ministry for Primary Industries (MPI) High Risk Site Surveillance System (HRSS), oversees the monitoring of arborescent plants near likely points of pest entry, such as airports, seaports and container devanning sites (
The efficacy of a biosecurity program that uses sentinel plants, either for risk assessment or surveillance will be affected by several factors and these need to be considered when designing the program. These include: i) is there a scientific aim for the program; ii) the selection of sentinel plant species; iii) attributes of the potential invasive species/taxa of interest; iv) commonalities and differences between geographic origin/location of the sentinel plants and invaders, including habitat and environmental matches; v) appropriate technologies for detection of invasive species; vi) appropriate frequency of monitoring; and vii) effective communication of results to groups of interest. These factors may interact with each other. For example, the invasive species/taxa of interest will determine the most appropriate sampling methods for detection. Consideration of such factors, and their interactions, in the design phase of the biosecurity program will facilitate its successful implementation and ensure it achieves its purpose.
A purely protective biosecurity program does not require a scientific goal but there are considerable benefits for such an inclusion, not least being the validation of the program and possible improvements to future programs based on the success, or otherwise, of the current program. Sentinel plants for risk assessment and surveillance can be used not only for the primary purpose of identifying and detecting new potential invaders (e.g.
If the program’s sole purpose is identification of potential new invaders, it is more common to monitor selected plants in situ from pre-existing botanic gardens or arboreta. The International Plant Sentinel Network (IPSN) was established to co-ordinate sentinel plant monitoring and data sharing across botanic gardens in multiple countries (described by
Sentinel plant programs choose plants of significant value to humans. That value may be environmental (endangered species, species that perform a valued non-economic service, or species that support key ecosystems); economic (plants grown for food and fibre), or cultural/aesthetic. New Zealand’s long geographic isolation has led to a high level of endemism amongst its flora (
In New Zealand, the cultural/aesthetic aspect includes a wide range of significant species of value to Māori (
When plants growing in situ are used as sentinels in programs with a research component, availability is an important criterion and can override other factors. If a sentinel plant program intends to test ecological theories about invasive species, as opposed to the empirical risk assessment described above, then the history of different taxa, or individual plants, may affect the results. For example, the rate of accumulation of new species has differed between plant taxa in Europe (
Expatriate sentinel plant programs may target particular pest species (e.g. glassy-winged sharpshooter, Homalodisca vitripennis (Germar),
If the pest of interest has invaded elsewhere, the impact of these invasions on plants in those locations may indicate vulnerable species that should be considered for inclusion in sentinel plant programs for surveillance in the country at risk of invasion. For example, studies of glassy-winged sharpshooter, H. vitripennis, on Australian and New Zealand native plant species growing in California, provided information on new insect-plant host associations of biosecurity concern to both countries (
In some cases, investigations are looking for the unknown – apparently harmless species that change hosts or that escape natural enemies in their native range to become significant pests in an invaded country. For example, the emerald ash borer, Agrilus planipennis Fairmaire is not a pest within its native range in Asia but became a significant pest after invading North America (
A possible clue to identifying a non-pest species that has the potential to become a significant risk in another country may be via examination of herbivorous invertebrate communities associated with plants native to that country and that are closely related to sentinel plant species of interest. Any herbivores associated with these closely related plant species, particularly where impacts are severe, should be investigated as risks and potential invaders if pathways, climate suitability, and hitchhiker potential enable long distance dispersal, survival and establishment of that species (e.g.
Insect pests and plant diseases generally have received the most attention within the sentinel plant context, in part because the signs and symptoms of damage are generally visible to both specialist researchers and casual observers. By comparison, indications of the presence of nematodes tend to be more cryptic, and their impacts overlooked. Of the nematode taxa, plant parasitic nematodes (PPN) provide the most concern to biosecurity officials and growers, because their effects on plant growth and production can be significant. PPN are small (generally less than 1 mm in length) and found mostly in and around plant roots, while a small number of important genera infect leaves and stems. Plant symptoms of nematode infection can often be mistaken for nutrient deficiency or attributed to other pests or diseases. Due to their small size, identification requires access to specialist equipment and expertise. Few species of PPN are currently recognized as invasive but this is undoubtedly because of insufficient investigation and recognition of their presence (
Central to the concept of sentinel plants is the question of geographic origins of potential invaders and selected sentinel plant species (Figure
Floral similarities between countries also facilitate invasion by “new” pests. For New Zealand, sentinel pōhutukawa plants for risk assessment that are grown in countries with substantial Myrtaceae flora (e.g. Australia, Pacific Islands, South America) allow the identification of new potential invaders that may enter New Zealand directly (Figure
As noted above, it is possible for potential invaders to switch hosts to unrelated plant species; this type of host shift is very difficult to predict. From New Zealand’s perspective, an unexpected host shift may be detected after a ‘bridgehead’ invasion (Figure
The choice of sampling methods used in a sentinel plant program, for either risk assessment or surveillance, should be determined by what is known about the potential invader(s). If the target is a known species or taxon, then specific sampling techniques may be able to be adopted to maximise the probability of pest detection, e.g.
A key step when dealing with unknown invaders is correct taxonomic identification based on morphological and/or molecular characteristics, at least to genus and preferably to species level (
Sentinel plants may be subject to a regular monitoring schedule or checks may be conducted intermittently, as time permits. In general, a regular and frequent schedule is likely to be more useful for biosecurity purposes, particularly when consistent sampling methods are used at each check (e.g. detection of Thaumastocoris peregrinus in New Zealand,
An easily overlooked, but essential, aspect of sentinel plant research is the need to communicate results to the relevant biosecurity authorities and potentially affected stakeholders. These need early warning of both potential and actual new invaders, particularly if significant impacts are expected, so that mitigation can be planned and implemented to minimise pest impact. While publication in peer-reviewed journals is critical for scientific veracity and quality, this does not obviate the need for wider communication of new research findings. Communication must be timely and relevant with the information presented in a way that non-specialists in government and industry organisations can understand, yet it must also acknowledge the inevitable uncertainties in research findings.
In New Zealand’s case, rapid communication is best directed to government agencies such as the Ministry for Primary Industries (MPI) (as New Zealand’s National Plant Protection Organisation) and the Department of Conservation (DOC) as well as the appropriate Crown Research Institutes, depending on the sectors or environments most likely to be affected by the new invader. The most affected sectors will also determine which industry stakeholders should be involved with a risk assessment or an incursion response. In general, early communication with authorities and stakeholders informs pest risk and pathway analyses, as well as raising awareness and vigilance amongst the affected groups. As part of this process, there needs to be effective channels to share feedback from government authorities and stakeholder organizations with research providers. This is essential to confirm that useful information has been received by all parties, to share information, and to support co-development of important pest risk and pathway analyses.
Most research using sentinel plants, whether to detect new invasions or assess risks, involves perennial woody tree species. Plants of environmental and cultural value are more likely to be monitored through botanic gardens and arboreta, which presumably reflects the availability of such species in alien environments. Annual plants, short-lived perennials, and grasses are under-represented in the literature, yet there are valued species within these groups e.g. snow tussock (Chionochloa rigida) is an iconic New Zealand species. It is not clear if these under-represented groups are less common in parks and botanic gardens and therefore simply unavailable for monitoring, or if these groups are actively excluded from sentinel plant programs either because the value of this approach is not recognized for such plants or research funding is unavailable.
The other significant group rarely included in sentinel plant programs for risk assessment are plants of economic importance. For example, many non-woody crop plants are grown outside of their native range where they are at risk of attack by local polyphagous pests (
Outside of programs focused strictly on biosecurity, but in many cases aligned to real or potential biosecurity breaches, sentinel plant programs for risk assessment can be used to develop pest control strategies, particularly where biological control of invasive plant species is considered. Sentinel plants may be used to identify potential biological control agents and/or to assess their efficacy (e.g.
Ideally, both in situ plants (in botanic gardens and arboreta) and planned plantings (research plantings) should be incorporated in target sentinel plant programs, because no single approach can cover all potential invaders, particularly plant pathogens (
Regular monitoring of established specimens of plant species that are valuable to New Zealand, particularly expatriate specimens of endemic species, is the most practical strategy because it contributes information about recognized pests in their country of origin, new pests that emerge through bridgehead invasions into other countries, and potential new invasions into New Zealand (Figure
Strategies for use of sentinel plants to enhance New Zealand’s (NZ) biosecurity.
Geographic location | In situ sentinel plants | Planned sentinel plantings |
Invader’s country of origin (sentinel plants for risk assessment) | Monitor 1) any plants damaged in country of origin that are valuable to NZ and 2) any valuable NZ species that are taxonomic relatives of plants damaged in country of origin. | Establish planned plantings of any potentially vulnerable species not already represented among in situ plants in the invader’s native geographic range. |
Other countries subject to a bridgehead invasion | Monitor 1) any plants damaged in the invaded range that are valuable to NZ and 2) any valuable NZ species that are taxonomic relatives of plants damaged in the invaded range. If the invader’s country of origin can be identified, follow recommended sentinel plant strategy within the invader’s native geographic range. | Establish planned plantings of any potentially vulnerable species not already represented among in situ plants in the invaded range and, if possible, the invader’s native geographic range. |
New Zealand (sentinel plants for surveillance) | Monitor 1) local specimens of any plant species damaged in the invader’s country of origin (if known), 2) local specimens of any species valuable to NZ that are damaged in other invaded countries, and 3) any valuable NZ species that are taxonomic relatives of plants that are either damaged in the invader’s country of origin (if known) or damaged in other invaded countries. Monitoring should include air and sea ports, botanical gardens, forestry plantations, home gardens etc., whose geographic location increases their likelihood of exposure to invaders. | Planned plantings may be less relevant in this context because rapid detection of a new invasion is best achieved through in situ plants occurring across a wider geographic landscape. At sites where biosecurity scientists can have input into long-term landscaping choices, it may be feasible to plant valuable species that augment in situ plants. |
Planned planting programs of sentinel plants for risk assessment are best used to address specific questions that cannot be answered using in situ plants in the invader’s country of origin and/or its invaded range or where robust data collection is required. The cost and logistics of sentinel plant programs will increase with complexity and inevitably there will be trade-offs between optimal data collection and manageability. However, such programs will be particularly important for plant taxa that are poorly represented in botanic gardens and arboreta, such as grasses, annuals and short-lived perennials and may also be justified in the case of economic crops. For example, ryegrasses (Lolium spp.) are New Zealand’s most valuable crop (
Challenges to implementation of planned sentinel plant programs include freedom to carry out research in overseas jurisdictions, remote management and monitoring of overseas field trials and data ownership as well as biosecurity, commercial and cultural considerations. Another significant challenge is that an ‘absence of evidence is not evidence of absence’, i.e., sentinel plants can provide positive evidence of a pest-plant interaction, but the lack of such interaction does not prove conclusively that the interaction will never occur. This is particularly important for plant pathogens, where the conditions supporting infection may be highly specific (
Over and above these is the challenge of identifying the specimens collected in the studies, especially if they are undescribed, and the cost of carrying out the research. However, this approach may provide a better platform to assess impacts from invaders, as it allows for experimental replication, site selection, and may give some control over the degree of exposure to the invasive species. Many crop and pasture species are grown worldwide so sentinel plant projects with such species may be easier to implement than for native or endemic species, due to fewer biosecurity and cultural concerns around planned planting of the chosen species at the experiment sites. For these economically important species, the cost of sentinel plant programs that enable pre-emptive mitigation of potential pest impact would undoubtedly result in a positive cost benefit analysis, where the cost of investigation is far exceeded by the economic savings gained from preventing an invasion.
As financial and logistic constraints are likely to limit the scope of sentinel plant programs, so collaboration and information sharing between countries is essential, as the IPSN demonstrates. Regular monitoring of valuable New Zealand species that are present in botanic gardens and arboreta is an important strategy for New Zealand’s biosecurity; but particularly for commercial species and those with high cultural value, there is also a case for planned sentinel plant programs whereby these species are grown overseas and regularly monitored for evidence of colonization by exotic invertebrate pests and plant pathogens.
Botanic gardens can act as early warnings of exotic pests and diseases as well as increasing knowledge of exotic species presence/absence (
Expatriate sentinel plant research using deliberate plantings has shown the potential to identify new insect-plant host associations, while also demonstrating that there can be significant challenges to identifying key phytophagous taxa when taxonomic databases or resources are lacking (
As a working sentinel plants framework,
As a biosecurity pre-border strategy, expatriate sentinel plants provide the advantage of early warning of pest and disease attack, but selection criteria and desired outcomes need to be carefully planned as does a mechanism to prioritize risk. For New Zealand, an area that is lacking from the sentinel plant approach to border biosecurity is their use for commercial crops, particularly for the agricultural sector. The sentinel plant approach can be a component of New Zealand’s biosecurity platform, but the global examples presented in this review demonstrate its potential to contribute to New Zealand’s biosecurity preparedness. Continued monitoring of plants near likely invasion sites within New Zealand through the HRSS program (
MRM and SM carried out the literature search and wrote the paper, BIPB contributed to writing of the manuscript, and along with LA and NB contributed to collection of specimens and interpretation of data for the project; DT, KBW and JK contributed to the development of the project and review.
The research was funded by AgResearch and The New Zealand Institute for Plant & Food Research Ltd via the Better Border Biosecurity research collaboration (www.b3nz.org) with the support of the Ministry for Primary Industries (MPI) and Department of Conservation (DOC). We would like to acknowledge the contribution of David Havell (DOC), Quentin Paynter and Ines Schönberger (Manaaki Whenua – Landcare Research), Peter Henan and Brian Patrick (Wildland Consultants), Colin Ferguson and Nicky Richards (AgResearch Ltd.) for useful comments, suggestions and references during the writing of this manuscript, Karen Cousins (AgResearch Ltd.) for assistance in the literature review and Alice Baillie (AgResearch Ltd.) for the figure graphics. We also thank anonymous referees for helpful suggestions and comments during journal review.