Invasive alien species are widely recognised as significant drivers of global environmental change, with far reaching ecological and socio-economic impacts. The trend of continuous increases in first records, with no apparent sign of saturation, is consistent across all taxonomic groups. However, taxonomic biases exist in the extent to which invasion processes have been studied. Invasive forest pathogens have caused, and they continue to result in dramatic damage to natural forests and woody ecosystems, yet their impacts are substantially underrepresented in the invasion science literature. Conversely, most studies of forest pathogens have been undertaken in the absence of a connection to the frameworks developed and used to study biological invasions. We believe this is, in part, a consequence of the mechanistic approach of the discipline of forest pathology; one that has been inherited from the broader discipline of plant pathology. Rather than investigating the origins of, and the processes driving the arrival of invasive microorganisms, the focus of pathologists is generally to investigate specific interactions between hosts and pathogens, with an emphasis on controlling the resulting disease problems. In contrast, central to the field of invasion science, which finds its roots in ecology, is the development and testing of general concepts and frameworks. The lack of knowledge of microbial biodiversity and ecology, speciation and geographic origin present challenges in understanding invasive forest pathogens under existing frameworks, and there is a need to address this shortfall. Advances in molecular technologies such as gene and genome sequencing and metagenomics studies have increased the “visibility” of microorganisms. We consider whether these technologies are being adequately applied to address the gaps between forest pathology and invasion science. We also interrogate the extent to which the two fields stand to gain by becoming more closely linked.

coevolution, emerging, forest pathogens, invasion framework, invasive forest pathogens, microbial invasions, tree disease

Invasive alien species (IAS) present a major threat to global biodiversity, ecosystem services, economies and human health. In the present era of globalisation, and with no end in sight to the accumulation of alien species worldwide (Seebens et al. 2017), this threat continues to grow (Pyšek et al. 2020). The field of invasion science has been established to address the issues arising from the introduction of alien species and resulting biological invasions. It is grounded in invasion ecology, but has expanded to include non-biological lines of enquiry, including economics, ethics, sociology, and inter- and transdisciplinary studies (Hui and Richardson 2017). While IAS are represented by organisms across all taxonomic groups, much of the body of work in the field of invasion science has been focussed on plants and animals (Pyšek et al 2008; Wilson et al. 2020a). Many key texts fail to consider microorganisms, or if they are mentioned, they do so only briefly (e.g. Mooney et al. 2005; Lockwood et al. 2013). In contrast, there have been a number of recent reviews on microbial invasions, including invasive forest pathogens (IFPs), however, these have generally been written by microbiologists, or where dealing specifically with forest pathogens, forest pathologists (Desprez-Loustau et al. 2007; Fisher et al. 2012; Santini et al. 2013; Gladieux et al. 2015; Ghelardini et al. 2017). Nonetheless, IFPs remain generally poorly connected with invasion frameworks, limiting the application and usefulness of these concepts.

The low level of recognition regarding the importance of forest pathogens in invasion science is concerning, when considering the substantial effects of IFPs and their ability to completely alter landscapes. IFPs have been responsible for many disastrous outbreaks of diseases in commercial, natural and urban forests. Well known historical examples include chestnut blight (caused by Cryphonectria parasitica), Dutch elm disease (Ophiostoma ulmi sensu lato), Phytophthora cinnamomi in southwest Australia, and in more recent history, sudden oak death (Phytophthora ramorum) and ash dieback (Hymenoschyphus fraxineus) (e.g. Brasier and Buck 2001; Rizzo and Garbelotto 2003; Shearer et al. 2007; Pautasso et al. 2013; Rigling and Prospero 2018). These and other diseases have fundamentally altered ecosystems, with entire tree species practically eliminated from the landscape. For example, the second pandemic of Dutch elm disease is estimated to have killed between 30 and 50 million elms in the United Kingdom alone (Brasier 2008). Likewise, chestnut blight functionally removed mature American chestnut (Castanea dentata) trees from natural landscapes within 30 years of its arrival (Brasier, 2008; Loo, 2008), and sudden oak death is having a similar impact on tanoak (Notholithocarpus densiflorus) in Oregon and California (Cobb et al. 2012). Common ash (Fraxinus excelsior) is now threatened in much of its natural distribution across Europe, with mortality rates as high as 85% recorded from sites infected with H. fraxineus (Pautasso et al. 2013; Coker et al. 2019). In addition to dramatic changes in forest canopy composition, direct and indirect effects on communities, including losses of important ecosystem services, are increasingly reported following these invasions. Mitchell et al. (2014) highlighted the wide-ranging ecological implications of ash dieback resulting from H. fraxineus infection. Likewise, the invasive fungal pathogen Austropuccinia psidii (cause of myrtle rust), has significantly altered species richness and abundance in Australian rainforest communities, within a short period of time (Fernandez-Winzer et al. 2020).

Coevolution between forest pathogens and their hosts, together with pressures from competition, predation and parasitism, has contributed to the complexity and stability of natural ecosystems. Severe disease outbreaks by native pathogens under natural environmental conditions, are therefore rare (Burdon and Thrall 2009). Importantly, this coevolution between hosts and pathogens has occurred under a particular set of environmental conditions (Stenlid and Oliva 2016). Pathogens are therefore contained by geographical, environmental and evolutionary barriers, with these barriers impeding spread to novel hosts and limiting their potential to cause severe disease outbreaks. However, release from any one of these barriers may result in pathogenic behaviour, and the emergence of a new disease.

The term emerging infectious disease (EID) has its history in the medical and veterinary fields, but has also been applied to diseases of plants (Anderson et al. 2004). Of the three means by which an EID can arise, generally only one, the crossing of geographical barriers due to human mediated dispersal, is recognised as a process leading to biological invasions (Ogden et al. 2019). Within the context of forest pathology, a challenge when faced with the emergence of a new disease is determining whether this is due to the introduction of an alien species, or the consequence of a native pathogen being favoured by changing environmental conditions. The latter scenario has become increasingly common under conditions of habitat disturbance and climate change (Desprez-Loustau et al. 2006; Paap et al. 2018). The lack in knowledge of microbial biodiversity and ecology, speciation and geographic origin confound the problem of defining emerging diseases from an invasion perspective. While recent advances in molecular technologies have increased the “visibility” of microorganisms, the paucity of information remains a challenge. It is, therefore, understandable, but remains concerning, that pathogens are strikingly underrepresented in invasion science.

The clearest evidence for this underrepresentation is that among the IUCN list of 100 of the World’s Worst Invasive Alien Species (Lowe et al. 2000), only six are microorganisms. And of these, only three (Cryphonectria parasitica, Ophiostoma ulmi sensu lato and Phytophthora cinnamomi) are forest pathogens. A more recent example is that of the European Union list of alien species of Union Concern. Despite two updates, forest pathogens (and microorganisms in general) remain absent from this list (European Union 2019). Another example is South Africa’s http://invasives.org.za, which includes information about invasive plants, animals and insects, but not microorganisms, despite the presence of globally regulated species such as Austropuccinia psidii and Fusarium circinatum (Wingfield et al. 2008; Roux et al. 2013).

There have been previous calls for increased cooperation between microbiologists and invasion scientists. For example, Desprez-Loustau et al. (2007) highlighted the underrepresentation of fungi in the field of biological invasions, most likely due to a lack of scientific knowledge of fungal biodiversity and ecology. They hoped to raise awareness among mycologists and ecologists of the fungal dimension of invasions, and they identified the need to intensify research in fungal ecology to address the issue of future introductions. More recently, Wingfield et al. (2017) observed that forest pathologists have frequently undertaken epidemiological studies in the absence of any reference to, or reflection on, invasion science principles or frameworks, and called for closer collaboration between the disciplines.

This review interrogates the history of the disciplines of forest pathology and invasion science, seeking insights as to why the two fields have remained relatively unconnected. We consider several explanations for this disconnect and highlight the need to resolve these issues. By adopting the frameworks of invasion science, forest pathologists may be able to better understand how and why invasions occur. Importantly, also where, when and how invasions can be stopped or mitigated. The issue of microbial invasions has been described as one of the most pressing topics facing invasion science (Ricciardi et al. 2017; Thakur et al. 2019). Therefore, a greater inclusion of IFPs and microorganisms in general, is essential for the continued advancement of the field of invasion science. For the purpose of this review we consider IFPs in the strict sense, as a subgroup of IAS i.e. of alien origin and a consequence of human mediated dispersal.

As previously noted, when investigating a new forest disease, it is not always immediately obvious whether the outbreak results from the arrival of an alien pathogen, or is driven by environmental change. The term “emerging” does not require knowledge of the alien status of the causal agent, and encompasses the range of scenarios under which diseases of trees can develop. This includes damaging host-jumps that may occur following the establishment of an alien host. A notable example is that of Austropuccinia psidii. This rust fungus jumped from native Myrtaceae in its natural range in South America to introduced Eucalyptus (Coutinho et al. 1998; Glen et al. 2007). Disease may also emerge where an environmental barrier is lifted e.g. habitat disturbance or climate change leading to a native microorganism causing disease on a coevolved native host (Paap et al. 2017b, 2018).

Where disease establishes as a result of the introduction of an alien pathogen, this may be on either a native or alien host, or both. In some instances, this constitutes “pathogen reunion”, i.e. an alien pathogen arrives and establishes on a coevolved alien host, e.g. Teratosphaeria nubilosa, translocated with Eucalyptus trees, causing leaf blotch in plantation forests of South Africa (Hunter et al. 2008). Here, the novel environment together with monoculture plantings are conducive to disease development. An IFP may also establish on a naïve host which is alien to the invaded region e.g. Fusarium circinatum, causal agent of pine pitch canker, a devasting disease of plantation Pinus in South Africa (Wingfield et al. 2008). This fungus causes disease on Pinus spp. and with no congeners present in South Africa, has never jumped to native hosts. Lastly, there is the scenario of IFPs causing disease on native hosts, represented by some of the best-known forest diseases such as Dutch elm disease and chestnut blight. The challenge presented with regards to determining origins of disease-causing agents, as outlined in the above scenarios, has likely been a contributing factor to the historical underrepresentation of IFPs in invasion science.

Thousands of years of movement of plants, and with them the movement of microorganisms, has led to a situation where many pathogens are viewed as having cosmopolitan distributions i.e. naturalised (Santini et al. 2018). This is especially the case for agricultural crops. Historically, there has been less movement of forest trees than crop plants. But, with increasing international trade, especially the movement of plants for planting, and the growing use of planted forests, this situation is changing and resulting in increasing threats and challenges. However, the biogeography of most fungi (and microorganisms in general) remains largely unknown. The absence of such baseline data means that when a new disease emerges, it must be determined whether this is due to the arrival of an alien species, a host-jump by a native species to an alien planted host, or the result of a native pathogen that has evolved increased virulence or been favoured by changing environmental conditions. As such, assigning alien status is often challenging (Desprez-Loustau et al. 2010). For example, Diplodia sapinea, is an important pathogen of pines, causing various symptoms including shoot blight, canker, tip dieback, cone infections and blue stain (Swart and Wingfield 1991). It was first described in Scandinavia in 1822, but has a worldwide distribution and has caused disease losses in all pine plantation areas of the Southern Hemisphere, as well as in the USA, China and Europe (Desprez-Loustau et al. 2006). Some species of pine may suffer severe damage in non-native plantations, with the same species only being marginally affected in their natural range. Diplodia sapinea is present as a latent pathogen in healthy tissues (Bihon et al. 2011), with the incidence and severity of disease strongly correlated with stress factors (Swart and Wingfield 1991). It is probable that it was introduced to many regions with the movement of host material (Burgess and Wingfield 2002). Despite its global distribution and increasing importance under changing climatic conditions, and numerous population genetic studies using microsatellite markers (Brodde et al. 2019; Müller et al. 2019), the origin of D. sapinea remains unknown.

The problem of assigning alien status is exacerbated by the vast diversity of microbial taxa, their cryptic and inconspicuous nature, and our resultant poor knowledge of microbial communities. For example, the number of fungal species on earth is unknown, but estimates range from 1.5 to several million, the majority of which have not yet been described (Crous et al. 2015; Hawksworth and Lüking 2017). The lack of ‘visibility’ of microorganisms has been repeatedly provided as the reason for their absence from invasion science (Desprez-Loustau et al. 2007; Sakalidis et al. 2013; Wingfield et al. 2017; Thakur et al. 2019). Most IFPs remain undetected until visible negative impacts are observed within the recipient environment. In addition to the long lag times between arrival and detection, a diagnostics stage is required. The organism must be isolated, identified and Koch’s postulates (proof of causality) fulfilled, to definitively determine the causal agent. By the time the disease problem is noticeable, and the causal agent diagnosed, the pathogen is often well established. This complicates management, and makes IFPs very difficult to contain, let alone eradicate, particularly once they have established in natural environments. For example, the present outbreaks of Xylella fastidiosa ssp. multiplex in Europe have been much more challenging to manage in the natural Maquis environment where it has a wide host range, than X. fastidiosa ssp. pauca in commercial olive groves (CoDiRO, Olive Quick Decline Syndrome) (Landa et al. 2020). Another classic example is the impact of the ‘biological bulldozer’ P. cinnamomi in Australia. Management of this pathogen presents greater challenges in natural ecosystems (Dunstan et al. 2010) than in avocado and other crop plants (Drenth and Guest 2004; Ramírez‐Gil et al. 2017).

Microorganisms, including IFPs, have in part been overlooked in invasion science because of the vast diversity of taxa and problems relating to naming of organisms (e.g. Cowan et al. 2013; Hawksworth and Lücking 2017). For perspective, the phylogenetic “distance” amongst species of a single yeast genus, Saccharomyces, is equivalent to that between all of the known mammals and birds (Dujon 2006). This is before even considering other fungi, let alone the diversity amongst bacteria, viruses and oomycetes. It would be naïve to not acknowledge that within this vast diversity of organisms, very different biological strategies must exist for microbial invaders. This is in contrast to the move to unify into a single treatment the frameworks for studying all invasions, and it potentially dilutes our ability to address these invasions effectively (Wingfield et al. 2017). For example, Burgess and Wingfield (2017) identified seven different scenarios to account for how diseases of one genus, Eucalyptus, have moved and established within Australia and globally. Consequently, a framework for IFPs requires a nuanced approach to accommodate the overarching role of the environment in the outcome of novel interactions between hosts and pathogens.

A further confounding factor faced by forest pathologists is the challenge of accurate identification of microorganisms. Only in the last 30 years has there been a shift from the use of morphology-based to evolutionary biology-based species concepts (Harrington and Rizzo 1999; Taylor et al. 2000). Recent developments in molecular technologies and phylogenetic analysis have facilitated species identification at a much higher resolution than that based on morphology. There are now many examples of morphologically identical cryptic species that, without the application of DNA sequencing techniques, would never have been delineated as different species. For example, it was originally thought the pathogen causing cankers of Eucalyptus in South Africa belonged to the same genus as the fungus devastating chestnuts, Cryphonectria parasitica. It has since been determined, through the use of DNA-based technologies, that the disease on Eucalyptus can be caused by four different species, all belonging to the distantly related genus Chrysoporthe (Gryzenhout et al. 2004).

Name-based biosecurity will remain challenging for microorganisms. Disagreements regarding definitions of species present a confounding factor, and genetic diversity in microbe populations (with various genetic strains or mating types showing variation in virulence or host range) cannot be accounted for under a name-based approach (McTaggart et al. 2016). Rapid molecular diagnostics (Luchi et al. 2020), advances in high throughput sequencing (Hamelin and Roe 2019) and studies of microbial diversity in poorly explored ecosystems (Tedersoo et al. 2014; Desprez-Loustau et al. 2016) are areas of research with the potential to enhance our ability to better predict and prevent future invasions, and should continue to be pursued.

While there is an obvious lack of knowledge regarding the biodiversity, ecology, speciation and geographic origin of many IFPs, of all the categories of microorganisms, pathogens (including IFPs) are amongst those most widely studied. Information concerning the status (native or alien) is even less known for many other groups of microbes. The impacts of non-pathogenic microorganisms, including endophytes, saprophytes and mycorrhizal fungi, are less apparent than those of pathogens. Despite this, these microorganisms may still affect important ecosystems functions, and likely play an important role in facilitating invasions by other taxa. There has been a growing acknowledgement of the importance of studying and understanding these invasions (see Desprez-Loustau et al. 2007; Litchman 2010; Gladieux et al. 2015; Crous et al. 2016; Dickie et al. 2017; Thakur et al. 2019).

Within the discipline of invasion science, researchers studying different taxonomic groups and different environments have developed separate ways of investigating IASs. There have been efforts to reconcile these differences (see Blackburn et al. 2011; Gurevitch et al. 2011; Thomsen et al. 2011), however, forest pathologists (even more broadly microbiologists) are generally absent as authors from the literature in which the frameworks most widely used for studying invasions have been proposed. For example, the Blackburn et al. (2011) unified framework is predominantly focussed on animal and plant invasions. Wingfield et al. (2017) presented a response to this framework from a forest fungal pathogen perspective, highlighting the important issues relevant to understanding invasions by IFPs. Furthermore, how these are poorly understood and typically poorly considered in general invasion science literature. IFPs are essentially a subset of IASs (microorganisms causing disease on woody plants), and a subset of EIDs (those that establish by human mediated introduction). The terminology and frameworks of EIDs (e.g. Hatcher et al. 2012; Dunn and Hatcher 2015) and IASs (e.g. Blackburn et al. 2011) should thus both be explored to inform our understanding of the invasion process of forest pathogens. While microorganisms present a unique set of challenges with regard to being understood as IAS, acknowledging these challenges will assist in modifying frameworks to accommodate IFPs.

Studies of impacts of IFPs have often focussed on effects on other trophic levels (e.g. the impacts of Phytophthora cinnamomi on vegetation structure), as this is where negative impacts are most readily observed (Desprez-Loustau et al. 2007). The impacts of IFPs on microbial communities is a deeply understudied area. One example illustrating the potential for impacts at the same trophic level comes from studies of the invasion by the aggressive IFP Hymenoschyphus fraxineus (causal agent of ash dieback). Following invasion, H. fraxineus replaces the native decomposer H. albidus (McKinney et al. 2012). Another interesting example is the new invader Ophiostoma novo-ulmi completely replacing the less aggressive and old invader Ophiostoma ulmi in Europe (Brasier 1998). Thakur et al. (2019) proposed a “network” approach to provide a better understanding of interactions among species at different trophic levels, following establishment of alien microorganisms. Monitoring such interactions over long time scales will enhance our ability to understand the dynamics and impacts of IFPs on hosts, communities and ecosystems (Thakur et al. 2019).

Examining the long-term impacts of invasions e.g. level of impact, extent and rate of spread, may provide insights into pathogen or environment traits linked to the outcome of the invasion. A well-documented example is that of oak powdery mildew in Europe. Desprez-Loustau et al. (2019) describe the ecological and evolutionary trajectory of this pathogen complex over the course of a century. This, from its initial impact characterised by severe damage typical of pathogen invasion dynamics (with disease epidemics resulting in tree mortality), to the current equilibrium between host and pathogen, which has resulted in decreased disease severity. Desprez-Loustau et al. (2019) utilise a modelling approach to investigate the eco-evolutionary dynamics of the oak powdery mildew pathosystem, and highlight the value of such systems to explore the evolution of virulence and resistance following invasions, in the context of changing environments.

A consolidated effort is required to move from studies of interactions between individual species to those at the community level. Perhaps this can be achieved by the network approach proposed by Thakur et al. (2019), or through landscape epidemiology, a recently developed field that merges concepts of disease epidemiology with landscape ecology (Holdenrieder 2004; Lundquist and Hamelin 2005; Meentemeyer et al. 2012). This discipline links molecular and microbial observations of disease distribution with measurements of biotic and abiotic conditions, incorporating spatiotemporal complexity in epidemiological systems at the landscape level. Further, Oliva et al. (2020) proposed the development of a functional ecology approach to forest pathology, focussing on building functional trait databases to assist forest pathologists in dealing with the increasingly complex problems posed by forest pathogens under global change.

There are numerous examples of successful eradication of plant pathogens from man-made settings, particularly in controlled environments such as greenhouses (Pluess et al. 2012). However, eradication of established IFPs in natural ecosystems is incredibly challenging, and the few successful cases of IFP eradication known globally were achieved prior to spread into natural ecosystems. For example, fire blight is a destructive and highly infectious disease of apples, pears and other members of the family Rosaceae, caused by the bacterium Erwinia amylovora. In 1997, fire blight was detected in Australia, at the Royal Botanic Gardens, Melbourne (Jock et al. 2000). Following this detection, an intensive eradication and surveillance programme was undertaken, leading to successful eradication (Rodoni et al. 2006). Fusarium circinatum, a fungal pathogen that causes pitch canker disease of pine (Gordon 2006; Wingfield et al. 2008), is considered to be one of the most important pathogens affecting Pinus seedlings and mature trees in many countries. Fusarium circinatum outbreaks have been officially eradicated in France and Italy, with the success of the eradication efforts attributed to early detection, constant surveillance and control measures (Vainio et al. 2019). In each of these examples, eradication was likely only possible due to detection in the very early stages of establishment, with outbreaks confined to urban environments such as gardens, parks and nurseries. The earlier diseases are detected, and management interventions initiated, the greater the likelihood that eradication or containment measures will be successful, and at lower economic and environmental cost (Luchi et al. 2020).

The examples of the fire blight and pitch canker diseases were of pathogens well-known elsewhere in the world. Consequently, they were relatively easily recognised when they first appeared and techniques and tools for identification were well-established, facilitating rapid diagnostics. This is very different in the case of tree diseases of unknown cause such as pine wilt caused by the pine wood nematode (Bursaphelenchus xylophilus), or sudden oak death caused by P. ramorum; both took many years, in the former case decades, before the causal agents became known (Mamiya 1983; Fielding and Evans 1996; Werres et al. 2001). A recent example demonstrating the issues arising from knowledge gaps in fungal diversity, exacerbated by limited surveillance, is that of ash dieback in Europe. The first reports of dieback were from Poland in the early 1990s; however, it was not until 2006 that the cause of mortality was found to be a biotic agent, Chalara fraxinea (Pautasso et al. 2013). Initially, this anamorphic fungus was linked morphologically to a saprotrophic leaf colonising ascomycete, Hymenoschyphus albidus. This species was long known in Europe, but not as a fungus causing disease. Only five years later did molecular investigations show the teleomorph of C. fraxinea was actually a previously undescribed cryptic species (Queloz et al. 2011), the IFP H. fraxineus. This long delay in recognising the alien origin of the fungus precluded its inclusion in quarantine lists. By the time its alien status was recognised, the pathogen and resulting ash mortality had already reached many other European countries.

There are many examples of IFPs that were not known to cause disease, and others even unknown to science, prior to their establishment in a novel environment (Brasier 2008; Wingfield et al. 2015). This lack of baseline information presents major challenges with regards to predicting the next microbial invader, and constrains our ability to undertake pest risk analysis (Roy et al. 2017). Horizon scanning (systematic examination of potential threats and opportunities) presents an opportunity to prioritise actions and identify knowledge gaps (Roy et al. 2017). The IUCN Environmental Impact Classification for Alien Taxa (EICAT) is a horizon scanning tool developed as an objective framework for the assessment of all taxa (Hawkins et al. 2015; Kumschick et al. 2020). Mechanism 5 of the framework provides for classification of impact by parasites and pathogens, however, the framework has, to the best of our knowledge, not yet been applied to any IFPs, either by forest pathologists or invasion scientists.

Eschen et al. (2019) proposed the concept of ex-patria sentinel plantings (sentinel plantations), i.e. species native to a plant importing continent growing in an exporting one, monitoring these plants can lead to the identification of novel pathogen-host associations; and of in-patria sentinel plantings (sentinel nurseries), i.e. species native to the exporting continent, growing in their own continent. Identification of native pest-host associations provide information for the risk of introducing harmful organisms through the trade of plant commodities. Such efforts contribute relevant information to gap fill pest risk analysis, and can aid the development of measures to mitigate introduction risks (Britton et al. 2010; Eschen et al. 2019).

The paucity of knowledge for many aspects of microorganisms has presented challenges to understanding them as IASs, and has likely led to their underrepresentation in the invasion science literature. Advances in molecular techniques have provided powerful tools with which to study IFPs. This arises as techniques make it possible to identify pathogens more easily and accurately, greatly enhancing our knowledge of these organisms and their biogeography and ecology. Hamelin and Roe (2019) and Luchi et al. (2020) provide comprehensive reviews of advances in molecular methods and genomic tools, and their potential applications for bio-surveillance. However, forest pathologists need to be sure to ask the appropriate questions, if they are to adequately apply these tools, and this relies on an understanding of ecology (Zinger et al. 2019).

Technologies are advancing rapidly, and are commonly ahead of available knowledge of the pathogen systems being studied. Consequently, there is a risk for incorrect assumptions to be made due to poor sampling strategies (Zinger et al. 2019). Thus, forest pathologists should more actively apply ecological concepts to the pathosystems they study. High-throughput molecular techniques may contain sequencing errors, lack of replication, experimental contamination and PCR (primer) induced biases are all potential pitfalls requiring consideration (Dickie 2010; Zinger et al. 2019). There are, however, now a number of examples where newly developed molecular tools have been successfully utilised to investigate pathways of introduction and spread of IFPs (e.g. Dutech et al. 2012; Garbelotto et al. 2013; Gross et al. 2014; Landa et al. 2020).

Trees live for very long periods and can be exposed to pathogens over their lifespan. They establish complex interactions among both beneficial and detrimental microorganisms including those that make up their microbiomes (Kemler et al. 2013; Thompson et al. 2017). Therefore, a more ecological, rather than a purely mechanistic approach, needs to be applied to the study of tree pathosystems. Equally, the role of microorganisms as invasives, as well as in influencing the invasibility of environments, must become an area of research focus within invasion science. In addition to the arrival of IFPs, the health and resilience of forest ecosystems worldwide is being impacted by global change factors including climate and land use change and increased pollution. The effects of forest disturbances (wildfires, droughts, storms, pest and pathogen outbreaks) will be altered under these conditions, with the potential for increased vulnerability to IFPs. A rise in complex diseases and tree declines under global change is a major challenge facing forest pathologists (Anderson et al. 2004; Desprez-Loustau et al. 2006; Pautasso et al. 2015; Trumbore et al. 2015; Ghelardini et al. 2016).

Invasions by pathogens into forest ecosystems lead to the decline and loss of keystone species, resulting in irreversible impacts. By not using the terminology of invasion science, and by remaining disconnected from the frameworks developed and used to study biological invasions, much of the work of forest pathologists has been ignored by the wider invasion science community. Aligning terminologies and experimental designs with those utilised by invasion scientists will allow forest pathologists to reach a larger audience, in turn generating opportunities for collaboration.

For well-studied pathosystems, forest pathologists have a deep understanding of the biology of the organisms they work with. This adds layers of complexity, but also allows for more nuanced explanations. The disease triangle is a central component of plant pathology, illustrating the interactions between a host, a pathogen, and an environment – the three key aspects determining the extent to which disease will develop. This approach may also bring benefits to invasion ecology. For example, Perkins et al. (2011) proposed an adaptation in the form of the invasion triangle, incorporating the three components – the invader, site biotic characteristics, and environmental conditions of the site, as a tool for understanding and predicting why species are invasive in specific environments.

Microorganisms are gaining greater attention in the field of invasion science. As noted by Ricciardi et al. (2017), microbial ecology is becoming increasingly relevant to understanding and managing invasions. These organisms cannot be ignored. They constitute important components of all ecosystems, and are a vital part of community ecology and ecosystem functioning, as well as representing an important component of IASs. In the same way that disturbance may facilitate invasions (Wilson et al. 2020), IFPs play a considerable role in modifying ecosystems. And where a native forest species is functionally eliminated from an ecosystem following the establishment of a high impact IFP, an empty niche remains, with the potential for this to be filled by an alien plant species.

There has been a recent call for pathologists and entomologists to work together in response to the rising threat to forests posed by invasive pests and pathogens (Jactel et al. 2020). The authors argue that while traditionally considered separate disciplines, many tools and conceptual frameworks underpinning pathology and entomology can and should be shared, to meet the common goal of improved forest protection. Similarly, Nunez et al. (2020) proposed the strengthening of collaborations between ecologists, epidemiologists, sociologists, and biomedical researchers, to develop an expanded invasion science discipline (see also Hulme et al. 2020). Such an approach, embedded in the philosophy of the “One Health” concept recognising the interrelatedness of human, animal and ecosystem health (Xie et al. 2017), has the potential to make meaningful contributions to global biosecurity.

Against this background, a unified framework inclusive of IFPs should be designed. This should incorporate the basis of existing frameworks but also acknowledge and accommodate their shortfalls. This approach will facilitate the establishment of a more inclusive and a truly unified framework in the future (Wilson et al. 2020b). Clearly, the continued promotion and application of multiple disciplinary approaches to forest pathology and invasion science research is critical, if we are to adequately understand and address the complex challenges of identifying and managing forest pathogen invasions.

This paper emerged 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. We thank the three reviewers, whose suggestions have enabled us to greatly improve the originally submitted manuscript.