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Seedling height (log e (x + 1), cm) (a,b) and number of leaves (log e (x)) (c,d) through time for Melaleuca quinquenervia (light grey, square), Leptospermum laevigatum (dark grey, triangle) and Baeckea linifolia (black, circle) seedlings in control (dashed lines, open symbols) and Puccinia psidii treatment conditions (solid black lines and symbols). Graphs (a) and (c) show results for seedlings grown individually (Experiment 1), graphs (b) and (d) show results for seedlings grown in mixed-species assemblages (Experiment 2). Vertical lines represent AE 1 SE.
Source publication
Exotic fungal pathogens can substantially affect individuals and populations of susceptible native plant species, potentially resulting in changes in community structure and composition. Austropuccinia psidii (myrtle rust) is a pathogenic fungus native to South America that affects species in the plant family Myrtaceae. The pathogen was introduced...
Contexts in source publication
Context 1
... difference among the species in the effect of A. psidii on seedling height through time was nonsignificant (Interaction Treatment*Species*Week; v 2 (2) = 5.003; P = 0.0819; Table 2; Fig. 2a). However, species that were treated with A. psidii were shorter towards the end of the experiment compared to the control, with the difference in seedling height between control and treated seedlings increasing through time (Interaction Treatment*Week; v 2 (1) = 8.627; P = 0.003). At the end of the experiment, average height of L. ...
Context 2
... effect of A. psidii treatment on total number of leaves depended on the combination of the identities of the species and time (Interaction Treatment*Species*Week; v 2 (2) = 6.673; P = 0.036; Table 2; Fig. 2c). Melaleuca quinquenervia and L. laevigatum had less leaves in the A. psidii treatment compared with the control through time. However, M. quinquenervia showed a greater difference between control and A. psidii treatment as time progressed, with a 29% reduction by the end of the experiment for this species compared to 20% for L. ...
Context 3
... were found in the effect of the A. psidii treatment on seedling height for the three species through time (Interaction Treatment*Species*Week; v 2 (2) = 11.351; P = 0.003; Fig. 2b). Leptospermum laevigatum had the tallest seedlings in the first weeks of the experiment, although towards the end of the experiment its growth declined in the A. psidii treatment resulting in 15% smaller seedlings compared to the control. The impact of A. psidii treatment on M. quinquenervia was substantial, with the difference in ...
Context 4
... effect of Austropuccinia psidii treatment on the number of leaves in mixed species assemblages was determined by the combination of species identity and time (Interaction Treatment*Species*Week; v 2 (2) = 6.552; P = 0.038; Fig. 2d). For all three species the number of leaves in the control treatment Fig. 3. Results of experimental treatments on plant growth for the three study species. (a) Total biomass (log e (x + 1), (b) root biomass (log e (x + 1), (c, g) shoot biomass (log e (x + 1), (d) leaf mass fraction, (e) stem mass fraction and (f) root mass fraction ...
Context 5
... difference among the species in the effect of A. psidii on seedling height through time was non- significant (Interaction Treatment*Species*Week; v 2 (2) = 5.003; P = 0.0819; Table 2; Fig. 2a). However, species that were treated with A. psidii were shorter towards the end of the experiment compared to the control, with the difference in seedling height between control and treated seedlings increasing through time (Interaction Treatment*Week; v 2 (1) = 8.627; P = 0.003). At the end of the experi- ment, average height of L. ...
Context 6
... did not present symptoms of infection, final seedling height was reduced by 30% in the A. psidii treatment in comparison with the control. The effect of A. psidii treatment on total number of leaves depended on the combination of the identi- ties of the species and time (Interaction Treat- ment*Species*Week; v 2 (2) = 6.673; P = 0.036; Table 2; Fig. 2c). Melaleuca quinquenervia and L. lae- vigatum had less leaves in the A. psidii treatment compared with the control through time. However, M. quinquenervia showed a greater difference between control and A. psidii treatment as time progressed, with a 29% reduction by the end of the experiment for this species compared to 20% for L. ...
Context 7
... were found in the effect of the A. psidii treatment on seedling height for the three species through time (Interaction Treatment*Species*Week; v 2 (2) = 11.351; P = 0.003; Fig. 2b). Leptospermum laevigatum had the tallest seedlings in the first weeks of the experiment, although towards the end of the experiment its growth declined in the A. psidii treatment resulting in 15% smaller seedlings com- pared to the control. The impact of A. psidii treat- ment on M. quinquenervia was substantial, with the difference in ...
Context 8
... effect of Austropuccinia psidii treatment on the number of leaves in mixed species assemblages was determined by the combination of species identity and time (Interaction Treatment*Species*Week; v 2 (2) = 6.552; P = 0.038; Fig. 2d). For all three spe- cies the number of leaves in the control treatment Fig. 3. Results of experimental treatments on plant growth for the three study species. (a) Total biomass (log e (x + 1), (b) root biomass (log e (x + 1), (c, g) shoot biomass (log e (x + 1), (d) leaf mass fraction, (e) stem mass fraction and (f) root mass fraction ...
Citations
... In Australia, Myrtaceae is the most diverse plant family, harbouring c. 1,600 species (Glen et al., 2007), over a quarter of the world's total of c. 5,500 species (Wilson, 2011). They are common and often dominant in rainforests, Eucalyptus forests (Tng et al., 2013), shrublands (Wills & Read, 2017), and wetlands (Fernandez Winzer et al., 2018). In contrast, in Hawaiʻi, Myrtaceae diversity is low (eight native species) and a single tree species (Metrosideros polymorpha) is the most abundant in forest ecosystems (Imada, 2012;Barton et al., 2021). ...
Aims
The Myrtaceae is a woody family that plays an important role in forest ecosystems globally. The recent spread of myrtle rust, caused by a fungal pathogen (Austropuccinia psidii), from its native South America into New Zealand (NZ) highlights the need to quantify the ecological importance of Myrtaceae in NZ woody ecosystems.
Location
New Zealand.
Methods
Using NZ nationwide forest and shrubland inventory data, collected from 2009 to 2014, we quantified the ecological importance of Myrtaceae based on its richness and abundance relative to co-occurring woody families. We then explored how climate and forest stand structure affect Myrtaceae importance in general and by tribe and growth form. Finally, we compared functional traits associated with plant growth and reproductive strategies with other dominant woody families and determined Myrtaceae’s contributions to community-weighted mean (CWM) trait values.
Results
Myrtaceae occurred in 74% of the study plots and its importance value was the second highest across the woody families. It was the only one in which climbers substantially contributed to the importance value (17%). Greater Myrtaceae importance values were associated with warmer and more mesic climates and early forest successional stages. Climate associations were similar within tribes and growth forms, whereas forest structure effects varied. Myrtaceae was functionally distinct from most co-occurring woody families. Contributions to CWM wood density, maximum height, and specific leaf area values were significantly greater than expected from its importance value.
Conclusions
Myrtaceae is the second-most ecologically important woody family in NZ woody ecosystems. The family has a distinctive functional trait spectrum associated with high wood density and tall stature, ensuring large and enduring carbon stocks. There will potentially be large and deleterious outcomes in forest ecosystems if taxon-specific pathogens, such as Austropuccinia psidii, spread and significantly reduce Myrtaceae importance.
... This rust is an obligate biotoph, and it takes nutrients from the host as a source of carbon to grow (Chock 2020). Austropuccinia psidii infection can reduce the growth of the plant and defoliation (Winzer et al. 2018), blighting on the stem, and tree dieback (Pegg et al. 2017), reduces fruit quality, thereby causing premature dropping of fruits and seedling death (Sutherland et al. 2020). Its infection symptoms on mature leaves are necrotic spots and a few uredinia (Beresford et al. 2019). ...
Faradilla FA, Prihatini I, Suranto, Susilowati A. 2022. Genetic variation of Austropuccinia psidii in some species of Myrtaceae as host plants in Java, Indonesia based on simple sequence repeats (SSR) markers. Biodiversitas 23: 256-263. Austropuccinia psidii is pathogenic rust with a wide host and is considered a biosecurity threat to the Myrtaceae family in many countries. The genetic variation of this rust in Java, Indonesia is poorly reported. Therefore, this study aimed to determine the genetic variation among A. psidii from different Myrtaceae hosts, namely Syzygium polyanthum, S. myrtifolium, and Melaleuca cajuputi from three different locations in Java using seven simple sequence repeats (SSR) markers. Data were collected from 28 A. psidiisamples from three different hosts and locations in Java. The genetic variations of A. psidii were found in six isolates in locus USYD_Pp168, PpSSR161, and PpSSR195*. The results showed that the expected heterozygosity value among 12 isolates of A. psidii is 0.312. The dendrogram illustrates two clusters constructed with cluster I consisting of subcluster IA (S1, S3, S4, S5, K1, K2, K3, K4, and P1) and IB (P2); and cluster II consists of isolates S2 and S6. Principal Coordinate Analysis (PCoA) was used to demonstrate the similarity and dissimilarity among isolates based on microsatellite sites. Axis 1 and 2 explained 87.7 % of the total variations and sep a rated isolate S1, S2, S3, S4, S6 from other isolates, and grouping the rest of isolates together. The dendrogram and PCo analysis demonstrated A. psidii isolates tend to have close genetic similarity based on their host.
... The invasive potential of A. psidii is evident by its successful spread to 27 countries across several continents to date (see Carnegie and Pegg 2018, Table 1 for a complete list). While most fungal pathogens infect just a handful of species, A. psidii is known to infect 539 species worldwide from 86 different genera (Giblin and Carnegie 2014a;Makinson 2018a;Soewarto et al. 2018;Fernandez Winzer et al. 2018b;Berthon et al. 2019). In Australia alone, there are 393 native species from 52 genera known to be susceptible through susceptibility tests and/or field observations (Giblin and Carnegie 2014b;Fernandez Winzer et al. 2018b;Makinson 2018a;Berthon et al. 2019). ...
... While most fungal pathogens infect just a handful of species, A. psidii is known to infect 539 species worldwide from 86 different genera (Giblin and Carnegie 2014a;Makinson 2018a;Soewarto et al. 2018;Fernandez Winzer et al. 2018b;Berthon et al. 2019). In Australia alone, there are 393 native species from 52 genera known to be susceptible through susceptibility tests and/or field observations (Giblin and Carnegie 2014b;Fernandez Winzer et al. 2018b;Makinson 2018a;Berthon et al. 2019). It is vital that the effects of A. psidii on Australian Myrtaceae species are well understood as Australia is home to 40% of the global Myrtaceae species (2250) and 60% of the Myrtaceae genera (80) (Grattapaglia et al. 2012;Makinson 2014). ...
... The successful use of fungicide in controlling A. psidii in nurseries and forestry plantations suggests the possibility of targeted fungicide treatment as a potential management tool for A. psidii-susceptible species. However, this would be prohibitively costly in non-commercial natural environments (Ferreira 1983;Glen et al. 2007;Fernandez Winzer et al. 2018b). We suggest that seed and tissue collection is critical for the conservation of these species, and in addition conservation efforts could focus on screening for A. psidii resistance genes (Howard et al. 2015). ...
In 2010, the invasive pathogen Austropuccinia psidii was detected in Australia, posing a threat to vegetation communities containing susceptible Myrtaceae species. A large-scale field experiment tested the direct and indirect effects resulting from the infection of two highly susceptible rainforest species, Rhodamnia rubescens and Rhodomyrtus psidioides. Community-level impacts were assessed at three sites per study species in New South Wales, Australia. For R. rubescens, 20 plots containing an adult tree each were established per site. Each plot was designated one of four treatments: fungicide spray of the understorey only, canopy only, both or none (control). For R. psidioides, 10 plots containing only seedlings were established per site, with each plot designated to one of two treatments: fungicide spray or no spray (control). Richness and abundance of co-occurring understorey species were assessed every 4 months for a 24-month period, and changes in canopy transparency were assessed for R. rubescens. The R. rubescens control canopy plots were found to have greater canopy transparency (direct effect) which caused a reduction in the understorey richness and total abundance (indirect effects). For treated canopy plots, richness was similar but total abundance increased in fungicide treated understorey plots, suggesting a direct effect of the pathogen on understorey species. Understorey plots treated with fungicide had significantly greater abundance of R. rubescens and R. psidioides seedlings compared to control plots. This study shows that in a short time period, infection by an invasive fungal pathogen has resulted in changes in species richness and abundance in Australian rainforest communities.
... The ecological impacts of A. psidii are alarming, with the disease causing significant damage and tree mortality (Carnegie et al., 2016;Pegg et al., 2017). The results demonstrated a growth rate reduction in plants severely infected by A. psidii, compared to resistant and control plants, a similar response to that was previously reported for Melaleuca quinquenervia, Leptospermum laevigatum, Baeckea linifolia (Winzer et al., 2018) and Eucalyptus globulus (Balmelli et al., 2013). Quambalaria pitereka also reduces growth with increasing severity of infection (Johnson et al., 2009;Lan et al., 2011). ...
Eucalypt forests and industrial plantations are threatened by fungal pathogen outbreaks that compromise timber and non-timber products and tree survival. Understanding host-pathogen interactions may contribute to the development of disease management strategies and the selection of resistant genotypes. Resistant and susceptible plants respond differently to disease infection, presenting variations of phenotypic traits, such as leaf physical and chemical parameters that may influence host-pathogen interactions. This study evaluated physical and chemical responses of Corymbia citriodora subsp. variegata to two fungal pathogens, Quambalaria pitereka (a co-evolved pathogen) and Austropuccinia psidii (an established exotic pathogen), using severity of infection as an indicator of plant resistance/susceptibility. Our primary aim was to quantify differential plant responses between uninoculated (controls), susceptible (severely infected) and resistant plants for each pathogen. Plant growth rate, leaf toughness and foliar secondary metabolite profiles of control, resistant and susceptible plants were compared 14 days after pathogen inoculations. Leaf secondary metabolite profiles were analysed from uninfected regrowth of the same plants 90 days after inoculation. The results indicated that only susceptible plants elicited responses to pathogen damage. Susceptible plants infected by Q. pitereka had greater leaf toughness, and susceptible plants infected by A. psidii had reduced growth rates and altered expression of secondary metabolites in comparison to control and resistant plants. Austropuccinia psidii infection led to a reduction in the proportion of monoterpenes and monounsaturated hydrocarbons and an increase in long chain hydrocarbons. No differences in secondary metabolite profiles were found between the treatments 90 days after inoculation, suggesting that differences observed were in response to severe infection and that leaf chemistry is not a good predictive biomarker of susceptibility in C. citriodora subsp. variegata.
... (Berthon et al. 2018; Pegg et al. 2014b). Fernandez Winzer et al. (2018 also found that species in a coastal swamp woodland considered more tolerant of A. psidii only became infected after other more susceptible species such as Melaleuca quinquenervia ...
Austropuccinia psidii (myrtle rust) is one of the most significant threats to plant industries and biodiversity in the Australasian region. Susceptibility phenotypes of Australian native Myrtaceae to A. psidii have varied significantly since the pathogen was first detected in Australia in 2010, with some species appearing to increase in susceptibility over time. We hypothesise that increased inoculum concentrations in natural ecosystems may be contributing to observed changes in susceptibility phenotypes. A study was undertaken to determine the effect of A. psidii inoculum concentration on myrtle rust disease incidence and severity on five native (Rhodamnia rubescens, Syzygium hemilamprum, S. leuhmanii, S. moorei and S. oleosum) and one exotic (S. jambos) species of Myrtaceae under controlled conditions. Disease incidence and severity were found to increase across all species as inoculum concentration increased, with notable increases for species considered to be tolerant or of lower susceptibility to A. psidii. This improved understanding of the influence of increasing inoculum A. psidii concentrations on susceptibility phenotypes can now be integrated with current management and research plans, to predict and mitigate the impact of A. psidii on Australian native biota and ecosystems.
... Thereafter, plants from the different treatments were kept in two separate glasshouses (experimental units), with the same climatic conditions as described previously, to ensure no cross-contamination occurred. Ideally, we would have used at least two glasshouses per treatment (see Fernandez Winzer et al. 2018b) or individual structures within each glasshouse to avoid Rondanini et al. 2003). However, this was not possible due to space and biohazard constraints. ...
... For some of our study species, we found that A. psidii reduced the maximum height of the plants, but did not increase branching, in terms of either stem number or biomass. Fernandez Winzer et al. (2018b) reported similar decreases in the height of infected plants for three coastal woodland species. Interestingly, these species showed considerable betweenand within-species variation (B. ...
... It has been suggested that the between-species variation may be a result of different susceptibilities, while the within-species variation may be explained by differing climatic conditions, resource availability and number of re-infection events between studies (Smith 2006). Also consistent with our results, Fernandez Winzer et al. (2018b) reported that branching was not altered by A. psidii after a single inoculation event in the three coastal woodland species mentioned above. Because of this, it can be suggested that increased branching may only occur after successive reinfections of seedlings (that is, over a longer time period) or in plants at more advanced stages in their development (Fernandez Winzer et al. 2018b). ...
In 2010, the parasitic fungus Austropuccinia psidii (myrtle rust) was detected in Australia. Austropuccinia psidii infects immature growth of myrtaceous species. Many of Australia’s myrtaceous species occur within fire‐prone vegetation communities and have the capacity to resprout after fire. Therefore, it is likely that new post‐fire growth may be vulnerable to A. psidii infection, causing subsequent flow‐on effects to species’ persistence and community dynamics. The aim of this study was to test the impacts of A. psidii on native Australian Myrtaceae species after fire. We grew eight native susceptible species in a glasshouse experiment before burning them and inoculating the resprouting new growth of half the plants with A. psidii. We assessed the effect of A. psidii on the architecture, growth and biomass allocation of our study species. Although general patterns were observed across species, results were found to be species‐specific. Austropuccinia psidii significantly reduced the height of two of the eight species (Callistemon citrinus and Eucalyptus moluccana), but none of the species had increased branching. As expected, specific leaf area was lower (9%) in inoculated plants – although only significant for C. citrinus and E. dalrympleana – and leaf biomass was greater (15%), but significant for Angophora costata only. Finally, biomass allocation did not significantly differ between infection treatments. We can conclude that the effect of A. psidii infection on fire‐damaged plants has significant impacts on plants at the species level, which may have flow‐on effects at the community level, especially after repeated infections. Furthermore, these impacts may be exacerbated in the future under climate change, as the predicted increase in frequency and intensity of fires across Australia will result in more frequent new growth availability, providing more opportunities for A. psidii infection.
... Rust fungi (Pucciniales) constitute one of the largest groups of plant pathogens, with about 7,800 described species (Helfer, 2014), and some rust species can have large economic and ecological impacts. For example, myrtle rust (Austropuccinia psidii) is currently decimating a wide range of Myrtaceae around the world (Fernandez Winzer, Carnegie, Pegg, & Leishman, 2018;Glen, Alfenas, Zauza, Wingfield, & Mohammed, 2007), such as the endemic Eugenia koolauensis in Hawai'i and the endemic Rhodamnia rubescens in native forests in Australia (Carnegie et al., 2016). ...
Plant pathogens such as rust fungi (Pucciniales) are of global economic and ecological importance. This means there is a critical need to reliably and cost‐effectively detect, identify, and monitor these fungi at large scales. We investigated and analyzed the causes of differences between next‐generation sequencing (NGS) metabarcoding approaches and traditional DNA cloning in the detection and quantification of recognized species of rust fungi from environmental samples. We found significant differences between observed and expected numbers of shared rust fungal operational taxonomic units (OTUs) among different methods. However, there was no significant difference in relative abundance of OTUs that all methods were capable of detecting. Differences among the methods were mainly driven by the method's ability to detect specific OTUs, likely caused by mismatches with the NGS metabarcoding primers to some Puccinia species. Furthermore, detection ability did not seem to be influenced by differences in sequence lengths among methods, the most appropriate bioinformatic pipeline used for each method, or the ability to detect rare species. Our findings are important to future metabarcoding studies, because they highlight the main sources of difference among methods, and rule out several mechanisms that could drive these differences. Furthermore, strong congruity among three fundamentally different and independent methods demonstrates the promising potential of NGS metabarcoding for tracking important taxa such as rust fungi from within larger NGS metabarcoding communities. Our results support the use of NGS metabarcoding for the large‐scale detection and quantification of rust fungi, but not for confirming the absence of species.
... Exotic pathogens have caused irreversible damage to flora and fauna within a range of ecosystems worldwide. Popular outbreaks include the enormous devastations of chestnut blight (Endothia parasitica) on American chestnut trees (Castanea dentata) in the U.S. [1][2][3], sudden oak death (Phytophthora ramorum) on oak populations (Quercus agrifolia) in Europe, California, and Oregon [4][5][6], dieback (Phytophthora cinnamomi) on hundreds of hosts globally [7][8][9], and myrtle rust (Austropuccinia psidii) on Myrtaceae family plants in Australia [10][11][12][13]. The effects of the latter case have raised national alerts and response programmes given the extensive host range and the ecological and economic importance of Myrtaceae plants in the Australian environment [14][15][16][17]. ...
The environmental and economic impacts of exotic fungal species on natural and plantation forests have been historically catastrophic. Recorded surveillance and control actions are challenging because they are costly, time-consuming, and hazardous in remote areas. Prolonged periods of testing and observation of site-based tests have limitations in verifying the rapid proliferation of exotic pathogens and deterioration rates in hosts. Recent remote sensing approaches have offered fast, broad-scale, and affordable surveys as well as additional indicators that can complement on-ground tests. This paper proposes a framework that consolidates site-based insights and remote sensing capabilities to detect and segment deteriorations by fungal pathogens in natural and plantation forests. This approach is illustrated with an experimentation case of myrtle rust (Austropuccinia psidii) on paperbark tea trees (Melaleuca quinquenervia) in New South Wales (NSW), Australia. The method integrates unmanned aerial vehicles (UAVs), hyperspectral image sensors, and data processing algorithms using machine learning. Imagery is acquired using a Headwall Nano-Hyperspec ® camera, orthorectified in Headwall SpectralView ® , and processed in Python programming language using eXtreme Gradient Boosting (XGBoost), Geospatial Data Abstraction Library (GDAL), and Scikit-learn third-party libraries. In total, 11,385 samples were extracted and labelled into five classes: two classes for deterioration status and three classes for background objects. Insights reveal individual detection rates of 95% for healthy trees, 97% for deteriorated trees, and a global multiclass detection rate of 97%. The methodology is versatile to be applied to additional datasets taken with different image sensors, and the processing of large datasets with freeware tools.
... Highly susceptible plants show no signs of resistance and have high . b (Winzer et al., 2017). c (Pegg et al., 2014). ...
Myrtle rust (Austropuccinia psidii) is an invasive rust fungus that attacks species of the Myrtaceae family, one of
the most dominant plant families in Australia. The potential extent of myrtle rust affected areas and the high
number of potential host species make a species prioritisation scheme essential to direct conservation and
management efforts. This study builds on previous work by: compiling an up-to-date list of myrtle rust occurrences
and host species; mapping current and future climate suitability for myrtle rust; and identifying host
species at risk based on range overlaps and susceptibility data.
Suitable habitat for myrtle rust is restricted to eastern and southern coastal areas of Australia, with minor
areas in the Northern Territory and Western Australia. This coastal distribution remains present under future
climates, with some extension in inland New South Wales and Tasmania, and a reduction of suitable habitat in
northern Queensland and Western Australia. Contrary to previous studies, our results indicate that south-west
Western Australia has low climatic suitability for myrtle rust. Under current climate, 1285 Myrtaceae species are
at risk of exposure to myrtle rust. This number decreases to 1224 species under future climate.
We divide species exposed to myrtle rust into three priority categories, giving highest priority to species with
at least 70% of their range overlapping regions climatically suitable for myrtle rust under current or future
climates. We find 23 species are of high priority for conservation action. Finally, we provide a series of recommendations for management of species within each priority category.
Globalisation has resulted in the spread of infectious plant diseases to new regions and host species and the novel disease caused by myrtle rust poses a global threat to naïve hosts in the Myrtaceae family of plants. This study uses a focal species, Tristaniopsis exiliflora, to explore the climatic and microclimatic preference of the myrtle rust disease (Austropuccinia psidii). Populations of T. exiliflora were sampled across the species distribution in Far North Queensland, Australia, modelling A. psidii severity as a function of macro- and micro-environmental variables. Disease severity was found to increase with annual precipitation and foliage projective cover, and decrease with maximum temperature and valley confinement. A subsampled population found that individuals with lower canopy heights experienced more severe disease. Our results suggest that, in tropical environments with seasonal rainfall, A. psidii virulence is reduced when mean annual rainfall is less than 1500 mm and virulence is substantially reduced when maximum temperatures exceed 32 °C. The climatic drivers identified in this study align with optimal in vitro conditions for A. psidii germination and development. This suggests that climatic conditions are regulating myrtle rust in natural ecosystems at a broader scale, and that increased conservation efforts should focus on species with narrow climatic distributions and highly susceptible regions such as the Wet Tropics World Heritage Area.
