Niche shift and global potential distribution of the invasive species Trioza erytreae, vector of the citrus Huanglongbing disease

doi:10.21203/rs.3.rs-2375084/v1

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Niche shift and global potential distribution of the invasive species Trioza erytreae, vector of the citrus Huanglongbing disease

https://doi.org/10.21203/rs.3.rs-2375084/v1

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Invasive species pose a major threat to biodiversity, ecological structure of habitats and agriculture, especially in a setting of climatic change. The impact of these species also has a major role in the spread of exotic vector-borne diseases, which may cause substantial economic losses in agriculture if cultivated species are among those affected by these diseases. The African citrus psyllid, Trioza erytreae (Del Guercio), has recently become an invasive species in Europe. This species, which has been known as a pest of trees in the family Rutaceae in Africa for a long period of time, is cause for major concern by its potential effects on citrus orchards, of particular economic importance in southern European countries. Through the evaluation of macroclimatic niches occupied by invasive and native populations and the use of species distribution modelling, we have predicted the potential global geographic distribution of the species, which shows high suitability in a wide range of areas in every continent, as well as quantified and evaluated differences in the macroclimatic niches occupied by invasive and native populations of the species, demonstrating a high similarity and therefore conservatism between the climatic conditions occupied by the species in both ranges. These results provide valuable information that can be used in planning conservation actions in order to reduce risk of invasion by the species.

Climate change

Invasive species

Niche conservatism

Niche stability

Species Distribution Modelling

Pest

Trioza erytreae is a major pest of citrus trees worldwide that has recently been introduced to Europe, posing a major threat to citrus orchards in the continent
T. erytreae shows high suitability in coastal and temperate areas worldwide
T. erytreae shows niche conservatism between native and exotic populations

Invasive species pose a major threat to biodiversity, ecological structure of habitats and agriculture (Jackson et al. 2015), especially in a setting of climatic change, in which a species may attain a larger potential for invasion due to more favorable environmental conditions. The impact of these species in exotic settings threatens not only the native biodiversity of these invaded areas, but its communities, potentially altering the ecosystem as a whole (Elton 1958; Lodge 1993; Simberloff et al. 2013; Mateo et al. 2015). The impact of these species is not however, solely restricted to concerns pertaining to the conservation of biodiversity and ecosystems, but also have a major role in the spread of exotic vector-borne diseases which may not only significantly impair the survivability and fitness of native species, but huge economic losses in agriculture if cultivated species are among those affected by these diseases (Lambin et al. 2010).

Predicting areas and locations where alien species (species occurring outside of their natural range through human action, either intentionally or unintentionally) might establish and spread is of great importance for the avoidance and prevention of biological invasions. The use of species distribution models (SDMs) is an especially useful tool with high predictive capabilities when used in accordance with data obtained from the species’ occurrences and the respectively relevant bioclimatic variables for these areas (Peterson et al. 2008), allowing the prediction of areas that have not yet been colonized by the species but may be suitable for stable populations to develop in due to similarity in climatic conditions, and essentially allowing preventive measures to be taken in said areas in order to avoid colonization. The use of SDMs is particularly important in a context of climate change, in which the potential distribution of invasive species may either change or increase the area suitable for colonization, with the species’ distribution changing towards conditions suitable for its proliferation (Abellán et al. 2017; Guisan et al. 2013).

A key aspect of biological invasions is to know how alien species respond to new environmental conditions, and the extent to which their realized (i.e., occupied) niche is conserved throughout the invasion process (Guisan et al. 2014). Because the native range might not encompass the full range of environmental conditions in which the species can survive and reproduce (i.e. the fundamental niche), as a result of constraints imposed by biotic interactions and dispersal limitations (e.g. geographic barriers), the species may fill different parts of their fundamental niche during the invasion, leading to a change in the realized niche (Bates and Bertelsmeier 2021). Thus, exploring niche shifts between native and invasive ranges can assist assess limitations and uncertainties of SDM predictions, as they rely on the assumption of niche conservancy between both ranges, and may provide additional insights useful in understanding range expansion and the invasion potential of alien species (Guisan et al. 2014).

The African citrus psyllid, Trioza erytreae (Del Guercio) (Hemiptera: Triozidae) has recently become an invasive species in Europe (Cocuzza et al. 2017). This species, which has been known as a pest of trees in the family Rutaceae in Africa for a long period of time (Van der Merwe 1941), is cause for major concern by its potential effects on citrus orchards. This insect damages the plant directly by feeding from it and, more importantly, indirectly as a vector of the citrus greening disease or Huanglongbing (HLB) (McClean and Oberholzer 1965; Moll and Martin 1973; Aidoo et al. 2019), caused by gram-negative bacteria, Candidatus Liberibacter spp. HLB is one of the most devastating citrus diseases in the world, negatively affecting the plant in a number of ways and decreasing citrus production in both quality and quantity, and therefore becoming a major threat to the survival of the citrus industry worldwide (Bové 2006; Gottwald et al. 2007).

T. erytreae, which is probably native to southeastern Africa (Van der Merwe 1941), was first recorded outside of its native range on various neighboring islands such as St. Helena, Madagascar and in the Mascarene islands of Mauritius and Reunion (Catling and Atkinson 1974; Hollis 1984; Aubert 1987; Aubert et al. 1988; Samways 1990), as well as the Arabian Peninsula (Bové and Garnier 1984). The species was later recorded in some Macaronesian islands: first in Madeira (Portugal) in 1994 (Carvalho and Aguiar 1997) and then in the Canary Islands (Spain) in 2002 (González et al. 2013). More recently, in 2014, this psyllid finally reached continental Europe throughout the northeastern of the Iberian Peninsula (Cocuzza et al. 2017), rapidly spreading to eastern Portugal and northeastern Spain throughout the recent years (Pérez-Otero et al. 2015; Arenas-Arenas et al. 2019), with the potential to further expand throughout Europe and the Mediterranean. Although HLB has not been detected yet in European countries (Cocuzza et al. 2017; Siverio et al. 2017), T. erytreae has a serious threat to the citrus industry in these areas, as shown by the other main vector of HLB, the Asian citrus psyllid, Diaphorina citri Kuwayama, which has spread rapidly in some of the citrus producing areas of America (Bové and Rogers 2015).

In this study, we aim to (i) evaluate the similarities in the macroclimatic niches occupied by invasive and native populations and quantify both niche unfilling and niche expansion of the species between the different native and invaded distributions; and (ii) predict the level of risk and suitability of this species potential global geographical distribution in both the present and in the future in a setting of climate change with the use of SDMs. While some local and regional studies have explored the potential distribution of this species (e.g. Richard et al. 2018; Benhadi-Marín et al. 2020), this study represents the first attempt to estimate potential areas at a global scale. The obtained results can provide valuable information that can be used in planning conservation actions and in order to reduce risk of invasion of areas suitable for colonization by the species, as well as to mitigate economic loss of produce in the case of species that pose a threat to cultivated crops and produce.

Species’ occurrence and climate data

We compiled occurrence records for T. erytreae in its native range and invaded areas from GBIF (Global Biodiversity Information Facility, www.gbif.org; accessed September 2021), books, articles and official reports (Table S1). Those locations with missing coordinates but with accurate descriptions of the location were georeferenced in order to obtain a larger number of occurrences. Locations were integrated into a Geographic Information System (GIS) at 5‐arcminute resolution (approximately 10 × 10 km), and duplicate samples within the same grid cell were handled as single observations. Final sample size was 405 grid cells with the presence of the species (84 native and 321 invaded; Fig. 1).

Nineteen bioclimatic variables were obtained from WORLDCLIM version 1.4 (available at http://www.worldclim.org; Hijmans et al. 2005) for present and future (years 2050 and 2070) climatic conditions at 5 arc‐minutes resolution. For the climate change scenarios, we considered two Representative Concentration Pathways (RCP), 4.5 and 8.5, representing moderate and high future warming scenarios, respectively, and 17 general circulation models (GCMs) available in WORLDCLIM for these RCP.

Niche shift analyses

In order to identify and assess potential niche changes for T. erytreae between native and invaded ranges, we compared native (African) and introduced (European) occurrences in the environmental space following the procedure proposed by Broennimann et al. (2012), which involves three main steps. First, a principal components analysis (PCA) was utilized in order to summarize environmental variables in a two-dimensional environmental space, which was calibrated using the 19 bioclimatic variables obtained from the Worldclim database. The two first PCA axes were then used to create a gridded climate space of 100 x 100 square cells, each cell corresponding to a unique set of global climate conditions. These two PCA axes accounted for 71.40% of the variation in the raw climatic data. The first axis predominantly represented a gradient of precipitation and temperature seasonality while the second axis represented a temperature gradient. Second, we calculated the density of occurrences across the environmental space with the use of a kernel density function, which converts native/invaded occurrences of the species and the available climate in the native/invaded range (i.e. background conditions) into densities in order to correct for bias in sampling effort and environmental availability, respectively. The background conditions for the native and the invaded ranges were defined as those within the minimum convex polygons encompassing native and invaded occurrence records, respectively, buffered by one degree. Third, we measured niche overlap across the environmental space with the use of Schoener’s D, calculated from the occurrences in the environmental space depicted by the first two axes of the PCA (Warren et al. 2008; Broennimann et al. 2012). This index indicates the overall niche similarity between the two ranges over the whole climatic space and varies between 0 (no overlap) and 1 (complete overlap). We then conducted niche similarity tests (Warren et al. 2008) to assess whether the environmental niches occupied in both ranges are more similar than expected by chance. In this test, the observed value of D is compared against a null distribution of 1000 simulated values obtained by overlapping the niche of the native range with simulated niches from drawing the same number of invaded occurrences at random within the available climatic conditions of the invaded range and vice versa. The niche similarity test is thus bidirectional. The rejection of niche similarity hypothesis indicates that the niche overlap between native and invasive niche is larger than expected by chance given the available environmental conditions in invaded and native ranges (Warren et al. 2008).

In order to further investigate the niche dynamics of T. erytreae we also computed three niche shift metrics as proposed by Guisan et al. (2014) using the occurrence and environmental density grids described above: niche expansion, niche unfilling and niche stability. Niche expansion refers to those climatic conditions that are available in both native and invasive ranges but only occupied in the invaded range. Niche unfilling indicates climatic conditions that are available, but not yet occupied, in the invaded range, reflecting the degree of climate equilibrium. Finally, niche stability indicates conditions filled in both native and invaded ranges. These metrics were calculated from the area of environmental conditions shared by both native and exotic distributions, that is, the intersection of environmental conditions shared by both ranges. All niche analyses were performed with the package ecospat (Di Cola et al. 2017) in R (R Core Team, 2017).

Species distribution modeling

We estimated the current and future global potential distribution of T. erytreae through an ensemble species distribution modelling approach (Araújo and New 2007). To avoid redundancy and collinearity among bioclimatic variables, a subset of eight variables from pairs of highly correlated variables (Pearson r > 0.8) were retained. The selected variables were: annual mean temperature (bio1), mean diurnal range (bio2), temperature seasonality (bio4), annual precipitation (bio12), precipitation of driest month (bio14), precipitation seasonality (bio15), precipitation of warmest quarter (bio18) and precipitation of coldest quarter (bio19). Since the potential range distribution of invasive species is best addressed using its global coverage (see Broennimann and Guisan 2008), we used the pooled range (i.e. native and invaded ranges) to calibrate the models. The training area was defined as the four minimum convex polygons encompassing the occurrence records from Africa, the Iberian Peninsula, the Canary Islands, and Madagascar plus the Mascarene Islands, respectively, buffered by one degree. In order to reduce spatial bias in our occurrence dataset, especially due to the oversampling in Europe compared to the native range, we spatially thinned our original dataset with the R package spThin (Aiello-Lammens et al. 2015) to ensure that all occurrences were all at minimum 50 km distance from one another, yielding 66 records in the final dataset.

Ensemble models were fitted with the Biomod2 R package (Thuiller et al. 2021) using four SDM algorithms: generalized linear models (GLMs), generalized additive models (GAMs), random forest (RF) and maximum entropy (Maxent). For each algorithm, model parameters were set using the Biomod2 tuning function using a 10-fold split sampling (90% training data and 10% test data) to evaluate the models. The highest receiver operator curve (ROC) was used to select the optimal model using the largest value. Once optimal parameters were set, for each individual SDM algorithm, ten replicate models were constructed and, in each model, all occurrence records were partitioned randomly into a calibration set (training set = 80% of all records) and a testing set (validation set = 20%). Model accuracy was assessed on the test data using the area under the receiver operating characteristics curve (AUC) and the true skill statistic (TSS).

The ensemble model was built based on the four SDM algorithms, each weighted based on the cross-validated TSS values. The predictive performance of the ensemble model was evaluated based on AUC, TSS, sensitivity (proportion of true positives correctly identified), specificity (proportion of true negatives correctly identified), and the Boyce index. The relative importance of each predictor variable for model building was assessed throughout the built-in Biomod2 function, which uses 1 minus the Pearson's correlation between the predictions of the full model and the predictions of the model where the target variable was randomised (Thuiller et al. 2021). Based on the final models, climatic suitability projections were made for current and future climatic conditions at global scale. Since model transferability can be problematic when extrapolating to areas or time periods with conditions non-analogous to those where the model was calibrated (Fitzpatrick and Hargrove 2009), we conducted Multivariate Environmental Similarity Surface (MESS) analysis as implemented in the R package dismo (Hijmans et al. 2017).

Niche dynamics

Overlap between the native and invaded realized niches of T. erytreae was low (D = 0.101), as estimated from the multivariate environmental space (Fig. 2). Nevertheless, results of the one-tailed niche similarity test showed that the observed value of niche overlap was significantly higher than expected by chance (p-value < 0.05 in both directions; Fig. S1), indicating niche conservatism between the exotic and native distributions of the species. Niche shift indices also indicated a moderate degree of niche expansion (0.499) and niche stability (0.501), and a relatively low degree of niche unfilling (0.367). While most of available environmental conditions within the invaded range fall inside the environmental conditions of the native range, the median of the distribution of T. erytreae in the invaded range moved towards a lower precipitation, stronger seasonality and lower temperature relative to the native range (Fig. 2). Notably, the realized niche expanded into areas with lower temperature and slightly lower precipitation and stronger seasonality. On the other hand, some small areas with higher temperature are only occupied in the native range (i.e. unfilling).

Current and future potential distributions

Ensemble model performed considerably better than random, with an AUC, TSS and Boyce Index values of 0.983, 0.887 and 0.962, respectively, therefore demonstrating high performance in predicting the species’ potential distribution. Variables which contributed most to the ensemble model were annual mean temperature (52.9%), mean diurnal range (38.7%) and precipitation of driest month (19.5%) (see Table S2).

T. erytreae shows an overall large potential distribution at global scale, with areas climatically suitable located in every continent (Fig. 3). MESS results showed that most areas of North America and northern Asia appear to have background environmental conditions outside the range of that found in the calibration range (Fig. S2). Hence, model projections in these regions are extrapolations subjected to high uncertainty, so they should be taken with caution. Excluding these uncertain regions, global current areas of highest climatic suitability are located mainly in subtropical and temperate areas (Fig. 3), so that the probability of presence of T. erytreae was highest at moderate to warm temperatures. The species’ native range seems to be confined to sub-Saharan Africa, Madagascar and the southern part of the Arabian Peninsula. Projecting the model globally identified suitable climatic conditions at the sites where the species has established invasive populations, and revealed that suitable conditions also exist throughout most areas of western Europe, northern Africa, eastern Asia, southern Australia, eastern and southern areas of North America and eastern and western South America, as well as the southern tip of the continent. The species also shows high suitability in islands throughout the Atlantic, Pacific and Indian oceans.

SDM results also suggest that the suitable environments for T. erytreae under future climate change will decrease in spatial extent, as well as will shift towards higher latitudes (Fig. 3 and Fig. S3). Though both examined RCPs scenarios (RCP 4.5 and RCP 8.5) suggest this decrease in the potential area of distribution of the species, the latter, that is, the 8.5 emission scenario shows a more severe reduction in suitable area as well as a more prominent shift toward northern latitudes for years 2050 and 2070. Predictions show a considerable loss of suitable conditions at the native range under scenarios of climate change, as well as different areas of North America, South America, Europe, eastern Asia and Australia. On the other hand, new areas with suitable conditions under climate change are mainly located in northern Europe, northeastern North America and southern South America.

T. erytreae poses a major threat to citrus plantations around the world, especially in areas in which it has already been introduced to, with clear signs of expansion of the species’ distribution under current climatic conditions. A prime example of this rapid expansion of the species’ distribution can be observed, as previously stated, in the Iberian Peninsula, with the rapid spread of the species through the western portion of Portugal and north-western and south-western Spain in the last years (Arenas-Arenas et al. 2019). Our results point to niche conservatism throughout this invasion process, with the species occupying areas relatively similar in climate to those of native populations. Furthermore, our findings show that many areas around the globe are potentially suitable for the establishment of the species.

The comparison of the niches in the native and invaded ranges provides useful information of the extent to which realized niches of this species are maintained during its invasion (Guisan et al. 2014). Although most of the available climatic space in the invaded range (European populations) fall inside the environmental conditions of the native distribution, our results indicate that the median of both the invaded niche of the species and its environmental background tend to occupy areas with lower precipitation, stronger seasonality and higher temperature relative to the native ones (Fig. 2). Nevertheless, this niche shift could be just reflecting the difference in the availability of climatic conditions in both geographical areas (Warren et al. 2008; Broennimann et al. 2012). In fact, we found that the native and invaded realized niches of T. erytreae are statistically more similar that expected by chance given the available conditions in both ranges, suggesting niche conservatism. In the same sense, niche stability is moderate to high, indicating that a considerable proportion of the exotic niche overlaps with the native niche, also pointing to niche conservatism (see Callen and Miller 2015; Strubbe et al. 2015; Hu et al. 2016). That is, native niche characteristics of T. erytreae are at least partially conserved during the invasion process in Europe. Because niche conservatism is an assumption of SDM approaches (i.e. niches are assumed to remain conserved when models are transferred in space or time; Wiens et al. 2009), these results provide confidence to the potential distributions obtained for this species (see below).

The moderate degree of niche expansion in the exotic European populations indicates the occurrence of the species within the invaded range in analog environmental conditions that are not occupied in the native range (Guisan et al. 2014). The absence of T. erytreae in areas with lower precipitation, stronger seasonality and slightly lower temperature within the native range seem to indicate the presence of other factors that impede the species colonization; whether this is due to biotic factors (such as predation, competition or lack of host plants), abiotic factors (such as topography and presence of natural barriers), or both, is unknown. Furthermore, because the sampling is relatively incomplete within the native area of distribution for this species, the effects of biased and incomplete data on the obtained values of range expansion cannot be ruled out. On the other hand, niche unfilling is low in the intersection of the native and exotic environmental conditions, suggesting that the species has colonized most of its native realized niche in its invaded range. The suitable climate spaces that remain unoccupied within the invaded range, which represent mainly higher temperatures, are likely related to the fact that this is a relatively recent invasion and the species has not had enough time to colonize the full extent of its native realized niche (see e.g. Strubbe et al. 2013; Polidori et al. 2018; Poursanidis et al. 2020).

The species appears to be particularly suited to temperate climates with moderate temperatures and moderate to high levels of humidity (Moran and Blowers 1967; Catling 1969; Cocuzza et al. 2017), though our model projections indicate that mean temperature is the most relevant variable in predicting the suitability of the species. The potential distribution of T. erytreae at global scale seems to support this, since the species’ potential distribution is mainly restricted to coastal areas of western Europe, western and southeastern North America, eastern and western South America, eastern Asia, southeastern and southern Australia and its native continent of Africa, as well as particularly high suitability in subtropical and temperate island territories (as is the case for the Canary islands, the Azores islands, Polynesian islands, the Mascarene islands, etc.). It is interesting to note that some of the continental areas occupied by the species in the native range, such as in the Great Rift Valley, have mild temperatures below 28 º C appropriate for the species in the continent, further supporting our results of suitability of the species in temperate regions (Kassie et al. 2013) as these areas share the same climatic conditions of the previously mentioned coastal areas in which the species may expand its range.

Interestingly, while under current climatic conditions T. erytreae could, in fact, expand its current distribution significantly, future predictions for 2050 and 2070 under a context of climate change suggest a significant decrease of potentially suitable areas in the two different scenarios presented (RCP 4.5 and RCP 8.5); a steady increase of carbon emissions and its subsequent effects on the climate negatively affecting the global suitability of the species, with the latter scenario having an even more significant reduction of current potential areas. This is likely due to the fact that the species is not well-adapted to higher temperatures (Aidoo et al. 2018, 2019), restricting even further its potential distribution to coastal areas that maintain more temperate climates worldwide. Nevertheless, its distribution under future climatic conditions, as is expected, also would expand to areas closer to the poles that would become more temperate, with milder temperatures suitable for the species, this event being even more accentuated in the latter scenario.

Predictions on the potential distribution of the studied species may give insights on areas in which the species is more likely to expand its distribution, but may not be powerful enough in assessing areas in which the species could not establish (Polidori and Sánchez-Fernandez 2020), since these are only based on recorded presence of individuals of this species. The limited sampling of the species’ native distribution may be contributing to this potential issue, therefore altering the species’ actual potential distribution, as sampling effort appears to be higher in the species’ exotic range than in its native distribution. Other limitations intrinsic to the process of SDMs exist, since only climatic variables were used, though many other variables may affect the species’ distribution, such as biotic variables including competition, predation and availability of biotic resources, as well as the dispersion potential of the species (Jiménez-Valverde et al. 2008). SDMs also assume that the species is at equilibrium with its environment, which may or may not be the case for this particular species within its invaded range (Gallien et al. 2012), therefore limiting our model’s prediction capabilities. Though these limitations are intrinsic to the modelling process, the use of SDMs’ predictive capabilities proves useful in predicting climatic suitability for the studied species and largely fit with empirical data obtained from the species’ occurrences (Peterson et al. 2008).

Several recent studies have also modeled the potential distribution of T. erytreae at smaller spatial scales (Richard et al. 2018; Benhadi-Marín et al. 2020; Espinosa-Zaragoza et al. 2021), the results of which are not fully congruent with our predictions, likely due to some methodological limitations of these previous papers. SDMs should be performed using all of the species’ occurrences, that is, its global coverage, and not only those occurring in either exotic populations or native ones, in order to obtain more reliable results and models which ensure prediction of the future spread of the species, as proposed by Broennimann & Guisan (2008). Omitting native occurrences (e.g. Benhadi-Marín et al. 2020) may yield biased results in regards to the species’ suitable conditions, that is, greatly restricting the species’ potential distribution to conditions only occupied in invaded areas, likely not yet in equilibrium, and omitting possible conditions which are only occupied in its native range. This is particularly important in the case of T. erytreae, since the species occupy a broader range of environmental conditions in the species’ native range than in its invaded range, as can be observed through our analysis of niche dynamics. Similarly, using only native occurrences (e.g. Richard et al. 2018; Espinosa-Zaragoza et al. 2021) can omit parts of the fundamental niche only present in the invaded range, for example due to biotic constraints acting in the native distribution but not in the invaded one (Broennimann and Guisan 2008). Our results, based on data from both native and invaded ranges, therefore yield a more realistic potential distribution for the species.

Overall, our results indicate that T. erytreae may occupy areas far beyond its current exotic distribution in Europe, particularly expanding further throughout coastal areas of western Europe, and having potentially highly suitable areas in temperate climates of all other continents, as well as high suitability in island environments these often constituting major citrus growing regions due to the favorable climatic conditions for said fruit crop (Liu et al. 2012). While the causative agent of HBL, the gram-negative bacteria Candidatus Liberibacter spp., is currently not present in introduced European populations of the psyllid (Arenas-Arenas et al. 2019), an expansion of the species’ distribution could further increase the probability of accidental introduction of the pathogen in these and other potentially suitable areas around the globe. The exposure to the bacterium can implicate a rapid spread of it and the disease, as only a few infected individuals are needed to transmit the causal agent of the disease (Van Vuuren and Van Der Merwe 1992; Cocuzza et al. 2017). Thus, an introduction of this pathogen in the invaded populations would likely transmit the disease throughout the current established populations of the psyllid and essentially through projected areas in which the species may establish if invasive populations continue to expand beyond their current range, severely hindering citrus production in affected areas (Gottwald 2010). Nevertheless, while large areas of the Americas, Africa, Asia and Australia show high suitability for the disease, in Europe only the Iberian Peninsula and the United Kingdom seems to be suitable, although marginally (Ajene et al. 2020). It is also important to note that T. erytreae is a polyphagous psyllid (Catling and Atkinson 1974; Aidoo et al. 2018), meaning that it feeds on representatives of the Rutaceae family as a whole, and though perhaps not of economic significance, the possibility of it spreading and affecting native species where the species may potentially establish populations is also to be taken into account.

Several other issues arrive if the species occupies other areas suitable for its establishment, particularly when taking into account areas shared by another psyllid, Diaphorina citri (Lallemand et al. 1986), which carries an Asian variant of the bacterium, Candidatus Liberibacter asiaticus. This form of the bacterium is, in contrast to the form usually transmitted by T. erytreae, Candidatus Liberibacter africanum, heat tolerant, which may pose further threats to citrus orchards and other genera in the family Rutaceae in areas in which the African form of the bacterium may not grow (Garnier et al. 1984; Jagoueix et al. 1996; Sagaram et al. 2009; Pelz-Stelinski et al. 2010), as T. erytreae is also capable of transmitting the Asian form of the bacterium (Lallemand et al. 1986; Ajene et al. 2019). This event would require an overlap between T. erytreae and D. citri populations, which has yet to be documented.

While it is currently unknown how the species first arrived to Europe, it is highly likely that it was transported by shipping of citrus saplings and fruits, particularly through galls present on the leaves of these commercially imported products (Catling 1969). This is particularly the case for most introduced species of gall producing hemipterans, as the small size and position of these galls on the leaves allow them to pass undetected. The accidental introduction of T. erytreae has in fact occurred independently on at least three different occasions (Macaronesia, the Mascarene Islands and the Iberian Peninsula) (Cocuzza et al. 2017); whether this introduction occurred directly from native African populations or already introduced populations (such as introduction to the Iberian Peninsula from populations present in the Canary Islands) is currently unknown.

Our findings through the use of the analysis of niche dynamics and predictive efforts regarding T. erytreae’s potential distribution provide useful information for anticipating the potential colonization of the African citrus psyllid and the spread of the HBL disease, contributing to the early alert o and the implementation of preventive measures, especially in areas that they have not been reported, in order to mitigate economic loss in the citrus industry.

Author Contribution Statement:

Author contributions: PA and MAL conceived the ideas. SPB and PA collected and compiled the data. SPB and PA analyzed the data. SPB and PA led manuscript writing. All authors contributed critically to the drafts and gave final approval for publication.

Funding

No funds, grants or other support was received.

Competing Interests

The authors declare no conflict of interest.

Author Contributions

Pedro Abellán and María Ángeles López conceived the ideas. Sergio Pérez-Bonet and Pedro Abellán collected and compiled the data. Sergio Pérez-Bonet and Pedro Abellán analyzed the data. Sergio Pérez-Bonet and Pedro Abellán led manuscript writing. All authors contributed critically to the drafts and gave final approval for publication.

Data Availability

The datasets generated and analysed during the current study are available in open access repository of the University of Seville (https://idus.us.es/handle/11441/32574) [in progress].

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Niche shift and global potential distribution of the invasive species Trioza erytreae, vector of the citrus Huanglongbing disease

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