The paths of the galls: differences in the ecology and distribution of two European ok galls wasps Andricus dentimitratus and Andricus pictus

Research Article The Paths of the Galls: Differences in the Ecology and Distribution of Two European Oak Gall Wasps Andricus dentimitratus and Andricus pictus Lola F. Multigner , 1 Diego Gil-Tapetado , 1 Jose Luis Nieves-Aldrey , 2 and José F. Gómez 1 1 Universidad Complutense de Madrid, Facultad de Ciencias Biológicas, Departamento de Biodiversidad, Ecología y Evolución, José Antonio Novais 12, 28040 Madrid, Spain 2 Museo Nacional de Ciencias Naturales (CSIC), Calle José Gutiérrez Abascal 2, 28006 Madrid, Spain Correspondence should be addressed to José F. Gómez; [email protected] Received 6 August 2022; Revised 23 September 2022; Accepted 7 October 2022; Published 30 November 2022 Academic Editor: Naureen Rana Copyright © 2022 Lola F. Multigner et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Andricus dentimitratus (Rejtõ, 1887) and Andricus pictus (Hartig, 1856) are two European gall wasps (Hymenoptera,Cynipidae) that induce galls on species of Quercus. The distribution and ecological niches of these species have not been studied in detail, though they are known to have a different distribution pattern in the Iberian Peninsula in Europe. To investigate this difference and its potential relationship with climate and host species distribution, we analysed the potential distribution of both species in the Iberian Peninsula using six algorithms and a consensus model based on 600 iterations for each species. We compared the models obtained for each species with the distribution of their host Quercus species. The results show that A. dentimitratus and A. pictus have a complementary distribution delimited by the Ebro valley, with A. dentimitratus occurring northeast of the valley and A. pictus southwest. The observed distribution patterns might be due to differences in the climatic requirements of each species or to the distribution of their host species given that A. dentimitratus is specifictoQ. humilis and Q. cerris (except in the northeastern Iberian Peninsula) and A. pictus, to marcescent Mediterranean oaks (Q. faginea and Q. pyrenaica) and Q. suber. We propose two hypotheses to explain the nonoverlapping distribution of the two gall wasp species in the Iberian Peninsula: in the first scenario, A. dentimitratus arrived to the to the Iberian Peninsula from the eastern Palearctic by way of Europe and A. pictus, from the north coast of Africa; in the second, their distribution is a result of their speciation in different glacial refugia: A. dentimitratus in the Italian Peninsula and A. pictus in the Iberian Peninsula. 1. Introduction Cynipidae (Hymenoptera:Cynipoidea), also known as gall wasps, includes about 1400 species worldwide, of which around 140 occur in the Iberian Peninsula [1, 2]. These wasps induce galls on specific host plant species. For instance, members of the tribe Cynipini are strictly associated with species within the family Fagaceae [2]. Two phylogenetically close species included in this tribe are Andricus pictus (Hartig, 1856) and Andricus dentimitratus (Rejtõ, 1887), which both form galls on the acorn cups of deciduous or marcescent oaks (Quercus L.), often causing the fruit to spoil [3]. Many species of the genus Andricus have an heteroecic life cycle in which the sexual generation is induced on oaks of the section Cerris (e.g., Quercus cerris L. or Quercus suber L.) and the parthenogenetic generation, on deciduous or marcescent oaks of the section Quercus (e.g., Quercus pubescens or Quercus pyrenaica Willd.) [4]. Although known to occur in A. pictus and A. dentimitratus, the sexual generation has not been found nor described in either species, and only galls produced by the parthenogenetic generation have been described to date. Molecular data has confirmed the Hindawi Journal of Zoological Systematics and Evolutionary Research Volume 2022, Article ID 8488412, 14 pages https://doi.org/10.1155/2022/8488412 existence of sexual generations of A. pictus in the species complex Andricus burgundus (Giraud, 1859), which was previously considered a single species that develops exclusively on Q. suber [5]. The typical sexual gall of A. burgundus develops in inflorescences is 2.0-2.5 mm long, oval, with gall surface brown to yellowish in colour, thin-walled, and with a larval chamber filling the entire gall [2]. Regarding A. dentimitratus, only a few female specimens have been found that could be the sexual generation of this species, but neither the male nor the galls of this generation have been described [2, 6]. Despite the small size of these insects (about 5mm in length), the galls induced by the parthenogenetic generation, their extended phenotype, are conspicuous and distinguishable (Figure 1). The galls of A. pictus are typically 1 to 2 cm in diameter (although the size is variable) and have three crowns that project from a cylindrical or conical body: a basal crown that surrounds the acorn bud, a wider middle crown, and a smaller apical crown that encircles an apical orifice connected to a single larval chamber (unilocular gall) located in the centre of the gall. The galls of A. dentimitratus (2.5–3.5cm in diameter) have two crowns that project from a small central body enclosing the single larval chamber: an upper crown that is relatively flattened, and a larger bottom one that wraps around the acorn. Both galls are reddish or garnet in colour and have a very sticky surface; after maturation, they become brown or woody and less viscous [2, 7]. With respect to host-gall wasp specificity, A. pictus induces galls most frequently on Q. pyrenaica, but also on Quercus faginea Lam. and occasionally on Quercus lusitanica Lam. and Quercus canariensis Willd. [2]. The species develops during the summer and matures in October with adults emerging in February of the following year [2]. In the Iberian Peninsula, the galls of A. dentimitratus develop on Quercus humilis Mill. and occasionally on Quercus robur. The species develops during the summer and matures at the end of the season with adults emerging in the spring of the following year [2]. The distributions of A. pictus and A. dentimitratus present a case of seemingly marked spatial complementarity. Andricus pictus is distributed in central, southern and western Iberia, and in North Africa. Though the species has also been cited in other areas, including northeastern Iberia and Iran, these records are likely misidentifications. By contrast, A. dentimitratus is distributed throughout southern Europe, in southern France, the Italian Peninsula, Sicily, Austria, and Hungary. In the Iberian Peninsula, this species is found only in Catalonia, in the northeast of this territory (Pujade-[8, 9]). Based on this distribution pattern, the Iberian System and the Ebro valley appear to constitute barriers separating the two cynipids. The processes influencing the historical and current distribution and dispersion of these two species of Cynipidae are largely unknown. To address this question, we use species distribution models (SDM) to predict the distribution of A. pictus and A. dentimitratus and their areas of greatest habitat suitability and overlap. Considering these data and their ecology and biogeography, we develop and evaluate hypotheses about the evolutionary processes that have shaped the distribution of these cynipids. Several recent studies have applied SDM to analyse Cynipidae in the Iberian Peninsula including Cynipini associated with Quercus L. host plants [10], the Asian chestnut gall wasp Dryocosmus kuriphilus (Yasumatsu, 1951; [11]) and species of Diplolepis on Rosa L. host plants [12]. Following this framework, this study is aimed at describing and analysing the distribution of A. pictus and A. dentimitratus using statistical models of habitat suitability based on bioclimatic variables. In addition, we discuss two phylogeographic hypotheses to approach the natural history of both species in the western Palearctic, thereby reducing the Wallacean and Hutchinsonian shortfalls [13] related to these cynipids. 2. Material and Methods 2.1. Data Collection. We collected all available and accessible georeferenced occurrence records of A. pictus and A. dentimitratus from the literature [1, 8, 14–31], the online repository Global Biodiversity Information Facility (GBIF, http:// www.GBIF.org), and the citizen science platform databases Biodiversidad Virtual (http://www.biodiversidadvirtual .org), iNaturalist (http://www.iNaturalist.org) and http:// Observation.org. In our search for occurrence records, we also considered all synonymies of both species, specifically the combinations Andricus panteli [31] and Cynips panteli (Kieffer, 1901), as synonyms of A. pictus (Hartig, 1856), and the combinations Andricus viscosus Nieves (Aldrey, 1986) and Cynips mayri (Kieffer, 1897) as synonyms of A. dentimitratus (Rejtõ, 1887) [8]. Erroneous records from iNaturalist resulting from misidentifications were also corrected by validation of the georeferenced photographs. Some records from the literature mention a population or municipality, but not coordinates. In these cases, we considered the coordinates of the centroid of the locality. We obtained a total of 106 records of A. pictus and 210 of A. dentimitratus. After eliminating data with redundant coordinates, 89 records of A. pictus and 160 of A. dentimitratus were used to establish the habitable area of both species on a European scale. To model the potential distribution of both species specifically within the Iberian Peninsula and North Africa, we used only the presence points within these areas. In this case, 87 records of A. pictus and 103 of A. dentimitratus were used in the models (Supplementary Table S1). We analysed the composition of the data of both species and their accumulation over time through trend lines and linear regressions. 2.2. Variable Selection. We modelled the suitability of the territory of A. dentimitratus and A. pictus only in the Iberian Peninsula and North Africa because both species occur in these areas. Climatic data was derived from the 19 bioclimatic variables from the WorldClim database version 2.1 ([32]; http://www.worldclim.org) obtained at a spatial resolution of 30 seconds (1×1km). Of these 19 variables, we selected those that had the most biological significance on the species of Cynipidae (see [12]), making sure that there was no correlation between the variables. We discarded Bio8 and Bio9 because they showed unrealistic climatic 2 Journal of Zoological Systematics and Evolutionary Research patterns in some areas of the Iberian Peninsula, which can introduce bias in the models [33]. The other variables were analysed by a dissimilarity dendrogram using Euclidean distances (Supplementary Material, Figure S1), and we selected those above the threshold of 0.3 (i.e., those that showed less than 70% correlation). Within each cluster below the threshold, we chose the most biologically meaningful variable according to the ecology of the species (e.g., life cycle, phenology, and gall biology). When the meaning was not clear, we selected the most derived variables, i.e., those that referred to a specific period, as they were more informative than the remaining variables. Finally, for the (a) (b) Larval chamber Apical crown Middle crown Basal crown wrapping the acorn Narrowing (c) (d) (e) Larval chamber Apical crown Basal crown wrapping the acorn Narrowing (f) Figure 1: Andricus pictus galls on Quercus pyrenaica (a, b), schematic of the A. pictus gall (c), Andricus dentimitratus galls on Quercus sp. (d, e), and schematic of the A. dentimitratus gall (f). 3Journal of Zoological Systematics and Evolutionary Research final variable selection, we applied a variance inflation factor (VIF) [34] and only chose variables with a value lower than 5. The final variables selected for the analysis were Bio3, Bio4, Bio11, Bio16, Bio17, and Bio18 for A. dentimitratus and Bio2, Bio3, Bio10, Bio16, and Bio7 for A. pictus (Table 1). 2.3. Potential Distribution Models and Phylogeographic Hypotheses. The potential distribution of each species was estimated using species distribution models (SDMs) based on suitability and climatic variables, following the methodology described by Polidori et al. [35] and Gómez true [36]. We used the following algorithms: general linear model (GLM; [37]), general additive model (GAM; [38]), artificial neural network (ANN; [39]), classification tree model (CTA; [40]), random forest (RF; [41]), and maximum entropy (MaxEnt; [42]). To calculate pseudoabsence and background points, we first generated an environmental coverage model. This model assumes that a species can only be present in the areas where all the climatic variables are within the species tolerance range, estimated as between the maximum and the minimum value of each variable founded at the presence points of the species [11, 43]. Additionally, to assess host dependence of Andricus on species of Quercus, we combined the maps of the habitable area derived from the environmental coverage model with chorological distribution maps of Q. humilis for A. dentimitratus, and Q. faginea and Q. pyrenaica for A. pictus and examined their areas of overlap. Other host tree species were not considered due to the low spatial relationship between species occurrence and host distribution in the study area. For instance, although Q. robur is common and abundant in northern Iberia, A. dentimitratus is absent in this area (see Figure 2). The chorological maps were obtained from the European Atlas of Forest Tree Species published by the European Commission in March 2016 [44]. The overlapping areas were considered the species’habitable area. Background points were generated in the regions within the habitable area, whereas pseudoabsence points were generated in the areas where the variables were outside the tolerance range and/or where the Quercus species were absent. We split the presence and background data into two data sets, and we ran the models with 75% of the data in order to evaluate the final models using an external AUC (Area Under the receiver operating characteristic (ROC) Curve) evaluation procedure [45] with the remaining 25% of the data. The AUC was used to assess the discrimination capacity of the models: 0.5 indicates no discrimination, 0.6–0.8 indicates acceptable discrimination, and 0.8–0.9 indicates high discrimination [46]. We performed 100 replicates for each of the six algorithms (for a total of 600 individual models) and obtained a consensus model using the average of each individual model that passed the internal AUC evaluation (>0.7). Table 1: Data on the bioclimatic variables and altitude at the presence points of each species: mean, standard deviation (SD), and maximum (Max) and minimum (Min) values. A. dentimitratus A. pictus Mean SD Max Min Mean SD Max Min Bio1 = annual mean temperature 12.01 2.09 16.19 4.75 12.65 2.40 17.76 7.56 Bio2 = mean diurnal range (mean of monthly (max temp–min temp)) 9.23 0.94 11.03 6.11 10.35 1.49 14.38 6.55 Bio3 = isothermality (Bio2/Bio7) (×100) 35.65 2.43 41.55 26.76 37.93 2.81 44.28 32.20 Bio4 = temperature seasonality (standard deviation × 100) 607.57 50.35 779.55 461.31 609.02 81.89 710.03 327.20 Bio5 = max temperature of warmest month 26.34 2.10 30.82 20.04 28.48 2.39 34.12 22.70 Bio6 = min temperature of coldest month 0.47 2.35 6.30 -6.20 1.16 3.00 8.28 -3.80 Bio7 =temperature annual range (Bio5-Bio6) 25.87 1.73 29.68 18.85 27.32 3.42 33.29 15.75 Bio8 = mean temperature of wettest quarter 12.61 3.50 19.60 1.93 8.23 2.44 13.89 1.98 Bio9 = mean temperature of driest quarter 12.98 8.26 23.73 0.18 20.02 3.58 24.81 3.30 Bio10 = mean temperature of warmest quarter 19.79 2.01 23.73 12.87 20.62 1.92 25.01 15.90 Bio11 = mean temperature of coldest quarter 5.09 2.36 10.26 -1.99 5.83 2.96 12.66 0.94 Bio12 = annual precipitation 771.43 156.28 1425.00 255.00 644.52 222.63 1388.00 380.00 Bio13 = precipitation of wettest month 95.77 21.55 189.00 31.00 90.34 38.56 212.00 44.00 Bio14 = precipitation of driest month 33.47 12.56 66.00 8.00 12.87 6.11 29.00 1.00 Bio15 = precipitation seasonality (coefficient of variation) 29.08 8.37 59.07 13.60 46.47 12.21 75.66 30.31 Bio16 = precipitation of wettest quarter 254.79 53.84 506.00 84.00 251.56 107.82 599.00 124.00 Bio17 = precipitation of driest quarter 127.96 40.41 236.00 34.00 57.51 19.64 97.00 14.00 Bio18 = precipitation of warmest quarter 165.48 52.61 251.00 43.00 62.87 21.37 130.00 22.00 Bio19 = precipitation of coldest quarter 180.26 60.40 387.00 63.00 230.21 117.15 599.00 78.00 Altitude 568.81 369.87 1955.00 4.00 832.24 387.30 1717.00 47.00 4 Journal of Zoological Systematics and Evolutionary Research We verified the relationship between the presence of each species and the values of the variable that most influences the distribution of the species. For this purpose, we used an ANOVA to compare the values of the most important variables at the presence and pseudoabsence points. Finally, to discuss the phylogenetic context inferred from the SDMs, we made a series of maps showing the distribution of the host species of Quercus on which the analysed species depend: Q. pyrenaica,Q. faginea,Q. humilis,Q. suber, and Q. cerris. A. dentimitratus A. pictus Quercus faginea Quercus humilis Quercus pyrenaica Quercus robur (a) A. dentimitratus A. pictus Quercus cerris Quercus suber (b) Figure 2: Occurrence data of A. dentimitratus and A. pictus across Europe and in the Iberian Peninsula, and the distribution of host tree species of the parthenogenetic (a) and sexual (b) generations. 5Journal of Zoological Systematics and Evolutionary Research The variable selection process, SDMs, and their evaluation and statistical analyses were all performed in R 4.0.5 [47] using RStudio 1.4.1106 [48] and the packages HH version 3.1-43 [49], biomod2 version 3.1-64 [50], raster version 2.0-12 [51], and ggplot2 [52]. The maps, environmental coverage models and background, and pseudoabsence points were generated in ArcGIS desktop 10.6.1 [53]. 3. Results 3.1. Analyses of the Occurrence Data. The occurrence data for A. dentimitratus were obtained mostly from georeferenced databases associated with citizen science platforms, whereas those for A. pictus were mostly from bibliographic sources (Figure 3(a)). The data on A. dentimitratus are more recent than those on A. pictus (mean = 2008:56,SD = 13:75 vs. mean = 1984:04,SD = 32:49). For A. dentimitratus, the data follows two trends: one before 2008 (R2=0:8294) indicating the accumulation of about two new records each year and another one (R2=0:8367) indicating the accumulation of around 10 records each year (Figure 3(b)). This difference is due to the emergence of virtual citizen science platforms at the end of the 2000s, which have facilitated the acquisition of new occurrence records. According to the exponential trend of accumulated data for A. pictus (R2=0:8903, calculated using data from only the last 50 years, to avoid a distortion that would be caused by the lack of records from 1912 to 1975), around two new occurrences were registered each year. The records for A. dentimitratus were from throughout Europe, particularly Austria, France, Italy (including Sicily and Sardinia), and northeastern Spain (Catalonia) (Figure 2). The species has been cited in more countries; however, these records were not georeferenced and thus excluded from this study. The occurrence data for A. pictus were mainly restricted to Spain (except the northeast area), Portugal, and North Africa (Morocco, Algeria, and Tunisia). 3.2. SDMs of A. dentimitratus and A. pictus and Overlapping Areas. The consensus models generated for A. dentimitratus and A. pictus (Figure 4) show a complementary distribution in the Iberian Peninsula. While A. dentimitratus is restricted to the region north and northwest of the Ebro valley, and also in southern France, A. pictus is distributed across the Iberian, Central and Baetic systems, and the central and coastal region of Portugal and North Africa, especially in mountainous regions. The AUC values of the external evaluation of the consensus models were greater than 0.9 (0.997 for A. dentimitratus and 0.92 for A. pictus), indicating their high capacity to discriminate between presences and absences. Analysis of the bioclimatic variables showed significant differences between the habitable areas of the two species (Table 1). The most important variables in the model for A. dentimitratus were Bio18, precipitation of warmest quarter (mean contribution = 61:28%) and Bio17, precipitation of driest quarter (mean contribution = 24:55%); in the model for A. pictus, Bio10, mean temperature of warmest quarter (mean contribution = 56:67%) and Bio 17, precipitation of driest quarter (mean contribution = 37:78%) (Table 2). We also observed significant differences in these variables between high and low suitability areas (Figure 5(a)–5(c)). According to the comparison of Bio17 as a relevant variable in the models of both species, A. pictus prefers areas with low precipitation in the driest quarter (Figure 5(d)). With the obtained models, we observed spatial overlap between the potential distributions of the gall wasp species and that of the Quercus trees upon which the parthenogenetic generation develops (Figure 2(a)). Specifically, the high suitability areas predicted for A. dentimitratus overlap with the distribution of Q. humilis, and those areas for A. pictus, with that of Q. faginea or Q. pyrenaica. 4. Discussion 4.1. Species Distribution Models. The most influential bioclimatic variables in the SDM for A. dentimitratus were precipitation of the warmest quarter (Bio18) and precipitation of the driest quarter (Bio17). This species’occurrences were associated with high values of the variables (p<0:0001, see Figures 5(a), 5(b) and 5(d)), indicating that it prefers climates with less summer drought. The oak wood forests of Q. humilis in Catalonia (northeastern Spain) where A. dentimitratus is highly abundant are characterised as having a climate intermediate between Mediterranean and Atlantic, with characteristics of each climate type. For A. pictus, the most important variable was the mean temperature of the warmest quarter (Bio10), indicating the species prefers milder temperatures (p<0:0001, see Figure 5(c)). This finding is consistent with its presence at higher altitudes and with the climate preference of its host oaks: a mountain climate with strong winter frosts and high summer temperatures (supra-Mediterranean areas) [54]. The AUC of the A. dentimitratus model was only slightly higher than that of the A. pictus one (0.997 vs 0.92, see Figure 4), indicating the two models are qualitatively similar despite important differences between the characteristics of the data used for each. For instance, the occurrences of A. dentimitratus were more numerous and recent than those of A. pictus because they were mostly from virtual citizen science platforms (see Figure 3(a)), which have become enormously useful data sources for species distribution modelling studies (e.g., [12, 35, 55]). This difference is most evident in the data accumulation trend line observed for A. dentimitratus (see Figure 3(b)), which was very similar to that of A. pictus up until 2010 when the amount of data started to increase dramatically, coinciding with the growth of these platforms during the last decade. Considering the wider distribution area of A. pictus, one would expect that its records would also greatly increase on these platforms. A possible explanation for the higher abundance of A. dentimitratus records in the citizen science databases may be that the number of active users is higher in the Iberian northeast compared with the other regions. Moreover, A. pictus has been generally less well studied than A. dentimitratus, particularly in recent decades with most studies of the species having been published between 1970 and 1990, mainly by Nieves-Aldrey (e.g., [1, 17–24]). The occurrence data of A. 6 Journal of Zoological Systematics and Evolutionary Research pictus were so scarce in both the citizen science databases and the literature that we had to rely on older records, including some observations from the early 20th century [31], that were restricted to specific territories. Data older than 50 years may be uninformative, or worse, misleading, with respect to the bioclimatic variables as climatic conditions may have changed significantly since that time. For instance, we might have inferred the presence of the species in places where it may no longer be able to inhabit. Nevertheless, differences between the occurrence data used for 26 39 Data source A. dentimitratus 19% 12% 69% 145 Data source A. pictus 38 36% 67 63% 1 1% Bibliography Citizen science Other Bibliography Citizen science Observation (a) Accumulated data Observations Year 1905 1898 1912 1919 1926 1933 1940 1947 1961 1954 1968 1975 1982 1989 1996 2003 2010 2017 2021 y = 1.6509x – 3215.2 R2 = 0.9071 Observations 0 20 40 60 80 120 100 140 Date of the observations A. pictus Year 1980 1982 1985 1987 1989 1993 1998 2002 2005 2009 2011 2013 2015 2017 2019 2021 y = 3.5301x + 3.7842 R2 = 0.917 y = 12.591x + 34.576 R2 = 0.887 Observations 0 50 100 150 200 250 Date of the observations A. dentimitratus (b) Figure 3: Georeferenced occurrence records according to source (a) and date (b). In (b), both yearly observations and accumulated data and associated trend lines are shown. 7Journal of Zoological Systematics and Evolutionary Research High : 0.925 Low : 0.002 0.0 0 2 4 6 8 10 0.2 0.4 0.6 0.8 0.0 0.0 0.2 0.4 0.6 0.8 1.0 0.4 AUC = 0.997 0.8 0.0 0.2 0.4 0.6 0.8 Absence Presence (a) High : 0.836 Low : 0.003 0.0 0.0 1.0 2.0 3.0 0.2 0.4 0.6 0.8 0.0 0.2 0.4 0.6 0.8 Absence Presence 0.0 0.0 0.2 0.4 0.6 0.8 1.0 0.4 0.8 AUC = 0.92 (b) Figure 4: Habitat suitability models for A. dentimitratus (a) and A. pictus (b). Under each map: a graph showing the number of occurrences (red line) and pseudoabsences (blue-dashed line) according to the habitat suitability predicted by the consensus model (left), a boxplot of presence (red) and pseudoabsence (blue) according to the habitat suitability (centre), and a representation of the AUC of the consensus model (right). 8 Journal of Zoological Systematics and Evolutionary Research each model did not seem to affect the quality of the model, as both were equally robust according to the AUC. Previous studies of A. dentimitratus have suggested that its galls can be induced on Q. robur [2, 8, 25]; however, our results support the idea that the species develops its parthenogenetic generation exclusively on Q. humilis, not only in the Iberian Peninsula but throughout the rest of Europe. According to our findings, the species is absent in regions of the Cantabrian coast and the Pyrenean foothills where climatic conditions are favourable for the species and where Q. robur is abundant, (see Figure 2(a)) but Q. humilis is rarely found [56, 57]. All records of the species on Q. robur are Table 2: Contribution of each of the selected variables to the final distribution models. A. dentimitratus A. pictus Bio3 Bio4 Bio11 Bio16 Bio17 Bio18 Bio2 Bio3 Bio10 Bio16 Bio17 GLM 0.85 0.14 0.33 5.90 0.00 97.77 0.22 15.93 98.55 0.11 35.30 ANN 2.19 10.29 2.09 14.93 21.86 70.51 6.46 12.17 20.11 58.08 71.33 CTA 0.00 20.83 0.00 4.47 69.94 15.16 0.48 5.71 64.17 9.72 32.56 RF 0.70 3.97 1.12 5.40 12.48 16.15 11.91 20.87 24.43 10.66 20.47 MAXENT 4.19 8.89 9.82 12.18 21.62 81.43 11.11 27.70 42.31 10.10 28.76 GAM 18.70 9.10 12.45 33.49 21.42 86.67 5.13 15.24 72.48 22.73 38.27 Mean 4.44 8.87 4.30 12.73 24.56 61.28 5.89 16.27 53.67 18.57 37.78 Values are represented as percentages. Variable abbreviations: Bio2: mean diurnal range; Bio3: isothermality; Bio4: temperature seasonality; Bio10: mean temperature of warmest quarter; Bio11: mean temperature of coldest quarter; Bio16: precipitation of wettest quarter; Bio17: precipitation of driest quarter; and Bio 18: precipitation of warmest quarter. Occurrences 0 50 100 150 Precipitation of warmest quarter 200 250 p < 0.0001 A. dentimitratus Pseudoabsences (a) Occurrences 0 50 100 150 Precipitation of driest quarter 200 250 p < 0.0001 A. dentimitratus Pseudoabsences (b) Occurrences 15 20 25 Temperature of warmest quarter 30 p < 0.0001 A. pictus Pseudoabsences (c) 50 100 150 Precipitation of driest quarter 200 p < 0.0001 A. dentimitratus A. pictus (d) Figure 5: Differences in the values of the most important variables for the two species according to the degree of habitat suitability: high (occurrences) and low (pseudoabsences). (a) Bio18 (precipitation of the warmest quarter), A. dentimitratus; (b) Bio17 (precipitation of the driest quarter), A. dentimitratus; (c) Bio10 (mean temperature of the warmest quarter), A. pictus; (d) difference in the values of Bio17 (precipitation of the driest quarter) between the presence points of A. dentimitratus and A. pictus. 9Journal of Zoological Systematics and Evolutionary Research