Introduction

Spiders, order Araneae, are the main arthropod predators in the terrestrial ecosystems1. Spiders with nearly 50,000 species in 130 families are one of the most diverse groups of metazoan2. These venomous arachnids are proposed to be used for pest control in agroecosystems3. The spider venom and silk are subject of composition studies4 and application in pharmaceutical5, and technology of biomaterial6, respectively.

The Huntsman spiders, family Sparassidae, are large ambush predators partitioned in various habitats from humid rain forests to arid sand deserts. The family currently comprises 1290 described species in 89 genera2. The Stone huntsman spiders, genus Eusparassus Simon, 1903, composed of the largest predatory spiders (leg-span up to 14 cm) inhabiting xeric and subxeric regions of Africa, Mediterranean Europe via the Middle East to Central Asia7,8. Like other spiders, Eusparssus species are generalist predators but they mainly prey on insects and are able to subdue small vertebrates, indicating them as potential apex arthropod predators in the desert ecosystems8,9. Eusparassus represents one of the successful taxa from evolutionary perspective since it exists from at least 50 million years ago in the early Tertiary according to evidence of the amber fossil in Europe10. The genus currently comprises 30 species, majority of them are classified into six morphologic species-groups: the Eusparassus doriae, dufouri, jaegeri, vestigator, and walckenaeri8 while molecular phylogeny recovered and confirmed them as phylogenetically defined clades (exc. vestigator; no DNA data) based on four molecular markers11. The dufouri clade members are distributed in NW Africa and the Iberian Peninsula neighbouring the walckenaeri clade members which occur in Eastern Mediterranean, NE Africa, and the Arabian Peninsula. These two clades recovered as closely related taxa according to phylogenetic inferences11. The Eusparassus members and the entire family Sparassidae have never been the subject of any ecological niche modelling studies to date and our knowledge about factors that shaped their evolutionary history is scarce.

Every kind of living form has a range of specific environmental characteristics within which can have positive population growth; this range is called an ecological niche12. There are two kinds of ecological niches, the fundamental niche which is solely influenced by abiotic, and the realized one which is the result of interaction with biotic factors13. Species Distribution Modelling (SDM) methodologically uses a variety of statistical methods concerning large-scale climatic and topographic variables to estimate the ecological niche of taxa in relation to underlying environmental gradients14. These models are important tools in ecology, evolution and biogeography studies15,16,17,18. They have been used in studying niche evolution, niche dynamic, and niche comparisons in different taxonomic groups above and below species level15,16,19,20,21. Spiders have rarely been the subject of ecological niche modelling studies22,23. The previous SDM studies on spiders were geographically restricted to Europe and America devoting mainly to medically important biting spiders24,25,26,27, potentially model taxa to study biogeography and conservation biology28,29,30, and potentially endangered spiders31,32,33.

Here we applied the independent lines of evidence-based studies including morphology7,8 and molecular phylogeny11 integrated to geographical and environmental data to investigate the distribution modelling of two spider clades, E. dufouri clade (western Mediterranean Europe and Africa) and E. walckenaeri clade (eastern Mediterranean and partly in the Middle East and NE Africa), to test whether these two allopatric clades are different based on their ecological niches.

Results

Models performance

All niche models developed in this study performed well based on AUC metric (the dufouri clade’s ecological niche model: AUC = 0.976 ± 0.011, the walckenaeri clade’s ecological niche model: AUC = 0.982 ± 0.009, the dufouri clade’s climate niche model: AUC = 0.922 ± 0.016, and the walckenaeri clade’s climate niche model: AUC = 0.947 ± 0.021).

Ecological niche model

The model predicted that the environmental condition of the present distribution range of the dufouri clade is suitable for the walckenaeri clade members and vice versa (Figs. 1, 2). The potential distribution range of the walckenaeri clade was estimated much more widely extending into those of the dufouri clade in NW Africa and Iberia. On the other hand, the environmental condition in the western Mediterranean (Iberian and NW Africa), where the dufouri clade is distributed, is potentially appropriate for the walckenaeri clade (Fig. 2). Moreover, the eastern Mediterranean (Greece and Turkey) had suitable environmental conditions for the dufouri clade as well (Fig. 1).

Figure 1
figure 1

Distribution model of the dufouri clade. The distribution model was created using Maxent software 3.4.1 (https://biodiversityinformatics.amnh.org/open_source/maxent/) and mapped in QGIS 3.22.3 (https://www.qgis.org). The spider was photographed by Majid Moradmand.

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Figure 2
figure 2

Distribution model of the walckenaeri clade. The distribution model was created using Maxent software 3.4.1 (http://biodiversityinformatics.amnh.org/open_source/maxent/) and mapped in QGIS 3.22.3 (https://www.qgis.org). The spider was photographed by Majid Moradmand.

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Ecological niche across geographical and environmental spaces

Comparing the ecological niche of the dufouri and walckenaeri clades using two identity tests, the Schoener’s D and Warren’s I showed that their niches are different only in geographical space but are similar in environmental space (Fig. 3). Results of two background tests, the Schoener’s D and Warren’s I showed that ecological niches of the dufouri and walckenaeri clades are similar in both geographical and environmental spaces (Fig. 4).

Figure 3
figure 3

Results of identity test for the two clades (dufouri and walckenaeri) across the geographical and environmental spaces. Panels show histograms of 100 simulations of identity tests using two different metrics; the Schoener’s D and Warren’s I. Dotted lines indicate observed values. The figure is created using ENMTools 1.0.4 (https://github.com/danlwarren/ENMTools).

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Figure 4
figure 4

Results of background test for the two clades (dufouri and walckenaeri) across the geographical and environmental spaces. Panels show histograms of 100 simulations of background tests using two different metrics; the Schoener’s D and Warren’s I. Dotted lines indicate observed values. The figure is created using ENMTools 1.0.4 (https://github.com/danlwarren/ENMTools).

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Environmental variables and response curves

Results showed that the annual mean temperature (Bio1) with 44.9% contribution followed by the Normalized Difference Vegetation Index (NDVI) with 15.4% contribution were the most influential variables in shaping the ecological niche of the dufouri clade (Table 1). On the other side, for the walckenaeri clade, the Topographic Heterogeneity (TH) with 34% contribution and the annual mean temperature with 24.9% contribution were found to be the most important determinants of the ecological niche. Comparing the two clades, revealed that on one hand, the NDVI had much more influence on the dufouri clade (15.4%) than on the walckenaeri clade (3.6%); on the other hand, the TH had a greater impact on the walckenaeri clade (34%) than on the dufouri clade (7.9%). The response curves of the dufouri and the walckenaeri clades which were created using the environmental variables were similar and mostly unimodal (Fig. S1).

Table 1 Results of variable importance for the two clades (dufouri and walckenaeri).
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Climate change modelling

Results of predicting the impacts of climate change on the distribution of the two clades showed that climatically suitable areas will increase in the future (Fig. 5). Based on RCP 8.5 until 2070, climatically suitable habitats for the dufouri clade will increase between 16% (CCSM4) to 29% (MIROC5). Climatically suitable habitats for the walckenaeri clade will increase by 14% based on CCSM4 and while based on MIROC5 will remain stable under climate change (only 0.07% increase is expected). The response curves of the dufouri and the walckenaeri clades which were created using the bioclimatic variables were very similar and all unimodal (Fig. S2).

Figure 5
figure 5

Climate suitability maps for the dufouri clade (left) and walckenaeri clade (right) for current (A) and future climate (2070), under CCSM4 RCP 8.5 (B) and MIROC5 RCP 8.5 (C), representatives of each clade, habitus from frontal view (D). The suitability maps were created using Maxent software 3.4.1 (http://biodiversityinformatics.amnh.org/open_source/maxent/) and mapped in QGIS 3.22.3 (https://www.qgis.org). The spiders were photographed by Majid Moradmand.

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Discussion

Despite being the most diverse group of organisms, but the terrestrial arthropods have rarely been used in the species distribution modelling studies compared to other animal phyla27,34, since the scarcity of available distribution data and fewer taxonomic studies23. Here, we estimated the potential distribution of the two clades of the spider genus Eusparassus in the Western Palearctic using ecological niche modelling. The two Eusparassus clades: dufouri and walckenaeri, are diagnosed by morphology, and distributed allopatrically in different geographic regions8, indeed molecular phylogeny recovered them as distinct monophyletic clades11. The result of the current study revealed that the environmental factors are not drivers of their distribution patterns and no significant niche differentiation was observed between these two clades.

The majority of the SDMs are built at the species level. But it is recommended that the taxonomic resolution below or above species level should be considered in distribution modelling21,35,36. Recently, applying other evolutionary taxonomic units to estimate spatial modelling has been developing but under different terms. For instance, the lineage-level based distribution models or LDM37 used intraspecific lineages of various species (e.g.16,21,38), and spatial distribution modelling at the Clade-level, applied data of inter-and intraspecific sampling for spatial modelling (e.g.39).

Most studies showed that climatic variables are the main driver of organism distribution and diversification40. The distributions pattern of spider communities is mainly influenced by the environmental variables (e.g.41,42), however, niche conservatism was observed in closely related spider taxa26. Studies on the subterranean spiders showed partial niche overlap between close relatives33. Investigation on spider diversification during evolutionary time with conservative climatic niche but allopatric distribution pattern is also reported in the spider family Ctenidae30. Ecologically similar but geographically different taxa are found in different groups of organisms too39 including insects40,44,45 and vertebrates46,47.

The diversification in two allopatric Eusparassus clades without divergence in the ecological niche is reported here. Both Eusparassus clades: dufouri and walckenaeri are recovered highly monophyletic and closely related lineage to each other and partitioned into two distinct geographic regions. There is no evidence of sympatric distribution of the species of these two clades except occasional overlap in their neighbouring borders8. Our result revealed that the geography and niche conservatism are the main drivers of diversification of these clades.

The responses of the dufouri and walckenaeri clades to environmental variables were generally similar. However, the impacts of environmental variables on the clades seem to be different between the two clades. Importantly, the impacts of NDVI vs. TH on the clades are correspondence with the field observation of the clade members in their natural habitats. Some species of the dufouri clade were collected from vegetation and trees showing foliage and arboreal habitat preferences of this group (see references7,8). In contrast, the walckenaeri clade members are well known as inhabitants of stony deserts where they mainly build their silken retreats under stones8,9. These pieces of evidence explain why NDVI and TH have significant impact differences in the dufouri and walckenaeri clades, respectively.

The topology of the respond curves to environmental and bioclimatic variables showed some levels of the narrow range in the optimum and accordingly high limits of tolerance. Any change in the optimal environmental condition can lead to a decrease in taxa performance and reach the zone of intolerance48. These data indicate that the clades are environmental specialists and sensitive to change in the corresponding environmental variables. We found out that the two clades’ climatically suitable habitats will increase under future climate (the year 2070) but because the two clades are characterized with a narrow range in the environmental optimum, we believe that they are vulnerable to climate change. The environmentally specialist spiders have poorly developed abilities of dispersal49. While aerial dispersal or ballooning is an efficient mechanism in spiders1, there is no evidence of this behaviour in Sparassidae, indicating their limited capability of dispersal compared to ballooning competitors. The lack of dispersal performance would cost the clade members by limiting them from reaching a suitable habitat. Consequently, the ongoing climate change would negatively affect the clades, and probably eliminate them from their habitats producing them as “climate change losers”. Since these spiders are the apex predators in their environment, thus planning conservation strategies are highly recommended.

Methods

Distribution data

Species distribution data of the dufouri and walckenaeri clades (three species per each, total N = 6 species) reconstructed after molecular phylogenetics11 were applied for georeferencing. The locality data of these species occurrences were obtained from different sources, partially by direct sampling in the field using GPS but mainly from museum collection labels and publications7,8 and GBIF source50. For the collection labels without coordination (containing just the exact geographical names), the online global gazetteers version 2.2 (http://www.fallingrain.com/world) was applied to assign longitude and latitude (georeferencing) to each locality. All forms of geographic coordinates were converted into decimal degrees. The data were used to build up an occurrence database of the studied taxa (Fig. 6). We carefully checked the clades data to clean the duplicate records. Because the environmental data were available at 5 km resolution, therefore we thinned the dataset to ensure that observations were at least 5 km apart. Overall, 133 distribution records were used in ecological niche modelling of walckenaeri clade and 111 occurrence records for dufouri clade.

Figure 6
figure 6

Distribution records of the dufouri clade and walckenaeri clade on a topographic overview of the study area. Elevation map was obtained from the Shuttle Radar Topography Mission (SRTM) elevation model (https://srtm.csi.cgiar.org/) and mapped in QGIS 3.22.3 (https://www.qgis.org). The spiders were photographed by Majid Moradmand.

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Environmental predictors

In this study, to develop an ecological niche model for each clade we used a combination of variables reflecting climate, topography, and plant productivity (Table 2). Climate variables (annual temperature (Bio1) and annual precipitation (Bio12)) and Solar Radiation Index at ~ 5 km spatial resolution were downloaded from WorldClim51. A digital elevation model(from the Shuttle Radar Topography Mission (SRTM) elevation model)52 of the study area was used to generate two topography variables; elevation and topographic heterogeneity (TH) in the raster package53. Then, the normalized difference vegetation index (NDVI) was used as an indicator of plant productivity, which may reflect resource availability. To avoid multicollinearity problems among variable predictors54, a variance inflection factor (VIF)55 analysis was run using the ‘usdm’ package56. We found low collinearity among the environmental variables (annual temperature = 6.977, annual precipitation = 2.554, elevation = 3.323, topographic heterogeneity = 1.636 and NDVI = 2.637).

Table 2 The list of environmental variables used for modelling Eusparassus clades in the current study.
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Ecological niche modelling and niche comparison

There are various statistical methods for SDM, but one of the most frequently applied methods is the maximum-entropy approach implemented in Maxent57. The efficacy of Maxent is proved to be useful in estimating the suitable environmental distribution range of the organisms such as spiders (e.g.,24,28,29,58). In this study, we used the maximum entropy approach59 to develop the ecological niche of the two phylogenetically clades (dufouri and walckenaeri) across their distribution range. For our models, maximum iterations were set to 500, convergence threshold was 0.0001, and 10,000 background locations were chosen from the entire study area (Fig. 5). Maxent output format was set Cloglog which gives an estimate between 0 and 1 of probability of presence. We applied the cross-validation method in Maxent and distribution points were randomly split into 10 folds containing an equal number of occurrences, and training models were created by eliminating each fold in turn60. Models performance was assessed using the Area Under the Curve (AUC) metric of the Receiving Operator Characteristic (ROC) curve43,59,61.

Ecological niches of the two clades were compared using identity and background tests and two different metrics, the Schoener’s D62 and Warren’s I63. Further, to understand whether niche similarity is smaller or larger than expected with respect to the clades’ geographical distribution we performed a background test using the Schoener’s D62 and Warren’s I63. We compared the two clades' ecological niches in geographic and environmental space separately64.

Climate change assessment

We used the maximum entropy approach to predict the impacts of climate change on the two phylogenetically clades (dufouri and walckenaeri) across their distribution range. Two general circulation models of CCSM4 and MIROC5 for 2070 (average for 2061–2080) under the representative concentration pathways (RCP 8.5) were used. To predict the future distribution of the two clades the following nine bioclimatic variables were used: mean diurnal range (Bio2), temperature seasonality (Bio4), mean temperature of wettest quarter (Bio8), mean temperature of driest quarter (Bio9), precipitation of wettest month (Bio13), precipitation of driest month (Bio14), precipitation seasonality (Bio15), precipitation of warmest quarter (Bio18) and precipitation of coldest quarter for current (Bio19) and future climatic conditions. Bioclimatic variables for current and future climatic conditions were downloaded from Worldclim (https://www.worldclim.org/). In Maxent models, maximum iterations were set to 500, convergence threshold was 0.0001, and 10,000 background locations were chosen. To estimate the area of suitable habitats of each clade under current and future climatic conditions, we first converted continuous model outputs to presence/absence maps using the 10th percentile training presence threshold35,65,66. Then calculated area of suitable habitats under current and future climatic conditions using Raster package in R environment v. 3.4.3. Like ecological niche models for climate niche models, we applied the cross-validation method in Maxent and distribution points were randomly split into 10 folds containing an equal number of occurrences, and training models were created by eliminating each fold in turn60. Models' performance was assessed using the Area Under the Curve (AUC) metric of the Receiving Operator Characteristic (ROC) curve43,59,61.