Since Hutchinson’s concept of the environmental niche was proposed [1], how environment conditions determine species distributions has been one of the classic questions in ecology and evolutionary biology [2–5]. While it can be relatively difficult to measure a species’ fundamental environmental niche, the realized niches (ecological niches) can be estimated by empirical studies for most species [2, 6–10]. It has become increasingly important to describe and understand the extent to which species’ realized environmental niche can change rapidly (i.e., niche shift) or remain stable (i.e., niche conservatism) in the context of ongoing global change [4]. Thus, comparing the differences and dynamics of species’ environmental niches between different geographic areas or time periods, across a range of different taxa, is urgently needed to support a broader understanding of these phenomena, particularly for invasive species [2, 4, 7, 11].
Biological invasions provide good opportunities to explore the mechanisms important during colonization of new environments, and to investigate whether invasive species retain their niches when moving to new areas with environment conditions that differ from their native ranges [3, 12–14]. Previous reports on terrestrial plants, invertebrates, fish, amphibians, reptiles, and birds concluded that niche shifts are rare overall between native and invaded ranges [8, 13, 15–20]. However, the assumption of niche conservatism has been challenged by increasing evidence of shifts from several taxonomic groups in recent years (e.g., plants, insects, aquatic invertebrates, aquatic vertebrates, mammals) [15, 21–28]. The generality of conclusions about niche shift are unclear since studies of invasive species are heavily biased towards relatively few taxa (e.g., over 60% on insects and plants [11]). Understanding whether invasive species will typically be restricted in their new ranges by niche conservatism, or whether shifts may allow broader distributions is important to conservation efforts. As one of the major drivers of global change, introduction and spread of invasive species can trigger biodiversity loss and ecosystem disruption in various ways [25, 29]. This may include agricultural and forestry losses through reduced yields and pathogen transmissions [30], and negative effects on human well-being due to invasive vectors of human diseases (such as the mosquito Aedes aegypti [31]). Therefore, exploring how niche changes may be part of invasion processes, and thus being able to predict distribution and spread, is critical for evaluating the impacts of invasive species [25, 32]. Such studies can be key to informing spatial prioritization and management policies against biological invasions [33].
There are a number of considerations necessary when seeking to determine whether biologically relevant ecological niche shifts have occurred. First, the most commonly used metrics measuring differences between realized environmental niches so far are changes of the niche centroid, such as the Euclidean distance between the mean positions of the native and exotic niche spaces [21], and the change of niche overlap, such as Schoener’s D index [34–36]. However, an absence of a niche centroid shift does not necessarily indicate no real niche change [2]. A change of the niche envelope might occur without a shift in the centroid as a result of symmetric expansion, contraction, or displacement within environmental space. For example, a move to both warmer and colder or wetter and drier conditions may occur in such a way that the average temperature or precipitation niche positions keep stable [2, 17, 18, 21, 37, 38]. Thus, it is more appropriate to use more comprehensive measures of niche, such as Guisan et al. [2] unifying framework that decomposes niche change into three situations: unfilling (proportion of the native niche that does not overlap with the exotic niche), stability (proportion of the exotic niche overlapping with the native niche), and expansion (proportion of the exotic niche that does not overlap with the native niche). Second, demonstrating meaningful niche shifts may depend on choosing biologically relevant environmental variables for analysis [39, 40]. Third, mapping the availability of environmental conditions in geographic space could also be crucial for exploring niche differences between native and exotic ranges of an alien species [2]. Some environmental conditions that are common in the native range might be rare in the exotic range, and vice versa, because of the niche-biotope duality [41]. This may produce results that indicate niche shifts, but in reality this would arise from differences in the occurrence of conditions in different parts of the range, even if these do not impact the success of the species under study [5, 38]. Therefore, for a robust understanding of niche change of an invasive species, a standardized study should measure niche centroid dynamics and decompose the three niche-shift elements, simultaneously, while also considering the relative availability of multiple environment parameters with an understanding of how these are biologically relevant to the species under study. We used this approach to study the ecological niche of the invasive Australian redback spider (Latrodectus hasselti).
Generally, two approaches have been used in analyzing niche shifts of invasive species: comparisons of environmental attributes of native and exotic ranges based on direct observation of sites, and exotic ranges and detecting the overlaps of reciprocal predictions of native and exotic geographical distributions based on the outcomes of ecological niche models (ENMs; also named species distribution models, SDMs) [2, 4, 7, 34, 36, 42]. The first method uses univariate or multivariate tests or principle component analysis (PCA), is an ordinal way to quantify niche difference, and has higher accuracy overall than the second method. However, this approach provides a less mathematical representation of the niche than the ENM method, and does not allow optimization of weighting among factors based on their importance in the species’ ecology [2, 26, 42]. The ENM method predicts the invaded distribution with the model fitted in the native range, and vice versa, and then compares the situations of the two predictions [36, 42, 43]. It is a visualized way to detect niche difference and is particularly useful in assessing ENM transferability between native and exotic ranges [44]. Here, we take an integrated approach that utilizes the strengths and minimizes the weakness of each method by conducting ordinal analyses based on the results from ENMs to quantify ecological niche shifts [2, 34].
In addition to a focus on environmental factors, we also examine effects of human activities in our models. Human activities have obvious impacts on many ecological processes and distributions of animals and plants at different spatial and temporal scales, and this is particularly true for invasive species [25, 45–47], many of which are adapted to human-disturbed environments [47–50]. It has been suggested that alien species usually establish in disturbed areas at the early stages of the invasion process before range expansion [51]. Thus, anthropogenic impacts can affect the niche space of invasive species and should be identified as a promoter of invasion success under integrative scenarios [25, 45, 47]. There is some evidence that adding human footprint to climatic variables can improve predictions (e.g., in terrestrial plants [52]). Nevertheless, the role of human disturbance in mediating niche changes has received much less attention than other factors [18, 53].
In this study, we compared the ecological niche of invasive Australian redback spiders (L. hasselti, Thorell 1870, Araneae: Theridiidae) in its native and exotic ranges using an integrative approach that includes measures of human activities. The widow spiders (genus Latrodectus) include over 30 species found around the world [54] with medically important, neurotoxic venom [55], which makes invasive populations a particular concern [56]. Spiders in this genus are generalist predators that can survive for months without food, have a high reproductive output [57, 58], and may be easily introduced to new areas by human transport [59, 60], but nevertheless, to date only two species have been reported to be invasive (L. hasselti and L. geometricus [54]). L. hasselti is native to Australia, where it is common in urban habitats, and it has established populations in New Zealand (first recorded in 1981-1982 [61, 62]), Japan (first recorded in 1995 [63]), India [64], and Southeast Asia (the Philippines [65]), likely through international cargo shipments of steel, produce, or wood [66]. Here we examine the niche of native and exotic populations of L. hasselti using ENM and ordinal comparisons combined with considerations of environmental availability, and including analyses of niche centroid change, unfilling, stability, and expansion. In addition, we hypothesized that human impact supports the successful establishment of this anthropophilic species [66]. Thus, we also compare the influence of human disturbance on native and invasive populations.