Global Climate Change (GCC) is one of the most critical threats for global biodiversity with a profound influence on species’ range expansion and contraction (Bellard et al., 2014). Several responses have already been observed in biological systems (e.g., Martínez-Meyer, 2005; Tingley et al., 2009; Garcia et al., 2014); among others, it generates important changes in the patterns of distribution in both, space and time; inducing at best, shifts in latitudinal and altitudinal distribution of species, or, at worse, local or even total extinctions (Bellard et al., 2014). However, the responses to climate change are independent among species, and the impacts and extent of these predicted changes remain largely unknown for most of the species.

By studying the climatic requirement of a given species, it is possible to infer its potential sensitivity to GCC (Nori et al., 2016; Rinnan and Lawler, 2019). For example, the species’ breadth of the climatic niche could be seen as a measure of acclimation of the species to potential changes in local environmental changes. Also, the position (i.e., marginality) of the climatic requirements of the species in regard with the available climatic space could be an indicator of the probabilities to lose a portion of its climatic niche when a climatic change occurs; especially for those species with climatic requirements highly dissimilar to the mean conditions of the region as the most harmed (Araújo et al., 2006; Thuiller et al., 2011). Also, based on comparisons between the current climate and hypothetical future climate across the distribution of a given species, it is possible to infer the areas and magnitudes where the most remarkable exposition to climate change are expected, and so estimate the vulnerability of the species to these hypothetical climate scenarios (Rinnan and Lawler, 2019).

Another silent but substantial impediment to conserve biodiversity, yet little explored concerning its potential synergy with GCC, is the lack of knowledge of biodiversity (Hortal et al., 2015). Several clades of species remain unknown, generating a significant discrepancy between formally described species and the number of species that exist (Linnaean shortfalls). Also, many essential components related to the described species, such as their geographical distribution (Wallacean shortfall), or phylogenetic relationships (Darwinian shortfall) remain uncertain (Diniz-Filho et al., 2013; Hortal et al., 2015). The issue of species delimitation has been confused by a problem involving the concept of species itself, leading to decades of controversy concerning both the definition of the species category and methods for inferring the boundaries and numbers of species (De Queiroz, 2007). These knowledge and conceptual gaps limit the possibility to accurately assess the conservation status threat that species are really undergoing and, consequently, to effectively protect them (Nori et al., 2020; Rojas-Soto et al., 2010; Scherz et al., 2019).

It is essential to note that all these shortfalls in knowledge could be strongly related to the real vulnerability of the species to GCC. For example, the increase in the taxonomical/systematic knowledge of a given group through a phylogenetic revision (filling Darwinian shortfall) generally directly impacts the number of its species (Linnaean shortfalls). The splitting/synomizations of the species group generate immediate changes in species distributions (filling Wallacean shortfalls), which directly affect our knowledge on the species vulnerability and irreparability in terms of conservation (Scherz et al., 2019). Note that one of the possible consequences of these changes is a direct and measurable effect in the exposition of the new (currently updated) species to GCC, given for a possible increase in the marginality and decrease in their breadth climatic niches. This situation is especially worrying but unfortunately common in the “new world” biodiversity; in fact, in many developing countries, the “original/initial” species descriptions were based on huge unspecific field trips, where a large number of collected specimens were deposited in collections far from the collections sites and associated with inaccurate taxonomic descriptions from naturalists or general taxonomists. However, over the last few years, the accumulation of systematic, taxonomics and phylogenetic knowledge in diverse groups, hand in hand with the new and improved methodological approaches, triggered a cascade of changes characterized by an increase in the number of species’ groups. For example, among reptiles [e.g., Phymaturus (Lobo et al., 2019)], Amphibians [e.g., Hypsiboas (Funk et al., 2012)]; birds [e.g., Aulacorhynchus (Winker, 2016)], and mammals [e.g., Ctenomys (Parada et al., 2011)], just for cite a few recent examples where the phylogenetic analysis, have revealed the real complexity of speciation processes, and therefore an upgrade of the taxonomy, which has increased up to 100% the new species in the Neotropic.

Cascading taxonomy changes within a given clade generated by theoretical and methodological advances, now composed by a more significant number of species with narrow distributions, will generate important changes in the vulnerability to GCC than we initially thought and estimated for such given clade. This study aimed to test if gaps in the knowledge of taxonomic and systematic relationships inside clades could generate bias estimating of more accurate species vulnerability to climate change. Specifically, we investigated how the filling of Linnaean/Darwinian shortfalls in a given clade promote changes in the vulnerability of its species to GCC, due to inherent modifications on their niche’ breadths and marginalities. For that, used five well taxonomically studied groups of Argentinian lizards and estimated and compared their vulnerability to global climate change before and after their recent taxonomical radiation (as a product of the filling of Linnean shortfalls).

All ecological niche models showed good performance with AUC values that ranged between 0.744 (original Liolaemus fitzingerii in 1980) and 0.98 (current Phymaturus ceii) with SD=0.07. The models also performed satisfactorily under the pROC test, with an average of 1.71, and SD=0.20 (Table S1). For all groups, the original described species’ climatic niche breadth was significantly greater than the updated ones (W=131, P=0.0005). On average, the current species’ breadth of the climatic niche represents a 15% (SD=0.15) of the volume of the original described one (Table 1, Fig. 2).

Fig. 2.

Climatic niche breadth, shown as minimum volume envelopes (MVE) overlap for each species complex. The red MVE represents the original (former) species climatic niche breadth when the current species MVE are signaled with different colors. For all the cases, the environmental space is delimitated by PC1 on x-axis, PC2 on y-axis, and PC3 on z-axis. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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Niche marginality was significantly lower (W=27, P=0.0189) for the originally described species for the five analyzed species groups, being average between 20% to 78% more marginal for the current species’ niche than the original species’ niche (Table 1). The sensitivity was greater for current species than the original species (W=5, P=0.0006), ranging on average 3.2 times more sensitive (a comparison made between current species derived from Liolaemus anomalus and the original species) to 11.2 times more sensitive (a comparison made between current species previously confused with original P. palluma and the original species). Finally, species vulnerability was also significantly higher (W=2, P=0.0004) for the current species than for the originally described species, for both future climate scenarios, ranging on average from 59% greater for species derived from the original P. antofagastensis, to 177% greater for current species derived from the original P. palluma (Table 1, Fig. 3).

Fig. 3.

Relative vulnerability to GCC. The vulnerability is the average of the two selected scenarios (GCMs; BCC-CSM1-1 and NIMR-HADGEM2-AO) for the year 2050 and RCP of 6.0. The horizontal dashed line represents the estimated vulnerability to GCC of the original species, the green bars shown the relative vulnerability to GCC for the current species with the original ones. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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Our results show that considering a species complex as a single taxon implies underestimating of the species’ vulnerability to GCC; this fact logically should have a direct impact on the species risk assessment (Scherz et al., 2019). This underestimation of vulnerability to GCC occurs when a complex of species is considered as a single entity, with a consequent greater geographical distribution (in many cases including all the distributions of current derived species). This fact not only implies a greater distribution, but in general a greater volume of its climatic niche, which ultimately translates into an apparent lower vulnerability to GCC. Conversely, if a complex is split in several species (lineages), the original niche is also fragmented, and the resulting niches become logically smaller and in more marginal positions regarding the available conditions. This reduction implies a lower capability of the derived (updated) species to changing conditions than was estimated for the species’ complex as a whole (and based on the same geographic information).

The need for splitting complexes of species resides in the accumulation of evolutionary/phylogenetic knowledge (Ryder, 1986; Zink, 2004) that fills the Darwinian and Linnaean shortfalls on poorly studied groups, and their updating to cover the Wallacean shortfalls (sensu Hortal et al., 2015) eventually. The recognition of independent lineages based on new sources of evidence, methodologies, and theoretical advances provides a rational basis for prioritizing taxa for conservation effort (Ryder, 1986; Scherz et al., 2019). Almost three decades ago, Moritz (1994) pointed out that the overriding purpose of defining evolutionary lineages is to ensure that historical heritage is recognized and protected and that the evolutionary potential is maintained. He particularly stated that “For a given set of populations, we cannot predict future outcomes, but we can make inferences about the evolutionary past.” However, nowadays, we can make such future inferences via Ecological Niche Modelling. We also have the opportunity to evaluate the potential effect of GCC over independent lineages (previously hidden by Linnaean shortfalls within traditional taxonomy); these techniques are helping us to achieve new conservation approaches and, accordingly, improve the recognition of conservation risk status of species.

Also, our results provide evidence that when the phylogeny is poorly studied, the current formal names of the species could be a “pitfall” regarding their risk assessment (and conservation status). The delimitation of the species’ distribution areas should be based on a taxonomic update under phylogenetic analysis, following new theoretical and methodological perspectives, and using a more significant number of characters and specimens across geography. Therefore, despite the extent of the distribution areas being a critical aspect of determining the species’ vulnerability (e.g., IUCN, 2020), it should not be a decisive criterion until there is such an update on the species’ distribution areas. The current existence of Darwinian and Linnaean shortfalls along diverse regions and biodiversity groups should encourage to fill urgently - or at least estimate- such gaps, as an essential to accurate decision-making. In light of this, we are warning about the current application of a weak criterion on these regions and taxa, which could determinate a very high extinction risk for many species, even those not yet described by science.

A small niche breadth indicates more specific climatic requirements and so low adaptability to novel conditions. Besides, a high niche marginality implies that a given species inhabits climatic regions with a higher possibility of disappear under changing conditions. For that, those species with greater niche marginality and a smaller niche breadth are the most vulnerable to the effect of GCC (Araújo et al., 2006; Nori et al., 2016; Thuiller et al., 2011), this had never been contextualized in regard of the most important knowledge shortfalls in biogeography. We pinpointed that, as Darwinian and Linnaean knowledge gaps are filling, new species emerge based on the split from the original ones. These new species are prone to have not only smaller distributions but narrower and more marginal niches, which automatically allow identifying their low capacity to face new environmental conditions, and therefore, higher vulnerability to the effect of GCC. This analysis highlights the importance of systematics, taxonomy, and biogeography in the species risk assessments (Nori et al., 2020, 2018; Scherz et al., 2019).

As stated, in many cases, the updated current species comes from the advances in the phylogenetic knowledge of the groups (instead of field discoveries; e.g., Parada et al., 2011; Winker, 2016; Lobo et al., 2018), and the lack of this phylogenetic knowledge reach a significant underestimation of the species vulnerability to GCC. It is important to note that science only knew (i.e., was described) a small portion of the existing species (Hortal et al., 2015; Mora et al., 2011), and we do not have a compressive knowledge of phylogenetic relationships among most taxonomical groups of known species (Diniz-Filho et al., 2013). The underestimation of the species’ vulnerability to GCC is a common currency across the world. These are and will become more common scenarios across the globe for most taxa (i.e., groups with a lack of in-depth taxonomical and phylogenetic studies). Thus, they might be significantly exacerbated in the most biodiverse and developing countries, where there are still enormous knowledge gaps, and taxonomical arrangements have become frequent in recent years (Funk et al., 2012; Lobo et al., 2019; Winker, 2016). It is also logical to think that underestimating climate change vulnerability is superior in low or not well-studied groups, such as arthropods or deep-ocean biodiversity, for whom knowledge gaps are presumably much more significant than the examples here addressed (James Griffiths et al., 2014). We can conclude that the explicit recognition of the real components of biodiversity, and consequently the filling of knowledge shortfalls, will be increasingly significant for the conservation of natural populations (Nori et al., 2020, 2018; Scherz et al., 2019), including the estimation of their vulnerability to GCC.

None.