A high mountain lizard from Peru: The world’s highest-altitude reptile

Life at high altitudes is particularly challenging for ectothermic animals like reptiles and involves the evolution of specialised adaptations to deal with low temperatures, hypoxia and intense UV radiation. As a result, only very few reptile taxa are able to survive above 5,000 m elevation and herpetological observations from these altitudes are exceedingly rare. We report here an exceptional observation of a lizard population (Liolaemus aff. tacnae; Reptilia, Squamata) from the high Andes of Peru. During an ascent of Chachani mountain (6,054 m, 16°11'S, 71°32'W), we observed and documented photographically this species living between 5,000 and 5,400 m above sea level. Following a review of literature, we show that this is the highest known record of a reptile species.


Introduction
Adaptation to high elevation life in reptiles implicates different specialised anatomical and physiological strategies (Huey 1982;He et al. 2013;Reguera et al. 2014;Kouyoumdjian et al. 2019), which scientists are recently beginning to understand at the genetic level (Yang et al. 2014;Yang et al. 2015;Li et al. 2018). Factors identified as important in reptiles for allowing survival at the upper altitudinal limits relate to food availability and capacities for tolerating hypoxia and low temperatures (Navas 2002;Lu et al. 2018;Gangloff et al. 2019). Prior to this publication, the highest known altitude records for reptiles came from species in two lizard genera, Phrynocephalus (up to 5,300 m) from the Tibetan plateau and Liolaemus (up to 5,176 m) from the Andes (Zhao et al. 1999;Aparicio and Ocampo 2010;Li et al. 2017).
The South American genus Liolaemus constitutes one of the most diverse genera of reptiles known on Earth, with more than 270 species described to date Huamaní-Valderrama et al. 2020); it is distributed from the Central Andes in Peru to Patagonia in Argentina (Pincheira-Donoso et al. 2008;Aguilar et al. 2013;Abdala et al. 2020). This includes the coastal regions of southern Peru and northern Chile (Valladares et al. 2004;Villegas-Paredes et al. 2020), as well as southern Brazil (Verrastro et al. 2003) and demonstrates a broad adaptive radiation of the genus in the region . In Peru, 28 species in the genus Liolaemus have been described to date (Chaparro et al. 2020;Huamaní-Valderrama et al. 2020;Arapa-Aquino et al. 2021), although recent phylogenetic analyses have shown that this number is likely an underestimate, given the existence of several undescribed lineages or "candidate species" (Aguilar et al. 2017(Aguilar et al. , 2018Abdala et al. 2020;Huamaní-Valderrama et al. 2020).
of Arequipa in south-western Peru. At approximately 09:00 hrs (local time) and at an elevation of 5,000 m, we observed from a distance of approximately five metres two small lizards moving and then hiding between large rocks, making further observations difficult. Later, during the same day, between 10:00 and 12:00 hrs (local time), a total of ten lizards of the same characteristics were observed between 5,000 and 5,400 m of elevation (Fig. 1A), where they were moving amongst the rocks. One individual was photographed at 5,400 m elevation (Fig. 1B), with coordinates 16°10'57"S, 71°32'02"W (Fig. 2). The habitat at the site is characterised by large rocks on the mountain slopes and the almost complete absence of vegetation (Fig. 1A), with only small herbaceous plants growing near the protected underside of rocks. The lizards were exclusively saxicolous, being observed moving only on rocky substrate.
Based on the pattern, colouration and size (approx. 11 cm total length) of the observed animals, we consider them to belong to the alticolor-bibronii group of the genus Liolaemus. We provisionally assign this population to Liolaemus aff. tacnae, because of its similarity to the L. tacnae which inhabits Chiguata (4,000 m elevation), approx. 30 km SE of Chachani mountain (Aguilar et al. 2013). However, a more detailed analysis is needed, including use of morphological and/or molecular evidence, to determine with more confidence the taxonomic status of this high mountain population.
The present observations represent the highest documented record for the genus Liolaemus, surpassing by more than 200 m elevation the previous record holders:   Table 1. two Bolivian populations of Liolaemus reported between 5,060 and 5,176 m (Aparicio and Ocampo 2010). Тhis population of L. aff. tacnae represents the reptile species that lives at the highest altitude on Earth (Table  1), exceeding by 100 m the record documented for the Asian species Phrynocephalus erythrurus, which inhabits the Tibetan plateau between 4,500 and 5,300 metres elevation (Zhao et al. 1999;Li et al. 2017).
The ongoing global warming trend has probably facilitated the survival of L. aff. tacnae at this record high site. The genus Liolaemus is well-adapted to a broad range of environments (Pincheira-Donoso et al. 2015) and climate change is expected to favour the expansion of species at their upper altitudinal limits (e.g. Wilson et al. 2005, but also see Parmesan 2006 for exceptions). This is particularly true for ectothermic animals, such as the lizards, whose vital functions are known to be directly dependent on ambient temperatures (Sinervo et al. 2018).

Conclusions
We hope that this report will encourage future research into the physiological mechanisms that allow these animals to live at such extremely high elevations through adaptations to low temperatures and low oxygen availability (e.g. Bennett and Ruben 1975;Lu et al. 2015;Cordero et al. 2017;Gangloff et al. 2019).