Microhabitat use, daily activity pattern and diet of Liolaemus etheridgei Laurent, 1998 (Reptilia: Liolaemidae) in the Andean Polylepis forests of Arequipa, Peru
 
Irbin B. Llanqui1, Bryn Edwards3, Evaristo López Tejeda2
 
1 Escuela de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos, Av. Venezuela s/n, Cercado, Lima, Peru.
2 Escuela de Biología, Universidad Nacional de San Agustín de Arequipa, Av. Alcides Carrión s/n, Cercado, Arequipa, Peru.
3 Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, United Kingdom.
 
* Corresponding author: E-mail: illanquia@unmsm.edu.pe
 
Running head: Microhabitat use, daily activity pattern and diet of Liolaemus etheridgei
 
Abstract
This study describes the microhabitat use, daily activity pattern and diet of Liolaemus etheridgei Laurent 1998 in the El Simbral and Tuctumpaya Polylepisforests in Arequipa, Peru. El Simbral is a fragmented forest, whereas Tuctumpaya is unfragmented. Our results reveal that L. etheridgei shows no positive selection for any of the microhabitats we identified in Polylepis forests; on the contrary, it selects negatively against Polylepis trees and non-thorny bushes. The daily activity patterns indicate a bimodal pattern with peaks at 9:00-10:59 and 13:00-13:59 h. The diet of L. etheridgei consists mainly of plant material, and the most important animal prey category is Lygaeidae: Hemiptera, which is selected for positively. In particular, microhabitat selection varied for non-thorny bushes, which were selected negatively in the Tuctumpaya population but neither positively nor negatively in the El Simbral population. According to the proportions of plant material found, the L. etheridgei from El Simbral were found to be omnivorous, whereas the Tuctumpaya population was herbivorous. However, the percentage of plant material consumed in the El Simbral population was close to the critical value for herbivory-omnivory. We conclude that the three ecological aspects of L. etheridgei studied here are virtually identical in El Simbral and Tuctumpaya; therefore, this species is not affected significantly by the currentfragmentation of forest.
Keywords: Liolaemus montanus group, resource selection, bimodal activity pattern, herbivory, omnivore
 
Introduction
The Liolaemus genus consists of a large group of lizard species distributed from the central Andes of Peru to Tierra del Fuego in Southern Chile and Argentina, within an elevational range of 0 to 5000 m.a.s.l. (Lobo, Espinoza, and Quinteros, 2010; Abdala et al., 2019). Currently, there are thirty seven Liolaemus species recorded in Peru (Uetz and Hošek, 2022), and it is thought that this number will continue increasing (Gutiérrez et al., 2018). However, there is still a lack of ecological studies for most of these species, which limits our knowledge of their population status and how they should be managed. Some insights into the ecology of Liolaemus species in Peru come from short natural history notes in taxonomical studies (but see Llanqui, 2020; Olivera Jara and Aguilar, 2020). For example, Chaparro et al., (2020) report an observation of L. qalaywa eating the amphibian Pleurodema marmoratum and some larval insects; Huamani-Valderrama et al., (2020) report the consumption of coleopteran larvae and lepidopteran adults by L. anqapuka. Gutiérrez et al., (2018) reports the consumption of Carabidae: Coleoptera, Aranea and larvae by L. evearistoi. However, thorough ecological information is limited, especially when compared with studies on Argentinian or Chilean species. This is of particular concern for multiple Liolaemus species in Peru, such as L. anqapuka, L. annectens sensu lato, L. insolitus, L. polystictus, L. qalaywa and in general, the L. montanus species group, which are threatened permanently by agriculture, mining activities, urban expansion, habitat fragmentation and climate change (Aguilar et al., 2017; Aguilar-Puntriano et al., 2019; Chaparro et al., 2020; Huamani-Valderrama et al., 2020; Olivera Jara and Aguilar, 2020). Thus, a better understanding of the ecology of these lizards is necessary in order to propose efficient conservation actions.
 
Liolaemus etheridgei is distributed in the Arequipa and Moquegua Regions in southern Peru (Laurent, 1998; Llanqui, 2020), occupying the scrubland, shrubland, and Polylepis woodland habitats found there. The Polylepis woodlands are present throughout the distribution of L. etheridgei, comprising small areas of relictualwoodland. However, the role of these woodlands in sustaining L. etheridgei  populations is unclear (see Lloyd and Marsden, 2008). Of the nineteen Polylepisspecies recognised in Peru (Mendoza and Cano, 2011), thirteen (68%) have been included in a threatened category nationally (Decreto Supremo 043-2006-AG. Available from https://www.serfor.gob.pe/portal/wp-content/uploads/2016/03/D.S.-N-043-2006-AG-Aprueban-Categorizacin-de-Especies-Amenazadas-de-Flora-Silvestre.pdf [Accessed 24 April 2021]), urging further investigation into their decline. This study focused on two Polylepis rugulosa Bitter, 1911 (local name “Queñua”) relicts with differring levels of fragmentation: El Simbral and Tuctumpaya. El Simbral is a forest fragmented by the Moquegua-Arequipa Road and with smaller trees, while Tuctumpaya remains unfragmented and with taller trees. In this study we aim to describe three aspects of the ecology of L. etheridgei in Polylepis forests: microhabitat use, daily activity pattern and diet. We will also compare the differences in these aspects between the populations inhabiting fragmented and unfragmented forests. Differences in these aspects could indicate changes due to habitat deterioration. We also focus on these aspects as theirdivergence can lead to the ecological diversification of Liolaemus species (Jaksić, Núnñez, and Ojeda, 1980). For microhabitat use, we expect L. etheridgeipopulations to select Polylepis trees positively as they have commonly been thought to be an essential resource for this lizards (Gutiérrez et al., 2010). For the differences in daily activity patterns, we expect L. etheridgei to be active for longer in El Simbral due to low tree cover, allowing for more sunlight hours. Finally, we expect the diet to be more diverse in the Tuctumpaya population due to a diverse community of prey species in the unfragmented forest.
 
Material and Methods
Study area.
Fieldwork was conducted within the Polylepis forests (Polylepis rugulosa Bitter 1911) in the buffer zone of the Salinas y Aguada Blanca National Reserve (SABNR), Arequipa, Peru (Figure 1). The habitat is comprised of shrub-like vegetation, including Adesmia spinossisima, Baccharis spp., Chuqiraga rotundifolia, Mutisia acuminata, Parasthrephia lepidophylla, Senecio graveolens, S. nutans, while herbaceous species include Belloa piptolepis, Calamagrostis breviaristata, Festuca orthophylla, Gnaphalium purpureum, Sysirinchium chilense, Werneria aretioides (Mendoza, Cano, and Vento, 2010). We studied the lizard populations of two distinct areas, locally called “El Simbral” and “Tuctumpaya”. Both of the areas are located within the Pichu Pichu volcano's lowland area, which has been subject to various anthropogenic pressures. El Simbral is located in the Chiguata District in Arequipa. It is comprised of Polylepis forest fragmented by a road passing through the Moquegua and Puno Regions of Southern Peru (Figure 2). Tuctumpaya is located in the Pocsi District of Arequipa. In contrast, the Polylepisforest here is continuous, with a higher average tree height compared to El Simbral (Figure 2). The two areas provide an ideal comparison for studying the effects of fragmentation on the populations inhabiting them.
 
Methods
All data was collected between July and November 2013, within the dry season in the SABNR. We followed the Type I design for resource selection studies to collect data on the use and resource availability at the population level (Manly et al., 2002). For both El Simbral and Tuctumpaya, we installed 30 quadrats of 20×20 m, within a total area of ~475 Ha and between an elevation range of 3600 and 4200 m. These quadrats were randomly selected using QGIS version 1.8.0. In each quadrat, we determined the abundance of nine microhabitats: 1) Polylepis trees, 2) Scrubland, 3) Thorny bushes, 4) Non thorny bushes, 5) Rocks (Major diameter > 1m), 6) Small rocks (Major diameter ≤ 1m), 7) Uncovered land, 8) Dry organic matter, and 9) Nordenstamia longistyla. Nordenstamia longistyla is an Asteraceae shrub which was abundant in our study area. We estimated the coverage of each microhabitat in the quadrats using the Crown-Diameter method (Mueller-Dombois and Ellenberg, 1974) but instead using the ellipse equation (see García-De la Peña et al., 2012). Uncovered land coverage was then calculated by subtacting the total area of the quadrat from the combined area of the microhabitats. In each area, the microhabitat coverages were averaged. The final means were considered to be estimates of the relative abundances of each resource within the forests and, therefore, a measure of their availability (Manly et al., 2002).
 
L. etheridgei individuals were searched for using the Visual Encounter Survey (VES) (McDiarmid et al., 2012). Each quadrat was only surveyed once, and were randomly assessed during the daytime between 8:00-17:00h. In all quadrats, surveys were carried out by two observers who walked, one behind the other, in a zigzag pattern across the quadrat for 30±5 minutes. We recorded the microhabitat of where each individual was encountered. We also recorded the time of encounter and the activity of the individual. In order to assess diet, several individuals were collected by hand, euthanised with Halatal, fixed in 10% formalin and preserved in 70% ethanol. In addition, to study prey availability, we randomly installed six lines of pitfall traps (20 traps separated 10 m apart) in El Simbral and Tuctumpaya. The pitfall traps consisted of 1L plastic containers filled with 0.5L of water plus washing up liquid. Pitfall trap lines were left for 48h; then, the specimens were collected and preserved in 70% ethanol. Specimens collected were deposited in the scientific collection of the Herpetology and Entomology Departments of the Museo de Historia Natural de la Universidad San Agustín de Arequipa (MUSA) in Peru.
 
Laboratory
To study the diet of L. etheridgei, 33 adult specimens were dissected (El Simbral: 4 males + 10 females = 14, Tuctumpaya: 8 males + 11 females = 19), and their stomach contents extracted. Most of the stomach items were identified at Family level using specialised bibliography (Borror, de Long, and Triplehorn, 1981) and by comparison to reference material collected in the pitfall traps. However, some were identified until a higher taxonomical level (see Table 2). Amongst the contents, plant material was also present. Thus, all taxonomical items plus the plant material were considered prey categories like in similar lizard diet studies (e.g. Semhan, Halloy, and Abdala, 2013). Weight measurements were taken for each prey category using a digital scale (Anyload ES-203HA precision 200g x 0.001 g).
 
Data analyses
We assessed the microhabitat use with selection ratios: