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International Journal of Zoology and Animal Biology Research Article 14 min read

The Influence of Habitat on the Morphology of Liolaemus Lizards

Tulli MJ*
* Corresponding author
ISSN: 2639-216X  10.23880/izab-16000647  Received: January 10, 2025  Published: February 12, 2025
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Keywords
External Traits Apparatus Locomotor Substrate Liolaemus
Abstract

The morphology of an organism reflects its lifestyle (and that of its ancestors). Biomechanical theory predicts the existence of clear relationships between morphology and habitat use, given that the physical demands acting on the locomotor system are different in different habitats. Accordingly, the phenotype provides valuable information about the relationship between morphology and habitat structure and how these associations evolve as a response to changing environment. Here, present a study about relationship between morphology and habitat use in 37 species of Liolaemus lizards females and males that exploit different habitats. The main goal is to investigate if the general morphology of the locomotor apparatus (limbs and digits) in male and female Liolaemus reveals complex relationships with their ecology. The main results were head length and interlimb length, showed differences between sexes. Males presented bigger heads and females more distance between limbs. Meanwhile, for the habitat use arenicolous and terrestrial species showed shorter digits, arm, and crus. Arboreal species showed a larger interlimb. These results provide valuable insights into the morphological variation and sexual dimorphism within the Liolaemus genus.

Introduction

The general theoretical principle of adaptive variation based on natural selection [1] predicts that there should be a correlation between the design and ecology of organisms, such that the mechanical demands imposed by ecological factors are reflected in the morphological changes of the system involved. This is a generalized point of view that the morphology of an organism reflects its lifestyle (and that of its ancestors) [2, 3, 4]. Biomechanical theory predicts the existence of clear relationships between morphology and habitat use, given that the physical demands acting on the locomotor system are different in different habitats [5]. Accordingly, the phenotype provides valuable information about the relationship between morphology and habitat structure [6, 7, 8], and how these associations evolve as a response to changing environments [9, 10, 11].

Lizards exhibit diverse locomotor abilities, including swimming, running, jumping, and flying, essential for various physiological functions such as foraging, predator avoidance, and reproduction [12]. The success of these functions, and ultimately survival, depends on factors related to the locomotor system, such as running speed, endurance, and maneuverability [13, 14]. These factors are, in turn, influenced by a combination of characteristics, including morphology, biochemistry, and physiology, which vary significantly among organisms. This suggests that individual variation in locomotor ability can be both repeatable and heritable in some animal species (e.g., lizards, and mammals)  [15]. This highlights the importance of investigating the evolution of the locomotor system to understand the mechanisms driving the diversity of organismal functions. Traditionally, have been suggested that variations in locomotion modes are correlated with variations in the anatomy of the locomotor apparatus, specifically the limbs and digits [16, 17, 18, 19]. Based on this premise, several studies have explored the evolutionary relationships between morphology and microhabitat use in lizards Liolaemus [20, 21, 22, 23], Anolis [24], Sceloporines [25], Lacertidae [26], Niveoscincus [27, 28], Tropidurus [29, 30, 31], Gekkonidae [32, 33].

Species of the genus Liolaemus represent an excellent model system for exploring the relationships between morphology, ecology, and behavior. As one of the world’s most diverse and species-rich lizard genera, Liolaemus boasts approximately 285 described species [34]. Widely distributed across South America’s arid and semi-arid regions, from Tierra del Fuego in southern Argentina to central Peru, Liolaemus inhabits a broad range of habitats, including open. Terrestrial environments with rocky or gravelly surfaces, loose or firm aeolian sand, and even areas with denser vegetation such as grasses, herbs, shrubs, and trees [22, 23]. While some researchers posit that lizard morphology should exhibit significant interspecific variation to accommodate different ecological niches [24], Liolaemus species demonstrate remarkable morphological versatility. This adaptability enables them to thrive in diverse environments, effectively performing various tasks across different substrates, as long as they remain at ground level. However, studies on sexual dimorphism in size and shape within the genus are relatively scarce [35, 36, 37]. In this context, this study aims to investigate if the general morphology of the locomotor apparatus (limbs and digits) in male and female Liolaemus reveals complex relationships with their ecology. Additionally, the sexual dimorphism hypothesis was tested based on the main proposed hypothesis. Sexual selection theory predicts that larger males will have higher reproductive success due to advantages in competition for mates [38]. This is larger body sizes or allometric growth of structures used in male-male competition, such as large heads [39, 40]. For females, an alternative hypothesis is the fecundity advantage hypothesis. This proposes that female fecundity is correlated with body size, leading to selection for larger females [41, 42]. Thus the hypothesis of this work is hypothesize that male saxicolous species will exhibit more robust limbs and larger heads related to those inhabiting sandy habitats and females. Conversely, it is expected that females to display a more robust body and slender limbs. This research will contribute significantly to our understanding of Liolaemus, filling critical knowledge gaps regarding the relationships between morphology, locomotor abilities, and sexual dimorphism within this diverse genus.

Material and Methods

Data Collection

In this study, 761 adult specimens from 37 species, males and females of lizards belonging to the Lioalemus genus (Table S1). The species selected to explore a diversity of habitats arenicolous, saxicolous, arboreal, and terrestrial. All specimens belong to systematic collections and are in Table 1.

SpeciesHabitat use
Liolaemus albiceps2
Liolaemus baguali3
Liolaemus bibroni2
Liolaemus canqueli2
Liolaemus cei3
Liolaemus coeruleus3
Liolaemus crepuscularis2
Liolaemus cuyanus1
Liolaemus darwini2
Liolaemus dorbignyi4
Liolaemus elongatus4
Liolaemus escarchadosi3
Liolaemus fitzingeri2
Liolaemus goetschi2
Liolaemus hatcheri3
Liolaemus hermannunezi2
Liolaemus inacayali2
Liolaemus irregularis2
Liolaemus kingii3
Liolaemus kolengh3
Liolaemus koslowskyi2
Liolaemus kriegi4
Liolaemus lineomaculatus2
Liolaemus magellanicus2
Liolaemus melanops2
Liolaemus multimaculatus2
Liolaemus ornatus2
Liolaemus petrophilus4
Liolaemus pictus5
Liolaemus poecilochromus3
Liolaemus rothi2
Liolaemus salinicola1
Liolaemus sarmientoi2
Liolaemus scapularis1
Liolaemus tenuis5
Liolaemus xanthoviridis2
Liolaemus zullyi3

Table 1: List of the species used in this study. Numbers of the habitat use the literature cited and personal observations: 1: ar

Measurements

We used Twenty one linear measurements from the body and limbs of each specimen were taken (Table 2). The following morphological traits were measured directly from lizards using digital calipers (Mitutoyo CD-15B; ±0.01 mm) on the right side of the body: body size (snout-vent length – SVL), the distance between limbs (interlimb length – ILL), maximum head width (HW), head length (HL: from the anterior border of the external auditory meatus to the tip of the snout), tail length (LT: from vent to tail tip), and tail width (WT: at the base of the tail); and elements of fore and hind limbs [forelimbs: arm length (ArmL), antebrachium length (AL), dorsum of manus length (ML), dorsum of manus width (MW), and lengths of the digits (DI-II-III-IV and V); hind limbs: thigh length (TL), crus length (CL), foot length (FL; distance from the ankle until the base of the toes), and lengths of the toes 3 (T3), 4 (T4), and 5 (T5) (Table S1).

VariablesPC1PC2
ILL-0.0410.624
HL-0.37-0.615
HW-0.560.004
TL-0.222-0.497
TW-0.467-0.273
ArmL-0.7370.102
AL-0.6920.057
ML-0.5940.617
MW-0.5650.457
DI-0.7430.294
DII-0.8080.235
DIII-0.8980.127
DIV-0.7980.214
DV-0.7330.166
T3-0.815-0.208
T4-0.6-0.485
T5-0.777-0.134
TL-0.587-0.225
CL-0.711-0.485
FL-0.669-0.113

Table 2: Coefficients representing the association of each morphological variable with the first two principal components (PC). V

Statistical Analyses

The data was log-transformed and assessed using Kolmogorov-Smirnov tests to determine if the morphological variables met the normality assumption. Homoscedasticity was evaluated through a visual examination of the data. To account for size effects, size-corrected morphological variables were analyzed using multiple regressions with snout-vent length (SVL) as the independent variable and morphological data as the dependent variable. Residuals from this regression were then used in subsequent analyses. A Principal Component Analysis (PCA) was performed to reduce the dimensionality of the morphological data.

One-way ANOVA was conducted on each principal component with habitat use as a factor to test sex-specific habitat use. After that, a multivariate analysis of variance (MANOVA) was performed with those variables with high loading in the PCA using habitat use and sex as categorical variables. Then to determine which means are significantly different from one another a False Discovery Rate (FDR) was performed. This method increases the chances for detecting significant differences when multiple tests are applied simultaneously and tend to larger Type I error [43, 44]. All analyses were performed in the R Environment [45] using appropriate packages.

Results

All morphological traits correlated positively with SVL in males and females. Principal Component Analysis (PCA) revealed that the first two principal components (PC1 and PC2) captured a substantial portion of the morphological variation explaining 67% of the total variance. PC1, which accounted for 42.8% of the variation showed a strong and negatively association with digits and limb proportions (Table 1). PC2 explained 12% of the morphological variation, explaining a smaller proportion of the variance, was positively associated with interlimb and manus length and negatively with head length (Table 1).

The scores from each PC axis were used in a one-way ANOVA with habitat use as the main effect differed only on the first axis (PC1 F(1, 146)= 226.2, p= 0.00001; PC 2 F(1,

146)= 311.2, p= 0.90); showing a gradient of decreasing from terrestrial, and saxicolous with higher values to arenicolous until arboreal species with lesser values (Figure 1). The MANOVA analysis revealed significant sexual dimorphism in head length and interlimb distance (Sex: λ=0.34, F (60,

141.06) =1.022, p<0.44; Habitat use: λ=0.03, F (60, 141.06) =5.05, p<0.00). After MANOVA only two variables, head length and interlimb length, showed differences between sexes. Males presented bigger heads (λ=0.56, F (20, 52) =2.04, p<0.02; (Figure 2a) and females more distance between limbs (Figure 2b). However, using habitat use as a categorical factor arenicolous and terrestrial species showed shorter digits, arm, and crus. Meanwhile, the arboreal showed a larger interlimb.

Discussion

The results of this study provide valuable insights into the morphological variation and sexual dimorphism within the Liolaemus genus. As expected, a strong positive correlation was observed between morphological traits and SVL in both sexes, indicating significant allometric scaling. This pattern is consistent with previous studies on lizards and suggests that body size plays a crucial role in shaping overall morphology [12]. Males exhibited larger heads, which may be related to sexual selection or differences in feeding ecology. Females, on the other hand, had longer interlimb distances, which could be associated with reproductive strategies or differences in foraging behavior [46]. These findings support the hypothesis of sexual selection favoring larger males and potentially different ecological roles for males and females.

Furthermore, the results also highlighted the influence of habitat use on morphological variation. These findings underscore the importance of habitat-specific adaptations in shaping the morphology of Liolaemus lizards. Arenicolous and terrestrial species exhibited shorter digits, arms, and crus, while arboreal species had longer interlimb distances. Sandy substrates can be unstable and energy- consuming to traverse having shorter limbs and digits may provide better stability and traction, and reducing energy expenditure during locomotion provides greater agility and maneuverability, allowing these lizards to quickly change direction and avoid predators even in terrestrial environments involve navigating over uneven terrain, rocks, and vegetation. Also, shorter digits can provide a broader base of support when the lizard is pushing against the sand to move forward or backward. This enhances stability in the loose, shifting substrate and providing better leverage for excavating burrow construction. Scansorial species as those arboreal Liolaemus showed a relative longer body (IIL) that could allow them for greater reach, enabling the lizard to grasp trunks that would otherwise be out of reach. Also, reach into crevices and narrow spaces in tree bark to access insects and other prey. Additionally, longer digits could provide a larger surface area for interlocking grasping onto vertical surfaces as trunks of trees, enhancing stability and preventing falls, and could be used to pry open bark or leaves to uncover hidden food sources.

Conclusion

This study provides a comprehensive understanding of morphological variation and sexual dimorphism within the Liolaemus genus. The results emphasize the role of allometry, locomotor adaptations, habitat use, and sexual selection in shaping the morphology of these lizards. Further research is needed to investigate the functional significance of these morphological differences and their impact on the ecology and behavior of Liolaemus species.

References

  1. Darwin C (1859) On the Origin of Species by Means of Natural Selection. John Murray, London, UK.
  2. Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23: 347-361.
  3. Wainwright PC (1991) Ecomorphology: Experimental Functional Anatomy for Ecological Problems.  Am Zool 31 (4): 680-693.
  4. Wainwright PC, Reilly SM (1994) Ecological Morphology: Integrative Organismal Biology. Chicago: University of Chicago Press, pp 1-9.
  5. Herrel A, Meyers JJ, Vanhooydonck B (2002) Relations between microhabitat use and limb shape in phrynosomatid lizards. Biol J Linn Soc 77: 149-163.
  6. Vanhooydonck B, Irschick DJ (2002) Is Evolution Predictable? Evolutionary Relationships of Divergence in Ecology, Performance and Morphology in Old and New World Lizard Radiations. In: Aerts P, D’Août K, et al. (Eds.), Topics in Functional and Ecological Vertebrate Morphology. Shaker publisher, Maastricht pp: 191-204.
  7. Schulte II JA, Macey JR, Espinoza RE, Larson A (2000) Phylogenetic relationships in the iguanid lizard genus _Liolaemus_: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal. Biol J Linn Soc 69: 75-102.
  8. Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation in anoles. Berkeley: California University Press.
  9. Herrel A, Vanhooydonck B, Porck J, Irschick D (2008) Anatomical basis of differences in locomotory behavior in _Anolis_ lizards: a comparison between two ecomorphs. Bull Mus Comp Zool 159: 213-238.
  10. Stuart YE, Campbell TS, Hohenlohe PA, Reynolds RG, Revell LJ, et al. (2014) Rapid evolution of a native species following invasion by a congener. Science 346 (6208): 463-436.
  11. Donihue CM, Herrel A, Fabre AC (2018) Hurricane- induced selection on the morphology of an island lizard. Nature 560: 88-91.
  12. Foster KL, Collins CE, Higham TE, Garland T (2015) Determinants of lizard escape performance: decision, motivation, ability, and opportunity. In: Cooper WE, Blumstein DT (Eds.), Escaping From Predators: An Integrative View of Escape Decisions. Cambridge University Press; pp 287-321.
  13. Pianka ER, Vitt LJ, Greene HW (2003) Lizards: Windows to the Evolution of Diversity. In: 1st (Edn.), University of California Press.
  14. McGuire JA (2003) Allometric Prediction of Locomotor Performance: An Example from Southeast Asian Flying Lizards. Am Nat 161: 337-339.
  15. Van Berkum FH, Huey RB, Tsuji JS, Garland T (1989) Repeatability of Individual Differences in Locomotor Performance and Body Size During Early Ontogeny of the Lizard Sceloporus Occidentalis (Baird & Girard). Funct Ecol 3(1): 97-105.
  16. Collette BB (1961) Correlation between ecology and morphology in anoline lizards of Havana, Cuba and southern of Florida. Bull Mus Comp Zool 125: 137-162.
  17. Odendaal FJ (1979) Notes on the adaptative ecology and behaviour of four species of _Rhoptropus_ (Gekkonidae) from the Namib desert with special reference to a thermorregulatory mechanism employed by _Rhoptropus_ _afer_. Madoqua 11: 255-260.
  18. Russell AP, Bauer AM (1989) The morphology of the digits of the golden gecko, _Calodactylodes_ _aureus_ and its implications for the occupation of rupicolous habitats. Amphibia-Reptilia 10: 125-140.
  19. Carrillo de Espinoza N, Rothenstein D, Salas A, Werner YL (1990) Radiation and convergence among desert geckos: _Phyllodactylus_ species resembling both _Ptyodactylus_ and _Stenodactylus_. Amphibia-Reptilia 11: 275-284.
  20. Jaksic F, Nuñez H, Ojeda F (1980) Body proportions, microhabitat selection, and adaptative radiation in Liolaemus lizards in Central Chile. Oecología 45: 178- 181.
  21. Tulli MJ, Cruz FB, Herrel A, Vanhooydonck B, Abdala V (2009) The interplay between claw morphology and microhabitat use in neotropical iguanian lizards. Zoology 112: 379-392.
  22. Tulli MJ, Abdala V, Cruz FB (2011) Relationships among morphology, clinging performance and habitat use in Liolaemini lizards. J Evol Biol 24: 843-855.
  23. Tulli MJ, Cruz FB, Kohlsdorf T, Abdala V (2016) When a general morphology allows many habitat uses. Integr Zool 11: 483-499.
  24. Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation in anoles. Berkeley: California University Press.
  25. Miles DB (1994) Covariation between morphology and locomotor performance in sceloporine lizards. In: Vitt LJ, Pianka ER (Eds.), Lizard ecology: historical and experimental perspectives. Princeton: Princeton University Press, pp. 207-235.
  26. Melville J, Swain R (2000) Evolutionary relationship between morphology, performance and habitat openness in the lizard genus _Niveoscincus_ (Scincidae: Lygosomidae). Biol J Linn Soc 70: 667-683.
  27. Melville J, Swain R (2003) Evolutionary correlations between escape behaviour and performance ability in eight species of snow skinks (_Niveoscincus_: Lygosominae) from Tasmania. J Zool (London) 261: 79-89.
  28. Kohlsdorf T, Garland T Jr, Navas CA (2001) Limb morphology in relation to substrate usage in _Tropidurus_ lizards. J Morph 248: 151-164.
  29. Kohlsdorf T, James RS, Carvalho JE, Wilson RS, Silva MDP, et al. (2004) Locomotor performance of closely related _Tropidurus_ species: relationships with physiological parameters and ecological divergence. J Exp Biol 207: 1183-1192.
  30. Grizante MB, Navas CA, Garland T Jr, Kohlsdorf T (2010) Morphological evolution in Tropidurinae squamates: an integrated view along a continuum of ecological settings. J Evol Biol 3: 98-111.
  31. Zaaf A, Van Damme R, Herrel A, Aerts P (2001a) Spatio- temporal gait characteristics of level and vertical locomotion in a ground-dwelling and a climbing gecko. J Exp Biol 204: 1233-1246.
  32. Zaaf A, Van Damme R, Herrel A, Aerts P (2001b) Limb joint kinematics during vertical climbing and level running in a specialist climber: Gekko gecko Linneus, 1758 (Lacertilia: Gekkonidae). Belg J Zool 131: 173-182.
  33. Abdala C, Laspiur A, Scrocchi G, Semhan R, Lobo F, Valladares P (2021) Las Lagartijas de la Familia Liolaemidae: Sistemática, distribución e historia natural de una de las familias de vertebrados más diversa del cono sur de Sudamérica. RIL Chile.
  34. Valdecantos M, Lobo F (2007) Dimorfismo sexual en Liolaemus multicolor y L.irregularis (Iguania: Liolaemidae). Rev Esp Herpetol 21: 55-69.
  35. Villavicencio HJ, Acosta JC, Cánovas MG, Marinero JA (2003) Dimorfismo sexual de _Liolaemus pseudoanomalus_ (Iguania: Liolaemidae) en el Centro de Argentina. Rev Esp Herpetol 17: 87-92.
  36. Cabrera MP, Scrocchi GJ, Cruz FB (2013) Sexual size dimorphism and allometry in _Liolaemus_ of the L. laurenti group (Sauria: Liolaemidae): Morphologic lability in a clade of lizards with different reproductive modes. Zool Anz 252(3): 299-306.
  37. Cox RM, Skelly SL, John-Alder HB (2003) A comparative test of adaptative hypotheses for sexual size dimorphism in lizard. Evolution 57: 1653-1669.
  38. Petrie M (1992) Are all secondary sexual display structures positively allometric and, if so, why? Behaviour 43: 173-175.
  39. Fairbairn DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Ann Rev Ecol Syst 28: 659-687.
  40. Koslowski J (1989) Sexual size dimorphism: a life history perspective. Oikos 54: 253-256.
  41. Zamudio KR (1998) The evolution of female-biased sexual size dimorphism: a population-level comparative study in horned lizards (Phrynosoma). Evolution 52: 1821-1833.
  42. Weller HG, Tabor G, Jasak H, Fureby C (1998) A Tensorial Approach to Computational Continuum Mechanics Using Object-Oriented Techniques. Comp Physics 12: 620-631.
  43. Benjamini Y, Yekutieli D (2001) The Control of the False Discovery Rate in Multiple Testing under Dependency. Annals Statist 29(4): 1165-1188.
  44. R Development Core Team (2022) R: A language and environment for statistical computing Vienna (Austria): R Foundation for Statistical Computing.
  45. Kratochvíl L, Frynta D (2002) Body size, male combat and the evolution of sexual dimorphism in eublepharid lizards (Squamata: Eublepharidae). Biol J Linn Soc 76: 303-314.
  46. Martins EP, Labra A, Halloy M, Thompson JT (2004) Large-scale patterns of signal evolution: an interspecific study of Liolaemus lizard head bob displays. Behaviour 68: 453-463.
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@article{tulli2025,
  title   = {The Influence of Habitat on the Morphology of Liolaemus Lizards},
  author  = {Tulli MJ},
  journal = {International Journal of Zoology and Animal Biology},
  year    = {2025},
  volume  = {8},
  number  = {1},
  doi     = {10.23880/izab-16000647}
}
Tulli MJ (2025). The Influence of Habitat on the Morphology of Liolaemus Lizards. International Journal of Zoology and Animal Biology, 8(1). https://doi.org/10.23880/izab-16000647
TY  - JOUR
TI  - The Influence of Habitat on the Morphology of Liolaemus Lizards
AU  - Tulli MJ
JO  - International Journal of Zoology and Animal Biology
PY  - 2025
VL  - 8
IS  - 1
DO  - 10.23880/izab-16000647
ER  -