Skip to main content
NCBI home page
Zoological Studies logoLink to Zoological Studies
. 2015 Feb 2;54:e24. doi: 10.1186/s40555-014-0099-y

Geometric morphometric analysis of the head of Microlophus atacamensis (Tropiduridae) in a latitudinal gradient

Soledad Ibáñez 1,*, Marcela A Vidal 1, Juan Carlos Ortiz 2, Fernando Torres-Pérez 3
PMCID: PMC6661439  PMID: 31966111

Abstract

Background: Clinal variation is defined as gradual variation in a character associated with geographic distance among sites. Microlophus atacamensis is a medium large lizard species which inhabits the intertidal zone of northern Chile, distributed from Antofagasta (23° 39′ S) to Arrayán, La Serena (29° 41′ S) in a gradient which could show clinal variation. Geometric morphometrics analyzes differences in shape independent of size; information about shape allows a more complete biological interpretation than information on morphological variation. This studyevaluated clinal variation in the head shape of M.atacamensis fromfive localities (Antofagasta, Paposo, Pan de Azúcar, Caldera, and Tres Playitas) using dorsal and lateral views, comparing form variation with latitudinal distribution. The heads of adults collected were photographed in lateral and dorsal views.

Results: The analysis did not find significant differences in form among the five localities, in contrast to the proposal of earlier studies, and no differences were recorded between the sexes. Possible reasons why these populations are not differentiated in the latitudinal gradient are discussed.

Conclusions: Our results show that there are no differences between the studied, among the explanations are that populationsof this species are subjected to similar environments that promote convergence of the structures analyzed.

Keywords: Atacama Desert, Lizard, Shape morphometrics, Head

BACKGROUND

The genus Microlophus (Squamata: Tropiduridae) has a disjunct distribution, rare in terrestrial vertebrates (Benavides et al. 2007). Twenty-one species are recog- nized; nine of these are found only in the Galapagos Islands, while the remainder are distributed along the coast and interior deserts of western South America, from southern Ecuador to northern Chile (Etheridge and De Queiroz 1988; Frost and Etheridge 1989; Frost 1992; Benavides et al., 2007). The species of the genus Microlo- phus form a monophyletic group of lizards, character- ized by apical disks in the hemipenis (Frost 1992). According to Dixon and Wright (1975), two groups are recognized in the genus whose monophyly is justified by characters of body scales and skin folds, occipitalis and peruvianus; this was later corroborated by Frost (1992) with osteological characters. Two subgroups are recog- nized within the peruvianusgroup; the first group groups interior species which feed on insects and terres- trial plants with no direct ecological relation to the intertidal zone: M. peruvianus, M. thoracicus, M. there- sioides, M. tigris, M. yanezi, M. theresiae, and M. tarapa- censis (Ortiz and Serey 1979); the second group is composed of intertidal species which feed on crusta- ceans and algae: M. heterolepis, M. atacamensis, and M. quadrivittatus (Ortiz and Serey 1979). In Chile, this genus is currently represented by M. atacamensis, M. quadrivittatus, M. yanezi, M. tarapacensis, M. there- sioides, and M. heterolepis (Ortiz 1980a), which are dis- tributed from Arica to Arrayán (La Serena) (Donoso- Barros 1949; Sepúlveda et al. 2006).

According to Donoso-Barros (1960), the origin of the genusMicrolophusin Chile began with M.peruvianus, which would have descended southward along the coast and then extended its range to the interior desert by way of the valleys. Ortiz (1980a) followed this logic but added that the distribution to the interior desert would have occurred through the Pampa del Tamarugal. Later, using isoenzyme data Victoriano et al. (2003) proposed that an ancestral lineage advanced from Peru towards the coast and later diverged into two groups; one was the ancestor of the M. quadrivitattus-M. theresioides group (one of whose subgroups still inhabits the interior desert) and the other was the ancestor of M. atacamen- sis. Based on a molecular phylogeny of data from many genes, Benavides et al. (2007) proposed that the origin of the Chilean clade was a migration from Peru to the in- terior desert; M.theresioides diverged and then dispersed along the Río Loa to the coast, giving rise to M. quadri- vittatus in the north and M. atacamensis farther south. This last proposal is questionable, since the limit of dis- tribution between M. quadrivittatus and M.atacamensis is near Antofagasta (Victoriano et al. 2003). Here, we de- scribe some characteristics of M.atacamensis.

M. atacamensis is a lizard species which inhabits the intertidal zone of northern Chile from Antofagasta (23° 39′ S, 70° 22′ W) to Arrayán, La Serena (29° 41′ S, 71° 19′ W) (Ortiz 1980b; Heisig 1993, Sepúlveda et al. 2006). This isa medium large (mean: 102.7 mm length) (Donoso- Barros 1966; Ortiz 1980b), corpulent species with dark brown color and black blotches on the dorsum; crest tenu- ous in the vertebral zone and mouth narrow. According to Ortiz (1980a) and Vidal et al. (2002) there is a spatial seg- regation between juveniles and adults in the height of the perch used for thermoregulation, as well as a difference between sexes; although males are larger, there was no sig- nificant difference in their regulation, both were thermo- conformers (Vidal et al. 2002). This species is omnivorous behavior, since they consumed mainly Diptera and algae obtained from the intertidal area (Ortiz 1980a; Vidal and Labra 2008; Fariña et al. 2008).

Clinal variation is defined as gradual variation of a character over geographic distance (Futuyma 1998). For example, Vidal et al. (2007) found latitudinal variation in coloration in Liolaemus tenuis; green increased and brown decreased from north to south. Sepúlveda et al. (2008) proposed a latitudinal gradient in the thermo- regulatory ability of M. atacamensis, in which northern populations have low average to which lizards experi- ence a Tb outside the selected temperature, while south this ability increases. Fariña et al. (2008) found a clinal pattern in the diet of M. atacamensis, in which algal consumption decreases and consumption of Diptera in- creases from north to south.

Many theoretical and empirical studies have focused on the adaptive significance of morphological clinal vari- ation (Trussell 2000; Martínez-Freiría et al. 2009). While some analyses of linear morphometry have been often used to test hypotheses related to morphological poly- morphism in a microevolutionary context (Endler 1977; Scolaro and Cei 1987; Quatrini et al. 2001), others are more holistic and quantitative analyses are then required to identify them and to appraise the selective forces re- sponsible for their evolution (Adams and Rohlf 2000). In fact, due to scale problems with linear measures, these do not take into account the morphological complexity of biological structures (Humphries et al. 1981; Rohlf and Bookstein 1987; Mousseau 1991; Warheit 1992). In the case of traditional (non-geometric) measurements, statistical techniques for measuring distances, relations among distances, areas, volumes, or angles are applied (Bookstein et al. 1999). However, the geometric morph- ometry preserves the geometry configurations of land- marks, by allowing a statistical representation of real forms or forms only (Rohlf and Slice 1990; Rohlf et al. 1996; Rohlf 1999; Rohlf and Corti 2000), whereas de- notes the geometric shape properties of a structure that is independent of size, position, and orientation of the same, while the form of an object includes both size and shape (Rohlf and Slice 1990; Adams and Rohlf 2000, Mitteroecker and Gunz 2009). This information on shape allows a more complete biological interpretation than morphological variation (Rohlf and Marcus 1993). In relation to clinal variation, results obtained in Liolae- mus show that, although there is not a clear pattern of latitudinal variation of the shape in L. tenuis (Vidal et al. 2005), there are significant differences between two geo- graphical areas (arid Mediterranean and oceanic with Mediterranean influence). These different geographic areas may act as partial barriers to gene flow in this spe- cies. Vidal et al. (2006) found divergence between L. pic- tus from the Isla de Chiloé and the Chilean continent in ocular extension and location of the labial commissure. Individuals from the island had more extended ocular orbits and a more posterior position of the labial com- missure than individuals from the continent, which may be attributed to differences in diet between these two lo- calities (Vidal et al. 2006).

In this study, we explored the morphological adjustment toclinal environment variation in the shape of the head of M. atacamensis in dorsal and lateral view in different lo- calities, comparing over a latitudinal distribution from 23° to 28° S. Considering that environmental temperature de- creases as latitude increases and previous data has shown variation in thermal and feeding in this species, we specif- ically attempted to test the hypotheses that the shape of the head varies latitudinally including more extended shape in the north for your diet and more compacted shape the south.

METHODS

We examined 111 adult individuals of M. atacamen- sis from the following localities (Figure 1, Table 1): Antofagasta, Paposo, Pan de Azúcar, Caldera, and Tres Playitas. The localities were grouped into five groups, due to their geographic proximity to the mentioned localities. All material is deposited in the Museo de Zoología of the Universidad de Concepción (MZUC). Digital photographs were taken of the head of each individual in dorsal and lateral views with a dSLR Canon T4 camera (Canon, Tokyo, Japan), using a 50-mm f/1.4 lens with a fixed focal length. In addition, specimens were placed 10 cm away from the camera using a fixed tripod. The quality of the photographs was optimized with the Microsoft Power Point 2010 program. Nine homologous landmarks were located in the dorsal view and eleven in the lateral view (Figure 2), coincident with intersections of cranial scales. The location of the homologous landmarks was performed using the proposal of Vidal et al. (2006), with the addition of new landmarks which are specific for the genus Microlo- phus. Coordinates were sampled from photographs in dor- sal and lateral view by using tpsDig 1.20 (Rohlf 2003a). The analyses followed the procedures of Rohlf and Slice (1990) and Rohlf et al. (1996). The X and Y coordinates of the biologically homologous landmarks were aligned and superimposed using the minimum squares method based on the generalized Procrustes analysis (GPA), thus remov- ing non-shape variation (Zelditch et al. 2004) in order to standardize the size and to translate and rotate the con- figurations of landmark coordinates using tpsRelw (Rohlf 2003b). We extracted relative warp scores, using the tpsRelw software according to Kaliontzopoulou et al. (2007). Using relative warps, we computed canonical scores for specimens of populations in order to visualize these variations. The deformation grids were produced by the regression of shape variables against canonical results (Rohlf 2003b). These variables are used in a multivariate analysis (Rohlf et al. 1996; Adams and Rohlf 2000). We used TpsRelw version 1.21 (Rohlf 2003b) to perform a principal component analysis.

Fig. 1.

Fig. 1.

Open in a new tab

Figure 1 Map of the localities of Microlophus atacamensis analyzed in this study. These localities were grouped into five groups due to geographic proximity.

Table1 Studied localities and their geographic coordinates.

Locality Geographic coordinates N Dorsalview N Lateralview
Antofagasta 23°37′ S,70°24′ W 36 31
Paposo 25°15′ S,70°23′ W 3 2
Pande Azúcar 26°04′ S, 70°35′ W 15 14
Caldera 27°04′ S,70°49′ W 26 25
TresPlayitas 28°27′ S,71°13′ W 6 8
Open in a new tab

N=sample size.

Fig. 2.

Fig. 2.

Open in a new tab

Figure 2 Landmarks selected for the dorsal (A) and lateral (B) views in Microlophus atacamensis. The lateral bar on each image represents 1 cm on the specimen.

To determine sexual dimorphism and variability among localities, we using an analysis of two-way MANOVA using sex and locality as factor on the matrix of relative warps. Centroid size was used as a size index, computed as the square root of the sum of the squared distances of a set of landmarks from their centroid (Marcus et al. 1996). The centroid size (log (CS)) of all individuals was com- pared with a two-way ANOVA using sex and locality as factor. The allometry calculations used in this work con- sisted of multivariate regression in which the explanatory variable is the CS, and the dependent variables are the var- iables of the shape (i.e., Procrustes residuals or PC scores, see Klingenberg 1996 and Depecker et al. 2006). Accord- ing to Bookstein (1991), allometry is defined as changes in the shape related to the increase in size, where significant results in the multivariate regression of shape on CS indi- cate an allometric effect of size on shape (Zelditch et al. 2004).

RESULTS

No significant differences were detected among localities, either in dorsal view (Wilk’s lambda = 0.23; p = 0.45) or lateralview (Wilk’s lambda= 1.77; p= 0.24), and no sexual dimorphism was found in dorsal (Wilk’s lambda = 0.31;p = 0.67) and lateral (Wilk’s lambda = 0.05; p = 0.63) views. The interaction between the two factors was not significant in both views, respectively (Wilk’s lambda dorsal= 1.65; p= 0.1; Wilk’slambda lateral = 1.06; p= 0.52). The first three principal components of shape ex- plained the majority of the variance for the dorsal and lateral views (96.9% and 86.6%, respectively, Figures 3 and 4). In the dorsal view (Figure 3), PC1 expresses a change in the shape of the head laterally (90.1% of the total Procrustes form variance), while in lateral view (Figure 4) it expresses the change in the posterior region (68.4% of the total Procrustes form variance). In both cases, PC1 shows changes in allometry. PC2 in dorsal view (5.6% of the total form variance) showing changes in the compression of the head on their sides; for the lateral view (12.6% of the total form variance), it shows the changes with a dorsal-ventral compression. The PC3 accumulates low variance, which is displayed on the pro- jected surface by the three components (Figures 3 and 4). In centroid size case, no significant differences were de- tected among localities, either in dorsal view (F(1,4) = 6.57; p= 0.54) or lateral view (F(1,4) = 0.21; p= 0.93), and no sex- ual dimorphism was found in dorsal (F(1,4) = 0.38; p= 0.54) and lateral views (F(1,4) = 0.06; p = 0.81). The interaction between the two factors was not significant in both views, respectively (F(1,4) = 1.19; p= 0.15; F(1,4) = 0.24; p= 0.91). Landmark 9 of the dorsal view and landmarks 1 and 11 of thelateral view were those which showed the greatest vari- ation, corresponding to the tympanic area. Although no significant differences among localities were detected in both views, there is a tendency to differentiate the loca- tions of Antofagasta from Caldera - Three Playitas in dor- sal view, and Caldera from Tres Playitas - and Pan de Azúcar in lateral view. The spatial ordering of the princi- pal components analysis (PCA) showed superimposition of all localities in the dorsal and lateral views (Figure 5). No allometric effect was detected in either dorsal orlateral view for the shape variables between the centroid size and the principal components (r= 0.08, p= 0.65 in dorsal view; r= 0.02, p= 0.83 in lateral view).

Fig. 3.

Fig. 3.

Open in a new tab

Figure 3 Form-space principal component analysis in Microlophus atacamensis in lateral view. The first three components account for 96.9% of the total form-space variance. Surfaces correspond to the shapes represented by negative and positive extremes of PC1 and PC2.

Fig. 4.

Fig. 4.

Open in a new tab

Figure 4 Form-space principal component analysis in Microlophus atacamensis in lateral view. The first three components account for 86.6% of the total form-space variance. Surfaces correspond to the shapes represented by negative and positive extremes of PC1 and PC2.

Fig. 5.

Fig. 5.

Open in a new tab

Figure 5 Centroid size (log) and standard deviation of the five localities in dorsal (A) and lateral (B) views.

DISCUSSION

A number of studies have been performed on chromo- somes, coloration, diet, thermoregulation, and geometric morphometrics which have provided evidence for clinal variation of lizards in Chile (Lamborot 1991; Lamborot etal. 2012; Vásquez et al. 2007; Vidal et al. 2007; Sepúlveda etal. 2008; Fariña et al. 2008; Vidal et al. 2008). In spite of these evidences, our results do not show clinal variation in head shape among the five studied localities of M. ataca- mensis. The PCA showed a superposition of all the local- ities both in dorsal and lateral view, indicating that the different morphs may be found in all the studied localities. However, this analysis showed some tendency to group the Pan de Azúcar and Tres Playitas localities in dorsal view, and Caldera and Tres Playitas in the lateral view (Figure 3). Although the results of the aposteriori analysis show a tendency of segregation in two relative warps in dorsal view and three in lateral view, the majority of the results obtained did not show significant differences among localities. Although Fariña et al. (2008) showed a latitudinal gradient in the diet of M. atacamensis, we did not find a similar pattern in the shape of the head as shown in the study of Vidal et al. (2006) in L. pictus. Kaliontzopoulou et al. (2010) found significant different differences in the form of the head of Podarcisbocagei, re- lated to the habitat utilized. In the present case, M. ataca- mensis uses the same habitat in its entire distribution range (Ortiz 1980b; Heisig 1993; Sepúlveda et al. 2006), which may explain in part the lack of clinal differences in head form. The same is true of L. petrophilus (Fontanella et al. 2012); although there are differences in the shape of the cranium from north to south, this is due to the fact that this species occupies different niches latitudinally. In Strengeriana maniformis, Pedraza and Campos (2007) did not find significant differences in the form of the gonopod among habits with and without mining contamination; they found, as in the present case, that the different morphs are distributed in both types of habitats, which may indicate that this species has some plasticity to min- ing contaminants. M. atacamensis may also have some plasticity in diet, depending upon the food available, explaining in part the lack of clinal variation in head form over a latitudinal range.

Also in this case, L. tenuis does not show a clinal vari- ation pattern in its morphological characteristics (Vidal et al. 2005). By contrast, in M. atacamensis, Ortiz (1980a) showed that the number of mid-line scales and number of vertebral scales increased from Antofagasta to Huasco. Also,Sepúlveda et al. (2008) hypothesized that in this spe- cies, size is related to the thermoregulatory gradient, since juvenile individuals (smaller) were the first to emerge in the morning and adults (larger) were the last to take ref- uge in the evening, suggesting that populations in the north should be smaller than those in the south. The liz- ard plays an important role in linking the intertidal and terrestrial environment within desert systems, since it feeds in the intertidal area (eating algae, isopods, and Diptera) and thermoregulates in the terrestrial area, defe- cating in the latter zone and thus contributing to its bio- mass and maintaining the trophic networks (Sepúlveda et al. 2006; Fariña et al. 2008). In this case, at larger sizes, there is increased bite force, improved prey handling effi- ciency, and a consequent shift to larger and harder foods (Verwaijen et al. 2002), therefore it was expected to yield a variation in the shape of the head of M. atacamensis. On the other hand, much importance has been given to the three-dimensional representation (3D) to estimate the var- iations due to the shape in an evolutionary context. Ac- cording Polly and MacLeod (2008), the success of our 3D eigensurface method, while qualified, is encouraging. Eigensurface analysis of the 3D topography of calcanea sorted them into the same functional spectrum that quali- tative functional analysis would have. While 3D surface scans of complicated morphological structures (e.g., bones, teeth, and shells) are increasingly easy to generate, this technique is not attainable for everyone, but we hope to conduct new studies to incorporate 3D images for popula- tion comparisons (Polly and MacLeod 2008).

On the other hand, according to Bruner et al. (2005), it is assumed that during development the scales either grow or do not grow but that no absolute reduction takes place. Concerning the length of the frontal scales, Bruner et al. (2005) suggest that males show an absolute enlargement but a relative reduction when compared to females (i.e., negative allometry) in sexual dimorphism case. In relation to clinal variation, there are no studies indicating that the scales tend to differ with latitude. However, using the scales as a reflection of the bones suggests that they are good indicators of change at this level (Costantini et al. 2007). In the case of M. ataca- mensis, there are no differences in head shape connect- ing to clinal variation, which involves conducting new studies to understand in an evolutionary context.

CONCLUSIONS

Our results show that there are no differences between the studied, among the explanations are thatpopulations of this species are subjected to similar environments that promote convergence of the structures analyzed.

Acknowledgments

Acknowledgements

We thank the Museo de Zoología of the Universidad de Concepción for supplying the samples used in this study. Finally, thanks to Lafayette Eaton, who made valuable suggestions which helped to improve this work. This study was financed by the Fondecyt project 1131009.

Footnotes

Authors’ contributions: SI obtained photographs of museum specimens used in this study and contributed to the writing the manuscript. MV directed the photo shoots of the museum specimens used in this study. She directed the construction of the manuscript and the geometric and statistical analysis of the study. JCO provided the museum specimens that were photographed and provided input on improving the manuscript. FTP was involved in revising the manuscript and provided new ideas to improve the version sent. All authors read and approved the final manuscript.

Competing interests: The authors declare that they have no competing interests.

References

  1. Adams D, Rohlf F J. Ecological character displacement in Pletodon: biomechanical differences found from a geometric morphometric study. Proc Natl Acad Sci U S A. 97:4106–4111. doi: 10.1073/pnas.97.8.4106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benavides E, Baum R, Mcclellan D, Sites J W. Molecular phylogenetics of the lizard genus Microlophus (Squamata, Tropiduridae): aligning and retrieving indel signal from nuclear introns. Syst Biol. 56:776–797. doi: 10.1080/10635150701618527. [DOI] [PubMed] [Google Scholar]
  3. Bookstein Fl ;, Bookstein F, Schafer K, Prossinger H, Seidler H, Fieder M, Striger C, Weber G, Arsuaga J L, Slice D, Rohlf F J, Recheis W, Mariam A, Marcus L. Comparing frontal cranial profiles in archaic and modern Homo by morphometric analysis. Cambridge University Press. 257:217–224. doi: 10.1002/(SICI)1097-0185(19991215)257:6<217::AID-AR7>3.0.CO;2-W. [DOI] [PubMed] [Google Scholar]
  4. Bruner E, Costantini D, Fanfani A, Dell&apos;omo G. Morphological variation and sexual dimorphism of the cephalic scales in Lacerta bilineata. Acta Zool. 86:245–254. [Google Scholar]
  5. Costantini D, Bruner E, Fanfani A, Dell&apos;omo G. Male-biased predation of western green lizards by Eurasian kestrels. Naturwissenschaften. 94:1015–1020. doi: 10.1007/s00114-007-0284-5. [DOI] [PubMed] [Google Scholar]
  6. Depecker M, Berge C, Penin X, Renous S. Geometric morphometrics of the shoulder girdle in extant turtles (Chelonii) J Anat. 208:35–45. doi: 10.1111/j.1469-7580.2006.00512.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dixon J, Wright J. A review of the lizards of the Iguanid genus Tropidurus in Perú. Contr. Sci. Nat. Hist. Mus. Contr Sci Nat Hist Mus Los Angeles. 271:1–39. [Google Scholar]
  8. Donoso-Barros R. Alimentación de Tropidurus peruvianus (Lesson) Biol Mus Nac Hist Nat Chile. 24:213–216. [Google Scholar]
  9. Donoso-Barros R. Ecología de los reptiles Chilenos. Invest Zool Chil. 6:65–72. [Google Scholar]
  10. Donoso-Barros R. Santiago, Chile): 1966. [Google Scholar]
  11. Endler J. Geographic variation, speciation, and clines. Univ. Press. pp. 283–367. [PubMed]
  12. Fariña J M, Sepúlveda M, Reyna M V, Wallem K P, Ossa-Zazzali P G. Geographical variation in the use of intertidal rocky shores by the lizard Microlophus atacamensis on the Atacama Desert coast. J Anim Ecol. 77:458–468. doi: 10.1111/j.1365-2656.2008.01361.x. [DOI] [PubMed] [Google Scholar]
  13. Fontanella F M, Feltrin N, Avila L J, Sites J W, Morando M. Early stages of divergence: phylogeography, climate modeling, and morphological differentiation in the South American lizard, Liolaemus petrophilus (Squamata: Liolaemidae) Ecol Evol. 2:792–808. doi: 10.1002/ece3.78. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Frost D R. Phylogenetic analysis and taxonomy of the Tropidurus group of lizards (Iguania: Tropiduridae) Am Mus Novit. 3033:1–68. [Google Scholar]
  15. Frost D R, Etheridge R. A phylogenetic analysis and taxonomy of iguanian lizards (Reptilia: Squamata) Mus Nat Hist Univ Kansas Misc Publ. 81:1–65. [Google Scholar]
  16. Futuyma D. Evolutionary biology. Sunderland, Massachusetts): Sinauer Associates, Inc; 1998. [Google Scholar]
  17. Heisig M. An etho-ecological study of an island population of Tropidurus atacamensis. Salamandra. 29:65–81. [Google Scholar]
  18. Humphries J M, Bookstein F L, Chernoff B, Smith G R, Elder R L, Poss S G. Multivariate discrimination by shape in relation to size. Syst Zool. 30:291–308. [Google Scholar]
  19. Kaliontzopoulou A, Carretero M A, Llorente G A. Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis lizards. J Morphol. 268:152–165. doi: 10.1002/jmor.10494. [DOI] [PubMed] [Google Scholar]
  20. Kaliontzopoulou A, Carretero M A, Sillero N. Geographic patterns of morphological variation in the lizard Podarcis carbonelli, a species with fragmented distribution. Herpetol J. 20:41–50. [Google Scholar]
  21. Klingenberg C P. Multivariate allometry. Plenum Press. pp. 23–49.
  22. Lamborot M. Karyotypic variation among populations of Liolaemus monticola (Tropiduridae), separated by riverine barriers at the Andean Range. Copeia. pp. 1044–1059.
  23. Lamborot M, Ossa C M, Vásquez M. Population cytogenetics of the "Northern Mod 1" chromosomal race of Liolaemus monticola Müller & Helmich (Iguanidae) from Central Chile. Gayana. 76:10–21. [Google Scholar]
  24. Marcus L F, Corti M, Loy A, Naylor Gjp, Slice De ;, Freiría F, Santos X, Pleguezuelos J M, Lizana M, Brito J C. Geographical patterns of morphological variation and environmental correlates in contact zones: a multi-scale approach using two Mediterranean vipers. Plenum Press. 47:357–367. [Google Scholar]
  25. Mitteroecker P, Gunz P. Advances in geometric morphometrics. Evol Biol. 36:235–247. [Google Scholar]
  26. Mousseau T A. Landmarks in morphometrics, or the shape and size of morphometrics to come. Evolution. 45:1991–1980. [Google Scholar]
  27. Ortiz J C. Estudios comparativos de algunas poblaciones de Tropidurus de la costa chilena. An Mus Hist Nat Valparaíso. 13:267–280. [Google Scholar]
  28. Ortiz J C. Revisión taxonómica del género Tropidurus en Chile. Actas de la Primera Reunión Iberoamericana de Zoología de Vertebrados. Ediciones del Ministerio de Universidades e Investigación. pp. 355–377.
  29. Ortiz J C, Serey I. Análisis factorial de correspondencias de las especies del género Tropidurus en Chile. Rev Med Exp Chile. 12:203–208. [Google Scholar]
  30. Pedraza M, Campos M. Estudio de la variación morfológica del gonopodo de Strengeriana maniformis (Brachyura: Pseudothelphusidae) mediante aplicación de Morfometría Geométrica. Caldasia. 29:143–152. [Google Scholar]
  31. Polly P D, Macleod N. Locomotion in fossil carnivora: an application of eigensurface analysis for morphometric comparison of 3D surfaces. Palaeontol Electron. 11:1–13. [Google Scholar]
  32. Quatrini R, Albino A, Barg M. Variación morfológica en dos poblaciones de Liolaemus elongatus Koslowsky 1896 (Iguania: Tropiduridae) del noroeste patagónico. Rev Chil Hist Nat. 74:639–651. [Google Scholar]
  33. Rohlf F J. Shape statistics: Procrustes superimpositions and tangent space. J Classif. 16:197–223. [Google Scholar]
  34. Rohlf F J. TPSRELW. Version 1.21. Department of Ecology and Evolution. Syst Zool. 36:356–367. [Google Scholar]
  35. Rohlf F J, Corti M. Use of two-block partial least squares to study covariation in shape. Syst Zool. 49:740–753. doi: 10.1080/106351500750049806. [DOI] [PubMed] [Google Scholar]
  36. Rohlf J F, Marcus L. A revolution in morphometrics. Trends Ecol Evol. 8:129–132. doi: 10.1016/0169-5347(93)90024-J. [DOI] [PubMed] [Google Scholar]
  37. Rohlf F J, Slice D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool. 39:40–59. [Google Scholar]
  38. Rohlf F J, Loy A, Corti M. Morphometric analysis of old world Talpidae (Mammalia, Insectívora) using partial-warp scores. Syst Biol. 45:344–362. [Google Scholar]
  39. Scolaro J A, Cei J M. A multivariate analysis of morphometric and exosomatic characters of Iguanid lizards of the patagonian Liolaemus kingi complex. J Herpetol. 21:343–348. [Google Scholar]
  40. Sepúlveda M, Vidal M A, Fariña J M. Microlophus atacamensis (Atacama Desert Runner) predation. Herpetol Rev. 37:224–225. [Google Scholar]
  41. Sepúlveda M, Vidal M A, Fariña J M. Seasonal and geographic variation in thermal biology of the lizard Microlophus atacamensis (Squamata: Tropiduridae) J Thermal Biol. 33:141–148. [Google Scholar]
  42. Trussell G C. Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution. 54:151–166. doi: 10.1111/j.0014-3820.2000.tb00016.x. [DOI] [PubMed] [Google Scholar]
  43. Vásquez M, Torres-Pérez F, Lamborot M. Genetic variation within and between four chromosomal races of Liolaemus monticola in Chile. Herpetol J. 17:149–160. [Google Scholar]
  44. Verwaijen D, Van Damme R, Herrel A. Relationships between head size, bite force, prey handling efficiency and diet in two sympatric lacertid lizards. Funct Ecol. 16:842–850. [Google Scholar]
  45. Victoriano P, Torres F, Ortiz J C, Parra L, Northland I, Capetillo J. Variación aloenzimática y parentesco evolutivo en especies de Microlophus del grupo "peruvianus" (Squamata: Tropiduridae) Rev Chil Hist Nat. 76:65–78. [Google Scholar]
  46. Vidal M A, Labra A. Dieta de anfibios Y reptiles. Science Verlag. pp. 453–482.
  47. Vidal M, Ortiz J C, Labra A. Sexual and age differences in ecological variables of the lizard Microlophus atacamensis (Tropiduridae) from Northern Chile. Rev Chil Hist Nat. 75:283–292. [Google Scholar]
  48. Vidal M A, Ortiz J C, Ramírez C C, Lamborot M. Intraspecific variation in morphology and sexual dimorphism in Liolaemus tenuis (Tropiduridae) Amphibia-Reptilia. 2005;26:343–351. [Google Scholar]
  49. Vidal M A, Veloso A, Méndez M A. Insular morphological divergence in the lizard Liolaemus pictus (Liolaemidae) Amphibia-Reptilia. 27:103–111. [Google Scholar]
  50. Vidal M A, Ortiz J C, Labra A. Sexual and geographic variation of color patterns in Liolaemus tenuis (Squamata, Liolaeminae) Gayana. 71:27–33. [Google Scholar]
  51. Vidal M A, Ortiz J C, Labra A. Intraspecific variation in a physiological thermoregulatory mechanism: the case of the lizard Liolaemus tenuis (Liolaeminae) Rev Chil Hist Nat. 81:171–178. [Google Scholar]
  52. Warheit K I. Proceedings of the Michigan morphometrics workshop. 41:392–395. [Google Scholar]
  53. Zelditch M L, Swiderski D, Sheets D, Fink W L. Geometric morphometrics for biologists: a primer. London): Elsevier; 2004. [Google Scholar]

Articles from Zoological Studies are provided here courtesy of Biodiversity Research Center, Academia Sinica

RESOURCES