Are you what you eat? A geometric morphometric ... - Oxford Academic

Biological Journal of the Linnean Society, 2009, 97, 677–707. With 12 figures

Are you what you eat? A geometric morphometric analysis of gekkotan skull shape JUAN D. DAZA1*, ALEXANDRA HERRERA2, RICHARD THOMAS1 and HÉCTOR J. CLAUDIO1 bij_1242

1 2

677..707

Biology Department, University of Puerto Rico, San Juan 00931-3360, Puerto Rico Biological Sciences Department, The George Washington University, Washington, DC 20052, USA

Received 29 September 2008; accepted for publication 4 December 2008

The morphological variation of the gekkotan skull, as visualized through dorsal and lateral views of a large sample of skulls (164 species; 68% of all gekkotan genera), was analysed using geometric morphometrics. We describe skull changes using variables associated with the contour variations (uniform components), as well as localized changes (partial warps). We defined dietary categories based on the available information for 105 species. These categories, together with phylogenetic affinities, were used as descriptors of the skull shape variables in subsequent statistical analyses. Changes based on the morphological variables are described and discussed in an ecological and phylogenetic context. We consider that this new information relating gekkotan phylogeny and diet will be useful in future phylogenetic analyses of this group. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 677–707.

ADDITIONAL KEYWORDS: diet – classification – relative warps – anatomy – uniform and non-uniform components.

INTRODUCTION The Gekkota is the third most species-rich lizard clade, comprising approximately 1250 species (Kluge, 2001; Zug, Vitt & Caldwell, 2001; Bauer, 2002; Uetz, 2008). Among the group, body shape and size varies remarkably. The morphology of the Gekkota has been particularly problematic because of the combination of plesiomorphic and apomorphic characters states (Estes, 1983; Conrad, 2004; Han, Zhou & Bauer, 2004). In previous cladistic analyses based on morphology, Gekkota have been found to be the sister taxon of Autarchoglossa (Estes, de Queiroz & Gauthier, 1988; Hallermann, 1988), or the more inclusive clade Evansauria (Conrad, 2008), Scincomorpha (Presch, 1988; Reynoso & Callison, 2000), and Anguimorpha (Evans & Chure, 1998; Gao & Norell, 1998; Reynoso, 1998), or have been placed in the clade Nyctisauria with dibamids, amphisbaenians, and xantusiids (Lee, *Corresponding author. E-mail: [email protected]

1998). Using molecular data, gekkotans are consistently found to be the sister group of all other squamates with the exception of dibamids (Townsend et al., 2004; Vidal & Hedges, 2004; Hugall, Foster & Lee, 2007); but see also Zhou et al. (2006). Other factors obscuring the higher level position of gekkotans are the uncertainty of the monophyly of Scincomorpha, gekkotan paedomorphy, and the paucity of the gekkotan and xantusiid fossil record (Evans, 2003; Hugall et al., 2007). Additionally, most gekkotans exhibit the so-called ‘gekkotan morphotype’, which is believed to be plesiomorphic body plan for Squamata, Scleroglossa, Nyctysauria, Scincomorpha, and Anguimorpha (Conrad, 2004). Indeed, some extant gekkotans might ‘seem’ as if they were representations of this ancestral bauplan, but some of them have reached such a degree of morphological specialization that they no longer resemble geckos. A dramatic example is the Pygopodidae. In terms of skull anatomy, gekkotans present a variety of apomorphic traits that puts them among

© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 677–707

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the most specialized groups among lepidosaurs (Han et al., 2004). Two of these modifications are the reduction of temporal arches and loss of the postorbital bar, which have resulted in remarkable skull mobility (Herrel, Aerts & De Vree, 2000). Additional transformations of the gekkotans include the shortening of the supratemporal process of the parietal and the ventral and dorsal fusion of frontal bones (Rieppel, 1984a; Conrad, 2008). Fusion among the dorsal midline bones of the skull, such as the premaxillae, nasals, and parietals, varies among the Gekkota and has been attributed to ongoing paedomorphosis (Stephenson, 1960; Kluge, 1967; Rieppel, 1984a; Maisano, 2001). In miniaturized forms, the dorsal bones of the snout are imbricate, and there is an increase in the degree of overlap with size reduction; this was considered to be a response to the reduction in size and the necessity of strengthening the skull (Daza et al., 2008). Gekkotans range in size from the smallest amniotes yet described (i.e. the miniaturized Sphaerodactylus ariasae; mean snout–vent length = 16 mm; Hedges & Thomas, 2001) to forms, such as the extinct giant gecko from New Zealand Hoplodactylus delcourti (snout–vent length = 370 mm; Bauer & Russell, 1986a, b, 1988). Size alone is one important factor that can account for changes in morphology; larger organisms are usually shaped differently than smaller ones (Zelditch et al., 2004), and this observation applies to both ontogenetic (growth) and phylogenetic (comparison of related forms) backgrounds (Thompson, 1948). The skeletal system in particular is affected by scaling (Schmidt-Nielsen, 1975; Schmidt-Nielsen, 1984). The section of the skull containing the brain and sense organs follows a negative allometric pattern as the animal reduces in size, comprising a requirement that maintains a minimal functional volume in these organs (Hanken, 1983; Rieppel, 1984b; Palombo, 2001). Thus, it is reasonable to expect that, along a size gradient, animals would have distinct skull morphologies instead of being simply replicates of the same bauplan at different scales. The pygopodid Aprasia repens has one of the smallest skulls, measuring 5.02 mm (UMMZ 173865; Rieppel, 1984b), and, at this size, the skull is solid, elongated, and rectangular in shape. At the other extreme of the size range, the skull of the diplodactylid H. delcourti measures 80.3 mm (MNHM 198535; Bauer & Russell, 1986a; Bauer & Russell, 1988). This more massive skull is relatively shorter and broader. The variation in skull size between these limits is approximately one order of magnitude, the largest being approximately 15 times longer than the smallest and most likely hundreds of times the volume, which is a critical feature for understanding morphological variation in the shape of gekkotans.

Size differences, especially in skull diameter and length, lead to other changes. As the skull length decreases, the relative size of the otoocipital region (basicranium) increases (Fig. 1) (Rieppel, 1984b) as a result of the relative increase of the brain, sense organs, and feeding mechanisms (Rieppel, 1996). An example of an anatomical part being affected during the miniaturization process in gekkotans is the paroccipital process (Fig. 1), which, when compared with large gekkotans, changes from being long and slender to short and stout, occupying an important area in the rear part of the skull. Parietal contact with the supraoccipital becomes extensive, reducing the metakinetic joint, obliterating the post-temporal fossa (Fig. 1) (Rieppel, 1996), limiting the space for the insertion of the neck muscles rectus capitis and longisimus capitis (Al Hassawi, 2007), and displacing their insertion points to a more anterior point on the skull roof. Morphological changes related to miniaturization of the lizard skull have also been correlated with other changes, such as the body elongation and limb reduction in fossorial forms (Rieppel, 1996), that are not found in nonburrowing miniaturized lizards in which different eco-morphological adaptations might be taking place. Gekkotan skull diversity has been analysed in morphometric studies together with other lizard clades. These studies of a huge diversity of lizards have yielded interesting findings, such as the morphometric corroboration of the basal split between the ‘fleshtonged’ Iguania and ‘scaly tonged’ Scleroglossa (Stayton, 2005), which is the dominant morphological hypothesis and appears to have an approximate association with differences in foraging mode (Herrel, 2006). Another finding of previous morphometric studies in lizards is that the herbivorous skull differs from skulls of omnivorous and carnivorous species (Metzger & Herrel, 2005; Herrel, 2006), with this comprising a difference that has developed independently in at least eight squamate families (Stayton, 2006). Although these studies are important for inferring general patterns of skull anatomy throughout the crown group of squamates, a study with a reduced scope but greater depth should identify details of other underlying processes taking place among closely-related forms. In the present study, we conducted geometric morphometrics analyses (Bookstein, 1991) using dorsal and lateral views of the gekkotan skull. The dorsal view is used in these types of analyses for two reasons. The first is biological and is justified by the fact that gekkotans generally have a broad depressed skull (Kluge, 1967; Ma & Xia, 1990), especially in exclusively arboreal forms, where the body often becomes flattened (Camp, 1923). The other reason is technical; the skulls (without the jaws), when


ANALYSIS OF THE GEKKOTAN SKULL

679

Figure 1. Posterior view of the skull of a large (A) and a miniaturized (B) gekkotan. A. Uroplatus henkeli (JFBM 15833) and Gonatodes albogularis (FMNH 55929). Diagonal lines indicate the basicranium. bp, basipterygoid process; ees, extracranial endolymphatic sacs; epi, epipterygoid; fm, foramen magnum; occ, occipital condyle; pa, parietal; pof, postorbitofrontal; pop, paroccipital process; ppp, postparietal process; pt, pterygoid; p-tf, post-temporal fossa; q, quadrate; sq, squamosal.

positioned on a flat surface and viewed dorsally, allow more efficient comparisons within individual images, offering less variability than images obtained in lateral view, which are more susceptible to changes produced by different observation angles. Each view (i.e. dorsal and lateral) was treated separately because each one can provide different information, although reference is made to common transformations. The three main goals of the present study were: (1) to provide an objective description (by means of geometric morphometric techniques) of the amount of variation in the skull using lateral and dorsal views

for each of the gekkotan families; (2) to describe which particular areas of the skull show more morphological changes across the phylogeny; and (3) to determine whether variations in skull shape can be explained by allometry or are correlated with feeding behaviour. The descriptions of skull transformations are not in a strict phylogenetic context; we intend to describe the variation observed within the Gekkota sample in the form of new characters; which will be tested in a cladistic analysis elsewhere. Some changes are discussed in a cladistic framework and can be ascribed to convergent (homoplastic) or conservative (plesiomorphic) patterns, although we focus special


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attention on the relative position of the specimens in the morphospace.

MATERIAL AND METHODS SPECIMENS

SAMPLED AND DIGITALIZATION OF IMAGES

One hundred and sixty-four species from 73 genera were sampled (68% of all gekkotan genera); we collected a total of 382 digitized specimens from 15 zoological collections (see Supporting Information, Appendix S1); some of these images were loaned by Dr Tristan Stayton (Bucknell University) from his previous geometric morphometrics analysis. Taxonomic content was determined by what taxa were available in museums (see Supporting Information, Appendix S2). The specimens included representatives of all seven families of Gekkota according to the most recent taxonomic arrangements (Gamble et al., 2008a, b). We kept this analysis limited to the Gekkota to increase correspondence among morphological loci; in this way, we avoid difficulties in determining homologous structures, such as may be encountered in morphological characters when they are used in broad-scale phylogenetic analyses (Rieppel, 2007). All specimens were well ossified and had closed parietal fontanelles to insure that they had reached sexual maturity (Maisano, 2000; Maisano, 2001). This aspect of their anatomy is important because we expect that the landmarks selected had reached their final form and would not add further bone during growth. The landmarks used also are represented as the same character state in all specimens. This is a good indication of sameness, which refers to historical continuity through inheritance with modification (Wagner, 2007). With all these considerations, we are confident that the landmarks are homologous. Information about the sex was not available for all specimens, so we disregarded sex in the statistical analyses, although we are aware that, in some lizard species, males have larger heads than females (Verwaijen, Van Damme & Herrel, 2002). In addition, extreme sexual dimorphism has not been reported in gekkotans. Two data files were created: one for the dorsal analysis (362 specimens) and another for the lateral analysis (200 specimens). One hundred and seventy specimens are present in the two data sets. The images used come from digital pictures, computed tomography scan images, and cleared and stained specimens (Alcian blue, Alizarin red staining of bone and cartilage). Landmarks were traced directly from the cleared and stained specimens using a camera lucida attached to a dissecting microscope; the drawings of the landmarks were then scanned and combined with the other files.

LANDMARKS Only unambiguous loci in anatomical structures were used; thus we are specifying that the points are homologous (Zelditch et al., 2004) Landmark types I, II, and III (Bookstein, 1991) were used. We selected eleven landmarks in both lateral and dorsal views (Fig. 2) and marked them with tpsDIG2 (Rohlf, 2006) on all the specimens. Landmarks for the dorsal view (Fig. 2A) and lateral view (Fig. 2B) analyses are defined in Table 1. Landmarks L6 and D9 represent the same reference pair, as does the pair L11/D5. In the genus Lygodactylus, the postorbitofrontal is absent; in this case, the landmarks corresponding to it were positioned next to the lateral edge of the fronto-parietal suture. Because the gekkotan skull is highly kinetic, we took the precaution of selecting only landmarks in fixed positions or closer to pivot of joints; this might minimize the effect of rotation of some elements caused by post-mortem movements.

DIET

CATEGORIES

Using the dietary information for 105 gekkotan species (Table 2), we divided them into five categories: (G) generalist predators that feed on any type of prey, either small or large; (I) invertebrate predators that feed on predominantly small prey; (V) vertebrate predators that feed on large prey, almost exclusively tetrapods (e.g. saurophagous lizards such as the pygopodid Lialis burtonis); ingestion of their own skin appears to be widespread among geckos and, therefore, lizard skin was not included in the diet analysis; (O) omnivorous predators, animals feeding on any kind of prey and plant products; and (P) plant products consumers (phytophagous); in gekkotans true herbivory or feeding on fibrous and tough foliage (Metzger & Herrel, 2005) has not evolved. Some of them are inclined to feed on plant-derived substances such as floral parts (i.e. anthers, stamens, nectar), fruits, or sap. In the process of defining these categories, we ignored the reports of leaves in the diets, because we considered this consumption to be unintentional. Of the species whose diet has been documented, we have 40 represented in the two data sets. Foraging mode was not considered because it has been hypothesized that its correlation with diet is spurious (Huey & Pianka, 1981; Vitt & Pianka, 2006).

ANALYSES The landmark configurations in the dorsal and lateral planes were analysed with tpsRelw, version 2.04 (Rohlf, 2006). Camera-to-subject distance was not monitored, images were taken at variable magnifications, and just a subset of the images presented a scale bar (87% of the specimens in dorsal and 83% in



681

Figure 2. Landmarks used in dorsal (A) and lateral (B) analysis plotted onto the skull of Tarentola americana (AMNH R-17726). Scale bar = 10 mm.

the lateral views). Accordingly, we did not use centroid size as a measure of magnitude to test for allometry (Zelditch et al., 2004). Instead, we measured skull lengths in the specimens where the scale bar was present and used this value in a sub-set of the data to test for allometry. The analyses were carried sensu Cavalcanti (2004). One of the outputs is the weight matrix ‘W’, where the uniform and non-uniform (partial warps) components of shape are estimated. These components are appropriate for statistical analysis based on the general linear model (Rohlf & Slice, 1990). Uniform components (u1 and u2) indicate global (affine) variation of the shape; u1 represents changes along the landmarks in the x-axis (skull length in both dorsal and lateral views analyses), whereas u2 refers to the changes in the y-axis, skull width and height in the dorsal and lateral analyses, respectively. The remaining shape variables are the non-uniform components (partial warps) and describe local, non-

affine shape changes. These were analysed by a principal component analysis (relative warps analysis) to evaluate localized shape changes. The results of this analysis were visualized with deformation grids. In all of the figures, we used families and diet as qualitative categories. In scatter plots of RW1 versus RW2 and RW3, the closest specimen to the origin and the extreme points along the axis were drawn. These extreme specimens were used as reference taxa for describing morphological changes.

STATISTICAL

ANALYSIS

Shape variables (i.e. uniform and non-uniform components) were evaluated statistically: the Pearson correlation coefficient was calculated between the uniform components (u1, u2), analysing Gekkota as a whole, and using family and diet categories as descriptors. These correlations were performed to evaluate whether the two components are indepen-


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Table 1. List and definition of landmarks used on dorsal (D) and lateral (L) analyses

Dorsal view D1

Type

Definition

III

Anterior-most part of the premaxilla Lateral edge of the premaxilla-maxilla left suture Posterior most part of the ascending nasal process of the premaxilla

D2

I

D3

II

D4 D5

II II

D6

II

D7

I

D8

I

D9

II

D10

II

D11

Posterolateral tip of the nasal Edge of the posterior process of the jugal Lateral angular point of postorbitofrontal, where anterior and posterior process met. In specimens with rounded lateral edge, the landmark was placed in the middle of the curvature Lateral edge of the frontoparietal suture Middle point of the frontoparietal suture Posterior edge of the posteromedial process of the parietal Posterior edge of the left squamosal or postparietal process of the parietal bone

III

Intercondylar space at the basioccipital bone

III

Anterior edge of the premaxilla, at the margin of the tooth row

L2

II

L3

I

Posterior most extension of the left narial opening Posterior edge of the dorsal process of the left prefrontal bone

L4

II

L5

II

L6 L7

II III

L8

II

L9

II

L10

II

Anterior tip of the basipterygoid process of the sphenoid

L11

II

Tip of the posterior process of the jugal

Lateral view L1

Most ventral edge of the left postorbitofrontal Anterior end of the crista alaris of the left prootic Posterior edge of the parietal(s) Posterior edge of the skull, at the level of the dorsal border of the quadrate Posterodorsal edge of the quadrate head Posterior tip of the quadrate process of the left pterygoid bone

dent or not, and to address two questions: (1) are changes along the skull length related to changes along the skull width and height and (2) can these changes be better explained by taxonomic affinities or feeding behaviour? The next step was to test the differences in the shape variables among the groups; we carried out multivariate analysis of variance with the u1 and u2 in both categories, initially combined (i.e. both uniform components simultaneously) and, second, with each component separately. The same approach was applied to the non-uniform components (partial warps), although they were not evaluated separately. Analysis of variance was performed to test differences in skull length by family and diet categories. Tukey’s honestly significant difference test was performed to determine pairwise differences between the skull length and the diet of the animals. To test for allometry, multiple correlations were performed between the skull length and the full shape space (both uniform and non-uniform components). Finally, RW1 was correlated with families and diet categories. All statistical analyses were performed in STATISTICA (StatSoft, 2007); plots were created in SigmaPlot (Systat, 2007) and assembled in Adobe Illustrator CS3.

RESULTS THE

OUTLINE OF THE GEKKOTAN SKULL

Contour variations (i.e. global variations of shape) were identified by means of the uniform components. For the entire sample in both data sets, explicit deformations were present in the anteroposterior (u1, shearing) and mediolateral/dorsoventral (u2, dilation–compression) axis (Figs 3, 4). The uniform components of skull shape differed between diet and taxonomic families categories. The differences were statistically significant when these components were analysed together and separately (Table 3). In the lateral view, there are significant differences among the components in the family category. In the diet category u1, and u1 + u2 were not significantly different; only u2 was marginally significant. For both taxonomic families and diet categories, Pearson correlation coefficients were higher in the analyses of the dorsal view data (Table 4). Almost all the correlations were negative [i.e. a high value in u1 (skull length) predicts a low value in u2 (skull width)]. The highest positive correlation was obtained for the sample of pygopodids, indicating that, in those specimens, there is a direct relation between skull length and both width and height variables. Another positive correlation was found between u1 and u2 for



683

3 14, 31, 33, 34 14, 25, 34 1, 6, 8, 10, 14, 15, 16, 21, 25, 28, 29, 31, 34, 35, 42, 47, 55 22, 25

Diplodactylus conspicillatus Diplodactylus damaeus Diplodactylus pulcher

I

Diplodactylus stenodactylus Diplodactylus tessellatus Eurydactylodes vieillardi Hoplodactylus duvaucelii Hoplodactylus maculatus Oedura reticulata Oedura tryoni Phyllurus isis

I

Phyllurus nepthys

I I

X

X

14, 15, 17, 21, 25, 30, 31, 33, 34, 35 3, 22, 47

3, 14, 15, 17, 22, 25, 28, 29, 31, 34, 35 14, 15, 17, 21, 22, 25, 30, 31, 33, 34, 35 15

I I V

X

P

X

I I I

X

X

Mass/Volume

Food item

Lateral views

I I I I

Qualitative

crassicollis exsuccida geitaina sauvagii

3, 14, 31, 33

Frequency

Bavayia Bavayia Bavayia Bavayia

I

Numbers

Diplodactylidae Bavayia cyclura

Dorsal views

Diet Type

Table 2. Diet composition of 105 species of gekkotans

X

X

X

X

X

X X X X

X

X

X

X

X

X

X

X

X

X

X

X

X

X

X

52

X

Bauer & DeVaney (1987); Bauer & Sadlier (2000) Bauer & Sadlier (2000) Bauer & Sadlier (2000) Bauer & Sadlier (2000) Bauer & DeVaney (1987); Bauer & Sadlier (2000) Pianka & Pianka (1976) Henle (1991)

X

Pianka & Pianka (1976); Pianka (1986) Pianka & Pianka (1976); Pianka (1986) Henle (1991)

X

40

X X X X X

I

21, 25, 31,35

X

Phyllurus ossa

I

14, 25

X

Phyllurus platurus

I

X

Pseudothecadactylus lindneri

G

2, 4, 5, 6, 8, 14, 16, 20, 21, 22, 25, 28, 31, 33, 35, 42 3, 38, 40

Rhacodactylus auriculatus

O

1, 4, 14, 15, 21, 24, 25, 28, 31, 33, 34, 35, 40, 42, 43, 48, 49, 51, 52

X

X

Bauer & Sadlier (2000) Barwick (1982) Whitaker (1987)

3, 14, 21, 22, 25, 35 21, 25 21, 25, 35

X

References

X

X

X

X

X

Greer (2006) Bustard (1968b) Couper & Gregson (1994) Couper & Gregson (1994) Couper & Gregson (1994) Green (1973); Rose (1974); Doughty & Shine (1995) Bauer (1990a); Husband & Irwin (1995); Greer (2006) Bavay (1869); Bauer (1985, 1990a, b); Bauer & DeVaney (1987); Bauer & Vindum (1990); Bauer & Sadlier (1994, 2000)


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J. D. DAZA ET AL.

Rhacodactylus leachianus

Qualitative

X

Frequency

X

Numbers

Lateral views

O

Mass/Volume

Dorsal views

Rhacodactylus ciliatus

Food item

Diet Type

Table 2. Continued

3, 52

X

O

15, 37, 45, 52

X

Rhacodactylus sarasinorum Rhacodactylus trachyrhynchus Rhynchoedura ornata

I

15, 16

X

X

3, 52

X

X

14, 15, 16, 33, 47

Strophurus assimilis

P

Strophurus ciliaris

I

X

Strophurus elderi

I

X

Strophurus intermedius Strophurus michaelseni Strophurus rankini Strophurus spinigerus

I

Strophurus strophurus

I

O I

X

I I O

Carphodactylidae Nephrurus asper

21, 31, 34, 35 1, 3, 13,14, 21, 22, 23, 24, 25, 31, 33, 34, 35, 47, 53, 55 8, 13,14, 15, 17, 21, 23, 24, 25, 28, 29, 31, 32, 33, 34, 35

I

X

X

X

X

X

X

X

X

X

X

X

X

How et al. (1986)

X X

X X

X X

How et al. (1986) How et al. (1986); Greer (2006)

X

X

X

X

X X

X

4, 21, 25

Nephrurus deleani Nephrurus laevissimus

G G

X

X

Nephrurus levis

G

X

X

Nephrurus milii

V

X

X

Nephrurus sheai Nephrurus vertebralis Saltuarius cornutus Saltuarius salebrosus

40 4, 8, 10,14, 15, 17, 21, 22, 25, 28, 29, 31, 33, 35, 40, 42, 47 4, 10, 14, 15, 17, 21, 25, 31, 39, 40

X

Pianka & Pianka (1976); How et al. (1986) X X

X

X

X

X

X

X

3, 39

X

I

22, 35

X

G

4, 10, 14, 15, 31, 40, 42 14, 21, 25 14, 21, 25

I I

X

Bauer & Sadlier (2000); Kullmann (1995) Roux (1913); Mertens (1964); Bauer & DeVaney (1987) Roux (1913) Meier (1979); Myers & Pether (1997) Hosmer (1956); Pianka & Pianka (1976) Gaikhorst & Lambert (2005) Pianka & Pianka (1976); How, Dell & Wellington (1986) Pianka & Pianka (1976); How et al. (1986) How et al. (1986)

53 4, 8, 10,14, 15, 21, 23, 24, 25, 28, 29, 31,32, 33, 35, 42, 47 8, 10,14, 15, 21, 22, 23, 24, 25, 28, 29, 31, 33, 34, 35, 47, 55 14, 21, 25, 31, 33, 34, 35, 47, 55 14, 25, 31, 35

References

X

X

X X X

Couper & Gregson (1994) Harvey (1983) Pianka & Pianka (1976) How et al. (1990); Pianka & Pianka (1976) McPhee (1979); Bauer (1990a); How et al. (1990) Couper & Gregson (1994) Pianka & Pianka (1976) Couper et al. (1993) Couper et al. (1993)



685

I

Delma inornata

I

Lialis burtonis

V

Lialis jicari

V

Pygopus lepidopodus

G

X

X

Pygopus nigriceps

I

X

X

Coleonyx brevis

I

X

X

Coleonyx variegatus

O

X

X

Eublepharis macularius

V

X

X

Eublepharis turcmenicus Sphaerodactylidae Aristelliger cochranae

X

X

33, 35 33 3, 14, 21, 25, 28, 31, 33, 35 3, 8, 14, 16, 21, 25, 33, 35 3, 14, 21, 25, 35

X

X

X

X

X X X

X

X

X

37, 39, 42, 43, 44

X

X

X

43

X

3, 14, 21, 25, 31, 33, 38, 43 3, 10, 14, 25, 31, 33

X

X

X

X

X

X

X

X

X

X

X

X

X

X

Food item

Qualitative

Delma impar

Frequency

I I I

Numbers

Pygopodidae Aprasia Aprasia aurita Delma

10, 12, 13, 14, 16, 22, 25, 27, 28, 29, 31, 33, 34, 35 10, 11, 12, 14, 15, 21, 22, 25, 28, 31, 33, 42, 47, 49, 51 39, 40

V

39

G

11, 14, 22, 25, 31, 33, 34, 35, 40, 41 1, 2, 4, 5, 8, 9, 11, 13, 14, 16, 19, 21, 22, 24, 25, 26, 27, 28, 29, 31, 33, 34, 35 1, 2, 4, 5, 8, 9, 11, 13, 14, 16, 22, 25, 28, 29, 33, 34, 42 1, 2, 4, 5, 9, 11, 14, 16, 20, 21, 22, 25, 28, 29, 31, 33, 34, 42

Coleodactylus amazonicus

I

Coleodactylus septentrionalis

I

Gonatodes hasemani

I

Gonatodes humeralis

O

X

Pristurus

I

X

X

Lepidoblepharis xanthostigma

G

X

X

X

Mass/Volume

Lateral views

Dorsal views

Diet Type

Table 2. Continued

1, 4, 5, 8, 9, 11, 13, 14, 15, 16, 20, 21, 22, 25, 28, 29, 31, 33 34, 35, 42, 47, 54 14, 22, 25, 28, 31, 33, 34 14, 16, 21, 22, 29, 35, 37

X

X

X

X

References

Webb & Shine (1994) Greer (2006) Patchell & Shine (1986) Nunan (1995) Patchell & Shine (1986); Nunan (1995) Patchell & Shine (1986) Patchell & Shine (1986) Hoser (1985); Patchell & Shine (1986) Patchell & Shine (1986) Dial (1978)

Parker & Pianka (1974) Prater (1922); Smith (1935); Minton (1966); Daniel (1983) Szczerbak & Golubev (1986)

X

Gifford, Powell & Steiner Jr, 2000 Vitt et al. (2005)

X

Vitt et al. (2005)

X

X

X

X

X

X

X

X

Nascimento, Avila-Pires & Cunha (1988); Vitt et al. (2005) Nascimento et al. (1988); Vitt et al. (2005)

X

Arnold (1993) Vitt et al. (2005)


686

J. D. DAZA ET AL.

X

I

X

Sphaerodactylus townsendi

I

X

Sphaerodactylus vincenti Teratoscincus scincus Phyllodactylidae Gymnodactylus geckoides

X

3, 4, 5, 10, 14, 17, 21, 22, 23, 25, 31, 33, 34, 35, 42, 47 12, 13, 14, 25, 29, 31, 33 8, 10, 14, 19, 20, 22, 25, 29, 30, 31, 33, 35, 42 1, 4, 5, 8, 9, 11, 12, 14, 15, 17, 20, 25, 29, 30, 31, 33, 34, 35, 40, 45, 47

X

I V

X

I

Homonota gaudichaudi Ptyodactylus hasselquistii

I I

X

X

Tarentola mauritanica

G

X

X

Thecadactylus rapicauda

I

X

X

1, 10, 14, 21, 25, 35

G

X

X

3, 10, 14, 21, 22, 25, 31, 33, 37, 40, 42

Gekkonidae Chondrodactylus angulifer

Christinus guentheri

I

4, 7, 14, 15

Colopus wahlbergii

I

Cyrtodactylus cavernicolus Cyrtodactylus louisiadensis

V

3, 10, 14, 21, 22, 25, 28, 33, 35, 42 45

V

37, 38

Qualitative

I

X

Frequency

Quedenfeldtia trachyblephara Sphaerodactylus macrolepis

1, 5, 9, 11, 13, 14, 16, 22, 25, 27, 28, 29, 31, 34 14, 22, 25, 28, 31, 33, 34 1, 2, 4, 5, 8, 11, 14, 16, 20, 21, 22, 25, 27, 28, 31, 33, 34, 42 1, 2, 4, 5, 8, 11, 13, 14, 16, 19, 20, 21, 22, 25, 26, 27, 31, 33, 34, 42 1, 8, 13, 14, 16, 20, 21, 29, 31, 33, 34, 35 39

Numbers

X

Mass/Volume

I

Food item

Dorsal views

Pseudgonatodes guianensis

Lateral views

Diet Type

Table 2. Continued

References

X

Duellman (1978); Vitt et al. (2005)

X

Arnold (1993)

X

X

Gaa-Ojeda (1983)

X

X

Gaa-Ojeda (1983)

Steinberg et al. (2007) X X

X

Colli et al. (2003); Vitt et al. (2007)

X

X

Marquet et al. (1990)

X

X

X

Perry & Brandeis (1992)

X

X

X

Rieppel (1981); Barbadillo (1987); Gil, Guerrero & Pérez-Mellado (1994); Hódar et al. (2006) Beebe (1944); Hoomoed (1973); Martins (1991); Avila-Pires (1995)

X

X

X

X

Loveridge (1947); Brain (1962); Haacke (1976); Pianka & Huey (1978); Letnic & Madden (1997) Cogger, Sadlier & Cameron (1983); Greer (2006) Pianka & Huey (1978)

X

Harrison (1961)

X

Wilcox (1999); Greer (2006)

X

X

Minton (1966)



687

Qualitative

Frequency

Numbers

Mass/Volume

Food item

Lateral views

Dorsal views

Diet Type

Table 2. Continued

Gehyra australis

O

40, 53

X

Gehyra dubia

P

3, 52, 53

X

Gehyra variegata

G

4, 8, 11, 14, 15, 17, 21, 22, 24, 25, 28, 29, 30, 31, 32, 33, 34, 35, 39, 40, 42, 47

Gehyra vorax

P

52

X

Gekko gecko

V

X

X

40, 44, 45, 46

X

Hemidactylus brookii Hemidactylus flaviviridis Hemidactylus frenatus

V V

X

X

40 40

X X

G

X

X

14, 15, 18, 25, 28, 31, 33, 34, 35, 40

Hemidactylus garnotii

O

X

X

15, 21, 22, 25, 31, 35, 47

X

Hemidactylus leschenaultii Hemidactylus mabouia

V

X

X

40, 46

X

G

X

X

8, 14, 29, 38, 39, 40

Hemidactylus maculatus Hemidactylus turcicus

V

40

G

Hemiphyllodactylus typus Heteronotia binoei

I

1, 4, 13, 14, 16, 20, 21, 22, 25, 26, 28, 29, 31, 32, 33, 34, 35, 36, 39 1, 21, 34

G

4, 13, 14, 15, 17, 21, 22, 25, 28, 29, 30, 31, 33, 34, 35, 39, 42, 47

X

X

X

X

X

X

X

X

X

X

X X

X

X

X X

X

X

X

References McCoid & Hensley (1993) Burnett & Nolen (1996); Bustard (1969); Greer (2006) Bustard (1968a); Pianka & Pianka (1976); Henle (1990); Burnett & Nolen (1996) Gibbons & Clunie (1984) Boulenger (1912); Smith (1935); Rose (1950); Dollinger (1971); Auffenberg (1980); Obst, Richter & Jacob (1984); Tikader & Das (1985) Martínez-Rica (1974) Daniel (1983); Mahendra (1936) Tyler (1961); Chou (1974); Sahi (1979); Bolger & Case (1992); Bauer & Sadlier (2000) Cagle (1946); La Rivers (1948); Oliver & Shaw (1953) Sumithran (1982); Dattatri (1984) Loveridge (1947); Rivero (1998); Zamprogno & Teixeira (1998) Daniel (1983) Hunt (1957); Salvador (1981); Saenz (1996); Krysko, Hooper & Sheehy III (2005) Oliver & Shaw (1953) Bustard (1968b); Pianka & Pianka (1976); Henle (1991)


688

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X

Lygodactylus angularis Lygodactylus capensis Nactus arnouxii

V

40

I

X

I

X

3, 14, 22, 25, 28, 31, 33, 35, 42 4, 6, 7, 8, 10,14, 15, 25, 31, 33, 35, 42, 47

Pachydactylus bribonii Pachydactylus capensis Pachydactylus rugosus Phelsuma madascariensis

I

X

3, 10, 14, 21, 22, 25, 28, 31, 33, 35, 42 3, 10, 14, 21, 22, 25, 28, 31, 33, 35, 42 3, 14, 21, 22, 25, 28, 31, 33, 35, 37, 42 15, 40

X

Ptenopus garrulus

I

X

Ptychozoon kuhli Tenuidactylus caspius

V V

3, 4, 11, 12, 14, 21, 22, 25, 27, 28, 31, 32, 33, 35, 42 40 39

I G G

X

Food item 7, 14, 20, 22, 25, 33, 34, 35, 41, 47, 49, 50, 51, 52

Qualitative

X

Frequency

Lateral views

O

Numbers

Dorsal views

Lepidodactylus lugubris

Mass/Volume

Diet Type

Table 2. Continued

X

X

References

X

La Rivers (1948); Oliver & Shaw (1953); Miller (1979); McCoy (1980); McCoid & Hensley (1993); Hanley, Bolger & Case (1994); Perry & Ritter (1999) Loveridge (1947)

X

Pianka & Huey (1978)

X

X

Medway & Marshall (1975); Bauer & DeVaney (1987) Pianka & Huey (1978)

X

X


X

X


X

García & Vences (2002); Krysko et al. (2005) Pianka & Huey (1978); Hibbitts et al. (2005)

X

X

X

X

X

X X

Mitchell (1986) Szczerbak (1981)

Those species included in the analysis are indicated. See text for diet type. Numbers represent food items: 1, Gastropoda; 2, Oligochaeta; 3, Unspecified Arthropoda; 4, Chilopoda; 5, Diplopoda; 6, Crustacea; 7, Amphipoda; 8, Isopoda; 9, Opiliones; 10, Scorpiones; 11, Pseudoscorpionida; 12, Solfugida; 13, Acari; 14, Araneae; 15, Unspecified Insecta; 16, Collembola; 17, Thysanura; 18, Odonata; 19, Embiopetera; 20, Dermaptera; 21, Blattaria; 22, Isoptera; 23, Mantodea; 24, Phasmida; 25, Orthoptera; 26, Psocoptera; 27, Thysanoptera; 28, Hemiptera; 29, Homoptera; 30, Heteroptera; 31, Coleoptera; 32, Neuroptera; 33, Hymenoptera; 34, Diptera; 35, Lepidoptera; 36, Trichoptera; 37, Unspecified Tetrapoda; 38, Frogs; 39, Lizards; 40, Geckos; 41, Gecko eggs; 42, Gecko skin; 43, Skinks; 44, Snakes; 45, Birds; 46, Rodent; 47, Plant material; 48, Leaf; 49, Anthers; 50, Nectar; 51, Stamens ; 52, Fruits; 53, Sap; 54, Fungus; 55, Sand.

gekkotans feeding on vertebrates in the lateral view analysis. The u1 component obtained in the dorsal view analysis (Figs 3A, 4) shows shearing in both directions. From the origin to the negative direction, there is a noticeable shift in the position of the occipital condyle (Fig. 2A, D11) to a more interior position in the skull; the specimens located in that direction have

concave posterior edge; this is the case of long headed gekkonids (Uroplatus fimbriatus). In the opposite direction, the posterior edge of the skull becomes more convex. The u2 component shows dilation toward the positive, with a notable increment of the width between the middle point of the fronto-parietal suture and the lateral vertex of the postorbitofrontal; similarly, the articulation point of the quadrate with



689

Figure 3. Uniform (affine) transformations in dorsal (A) and lateral (B) analysis. Compression/dilation on the lateromedial and dorsoventral planes, and shearing in the anteroposterior plane. Arrows indicate the direction from the reference configuration. Only the landmarks of the left side are shown in (A).

the skull is displaced laterally. These changes produce broad-headed geckos such as Homonota darwini. In the opposite direction, the skull is extremely compressed, almost half the width of the mean shape, as in L. burtonis. In the lateral view analyses, the shearing of the skull along the u1, from the origin to the negative direction, causes the ventral landmarks to be shifted posteriorly, indicating a shortening of the snout; in the opposite direction, the snout is enlarged. The component u2 arranges the specimens according to the relative skull height; the specimen with the relatively tallest skull was the carphodactylid Nephrurus levis (BMNH 1910.5.28.2) and the relatively flattest skull was L. burtonis (JFBM 15829).

LOCALIZED

CHANGES IN THE SKULL OF GEKKOTANS

The partial warps were different between the two categories in both analyses. The differences among

the partial warps were also significant when analysed together with the uniform components (full shape space; Table 3). Eighteen relative warps were derived from each geometric morphometric analysis. The first three relative warps accounted for 72.31% of the variation in the dorsal view and 51.46% in the lateral view analysis (Fig. 5). RW1 was plotted against RW2 and RW3 (Figs 5, 6). The closest specimen to the origin in each scatter plot was used as a base with description of changes being given to and from it: Afroedura transvaalica (RW1 versus RW2, Fig. 7) and Gehyra mutilata (RW1 versus RW3; Fig. 8) in the dorsal analysis and Teratoscincus microlepis (RW1 versus RW2; Fig. 9) and Tropiocolotes tripolitanus (RW1 versus RW3; Fig. 10) in the lateral analysis. Using the origins as starting point, we describe changes in skull morphology along the axis in the positive (↑, →) and negative (↓, ←) directions:


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J. D. DAZA ET AL.

Figure 4. Scatter plots for the uniform components for the two descriptors; A, C (Family) and B, D (Diet). Light grey shades enclose the specimens by category.

1. Afroedura transvaalica ↓ Uroplatus (Fig. 7). Changes in this direction are very similar to the changes from G. mutilata ↓ Uroplatus (Fig. 8). In this direction, the snout is extremely amplified, being almost two-thirds the length of the skull. This change in proportion is mainly because of the hypertrophied nasal and maxilla. The premaxilla and the jugal do not grow at the same rate, and they became relatively smaller. Because the snout increases in length, the fronto-parietal suture is displaced posteriorly. The separation between the posterior edge of the jugal and the lateral vertex of the postorbitofrontal becomes shorter, in part due to the lateral displacement of the latter. The jugal and the posterior process of the maxilla are moved laterally, becoming aligned with the lateral edge of the quadrate bone. The parietal becomes relatively shorter and squarer; the space between the posterior edge of the parietal and the occipital condyle is almost obliterated, in part by the transformation

of the posterior edge of the skull from convex to concave. 2. Afroedura transvaalica ↑ Sphaerodactylus klauberi (Fig. 7). In this direction, the snout is shortened, and the skull profile is compressed, changing from broad to narrow. The premaxilla becomes wider anteriorly, forming almost exclusively the tip of the snout. This bone is relatively constant along the gradient change but, because other bones of the skull are reduced, it appears progressively longer, becoming closer to the nasals. The frontoparietal suture curves anteriorly and becomes closer to the nasals. Some reduction in size of the nasal bones may occur, but this could be an artefact of the overlapping of elements in the snout. The parietal bones gradually transform from square to rectangular. The squamosal bone is directed laterally and the occipital condyle bulges out posteriorly. The lateral edge of the squamosal becomes aligned with the jugal.


691

ANALYSIS OF THE GEKKOTAN SKULL Table 3. Statistical analyses performed on the morphological variables Test

Variables

Category

Wilks’ L

F

P

Dorsal analysis MANOVA ANOVA ANOVA MANOVA MANOVA MANOVA ANOVA ANOVA MANOVA MANOVA ANOVA ANOVA

u1, u2 u1 u2 Partial warps u1, u2, partial warps u1, u2 u1 u2 Partial warps u1, u2, partial warps Skull length Skull length

Diet

0.61912

Family

0.32542 0.28627 0.36119

17.61 23.83 3.88 5.01 5.00 33.97 38.80 33.58 10.30 11.53 53.21 30.66

0.000* 0.000* 0.004* 0.000* 0.000* 0.000* 0.000* 0.000* 0.000* 0.000* 0.000* 0.000*

Lateral analysis MANOVA ANOVA ANOVA MANOVA MANOVA MANOVA ANOVA ANOVA MANOVA MANOVA

u1, u2 u1 u2 Partial u1, u2, u1, u2 u1 u2 Partial u1, u2,

Diet

0.88744

Family

0.39909 0.37390 0.62669

1.68 0.93 2.35 1.55 1.45 6.93 10.15 4.25 3.78 4.37

0.105 0.450 0.059† 0.007* 0.015* 0.000* 0.000* 0.001* 0.000* 0.000*

0.07149 0.04137 Diet Family

warps partial warps

warps partial warps

0.12631 0.07397

*Statistically significant differences. †Marginally significant. ANOVA, analysis of variance; MANOVA, multivariate analysis of variance.

3. Afroedura transvaalica ↑ Pygopus nigriceps (Fig. 7). The skull profile in general becomes narrower. The snout is shortened by reduction of nasals and the anterior displacement of the frontoparietal suture, almost achieving the level of the posterior process of the jugal. The parietal bone(s) become(s) rectangular and elongated, leaving a space between the posteromedial process of the parietal and the supraoccipital (post-temporal fossae). By contrast to the changes toward S. klauberi, the fronto-parietal suture is straighter, and the jugal becomes aligned with the quadrate instead of the squamosal. 4. Afroedura transvaalica ← Pristurus (Fig. 7). Changes in this direction are very similar to the changes from G. mutilata → Pristurus (Fig. 8). In general, the skull becomes slightly narrow. The snout elongates, becoming almost arrow-shaped. The premaxilla is hypertrophied, forming exclusively the tip of the snout. The nasals are shortened and posteriorly located. These changes generate very large external nares. The frontoparietal suture is shifted posteriorly, and the parietals become shorter and squarer. The

postorbitofrontal vertex is shifted posterior to the fronto-parietal suture. The distance between the posteromedial process of the parietal and the occipital condyle is reduced. 5. Afroedura transvaalica → Homonota darwinii (Fig. 7). In this direction, the snout becomes broader, as demonstrated by the lateral displacement of the jugal and maxilla. The length of the snout is somewhat shorter because the premaxilla and nasals growth relatively smaller. The distance between the jugal and the postorbitofrontal becomes reduced by anterior projection of the latter, and the anterior shift of the fronto-parietal suture. The parietal(s) and the occipital condyle move forward. 6. Gehyra mutilata ↑ L. burtonis (Fig. 8). By contrast to other gekkotans where the snout elongates, in this direction, all the superficial bones of the facial series of the dermatocranium are hypertrophied (i.e. premaxilla, maxilla, nasals). Similar to transformation 5 above, the snout tip is exclusively formed by the premaxilla. The most radical transformation is seen in this direction in terms of extreme elongation and lateral compression of the


692

J. D. DAZA ET AL.

Table 4. Pearson correlation coefficient values between the morphological variables and the descriptors Dorsal analysis

Lateral analysis Skull length versus

u1 versus u2

RW1

Skull length versus u1 versus u2

RW1

Group

r (dorsal)

P

r (dorsal)

P

r (lateral)

P

r (lateral)

P

Invertebrates Vertebrates Generalist Plant material consumer Omnivorous Gekkota Diplodactylidae Carphodactylidae Pygopodidae Eublepharidae Sphaerodactylidae Phyllodactylidae Gekkonidae

-0.353 -0.668 -0.589 –

0.000* 0.000* 0.000* –

-0.813 0.02 -0.461 –

0.000* 0.911 0.002* –

-0.154 0.613 -0.075 –

0.386 0.000* 0.706 –

-0.774 -0.039 -0.271 –

0.000* 0.84 0.211 –

-0.89 -0.301 -0.773 -0.871 0.837 -0.56 -0.154 0.035 -0.234

0.000* 0.000* 0.001* 0.005* 0.019* 0.005* 0.076† 0.828 0.029*

-0.768 -0.717 -0.89 0.455 -0.202 -0.369 -0.814 -0.67 -0.661

0.000* 0.000* 0.000* 0.258 0.664 0.083 0.000* 0.000* 0.000*

-0.419 0.034 -0.171 -0.188 0.7 -0.238 -0.026 -0.286 0.038

0.074 0.633 0.559 0.628 0.080† 0.326 0.909 0.14 0.758

-0.602 -0.458 -0.62 -0.374 0.079 0.073 -0.639 -0.41 -0.499

0.011* 0.000* 0.018* 0.321 0.867 0.768 0.001* 0.030* 0.000*

u1 -0.713

Gekkota

u1 0.000*

-0.399

u2 Gekkota

0.083

0.000* u2

0.143

-0.032

0.681

*Statistically significant. †Marginally significant. Values in bold indicate high correlations.

skull; throughout this change, the fronto-parietal suture moves forward towards the mid-point of the skull, the jugal also becomes aligned with the squamosal, and the postorbitofrontal becomes very reduced. The parietal(s) become(s) elongated and rectangular. The space between posteromedial process of the parietal and the occipital condyle increases, creating large post-temporal fossae. 7. Gehyra mutilata ↑ Pseudogonatodes barbouri (Fig. 8). The snout becomes shorter but the premaxilla changes as in S. klauberi, where it is very long and has shifted toward the posterior nasal process. The maxilla is shortened. The postorbitofrontal vertex is shifted anterior to the frontoparietal suture, which is shifted anteriorly and is also curved. The jugal becomes aligned with the squamosal. The supraoccipital becomes more prominent and exposed, and the space between posteromedial process of the parietal and the occipital condyle increases but, in contrast to transformation 5 above, a post-temporal fossa is not formed. The occipital condyle bulges out. 8. Gehyra mutilata ← Coleonyx mitratus (Fig. 8). In general, the skull becomes compressed laterally

and is relatively longer. The snout is longer, mainly by elongation of nasals and the frontal bone. The premaxilla is short and broad, still forming the tip of the snout. Contrary to transformations 5 and 7 above, the postorbitofrontal vertex is shifted to an anterior position. The occipital condyle moves anteriorly into the skull. General changes along RW1, from the negative to the positive direction, comprise: snout shortened, premaxilla broadened anteriorly, its ascending nasal process enlarged, nasals shortened, jugal aligned with the squamosal producing a low profile of the skull; fronto-parietal suture changing from straight to curved anteriorly, its position shifted to the middle of the skull. The orientation of the quadrate shifts from a lateral to an anterior position; the space between the posteromedial process of the parietal and the occipital condyle becomes larger, in part due to the bulging of basioccipital. Simultaneously, the rear edge of the skull changes from concave to convex. Along RW2 from the negative to the positive direction, the snout is shortened slightly and broadened. The ascending nasal process of the premaxilla and the



693

Figure 5. Scatter plots of the relative warps 1, 2, and 3, for dorsal (A, B) and ventral (C, D) analyses. Specimens are sorted by family, as indicted by symbols and the light grey shading.

nasals become shorter; the fronto-parietal suture moves anteriorly, although it does not reach the middle of the skull. The lateral vertex of the postorbitofrontal changes from being aligned with the jugal to being aligned with the squamosal. The parietal becomes rectangular, and the posteromedial process moves forward, increasing the space between it and the occipital condyle. On the RW3 from the negative to the positive direction, the changes are a combination of the changes seen in RW1 and RW2. The snout becomes broader with the ascending nasal process of the premaxilla enlarged; the maxilla is also enlarged, extending posteriorly; and the fronto-parietal suture becomes curved and situated anteriorly. The main changes in lateral skull morphology along RW1, RW2, and RW3 axes comprise: 9. Teratoscincus microlepis ↓ Uroplatus (Fig. 9). Changes in this direction are very similar to the changes from T. tripolitanus ↓ Uroplatus

(Fig. 10). As was seen in the dorsal analysis, the snout is enlarged in this direction, which produces a movement of the jugal towards the basipterygoid process and the most ventral edge of the postorbitofrontal towards the crista alaris. In the back of the skull, the posterior edge of the quadrate moves caudad to the posterior part of the skull behind the fenestra ovalis, which creates a distinct condition where the auditory meatus is oriented lateroposteriorly. The dorsal process of the prefrontal is lifted to the level of the skull table and, in some specimens, the portion of the frontal behind the dorsal process can be higher than the skull table, as in Uroplatus. 10. Teratoscincus microlepis ↑ Lepidoblepharis xanthostigma (Fig. 9). Changes in this direction are very similar to the changes from T. tripolitanus ↑ L. xanthostigma (Fig. 10). In this direction, the skull is depressed and the snout is reduced. The ventral edge of the postorbitofrontal is shifted to


694

J. D. DAZA ET AL.

Figure 6. Scatter plots of the relative warps 1, 2, and 3, for dorsal (A, B) and ventral (C, D) analyses. Specimens are sorted by diet, as indicted by symbols and the light grey shading.

the middle of the skull. The dorsal process of the prefrontal moves down anteroventrally. The posterior part of the quadrate process of the pterygoid rises, reducing the ventral projection of the skull and making it flatter. The posterior edge of the quadrate moves forward to a more anterior position in the basicranium. 11. Teratoscincus microlepis ← Rhacodactylus auriculatus (Fig. 9). A small increase in snout length occurs. The skull table rises and the dorsal process of the prefrontal moves somewhat downward. The most visible change is the extreme ventral projection of the postorbitofrontal. The posterior part of the quadrate process of the pterygoid rises, but the ventral profile is not flat because the pterygoid is curved downwards. 12. Teratoscincus microlepis → Eublepharis macularius (Fig. 9). In general, the skull becomes higher; the snout length is reduced and the ventral projection of the postorbitofrontal becomes level with the dorsal process of the pre-

frontal and the skull table. The distance between the skull table and the crista alaris is increased. The ventral process of the pterygoid moves ventrad. 13. Tropicolotes tripolitanus ← L. burtonis (Fig. 10). The skull becomes extremely compressed and elongated. In the snout, this compression is even more extreme than indicated by the landmarks because the ventral edge of the maxilla is concave and elongated. The jugal and the fronto-parietal suture move forward to the middle of the skull. The quadrate process of the pterygoid rises, reducing the skull profile. The dorsal process of the prefrontal, postorbitofrontal, and the jugal approach each other, defining the orbit a bit more clearly. These landmarks are well separated from the landmarks on the basicranium. 14. Tropicolotes tripolitanus → Pristurus carteri (Fig. 10). The snout profile becomes higher, indicated by the rising of the dorsal process of the prefrontal. The jugal descends and the basiptery-



695

Figure 7. Species located at the extremes when RW1 is plotted against RW2 in dorsal view. Closest specimen to origin: Afroedura transvaalica (BMNH 1960.1.7.6). Clockwise: Sphaerodactylus klauberi (UPRRP 6426), Pygopus nigriceps (AMNH R-24915), Homonota darwinii (FML uncataloged), Uroplatus sp. FMNH 250684), Pristurus sp. (AMNH R-20056).

goid process approach to it. The postorbitofrontal is positioned very close to the crista alaris. The quadrate process of the pterygoid lowers, making the back part of the skull higher. General changes along the RW1, from the negative to the positive direction comprise: skull compressed, snout reduced in length, postorbitofrontal and frontoparietal suture moved forward to the middle of the skull, the posterior edge of the quadrate moved away from the posterior edge of the skull, skull table risen, becoming the highest point of the cranium. Along the RW2 from the negative to the positive direction, the skull dilates, the snout is shortened slightly, the ventral process of the postorbitofrontal changes from being ventrally directed to being level with the dorsal process of the prefrontal and the skull table; the basipterygoid process and the quadrate process of the pterygoid are lowered, conferring a higher profile to the basicranium. RW3 also indicates dilation of the

skull and backward movement of the postorbitofrontal. The posterior edge of the quadrate moves from being dorsal to the most posterior edge of the skull to a position in front of it; the basipterygoid process grows downward, reducing its distance from the jugal and increasing the basicranium elevation.

DIET

AND THE SKULL SHAPE OF GEKKOTANS

In the dorsal analysis, diet was a less powerful descriptor of the morphological variables than taxonomic families. In all trials, there were significant differences among the means of the components of shape, which were analysed combined and separated (Table 2); family categories obtained F-values higher than diet. In the analysis of lateral views, diet was a very ineffective descriptor of the morphological variables, demonstrating only significant differences between the partial warps and the full shape space (u1, u2, partial warps).


696

J. D. DAZA ET AL.

Figure 8. Species located at the extremes when RW1 is plotted against RW3 in dorsal view. Closest specimen to origin: Gehyra mutilata (USNM 499247). Clockwise: Lialis burtonis (AMNH R-20883), Pseudogonatodes barbouri (AMNH R-146757), Pristurus sp.(AMNH R-20032), Uroplatus sp. (FMNH 250684).

With a few exceptions, gekkotans are predators (Figs 11, 12; Table 2). Insects are their most common prey, comprising 60% of the overall diet choice. They prey on 21 orders of insects, with orthopterans predominating (60 of the 105 species with diet information). Other important orders were Coleoptera, Hymenoptera, Blattaria, and Lepidoptera. The second most important group was the Arachnida (15%), in which six of the extant orders (Opiliones, Scorpiones, Pseudoscorpiones, Solifugae, Acari, and Araneae) were preyed upon. The spiders are a very important group, consumed by 62 of the species with diet information, and slightly outnumbering orthopterans. A diet comprising only invertebrates was found in members of each one of the families (Fig. 12). In the plots of the uniform components of the dorsal analyses, all the specimens that experienced shearing in the positive direction preyed mainly on invertebrates (Fig. 6). As indicated by the contour of these animals, they have an occipital condyle that bulges, which is a general character of miniaturized forms repre-

sented in the sample by some sphaerodactylids and pygopodids. Diets including vertebrates are found in members of all families except in the Phyllodactylidae (Fig. 12). In the sample, 58 species of gekkotans fed on tetrapods (7%), with 48 being saurophagous (including snakes), although other prey such as frogs, rodents and birds have been reported. From the analysis of the skull shape, the most obvious adaptation to this diet was in the pygopodids of the genus Lialis, whose skulls are compressed in both the dorsal and lateral planes (Figs 8, 10). Teratoscincus scincus, which also feeds on vertebrates, has a long snout, as indicated by the proximity of the postorbitofrontal (which clasps the fronto-parietal suture) to the crista alaris. A long snout might be an adaptation to a vertebrate diet, although it is not necessarily unique to these animals. The long snout may indicate greater mesokinetic flexing and better handling of larger prey. Gekkotans feeding on both vertebrates and invertebrates were found in all families (Fig. 12) and



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Figure 9. Species located at the extremes when RW1 is plotted against RW2 in lateral view. Closest specimen to origin: Teratoscincus microlepis (AMNH R-88524). Clockwise: Lepidoblepharis xanthostigma (USNM 313834), Eublepharis macularius (CM 67524), Uroplatus fimbriatus (BMNH 61.3.20.9), Rhacodactylus auriculatus (UMMZ 190951).

Figure 10. Species located at the extremes when RW1 is plotted against RW3 in lateral view. Closest specimen to origin: Tropiocolotes tripolitanus (BMNH 97.10.28.7). Clockwise: Lepidoblepharis xanthostigma (USNM 313834), Pristurus carteri (BMNH 1971.44), Uroplatus fimbriatus (BMNH 61.3.20.9), Lialis burtonis (JFBM 15829).

omnivory was scored in the Diplodactylidae, Eublepharidae, Sphaerodactylidae, and the Gekkonidae (Fig. 12). Phytophagy has been reported only in the Gekkonidae and Diplodactylidae (Fig. 12) and appears to be a derived behaviour among gekkotans. There are records of gekkotans consuming floral parts, such as anthers, nectar, and stamens. Four

species lick sap from trees and Hoplodactylus maculatus is truly frugivorous (Whitaker, 1987). Gekkotans with these types of feeding behaviour were too poorly represented in both data sets to produce statistically significant values, although some general results can be pointed out. Hoplodactylus maculatus and Hemidactylus garnotii were the only two species that could be categorized as phytophages. These two


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Figure 11. Chart with the food items consumed by gekkotans, based on previous observations of 105 species.

Figure 12. Phylogenetic relationships of Gekkota and feeding behaviour. I, invertebrate predators; V, vertebrate predators; G, generalist predator; O, omnivorous; P, plant material consumers (tree topology sensu Kluge & Nussbaum, 1995; Conrad, 2008; Gamble et al., 2008b). © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 677–707


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Table 5. Values obtained from the Tukey’s honestly significant difference test for the dietary groups

Generalist Vertebrates Invertebrates Plant material consumer* Omnivorous

Generalist

Vertebrates

Invertebrates

Plant material consumer*

Omnivorous

–

0.000048 –

0.000017 0.000017 –

0.96083 0.199071 0.662347 –

0.870899 0.000031 0.00002 0.997859 –

*Small sample size. The values are the P-values for each pairwise comparison of the skull length mean values. Values in bold indicate differences among groups.

species are distributed in different quadrants in all the scatter plots. Only H. maculatus is clustered with species that exhibit shortening of the snout and higher skulls, which is a combination of characters that has been attributed to truly herbivorous lizards (Metzger & Herrel, 2005). Hemidactylus garnotii appeared to be distributed around lizards with an inclination to increased snout length.

MORPHOLOGICAL

CHANGES ATTRIBUTABLE

TO SKULL SIZE

There were statistically significant differences between skull length in both family and diet categories (Table 3). In this case, diet performs better as a descriptor because there is a direct relationship between size and the kind of prey. Again, Pearson correlation coefficients were higher for the dorsal than for the lateral analysis. In the dorsal analysis for all Gekkota, the correlation was high between component u1 (i.e. global changes along the anterodorsal axis) and skull size (Table 4). The relation was negative, however, which could be explained as a result of changes in the rear part of the skull: as size increases, the posterior edge becomes concave, generating a relatively shorter distance between the tip of the snout and the occipital condyle. In the opposite direction, when skull size reduces, the posterior edge becomes convex, generating a relative higher distance between the same parts. We found similar Pearson correlation coefficients when skull length was compared with the RW1, with statistical significance for the families Diplodactylidae, Carphodactylidae, Sphaerodactylidae, Phyllodactylidae, and Gekkonidae. The mean size of the skull of phytophages was not different from the sample of generalist, invertebrate, vertebrate, and omnivorous predators; the same was also found for omnivorous and generalist predators (Table 5).

DISCUSSION Geometric morphometrics analysis (GMA) is a powerful tool that allows the comparison of multiple

specimens to infer general patterns of shape variation. To describe changes in three-dimensional structures, it is advantageous to analyse shape variation in different planes. Phylogenetic affinity (family) was a better descriptor of skull shape than feeding behaviour. Similar conclusions were found in GMA of the Rhynchocephalia (Jones, 2008). With the exception of herbivory and omnivory, which have evolved in several lineages, it is difficult to study the effects of diet on the morphology (Cooper, 2000). One factor affecting the poor performance of diet as a descriptor of the skull is that the categories defined are not discrete, and there might be similarities in their food item contents. For example, the generalist and vertebrate categories share vertebrate prey items, as do the omnivores and generalists. On the other hand, other factors might be more important in shaping the skull of some groups such as the Pygopodidae. This group occupies a wide range of habitats, including subterranean ones (Underwood, 1957; Gans, 1986), and this may have evolved at least two times (Shine, 1986) in this group. They also exploit different prey (Shine, 1986), with some taxa feeding exclusively on ants (Aprasia) and others being saurophages (Lialis) that prey upon geckos, skinks, and snakes (Patchell & Shine, 1986). This group also appears to comprise the only true wide-foraging members of the Gekkota (Bauer, 2006). All of them were found to have undergone lateral and dorsoventral compression of the skull. Among tetrapods, body elongation has been correlated with morphological changes such as limb loss (Gans, 1975); it is possible that, in the case of pygopodids, changes in the skull are also coupled with limb loss. The morphological differences found between animals feeding exclusively on invertebrates versus the other categories might be explained by size differences only. For example, the miniaturized sphaerodactylids clustered by skull shape in an area where the snout is shortened and compressed, the lateral profile narrowed, and quadrates directed anteriorly. These changes lead to a reduction in the length of the


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jaw, which mechanically translates into a slower closing speed than that occuring in animals with longer jaws (Metzger & Herrel, 2005). These animals are specialists on ground-dwelling invertebrates such as earthworms, millipeds, collembola, acari, pseudoscorpions, opiliones, and embiopterans, with some of them comprising slow moving prey of small size. Another consequence of having relatively shorter skulls is the increase of the jaw closing in-lever, which might generate higher bite forces. Overlapping of bones in the snout, as corroborated by results obtained in the present study, might be a response to this increase of mechanical stress. In general, animals with larger skulls are capable of exploiting a wide range of food items, whereas small-headed animals are constrained to prey on small sized animals, especially invertebrates. Differences in head and body size have an effect on bite force capacity, which is important for prey selection, either directly, or via prey handling efficiency (Verwaijen et al., 2002; McBrayer & Corbin, 2006; Reilly & McBrayer, 2006). Invertebrate predation is widespread and is most likely the ancestral condition for gekkotans (e.g. most geckos are generalist arthropod feeders; Bauer, 2006); additionally, a general shift to above ground microhabitats is present in this clade (Vitt et al., 2003). These two factors, when coupled with the development of digital scansors, allow many gekkotans to move on perpendicular or inverted substrates where many spiders dwell. This might be an explanation for their frequent predation on spiders. Feeding on vertebrates is also widespread among gekkotans and might also have been present subsequent to the origin of the group. Some of these species (i.e. the generalists or the omnivores) might consume other prey, but some species appear to have become exclusive saurophages. Saurophagy has been reported in pygopodids, diplodactylids, and gekkonids. Some omnivorous eublepharids with an active foraging mode have been reported to demonstrate chemosensory discrimination for both prey and predators (Dial, 1978; Dial, Paul & Curtis, 1989). Diplodactylids of the genus Rhacodactylus lingually discriminate plant and animal foods, which is a trait that Cooper (2000) considered to be derived. These discrimination systems should be determined by an examination of stomach contents and studies of olfaction and gustation (i.e. the vomeronasal system). Metzger & Herrel (2005) found omnivores not to comprise intermediate forms that are distinct from carnivorous and herbivorous lizards. The results of the present study demonstrate that omnivorous gekkotans are intermediate forms with no uniquely distinct morphology. With the few exceptions listed, gekkotans skulls are not specialized to a particular feeding behaviour. This

lack of specialization might be related to the tremendous morphological modifications that the skull has experienced, producing a highly kinetic skull in gekkotans (Herrel et al., 2000) compared to other lizards. Other specializations not detected by these analyses might be important for feeding behaviour. Examples include the increase of tooth loci in Uroplatus and the dental specializations among the genus Rhacodactylus, which have been strongly correlated with changes in feeding behaviour (Bauer & Russell, 1990). Another explanation for this apparent independence of diet and skull shape is that the general skull phenotype permits the species to feed upon as many items as possible. Gans (1993) stressed that animal phenotypes could be interpreted by considering the merits of adequacy rather than optimality. If this is the case, we are not faced with a close structure– function match. By contrast, most gekkotans appear to exhibit a bauplan that was probably acquired early in their phylogenetic history because they resemble forms such Eichstaettisaurus schroederi, which, although not a true gekkotan, is a basal scincogekkonomorph (Conrad, 2008). Thus, the nature of the changes in skull morphology are more linked to phylogeny than to trophic environment. These results appear to be at odds with those obtained by Metzger & Herrel (2005), who found a clear relationship between dietary and phenotypic specialization in lepidosaurs, ‘As indicated in the nonphylogenetic analyses, herbivores show a tendency towards having skulls, muzzles, retroarticular processes and tooth rows with a relatively reduced length and relatively taller skulls than those of both carnivores and omnivores’ (Metzger & Herrel, 2005). However, it should be taken into consideration that, in the present study, a larger sample of gekkotans was considered as well as more partitioned trophic niche categories. Homoplasy frequently accompanies a size decrease in closely-related groups (Hanken & Wake, 1993). GMA allowed differences to be distinguished in the pattern of morphological change that is attributable to miniaturization. Although miniaturized pygopodids and sphaerodactylids converge in terms of having shorter snouts, sphaerodactylids are distinguished from the pygopodids by having the jugal aligned with the lateral edge of the squamosal, instead of the quadrate. This change produces a narrow skull in pygopodids and a wider basicranium in the sphaerodactylids. These two groups present very different foraging strategies: active foraging in pygopodids and sedentary foraging in sphaerodactylids (Bauer, 2006); these two groups of gekkotans also converge in terms of being diurnal; with the data of the analysis, we were unable to detect any noticeable change attributed to diurnal habits, such as a reduction in eye diameter.


ANALYSIS OF THE GEKKOTAN SKULL Some of the changes observed in regions of the skull are correlated: a shortening of the snout is coupled with enlargement of the premaxilla and shortening of the nasals. In general, when the snout is reduced, the skull becomes higher, although there are some exceptions, such as species of Pristurus, which have a large snout and a high skull table. The description of changes on the gekkotan skull revealed new sources of variation that are the basis for the description of new characters of phylogenetic utility. Other factors not considered in the present study do not appear to be very relevant to the shaping of the skull. Habitat use was found to be an important factor shaping the body in lizards. Anolis lizards from the Caribbean constitute a well-known example of ecology explaining general morphology (Williams, 1983; Losos et al., 1998). Although, in the West Indies, morphological specialization appears to be predictable based on ecology, this ecomorph phenomenon does not apply to mainland species (Irschick et al., 1997; Velasco & Herrel, 2007). Locomotor performance also has been assumed to be an important factor in body shape; for example, cursorial species have relatively high heads and trunks compared to climbing species (Vanhooydonck & Van Damme, 1999). Relative limb dimensions in geckos from these two contrasting habitats were not found to differ consistently (Zaaf & Van Damme, 2001) and, in tropidurine iguanians, the head is not constrained by habitat, with no significant differences being found between species occupying horizontal and vertical surfaces (Kohlsdorf et al., 2008). In gekkotans, this also appears to be the case because a variety of head shapes is found in both terrestrial and scansorial species. In cryptozoic and burrowing gekkotans, the effect of habitat might be significant and is probably worthy of examination in future studies.

ACKNOWLEDGEMENTS We thank Virginia Abdala, Aaron M. Bauer, Jack L. Conrad, David L. Bruck and an anonymous referee for critically reading and editing this manuscript. Tomas Hrbek and Eugenio Santiago provided comments and ideas during the development of this project. We would like to thank Tristan Stayton for sharing the digital pictures that he obtained from several Museums and Institutions in USA. We also want to thank especially Colin McCarthy from Natural History Museum in London; Darrel Frost and David Kizirian from the American Museum of Natural History in New York; Maureen Kearney and Alan Resetar of the Field Museum in Chicago; and Tony Gamble from the Bell Museum of Natural History at the University of Minesota, for granted access to gekkotan specimens. Robert J. Pascocello

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and Carla Restrepo helped us to solve methodological difficulties. It would have been impossible to accomplish this research without the support of Andres Daza, Freddy Daza, Maria Teresa Vaca, families Sinko-Uribe (London) and Alarcón (New York City), and the Decanato de Estudios Graduados (DEGI) at the University of Puerto Rico.

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SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article: Appendix S1. Institutional abbreviations. Appendix S2. List of specimens. Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.
