Research Article |
Corresponding author: Aurelio Ramírez-Bautista ( ramibautistaa@gmail.com ) Academic editor: Aaron Bauer
© 2016 José Daniel Lara Tufiño, Adrián Nieto Montes de Oca, Aurelio Ramírez-Bautista, Levi Gray.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Lara-Tufiño JD, Nieto-Montes de Oca A, Ramírez-Bautista A, Gray LN (2016) Resurrection of Anolis ustus Cope, 1864 from synonymy with Anolis sericeus Hallowell, 1856 (Squamata, Dactyloidae). ZooKeys 619: 147-162. https://doi.org/10.3897/zookeys.619.9650
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In this study, based on a morphological analysis, the resurrection of the name Anolis ustus
Anolis , Atlantic versant, dewlap, hemipenes, Yucatan Peninsula
The name Anolis sericeus has a relatively old and complex taxonomic history. Anolis sericeus was described by
Nonetheless, preliminary observations of substantial geographic variation in several morphological characters (e.g., dewlap size, hemipenial morphology, and numbers of dorsal and ventral scales) among populations of A. sericeussensu
We examined specimens from most of the geographic distribution of A. sericeussensu
The remaining examined specimens were borrowed from the following collections:
Measurements were taken under a microscope trademark Leica (model MS-512X) with a digital caliper trademark Mitutoyo (model CD-8”CX) and recorded to the nearest 0.1 mm. Nomenclature of measured characters follows
SVL snout-vent lenght
TL tail length
HL head length
HW head width
SL snout length
LDIS longitudinal diameter of the interparietal scale
TDIS transverse diameter of the interparietal scale
NRL naris-rostrum length
IL internarial length
DA dewlap area
AGL axilla-groin length
FL forearm length
ShL shank length
LFT length of the fourth toe
DLW dilated lamellae width
NPS number of postrostral scales
NIS number of internasal scales
NSSSS number of scales separating supraorbital semicircles
NLS number of loreal scales
NSuperciliary number of superciliary scales
NSupraoculars number of supraocular scales
NSupralabials number of supralabial scales
NInfralabials number of infralabial scales
NPS number of postmental scales
NLFT number of subdigital lamellae of fourth toe (from the lamella situated at the level of the joint of phalanges III and IV to the beginning of the terminal lamellae
NTL number of terminal lamellae
NDS number of dorsal scales
NVS number of ventral scales
In addition, the number of gorgetal scales (NGS) in males was recorded. In this review variation in color pattern was not considered because of changes in pattern with preservation. Dewlap area was measured on field specimens only. The area was measured by tracing the outline of the extended dewlap onto a sheet of grid paper with 1 mm2 squares, and counted the number of squares that were completely within the outline. Nomenclature for hemipenial structures follows
Each examined character was tested for normality with a Komolgorov-Smirnov test using the statistics program STATISTICA v. 7 (
In the PCA for males, the first three principal components explained 47.11% of the variation in the analyzed characters, of which 18 were highly correlated with these components (Table
Ordination diagram of principal components 1 and 2 from the PCA of morphological data for males. Circles represent specimens from Tamaulipas, Hidalgo, and northern and central Veracruz; triangles represent specimens from southern Veracruz and western Tabasco; squares represent specimens from the Yucatan Peninsula. Blue circles represent specimens from near the type locality of Anolis sericeus. The red square indicates the syntype specimen of A. ustus.
Statistics from the PCA for males and females. Correlation coefficients among characters for the first three principal components. * Characters that explained the highest percentage of variation for each component. Also shown here are the eigenvalue, explained variance, and accumulated explained variance for the first three components.
Characters | Males | Females | ||||
---|---|---|---|---|---|---|
PC1 | PC2 | PC3 | PC1 | PC2 | PC3 | |
SVL | -0.85173* | -0.20534 | 0.07991 | -0.85924* | -0.11391 | 0.06696 |
TL | -0.63747* | 0.42139 | 0.14205 | -0.08738 | 0.10816 | -0.15747 |
HL | -0.75132* | -0.21300 | 0.02761 | -0.51013* | -0.11974 | -0.10871 |
HW | -0.89301* | -0.01137 | 0.08725 | -0.85500* | 0.11310 | -0.03773 |
SL | -0.16205 | -0.76203* | 0.06875 | -0.62754* | -0.47109 | -0.06681 |
LDIS | 0.02718 | -0.38966 | -0.41556 | -0.18201 | -0.09325 | -0.00660 |
TDIS | -0.26775 | -0.34381 | -0.40685 | 0.03118 | -0.37480 | 0.07133 |
NRL | -0.59741* | -0.35489 | -0.15510 | -0.37018 | 0.16997 | -0.64634* |
IL | -0.53550* | -0.21165 | -0.22670 | -0.17989 | 0.16189 | -0.63214* |
AGL | -0.61223* | -0.32925 | 0.15488 | -0.79493* | -0.22509 | 0.24664 |
FL | -0.67579* | 0.15599 | -0.10419 | -0.73863* | 0.25637 | 0.21445 |
ShL | -0.79747* | 0.35656 | -0.10989 | -0.61786* | 0.51700 | 0.30123 |
NLFT | -0.40566 | -0.09677 | -0.16376 | -0.39755 | 0.25495 | 0.36898 |
DLW | -0.49120 | -0.06745 | 0.20022 | -0.35303 | 0.03498 | -0.11668 |
NPS | -0.55101* | 0.07934 | 0.26717 | -0.19525 | 0.52569* | -0.29213 |
NIS | -0.62932* | -0.00681 | 0.34277 | -0.48324 | 0.12972 | -0.56355 |
NSSSS | 0.21946 | 0.18801 | 0.61755* | 0.10245 | 0.22969 | -0.07205 |
NLS | -0.24362 | 0.11200 | 0.66801* | -0.23420 | 0.34496 | 0.35073 |
NESupraoculars | -0.25903 | 0.03750 | 0.14125 | -0.42631 | 0.27921 | -0.05066 |
NSuperciliary | 0.24871 | -0.46196 | 0.08580 | 0.19944 | -0.39344 | -0.41732 |
NSupralabials | -0.3210 | -0.44249 | 0.04213 | -0.18859 | -0.37790 | 0.42922 |
NInfralabials | -0.29243 | -0.47001 | -0.05932 | -0.34863 | -0.26685 | 0.06765 |
NPS | 0.07640 | 0.10760 | -0.04845 | -0.09248 | 0.30053 | -0.38155 |
NLFT | 0.38912 | 0.35547 | 0.46492 | 0.20960 | 0.44236 | 0.20140 |
NTL | -0.26142 | -0.22149 | -0.09782 | -0.05959 | -0.07437 | -0.47491 |
NDS | 0.08872 | -0.70684* | 0.25048 | -0.31800 | -0.61508* | 0.00925 |
NVS | -0.02688 | -0.66557* | 0.44827 | -0.15787 | -0.69712* | -0.15984 |
DA | -0.52824 | 0.76774* | -0.11198 | -0.09344 | -0.67078* | -0.02167 |
NGS | -0.47798 | 0.78351* | -0.11481 | - | - | - |
Eigenvalue | 7.00 | 4.58 | 2.13 | 5.08 | 3.45 | 2.55 |
Explained variance (%) | 24.05 | 15.80 | 7.35 | 18.15 | 12.30 | 9.11 |
Accumulated variance (%) | 24.05 | 39.80 | 47.20 | 18.15 | 30.45 | 39.58 |
GDA for males showed that the first two functions explained 100% of the total variance; Wilks’s lambda test indicated that SVL, SL, NGS, and DA are the characters that allow discrimination among groups (Table
Ordination diagram from the GDA analysis of the morphological data for males. Circles represent specimens from Tamaulipas, Hidalgo, and northern and central Veracruz; triangles represent individuals from southern Veracruz and western Tabasco; squares represent individuals from the YP. Blue circles indicate specimens collected near the type locality of Anolis sericeus. The red square indicates the syntype of A. ustus.
The Own Root and Explained Variance of canonical functions 1 and 2, and results from Wilks’ Lambda tests from GDA of morphological data for males. Only statistically significant morphological variables according to Wilks’s Lambda test are presented. * p < 0.05.
Character | Canonical function 1 | Canonical function 2 | Wilk’s Lambda | F | p |
---|---|---|---|---|---|
SVL | -0.0656 | -0.2333 | 0.8896 | 3.2877 | 0.0450* |
TL | 0.0314 | -0.0151 | 0.9573 | 1.1809 | 0.3149 |
HL | 0.0138 | -0.4059 | 0.9462 | 1.5055 | 0.2312 |
HW | -0.0147 | 0.4540 | 0.9895 | 0.2802 | 0.7567 |
SL | -0.3391 | -1.6851 | 0.7992 | 6.6572 | 0.0026* |
NRL | -0.7577 | 0.6368 | 0.9740 | 0.7063 | 0.4980 |
IL | -0.3024 | -1.7315 | 0.9075 | 2.6980 | 0.0765 |
AGL | -0.0966 | 0.0590 | 0.9862 | 0.3685 | 0.6934 |
FL | 0.2231 | -0.0495 | 0.9705 | 0.8054 | 0.4522 |
ShL | -0.1509 | -0.2002 | 0.9862 | 0.3694 | 0.6928 |
NPS | -0.0724 | -0.4489 | 0.9440 | 1.5692 | 0.2177 |
NIS | 0.4141 | -0.0372 | 0.9674 | 0.8914 | 0.4161 |
NSSSS | -0.1466 | 0.3262 | 0.9809 | 0.5159 | 0.5998 |
NLS | -0.1596 | -0.3107 | 0.9710 | 0.7903 | 0.4589 |
NDS | -0.0333 | -0.0710 | 0.9014 | 2.8966 | 0.0639 |
NVS | 0.0386 | 0.0568 | 0.9606 | 1.0861 | 0.3449 |
NGS | -0.1724 | -0.7870 | 0.8599 | 4.3144 | 0.0183* |
DA | 0.1726 | 0.0445 | 0.3439 | 50.5422 | 0.0000* |
Own Root | 17.0669 | 3.4759 | – | – | – |
Explained Variance (%) | 0.8308 | 1.0000 | – | – | – |
The Own Root and Explained Variance of canonical function 1 for female morphological data obtained with GDA. Only statistically significant morphological variables according to Wilks’s Lambda test are presented. * p < 0.05.
Character | Canonical Function 1 | Wilk’s Lambda | F | p |
---|---|---|---|---|
SVL | -0.12862 | 0.959861 | 2.21631 | 0.142485 |
LCA | -0.07654 | 0.992848 | 0.38178 | 0.539296 |
WH | 1.91975 | 0.818575 | 11.74666 | 0.001186* |
LH | -0.74607 | 0.941677 | 3.28255 | 0.075687 |
LNR | -1.27415 | 0.972540 | 1.49646 | 0.226628 |
LEN | 0.76652 | 0.970452 | 1.61375 | 0.209514 |
AGL | -0.00895 | 0.999859 | 0.00747 | 0.931467 |
FL | -0.01099 | 0.999978 | 0.00118 | 0.972746 |
ShL | 0.84336 | 0.839738 | 10.11490 | 0.002458* |
NPS | 0.14725 | 0.985193 | 0.79654 | 0.376163 |
NDS | -0.06274 | 0.926137 | 4.22696 | 0.044726* |
NVS | -0.09454 | 0.879576 | 7.25631 | 0.009440* |
DA | -0.09182 | 0.737254 | 18.88838 | 0.000063* |
Own Root | 4.75 | _ | _ | _ |
Accumulated Variance (%) | 100 | _ | _ | _ |
Mean ± standard deviation and range for the most important morphological characters according to the GDA.
Character | Males | Females | |||
---|---|---|---|---|---|
AV1 (n = 26) | AV2 (n = 24) | YP (n = 23) | AV (n = 35) | YP (n = 32) | |
SVL | 45.72 ± 2.71 (38.52–49.94) |
39.49 ± 1.32 (36.5–42.38) |
41.50 ± 2.20 (37.36–44.59) |
41.33 ± 2.48 (38.21–53.01) |
44.28 ± 3.8 (35.07–48.93) |
SL | 5.3 ± 0.39 (4.47–6.02) |
4.56 ± 0.29 (3.99–5.85) |
5.7 ± 0.44 (5.0–6.93) |
5.14 ± 0.46 (4.16–6.08) |
5.56 ± 0.50 (4.83.6.56) |
ShL | 10.79 ± 0.95 (9.9–13.38) |
9.52 ± 0.57 (8.52–10.78) |
8.47 ± 0.49 (7.54–9.78) |
10.0 ± 1.0 (8.32–11.42) |
8.7 ± 0.6 (7.22–9.91) |
NDS | 48.92 ± 6.55 (36–62) |
43.59 ± 6.09 (37–60) |
57.5 ± 7.60 (44–78) |
47.5 ± 7.62 (37–60) |
56.7 ± 5.66 (45–71) |
NVS | 42.15 ± 6.14 (32–54) |
38.59 ± 5.24 (31–51) |
47.7 ± 4.55 (39–59) |
39.4 ± 6.11 (28–47) |
48.3 ± 6.72 (37–66) |
DA | 97.3 ± 8.12 (85–120) |
92.13 ± 5.36 (83–110) |
45 ± 5.9 (31–58) |
30.14 ± 4.8 (31–40) |
41.1 ± 5.1 (32–50) |
NGS | 8.53 ± 0.58 (8–9) |
8.31 ± 0.47 (8–9) |
5.4 ± 0.61 (4–6) |
- | - |
Forty out of 78 examined males had everted hemipenes (29 from the AV and 11 from the YP). Four different hemipenial morphologies were found. The geographic distribution of these morphologies is shown in Fig.
Statistical analyses showed three morphologically different groups of males (AV1, AV2, and YP), although only two of females (AV and YP). However, we consider that the morphological evidence that separates the two groups of males from the AV is not enough to question their conspecificity, because they only differ in average SVL and SL from those of the group AV1 (Table
The YP group was distinguishable from the AV groups in both males and females. The characters with the largest contributions to the separation of the AV and YP groups included SVL, SL, and NGE in males; HW and ShL in females, and DA, NDS, and NVS in both sexes. Of these characters, the one with the largest contribution to the separation of the AV and YP groups was dewlap size (DA). The differences in dewlap size between males and females of both groups were obvious (Fig.
The dewlap has been regarded as a taxonomically important character in Anolis by many authors (summarized in
Male A. sericeus from the AV and YP groups also differed in hemipenial morphology (Fig.
Although differences in hemipenial morphology between populations may not warrant recognition of the differentiated populations as distinct species (see above), we argue that the other consistent morphological differences between the AV and YP groups of A. sericeus do warrant their recognition as distinct evolutionary lineages. Because the type locality of A. sericeus is in Veracruz (El Lencero, Xalapa), the lineage in Tamaulipas, Hidalgo, Querétaro, Veracruz, and Tabasco should retain this name, whereas the oldest available name for the lineage in Campeche, Yucatán, Quintana Roo, and Belize is Anolis ustus Cope 1856 (type locality = “Belize”). Anolis kidderi
The specimens from Tabasco (two males and two females) were placed within the AV group with the specimens from Veracruz, Hidalgo, and Tamaulipas in our analyses, and possessed the diagnostic characters of this group: the dewlap is large in males and small in females, and both males and females have low counts of NDS and NVS. In contrast, and despite the geographic proximity between their localities and those of the specimens from Tabasco, the specimens from Campeche (seven males and nine females) belonged into the YP group and possessed the diagnostic characters of this group: the dewlap is small in both males and females and the NDS and NVS counts are high. Recent field work in southern Campeche, between the coordinates 18°07'38.67"N, 91°36'43.91"W and 18°22'48.60"N, 91°11'54.32"W (WGS84) revealed an abrupt transition in form (LNG, unpublished). While every non-Yucatan population within the A. sericeus group exhibits strong sexual dimorphism in dewlap size between males and females, A. ustus stands out as the one lineage that is easily diagnosable morphologically. Additional studies are needed to determine the existence of a contact zone between the two groups, and the existence and extent of any gene flow between them.
There were no evident differences in behavior or microhabitat between the AV and YP groups of A. sericeus. Individuals of both groups were observed perching between 30 and 400 cm on grasses, branches, or thin trunks. Also, individuals of both groups were found in open areas bordering dense vegetation, pasture land, and crop fields. In our experience, lizards in the A. sericeus group tend to be quite variable in morphology, habitat preference, and behavior.
We thank A. Sánchez González, J. Márquez Luna, and P. Octavio Aguilar for their comments on the first version of this manuscript. We thank to L. M. Badillo Saldaña, R. Hernández Austria, J. Becerra López, I. Reaño Hernández, R. Cruz Elizalde, A. Alamillo Paredes, D. Juárez Escamilla, M. Rojas Domínguez, and C. Berriozabal-Islas for their comments and help in the field. For the loaning of specimens we are very grateful to I. Goyenechea, R. Coates Estrada, R. Cedeño, J. Morales Mávil, S. A. Terán Juárez, and F. Leyto. We also thank L. Welton and R. Glor for their revision of the specimens of Anolis sericeus from Belize; J. Streicher and P. Campbell for their help in the examination of the specimens and photos collected from the syntypes of Anolis ustus; S. Rogers for sending data of specimens of A. sericeus from Belize, and the families Ramírez-Bautista and Solís-Badillo for their hospitality during the fieldwork. We thank B. Stephenson and L. Wilson for reviewing the English language in this manuscript. We are grateful to K. E. Nicholson and G. Köhler for their revision of the manuscript and the comments to improve, we also thank to A. Bauer for his great help in this work. Finally, we thank the people of the communities of Puerto Oscuro, La Palma, Quetzalapa, Acuimantla from the state of Hidalgo; El Lencero, Xotla, Laguna Escondida, Montepío, and Catemaco of state of Veracruz; and the people of Laguna Guerrero, Chetumal, and Xul-ha of the state of Quintana Roo. This study was supported by the scientific permit number SGPA/DGVS/04149/15 issued by SEMARNAT (Secretaría del Medio Ambiente y Recursos Naturales).
Examined specimens
Anolis sericeus.- MÉXICO: Tamaulipas: Victoria: