Research Article |
Corresponding author: L. Lee Grismer ( lgrismer@lasierra.edu ) Academic editor: Uwe Fritz
© 2021 L. Lee Grismer.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Grismer LL (2021) A new genus for the tiny hawk Accipiter superciliosus and semicollared hawk A. collaris (Aves: Accipitridae), with comments on the generic name for the crested goshawk A. trivirgatus and Sulawesi goshawk A. griseiceps. Vertebrate Zoology 71: 419-424. https://doi.org/10.3897/vz.71.e69214
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Abstract
It is hypothesized that shape differences between the closely related sandstone night lizard (Xantusia gracilis) and the granite night lizard (X. henshawi) may be correlated with structual differences in their respective microhabitats. Multivariate and univariate analyses of 22 morphometric characters taken from the head, body, and limbs of both saxicolus specialists recovered statistically significant differences between them with X. gracilis having a wider head, longer snout, larger eyes, wider sternum, higher and wider pelvis, thinner limbs, longer forearms and thighs, and longer hind limbs. Many of these same proportional differences have been reported among very closely related saxicolus species in other lizard families (i.e. Eublepharidae, Gekkonidae, Phrynosomatidae) that also live on different rocky substrates. This supports the inference that morphometric differences between X. gracilis and X. henshawi are ecomorphological adaptations for navigating the substantially different substrates of their respective microhabitats. Xantusia gracilis is restricted to a loose, heterogeneous, sandstone microhabitat composed of large boulders, small rocks, and cliff faces where cracks, crevices, holes, and exfoliations are used as retreats versus the compact, more homogeneous, granite boulder microhabitat of X. henshawi where narrow spaces beneath exfoliations and cap-rocks are the preferred retreats.
Anza-Borrego, ecomorph, microhabitat, scansorial, saxicolus, Xantusiidae
The concept that an animal’s form has evolved in response to the way it navigates its habitat underpins the study of ecomorphology—the intersection of organismal morphology, life history, and adaptation (
The Night Lizard family Xantusiidae is a New World lineage composed of three genera and 35 generally nocturnal species that collectively range from Southwestern North America to southern Central America (
A. The Island Night Lizard, Xantusia riversiana, from Santa Barbara Island, Santa Barbara County, California—a habitat generalist. Photo by Gary Nafis. B. Heterogeneous habitat of X. riversiana on Santa Barbara Island. Photo by Gary Nafis. C. The Yucca Night Lizard, X. cf. vigilis, from Anza-Borrego, San Diego County, California–a vegetative specialist. D. Yucca habitat of X. cf. vigilis at Blair Valley, San Diego County. E. The granite night lizard, X. henshawi, from Deep Creek, Riverside County, California– a granite exfoliation specialist. F. Granite boulder habitat of X. henshawi at Lost Valley, San Diego County. G. The sandstone night lizard, X. gracilis, from the Truckhaven Rocks, San Diego County—a sandstone specialist. H. Sandstone habitat of X. gracilis at the Truckhaven Rocks, San Diego County.
Xantusia gracilis.
A. The sandstone boulder and cliff face habitat of Xantusia gracilis, Truckhaven Rocks, San Diego County, California. B. Slot canyon microhabitat of X. gracilis, Truckhaven Rocks. C. Crumbling, exfoliation-like microhabitat of X. gracilis, Truckhaven Rocks. D. Relatively smooth, compact granite boulder microhabitat of X. henshawi showing a cap-rock (at top) and an exfoliation (in lower right), Mountain Meadows, San Diego County, California. E. Granite boulder outcrop habitat of X. henshawi, Aguanga, Riverside, County, California.
Xantusia henshawi.
Locality of specimens of Xantusia henshawi used in this analysis. Based on distribution, all are presumed to belong to haploclade A of Lovich (2001) along with X. gracilis.
Catalog number | County | Locality |
LSUHC 1530 | Riverside | Aguanga |
LSUHC 1531 | Riverside | Aguanga |
LSUHC 1998 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 1999 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2000 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2001 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2002 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2004 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2005 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2006 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2007 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2009 | San Diego | Intersection of Deer Springs Road and Interstate 15 |
LSUHC 2010 | San Diego | Ranchita |
LSUHC 2011 | San Diego | Ranchita |
LSUHC 2013 | San Diego | Ranchita |
LSUHC 2015 | San Diego | Ranchita |
LSUHC 2016 | San Diego | Ranchita |
LSUHC 2017 | Riverside | Hemet |
LSUHC 2018 | Riverside | Hemet |
LSUHC 2019 | Riverside | Hemet |
LSUHC 2020 | Riverside | Aguanga |
LSUHC 2021 | Riverside | Aguanga |
The following 22 measurements were taken from the left side of the body when possible to the nearest 0.1 mm using Mitutoyo dial calipers under a Nikon SMZ 1500 dissecting microscope:
SVL (snout-vent length) – measured from the tip of the snout to the cloacal opening.
HL (head length) – measured from the tip of the snout to the posterior margin of the retroarticular process of the mandible.
HW (head width) – measured across the widest portion of the head, posterior to the eyes.
HD (head depth) – measured from top of the head above the center of the orbit to the ventral surface of the mandibles.
SL (snout length) – measured from the anterior margin of the bony orbit to the tip of the snout.
SW (sternal width) – measured from the articulation point of the humeri and the glenoid fossae across the sternum from one side to the other.
ED (eyeball diameter) – measured in a horizontal plane from the posterior to the anterior margins of the eyeball.
FLW (forelimb width) – measured from the anterior and posterior insertion points of the forelimb on the body.
FL1 (brachial length) – measured from the articulation point of the humerus and the glenoid fossa to the distal margin of the elbow joint while flexed 90°.
FL2 (forearm length) – measured from the proximal margin of the elbow joint while flexed 90° to the distal margin of the ulna while the wrist joint is extended.
FL3 (manus length) – measured from the distal margin of the ulna to the base of the 4th finger.
FL4 (fourth finger length) – measured from the base of the fourth finger to the tip of the claw.
FLL (forelimb length) – the sum of FL1–FL4. These data were used in separate analyses so as not to overleverage the analysis with forelimb dimensions.
AG (axilla-groin length) – measured from the posterior margin of the forelimb at its insertion point on the body to the anterior margin of the hind limb at its insertion point on the body.
PW (pelvic width) – measured from the lateral margins of the ilia across of the body.
PH (pelvic height) – measured from top of the illium to the ventral surface of the pubic bone.
HLW (hind limb width) – measured from the anterior and posterior insertion points of the thigh on the body.
HL1 (thigh length) – measured from the articulation point of the femur and the acetabulum to the distal margin of the knee joint while flexed 90°.
HL2 (tibia length) – measured from the proximal margin of the knee joint while flexed 90° to the distal margin of the tibia while the ankle joint is extended.
HL3 (pes length) – measured from the distal margin of the tibia to the base of the 4th toe.
HL4 (fourth toe length) – measured from the base of the fourth toe to the tip of the claw.
HLL (hind limb length) – the sum of HL1–HL4. These data were used in separate analyses so as not to overleverage the analysis with hind limb dimensions.
To ensure that allometric biases in the raw data were appropriately removed prior to analysis, hatchlings were omitted from the data set and the raw data were adjusted using the following equation: Xadj=log(X)-β[log(SVL)-log(SVLmean)], where Xadj=adjusted value; X=measured value; β=unstandardized regression coefficient for each population; and SVLmean=overall average SVL of all populations (
A principal component analysis (PCA) of the adjusted data was employed to visualize and assess the degree of difference in morphospatial clustering among Xantusia gracilis and X. henshawi. Principal component analysis is an unsupervised analysis that does not group individuals a priori according to species. All adjusted data were scaled to their standard deviation to ensure they were analyzed on the basis of correlation and not covariance. A subsequent supervised analysis, discriminant analysis of principal components (DAPC) from the ADEGENET package in R (
To search for and quantify significant morphological differences between Xantusia gracilis (n=11) and X. henshawi (n=22), all data were first tested for normality with an F-test. Those with homogeneous variances (p<0.05) were subjected to a Student’s t-test and those with unequal variances (p>0.05) were subjected to a Welch’s t-test. Both tests search for statistically significant different mean values (p<0.05) in all the characters between both species. Violin plots, embedded with boxplots, were generated for the characters bearing statistically different means in order to visualize their range and frequency of variation, mean, 50% quartile, and the degree of difference between the species. All data analyses were performed in R [v3.4.3] (
The PCA demonstrates that Xantusia gracilis and X. hensahwi occupy non-overlapping positions in morphospace among the collective ordination of the first two principal components (Fig.
Summary statistics and principal component analysis scores for the adjusted morphometric characters of Xantusia gracilis and C. X. henshawi. Abbreviations are listed in the Materials and methods.
PC1 | PC2 | PC3 | PC4 | PC5 | PC6 | PC7 | PC8 | PC9 | PC10 | PC11 | PC12 | PC13 | PC14 | PC15 | PC16 | PC17 | PC18 | PC19 | |
Standard deviation | 2.2054 | 1.7470 | 1.4168 | 1.2978 | 1.1505 | 1.0746 | 0.9953 | 0.9130 | 0.8209 | 0.8062 | 0.7670 | 0.7392 | 0.6512 | 0.5647 | 0.5257 | 0.4700 | 0.3956 | 0.3585 | 0.2336 |
Proportion of variance | 0.2432 | 0.1526 | 0.1004 | 0.0842 | 0.0662 | 0.0577 | 0.0495 | 0.0417 | 0.0337 | 0.0325 | 0.0294 | 0.0273 | 0.0212 | 0.0159 | 0.0138 | 0.0111 | 0.0078 | 0.0064 | 0.0027 |
Cumulative proportion | 0.2432 | 0.3958 | 0.4962 | 0.5804 | 0.6466 | 0.7043 | 0.7538 | 0.7955 | 0.8292 | 0.8617 | 0.8911 | 0.9184 | 0.9396 | 0.9556 | 0.9694 | 0.9804 | 0.9883 | 0.9947 | 0.9974 |
Eigenvalue | 4.8639 | 3.0519 | 2.0074 | 1.6842 | 1.3237 | 1.1547 | 0.9907 | 0.8337 | 0.6739 | 0.6500 | 0.5883 | 0.5464 | 0.4241 | 0.3189 | 0.2763 | 0.2209 | 0.1565 | 0.1285 | 0.0546 |
SVL | –0.0460 | 0.0228 | –0.0248 | –0.0261 | 0.0684 | –0.1519 | 0.9766 | –0.0130 | 0.0754 | –0.0590 | 0.0090 | –0.0255 | 0.0430 | –0.0102 | 0.0425 | –0.0083 | 0.0136 | 0.0200 | –0.0063 |
SW | –0.2892 | –0.1317 | –0.1023 | 0.0910 | 0.2057 | 0.4154 | 0.0675 | –0.1512 | –0.3248 | –0.0858 | –0.1846 | –0.1978 | –0.4010 | 0.0830 | –0.0303 | 0.2506 | 0.2321 | 0.3123 | 0.2526 |
PW | –0.2512 | –0.0802 | –0.1529 | 0.3721 | 0.1465 | –0.0176 | –0.0677 | –0.3703 | 0.0745 | –0.0421 | 0.1929 | –0.4709 | 0.3354 | –0.3291 | 0.1055 | –0.0410 | –0.2292 | 0.1113 | –0.2007 |
PH | –0.1867 | –0.3630 | –0.1312 | –0.1903 | –0.1488 | 0.0572 | 0.0208 | 0.4195 | –0.0990 | –0.0684 | 0.0696 | 0.1754 | 0.2863 | –0.2852 | –0.2235 | 0.3139 | –0.3085 | 0.2742 | 0.1269 |
AG | –0.1108 | 0.2409 | 0.3821 | 0.0879 | –0.3953 | 0.0238 | 0.0179 | 0.1533 | –0.1344 | –0.0526 | 0.3443 | –0.3094 | 0.2248 | 0.4206 | 0.1415 | 0.0975 | –0.0471 | 0.1767 | 0.2479 |
HL | –0.2116 | 0.0075 | –0.4318 | –0.0909 | 0.3720 | 0.0187 | –0.0681 | 0.1262 | 0.1352 | –0.2869 | 0.0702 | 0.0078 | 0.2013 | 0.5023 | 0.0509 | 0.1113 | –0.1491 | –0.3707 | 0.1272 |
HW | –0.3053 | –0.1526 | 0.0302 | –0.1844 | –0.1926 | 0.2856 | 0.0578 | –0.1830 | –0.3340 | 0.1723 | –0.0038 | 0.1887 | 0.4262 | –0.0951 | 0.0999 | –0.1738 | 0.3573 | –0.3721 | –0.0292 |
HD | 0.0081 | –0.2928 | –0.3123 | –0.0469 | –0.3221 | –0.1252 | 0.0199 | 0.2661 | 0.0584 | 0.3856 | –0.2227 | –0.5662 | –0.1361 | 0.1123 | 0.0306 | –0.0414 | 0.0891 | –0.2157 | –0.0212 |
SL | –0.2577 | –0.1572 | –0.2075 | –0.0470 | –0.0632 | –0.5067 | –0.0868 | 0.1029 | –0.3064 | –0.1576 | 0.1161 | 0.1626 | –0.2036 | 0.0379 | 0.3259 | –0.3725 | 0.0382 | 0.2865 | –0.0889 |
ED | –0.2577 | –0.0667 | 0.2509 | –0.2691 | 0.1566 | 0.2469 | –0.0406 | 0.1892 | 0.4907 | 0.1218 | –0.1264 | 0.0079 | –0.0145 | –0.0273 | 0.5796 | 0.0034 | 0.0185 | 0.1936 | –0.1562 |
HLW | 0.3574 | 0.0377 | –0.2416 | –0.2525 | 0.0224 | 0.1556 | 0.0336 | –0.0038 | –0.0648 | 0.2479 | 0.2246 | –0.0562 | 0.0488 | 0.0310 | –0.0119 | 0.2396 | –0.0296 | 0.2114 | –0.3282 |
HL1 | –0.3529 | 0.1922 | –0.0454 | –0.0006 | –0.0421 | –0.0825 | –0.0040 | –0.0578 | 0.2445 | 0.4127 | 0.2082 | 0.1154 | –0.2648 | –0.2445 | –0.1273 | –0.0254 | –0.2040 | –0.1569 | 0.4699 |
HL2 | –0.1740 | 0.3774 | –0.1458 | –0.1107 | 0.1231 | 0.3465 | 0.0597 | 0.2172 | –0.1894 | 0.1996 | 0.1832 | –0.0433 | –0.1015 | 0.0880 | –0.2176 | –0.4541 | –0.1989 | 0.1086 | –0.2820 |
HL3 | –0.2522 | 0.1909 | 0.0408 | 0.2413 | 0.1977 | –0.3155 | –0.0467 | 0.0682 | –0.0081 | 0.4223 | –0.3749 | 0.1487 | 0.3156 | 0.2341 | –0.2189 | 0.1763 | 0.1736 | 0.2612 | –0.1430 |
HL4 | 0.0042 | 0.3999 | –0.3671 | –0.0151 | –0.2082 | –0.0619 | –0.0041 | –0.1709 | –0.1529 | 0.1224 | 0.0656 | 0.1736 | –0.0619 | –0.0824 | 0.4443 | 0.4465 | –0.0003 | –0.0407 | –0.0312 |
FLW | 0.3487 | 0.0654 | –0.1820 | –0.2334 | 0.2797 | –0.0473 | –0.0435 | –0.0528 | –0.0168 | 0.1550 | 0.0096 | –0.1226 | 0.3234 | –0.0815 | 0.1305 | –0.2782 | 0.1859 | 0.2877 | 0.5633 |
FL1 | –0.0687 | 0.3241 | 0.1363 | –0.4109 | –0.0156 | –0.1196 | –0.0281 | –0.0762 | –0.2560 | –0.1797 | –0.5469 | –0.2552 | 0.0564 | –0.1626 | 0.0184 | 0.0051 | –0.3853 | –0.0866 | 0.0239 |
FL2 | –0.2166 | 0.1027 | 0.1193 | –0.4759 | 0.1490 | –0.2987 | –0.0930 | –0.0532 | 0.0827 | –0.1257 | 0.3310 | –0.2550 | –0.0767 | –0.1240 | –0.2801 | 0.2112 | 0.4371 | –0.0345 | –0.1439 |
FL3 | –0.1165 | 0.1300 | –0.3238 | –0.1213 | –0.4945 | 0.1219 | –0.0175 | –0.2852 | 0.4354 | –0.2624 | –0.1847 | 0.0797 | 0.0758 | 0.1193 | –0.2311 | –0.1652 | 0.1268 | 0.3024 | –0.0040 |
FL4 | 0.0129 | 0.3657 | –0.1499 | 0.3011 | –0.0147 | 0.0993 | –0.0150 | 0.5446 | 0.0443 | –0.2714 | –0.0791 | –0.0847 | 0.0657 | –0.3969 | 0.0477 | –0.0165 | 0.3661 | –0.0863 | 0.0181 |
Although Xantusia gracilis and X. henshawi do not differ significantly in SVL, they do differ in a number of other proportions. The Student’s and Welch’s t-tests of the adjusted data recovered 11 characters bearing statistically significant mean differences between them (Fig.
Summary statistics of Student and Welch’s t-tests. Shaded cells are those characters bearing significantly different means between Xantusia gracilis and X. henshawi. Character abbreviations are in the Materials and methods.
character | t-test | t value | p value |
HL | Welch’s | 0.7763 | 0.4453 |
HW | Welch’s | 4.6329 | 6.828e-05 |
HD | Student’s | 0.3646 | 0.7170 |
SL | Welch’s | 3.1815 | 0.0033 |
SW | Welch’s | 4.6399 | 6.938e-05 |
ED | Student’s | 3.3674 | 0.002 |
FLW | Welch’s | -13.362 | 3.48e-12 |
FL1 | Welch’s | -0.1597 | 0.0742 |
FL2 | Welch’s | 2.3969 | 0.023 |
FL3 | Welch’s | 1.4885 | 0.1551 |
FL4 | Welch’s | -0.5856 | 0.5674 |
FLL | Welch’s | 1.0322 | 0.3137 |
AG | Welch’s | 1.7186 | 0.1078 |
PW | Welch’s | 0.0271 | 0.0056 |
PH | Welch’s | 2.8392 | 0.0083 |
HLW | Welch’s | -7.1422 | 9.989e-07 |
HL1 | Student’s | 4.2352 | 0.0002 |
HL2 | Welch’s | 0.3227 | 0.7504 |
HL3 | Welch’s | 1.9674 | 0.0646 |
HL4 | Welch’s | -0.9722 | 0.3424 |
HLL | Welch’s | 2.2286 | 0.0341 |
The quantification of ecomorphological differences among species is important to many downstream analyses based on body size and shape. These types of data are not just necessary for comparative methods that combine phylogenies with phenotypic data to understand evolutionary processes such as the mode and tempo of trait evolution (
These data clearly demonstrate that Xantusia gracilis and X. henshawi are proportioned differently and do not scale equally across various components of their bodies. Overall, X. gracilis is more slender and less robust than X. henshawi (Fig.
A. Adult male Xantusia gracilis, Truckhaven Rocks, San Diego County, California. B. Adult female X. gracilis, Truckhaven Rocks. C. Juvenile X. gracilis, Truckhaven Rocks. D. Adult male X. henshawi, Deep Canyon, Riverside County, California. E. Adult female X. henshawi, Ramona, San Diego County, California. F. Adult female X. henshawi, Deep Canyon.
What little work has been done looking at morphological adaptations related to climbing and clinging ability among closely related species living on different rock substrates is illustrative. In the eublepharid gecko genus Goniurosaurus,
The above research opens up several avenues of inquiry as to the locomotor performance between Xantusia gracilis and X. henshawi on their respective substrates as compared to that on one another’s substrate. Experimental trials such as those done by Cobos et al. (submitted) where climbing and clinging ability are measured on different substrates among different ecomorphs, could be used to test the morphology-based inference here that a complex sandstone habitat and a more homogenous granitic substrate require different ecomorphologies. Additionally, similar experiments can be designed to test the effects of unequal scaling in the various components (e.g. different limb and head dimensions) within functional systems (e.g. the limbs and skull) in order to ascertain what adaptive value different allometric trajectories may have during the course of ontogeny.
I wish to thank Raquel Barbosa for taking the raw data and Amanda Kaatz, Jesse L. Grismer, and Evan S. H. Quah for several helpful discussions and comments concerning Night Lizards and ecomorphology. Bradford D. Hollingsworth (SDSNHM) provided helpful comments on the manuscript, sent me data on, and granted the loan of, specimens of Xantusia gracilis.
File 1
Data type: .pdf
Explanation note: Table S1. Raw mensural data from Xantusia gracilis from the Truckhaven Rocks, San Diego County, California and X. henshawi from throughout its range in San Diego County. SDNHM = San Diego Natural History Museum; LSUHC = La Sierra University Herpetological Collection, Riverside County, California. Abbreviations are in the Materials and methods..
File 2
Data type: .pdf
Explanation note: Table S2. Size-adjusted morphometric data. Order of specimens follows that in Table S1. Abbreviations are in the Materials and methods.