THE ANATOMICAL RECORD 297:337–340 (2014)

EDITORIAL The Anatomical Record is Alive With Leapin’ Lizards and Slitherin’ Snakes Are you aware that one of the earliest known transitional fossil form between lizards and snakes (Coniophis sp.) came from sites in Utah (Gardner and Cifelli, 1999) and Wyoming (Longrich et al., 2012). We, at The Anatomical Record, are proud of these discoveries in the intermountain West of the United States, in part because the editorial office has been located in Salt Lake City, UT since January 1, 2006. Our editorial board has twice taken advantage of the editorial office’s locale to dig for bony and leafy treasures in the nearby Fossil Lake area, which dates to the Eocene. One among us (KHA) even discovered a yet-to-be-identified new species of plant. This paleobotanical discovery has been donated to Fossil Butte National Monument in Kemmerer, WY. If you are into fossils, particularly of fish, plants, and dinosaurs, then Fossil Butte National Monument and the Natural History Museum of Utah (Rio Tinto Center at the University of Utah) should be added to your bucket list! We also have practical rationale for being proud of this special issue. For a number of years when the gross anatomy laboratory at the University of Utah was housed in an old military barracks (obtained from the adjacent, historical Ft. Douglas), many medical and graduate students became all too familiar with our local snake populations. Great Basin rattlesnakes (Crotalus sp.) frequently sunned themselves on the front steps of the building, essentially holding the students and faculty hostage in the gross anatomy laboratory. Often to the rescue was a well-known plastic surgeon and part-time gross anatomy instructor: Dr. Clifford C. Snyder. Dr. Snyder was also a renowned expert on the toxicology of venomous snakes and surgical approaches to treat unfortunate outcomes of snake–human encounters. Dr. Snyder would calmly encourage the snakes to leave by nudging them along, perhaps explaining why he always wore leather cowboy boots! However, he also reminded me (SCM) to never be the third person out the front door because the first person would wakeup the snake, the second would get the snake agitated, and the third would get bit! If you are into lizards and snakes, you definitely want to peruse the fascinating discoveries and descriptions that are published in this special issue of The Anatomical Record, guest-edited by Professor Juan D. Daza (Villanova University and Sam Houston State University). An additional hook to grab your attention is the cover illustration. It is original digital artwork


of an extinct gecko drawn by paleoartist Stephanie Abramowicz specifically for this special issue. If you are really into lizards and snakes, then we suggest that you also skirr and slink through more than 100 years of publications in The Anatomical Record. Why? Because the archive hosts nearly 100 papers about lizards and snakes, both extinct and extant. The earliest paper to appear between the covers of The Anatomical Record is by BW Kunkel in the 1915 issue (Kunkel, 1915). The topic of Kunkel’s paper is the paraphysis and pineal region of the garter snake. Twenty years later, LT Evans reported the effect of Antuitrin S on the male lizard, Anolis carolinensis (Evans, 1935). Antuitrin S was a pregnancyrelated endocrine compound extracted from urine of humans or whole pituitary glands of sheep by Parke Davis. Injection of Antuitrin S into young males during the winter months led to more courtship, coitus, and fighting behaviors, enlargement of the reproductive tract, faster movement, greater appetite, and more frequent molting. About a dozen more endocrinological studies are published during the remainder of the 1930s and the 1940s. Study subjects include horned lizards, garter snakes, geckos, fence lizards, and alligator lizards. The second half of the 20th century saw an explosion of publications on lizards and snakes in The Anatomical Record. Topics include effects of controlled temperature and day length on gonadal development (Bartholomew, 1950), gross and microscopic anatomy of the liver and gall bladder (Ells, 1954), osteology and musculature (Evans, 1955; Bellairs and Bryant, 1968; Throckmorton, 1978; Throckmorton and Saubert, 1982; Rubolini et al., 2006; Hall, 2009; Payne et al., 2011; Direnzo and Stynoski, 2012), endocrine and reproductive biology (Miller, 1952; Fox, 1956; Cavazos and Feagans, 1960; Neaves, 1971; Jacobs and Sis, 1980; Rhoten and Hall, 1981; Rhoten, 1982; Jones et al., 1983; Jones and Summers, 1984; Moscona, 1990; Young et al., 1999), and neurobiology (Zika and Singer, 1965; Colborn and Adamo, 1969; Proske, 1969; Gundy and Wurst, 1976; Baird and Lowman, 1978; Sligar and Voneida, 1981; Yeager et al., 1983; Pannese et al., 1984; McDevitt et al., 1993; Amemiya et al., 1996). Among the endocrinology papers are three reports by long-time American Association of Anatomists’ member William B. Rhoten, whose research focused on the pancreas of the garter snake (Rhoten and Hall, 1981; Rhoten, 1982,



1984). Other scientific topics covered by papers published between 1950 and 1999 in the Journal are cardiovascular biology (Prakash, 1960; Amemiya et al., 1999), tongue and mouth (Rabinowitz and Tandler, 1986, 1991; Toubeau et al., 1994; Iwasaki et al., 1996; Herrel et al., 1998, 1999), and the Harderian gland (Baccari et al., 1990; Rehorek, 1997). One of the Journal’s Associate Editors J. P. Timmermans is co-author of one of the papers on tongue, specifically tongue flicking in agamid lizards (Herrel et al., 1998). Near and dear to our hearts are two papers on the lung (Maina et al., 1989) and its surfactant system (Wetzstein et al., 1980). One of my (KHA) future mentors (during my postdoctoral fellowship at the University of California, San Francisco, UCSF) published a paper in The Anatomical Record in the year of my first breath. This future mentor was Malcolm R. Miller who, incidentally, was born in Salt Lake City in 1915. His endocrinology paper reported the normal histology and experimental alteration of the adrenal gland of the viviparous lizard, Xantusia vigilis (Miller, 1952). Rationale for his study was to investigate the role of the adrenal gland in regulation of water, mineral, protein, fat, and carbohydrate in non-mammalian vertebrates, about which little was known at the time. Malcolm published another paper in The Anatomical Record in 1987 (Miller and Beck, 1987), about 3 years after my postdoctoral fellowship was completed. His 1987 paper focused on heterotopic synaptic bodies in auditory hair cells in adult lizards. Among my fond memories of Malcolm and his wife, Jeanne (who together graduated with medical degrees from UCSF School of Medicine in 1945), is the terrariums of lizards that filled Malcolm’s laboratory on the 13th floor of the medical school building. Nearly half of the papers on lizards and snakes that are published in The Anatomical Record are reports from the beginning of the 21st century. This period of research brought studies of function in lizards and snakes to the Journal. Functional topics are binocular coordination of eye movement (King and Zhou, 2000), comparative functional analysis of hyolingual anatomy (Herrel et al., 2005), function of regenerating lymphatics (Blacker et al., 2007), and wound healing and regeneration (Delorme et al., 2012). Imaging also is used to gain new, 3-dimensional insights about the morphology of lizards and snakes (Hofstadler-Deiques et al., 2005; Costantini et al., 2010). Finally, a number of contributors to the special issue on lizards and snakes have publication track records in The Anatomical Record. Dr. Daza, the guest editor, has two recent publications on lepidosaurs (Daza and Bauer, 2010; Daza et al., 2011). Dr. Virginia Abdala is a co-author of Dr. Daza’s 2011 paper. Dr. Abdala and her team have two other publications that focus on the developmental basis of limb homology among lizards (Fabrezi et al., 2007) and the functional consequences of palmar tendons on grasping ability among lizards (Abdala et al., 2009). Dr. Bhart-Anjan S. Bhullar and colleagues have a previous paper on unusual abdominal musculature of squamate reptiles (Bhullar, 2009).

Dr. Carlos Jared and Marta Maria Antoniazzi and coworkers have an earlier publication on the rudimentary eyes of squamate fossorial reptiles (Foureaux et al., 2010). Lastly, Dr. Anthony P. Russell and his team have two prior publications on development of the leopard gecko (Wise et al., 2009; Wise and Russell, 2010). We thank these repeat authors! We hope that all of the authors of this special issue will also find a home for their next research reports in The Anatomical Record. We leave you with this wish: by reading the papers in this special issue, you will discover “what’s so special about squamates,” as posited by Dr. Daza in his editorial that accompanies this special issue. Kurt H. Albertine* Editor-in-Chief The Anatomical Record Scott C. Miller, Ph.D. Associate Editor The Anatomical Record

LITERATURE CITED Abdala V, Manzano AS, Tulli MJ, Herrel A. 2009. The tendinous patterns in the palmar surface of the lizard manus: functional consequences for grasping ability. Anat Rec 292: 842–853. Amemiya F, Nakano M, Goris RC, Kadota T, Atobe Y, Funakoshi K, Hibiya K, Kishida R. 1999. Microvasculature of crotaline snake pit organs: possible function as a heat exchange mechanism. Anat Rec 254:107–115. Amemiya F, Ushiki T, Goris RC, Atobe Y, Kusunoki T. 1996. Ultrastructure of the crotaline snake infrared pit receptors: SEM confirmation of TEM findings. Anat Rec 246: 135–146. Baccari GC, Minucci S, Di Matteo L, Chieffi G. 1990. Harderian gland and the lacrimal gland of the lizard Podarcis s. sicula: histology, histochemistry, and ultrastructure. Anat Rec 226: 269–278. Baird IL, Lowman GF. 1978. A study of the structure of the papilla neglecta in the lizard, Anolis carolinensis. Anat Rec 191:69–70. Bartholomew GA, Jr. 1950. The effects of artificially controlled temperature and day length on gonadal development in a lizard, Xantusia vigilis. Anat Rec 106:49–59. Bellairs AA, Bryant SV. 1968. Effects of amputation of limbs and digits of lacertid lizards. Anat Rec 161:489–495. Bhullar BA. 2009. A reevaluation of the unusual abdominal musculature of squamate reptiles (Reptilia: Squamata). Anat Rec 292:1154–1161. Blacker HA, Tsopelas C, Orgeig S, Daniels CB, Chatterton BE. 2007. How regenerating lymphatics function: lessons from lizard tails. Anat Rec 290:108–114. Cavazos LF, Feagans WM. 1960. Histochemistry and composition of the male reproductive tract of the horned lizard as affected by seasonal variation. Anat Rec 137:33–43. Colborn GL, Adamo NJ. 1969. The ultrastructure of sympathetic ganglia of the lizard Cnemidophorus neomexicanus. Anat Rec 164:185–203. Costantini D, Alonso ML, Moazen M, Bruner E. 2010. The relationship between cephalic scales and bones in lizards: a preliminary microtomographic survey on three lacertid species. Anat Rec 293:183–194. Daza JD, Bauer AM. 2010. The circumorbital bones of the Gehkota (Reptilia: Squamata). Anat Rec 293:402–413.


Daza JD, Diogo R, Johnston P, Abdala V. 2011. Jaw adductor muscles across lepidosaurs: a reeappraisal. Anat Rec 294: 1765–1782. Delorme SL, Lungu IM, Vickaryous MK. 2012. Scar-free wound healing and regeneration following tail loss in the leopard gecko, Eublepharis macularius. Anat Rec 295:1575–1595. Direnzo GV, Stynoski JL. 2012. Patterns of second-to-fourth digit length ratios (2D:4D) in two species of frogs and two species of lizards at La Selva, Costa Rica. Anat Rec 295:597–603. Ells HA. 1954. The gross and microscopic anatomy of the liver and gall bladder of the lizard, Sceloporus occidentalis biseriatus (Hallowell). Anat Rec 119:213–229. Evans HE. 1955. The osteology of a worm snake, Typhlops jamaicensis (Shaw). Anat Rec 122:381–396. Evans LT. 1935. The effect of antuitrin s on the male lizard, anolis carolinensis. Anat Rec 62:213–221. Fabrezi M, Abdala V, Oliver MI. 2007. Developmental basis of limb homology in lizards. Anat Rec 290:900–912. Foureaux G, Egami MI, Jared C, Antoniazzi MM, Gutierre RC, Smith RL. 2010. Rudimentary eyes of squamate fossorial reptiles (amphisbaenia and serpentes). Anat Rec 293:351–357. Fox W. 1956. Seminal receptacles of snakes. Anat Rec 124: 519–539. Gardner JD, Cifelli RL. 1999. A primitive snake from the Cretaceous of Utah. Special Pap Palaeontol London 60:87–100. Gundy GC, Wurst GZ. 1976. Parietal eye-pineal morphology in lizards and its physiological implications. Anat Rec 185: 419–431. Hall MI. 2009. The relationship between the lizard eye and associated bony features: a cautionary note for interpreting fossil activity patterns. Anat Rec 292:798–812. Herrel A, Aerts P, Fret J, de Vree F. 1999. Morphology of the feeding system in agamid lizards: ecological correlates. Anat Rec 254:496–507. Herrel A, Canbek M, Ozelmas U, Uyanoglu M, Karakaya M. 2005. Comparative functional analysis of the hyolingual anatomy in lacertid lizards. Anat Rec 284:561–573. Herrel A, Timmermans JP, De Vree F. 1998. Tongue flicking in agamid lizards: morphology, kinematics, and muscle activity patterns. Anat Rec 252:102–116. Hofstadler-Deiques C, Walter M, Mierlo F, Ruduit R. 2005. Software system for three-dimensional volumetric reconstruction of histological sections: a case study for the snake chondrocranium. Anat Rec 286:938–944. Iwasaki S, Yoshizawa H, Kawahara I. 1996. Three-dimensional ultrastructure of the surface of the tongue of the rat snake, Elaphe climacophora. Anat Rec 245:9–12. Jacobs VL, Sis RF. 1980. Ascending projections of the dorsal column in a garter snake (Thamnophis siritalis): a degeneration study. Anat Rec 196:37–50. Jones RE, Summers CH. 1984. Compensatory follicular hypertrophy during the ovarian cycle of the house gecko, Hemidactylus frenatus. Anat Rec 209:59–65. Jones RE, Summers CH, Austin HB, Smith HM, Gleeson TT. 1983. Ovarian, oviductal, and adrenal vascular connections in female lizards (genus Anolis). Anat Rec 206:247–255. King WM, Zhou W. 2000. New ideas about binocular coordination of eye movements: is there a chameleon in the primate family tree? Anat Rec 261:153–161. Kunkel SL. 1915. The paraphysis and pineal region of the garter snake. Anat Rec 9:607–636. Longrich NR, Bhullar BA, Gauthier JA. 2012. A transitional snake from the Late Cretaceous period of North America. Nature 488:205–208. Maina JN, Maloiy GM, Warui CN, Njogu EK, Kokwaro ED. 1989. Scanning electron microscope study of the morphology of the reptilian lung: the Savanna monitor lizard Varanus exanthematicus and the pancake tortoise Malacochersus tornieri. Anat Rec 224:514–522.


McDevitt DS, Brahma SK, Jeanny JC, Hicks D. 1993. Presence and foveal enrichment of rod opsin in the “all cone” retina of the American chameleon. Anat Rec 237:299–307. Miller MR. 1952. The normal histology and experimental alteration of the adrenal of the viviparous lizard, Xantusia vigilis. Anat Rec 113:309–323. Miller MR, Beck J. 1987. Heterotopic synaptic bodies in the auditory hair cells of adult lizards. Anat Rec 218:338–344. Moscona AA. 1990. Anatomy of the pancreas and Langerhans islets in snakes and lizards. Anat Rec 227:232–244. Neaves WB. 1971. Intercellular bridges between follicle cells and oocyte in the lizard, Anolis carolinensis. Anat Rec 170: 285–301. Pannese E, Ledda M, Arcidiacono G, Rigamonti L, Procacci P. 1984. A comparison of the density of microtubules in the central and peripheral axonal branches of the pseudounipolar neurons of lizard spinal ganglia. Anat Rec 208: 595–605. Payne SL, Holliday CM, Vickaryous MK. 2011. An osteological and histological investigation of cranial joints in geckos. Anat Rec 294:399–405. Prakash R. 1960. The heart and its conducting system in the lizard Calotes versicolor (Daudin). Anat Rec 136:469–475. Proske U. 1969. Nerve endings in skin of the Australian black snake. Anat Rec 164:259–266. Rabinowitz T, Tandler B. 1986. Papillary morphology of the tongue of the American chameleon: Anolis carolinensis. Anat Rec 216:483–489. Rabinowitz T, Tandler B. 1991. Ultrastructure of lingual salivary glands in the American chameleon: Anolis carolinensis. Anat Rec 229:489–494. Rehorek SJ. 1997. Squamate Harderian gland: an overview. Anat Rec 248:301–306. Rhoten WB. 1982. Continuous-perifusion tissue culture of fetal and adult pancreas of the lizard Anolis carolinensis. Anat Rec 203:165–173. Rhoten WB. 1984. Immunocytochemical localization of four hormones in the pancreas of the garter snake, Thamnophis sirtalis. Anat Rec 208:233–242. Rhoten WB, Hall CE. 1981. Four hormones in the pancreas of the lizard, Anolis carolinensis. Anat Rec 199:89–97. Rubolini D, Pupin F, Sacchi R, Gentilli A, Zuffi MA, Galeotti P, Saino N. 2006. Sexual dimorphism in digit length ratios in two lizard species. Anat Rec 288:491–497. Sligar CM, Voneida TJ. 1981. Efferent projections of the septum in the Tegu lizard, Tupinambis nigropunctatus. Anat Rec 201: 197–202. Throckmorton GS. 1978. Action of the pterygoideus muscle during feeding in the lizard Uromastix aegyptius (Agamidae). Anat Rec 190:217–222. Throckmorton GS, Saubert CW, IV. 1982. Histochemical properties of some jaw muscles of the lizard Tupinambis nigropunctatus (Teiidae). Anat Rec 203:345–352. Toubeau G, Cotman C, Bels V. 1994. Morphological and kinematic study of the tongue and buccal cavity in the lizard Anguis fragilis (Reptilia:Anguidae). Anat Rec 240: 423–433. Wetzstein HY, Stratton CJ, Olson N. 1980. The stereoscanning electron microscopy and ultrastructural histochemistry of the avian and reptilian surfactant systems: Indian dove, desert spiny and Taiwan golden skink lizards. Anat Rec 197: 63–73. Wise PA, Russell AP. 2010. Development of the dorsal circumorbital bones in the leopard gecko (Eublepharis macularius) and its bearing on the homology of these elements in the gekkota. Anat Rec 293:2001–2006. Wise PA, Vickaryous MK, Russell AP. 2009. An embryonic staging table for in ovo development of Eublepharis macularius, the leopard gecko. Anat Rec 292:1198–1212.



Yeager VL, Taylor JJ, Chang PL. 1983. Light microscopy of the pineal organ of two primitive lizards, Platyurus platyurus and Hemidactylus frenatus. Anat Rec 206:283–288. Young BA, Marsit C, Meltzer K. 1999. Comparative morphology of the cloacal scent gland in snakes (Serpentes: Reptilia). Anat Rec 256:127–138. Zika J, Singer M. 1965. The relation between nerve fiber number and limb regenerative capacity in the lizard, Anolis. Anat Rec 152:137–140.

*Correspondence to: Dr. Kurt Albertine, Editor-in-Chief, The Anatomical Record, University of Utah, Salt Lake City, UT 84108. Fax: 801/585-7395. E-mail: [email protected] Received 4 January 2014; Accepted: 4 January 2014. DOI 10.1002/ar.22873 Published online 31 January 2014 in Wiley Online Library (wileyonlinelibrary. com).

The anatomical record is alive with leapin' lizards and slitherin' snakes.

The anatomical record is alive with leapin' lizards and slitherin' snakes. - PDF Download Free
55KB Sizes 14 Downloads 0 Views