DERMAL IRIDOPHORES IN SNAKES; CORRELATIONS WITH HABITAT ADAPTATION AND PHYLOGENY
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University Microfilms International 300 N. ZEEB RD., ANN ARBOR. Ml 48106 8207900
Kleese, William Carl
DERMAL IRIDOPHORES IN SNAKES; CORRELATIONS WITH HABITAT ADAPTATION AND PHYLOGENY
The University of Arizona PH.D. 1981
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University Microfilms International
DERMAL IRIDOPHORES IN SNAKES; CORRELATIONS
WITH HABITAT ADAPTATION AND PHYLOGENY
by-
William Carl Kleese
A Dissertation Submitted to the Faculty of the
COMMITTEE ON ANIMAL PHYSIOLOGY (GRADUATE)
In Partial Fulfillment of the Requirements For the Degree of
DOCTOR OF PHILOSOPHY
In the Graduate College
THE UNIVERSITY OF ARIZONA
19 81 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE
As members of the Final Examination Committee, we certify that we have read
the dissertation prepared by William C- KIrf-sr
entitled Dermal Tri dophnrpg in Snakpg; rnrrplatinm; with
Habitat Adaptation and Phylogeny
and recommend that it be accepted as fulfilling the dissertation requirement
for the Degree of Doctor of Philosophy •
P. J , /K- /<9dP/ jDate 7
Date 'r - -7777771
Date
/v /9F/ Date
/VQfw-&& n Otj-, ml Date
Final approval and acceptance of this dissertation is contingent upon the candidate's submission of the final copy of the dissertation to the Graduate College.
I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement.
//' /Ar- • dissertation Director Date STATEMENT BY AUTHOR
This dissertation has been submitted in partial fulfillment of requirements for an advanced degree at The University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the library.
Brief quotations from this dissertation are allowable without special permissiom, provided that accurate acknowledgment of source is made. Requests for permission for extended quotation from or reproduc tion of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his judgment the proposed use of the material is in the interests of scholar ship. In all other instances, however, permission must be obtained from the author.
SIGNED: To my wife and our children for their patience, support and understanding. To Clyde R. Peeling and his Reptiland where my interest in herpetology was kindled and nurtured some years ago.
iii ACKNOWLEDGMENTS
I thank Dr. Robert B. Chiasson, Department of Veterinary Science,
University of Arizona, for assistance as research director, for time, facilities, and incidental financial expenditures, and for never-failing academic counsel and personal encouragement; Dr. Mac E. Hadley,
Department of General Biology, University of Arizona, for personal tutor ing in chromatophore biology and for use of his personal literature collection; Dr. James N. Shively, Department of Veterinary Science,
University of Arizona, assisted by Helen Thompson, Marjorie Nard and Jan
MacMillen, for use of facilities and for the preparation of hundreds of histological sections; Mr. Gopinath S. Rao, Department of Veterinary
Science, University of Arizona, for instruction in electron microscopy;
Dr. Wayne R. Ferris, Department of Cellular and Developmental Biology,
University of Arizona, for use of dark room facilities and for assistance with electron microscopy; Dr. John A. Rupley, Department of Biochemistry and Dr. Robert D. Feltham, Department of Chemistry, University of Arizona, for use of spectrophotometry equipment.
Specimens were supplied for sampling and study by the following individuals and institutions; Mr. Mark Dodero, San Diego Natural History
Museum; Dr. M. J. Fouquette, Arizona State University; Dr. Howard K.
Gloyd (deceased), personal collection; Dr. Charles H. Lowe, Jr.,-
University of Arizona; Mr. John Martin, personal collection; Sherman A.
Minton, Jr., M.D., personal collection; Dr. Charles W. Myers, American
iv V
Museum of Natural History; Dr> Max A. Nickerson, Milwaukee Public Museum;
Mr. Clyde R. Peeling, Clyde Peeling's Reptiland; Mr. Steven Prchal,
Arizona-Sonora Desert Museum; Dr. Douglas A. Rossman, Louisiana State
University; Dr. James Scudday, Sul Ross State University; Dr. Cecil
Schwalbe, University of Arizona; Dr. Thomas R. Van Devender, Arizona
Natural Heritage Program.
Dr. Robert B. Chiasson, Dr. Roger Conant and Dr. Sherman A.
Minton, Jr. each contributed data from their own unpublished research.
Financial support was obtained in part from Sigma Xi, The
Research Society, in part from The University of Arizona Graduate Student
Development Fund, and in part from personal funds. TABLE OF CONTENTS
Page
LIST OF ILLUSTRATIONS vii
LIST OF TABLES ix
ABSTRACT X
INTRODUCTION 1
METHODS AND MATERIALS 5
Sample Collection and Preparation 5 Microscopy and Reflectometry 5 Physical and Physiological Correlations ...... 7 Statistics 9
RESULTS 10
Iridophore Patterns 10 Reflectance and Albedo 26 Physical and Physiological Correlations 28
DISCUSSION 32
REFERENCES 37
vi LIST OF ILLUSTRATIONS
Figure Page
1. Reproduction of work graphs utilized in calculating the 250 nm to 750 ran wavelength range albedo for selected crotalid snakes 8
2. Transmitted light and polarized light photomicrographs of a transverse section of a single scale taken at a midbody dorso-lateral location from Agkistrodon contortrix phaeo gaster 16
3. Transmitted light and polarized light photomicrographs of a transverse section of a single scale taken at a midbody dorso-lateral location from Agkistrodon contortrix pictigaster 17
4. Transmitted light and polarized light photomicrographs of a transverse section of a single scale taken at a midbody dorso-lateral location from Agkistrodon caliginosus . . 18
5. Transmitted light and polarized light photomicrographs of a transverse section of a single scale taken at a midbody dorso-lateral location from Agkistrodon blomhoffii brevicaudus 19
6. Transmitted light and polarized light photomicrographs of a transverse section of a single scale taken at a midbody dorso-lateral location from Crotalus atrox 20
7. Transmitted light and polarized light photomicrographs of a transverse section of a single scale taken at a midbody dorso-lateral location from Crotalus durissus durissus . 21
8. Transmitted light and polarized light photomicrographs of a transverse section of a single scale taken at a midbody dorso-lateral location from Crotalus aquilus 22
9. Transmitted light and polarized light photomicrographs of a transverse section of a single scale taken at a midbody dorso-lateral location from Crotalus cerastes cerastes . 23
10. Survey electron photomicrograph of the dermis of Agkistrodon contortrix mokasen, illustrating the isolated cells iridophore pattern 24
vii viii
LIST OF ILLUSTRATIONS—Continued
Figure Page
11. Survey electron photomicrograph of the dermis of Crotalus scutulatus scutulatus, illustrating the heavily layered iridophore pattern 25
12. Reflection of light from the skin of selected crotalid snakes 27
13. Dendrogram of the genera Agkistrodon, Calloselasma, Deinagkistrodon and Hypnale annotated, with light microscopy data on iridophores 30
14. Dendrogram of the genera Crotalus and Sistrurus annotated with light microscopy data on iridophores 31 LIST OF TABLES
Table Page
1. Comparative data for correlation of iridophore pattern with dorsal coloration and/or ecological niche for 147 species and/or subspecies of snakes 11
ix ABSTRACT
Deep continuous layers of iridophores were discovered in certain
Asian Agkistrodon species. A survey of available snakes showed the banded
iridophores to be present in North American Crotalus and Sistrurus also,
indicating an unreported morphology to be a possibly common phenomenon.
Skin samples from 147 species and/or subspecies of snakes of the
families Leptotyphlopidae, Boidae, Colubridae, Elapidae and Viperidae were
examined and photographed by polarized light microscopy. Dermal iridophore
patterns were visually identified and categorized as 1) isolated cells,
2) lightly layered, 3) moderately layered and 4) heavily layered.
Selected specimens were examined and photographed by electron microscopy;
isolated iridophore ultrastructure and layered iridophore ultrastructure
patterns are illustrated and described.
Reflectometry of four selected crotalids reveals positive correla
tion between iridophore quantities and albedo, but habitat adaptation and
correlation of individual species/subspecies is difficult to show and only
subjectively suggested. Published phylogenies of the species of the
genera Agkistrodon, Calloselasma, Deinagkistrodon and Hypnale are revised
to reflect recent taxonomic works and are correlated with iridophore
pattern data. Phylogenetic relationships of Crotalus and Sistrurus are also revised with recent publications; they are neither supported nor
contradicted because layered iridophores occur in all of their phylo
genetic groups.
x INTRODUCTION
The formation and replacement of the squamate epidermis (Maderson et_al_. 1970) and the structure of the dermis (Schmidt 1914, von Geldern
1921, Rahn 1941, Maderson 1964) of squamates have been described. A characteristic feature of the reptilian integument is the presence of a complex pigmentation which includes melanophores, iridophores, xantho- phores and erythrophores.
Amphibian and reptilian chromatophores have been described by von
Geldern (1921), Parker (1938, 1948), Hadley and Quevedo (1967), Bagnara et al_. (1968), Bagnara et al. (1969), Alexander and Fahrenbach (1969),
Taylor and Hadley (1970), Rohrlich and Porter (1972), Miscalencu and
Ionescu (1972, 1973), Bagnara and Hadley (1973) , Nielsen and Dyck (1978) and Nielsen (1978); they are similar in most respects but there are some important differences. Amphibian epidermal melanophores respond to appro priate stimuli by aggregating or dispersing melanin granules; reptilian epidermal melanophores, with a certain few exceptions, are not capable of this (Hadley and Quevedo 1967, Taylor and Hadley 1970). The dermis of amphibians and reptiles usually contains several different chromato phores - melanophores, iridophores, xanthophores and/or erythrophores. In amphibians, and in a few reptiles, the dermal chromatophores disperse or aggregate cytoplasmic pigment organelles when appropriately stimulated, or complete cells may alter their shape and/or position. Such effects do not occur in the majority of reptiles (Bagnara and Hadley 1973).
1 2
Amphibians have a dermal chromatophore unit (Bagnara et al. 1968) arrangement of the cells, while reptiles, with the exception of some lizards, do not (Alexander and Fahrenbach 1969, Taylor and Hadley 1970,
Miscalencu and Ionescu 1972, 1973). The amphibian dermal chromatophore unit includes three types of chromatophores - melanophores, iridophores and xanthophores - in a layered arrangement. Xanthophores (and/or erythrophores) lie outermost, just beneath the basal lamina; iridophores are just beneath the xanthophores, and melanophores are the basal cell of the unit. The melanophores may be just beneath the iridophores or they may be somewhat dissociated from the other chromatophores; when all three types of cells are arranged in close association, there are no chromato phores in the deep dermis. Amphibian melanophores have numerous dendritic processes which reach upwards from the basal cells, pass the overlying iridophore(s), and extend laterally between the iridophore(s) and the more superficial xanthophore(s). Melanosomes, the pigment-carrying organelles of the melanophore, are moved about within the cell and its dendritic processes in response to certain hormones or neuronal stimulation. The iridophore alters its shape and size in counter-concert with melanin dispersion and the xanthophore may alter both its shape and its position in the chromatophore unit (Bagnara et al_. 1968, Taylor 1969, Nielsen 1978).
This movement of pigment and alteration of cell shape and/or position affect dramatic quick color changes in the amphibian. The action is termed physiological color change and is contrasted to morphological color change which involves an increase or reduction of pigment(s) over a period of several days or more in response to environment, season, breeding cycle, etc. (Bagnara and Hadley 1973). 3
In reptiles, a chromatophore unit similar to that of amphibians
occurs in the genus Anolis, with three minor differences: (1) there are
three or four layers of iridophores rather than just one, (2) the
processes of the melanophore(s) reach upward and around both the irido
phores and the xanthophore(s) rather than passing between the iridophores
and xanthophores, and finally (3) Anolis iridophores cannot alter their shape or size as do amphibian iridophores (Taylor and Hadley 1970).
One might surmise that an amphibian-like chromatophore unit
occurs in other lizards showing marked physiological color change; the
North American horned lizards (Phrynosoma) have been so reported (Parker
1938) and the master color-change artists, the African chameleons
(Chamaeleo), have been shown to be most dramatic (Zoond and Eyre 1934,
Sand 1935, Parker 1948).
The integument of two genera of snakes, Natrix and Vipera, has been examined by electron microscopy (Miscalencu and lonescu 1972, 1973), and these authors reported possible but questionable dermal chromatophore units for the European grass snake (Natrix natrix) and the positive lack of the unit in the European long-nosed viper (Vipera ammodytes). The principal types of chromatophores occur in their usual three-layered orientation in the dermis, but they are not clearly organized as func tional units. The ophidian iridophore platelets are randomly arranged rather than oriented in ordered rows as in amphibians and Anolis, and the melanophores have no upward-extending processes; neither melanosome move ment nor color change occur.
Chiasson (personal communication) observed iridophores in wide continuous layers several layers deep in the dermis of certain Asian 4
species of Agkistrodon and, with the use of polarized light, easily
determined the distribution and occurrence of the iridophores. I have
found the iridophore band described by Chiasson to be present in eight
out of twelve genera examined, indicating a possibly common phenomenon.
A study was designed to determine the morphology of the dermis in the area
of the iridophore band, using both light and electron microscopy, and
compare snakes with and without the band. My objectives were determina
tion of any possible physiological function through correlation with habitats and exploration of phylogenetic relationships through correlation
with published crotaline phylogenies. MATERIAL AND METHODS
Sample Collection and Preparation
Dorso-lateral skin samples were taken from a midbody location from
147 species and subspecies of snakes (Table 1). This group includes all members of the genera Agkistrodon, Calloselasma, Deinagkistrodon, Hypnale and Sistrurus, and approximately 60% of the genus Crotalus and 85% of
Thamnophis. Additional specimens from the families Leptotyphlopidae,
Boidae, Colubridae and Elapidae were also used for comparison. An indi vidual scale was carefully excised from each skin sample and prepared for histological study. With specimens of the genus Thamnophis, two samples were taken, one from the lateral stripe and one from the dorso-lateral area between stripes. Excised scales were fixed in 10% formalin, dehy drated to 100% ethanol, cleared with xylene, and embedded in Tissue Prep
(Fischer Scientific) at 60 C. Five-micrometer sections were cut trans versely with a steel knife and stained with hematoxylin and eosin.
Tissues for ultrastructural examination were fixed in 4% glutar- aldehyde, post-fixed in 1% osmium tetroxide, dehydrated to 100% ethanol, cleared with propylene oxide, and embedded in EMbed 812 (Electron
Microscopy Sciences) at 60 C. One-tenth-micrometer sections were cut with a diamond knife and stained with uranyl acetate and lead citrate.
Microscopy and Reflectometry
Thick sections (5.0 pm) were examined by polarized light
5 6
microscopy. Plastic polarizing discs (American Optical Co.) were placed
in the light beam path, one at the base of the ocular tube and one under
the condensor. Crossed polars was obtained by manual manipulation of the
exposed lower disc. Viewed in this light, iridophore patterns were cate
gorized in four groups: 1) isolated cells, 2) lightly layered, 3) moder
ately layered, and 4) heavily layered cells. Ultrathin sections (0.1 pm)
were examined by transmission electron microscopy utilizing routine
techniques.
Circular segments of whole skin 2.5 cm in diameter were taken from
midbody locations on cryo-anesthetized live rattlesnakes. The skin seg
ments were pressed between two layers of wet filter paper to obtain a
uniform flatness and reflection readings were taken immediately before tissue fluids evaporated. Reflectance was measured with a Zeiss PMQII
spectrophotometer and RA2 reflectance attachment. The angle of light reflectance was 45°; reflectance percentages were standardized with mag nesium carbonate. Two different specimens of each species were measured at 10 nm wavelength intervals from 250 nm to 750 nm inclusive. The paired data were averaged and the means were plotted graphically to produce a reflectance curve for each species.
Measurements below 250 nm wavelength represent the short wave ultraviolet (the mid-range and long wave ultraviolet from 250 nm to 400 nm were measured) which reaches the earth in only iieglible amount (Sellers
1965, p. 20) and does not affect biological systems. However, measure ments above 750 nm represent infrared radiation (infrared = 700 nm to approximately 1,000,000 nm) which does affect a considerable heat absorp tion in ectothermic animals. These measurements were not made because of 7
limitations of equipment used but would be a good subj ect for further
investigation when adequate facilities become available.
The term albedo refers to the percent reflected of total incident radiation over a wide range, usually the solar spectrum or the visible light wavelengths of 400 nm to 700 nm. In this study and in the context of this report, it is applied to the 250 nm to 750 nm wavelengths as this was the practical working limitation of the spectrophotometry equipment used. Albedo for a given species was calculated by plotting reflectance data on a work graph in which the wavelength axis was paralleled by one showing wave numbers per centimeter (Figure 1). Such a graph depicts wave numbers in simple arithmetic series and wavelength in logarithmic form, and generates an albedo curve which is a true physical representa tion and not skewed. On the work graph the curve representing incident solar radiation at the earth's surface (Sellers 1965, p. 20) was plotted above the albedo curve. The graph was then cut along the plotted curve lines and the resulting upper and lower segments were individually weighed on an analytical balance to the nearest tenth of a milligram.
The weight of the lower segment (area under the albedo curve) was calcu lated as a percent of the total weight of both segments (total irradiance) thus producing the albedo percentage.
Physical and Physiological Correlations
In addition to noting iridophore patterns, Table 1 includes tabulated data for principal dorsal colorations, habitats, latitudinal ranges and daily activity patterns. Desired correlative comparisons were made directly. Wavelength, nm 250 300 350 400 450 500 550 650 750 -i—r |i 1 I i |I I I I| I I I |I I I I'(I I |||l 111|11 I|l I 111
E o Incident solar radiation t. o-o-o Crofalus molossus molossus © 0.00008 a 0 M s - Crotalus atrox 'i Crotalus cerastes laferorepens and t. « Crotalus cerastes cercobombus are a CN 0.00006 not illustrated E u t. « Q. "a u 0.00004 •» 0 u e o o t. 0.00002
I I I 1 I 35,000 30,000 25,000 20,000 15,000 Wave Numbers per cm Figure 1. Reprduction of work graphs utilized in calculating the 250 nm to 750 nm wavelength range albedo lor selected crotalid snakes (correlated with Figure 12). 9
For phylogenetic correlations, a dendrogram of the genera
Agkistrodon, Calloselasma, Deinagkistrodon and Hypnale was constructed by- revising Brattstrom's (1964) dendrogram of Agkistrodon to reflect new and revised taxa published by Gloyd (1969, 1972a, 1972b, 1977, 1978). Data relating iridophore patterns were noted with each species and subspecies.
Phylogenetic correlations were made directly. A similar procedure for the rattlesnakes was done with a dendrogram from Brattstrom (1964) combined with a dendrogram from Klauber (1972) and then revised to reflect the taxonomic publications of Harris and Simmons (1978), Campbell (1978),
Campbell and Armstrong (1979) and Collins and Knight (1980).
Statistics
Chi square analysis was applied to the reflectance data.
Reflectance and albedo percentages were converted to frequency format by designating the reflectance as one category and absorbance (100% minus the reflectance percentage) as a second category. Each reflectance read ing thus generated two frequency quantities and a contingency table was formulated for each wavelength data set, i.e., a table for 250 nm, another for 260 nm, etc. Chi square was then calculated for each contin gency table in routine fashion. RESULTS
Iridophore Patterns
Among the 147 different snakes studied there are numerous occur rences of banded iridophores in crotaline snakes (Table 1). The colubrid genera Pituophis and Thamnophis, and the boid genus Python, also exhibit these bands. Although heretofore unreported, the close banding of irido phores is probably common among snakes.
The iridophore patterns denoted in Table 1 are in four categories:
1) isolated cells, 2) lightly layered, 3) moderately layered, or 4) heavily layered cells. The first category has no iridophores visible with
X400 polarized light microscopy, and is illustrated in Figures 2 and 6.
The lightly layered cells (Figures 3 and 7) have iridophores visible in one or two layers which occur peripherally or as isolated small groups.
The moderately layered cells (Figures 4 and 8) have one to three layers of iridophores lying side by side as a solid layer(s) across the entire scale. The heavily layered cells (Figures 5 and 9) are four or more cell layers deep extending across the entire scale.
Transmission electron microscopy revealed that the total cross- sectional area of dermis populated by chromatophores does not vary sub stantially within a genus. The principal difference between an isolated- cell iridophore pattern (Figure 10) and a heavily-layered iridophore pattern (Figure 11) is a marked increase in the density of the iridophore population, with no change in the remaining chromatophore (melanophore, 10 TABLE 1. Comparative data for correlation of iridophore pattern with dorsal coloration and/or ecological niche for 147 species and/or subspecies. Uaily Species/Subspecies Iridophore Pattern Principal Dorsal Coloration Habitat Type Latitude Range Activity
dark brown with forested, Aaklsrrodon hilineatus hilineatus scattered - 29°N 'adaptive fine white Barkings •esic to riparian 10
Mdiua brown with forested, Aekistrodon bilineotus rujscolus scattered - 21°N fine white Barkings •esic to riparian 18 adaptive
dark brown with forested, Aekistrodon hilineatus tavlori scattered 23 - 25°N adaptive fine white nrLings •esic to riparian
aoderately layered light brown with forested, Aekistrodon blonhoffii bloahoffii 24 - 39°N diurnal to heavily layered dark blotches aesic
heavily light brown with forested, Aekistrodon bloahoffii brevicaudus 3S - 41°N diurnal layered dirk blotches aesic to riparian
light bTown with forested, Avkistrodon bloohoffii rfnbitatus scattered 41°N dark blotches aesic diurnal
light brown with forested, Aekistrodon bloohoffii siniticus scattered 27 - 35°H diurnal dark blotches aesic
light brown with forested, Aekistrodon bloohoffii ussuriensis scattered 45 - 48°N diurnal dark blotches aesic
aoderately forested, Aekistrodon calieinosus dark brown 35 - 42°N adaptive layered aesic to riparian
light brown with forested, Aekistrodon contortrix contortrix scattered 28 - 37°N adaptive dark blotches aesic to riparian
yellowish-brown with forested, Aekistrodon contortrix laticinctus scattered 28 - 38°N adaptive reddish-brown blotches •esic to riparian
reddish-brown with forested, Aekistrodon contortrix aokasen scattered 32 - 42°N adaptive dark blotches aesic to riparian
scattered.to light brown with wooded, Aekistrodon contortrix oictieaster 28 - 32°N adaptive lightly layered dark blotches •esic to riparian
reddish-brown with forested, Aekistrodon contortrix ohaeoeaster scattered 37 . 42°N adaptive dark blotches aesic to riparian
aoderately light brown with grassland, Aekistrodon halvs halvs 43 - 52°N nocturnal layered dark blotches xeric to aesic
aoderately - light brown with grassland, Aekistrodon halvs caraeanus 41. 48°N nocturnal layered dark blotches xeric to aesic
aoderately light brown with grassland, Aekistrodon halvs cotrnatus 34 . 37°N nocturnal layered dark blotches xeric to aesic
aediun brown with forested, Aekistrodon hinalavanus scattered 26 - 30°N diurnal black blotches aesic aountains
light brown with forested, Aekistrodon intenaedius intenaedius scattered 43 - 52°H adaptive dark blotches •esic
aoderately layered light brown with grassland to Aekistrodon internedius caucasicus 35 - 43°N adaptive to heavily layered dark blotches forested, aesic
light brown with forested, Aekistrodon intenaedius stelneeeri scattered 43 - 49°N nocturnal dark blotches aesic
dark brown with forested, Aekistrodon oonticola scattered 24 - 27°N diurnal black blotches aesic
dark brown with wooded, Aekistrodon niscivorus niscivorus scattered 32 - J7°N adaptive black blotches riparian
dark brown with wooded, Aekistrodon oiscivorus conanti scattered 25 - J2°N adaptive black blotches riparian
wooded, Aekistrodon oiscivorus leucostoma 28 - 3S°N adaptive scattered dark brown riparian
gray with grassland to forested, Aekistrodon saxatilis scattered ' 35 - S3°N adaptive dark brown blotches aesic to riparian
aoderately dark brown with grassland to forested, Aekistrodon strauchi ' 31 . 36°N diurnal layered black spots xeric to aesic
light brown with forested, Boa constrictor constrictor scattered 1S°S1 . I0°N diurnal dark brown blotches riparian
'adaptive > diurnal or nocturnal as dictated by environaental conditions TABLE 1—Continued. Daily Latitude Species/Subspecies Iridophore Pattern Principal Dorsal Coloration Habitat Type Range Activity Pattern heavily gray with forested, Calloselasoa rhodostoaa 8°i; - i7°H layered dark brown blotches aesic to riparian nocturnal
light brown with wooded, Crotalus adaaanteus scattered 25 - 36°N adaptive black diaaonds aaslc to riparian
aoderately light brown with grassy to wooded, Crotalus aouilus 19 - 22°N adaptive layered dark brown blotches aesic
gray with grassy to bnishy, Crotalus atrox scattered 22 - 37°N adaptive white-aargined brown blotches seai-arid to aesic
olive with white-aargined forested, Crotalus basiliscus basiliscus scattered 18 - 27°N diurnal reddish-brown diaaonds seai-arid to aesic
gray-brown with white-aargined forested, Crotalus baailiscus oaxacus scattered 17°H diurnal dark brown diaaonds aesic
gTay-brown with sparse brush, Crotalus catalinensis scattered 26°N diurnal dark brown blotches seai-arid
heavily tan with arenaceous, Crotalus cerastes cerastes 54 - 37°N adaptive layered black spots seai-arid
heavily tan with arenaceous, Crotalus cerastes cercoboabus 28 - 34°H adaptive layered black spots seai-arid
heavily tan with arenaceous, Crotalus cerastes lateroreoens 30 - 34°N adaptive layered black spots seai-arid
scattered to yellowish with white-aargined grassy to wooded, Crotalus durissus durissus 9 - 19°N adaptive lightly layered dark brown diaaonds seai-arid to aesic
brown with yellow-line brushy, Crotalus durissus terrificus scattered 11 - 32°S adaptive reticulate diataond pattern seai-arid
light brown with white-aargined wooded, Crotalus durissus t2abcan scattered 17 - 22°N adaptive dark brown diamonds aesic to riparian
light brown with arenaceous to Crotalus enyo envo scattered 23 - 29°N adaptive dark brown blotches brushy, seai-arid
gray with arenaceous to Crotalus envo cerralv»»nsi» scattered 24°H adaptive black blotches brushy, seai-arid
pinkish with arenaceous to Crotalus exsul scattered 28°N adaptive brown blotches brushy, seai-arid
scattered to gray or yellow with brushy to wooded, Crotalus horridus 28 - 45°N adaptive lightly layered black crossbands aesic to riparian
gray with brushy to wooded, Crotalus interaedius interaedius scattered 19 - 21°N diurnal brown blotches seoi-arid to aesic
lightly aottled gray brushy to woded, Crotalus lepidus leoidus 22 - 32°N adaptive layered and brown semi-arid to aesic
greenish-gray with brushy to forested, Crotalus lepidus klauberi scattered 20 - 33°N diurnal dark brown bars seai-arid to aesic
gray with wooded, Crotalus lepidus norulus scattered 22 - 23°N diurnal dark brown bars aesic
aottled gray barren to brushy, Crotalus Bitehellii aitchellii scattered 23 - 28°N adaptive and brown seai-arid
pinkish with barren to brushy, Crotalus Bitehellii aneelensis scattered 29°N . adaptive brown blotches seai-arid
aottled pink, barren to brushy, Crotalus nitchellii suertensis scattered 30°N adaptive gray and brown seai-arid
tan with barren to brushy, Crotalus Bitehellii pvrrhus scattered 28 - 37°N adaptive black blotches seai-arid
gray with barren to brushy, Crotalus aitchellii steohensi scattered 35 - JS°N adaptive dark brown blotches seai-arid
lightly yellowish with wooded and rocky, Crotalus nolossus nolossus 26 - 36°N adaptive layered dark brown blotches aesic
yellowish with white-aargined grassy to wooded, Crotalus aolossus nirrescens scattered 17 - 23°K adaptive brown blotches aesic
gray with grassy to wooded, Crotalus polystictus scattered 19 - 22°N adaptive dark brown spots aesic to riparian
barren to wooded, Crotalus price! oricei aoderately layered gray with 23 - 3J°N diurnal to heavily layered brown spots aesic TABLE 1—Continued.
Latitude Daily Species/Subspecies Iridophore Pattern Principal DoTsal Coloration Habitat Type Activity Range Pattern blown with forested, Crotalus puslllus scattered IS - 20 N diurnal black blotches aesic
reddish-brown with barren to grassy, Crotalus ruber ruber scattered 26 - 34°N adaptive dark brown blotches seai-atid to aesic
yellowish with white-margined barren to brushy, Crotalm roher lucasensls scattered 23 - 26°N adaptive reddish-brown blotches scai-arld
heavily light brown with white-aargined arenaceous to brushy, Crotalm scutulatut scutulatus 21 - 38°N adaptive layered dark brown diaaonds seal-arid to aesic
olive-gray with barren to wooded, Crotalus scutulatus salvini scattered 19 - 21°N adaptive dark brown diamonds seal-arid to aesic
settled lavender, barren, Crotalus tlgTis scattered 27 - 33°N nocturnal pink and brown ami-arid
heavily gray with barren, Crotalus tortueensis 27°N layered brown blotches smi-arid adaptive
gray with barren to grassy, Crotalus triseriatus triserlatus scattered 21 - 24°N diurnal brown blotches aesic
aottled barren to brushy, Crotalus unicolor Mastered 11°N adaptive gray-brown seai-srld
aoderately layered gray with barren to grassy, Crotalus vlridis vlridis 28 - 51°N diurnal to heavily layered dark brown blotches aesic
aottled Crotalus viTldls abyssua barren, light brown 36°N diurnal aesic
gray with brushy, Crotalus viridis callginis 32°N diurnal dark brown blotches smi-arid
aottled forested, Crotalus viridis cerberus 32 - 36°N diurnal black and brown aesic
aoderately layered barren, Crotalus viridis concolor aottled yellow 37 - 41°N diurnal to heavily layered aesic
light brown with grassy to wooded, Crotalus viridis helleri scattered 28 - 35°N adaptive dark brown blotches seoi-arid to aesic
gray with Crotalus viridis lutosus scattered barren to wooded, dark brown blotches 36 - 45°N adaptive smi-arid to aesic
reddish-brown with barren to bnishy, Crotalus vlridis nuntlus scattered 35 - 37°K adaptive dark brown blotches seoi-arid to aesic
gray with barren to forested, Crotalus vlridis oreganus 35 - S1°N adaptive dark brown blotches saai-arid to aesic
brown with forested, Crotalus wlllardi wlllardi white bars 31 - 32 N diurnal aesic to riparian
lightly Crotalus wlllardi obscums gray with forested, layered 32 N diurnal white bars aesic to riparian
gray with forested, Crotalus wlllardi sllus scattered 27 - 31°H diurnal white bars aesic
light brown with forested, Dcinaeklstrodon acutus scattered 18 - 25°N adaptive dark brown blotches aesic
forested, e aoderately •ottled 7 - 12°N adaptive Hypnale hypnal layered gray and brown aesic
oedlua brown with forested, Hypnale nepa scattered 7 - 9°N adaptive dark blotches aesic
olive brown with forested, Hypnale walll scattered 7 - 9°N black spots aesic to riparian adaptive
Leptotyphlops hunllls hunilIs none light brown subterranean 27 - 36 N nocturnal
glossy black brushy to forested, Ophlophagus hannah 2 - 30 N adaptive (juvenile) aesic to riparian
heavily buff with grassy to wooded, Pltuophis aelanoleucus *ffinis 20 - 37°N diurnal layered brown blotches seoi-arid to aesic
lightly gray with grassy to forested, Python BPlorus bivlttatus 6°S - 27°N layered brown blotches aesic to riparian diurnal
gray with grassy to wooded, Slstnirus catenatus catenatus 38 - 46°N adaptive dark brown blotches aesic to riparian TABLE 1--Continued. Tany Latitude Species/Subspecies Iridophore Pattern Principal Dorsal Coloration Habitat Type Range Activity
scattered to gray with grassy, Sistrurus catenatus edwardsii 26 - 3»°N adaptive heavily layered brown blotches sai-arid to aesic
gray with grassy, Sistrurus catenatus terseninus scattered - 42°N adaptive brown blotches aesic to riparian 27
gray with wooded, Sistrurus niliarius niliarius scattered - 36°N adaptive dark brown blotches aesic 32
grayish-biown with grassy to wooded, scattered - 33°N adaptive Sistrurus ailiarius barbouri dark brown blotches aesic to riparian 25
light brown with grassy, scattered 27 - 3«°N adaptive Sistrurus niliarius streckeri dark brown blotches aesic to riparian
heavily gray with rocky and grassy, Sistrurus ravus ravus 18 - 20°N diurnal layered black blotches aesic
dark brown with grassy, Thannophis brachvstoaa scattered 41 - 42°N diurnal light brown stripe aesic to riparian
black with grassy, ThannoBhis butVeri scattered 39 - 4S°N diurnal yellow stripe aesic to riparian
unifora grassy to wooded, Thannophis chrvsocephalus scattered 16 - l»°N adaptive light brown aesic to riparian
scattered to nettled gray wooded, Thamoohis couch! coucKi 35 - 41°N diurnal lightly layered and black riparian
black with wooded, ThamnoDhis couchi aouaticus scattered 38 - 40°N diurnal yellow stripe riparian
checkered black and gray wooded, Thannophis couchi eieas scattered 35 - 38°N diurnal with yellow stripe riparian
unifora wooded, Thannophis couchi hannondi scattered 30 - 37°N diurnal gray riparian
olive with black spots grassy to forested, Thannophis cvrtonsis cvrtocsis scattered 22 - 3S°N adaptive and with OTange stripe aesic to Tiparian
brown with black spots grassy to wooded, Thannophis cvrtoosis collaris scattered 15 - 2?°N adaptive and with orange stripe aesic to riparian
blotchy brown and yellow barren to wooded, Thannoohis cvrtoosis ocellatus scattered 30 - 31°N adaptive with orange stripe nesic to riparian
uniforn grassy to wooded, Thannophis dieueti scattered 24 - 27°N adaptive gray aesic to riparian
black with forested, Thasmophis elesans elesans scattered 37 - 45°N diurnal yellow stripe aesic to riparian
dark brown with forested, Thannophis elesans biscutatus scattered 42 - 4J°N diurnal yellow stripe aesic to riparian
unifora grassy to forested, Thannophis eleeans errans scattered 23 - 30°N diurnal brown aesic to riparian
•ottled aulticolor with grassy to wooded, Thannophis elesans terrestris scattered 34 - 42°N diurnal yellow stripe aesic to riparian
brown with black spots grassy to forested, Thannophis elesans vaerans scattered 33 - 54°N diurnal and with white stripe aesic to riparian
brown with black spots grassy to forested, 18 - 29°N diurnal Thannophis eoues eoues scattered and with orange stripe aesic to riparian
olive with black spots grassy to forested, Thannophis eoues nesalops scattered 32 - 35°N diurnal and with orange stripe nesic to riparian
black with grassy to forested, Thannophis eoues virsatenuis scattered 24 - 29°N adaptive brown stripe aesic to riparian
dark brown with grassy to wooded, Thannophis sodmani scattered 16 - 20°N adaptive light brown stripe aesic to riparian
gray with black spots grassy to wooded, Thannophis aacrostesmus scattered 16 - 20°N adaptive and with orange stripe aesic to riparian
checkered greenish-yellow grassy to wooded, Thannophis aarcianus narcianus scattered 21 - 38°N adaptive and black with orange stripe aesic to riparian
checkered green and black grassy to forested, Thannophis aarcianus bovalli scattered 12 - 17°N adaptive with orange stripe nesic to riparian
checkered green and black grassy to forested, Thannophis aarcianus praeocularis scattered 16 - 20°N adaptive with orange stripe nesic to riparian TABLE 1—Continued. Daily Latitude Species/Subspecies Iriiophore Pattern Principal Dorsal Coloration Habitat Type Range Activity Pattern uniform grassy to wooded, Thaanophis aelanoeaster canescens scattered 19 - 21°N adaptive gray aeslc to riparian
light brown with dark brown spots grassy to forested, scattered 23 - 2S°N adaptive Thaanophis aendax and yellow stripe Basic to riparian
brown with grassy to wooded, Thaanophis ordinoides scattered 41 - 51°N orange stripe aeslc diurnal
black with grassy to wooded, Thaanophis eroxiaus eroxiaus scattered 31 - 43°N adaptive orange stripe aeslc to riparian
scattered to dark brown with CTftssy to traded, Thaanophis proxiaus alpinus 17°N adaptive lightly layered yellow stripe aesic to riparian
gray with grassy to wooded, Thaanophis nroxlaus diabolicus scattered 23 - 39°N adaptive orange stripe •esic to riparian
scattered to brown with grassy to wooded, Thaanophis proxisus orarius 24 - 31°N adaptive lightly layered yellow stripe •esic to riparian
scattered to blown with grassy to wooded, Thaanophis proxlaus nibrilIneatus 28 - 34°N adaptive lightly layered red stripe •esic to riparian
brown with grassy to wooded, Thaanophis proxisus Tutilorls scattered 9 - 23°N adaptive gray stripe •esic to riparian
aottled brown with grassy to wooded, Thaanophis radix radix scattered 3a - 46°N diurnal orange stripe aesic to riparian
brown with black spots grassy to wooded, Thaanophis radix havdenii scattered 35 - S3°N diurnal and yellow stripe aesic to riparian
olive with wooded to forested, Thamnophis rufipunctatus scattered 24 - 35°N diurnal dark brown spots riparian
reddish-brown with grassy to wooded, Thaanophis saurltuu saurilus scattered 30 - 43°N adaptive yellow stripe aesic to riparian
black with grassy to wooded, Thamnophis sauritus nitae scattered 28 - 30°N adaptive brdwn stripe aesic to riparian brown with grassy to wooded, Thaanophis sauritus sackenii scattered 2S - 32°N adaptive tan stripe aesic to riparian
dark brown with grassy to wooded, Thaanophis sauritus sententrionalis scattered 38 - 4S°N adaptive yellow stripe aesic to riparian
brown with grassy to forested, Thaanophis scalaris scalaris scattered 18 - 22°N adaptive yellow stripe aesic to riparian
dark brown with grassy to wooded, 25 - 53°N diurnal Thaanophis sirtalis sirtalis scattered yellow stripe aesic to riparian settled brown and black with grassy to wooded, Thannophis sirtalis annectens scattered 30 - 36°N diurnal orange stripe aesic to riparian
black with red spots and with grassy to wooded, Thaanophis sirtalis concinnus scattered 44 - 46°N diurnal yellow stripe aesic to riparian
aottled red and black with grassy to wooded, Thaanophis sirtalis dorsalis scattered 28 - 37°N diurnal yellow stripe riparian
gray with grassy to wooded, Thaanophis sirtalis fitchi scattered 38 - 60°N ' diurnal yellow stripe aesic to riparian
black with red spots and with grassy to wooded, Thamnophis sirtalis infernal is scattered 33 - 44°N diurnal yellow stripe aesic to riparian
brown with reddish bars and withi grassy to tooded, Thamnophis sirtalis parietalis scattered 34 - 60°N diurnal yellow stripe aesic to riparian
black with red spots and with grassy to wooded, Thamnophis sirtalis pickerinaii scattered 46 • 50°N diurnal yellow stripe aesic to riparian
dark brown with black spots grassy to wooded, Thamnophis sirtalis sealfasciatus scattered 41 - 43°N diurnal and with yellow stripe aesic to riparian
dark brown with grassy to wooded, Thamnophis sirtalis similis scattered 29 - 30°N diurnal yellow stripe aesic to riparian
black and red striped with grassy to wooded, Thamnophis sirtalis tetrataenia scattered 37°N diurnal yellow aedian stripe aesic to riparian
brown with grassy to forested, Thasmoohis suniehrasti scattered 13 - 20°N adaptive black spots aesic to riparian 16
B
Figure 2. A. Transmitted light photomicrograph of a transverse section of a single scale taken at a midbody dorso-lateral location from Agkistrodon contortrix phaeogaster (magnification X400) . B. Same section photographed with polarized light. 17
A
Figure 3. A. Transmitted light photomicrograph of a transverse section of a single scale taken at a midbody dorso-lateral location from Agkistrodon contortrix pictigaster (magnification X400). B. Same section photographed with polarized light. 18
A
Figure 4. A. Transmitted light photomicrograph of a transverse section of a single scale taken at a midbody dorso-lateral location from Agkistrodon caliginosus (magnification X400). B. Same section photographed with polarized light. 19
A
Figure 5. A. Transmitted light photomicrograph of a transverse section of a single scale taken at a midbody dorso-lateral location from Agkistrodon blomhoffii brevicaudus (magnification X400). B. Same section photographed with polarized light. 20
A
Figure 6. A. Transmitted light photomicrograph of a transverse section of a single scale taken at a midbody dorso-lateral location from Crotalus atrox (magnification X400). B. Same section photographed with polarized light. 21
A
Figure 7. A. Transmitted light photomicrograph of a transverse section of a single scale taken at a midbody dorso-lateral location from Crotalus durissus durissus (magnification X400). B. Same section photographed with polarized light. 22
B
Figure 8. A. Transmitted light photomicrograph of a transverse section of a single scale taken at a midbody dorso-lateral location from Crotalus aquilus (magnification X400). B. Same section photographed with polarized light. 23
Figure 9. A. Transmitted light photomicrograph of a transverse section of a single scale taken at a midbody dorso-lateral location from Crotalus cerastes cerastes (magnification X400). B. Same section photographed with polarized light. 24
Figure 10. Survey electron photomicrograph of the dermis of Agkistrodon contortrix mokasen, illustrating the isolated cells iridophore pattern (magnification X3000). 25
Figure 11. Survey electron photomicrograph of the dermis of Crotalus scutulatus scutulatus, illustrating the heavily layered iridophore pattern (magnification X3000). 26
xanthophore and erythrophore) density. There is a decrease in inter
cellular connective tissue but the total dermal volume supporting the
chromatophores remains stable.
Reflectance and Albedo
Figure 12 illustrates the reflectance of the skin of four selected
crotalid snakes, with N = 2 for each form illustrated, i.e., two different
live specimens were sampled for each species and subspecies, and the
average of the paired data points was plotted on the graph. A Chi square
analysis of the data from which the graph was generated indicates that a
species with layered iridophores has a higher dorsal integument reflec
tance than does a species with scattered iridophores (P <0.01). However,
heavily layered iridophores affect no greater reflectance than do moder
ately layered cells (P<0.01). As tested by Chi square, the graphed data
show the following (P < 0.01): a) in that portion of the curve generated
by 250 nm to 500 nm wavelength light, Crotalus molossus molossus >
Crotalus cerastes laterorepens = Crotalus cerastes cercobombus = Crotalus
atrox, b) at 525 nm wavelength, £. m. molossus > C. c_. laterorepens >
£. £. cercobombus = £. atrox, c) at 600 nm wavelength, £. m. molossus >
£. c_. laterorepens > C_. c_. cercobombus > £. atrox, and d) in that portion
of the curve between 650 nm and 750 nm wavelength light, £. m. molossus =
£. c_. laterorepens > £. £. cercobombus > £. atrox.
Incidental to obtaining the reflectance data, I found that indi
vidual specimens of a given species do not deviate substantially one from
the other. Inadequate numbers (N = 2 in all cases) were available for
statistical analysis. However, paired specimens were found to be 100
•• • Crofalus molossus molossus & & & Crofalus cerastes laterorepens 0 8® Crofalus cerastes cercobombus 1B B Crofalus atrox
••• ® •A •9 • * s. $ © A
A a^
4 0 ^ ..AA A ra - © ® i, B, OB @II ® ^
"" "
_ M a tt in J.. g a 1 j « i 250 300 350 400 450 500 550 600 650 700 750 Lighf Wave Length (nm) NJ Figure 12. Reflection o! light Irom the skin of selected crotalid snakes. 28
separated by a maximum of 3% reflectance at any wavelength. The separa
tion was commonly 1% or 2%, and in a few instances the reflectance per
centages of paired specimens were identical at a particular wavelength.
The albedo of each of the four snakes was determined by the
method already defined with the following results: Crotalus molossus
molossus = 36.6%, Crotalus cerastes laterorepens = 30.0%, Crotalus
cerastes cercobombus = 20.5%, and Crotalus atrox = 18.3%. Chi square
analysis of these data showed (P < 0.01): £. m. molossus > C. c.
laterorepens >£. £. cercobombus > £. atrox. Although the northern
black-tailed rattlesnake (£. m. molossus) has lightly layered iridophores
(comparable with £. durissus durissus, Figure 7 and Agkistrodon contortrix
pictigaster, Figure 3), the reflectance and the albedo of this form are
greater than that of the Colorado desert sidewinder (£. c. laterorepens)
and the Sonora sidewinder (£. £. cercobombus), both of which have heavily
layered iridophores (comparable with £. £. cerastes, Figure 9 and
Agkistrodon blomhoffii brevicaudus, Figure 5). All three forms exhibit greater reflectance and albedo than the western diamondback rattlesnake
(£. atrox) which has scattered iridophores (Figure 6).
Physical and Physiological Correlations
No statistically demonstrable correlations appear from the data obtained from microscopy combined with compiled data pertaining to physical coloration, habitat and habits (Table 1). However, an objective mental assessment of certain sub-groups of snakes leads to suggested correlation with habitat, and will be discussed.
The superimposition of iridophore pattern data onto dendrograms 29
of crotaline snakes examined (Figures 13 and 14) creates no contradictions
to previously established phylogenetic relationships. The Agkistrodon related species are supported in that the species bearing layered irido-
phores are descended from similar ancestors and never from ancestors bearing scattered iridophores. The relationships of the rattlesnakes, genera Crotalus and Sistrurus, are neither contradicted nor supported since all ancestral lines carry layered iridophores. HhH.hypnale -H.walli KEY A. Agkislrodon - -t-C.rhodostoma C. Calloselasma 4-A.sfrauchi -A.himalayanus D. Deinagkisfirodon H. Hypnale + Iridophores visible at X400 - Iridophores not visible at X400 () Number of subspecies
+A.caliginosus North +A.halys(3) America
-A.blomhoffii(5) -A.contortrix(5) -A. piscivorus(3) except +A. b. blomhoff ^except +A.c.pictigaster nd "HA.b.brevicaudus -A.bilineatus(3) I A.infermedius( pxcept +A.i.caucasic rA.saxafilis -D.acutus
ancient Asian stock
FIGURE 13. Dendrogram of the genera AakistrodonT Calloselasma, Deinaflkistrodnn nnrl Uyjuuie annotated with light microscopy data on iridophores. Figure adapted from Brattstrom(l964)and modified to reflect works of Gloyd (1969,1972,1977,1978). o KEY
C. Crotalus tCvir -C.m»Chellii(5) j^)orifsus(13) S. Sisfrurus +C.tortugensis |*C.poH^rensis, x Extinct species C.vergrandis Other symbols as in Fig.12 -C. ruber C.cafalinensis C.uni.color C.scutulatus(2) i"C.molossus(3)
-C.basihscus(2)Jtc horr,d(ls -C.adamanteus +C.triseriatus(4) +C.pricei(2) fCa i,us -C.eQyo(3) J-C.pU|illuJ y -S.miliarius(3) C.cerastes(3) J C.sfejnegeri C.intermedius(3) |*i*S.catenatus(3) tC wiljardi(5) rC.transverus, C.polystictus rC.lepjdus(4) +S.ravus(4) C.lannomi 'l
primitive immigrant stock FIGURE 14. Dendrogram of the genera CrfltffllMS and Sistrurus annotated with light microscopy data on iridophores; species not annotated were not sampled in the survey. Figure adapted from Brattstrom(l964)and modified to reflect works of Klauber(1972), Harris and Simmons(l978), Campbell(1978),Campbell and Armstrong(1979)and Collins and Knight(1980)- DISCUSSION
The occurrence of thickly layered iridophores in squamates has
been only cursorily reported in the literature. A heavy layer of irido phores in the dewlap of the green anole (Anolis carolinensis) was observed by Alexander and Fahrenbach (1969) without elaboration, illustration or description. Miscalencu and Ionescu (1973) described dermal iridophores in the European long-nosed viper (Yipera ammodytes) as a "thick layer", and one photograph suggests that this species may fall into my category three (moderately layered), but the photograph covers too little area for an acurate determination and the authors' discussion does not elaborate.
The discovery of heavy iridophore layering in the genus
Agkistrodon by Chiasson is significant. The subsequent observance of the iridophore band in eight out of twelve genera of snakes sampled indicates the morphology may be fairly common and simply heretofore unreported. I expect some other genera of snakes to show similar iridophore patterns.
The electron microscope examination of the dermis of snakes having markedly layered iridophores reveals the differences from species having scattered iridophores to be a few simple modifications. The total volume of dermis occupied by chromatophores within the species of a given genus is fairly regular, showing no change from an isolated-cell iridophore pattern to a heavily-layered iridophore pattern. The stable volume of chromatophore space becomes more densely populated with cells in the species exhibiting layered accumulations of iridophores.
32 33
The iridophores may increase in population density to reach a 20:1
ratio with other chromatophore types, these other cell types remaining in numbers comparable to species with isolated-cell iridophore patterns. The net effect is to increase the dorsal integument albedo by 100% or more,
depending on the presence or absence of many xanthophores or erythrophores
and the volume of melanin in the epidermis. As melanin principally
absorbs light, iridophores reflect light, and xanthophores (and erythro
phores) transmit light (Bagnara and Hadley 1973, Nielsen and Dyck 1978), the presence or absence of colored pigments above the iridophores will alter the net reflectance (Nielsen and Dyck 1978); this effect can be ob served in the reflectance graph (Figure 12) of four selected species of rattlesnakes.
The graph and associated albedo calculations show the albedo of the four forms to be as follows: Crotalus molossus molossus > Crotalus cerastes laterorepens > Crotalus cerastes cercobombus > Crotalus atrox.
However, the iridophores patterns of the four forms (see Table 1) is
£. £. laterorepens = £. c. cercobombus > £. m. molossus > £. atrox. These data are explained by the fact that m. molossus has a relatively heavy layer of xanthophores and relatively little epidermal melanin, thus in creasing the reflectance. C_. c_. laterorepens and C_. £. cercobombus have relatively few xanthophores accompanied by relatively more epidermal melanin, causing a decrease in the reflectance. Also, £. c_. laterorepens has less epidermal melanin than C_. c_. cercobombus in the specimens sampled; this is manifested in their respective reflectance curves.
Finally, £. atrox has few xanthophores and only scattered iridophores, which allows the dermal melanophores to absorb a large portion of the 34
incident light.
Possible habitat correlation to iridophore pattern has proven
difficult to examine statistically because of the many variations in total
chromatophore complement from species to species. Although it is not possible to state that any statistical correlation exists, it is note worthy that a visual evaluation of iridophore patterns shows all species and subspecies which have the extreme in heavily layered iridophores (as illustrated by Figure 9, Crotalus cerastes cerastes) are from semi-arid habitats having highly reflective ground surfaces derived from quartz particles. The desert-dwelling sidewinders (Crotalus cerastes) have an adaptive daily activity pattern, i.e., they may be diurnal or nocturnal, depending on season and weather (Conant, personal communication); the desert massasauga (Sistruru's catenatus edwardsi) is similar. These snakes would be exposed to a high incident radiation in diurnal activity; this condition suggests iridophores may confer some benefit. Allied to these observations, it is significant that the prairie rattlesnake
(Crotalus viridis viridis) of the United States becomes a sidewinder form in the Mexican desert portion of its range (Van Devender, personal communication), and midget faded rattlesnake (Crotalus viridis concolor) thrives in a barren, exposed habitat. Both subspecies have principally diurnal habits and they are the only Crotalus viridis subspecies which exhibit heavily layered iridophores. It may also be noted that most of the rock-dwelling species, which are protected by their habitat, exhibit scattered-cell iridophore patterns; examples of this are the several
Crotalus mitchelli subspecies and also Crotalus viridis abyssus. One may observe a number of species and subspecies which conform to this 35
subjective correlation of relative habitat conditions with iridophore patterns, but there-are also a number of exceptions. More extensive sampling is needed in order to make definitive statements.
My original hypothesis of possible phylogenetic correlations to iridophore patterns is supported. The dendrogram of Agkistrodon,
Calloselasma, Deinagkistrodon and Hypnale species (Figure 13) illustrates that species bearing layered iridophores are descended only from ancestral lines in which layered iridophores are present. That some species show a loss of layered iridophores and none show a development of layered irido phores signifys a genetic determination of iridophore patterns. Since all the specimens sampled of a given species or subspecies manifested the same phenotype, the usual procedure of crossbreeding phenotypes to ascertain genotypes is not practical. A worthwhile project would be an extensive, multi-year, multi-environment sampling of selected species groups to establish that no deviation from a set iridophore pattern does occur. If this is so, then iridophore patterns would be useful in certain phylo genetic analyses. When dealing with evolutionary hypotheses wherein all possible lines of descent carry layered iridophores, the tool is not use ful. This is illustrated by the rattlesnake dendrogram (Figure 14) where in layered iridophores are noted to be common to all descendent groups.
However, when attempting to locate the line from which all the rattle snakes were derived, the tool is then valuable because that searched for line must include the gene(s) for layered iridophores.
Though not originally an objective of this study, some additional comments may be made about the relationships shown by Figure 13 which illustrates Agkistrodon and immediately related genera. Brattstrom's 36
(1964) original hypothesis of a two-time migration of ancient ancestral
stock from Asia to North America is questionable. If A. acutus is truly
of another genus (Deinagkistrodon, Gloyd 1978), and if A. bilineatus and
A. piscivorous are to remain in their assigned genus, then the latter two
species are more closely related to the American copperheads (A.
contortrix) than to the Asian hundred-pace viper (D_. acutus). It is for
this reason that I have inserted a question mark in the second migration
line on the dendrogram. The alternative line of descendency is further supported by serological data (Minton, personal communication). Another questionable point is the closeness of the genera Calloselasma and Hypnale to Agkistrodon. It is more reasonable to suggest that they are derived from more ancient stock than as illustrated by Figure 13. This also is supported by Minton's unpublished serological data. REFERENCES
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