t h e Evolution o f t h e Venom Apparatus i n Snakes From Colubrids to Viperids & Elapids - Unknown - 1982

8/14/2019 t h e Evolution o f t h e Venom Apparatus i n Snakes From Colubrids to Viperids & Elapids - Unknown - 1982

http://slidepdf.com/reader/full/t-h-e-evolution-o-f-t-h-e-venom-apparatus-i-n-snakes-from-colubrids-to-viperids 1/14

Mem . Inst Butantan

46 : 106-118 1982

TH E EVOLUTION OF TH E VENOM APPARATUS INSNAKES FROM COLUBRIDS TO VIPER IDS ELAPIDS

Kenneth V. KARDONG *

ABST RACT: The venom app aratu s of poisonous snakes consistsof a fa ng and associated venom gland (or glands). Venomoussnakes evolved from nonvenomous ancestors. The course of thisevolution, the adaptive advantages of the changes a t each stage,and th e implications of the findings to snake phylogeny, phar-macology, and clinical stra tegies of tre atm ent of envenomationsar e the subject of this paper.

In particular, it is argued in this paper that: (1) both viperidand elapid snakes evolved from opisthodont ancestors; (2) theDuvernoy's gland in most colubrid snakes should not be seen asa gland "on its way" to becoming a venom gland, but should beexamined for the immediate biological role it plays in the life ofthose snakes possessing such a gland; (3 ) it would be useful todistinguish between a proper ty of an oral secretion e .g . toxin)and its biological role e .g . venom) ; (4 ) strategies of treatmentof envenomation would profit if it were more fully appreciatedwhy venom is composed of more than jus t a sui te of toxins.

INTRODUCTION

Th e venom app ara tus of poisonous snakes consists primarily of tw ocomponents: a modified tooth, the fang by which venom is delivered intoprey, and the venom gland (or glands) where toxin is produced andstored. Venomous snakes use th e venom appa rat us to rapidly kill pre yand secondarily in defense from their own enemies.

Th e structure of fan gs and venom glands ar e th e subject of manyrevealing descriptive papers e.g. Kochva and Gans, 1966; Rosenberg,1967; Nickerson, 1969; Gabe and Saint Girons, 1971; Halstead et al.,1978). However, clarifying the evolution of the venom apparatus has

proved to be a more contentious and elusive task (Smith and Bellairs,1947; Kroll, 1976). In part, t his ari ses from phylogenies of snakesconstructed upon only a general or anecdotal knowledge of the functionalmorphology of t he jaw apparatu s. Thus, the fir st purpose of t his paperis to review the functional role of both the apparatus and the evolutio -nar y antecedants of t he venom apparatus. This will lead to the formu-lation of focused hypotheses that yield testable predictions.

Department of Zoology. Washington State University U.S.A



KARDONG,

elapids.K. V. The evolution of the venom apparatus in snakes from colubridsMen Inst Butantan. 46:105-118 1982

viperids t

The conclusions reached herein about the evolution of the snakevenom apparatus shed a different light upon ophidian taxonomy and

phylogeny, venom pharmacology, and even upon clinical treatment ofsnakebite. Thus, th e second purpose of this paper is to discuss th eimplications of these conclusions for these related areas.

RESULTS

A) Evolut ion o f the Fang

1. Mo rp hologi ca l Series

Venomous snakes evolved from nonvenomous ancestors. Three

families of snakes are immediately involved: Colubridae, Viperidae, andElapidae (including sea snakes). Viperids and elapids are poisonoussnakes with sophisticated venom apparatuses used to quickly kill prey.However, most colubrid snakes are basically nonvenomous. True, somesuch as Dispholidus seem to parallel viperids and elapids in that theypossess a highly toxic venom apparatus and use it to rapidly kill prey.But, the vast majority of colubrids are truely nonvenomous.

The origin of viperid and elapid snakes from colubrids has been a

longstanding concern among those interested in advanced snakes (Bou-

lenger, 1893, 1896, 1917; West, 1895; Alcock and Rogers, 1902; Phisalix,1912, 1922). Several relationships have been proposed. One suggestsa single origin of venomous snakes from colubrids (Cope, 1900; Mosauer,1935) ; another that elapids arose from opisthoglyphous colubrids, and

viperids from proteroglyphous colubrids (Anthony, 1955). The rela-

tionship I use here is that both elapids and viperids evolved fromopisthoglyphous colubrid ancestors, but independently (Kardong, 1980).This evolution of venomous snakes from opisthoglyphs probably occurredseveral times (Kochva et al., 1967; Bprrgeois, 1968; McDowell, 1968;Savitzky, 1980 . However, despite a lipfely polyphyletic or igin of veno-mous snakes, these fall along but two pathways, one leading to viperids

and viper-like snakes, and the other to elapids and elapid-like snakes.It is beyond the scope of thi s paper t o identify how many times eachof these paths was traveled by evolving snakes. Instead, th e purposeis to analyze the general adaptive advantage of changes on each evolu-tionary highway.

If we focus our attention on the maxillary bone and the teeth i t

hears, then one can construct a simple morphological series ( s e n s u Maslin,1952) through which the maxilla and its teeth transform into the short-ened maxilla and f an g of elapids on the one hand, and viperids onthe other (Fig. 1) . Notice that within colubrids, there exists a range ofmorphological conditions. The first state, and presumbly phylogeneticallythe most primitive, is exhibited here by Pituophis wherein the shaft ofthe maxilla is long, its teeth numerous, and the dentition basically homo-dont s en s u EZdmund, 1969). In a more derived condition, as exhibitedby Di spholid us, the maxilla is shortened, the teeth reduced in number,



KARDONG, K. V. The evolution of the venom appar atu s i n snakes fro m eolubrids to viperidr

elapids. Mem. Znst. Rutantan, 46:105-118 1982

and the dentition heterodont. Heterodonty is achieved by the differen-

tiation of the posterior maxillary teeth that lengthen through this series,change shape, and eventually come to bear a groove along their sides.

EL PlDAE

iOLUBRIDAE

Fig. 1 Transformation series of the maxilla and teeth it bears within the family Colubridae and to

In elapids, this tooth has migrated forward to a more rostra1 position on the maxilla.In viperids, this tooth resddes a t the posterior end of th e maxilla, but kinetically rotatesforward during the str i Actual skulls depicted among the colubrids ar e those ofPituophis (left) and Dispkolidus (r ight) . A Naja and Vipera skull represent Elapidae andViperidae, respectively.

Evolution of the maxilla and its tee th within colubrids thus proceedsfrom an aglyphous to an opisthoglyphous condition. Between these twoextremes lie most colubrids showing graded, intermediate states. Forinstance, next after the initial condition would follow snakes that posses-sed maxillae with slightly elongated maxillary teeth e.g. Thamnophis) .Next would lie snakes possessing long, rear maxillary teeth, but withsecretion groves e.g. Crotaphopeltis). A secretion channel too appears



KARDONG, K. V. The evolution of the venom apparatus in snakes from colubrids to viperidselapids. Mem. Inst Butantan, 46:106-118 1982

in gradual stages. It would appear first, in this transformation series,as a corner between two adjacent teeth (Taub, 1967) and later as agroove within a tooth (Sarker, 1923).

This trend within colubrids to a shortened maxilla, reduced numberof teeth, and elongated poster ior tooth continues into the two venomousfamilies. But, the continuation of these trends is established in twodiffe rent ways. In viperids, the elongate posterior tooth (now a fang)lies a t th e re ar of the shortened maxillary bone. I n elapids, the elongatedposterior tooth (now also a fa ng ) lies not at th e rea r of th e shortenedmaxillary bone, but forward on the remaining shaft. Occasionally, smallteeth remain at; the posterior end of t he elapid maxilla marking the pointat which the fang once resided in elapid ancestors.

2 . Adaptive Advantages

a ) Accretion HypothesisA common view holds that these evolutionary changes in the maxilla

and its teeth are driven by the increasing and additive advantages longteeth serve in venom injection. Thus, by t i e accretion of progressive toxicbenefits, a venom system develops. This hypothesis predicts that theinitial and the subsequent role played by these teeth was in prey capture.

To tes t this prediction, several living species (Thamnophis, Crota-phopeltis) f alling within the middle stages of the transformation seriesamong colubrids were examined to see just how they used their maxillaeand posterior maxillary teeth. These species possess long posterior maxil-lary teeth. The results (Kardong, 1979, 1980; Wr ight, et al. 1979)showed that, i11 fact, they did not use these tee th extensively during preycapture. Instead, they used these teeth to manipulate prey once already

caught (see also Minton, 1944; Platt, 1969; Kroll, 1976). Thus, theseteeth, even though slightly elongated, did not serve to inject a venomduring prey capture, but instead aided swallowing by acting like smallhooks to give better purchase an the slippery or uncertain surface ofthe prey. Further, comparison of the posterior maxillary teeth and ofa venom fang revealed that the two are quite unalike (Schaefer, 1976;Kardong, 1979; Wright et al., 1979).

Thus, no support was found for the predictions of the accretionhypothesis, at least as applied to snakes within the middle of the trans-formation series.

b ) Deglutition Hypothesis

Altg2a t ive ly , I propose (Kardong, 1979; 1980) that these teeth

borne by,,maxillary bone initially functioned a s hooks or g aff s to improvepurchase during swallowing. This role favored, 1 ) elongation of theteeth, and (2 ) shortening of t he maxillary bone, two changes, in fact,present in the jaws of many colubrid snakes. Once long teeth along themaxillary bone had ari sen to serve the requirements of swallowing, thenthey would be preadapted to subsequent evolution into a new function,that of venom injection. But, the initial adaptive a va n ta ge of longmaxillary teeth was not related to venom injection, but instead toswallowing.



KARDONG. K. V. The evolution of the venom appa ratu s in snakes fr om colubrids to viperids

elapids. Mem Inst Butantan. 46:105 118. 1962.

B) Evolution of the Venom Gland

1. Morphological Series

The evolution of the venom gland, l ike th e previous evolution ofth e fang, begins within colubrid snakes. With in colubrids, the Duvernoy'sgland is the evolutionary predecessor of the venom gland (Gans andElliott, 1968; Kochva, 1978). A morphological series constructed nowfor th e Duvernoy's gland shows its t ransfo rmation into the venom glandof viperid and of elapid snakes (Fig. 2) .

ELAPIDAE V l PERIDAE

GLAND

Fig. 2 - Transformation series of Ddvernoy s gland. This gland appe ars fi rs t within the middleof the colubrid series. It arises near the posterior end of the supralabial gland SLG ) .Through the morphocline, the Duvernoy's gland transforms independently into the venomgland (VG) of elapid and viperid snakes.

2 . Adaptive Advantages

a ) Accretion Hypothesis

Again, the conentional view is that the Duvernoy's gland was

always slightly venomous and that the increasing, additive advantagesof venom injection drove the changes leading eventually to appearanceof a fully venomous gland. But, again there is reason to doubt thishypothesis. First, a s just mentioned, eventhough the teeth of colubrids



KARDONG, K. V. The evolution of the venom apparatus in snakes from colubrids to viperi s &

elapids. Mem. Znst. Butantan, 46:105-118 1982.

ar e long, they ar e otherwise structurally quite unlike fangs. Second,

most colubrid snakes do not have large storage areas to hold venom(Taub, 1967) to inject and rapidly kill prey.

Further, those who subscribe to this accretion hypothesis face aself -imposed paradox, what may be termed the "paradox of imperfec-tion". By the accretion hypothesis, possessors of a Duvernoy's gland are"on their way" to becoming highly venomous, but, as yet, possess onlya mild venomous capacity. But, in fact, most living colubrids are soendowed with long, posterior maxillary teeth (Marx and Rabb, 1972)and a Duvernoy's gland (Taub, 1967). In most part s of th e world, suchcolubrids live sympatrically with and outnumber in terms of species,venomous snakes such as viperids and elapids. The paradox lies in thefact that such colubrids with a presumed mildly venomous secretion,but "imperfect" venom apparatus, could be so successful with these two

families that possess a highly venomous and efficient venom apparatus.It does seem contradictory that colubrid species could compete and thriveusing an "imperfect" venom injection system as successful contempora-ries with elapids and viperids.

Perhaps, I have overstated or misstated the paradox. On the otherhand, the paredox may arise from a flawed hypothesis, the accretionhypothesis. Tyis, in fact, is my view. Most colubrids simply do not seemto use their oral secretions as venoms. Eventhough the oral secretionsof many colubrids are proving to be more toxic than previously suspectedMcAlister, 1963; Heatwole and Banuchi, 1966; Vest, 1981), still these

same species do not, in fact, use thei r oral secretions to rapidly kill p reyas do truely venomous snakes possessing fangs.

2 . De gl ut it io n HypothesisDuvernoy's gland secretion (in most colubrids) serves not as a

venom. This is to say, it does not serve to help rapidly kill prey dur ingprey capture. Instead, it must serve some other primary biological roleor roles for these species. Being associated with the swallowing behaviorof snakes, the secretion of Duvernoy's gland may reasonably be expectedto play a role in swallowing and/or digestion. However, without fur therbroad study of both the pharmacology of Duvernoy's gland secretionstogether with studies of the feeding behavior, it is premature to proposeany careful alternative hypothesis.

CONCLUSIONS

Early in the evolu,tion of the venom apparatus among snakes, theposterior maxillary teeth were long, but not yet fangs. Instead theyserved as spikes to help the snake grip slippery, bulky, or difficult preyduring swallowing. So too, the Duvernoy's gland was not yet a venomgland, but likely served some other biological role.

Certainly once these teeth were long and the Duvernoy's gland wellestablished, then this system was preadapted for the quite different role



KARDONG, K. V. The evolution of the venom apparatus in snakes from colubrids to viperi s

elapids. M e n Inat Butantan, 46:105-118 1982.

of quickly subduing prey. Lat er in it s evolution, the tooth/gland systemthen evolved under the increasing advantages derived from the ease and

efficiency of rapidly killing prey. But, prehension and envenomationwere not the initial roles that drove the early evolution of the glandularand dental elements in the jaws of colubrid snakes toward long, posteriorteeth on a shortened maxilla.

IMPLICATIONS

A) Snake Evolution

1 Vipe r i d i s and Elap ids - two venom modes

Both viperid and elapid snakes evolved independently from opistho-glyph ancestors. At least, this is the view I take based upon the argumentspresented herein. The alternat ive view th at elapids (or viperids) arosefrom proteroglyph ances tors is contradicted by the position of the venomgland (McDowell, 1968), embryonic development (Martin, 1899a,b.c;

Kochva 1963; 1965), and rear maxillary tooth structure, position, andfunction (Kardong, 1980 :273-274).

Upper jaw teeth in colubrids serve in two primary capacities-preh-ension and swallowing. Rut, these two activities are not always sharedequally among the teeth. Anterior teeth of the mouth tend more oftento be involved in prehension because they are f ir st to come into the vicinityof the prey and because they bear responsibility for snagging elusiveprey. Correspondingly, anterior teeth are often long and recurved reflect-ing their special role in prey capture (Frazzetta, 1966). Posterior teeth,on the other hand, tend to be involved in preingestion/swallowing mani-pulations. Because of the kinetic motion of the maxilla, rear teeth itbears lie a t an especially favorable mechanical position to aid in swallow-ing (Kardong, 1979). Consequently; posterior maxillary teeth ar e oftenlong and blade-shaped (Wright et al 1979).

The fang borne by the maxilla in elapids and viperids is, like anteriorteeth of colubrids, deployed principally during prey capture. I t is thusfashioned similarly. For instance, the fan g is conical and often recurved

(Klauber, 1956) ; it is located, during the strike, in the anterior partof the mouth. n this latter feature, however, this forward position inthe mouth is accomplished in two diff eren t ways. In viperids, the fa ngrides upon a highly kinetic maxilla th at erects during the strike to bringthe fang well forward in the mouth (van Riper, 1953; Kardong, 1975).In elapids, the fang rides on a less kinetic maxilla, but has undergonedur ing i ts evolution a forward migration so tha t it si ts in a more anteriorposition along th e shaf t of the maxilla (Fig. 1).Thus, fangs in the twogroups enjoy the advantages of an anterior position in the mouth, butthis is achieved differently-phylogenetic migration along the maxilla inelapids, kinematic rotation in viperids. Although elapids and viperidsare venomous snakes, they seem to be separately derived styles of avenomous mode of life. They diff er in the structural fea tures of the



KARDONG, K. V. The evolntion of the venom apparatus in snakes from colubrids to viperi selapids. Mem. Inst Butantan. 463105 118. 1982.

maxilla and fang just mentioned, relative toxicity of t lieir venoms (e.g.Minbn and Minton, 1969), and perhaps even in behavioral styles in t heir

stra tegies of prey capture (Naulleau, 1965; Kardong, 1982).

2) Duve rnoy's gland

The Duveriioy's gland in most colubrid snakes is unlikely a gland"on its way" to being a venom gland, but s h ~ u l dbe examined for theimmediate biological role it plays in the life o j ~those snakes possessingsuch a gland.

B) Pharmacology

1 ) Tox i n and Ve nom

A distinction should be made between a secretion that is a"toxin"

and one that is a "venom", at least as applied to snake secretions in abiological context. These two ter ms have grown up in the medical lite-rature with closely related meanings (e.g. Russell, 1980). I don't intendto propose redefinition in a medical or clinical context. However, thetransference of these terms into a biological context has led to confusion.As a result, some animals live with an undeserved reputation for dangerand even some medical strategies of tre atm ent of suspected envenoma-tions suffer from the confusion.

In a biological context, by "toxic" I mean the letha pro perty of achemical expressed as an LD.,, or LD,,,, for example; it is usuallyidentified and characterized under defined laboratory conditions. However,by the term "venomous" I mean the fu nc ti on of the secretion, specifically

the biological role (Bock, 1980) of the substance in the life of the animalproducing it. Observation of t he free ranging animal in its nat uralhabitat i s usually or ideally the basis for concluding (o r not) th at asecretion is used as a venom. The two ter ms rest on different conceptsso more is at issue than mere semantics.

If Duvernoy's gland secretion is shown to be toxic, some suggestfrom thi s alone that t he snake is likely venomous. However, ther e ar etwo reasons for resisting such a hasty conclusion.

2) Inci de nt al Byproduct

Firs t, to prove a substance toxic in character is insufficient to provei t venomous in practice. Toxicity can occasionally be an incidentalbyproduct. Fo r example, some components of human saliva a re toxic andpossess an@ LD50 (Bonilla t aJ 1971). Yet, no food humans consumerequire envenomation to make it safe to eat, nor are there enemiesthwarted by thre at of saliva injection. Toxicity is incidental and thoseseeking the biological role of saliva look, quite rightly, beyond thisproperty to i ts digestive roles to understand its chemical character. How-

ever, analysis of oral secretions from "nonvenomous" snakes has notalways been so sensible. Too often, only the property of toxicity ofthese secretions seems to have been seriously considered. Certainly, this



KARDONG, K. V. The evolution of the venom apparatus in snakes from colubrida to viperidselapids Mem. Znst Butantan, 46 : 105-118 1982.

is understandable. Lethal dose, if any, can be relatively easily demons-trated, and hence toxicity discovered; also, the toxicity alone makes the

substance medically important regardless of its actual biological function.Yet, in many colubrid secretions, toxicity might be, as with human saliva,incidental, a property with no or only secondary biological significance.It would be misleading to call humans "venomous" simply because theypossessed a "toxic" saliva. Similarly with snakes. In a biological context,distinguishing conceptually between a toxin and a venom should helpavoid such confusion.

3) Other Functions

There is a second reason for resisting the temptation to concludethat a toxic secretion is also automatically a venom. I n most colubrids,Duvernoy's gland secretion functions in capacities other th an a s a venom.Many colubrids possess well developed Duvernoy's glands, yet do not useits secretion to rapidly kill prey. To take an example, the wanderinggarter snake (Thamnophis elegans) possesses a Duvernny s gland secret-ion of alarming toxicity approaching that of some viperid snakes (Vest,1981; 1982), yet lacks the teeth to inject much secretion (Wright et al.,1979), and does not feed by bringing rapid death to the prey (Peterson,1978). It possesses the toxicity, but lacks the equipment and behaviorto use the secretion as a venom. The secretion from Duvernoy's glandor, for that matter, any secretion released from a specialized organ orgroup of cells may serve several functions. I t may funct ion as a venom,it may paralyze prey, it may tranquilize, it may aid digestion, and so on.In Thamnophis and similar colubrids, what then could be this secretion'sfunction ?

4) Alternative or Addition~~lFunctions

To date pharmacological and biological analysis of Duvernoy's glandsecretion has been preoccupied with toxicity (e.g. Philpot et al. 1977),

so one is lef t t o speculation about alternative functions. However, severalseem likely.

a) Lubrication

Besides Duvernoy's and venom glands, snakes possess additionalstr ips of glandular tissue along upper and lower lips (Taub, 1966) t ha trelease their products over the prey to lubricate its passage into theesophagus. Duvernoy's gland secretion, released a t the base of rea rmaxillary teeth, trickles down the sides of these teeth to likely finds it sway to the surface of the prey. Thus it could be an additional source oflubricant to facilitate swallowing.

b) Digestion

In viperid and elapid snakes, venom certainly contributes to rapidprey death, but has also been suspected of promtting digestion (Reichert,1936; Zeller, 1948) . Experimental work- njebting venom into mice andthen comparing rates of their digestion to controls - indicates thatrattlesnake venom actually speeds digestion (Thomas and Pough, 1979) .



KARDONG. K. V. The evolution of the venom n p ~ ~ r t u sn snakes from eolubrids to viperidselapids Mem. Znst Butantan, 46 : 105-118 0 .

Such venom attributes may be of adaptive value for snakes feeding onlarge numbers of prey in short periods of time or to enhance digestionin snakes from cold or temperate climates. Similar tests have not beendone for the secretion from Duvernoy's gland, but the possibility itserves a similar function seems worth investigating.

Snakes swallow their food without tearing or chewing. Digestiveenzymes released from the wall of the gut may not always complete theinward spread of digestion before tissues within the center of the bolusputrefy. Venom injected deep (Thomas and Pough, 1979) or Duvernoy'sgland secretion inoculated subcutaneously within the prey before swallow-ing may retard this putrefaction.

d) Detoxify Prey Sscretions

Many snakes, especially colubrids, feed on amphibians possessingskin glands which contain, depending upon the amphibian species, i rri tat -ing to actually poisonous secretions (Habermeihl, 1971; Lutz, 1971;Brodie and Tumbarello, 1978). Duvernoy's gland secretion in thosecolubrids regularly feeding on amphibians may help neutralize these skinsecretions released by the amphibian prey.

Further, these oral secretions could contribute to improved oralhygiene or prevent sticky material elaborated by prey from fouling the jaws dur in g swallowing (Gans, 1978; Jansen, 1982). My intent is notto settle the questions of what functions snake oral secretions serve.Instead, I wish to emphasize th at snakes, faced with a variety of problemswhile catching and swallowing prey, might possess various componentsin the Duvernoy's gland or venom gland secretions that serve a variety

of biological roles besides or in addition to envenomation.Even though introduced into the prey in small quantities compared

to a true venom, some propose that the Duvernoy's gland secretion mayslow or tranquilize the prey, thus making prey capture less risky andswallowing easier. Perhaps it does. But, tranquilizing prey differs fromenvenomation. Tooth form (Kardong, 1979; Wright et ag., 1979), maxil-lary bone structure (e. g. Bogert, 1943; Brattstrom, 1964), and behavior(e.g. van Riper, 1953; Klauber, 1956; Dullemeijer, 1961; Greene andBurghardt, 1978) differ from species that use venom predominantly tocapture and dispatch rather than just quiet prey. Consequently, tran-

quilization seems distinct from true envenomation as a prey handlingtechnique.

C ) Clinical Significance

Venom& ar e complex. Laboratory analysis proceeds by fractiona-tion into molecular components then to separate analysis of each fraction.Some components exhibit toxicity while other components seem to bewithout toxic effect (e.g. van Mierop, 1976; Russell, 1980) . These nontoxicfractions are usually classified as potentiators, activators, or amplifiersgg.spreading facto rs) of the toxic components. Generally thi s conclusion

sems on mark. However, some of these components of venom may lackto icity, because they are present for biological reasons other than to



KARDONG, K. V. The evolution of the venom apparatus in snakes from colubrids to viperi selapids. Mem. Inst Butantan, 46:105-118 1982

promote rapid prey death (e.g. Thomas & Pough, 1979). In fact, evendemonstrating toxicity in a particular component does not or ought not

to end the search fo r it s possible function. Other attributes , besidestoxicity, should be considered if one is to eventually understand thebiochemical action and interaction of all venom components.

One fruit ful place to begin such a n analysis may be with the secretionfrom Duvernoy's gland. The venom gland of viperids and elapid snakesevolved from the Ijuvernoy's gland; these venomous snakes feed uponsimilar foods and thus face generally similar problems with prey asmany "nonvenomous" colubrids. Certainly the venom of viperids andelapids functions primarily to rapidly kill prey, but components servingsecondary functions are most likely present as well. Venom is a suite ofchemicals, all of which go into a victim - toxins and nontoxins alike.Consequently, it seems advisable fo r stra tegies of tre atment of enveno-mations to be founded upon a knowledge of all components and their

biological roles, not jus t upon the action of th e toxins. Perhaps, somewhatironically, one place to focus such an analysis of snake venoms, is on"nonvenomous" colubrid snakes.

ACKNOWLEDGMENTS

My thanks go in particular to several institutions and persons whoover several years have helped me secure needed comparative specimens,namely the American Museum of Natura l History (C. W. Bleyers, R. G.Zweifel), California Academy of Sciences (A. E. Leviton), Field Museumof Natura l History (H. Marx, R. In ge r) , Museum of Comparative Zoology(E. E. Williams) National Museums of Rhodesia (D. G. Broadley),

Smithsonian Institution (R. I. Crombie, F. I. McCullough, G. R. Zug),University of Flo rida (W. Auffenber g), and University of Kansas Mu-seum of Natural History (W. E. Duellman). I appreciate the help of J.

Visser, Wildlife Documentaries (South Afric a) fo r securing livingspecimens. My special thanks and sincere appreciation go to Prof. A. R.Hoge and other organizers of the symposium on "Serpentes em Gerale Arthrop6des Pe(;onhentos for their invitation, help, and support.

BIBLIOGRAPHIC REFERENCES

ALCOCK, A. ROGERS, L. On the toxic propert ies of the saliva of certain"non-poisonous" colubrines. Proc . Ro y. Soc . (Lond.) , 70 :446-454, 1902.

ANTHONY, J. Es sai su r 1 Bvolution anatomique de I appareil venimeus des Ophidiens.

AnnSci

Natur . Zoo l. , 17:7-53, 1955.BOCK, W.J. The definition and recognition of biological adaptation. Amer . Zool. ,20 :217-227, 1980.

ROGERT, C.M. Denti t ionaf phenomena in cobras and other elapids, with noteson the adaptive modifications of their fangs. Bull . Amer. Mus Nu t . Hi s t .

81 285-360, 1943.

BON ILL A, C.A.; FI ER O, M.K. SEIFERT', W. Comparative biochemistry andpharmacology of salivary gland secretions. I. Electrophoretic analysis of theproteins in the secretions from hu man parotid and rept ilian (Duvernoy's) glands.J. Chromatogr., 56:368-372, 1971.







KARDONG, K. V. The evolution of the venom apparatus in snakes from colu rids to viperidselapids. Mem Inst Butantan. 46:105-118 1942.

RIPER, W., VAN. How a rattlesnake strikes. Sci. Amer., 189:100-102 1953.

ROSENBERG , H.I. Histology, histochemistry, and emptyi ng mechanism of thevenom glands of some elapid snakes. J. Morph., 123:133-156 196?.

RUSSELL, F. Snake venom poisoning. Lippincott 1980, p. 562.

QARKER S.C. A comparative study of the buccal glands and teeth of the Opis-thoglyph a, an d a discussion of the evolution of t he order fro m the A.glypha. Proc. 2001. Soc. Lond. (1) :295-322 1923.

SAVITZKY, A.H. The role of venom delivery s t r a t y i e s in snake evolution. Ev o-

lution, 34:1194-1204 1980.

SCHA EFER, N. The mechanism of venom tra nsf er from the venom duct to thefang in snakes. Herp etolog ica, 32 :71-76 1976.

SMITH, M. BELLAIRS, A. The head glands of snakes with remarks on theevolution of the parotid gland and teeth of Opisthoglypha. Linn. Soc. J. Zool .,41 :351-368 1947.

TAUB , A.M. Ophidian cephalic glands. J. Morph. 118:529-542 1966.

Comparative histological studies on Duvernoy's gland of colubrid snakes.

Bu ll . Ame r. Mus. N u t . H i s t . 138:l-50 1967.THOMAS, R.B. POUGH, F.H. The effec t of ratt lesn ake venom on digestion of

prey. Toxicon 17 :221-228 1979.

VEST, D.K. Envenomation following the bite of a wandering garter snake (Tham-

nophis elegans vagrans) Clin . Tox., 18 :573-579 1981.

The toxic Duvernoy's secretion of the wandergin garter snake (Tham-nophis elegans vagrans). Toxicon 1982 (i n pres s).

WES T, G.S. On the buccal glands and teeth of certai n poisonous snakes. Pr oc .2001. SO C.Lond. 812-826, 1895.

WRIG HT, D.L.; KARDONG, K.V. BENTLEY, D.L. The functional anatomy ofthe teeth of t he western terrestria l g art er snake, Thamnophis elegans. Herpe to-logica 35:223-228 1979.

ZELLER, E.A. Enzyms of snake venoms and their biological significance. In F. F.

Nord (ed.), "Advances in enzymology" , New York, Interscience Publ., 8:459-4951948.

Documents

t h e Evolution o f t h e Venom Apparatus i n Snakes From Colubrids to Viperids & Elapids - Unknown - 1982