Behaviors involved in courtship and male-male combat have been recorded in a taxonomically broad sample (76 species in five families) of snakes in the clade Boidae + Colubroidea, but before now no one has attempted to find phylogenetic patterns in such behaviors. Here, we present a study of phylogenetic patterns in such behaviors in snakes.
From the literature on courtship and male-male combat in snakes we chose 33 behaviors to analyze. We plotted the 33 behaviors onto a phylogenetic tree to determine whether phylogenetic patterns were discernible. We found that phylogenetic patterns are discernible for some behaviors but not for others. For behaviors with discernible phylogenetic patterns, we used the fossil record to determine minimum ages for the addition of each behavior to the courtship and combat behavioral repertoire of each snake clade.
The phylogenetic patterns of behavior reveal that male-male combat in the Late Cretaceous common ancestors of Boidae and Colubridae involved combatants raising the head and neck and attempting to topple each other. Poking with spurs was added in Boidae. In Lampropeltini the toppling behavior was replaced by coiling without neck-raising, and body-bridging was added. Phylogenetic patterns reveal that courtship ancestrally involved rubbing with spurs in Boidae. In Colubroidea, courtship ancestrally involved chin-rubbing and head- or body-jerking. Various colubroid clades subsequently added other behaviors, e.g. moving undulations in Natricinae and Lampropeltini, coital neck biting in the Eurasian ratsnake clade, and tail quivering in Pantherophis. The appearance of each group in the fossil record provides a minimum age of the addition of each behavior to combat and courtship repertoires. Although many gaps in the story of the evolution of courtship and combat in snakes remain, this study is an important first step in the reconstruction of the evolution of these behaviors in snakes.
Citation: Senter P, Harris SM, Kent DL (2014) Phylogeny of Courtship and Male-Male Combat Behavior in Snakes. PLoS ONE 9(9): e107528. https://doi.org/10.1371/journal.pone.0107528
Editor: Matthias Stöck, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Germany
Received: June 24, 2014; Accepted: August 20, 2014; Published: September 24, 2014
Copyright: © 2014 Senter et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper.
Funding: The authors have no support or funding to report.
Competing interests: The authors have declared that no competing interests exist.
Many reptilian behaviors are hardwired and stereotyped and therefore heritable . They can therefore be treated as evolutionary characters and mapped onto cladograms to find phylogenetic patterns in behavior, so as to reconstruct the evolution of behavior in a clade. This method has been applied to feeding behavior and defensive displays in snakes , but before now it has not been applied to snake courtship or combat behavior.
Courtship and male-male combat in snakes tend to follow ritualistic patterns, and a few reviews of such behavior patterns in snakes have been published –. Until recently, phylogenetic relationships among many snake genera were unknown, so phylogenetic patterns of these behaviors could not be analyzed. Now, however, recent phylogenetic studies of snake genes – have sufficiently clarified relationships to enable such analysis.
Previous authors have recorded data on courtship and male-male combat in 76 species of snakes, all within the clade Boidae + Colubroidea (Table 1). Although the sample includes less than 4% of the species in this very speciose clade, the sample's taxonomic coverage is sufficiently broad to elucidate phylogenetic trends in courtship and combat behaviors. We therefore undertook to identify any such trends.
From the literature on courtship and male-male combat behavior in snakes (Table 1) we chose 33 behavioral characters (hereafter abbreviated BC) to analyze. These are described in Table 2. For the “courtship” category we included some BCs that occur simultaneously with copulation, but we ignored postcopulatory BCs.
From recent phylogenetic studies on snakes we created a consensus cladogram of the species in our sample. Onto the consensus cladogram we then mapped each BC (Fig. 1, 2). For Colubroidea we used a recently-published phylogeny . It is missing some of the crotaline species in our sample, so for Crotalinae we used a recently-published phylogeny of Crotalinae . For Boidae we used two recently-published phylogenies , .
See Table 1 for references. On the chart on the right, the heavy horizontal lines separate families and subfamilies. On the cladogram, white circles represent families, gray oblongs represent subfamilies, and the gray square is a tribe. Suprageneric taxonomy follows reference . Taxonomic abbreviations: B = Boidae. b = Boinae. C = Colubridae. c = Colubrinae. cr = Crotalinae. d = Dipsadinae. E = Elapidae. L = Lamprophiidae. l = Lamprophiinae. la = Lampropeltini. n = Natricinae. P = Pythoninae. ps = Psammophiinae. px = Pseudoxyrhophiinae. V = Viperidae. v = Viperinae. For abbreviations of behavioral characters, see Table 2.
We used outgroup comparison to determine which BCs arose within Serpentes (snakes) and which might have been inherited from a squamate ancestor outside Serpentes and are therefore behavioral symplesiomorphies (ancestral BCs) of Boidae + Colubroidea. Outgroup comparison reveals that many of the behaviors listed above arose within Serpentes, because they are unrecorded in male-male combat and courtship of non-snake squamate (lizard) taxa , . BCs that are recorded in lizards include the bite, chin-rub, downward push, head bob, head raise (type 1), jerk (types 1 and 3), mouth gape, tail raise, tail quiver, tail wave, and tail whip . To determine which of these BCs are plausible candidates for behavioral symplesiomorphies of Boidae + Colubroidea, we evaluated the phylogenetic distribution of these behaviors across Squamata, using three previously-published molecular phylogenies of Squamata –. All three phylogenies agree that the successive outgroups to Serpentes are: Iguania + Anguimorpha, Teiidae + (Lacertidae + Amphisbaenia), Scincidae + (Xantusiidae + Cordylidae), and Gekkota.
Of the above BCs, the bite and the mouth gape and are widespread through all four lizard outgroups  and are therefore plausible candidates for behavioral symplesiomorphies of Boidae + Colubroidea. The other BCs are too limited or unclear in phylogenetic distribution to be plausible candidates. The head bob is common in Iguania, Lacertidae, and Scincidae , , , but shows no clear phylogenetic pattern across Squamata. The head raise is known only in a few iguanians and gekkotans . The chin-rub and downward push are found mainly in Varanidae, the jerk (type 1) in Chamaeleonidae and Varanidae, the jerk (type 3) in Chamaeleonidae and Scincidae, the tail raise in Iguania, the tail quiver in Iguania and Scincidae, the tail wave in Iguania and Scincidae, and the tail whip in Iguania and Varanidae , –.
It should be noted that the parameters that define each BC in the eye of an observer may be different from the parameters established by the genes governing each BC. It is therefore possible that BCs that are genetically different in different species may accidentally have been lumped together as one BC in our study. This caveat should therefore be understood to be present within the definition of each BC in Table 2.
Results for Combat
For male-male combat in snakes, some BCs are recorded only in one species (chin-rub, head-raise type 1, mounting [all types], mouth gape, spur rub, tail quiver, tail whip). Some other BCs show no clear phylogenetic trend, because they are recorded only in two or a few species that are phylogenetically disparate (bite, jerk type 3, mount type 2) (Fig. 1, 2). The bite and mouth gape are rare and phylogenetically erratic. There is therefore no support for the hypothesis that either is a behavioral symplesiomorphy of male-male combat for Boidae + Colubroidea.
For the other BCs, phylogenetic trends are discernible in at least some snake clades. The results for those BC are as follows.
This behavior is ubiquitous in Lampropeltini and is therefore ancestral for the clade. It also occurs in Boiga irregularis. It was not observed in the other colubrine in our combat sample, Masticophis taeniatus, but the M. taeniatus combatants fell down a hill during combat ; it is possible that a body bridge would have occurred if the combat had not thus been disrupted. It is therefore possible that the body bridge is ancestral for Colubrinae.
The coil (without simultaneous downward push) is rare outside Colubrinae but present in four of the five sampled colubrine genera. It is more parsimonious to infer that it is ancestral for Colubrinae and has possibly been lost in Lampropeltis (a two-step scenario) than to infer that it arose independently in Masticophis, Boiga, and Pantherophis + Pituophis (a three-step scenario).
This BC is present in the closely-related species Bitis gabonica and B. caudalis, which therefore may have inherited it from a common ancestor (a one-step scenario) rather than having acquired it independently (a two-step scenario).
This behavior is almost universal outside Colubrinae and is absent within Lampropeltini. It is therefore most likely ancestral for Boidae + Colubroidea and lost in Lampropeltini. Even if it is truly absent in the non-lampropeltine species in our sample for which it has not been observed, it is more parsimonious to infer that it was ancestral for Boidae + Colubroidea and lost multiple times (a four-step scenario) than to infer that the downward push was independently acquired in each clade for which all members in our sample exhibit it (a seven-step scenario).
Head raise (type 2)
The phylogenetic distribution of this BC nearly matches that of the downward push, and the two generally occur simultaneously during combat. As with the downward push, then, this behavior is most likely ancestral for Boidae + Colubroidea and lost in Lampropeltini. Even if it is truly absent in the non-lampropeltine species in our sample for which it has not been observed, it is more parsimonious to infer that it was ancestral for Boidae + Colubroidea and lost multiple times (a three-step scenario) than to infer that the downward push was independently acquired in each clade for which all members in our sample exhibit it (a four-step scenario).
Jerk (type 1)
This BC is present in the closely-related species Bitis gabonica and B. caudalis, which therefore may have inherited it from a common ancestor (a one-step scenario) rather than having acquired it independently (a two-step scenario).
This BC is documented in boas and one python, and may be ancestral for Boidae. It has not been reported in the other python in the sample (Morelia spilota), but for one observer the view of the posterior ends of the combatant pythons was obscured by water , and for the other observer the view of the posterior ends of the combatant pythons may have been obscured by coils . If the spur poke is truly absent in M. spilota, it is equally parsimonious to infer that it is ancestral for Boidae and lost in M. spilota or that it was independently acquired in the other two boids in the sample. Both scenarios are two-step scenarios.
This BC is recorded in three crotalines, a viperine, and one colubrine. No clear phylogenetic pattern is present, but its presence in several members of Viperidae raises the possibility that it is characteristic of Viperidae but has not been explicitly described in other vipers. More research is necessary to determine this. If it is truly absent in the viper species for which it is unrecorded, then it is more parsimonious to infer that it was independently acquired multiple times (a four-step scenario) than to infer that it was independently lost multiple times (an eight-step scenario).
Results for Courtship
For snake courtship, some BCs are recorded only in one species (breeding ball, body bridge, bounce, closed-mouth strike, head shake, tail raise, tail wave, tail whip). Some other BCs show no clear phylogenetic trend because they are recorded only in two or a few species that are phylogenetically disparate (breeding mass, head bob, lateral head rub, mouth gape, mounting type 1b, sway) (Fig. 1, 2). The bite and mouth gape are rare and phylogenetically erratic; there is therefore no support for the hypothesis that either is a behavioral symplesiomorphy for courtship in Boidae + Colubroidea.
For the other BCs, phylogenetic trends are discernible in at least some snake clades. The results for those BC are as follows.
Coital neck biting is prevalent in the Eurasian ratsnake clade Zamenis + (Elaphe + (Coronella + Lampropeltini)) and is likely ancestral for the group. It is undocumented in four species in our sample from this clade, but even if it has been lost in those four species, a single-origin scenario is more parsimonious (five evolutionary steps) than a scenario in which coital biting appeared convergently in each taxon within this clade (a seven-step scenario). Outside this clade, documented coital neck biting is rare and has no discernible phylogenetic pattern.
This behavior is undocumented in Boidae but is widespread enough in Colubroidea to infer that it is ancestral for Colubroidea. It usually occurs early in courtship, and its lack of documentation in some species may be due to some observers' having arrived after courtship had already begun. Even if the chin-rub is truly absent in the species in our sample for which it is undocumented, it is more parsimonious to infer that it is ancestral for Colubroidea and was lost multiple times (a 17-step scenario) than to infer that it was independently gained in each clade in which it is documented in all members (a 21-step scenario).
This behavior is documented in every family examined here except Elapidae. It may be ancestral for Boidae + Colubroidea, but its documented phylogenetic distribution is too sparse to be certain. If it is truly absent in the species for which it is undocumented, then it is more parsimonious to infer that it arose independently multiple times (a 13-step scenario) than to infer that it was present in the common ancestor of Boidae + Colubroidea and was lost multiple times (24-step scenario).
This behavior is present in females of both sampled species of Lachesis and may have been inherited from a common ancestor (a one-step scenario) instead of independently acquired (a two-step scenario). Its known phylogenetic distribution outside Lachesis is too sparse to draw further phylogenetic inferences.
Head raise (types 1 and 2)
Head raising, of which the two types can be considered to differ mainly in magnitude, is present mainly in Colubrinae. Its recorded distribution is too erratic to determine whether it is ancestral for the subfamily and has been lost in species in which it is unrecorded (a nine-step scenario) or has appeared convergently several times (a six-step scenario). The latter scenario is more parsimonious, but it is also possible that is some species it occurs but has not been observed.
Jerk (types 1, 2, and 3)
The jerk, of which the three types can be considered to differ mainly in magnitude, is unrecorded in Boidae and in the clade Natricinae + Dipsadinae but is prevalent in Viperidae, Elapidae, and Colubrinae and is recorded in one lamprophiid. It is therefore probably ancestral for Colubroidea and has been lost in Natricinae + Dipsadinae. The elevation of its magnitude to type 3 is universal in the sampled elapids. Because those three species phylogenetically bracket the Australasian elapid clade , type 3 is probably ancestral for that clade but cannot be inferred to be ancestral for Elapidae as a whole. Type 3 is also present in the one lamprophiid for which the behavior is recorded, and it is possible that a larger lamprophiid sample would reveal that it is ancestral for the clade Elapidae + Lamprophiidae. Type 3 is ubiquitous in Pantherophis, for which it is therefore probably ancestral. If the jerk is truly absent in the species for which is it undocumented, then it is more parsimonious to infer that it has been acquired multiple times (a 12-step scenario if changes in the type of jerk are not taken into account; 13 steps otherwise) than to infer that it is ancestral for Colubroidea and has been lost multiple times (a 19-step scenario).
This BC is recorded in both sampled species of Lachesis and is therefore more likely inherited from a common ancestor (a one-step scenario) than independently acquired (a two-step scenario).
Mounting (types 1–5)
Although unnecessary for intromission in snakes, mounting is nearly universal among the sampled species. It is therefore likely ancestral for Boidae + Colubroidea. However, its magnitude differs widely between taxa. The phylogenetic distribution of type 1 is too erratic and sparse to infer any phylogenetic pattern except in the two sampled species of Lampropeltis, which are more likely to have inherited it from a common ancestor (a one-step scenario) than to have acquired it independently (two steps). Type 2 is present in all three elapid species in the courtship sample and it is therefore more parsimonious to infer that it is ancestral for Australasian Elapidae (one step) than to infer that the three species acquired it independently (three steps). Outside Elapidae it exhibits no discernible phylogenetic pattern. Type 3 is present in all sampled members of Pythoninae, Ungaliophis + Lichanura, and Vipera. It may therefore be ancestral for each of those three clades. Elsewhere its phylogenetic distribution is too sparse and erratic to infer a pattern. Type 4 is widespread in Colubridae but is unrecorded in too many sampled colubrids to confidently infer that it is ancestral for the family. However, its phylogenetic distribution indicates that it is likely ancestral for Natricinae, Philodryas and Lampropeltini. It is present in both sampled species of Philodryas, which therefore more likely inherited it from a common ancestor (one step) than independently acquired it (two steps). It it is truly absent in the species for which it is unrecorded, then within Natricinae it is more parsimonious to infer that it was lost in those species (three steps) than that it was independently acquired in the others (four steps). In Lampropeltini both inferences involve two evolutionary steps and are therefore equally parsimonious. Type 5 is recorded in both sampled species of Lachesis, which therefore more likely inherited it from a common ancestor (one step) than independently acquired it (two steps).
This BC is recorded only in the sister genera Eunectes and Epicrates, which therefore more likely inherited it from a common ancestor (one step) than independently acquired it (two steps).
This BC is widespread enough in Boidae to infer that it is ancestral for the family. If it is truly absent in the species for which it is unrecorded, then it is more parsimonious to infer that it was lost in those species (three steps) than that it was independently acquired in the boid clades that exhibit it (five steps).
Our results, together with the fossil record, suggest the following scenario for the evolution of male-male combat behavior in snakes (Fig. 3). Its ancestral form for Boidae + Colubroidea included the head raise (type 2) with simultaneous downward push. This combination of BCs was present by the Cenomanian Age (early Late Cretaceous), the date of the clade's earliest known members . The spur poke was added in Boidae by the Paleocene Epoch, the date of the earliest known crown-group boid . The closed-mouth strike and jerk (type 1) were added in the ancestor of Bitis gabonica and B. caudalis (date unknown). In Lampropeltini the downward push and head raise (type 2) were lost and replaced by the coil and possibly also the body bridge by the mid-Miocene, the date of the earliest known lampropeltine .
Our results, together with the fossil record, suggest the following scenario for the evolution of courtship behavior in snakes (Fig. 4). Ancestrally, courtship in Boidae included the spur rub by the Paleocene, the date of the earliest known crown-group boid . Mounting (type 3) was added in Pythoninae by the early Miocene, the date of the earliest known member of Python . It was added in Ungaliophis + Lichanura by the mid-Eocene, the date of the earliest known member of the latter clade . The spur poke was added in Epicrates + Eunectes by the mid-Miocene, the date of the earliest known member of the clade . Ancestrally, courtship in Colubroidea included the chin-rub and jerk by the early Eocene, the date of the earliest known crown-group colubroid . Mounting (type 3) was added in the ancestor of Vipera berus and V. xanthina (date unknown); lateral punch and female cloacal gaping in Lachesis (date unknown); jerk (type 3) and mounting (type 2) in Australasian Elapidae by the early Miocene ; loss of jerk in Natricinae + Dipsadinae by the early Oligocene ; mounting (type 4) in Natricinae by the early Oligocene , Philodryas (date unknown), and Lampropeltini by the mid-Miocene ; coital bite in the Eurasian ratsnake clade Zamenis + (Elaphe + (Coronella + Lampropeltini)) by the early Miocene ; mounting (type 1) in Lampropeltis by the mid-Miocene ; and tail quiver in Pantherophis by the late Miocene .
Often, behaviors that occur in nature are unrecorded. An observer may miss the beginning or end of courtship or combat, a report may omit a behavior that an observer deems too obvious to explicitly state, and captive snake behavior may differ from behavior in the wild. Because of this uncertainty, an inference that a behavior is absent in a clade must be treated with caution. The scenarios presented above are therefore subject to modification pending further data.
Even so, this study shows that available data are sufficient to reveal interesting and important phylogenetic trends in some behavioral characters of combat and courtship in snakes. The results of the study also identify several behavioral characters that need more attention from future research, to help fill current gaps in our ability to reconstruct behavioral evolution in snakes.
This study is an important first step in elucidating the evolutionary history of courtship and combat behavior in snakes. Using available data we have filled in a few important parts of the picture of snake behavioral evolution. To fill in the rest of the evolutionary picture it will be necessary to record observations on combat and courtship behavior in many more snake species. We therefore look forward to further elucidation that future studies will provide.
The following people provided assistance. Tiara Rankins compiled the list of articles that we used for the study. Christine Giannoni (Field Museum Library) provided three of the articles. Sherrice Allen served as coordinator for BIOL 430, the undergraduate student research course under which this study began. Alex Pyron and five anonymous reviewers provided useful input that improved this paper.
Conceived and designed the experiments: PS. Performed the experiments: PS. Analyzed the data: PS SMH DLK. Contributed reagents/materials/analysis tools: PS SMH DLK. Contributed to the writing of the manuscript: PS. SMH DLK.
- 1. Carpenter CC, Ferguson CW (1977) Variation and evolution of stereotyped behavior in reptiles. In : Biology of the Reptilia, vol. 7. London: Academic Press. 335–554.
- 2. Greene HW (1994) Homology and behavioral repertoires. In: Homology: the hierarchical basis of comparative biology. San Diego: Academic Press. 369–391.
- 3. Davis DD (1936) Courtship and mating behavior in snakes. Zool Ser Field Mus Nat Hist 20: 256–290.
- 4. Shaw CE (1951) Male combat in American colubrid snakes with remarks on combat in other colubrid and elapid snakes. Herpetologica 7: 149–168.
- 5. Carpenter CC (1977 Communication and displays of snakes. Am Zool 17: 217–223.
- 6. Gillingham JC (1987) Social behavior. In: Snakes: ecology and evolutionary biology. New York: MacMillan. 184–209.
- 7. Slowinski JB, Lawson R (2002) Snake phylogeny: evidence from nuclear and mitochondrial genes. Mol Phyl Evol 24: 194–202.
- 8. Burbrink FT (2005) Inferring the phylogenetic position of Boa constrictor among the Boinae. Mol Phyl Evol 34: 167–180.
- 9. Pyron RA, Burbrink FT, Colli GR, Montes de Oca AN, Vitt LJ, et al. (2011) The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol Phyl Evol 58: 329–342.
- 10. Castoe TA, Parkinson CL (2001) Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). Mol Phyl Evol 39: 91–110.
- 11. Carpenter CC (1978) Ritualistic social behaviors in lizards. In: Behavior and neurology of lizards, an interdisciplinary colloquium. Rockville, Maryland: National Institute of Mental Health, Rockville. 253–267.
- 12. Vidal N, Hedges B (2005) The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. C R Biol 328: 1000–1008.
- 13. Mulcahy DG, Noonon BP, Moss T, Townsend TM, Reeder TW, et al. (2012) Estimating divergence dates and evaluating dating methods using phylogenomic and mitochondrial data in squamate reptiles. Mol Phyl Evol 65: 974–991.
- 14. Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13(93): 1–53.
- 15. Carpenter CC (1982) The aggressive displays of iguanine lizards. In: Iguanas of the world. their behavior, ecology, and conservation. Park Ridge, New Jersey: Noyes. 215–231.
- 16. Martins EP, Lamont J (1998) Estimating ancestral states of a communicative display: a comparative study of Cyclura rock iguanas. An Beh 55: 1685–1706.
- 17. Hunsacker D (1962) Ecological isolating mechanisms in the Sceloporus torquatus group of lizards. Evolution 16: 62–74.
- 18. Everett CT (1971) Courtship and mating of Eumeces multivirgatus (Scincidae). J Herpetol 5: 189–190.
- 19. Murphy JB, Lamoreux WE, Carpenter CC (1978) Threatening behavior in the angle-headed dragon, Goniocephalus dilophus (Reptilia, Lacertilia, Agamidae). J Herpetol 12: 4554–460.
- 20. Auffenberg W (1981) The behavioral ecology of the Komodo monitor. Gainesville: University Press of Florida.
- 21. Auffenberg W (1988) Gray's monitor lizard. Gainesville: University Press of Florida.
- 22. Auffenberg W (1994) The Bengal monitor. Gainesville: University Press of Florida.
- 23. Horn H-G, Gaulke M, Böehme W (1994) New data on ritualized combats in monitor lizards (Sauria: Varanidae), with remarks on their function and phylogenetic implications. Zool Garten N F 64: 265–280.
- 24. Langkilde T, Schwartzkopf L, Alford RA (2005) The function of tail displays in male rainbow skinks (Carlia jarnoldae). J Herpetol 39: 325–328.
- 25. Bennion RS, Parker WS (1976) Field observations on courtship and aggressive behavior in desert striped whipsnakes, Masticophis t. taeniatus. Herpetologica 32: 30–35.
- 26. Covacevich J (1975) Snakes in combat. Vict Nat 92: 252–253.
- 27. Hammond S (1988) Morelia spilotes variegata (carpet python). Male combat. Herpetol Rev 19: 37.
- 28. Rage J-C, Werner C (1999) Mid-Cretaceous (Cenomanian) snakes from Wadi Abu Hashim, Sudan: the earliest snake assemblage. Palaeontol Afr 35: 85–110.
- 29. Head JJ, Bloch JI, Hastings AK, Bourque JR, Cadena EA, et al. (2009) Giant boid snake from the Paleocene neotropics reveals hotter past equatorial temperatures. Nature 457: 715–717.
- 30. Holman JA (2000) Fossil snakes of North America. Origin, evolution, distribution, paleoecology. Bloomington: Indiana University Press.
- 31. Szyndlar Z, Rage JC (2003) Non-erycine Booidea from the Oligocene and Miocene of Europe. Kraków: Polish Academy of Sciences.
- 32. McGrew PO (1959) The geology and paleontology of the Elk Mountain and Tabernacle Butte area, Wyoming. Bull Am Mus Nat Hist 117: 121–176.
- 33. Cozzuol MA (2006) The Acre vertebrate fauna: age, diversity, and geography. J S Am Ea Sci 21: 185–203.
- 34. Rage J-C, Bajpai S, Thewissen JGM, Tiwari BN (2003) Early Eocene snakes from Kutch, western India, with a review of the Palaeophiidae. Geodiversitas 25: 695–716.
- 35. Scanlon JD, Lee MSY, Archer M (2003) Mid-Tertiary elapid snakes (Squamata, Colubroidea) from Riversleigh, northern Australia: early steps in a continent-wide adaptive radiation. Geobios 36: 573–601.
- 36. Ivanov M (2002) The oldest known Miocene snake fauna from Central Europe: Merkur-North locality, Czech Republic. Acta Palaeontol Pol 47: 513–534.
- 37. Murphy JB, Barker DG, Tryon BW (1978) Miscellaneous notes on the reproductive biology of reptiles. 2. Eleven species of the family Boidae, genera Candoia, Corallus, Epicrates, and Python. J Herpetol 12: 385–390.
- 38. Hanlon RW (1964) Reproductive activity of the Bahaman boa (Epicrates striatus). Herpetologica 20: 143–144.
- 39. Rivas JA (2000) The life history of the green anaconda (Eunectes murinus), with emphasis on its reproductive biology. Ph.D. dissertation, Knoxville: University of Tennessee.
- 40. Kurfess JF (1967) Mating, gestation, and growth rate in Lichanura r. roseofusca. Copeia 1967: 477–479.
- 41. Carpenter CC, Murphy JB, Mitchell LA (1978) Combat bouts with spur use in the Madagascan boa (Sanzinia madagascariensis). Herpetologica 34: 207–212.
- 42. Burger RM (1966) Observations on courtship behavior in Ungaliophis Mueller. Bull Chicago Herpetol Soc 31(4): 57–59.
- 43. Barker DG, Murphy JB, Smith KW (1979) Social behavior in a captive group of Indian pythons, Python molurus (Serpentes, Boidae) with formation of a linear social hierarchy. Copeia 1979: 466–471.
- 44. Greene MJ, Mason RT (2000) Courtship, mating, and male combat of the brown tree snake, Boiga irregularis. Herpetologica 56: 166–175.
- 45. Almeida-Santos SM, Marques OAV (2002) Male-male ritual combat in the colubrid snake Chironius bicarinatus from the Atlantic Forest, southeastern Brazil Amph-Rept. 23: 528–533.
- 46. Feio RN, Fernandes R, de Freitas TS (1999) Chironius flavolineatus (NCN). Herpetol Rev 30: 99.
- 47. Lillywhite HB (1985) Trailing movements and sexual behavior in Coluber constrictor. J Herpetol 19: 306–308.
- 48. Tinkle DW (1951) Peculiar behavior of indigo snakes in captivity. Copeia 1951: 77–78.
- 49. Moehn LD (1967) A combat dance between two prairie kingsnakes. Copeia 1967: 480–481.
- 50. Kennedy JL (1978) Field observations on courtship and copulation in the eastern king snake and the four-lined rat snake. Herpetologica 34: 51–52.
- 51. Lewke RE (1979) Neck-biting and other aspects of reproductive ecology of the Yuma kingsnake (Lampropeltis getulus). Herpetologica 35: 154–157.
- 52. Secor SM (1987) Courtship and mating behavior of the speckled kingsnake, Lampropeltis getulus holbrooki. Herpetologica 43: 15–28.
- 53. Gillingham JC, Carpenter CC, Brecke BJ, Murphy JB (1977) Courtship and copulatory behavior of the Mexican milk snake, Lampropeltis triangulum sinaloae (Colubridae). Southw Nat 22: 187–194.
- 54. Hammerson GA (1978) Observations on the reproduction, courtship, and aggressive behavior of the striped racer, Masticophis lateralis euryxanthus (Reptilia, Serpentes, Colubridae). J. Herpetol 12: 253–255.
- 55. Goldsmith SK (1988) Courtship behavior of the rough green snake, Opheodrys aestivus (Colubridae: Serpentes). Southw Nat 33: 473–477.
- 56. Gillingham JC (1979) Reproductive behavior of the rat snakes of eastern North America, genus Elaphe. Copeia 1979: 319–331.
- 57. Rigley L (1971) “Combat dance” of the black rat snake, Elaphe o. obsoleta. J Herpetol 5: 55–66.
- 58. Gillingham JC (1974) Reproductive behavior of the western fox snake, Elaphe v. vulpina (Baird and Girard). Herpetologica 30: 309–313.
- 59. Woodbury AM (1941) Copulation in gopher snakes. Copeia 1941: 54.
- 60. Gloyd HK (1947) Notes on the courtship and mating behavior of certain snakes. Nat. Hist. Misc 12: 1–4.
- 61. Bogert CM, Roth VD (1966) Ritualistic combat of male gopher snakes, Pituophis melanoleucus affinis (Reptilia, Colubridae). Am Mus Novit 2245: 1–27.
- 62. Kroll JC (1971) Combat behavior in male Great Plains ground snakes (Sonora episcopa episcopa). Texas J Sci 23: 300.
- 63. Ball RL, Ford NB (1999) Courtship and mating behavior in the diadem snake, Spalerosophis diadema cliffordi (Colubridae). Af J Herpetol 48: 27–31.
- 64. Langford GL, Borden JA (2004) Farancia abacura (mud snake). Courtship behavior. Herpetol Rev 35: 400–401.
- 65. Bels V (1987) Observation of the courtship and mating behavior of the snake Hydrodynastes gigas. J Herpetol 21: 350–352.
- 66. Halloy M, Scrocchi G (2003) Philodryas baroni (green snake). Courtship behavior. Herpetol Rev 34: 153.
- 67. Cechin STZ, Hartmann PA (2001) Philodryas olfersii (NCN). Courtship. Herpetol Rev 32: 187.
- 68. Aldridge RD, Bufalino AP, Khayyat P (2003) The mating season and the conflict between courtship and feeding in the watersnake, Nerodia sipedon sipedon. B. Assoc Herpetol Espan 14: 25–28.
- 69. Ford NB (1982) Courtship behavior of the queen snake, Regina septemvittata. Herpetol Rev 13: 72.
- 70. Noble GK (1937) The sense organs involved in the courtship of Storeria, Thamnophis and other snakes. Bull Am Mus Nat Hist 73: 673–725.
- 71. Ruthven AG (1912) On the breeding habits of Butler's garter snake. Biol Bull 24: 18–20.
- 72. Ruthven AG (1908) Variations and genetic relationships of the garter snakes. Bull US Natl Mus 1: 1–201.
- 73. Pisani GR (1976) Comments on the courtship and mating mechanics of Thamnophis (Reptilia, Serpentes, Colubridae). J Herpetol 10: 139–142.
- 74. Crews D, Garstka WR (1982) The ecological physiology of a garter snake. Sci Am 147(5): 158–168.
- 75. Holtzman DA (2001) Thamnophis sirtalis sirtalis (eastern garter snake). Courtship behavior. Herpetol Rev 32: 110.
- 76. Shine R, Allen S (1980) Ritual combat in the Australian copperhead, Austrelaps superbus (Serpentes, Elapidae). Vict Nat 97: 188–190.
- 77. Grant GA (1956) The mating of black mambas. Afr Wild Life 10: 111–113.
- 78. Curry-Lindahl K (1956) Mambas in combat. Afr Wild Life 10: 340–341.
- 79. Shetty S, Shine R (2002) The mating system of yellow-lipped sea kraits (Laticauda colubrina: Laticaudidae). Herpetologica 58: 170–180.
- 80. Shine R, Grigg GC, Shine TG, Harlow P (1981) Mating and male combat in Australian blacksnakes, Pseudechis porphyriacus. J Herpetol 15: 101–107.
- 81. Fleay D (1951) Savage battles between snakes. Walkabout 17: 10–13.
- 82. G (1992) Courtship behavior and male combat in the little whip snake Rhinoplocephalus flagellum (Elapidae). Herpetofauna 22: 14–21.
- 83. Walker SE, Ford NB (1992) Courtship and mating behavior in the brown house snake Lamprophis fuliginosus. J Herpetol 30: 416–418.
- 84. Aldridge RD, Bufalino AP, Robison C, Salgado C, Khayyat P (2005) Female sex-pheromone volatility and male uric acid excretion during courtship in captive African brown house snakes, Lamprophis fuliginosus. Amph-Rept 26: 576–582.
- 85. Haagner GV (1991) Rhamphiophis oxyrhynchus rostratus. Rufous beaked snake. Agonistic male behaviour. J Herpetol Assoc Afr 39: 25.
- 86. Campbell JA, Murphy JB (1977) Miscellaneous notes on the reproductive biology of reptiles. 1. Two colubrid snake species from the Malagasy Republic, Leioheterodon madagascariensis and Madagascariophis colubrina (Reptilia, Serpentes, Colubridae). J Herpetol 11: 228–230.
- 87. Mehta R, Ford NB (2001) Courtship in the Madagascar cat-eyed snake, Madagascarophis colubrina (Boiginae). Af J Herpetol 50: 115–120.
- 88. Burchfield PM (1982) Additions to the natural history of the crotaline snake Agkistrodon bilineatus taylori. J Herpetol 16: 376–382.
- 89. Schuett GW, Gillingham JC (1988) Courtship and mating of the copperhead, Agkistrodon contortrix. Copeia 1988: 374–381.
- 90. Carr AF Jr, Carr MH (1942) Notes on the courtship of the cottonmouth moccasin. Proc N Eng Zool Cl 20: 1–6.
- 91. Martin L (1984) An instance of sexual defense in the cottonmouth, Agkistrodon piscivorus. Copeia 1984: 774–776.
- 92. Perry J (1978) An observation of “dance” behavior in the western cottonmouth, Agkistrodon piscivorus leucostoma. J. Herpetol 12: 429–431.
- 93. Antonio FB (1980) Mating behavior and reproduction of the eyelash viper (Bothriechis schlegelii) in captivity. Herpetologica 36: 231–233.
- 94. Gillingham JC, Carpenter CC, Murphy JB (1983) Courtship, male combat and dominance in the western diamondback rattlesnake, Crotalus atrox. J Herpetol 17: 265–270.
- 95. Bonine KE, Stitt EW, Bradley GL, Smith JJ (2004) Crotalus atrox (western diamond-backed rattlesnake). Entrapment and opportunistic courtship. Herpetol Rev 35: 176–177.
- 96. Garcia de Langlada F (1975) Combat-dance between males of Brazilian Crotalus durissus. J Herpetol 9: 349–351.
- 97. Klauber LM (1956) Rattlesnakes. Their habits, life histories, and influence on mankind. Berkeley: University of California Press.
- 98. Sutherland IDW (1958) The “combat dance” of the timber rattlesnake. Herpetologica 14: 23–24.
- 99. Hayes WK (1986) Observations of courtship in the rattlesnake, Crotalus viridis oreganus. J. Herpetol (20: 246–249.
- 100. Reed RN (2003) Courtship and copulation in the Grand Canyon rattlesnake, Crotalus viridis abyssus. Herpetol Rev 34: 111–112.
- 101. Ripa D (1994) Reproduction of the Central American bushmaster (Lachesis muta stenophrys) and the black-headed bushmaster (L. muta melanocephala) for the first time in captivity. Bull Chicago Herpetol Soc 29: 165–183.
- 102. Campbell JA, Solorzano A (1992) The distribution, variation, and natural history of the Middle American montane pitviper, Porthidium godmani. In: Biology of the pitvipers. Tyler, Texas: Selva. 223–250.
- 103. Palmer WM, Williamson GM (1971) Observations on the natural history of the Carolina pigmy rattlesnake, Sistrurus miliarius miliarius Linnaeus. J Mitchell Soc 97: 20–25.
- 104. Harvey E (1964) Snake “dance”. Africana 2: 49.
- 105. Pitman CRS (1974) A guide to the snakes of Uganda. Codicote, UK: Wheldon and Wesley.
- 106. Akester J (1983) Male combat and reproductive behaviour in captive Bitis caudalis (A. Smith). Brit J Herpetol 6: 329–333.
- 107. Akester J (1979) Male combat in captive Gaboon vipers (Serpentes: Viperidae). Herpetologica 35: 124–128.
- 108. Andrén C (1986) Courtship, mating and agonistic behaviour in a free-living population of adders, Vipera berus (L.). Amph-Rept 7: 353–383.
- 109. Murphy JB, Barker DG (1980) Courtship and copulation of the Ottoman viper (Vipera xanthina) with special reference to use of the hemipenes. Herpetologica 36: 165–170.