How snakes eat snakes: the biomechanical challenges of ophiophagy for the California kingsnake, Lampropeltis getula californiae (Serpentes: Colubridae)

doi:10.1016/j.zool.2004.06.001

Zoology

Volume 107, Issue 3, 16 September 2004, Pages 191-200

https://doi.org/10.1016/j.zool.2004.06.001 Get rights and content

Abstract

In this study we investigated how ophiophagous snakes are able to ingest prey snakes that equal or exceed their own length. We used X-ray video, standard video, dissection, and still X-rays to document the process of ophiophagy in kingsnakes (Lampropeltis getula) feeding on corn snakes (Elaphe guttata). Most kingsnakes readily accepted the prey snakes, subdued them by constriction, and swallowed them head first. In agreement with previous observations of ophiophagy, we found that the predator snake forces the vertebral column of the prey snake to bend into waves. These waves shorten the prey's body axis and allow it to fit inside the gastrointestinal (GI) tract and body cavity of the predator. Dissection of a kingsnake immediately following ingestion revealed extensive longitudinal stretching of the anterior portion of the GI tract (oesophagus and stomach), and no visible incursion of the prey into the intestine. X-ray video of ingestion showed that the primary mechanism of prey transport was the pterygoid walk, with some contribution from concertina-like compression and extension cycles of the predator's vertebral column in two out of three observations. Complete digestion was observed in only one individual, as others regurgitated before digestion was finished. X-ray stills taken every 4 days following ingestion revealed that the corn snakes were about half digested within the first 4 days, and digestion was complete within 15 days.

Introduction

Many genera of snakes (e.g., Cylindrophis, Agkistrodon, Lampropeltis, Drymarchon, Ophiophagus, Micrurus, Atractaspis, and many others) have members that include snakes or other elongate prey as part or all of their diet (Greene, 1997). A few published observations indicate that some snakes are even able to ingest other snakes that equal or exceed their own body length (Hurter, 1893; Wall, 1921; Ditmars, 1931; Evans, 1948; Rose, 1962).

The finding that snakes can ingest snakes of equal or greater length raises several mechanical problems and questions. First, the caudal end of the stomach in snakes is located at approximately two-thirds of the distance from snout to vent (e.g., Bergman, 1953, Bergman, 1955). A prey snake that is equal in total length (TL) to the predator will be at least 50% longer than the distance from the tip of the predator's snout to the end of its stomach. How is the prey packed into the gastrointestinal (GI) tract and body cavity (pleuroperitoneal cavity) of the predator? Does the stomach stretch longitudinally to allow the prey snake to fill the full length of the body cavity (i.e., is the pylorus displaced caudally during swallowing)? Or might part of the prey snake advance past the pylorus and into the intestine, thereby filling the full length of the predator's body cavity? Or is the final position of the prey snake limited by the resting position of the stomach, leaving the caudal one-third of the predator's body cavity empty?

Second, if the two snakes are similar in total length, then the length of the prey will exceed the length of the predator's body cavity because its TL exceeds the snout–vent length (SVL) of the predator. Therefore, the prey will have to be folded or curled in some way in order to fit inside the SVL of the predator. Is the prey bent in half, coiled up, or thrown into waves to decrease its length and pack it into the space available? Or might one end of the prey be left to protrude from the mouth of the predator while the other end is gradually digested?

Preliminary answers for some of these questions are provided by published observations of snakes consuming snakes of equal or greater length (Hurter, 1893; Wall, 1921; Ditmars, 1931; Evans, 1948; Rose, 1962). In these previous observations, the entire prey snake was ingested—one end did not protrude from the predator's mouth during digestion. Ditmars (1931) shows an X-ray image of a prey snake inside a Florida kingsnake, Lampropeltis getula floridana. The vertebral column of the prey snake is bent into waves, and the thin tip of the prey's tail is folded backward into a hairpin loop near the head of the predator. Rose (1962) shows an X-ray of a neonatal Crotaphopeltis that swallowed one of its clutch mates, and Evans (1948) shows a cleared and stained preparation of a young Thamnophis that consumed another snake from the same litter. In both the X-ray and the cleared and stained preparation, the vertebral column of the prey snake is bent into waves, similar to the configuration in the image published by Ditmars. These previous descriptions of ophiophagy are brief, report single instances of ophiophagy, and generally describe only the end result of the process. Our goal in the present study is to document the entire process of ophiophagy from initial strike to the completion of digestion in multiple instances of California kingsnakes feeding on corn snakes of equal or greater total length. Our primary tool is X-ray video, which allows us to observe the process of ingestion over long periods of time in multiple individuals. Our results can then be compared with results from previous studies of snakes feeding on other prey types.

A few recent studies have investigated the mechanisms by which snakes ingest small prey (type I, sensuGreene, 1983), such as insects and snails (e.g., Sazima, 1989; Kley and Brainerd, 1999; Kley, 2001, Götz, 2002), but most previous studies have focused on the mechanics of feeding on relatively massive, bulky prey (type III, sensuGreene, 1983), such as mammals (e.g., Albright and Nelson, 1959a, Albright and Nelson, 1959b; Frazzetta, 1966; Cundall, 1983; Kardong and Berkhoudt, 1998; Moon, 2000; Kley and Brainerd, 2002). Our study will provide new data on the mechanisms by which snakes ingest massive, elongate prey (type II, sensuGreene, 1983), particularly massive, elongate vertebrate prey (type IIb, Cundall and Greene, 2000).

Our X-ray video results will be particularly interesting to compare with Kley and Brainerd's (2002) X-ray video study of alethinophidian snakes feeding on rodents. In this study, four distinct phases of prey transport were identified: oral, orocervical, cervical, and thoracic. Our X-ray video observations of ophiophagy will allow us to determine whether these same four phases occur when kingsnakes ingest corn snakes, and whether the relative contributions of each phase to prey transport are similar when snakes feed on these two very different prey types—rodents and snakes.

Section snippets

Materials and methods

Kingsnakes (L. getula) were used as the predator snakes ( $n = 4$ ; Table 1) because this species is known to include snakes in its natural diet (Wright and Wright, 1957; Van Denburgh, 1922) and because captive-bred individuals were readily available commercially. Corn snakes (Elaphe guttata) were used as prey snakes ( $n = 6$ ; Table 1). This species was chosen because they were snakes of appropriate size that were available commercially at the time of the experiments. All measurements of SVL and TL were

Results

Our observations led us to divide the process of a snake eating another snake into four distinct stages: (1) capture; (2) constriction; (3) ingestion; and (4) digestion. The results of our nine trials are summarised in Table 3.

In six of the nine trials, the kingsnake attacked the prey snake as soon as the prey was introduced into the predator snake's cage. In one trial there was a waiting period of approximately 0.3 h before the kingsnake attacked the prey snake, and in two trials the predator

Discussion

Our results are in general agreement with previously published reports of snakes feeding on snakes of equal or greater length than themselves (Hurter, 1893; Wall, 1921; Ditmars, 1931; Evans, 1948; Rose, 1962). We found that after a kingsnake ingested a corn snake of equal or greater length, the corn snake filled most of the length of the kingsnake's body cavity (Fig. 2, Fig. 3). The prey snake was not restricted to the anterior two-thirds of the predator's body cavity, as might be predicted by

Acknowledgements

We thank A. Crompton, K. Hartel, and F. Jenkins for use of facilities and equipment at Harvard University, and we thank R. McDiarmid, G. Zug, and the Division of Amphibians and Reptiles of the National Museum of Natural History for permission to dissect rare specimens in their collection. C. Kenaley, R. Levine, and T. Owerkowicz provided essential technical assistance. We thank H. Greene, S. Secor, and members of the Smithsonian's Division of Amphibians and Reptiles for helpful discussion of

References (52)

D. Cundall et al.
Feeding in snakes
N.J. Kley et al.
Post-cranial prey transport mechanisms in the black pinesnake, Pituophus melanoleucus lodingian X-ray videographic study
Zoology
(2002)
R. Skoczylas
Influence of temperature on gastric digestion in the grass snake, Natrix natrix, L.
Comp. Biochem. Physiol.
(1970)
R.G. Albright et al.
Cranial kinetics of the generalized colubrid snake Elaphe obsolete quadrivittata. I. Descriptive morphology
J. Morphol.
(1959)
R.G. Albright et al.
Cranial kinetics of the generalized colubrid snake Elaphe obsolete quadrivittata. II. Functional morphology
J. Morphol.
(1959)
P.L.R. Andrews et al.
The emetic reflex in a reptile (Crocodylus porosus)
J. Exp. Biol.
(2000)
R.A.M. Bergman
L’anatomie du genre Ptyas a Java
Riv. Biol. Colon.
(1952)
R.A.M. Bergman
The anatomy of Cylindrophis rufus (Laur.). I and II
Proc. Kon. Ned. Akad. Wet. Ser. C
(1953)
R.A.M. Bergman
The anatomy of Xenopeltis unicolor
Zool. Meded.
(1955)
R.A.M. Bergman
The anatomy of the Acrochordinae. I, II, III and IV
Proc. Kon. Ned. Akad. Wet. Ser. C
(1958)

R.A.M. Bergman

The anatomie of some Homalopsinae

Biol. Jaarb.

(1960)

R.A.M. Bergman

The anatomy of some Viperidae. I, II and III

Acta Morphol. Neerl.-Scand.

(1961)

R.A.M. Bergman

Die Anatomie der Elapinae

Z. Wiss. Zool.

(1962)

A.W. Blain et al.

A study of digestive phenomena in snakes with the aid of the Roentgen ray

Am. J. Roentgenol. Radium Ther.

(1942)

R.E. Boltt et al.

The functional anatomy of the head of the puff adder, Bitis arietans (Merr.)

J. Morphol.

(1964)

W.R. Branch et al.

Bitis caudalis (Horned Adder). Prey size

Herpetol. Rev.

(2002)

D. Cundall

Activity of head muscles during feeding by snakesa comparative study

Am. Zool.

(1983)

RL. Ditmars

Snakes of the World

(1931)

H.E. Evans

Clearing and staining small vertebrates, in toto, for demonstrating ossification

Turtox News

(1948)

T.H. Frazzetta

Studies on the morphology and function of the skull in the Boidae (Serpentes). Part II. Morphology and function of the jaw apparatus in Python sebae and Python molurus

J. Morphol.

(1966)

F.L. Frye

Biomedical and Surgical Aspects of Captive Reptile Husbandry

(1991)

C. Gans

The functional morphology of the egg-eating adaptations in the snake genus Dasypeltis

Zoologica

(1952)

C. Gans

BiomechanicsAn Approach to Vertebrate Biology

(1974)

M. Götz

The feeding behaviour of the snail-eating snake Pareas carinatus Wagler 1830 (Squamata: Colubridae)

Amphibia-Reptilia

(2002)

H.W. Greene

Scale overlap, a directional sign stimulus for prey ingestion by ophiophagous snakes

Z. Tierpsychol.

(1976)

H.W. Greene

Dietary correlates of the origin and radiation of snakes

Am. Zool.

(1983)

Cited by (37)

Snakes as bimonitors of environmental pollution: A review on organic contaminants
2021, Science of the Total Environment
Citation Excerpt :
However, little is known about negative effects of the vast majority of organic pollutants in snakes, and ecotoxicology reference values specifically derived for these reptiles are still lacking. Snakes and snake eggs are potential food of birds of prey (e.g., buzzards, eagles, hawks, herons, and owls), mammals (e.g., cats, coyotes, foxes, honey badgers, mongooses, opossums, raccoons, skunks, and wild boars), large fish (e.g., sharks) and crustaceans (e.g., manicou crabs), and bigger snakes (Lyle and Timms, 1987; Jackson and Mirick, 1993; Maitland, 2003; Jackson et al., 2004; Tashiro et al., 2020). Therefore, snakes contaminated with organic pollutants are exposure sources of these substances in their predators.
Monitoring data on organic pollutants published between the late 1960s and 2020 are reviewed to provide comprehensive and updated insights into their bioaccumulation characteristics, sources, and fate in snakes. Multiple organic pollutant classes including pesticides, polychlorinated biphenyls, chlorinated paraffins, dioxin-related compounds, alkanes, polycyclic aromatic hydrocarbons, flame retardants, plasticizers, etc., were detected in various aquatic and terrestrial snake species with concentrations and patterns varying between species and locations. In general, higher concentrations of organic pollutants were found in snakes collected from contaminated sites (e.g., densely populated, pesticide-treated, and waste processing areas), suggesting that snakes can serve as good biomonitors of environmental pollution caused by organic contaminants. Factors influencing concentrations and patterns of organic pollutants in snakes are discussed, providing an overview of current understanding about their accumulation, transformation, and elimination processes. Potential negative effects associated with organic pollutants in snakes and their predators are also considered. Based on such discussions, research gaps and future perspectives on the utilization of snake biomonitoring studies are addressed, heading towards an effective monitoring and assessment scheme for a variety of legacy and emerging organic pollutants in the environment.
Ontogenetic shifts and spatial associations in organ positions for snakes
2015, Zoology
Citation Excerpt :
An explanation for their more distal small intestine compared to other colubrids and to P. molurus and B. constrictor may stem from the fact that M. flagellum and L. getula feed on other snakes (Wright and Wright, 1957; Greene, 1997). A relatively longer esophagus and stomach and thus a more distally positioned small intestine may be a structural adaptation for ingesting long prey items such as snakes (Jackson et al., 2004). The relative position of the right kidney likewise did not separate out between colubrids and non-colubrids.
Snakes possess an elongated body form and serial placement of organs which provides the opportunity to explore historic and adaptive mechanisms of organ position. We examined the influence of body size and sex on the position of, and spatial associations between, the heart, liver, small intestine, and right kidney for ten phylogenetically diverse species of snakes that vary in body shape and habitat. Snake snout–vent length explained much of the variation in the position of these four organs. For all ten species, the position of the heart and liver relative to snout–vent length decreased as a function of size. As body size increased from neonate to adult, these two organs shifted anteriorly an average of 4.7% and 5.7% of snout–vent length, respectively. Similarly, the small intestine and right kidney shifted anteriorly with an increase in snout–vent length for seven and five of the species, respectively. The absolute and relative positioning of these organs did not differ between male and female Burmese pythons (Python molurus). However, for diamondback water snakes (Nerodia rhombifer), the liver and small intestine were more anteriorly positioned in females as compared to males, whereas the right kidney was positioned more anteriorly for males. Correlations of residuals of organ position (deviation from predicted position) demonstrated significant spatial associations between organs for nine of the ten species. For seven species, individuals with hearts more anterior (or posterior) than predicted also tended to possess livers that were similarly anteriorly (or posteriorly) placed. Positive associations between liver and small intestine positions and between small intestine and right kidney positions were observed for six species, while spatial associations between the heart and small intestine, heart and right kidney, and liver and right kidney were observed in three or four species. This study demonstrates that size, sex, and spatial associations may have potential interacting effects when testing evolutionary scenarios for the position of snake organs.
Effects of feeding on luminal pH and morphology of the gastroesophageal junction of snakes
2012, Zoology
Citation Excerpt :
In contrast to the esophagus in mammals, the straight and elongated esophagus of snakes joins the stomach with no apparent LES or barrier mechanism between the two organs (Luppa, 1977; Helmstetter et al., 2009). Whereas for most vertebrates (with the exception of birds that possess crops) the consumed meal is passed in its entirety into the stomach, the large and elongated meal of snakes will fill not only their stomach but extend into their esophagus (Pope, 1961; Greene, 1997; Jackson et al., 2004). Another seemingly unique feature among snakes is their ability to dramatically regulate gastric acid secretion and gastric luminal pH. For those few species examined, gastric acid production is literally shut down with the emptying of the stomach, allowing luminal pH to increase to ∼7 (Secor, 2003; Cox and Secor, 2010).
At the gastroesophageal junction, most vertebrates possess a functional lower esophageal sphincter (LES) which may serve to regulate the passage of liquids and food into the stomach and prevent the reflux of gastric contents into the esophagus. Snakes seemingly lack an LES and consume meals large enough to extend anteriorly from the stomach into the esophagus thereby providing the opportunity for the reflux of gastric juices. To explore whether snakes experience or can prevent gastric reflux, we examined post-feeding changes of luminal pH of the distal esophagus and stomach, the fine scale luminal pH profile at the gastroesophageal junction, and the morphology of the gastroesophageal junction for the Burmese python (Python molurus), the African brown house snake (Lamprophis fuliginosus), and the diamondback water snake (Nerodia rhombifer). For each species fasted, there was no distension of the gastroesophageal junction and only modest changes in luminal pH from the distal esophagus into the stomach. Feeding resulted in marked distension and changes in tissue morphology of the gastroesophageal junction. Simultaneously, there was a significant decrease in luminal pH of the distal esophagus for pythons and house snakes, and for all three species a steep gradient in luminal pH decreasing across a 3-cm span from the distal edge of the esophagus into the proximal edge of the stomach. The moderate acidification of the distalmost portion of the esophagus for pythons and house snakes suggests that there is some anterior movement of gastric juices across the gastroesophageal junction. Given that this modest reflux of gastric fluid is localized to the most distal region of the esophagus, snakes are apparently able to prevent and protect against acid reflux in the absence of a functional LES.
Heavy, Bulky, or Both: What Does “Large Prey” Mean to Snakes?
2023, Journal of Herpetology
The interaction of tooth shape and strike kinematics in the role of prey capture
2023, Snakes: Morphology, Function, and Ecology
OBSERVATION OF OPHIOPHAGY AND POSSIBLE ARBORAL BEHAVIOR IN MICRURUS DISTANS (SQUAMATA: ELAPIDAE) ON LEPTODEIRA SEPTENTRIONALIS (SQUAMATA: DIPSADIDAE) AND COMMENTS ON ITS DISTRIBUTION IN SINALOA, MEXICO
2023, Revista Latinoamericana de Herpetologia

View all citing articles on Scopus

View full text

How snakes eat snakes: the biomechanical challenges of ophiophagy for the California kingsnake, Lampropeltis getula californiae (Serpentes: Colubridae)

Abstract

Introduction

Section snippets

Materials and methods

Results

Discussion

Acknowledgements

Zoology

Comp. Biochem. Physiol.

Cranial kinetics of the generalized colubrid snake Elaphe obsolete quadrivittata. I. Descriptive morphology

J. Morphol.

Cranial kinetics of the generalized colubrid snake Elaphe obsolete quadrivittata. II. Functional morphology

J. Morphol.

The emetic reflex in a reptile (Crocodylus porosus)

J. Exp. Biol.

L’anatomie du genre Ptyas a Java

Riv. Biol. Colon.

The anatomy of Cylindrophis rufus (Laur.). I and II

Proc. Kon. Ned. Akad. Wet. Ser. C

The anatomy of Xenopeltis unicolor

Zool. Meded.

The anatomy of the Acrochordinae. I, II, III and IV

Proc. Kon. Ned. Akad. Wet. Ser. C

The anatomie of some Homalopsinae

Biol. Jaarb.

The anatomy of some Viperidae. I, II and III

Acta Morphol. Neerl.-Scand.

Die Anatomie der Elapinae

Z. Wiss. Zool.

A study of digestive phenomena in snakes with the aid of the Roentgen ray

Am. J. Roentgenol. Radium Ther.

The functional anatomy of the head of the puff adder, Bitis arietans (Merr.)

J. Morphol.

Bitis caudalis (Horned Adder). Prey size

Herpetol. Rev.

Activity of head muscles during feeding by snakesa comparative study

Am. Zool.

Snakes of the World

Clearing and staining small vertebrates, in toto, for demonstrating ossification

Turtox News

Studies on the morphology and function of the skull in the Boidae (Serpentes). Part II. Morphology and function of the jaw apparatus in Python sebae and Python molurus

J. Morphol.

Biomedical and Surgical Aspects of Captive Reptile Husbandry

The functional morphology of the egg-eating adaptations in the snake genus Dasypeltis

Zoologica

BiomechanicsAn Approach to Vertebrate Biology

The feeding behaviour of the snail-eating snake Pareas carinatus Wagler 1830 (Squamata: Colubridae)

Amphibia-Reptilia

Scale overlap, a directional sign stimulus for prey ingestion by ophiophagous snakes

Z. Tierpsychol.

Dietary correlates of the origin and radiation of snakes

Am. Zool.