Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Edited by David B. Wake, University of California, Berkeley, CA, and approved March 22, 2011 (received for review January 31, 2011)
Abstract
The independent evolutionary origin of a complex trait, within a lineage otherwise lacking it, provides a powerful opportunity to test hypotheses on selective forces. Territorial defense of an area containing resources (such as food or shelter) is widespread in lizards but not snakes. Our studies on an insular population of Taiwanese kukrisnakes (Oligodon formosanus) show that females of this species actively defend sea turtle nests by repelling conspecifics for long periods (weeks) until the turtle eggs hatch or are consumed. A clutch of turtle eggs comprises a large, long-lasting food resource, unlike the prey types exploited by other types of snakes. Snakes of this species have formidable weaponry (massively enlarged teeth that are used for slitting eggshells), and when threatened, these snakes wave their tails toward the aggressor (an apparent case of head-tail mimicry). Bites to the tail during intraspecific combat bouts thus can have high fitness costs for males (because the hemipenes are housed in the tail). In combination, unusual features of the species (ability to inflict severe damage to male conspecifics) and the local environment (a persistent prey resource, large relative to the snakes consuming it) render resource defense both feasible and advantageous for female kukrisnakes. The (apparently unique) evolution of territorial behavior in this snake species thus provides strong support for the hypothesis that resource defensibility is critical to the evolution of territoriality.
One of the primary tasks of evolutionary biology is to identify the selective forces and environmental circumstances that promote the evolution of specific traits. Paradoxically, widespread traits can be among the most difficult to interpret in terms of selective forces, because the current distribution of such a trait may provide little insight into the conditions under which it arose. In such cases, we may learn more from looking at the trait in lineages where it is rare than in ones where it is ubiquitous. For example, the selective forces responsible for the evolution of viviparity (live-bearing) and parental care in mammals are obscure, because the virtual ubiquity of these traits in living mammals likely results from a single ancient evolutionary origin of the trait in each case (1). Squamate reptiles offer more robust opportunities for analysis of the initial selective forces favoring these traits, because both viviparity and parental care are the exception rather than the rule among reptiles, and there have been many independent evolutionary origins of both traits (2, 3).
A similar situation arises when we attempt to identify the circumstances surrounding evolutionary shifts in social systems. One of the most widespread systems is territoriality, involving the active defense of a specific area (i.e., exclusion of conspecifics) by one or more individuals (4). The defended sites typically are centered around critical resources such as food supply, shelter, or mating opportunities (5). Territoriality can enhance fitness of an individual by providing more-or-less exclusive access to the resource in question (6). Mathematical models suggest that territoriality should evolve when the benefits of exclusive access to the resource outweigh the costs (risks, energy, time) required to detect and repel rivals; empirical measures of such costs and benefits in territorial species generally support that conceptual framework (7, 8).
Territorial defense of sites containing critical resources has evolved independently in many phylogenetic lineages of organisms, ranging from invertebrates to mammals (9, 10). However, territoriality is rare or absent in some types of animals. For example, among the major lineages of terrestrial vertebrates, territorial social systems are common in many birds, mammals, lizards, frogs, and salamanders, but they have never been reported in snakes (11). Although males of some snake species fight for access to receptive females, territoriality in the sense of prolonged area defense is unknown among ≈2,700 species of living serpents (11–14). A likely reason for this striking disparity between lizards and snakes involves their trophic ecology; most lizards consume small prey (and, thus, a defensibly sized area may contain enough resources to support an individual predator), whereas most snakes take relatively large prey and feed infrequently (and, thus, may have to move extensively to locate enough edible items). Theory also suggests that when only a subset of individuals within a population exhibits territoriality, the identity of that group will be determined by their territory-holding potential, for example, their ability to defeat rivals in combat (15).
In the course of fieldwork on a tropical Asian island, one of us (W.-S.H.) discovered territorial behavior in a snake species. The apparent lack of territoriality in other snake species means that this case provides a robust opportunity to test predictions about the environmental features (notably, a defensible food resource) and species attributes (notably, intraspecific variation in resource-holding potential) thought to facilitate the evolution of territoriality.
Results
Sequence of Arrival of Snakes at Turtle Nests.
We observed 105 green sea turtle nests being laid and captured 413 kukrisnakes (274 adult males, 139 adult females) a total of 819 times. Marked snakes searched for nests at dawn and at sunset, continuing after dark. Nests on which we conducted focal observations were located by snakes 0.5–8.5 h (n = 17) after the female turtle had finished covering the nest (Table 1). Male snakes were the first to arrive at all 17 nests (Table 1; against a null hypothesis of equal numbers of each sex, χ2 = 17.0, 1 df, P < 0.0001). This trend for males to arrive first cannot be due simply to male snakes outnumbering females in the overall beach population [see above, sex of first arriver against a null hypothesis of 66% male (as in our capture sample), χ2 = 8.76, 1 df, P < 0.001].
View this table:
Table 1.
The duration of delays between oviposition by sea turtles (C. mydas,
) and the arrival of male (♂), female (♀), and juvenile (J) kukrisnakes (O. formosanus) at 17 turtle nests during a 12-h period after egg laying by turtles
Fate of Turtle Nests Subject to Predation.
Surviving turtle eggs hatched 50–60 d after deposition (n = 62 nests). When we dug into nests soon after most hatchlings had left, we always found a single female snake and several unfertilized turtle eggs (mean ± SE = 10.2 ± 2.0 eggs, n = 12 nests). After we recovered those nests, the female snakes dug burrows to the surface (mean length = 46 cm) and were seen with their heads protruding from the resulting holes (3.4 ± 0.4 cm in diameter; occupancy duration 8–22 d, mean = 12 d, n = 30). After those females left, we confirmed that all unfertilized eggs had been consumed.
Behavior of Snakes After Arrival at the Nest.
The behavior of kukrisnakes arriving at a turtle nest differed between the sexes and depended on order of arrival. When all snakes arriving at a nest were male, they entered the nest and remained within it, presumably feeding on eggs (time between arrival of the first snake and final abandonment of the nest by all snakes: range 5–24 h, mean = 7 h, n = 35 nests). When males arrived first, and outnumbered females, all of the turtle eggs in a nest were consumed rapidly (in three nests where we had accurate records of snake arrival and departure, all snakes departed within 5 d, no new snakes entered the nest after that time, and excavation of these nests confirmed that all eggs had been consumed).
As soon as female snakes arrived at a nest, we saw other snakes being forcefully expelled (as inferred by rapid retreat, sometimes with fresh wounds). Males that had been expelled often remained nearby and tried to reenter nests (n = 82 of 105 that were watched). The probability that a late-arriving male would remain within a nest was lower if a female snake was already present in the nest (2 of 22, = 9%) than if no female snakes were present in the nest (20 of 25 = 80%; χ2 = 23.6, 1 df, P < 0.0001).
Forced Introduction Trials.
Of 26 trials in which we added snakes forcefully to nests containing 1–5 females, the probability that the snakes we added would remain inside the nest for at least 30 min was high in the case of juveniles and adult females (23 of 26 trials, in both cases) but 0 of 26 for adult male snakes. That is, juveniles and other females, but not males, often were able to remain in the nest despite the presence of a resident female snake (χ2 = 40.9, 1 df, P < 0.0001). These experiments also provided direct observations of snakes attacking each other. Because threatened kukrisnakes present a coiled tail toward an adversary, the tail is often bitten by the other snake during intraspecific encounters (Fig. 1A). We observed snakes emerge from turtle nests with fresh cuts on their tails (Fig. 1D).
Fig. 1.
Territorial defense of sea turtle nests by kukrisnakes on Orchid Island, Taiwan. (A) A male snake waves its tail at conspecifics during a combat bout. (B) A female missing a substantial portion of its tail, which has been severed near the cloaca. (C) An early-arriving male kukrisnake entering a turtle nest. (D) Three males (two exhibiting fresh injuries to the tail) that had been expelled by a female conspecific and were lingering outside the nest. (E) Five female snakes that dug a burrow above a sea turtle nest and defended the area against other snakes. (F) The remains of 102 turtle eggs that were consumed inside a single nest over a 5-d period.
Field-Enclosure Trials.
Our field-enclosure experiment provided further evidence that female kukrisnakes repel males. In 14 trials that began with one male plus one female, the male left the nest in all 14 cases. In contrast, only two snakes left the nest in 14 trials involving two female snakes, and only five snakes departed in 14 trials involving two male snakes (χ2 = 17.5, 2 df, P < 0.001).
Correlates of Tail Injury.
The potential effects of tail injury on fitness are greater for male snakes than for females. Not only are the hemipenes housed within the tail (taking up the anterior-most 21% of the tail length, based on dissections of eight museum specimens), but these structures may be at particular risk because male kukrisnakes evert their hemipenes during the defensive tail display (16). In keeping with this putative sex difference in vulnerability, loss of >45% of the tail was more common in female kukrisnakes than in males (52 of 139 = 38% vs. 69 of 274 = 25%, Wald χ2 from logistic regression = 15.06, P < 0.001; Fig. 2). Severe truncation of the tail was especially common in very large females, but not males (main effect of SVL χ2 = 1.56, P = 0.21; interaction sex × SVL χ2 = 12.44, P < 0.001). In 14 cases, large female snakes had lost almost all of their tails (Fig. 2); a male snake losing so much of its tail would have lost its hemipenes (and, thus, reproductive capacity) also.
Fig. 2.
Patterns of tail loss due to injury in kukrisnakes, O. formosanus, from a field study on Orchid Island. The graph shows data for tail length relative to snout-vent length separately for the two sexes and for individuals with intact tails versus tails that have been truncated by injury. F-TSL, female, tail truncated; F-n, female, tail intact; M-TSL, male, tail truncated; T-n, male, tail intact.
Tail injuries were more frequent in snakes from Orchid Island (52 females and 69 males, totaling 121 of 413 individuals) than in conspecific specimens from Taiwan and mainland Asia examined in museum collections (3 of 48; Wald χ2 = 9.09, 1 df, P = 0.003). Moreover, most tail injuries in snakes from the mainland comprised relatively minor scarring, whereas tail injuries were often severe in Orchid Island snakes.
Discussion
Females in an island population of Taiwan kukrisnakes vigorously defend sea turtle eggs against conspecifics, over a period of up to several weeks. Territoriality (site defense) is rare in snakes, although anecdotal reports on African elapids and psammophines (17, 18) suggest that other snake taxa also may exhibit territorial behavior; such possibilities warrant further investigation. Pending confirmation of other cases of territoriality in snakes (and even allowing for alternative phylogenetic hypotheses), the closest living relatives of Oligodon formosanus known to exhibit territoriality are scincomorph lizards that diverged from the snake clade in the Jurassic, >150 million years ago (19) (Fig. 3).
Fig. 3.
Evolution of territoriality mapped on a conventional phylogeny of lizards and snakes (modified from refs. 30 and 31); recent novel topologies mainly differ in placing iguanians as sister to anguimorphs plus snakes (19) and, thus, do not affect our conclusions about the loss and gain of territoriality in this group; number of species in parentheses). Bars show presence and origin (dark), the occurrence of territorial social systems (hatched), and the absence and loss (open) of territoriality, as inferred by MacClade (32).
First, we consider some caveats to our conclusions. Because the critical behaviors occur underground, some of our conclusions are based on inference rather than direct observation. For example, we attribute the higher incidence of tail injuries on Orchid Island snakes to intraspecific agonistic encounters, rather than to injuries inflicted by other kinds of predators. In support of that inference, there were no nocturnal snake predators in our study area, so that the presence of snakes emerging from turtle nests with fresh injuries to their tails provides strong evidence that those injuries were obtained from territory defenders. The higher incidence of tail injuries in Orchid Island snakes (the only ones known to eat turtle eggs) also fits with this interpretation, as do our observations of combat bouts between snakes during the trials where we induced snakes to enter already-occupied turtle nests.
The apparently unique occurrence of territorial site defense in female kukrisnakes accords well with predictions of theoretical models based on (i) the economic defensibility of resources and (ii) the ability to repel conspecific competitors. Below, we consider these two issues in turn. For Taiwanese kukrisnakes, a sea turtle nest comprises a massive prey resource that can be accessed for weeks after its initial discovery. At one nest that we opened before and after snake predation, five snakes consumed 102 eggs in 5 d. Even allowing 50% loss for shells and spillage, an average nest of 105 45-g eggs (20) would allow five snakes (averaging 117 g each) to consume four times their own mass. The relatively small area of the nest facilitates surveillance and deterrence of conspecific intruders. We are not aware of any other snake species whose feeding ecology would provide such a direct energetic reward for expulsion of rival conspecifics. Turtle eggs are (i) large food items, (ii) highly clumped in occurrence, (iii) sedentary, (iv) not maternally defended, and (v) remain edible for long periods of time. Plant material frequently satisfies all of these criteria (e.g., one could imagine an herbivorous iguana defending a tree with edible leaves), but all snakes are carnivores (11). The only snake prey types that would provide a continuing food resource are clutches of eggs, but although eggs are commonly eaten by snakes (21), a single clutch generally contains too little food to support a snake for a long period.
The eggs and larvae of social insects meet most of the criteria outlined above and are used by “blindsnakes” (Scolecophidians), a fossorial taxon with reduced eyes and highly specialized mouthparts for ingestion of these tiny prey items (11, 22). However, those trophic specializations mean that blindsnakes lack the second precondition for the evolution of resource defense: weaponry capable of repelling intraspecific competitors. It is difficult to imagine a scolecophidian inflicting any kind of injury on another snake. In contrast, the formidably enlarged maxillary teeth of O. formosanus can cause deep slashing wounds (H.W.G., personal observation). Enlarged maxillary teeth are common in snakes that consume reptile eggs and have evolved convergently in several lineages (23). Oophagy and enlarged rear teeth are widespread in the kukrisnake lineage and related genera e.g., Stegonotus (24). Coincidentally then, the prey resource allowing economic defensibility (a large clutch of unattended reptile eggs) also has favored the evolution of a specialized dentition that facilitates a snake's capacity to exclude conspecifics by the ability to inflict severe wounds during combat bouts.
One interesting pattern is that territorial defense is exhibited by female kukrisnakes rather than by the larger and more numerous males. Sex differences in the fitness costs of intraspecific fighting likely explain this pattern. Kukrisnakes show an unusual stereotyped display during intraspecific combat, involving tail-waving toward the adversary as well as hemipenial eversion in males (16). Damage to the tail from the enlarged teeth of a rival kukrisnake thus could be far more costly to a male than a female; even if the hemipenes are not injured directly, a reduction in tail length might severely compromise mating success (25, 26). In contrast, damage to the short slender tail of a female would not greatly impede her movement or reproduction. Unusual circumstances thus have favored this surprising evolution of territorial behavior (Fig. 3), such that only females can defend a long-lasting and abundant supply of food with little additional cost. The apparent inability of males to remain in nests with territorial females may have favored active searching by males for newly laid (and hence unoccupied) nests, resulting in a strong trend for males to find nests before females.
On a more general note, the occurrence of territoriality in a single population of snakes, within a clade of ≈2,700 species of otherwise nonterritorial serpents (Fig. 3), underscores the fragility of current generalizations about social systems, even in well-studied taxa such as terrestrial vertebrates. Future studies, especially on the species-rich biota of tropical regions, undoubtedly will reveal yet more examples of behavioral and social diversity. Species such as the kukrisnakes of Orchid Island, where a single taxon within a diverse taxonomic group displays the independent evolution of a complex trait, provide robust opportunities to test the validity of existing explanatory schemes for such traits.
Methods
Study Area and Species.
Orchid (Lanyu) Island lies off the southeastern coast of Taiwan and experiences a tropical climate (20). The study beach is bordered by a sand dune that is vegetated by patches of mixed false pineapple (Pandanus odoratissimus) interspersed with silver-grass (Miscanthus floridulus) and saddle vine (Ipomoea pescaprae). Nesting green sea turtles (Chelonia mydas) lay their eggs between the dune and the open beach from May to October, with female turtles digging relatively deep nests (mean = 65 cm from ground surface to uppermost egg, 130 cm to lowermost egg: T-H. Chen, personal communication) in which they deposit their eggs (mean = 105 eggs per clutch, range 44–162; mean egg mass 45 g, range 39–50 g; ref. 20). The eggs are laid at a very early stage of embryogenesis, and incubation requires ≈8 wk at an average temperature of 29.2 °C (27).
A snake (the Taiwanese kukrisnake, O. formosanus) enters these turtle nests (often, soon after the eggs are laid) and consumes the contents of eggs, using its elongated rear teeth (which give it the name “kukri” snake, after the distinctively shaped knife used by Nepalese Gurkha soldiers; ref. 28) to slit the shell and provide access to the yolk (29). Taiwanese kukrisnakes are medium-sized [females to 48.9 ± 0.6 cm snout-vent length (SVL), males to 51.8 ± 0.4 cm SVL; ref. 20] with a broad geographic distribution over southern China and northern Vietnam; however, consumption of sea turtle eggs has been reported only in the Orchid Island population (20).
Data Collection.
We conducted a behavioral study on a 1,800-m2 section of beach on the island (22°03′N, 121°33′E) between May and October (the turtle nesting season on the beach) from 1997 to 2007. The study site was visited three to eight times per day from May to August, with briefer visits (7 d per month) in September and October. On each visit, we captured snakes and recorded their sex by hemipenial eversion and tail shape (to accommodate the paired hemipenes, males have longer and stouter tails than females at the same body length; ref. 20). Body size (snout-vent length and tail length) was determined with a tape measure (±1 mm). Tails were examined for injuries; these snakes wave their tails at conspecifics during combat bouts (Fig. 1A) and intense combat can result in major slashing injuries from the elongate rear teeth (see Fig. 1B). Each snake was marked with a PIT tag inserted between the trunk muscles and skin. Snakes were weighed with an electronic balance (±0.01 g), and then released at their sites of capture.
Our frequent visits meant that we were present when many turtles were nesting and, thus, were able to record the timing and sequence of arrival of snakes at those nests during and after the turtle oviposition period. Typically, arriving snakes immediately began to burrow down into the nest chamber (Fig. 1C); later-arriving conspecifics that also attempted to enter the nest (using burrows dug by earlier-arriving animals) often were repelled by resident snakes (as indicated by rapid retreat from the burrow, sometimes with fresh tail-wounds; Fig. 1D). We continued to monitor the turtle nests until turtle hatchlings had left, and then we dug into the nest, recorded the total number of unfertilized eggs, and examined any remaining snakes. We then recovered the nest and observed it until the snakes dug their way out from the nest. We recorded the depth of each sea turtle nest and snake burrow, as well as the number of snakes in each burrow.
To confirm that the apparent repulsion of later-arriving snakes was due to the presence of earlier-arriving conspecifics (especially females, see below), we conducted experimental trials (n = 26 burrows) by introducing 1–4 males, females, or juveniles into burrows already inhabited by females, then recording the outcome of the encounter (whether the “intruder” remained within the nest for at least 30 min; Fig. 1E). We also built 42 field cages (1 × 1 m, with one sea turtle egg buried within a chamber 10 cm below the sand surface) and released combinations of snakes (14 cages in each treatment: 1 male plus 1 female, 2 males, or 2 females) into the cage to test the hypothesis of territorial exclusion by females.
To compare the incidence of tail injuries (likely sustained during intraspecific combat bouts; see Fig. 1B and below) between Orchid Island snakes and conspecifics from other parts of the species’ range, we examined preserved specimens in collections of the American Museum of Natural History, the California Academy of Sciences, the Museum of Vertebrate Zoology at the University of California Berkeley, the National Taiwan Museum, and the Taiwan Endemic Species Research Institute.
Statistical Analyses.
We used goodness-of-fit analyses to evaluate differences in arrival time to turtle nests between male and female snakes and to evaluate whether the prior presence of either a male or female snake affected the probability of a later-arriving snake (either male or female) leaving the nest soon after it entered (presumably as a result of territorial defense by resident snakes). To test the hypothesis that the presence of a female snake deterred other snakes from entering a turtle nest, χ2 statistics from a test of independence were used to compare the number of snakes leaving a freshly laid turtle nest in equivalent periods (of 30 min each) immediately after female snakes had arrived, versus at other times when no females had arrived. A goodness-of-fit test was also used to test the hypothesis of territorial exclusion by females in field-enclosure trials. We used logistic regression (based on the binomial distribution and logic link function) with SVL and sex as independent variables, and tail damage as the dependent variable, to test the hypothesis that the incidence of tail damage was influenced by an interaction between a snake's sex and its body size. We also used logistic regression to compare the incidence of tail injuries among kukrisnakes from Taiwan, mainland China, and Orchid Island populations and to compare the frequency of tail loss between sexes.
Acknowledgments
We thank C. H. Chang, R. K. Lee, and several assistants for helping W-S.H. in the field; C. C. Austin, K. Adler, A. Mori, H. Ota, and K. R. Zamudio for assistance with the manuscript; and C. J. Cole, R. Drews, J. Vindum, and J. T. Lin for permission to examine specimens in their care. The work was conducted under animal ethics permit NMNSHP97-001 and was supported by the Kuo Wu Hsiu Luan Culture and Education Foundation and the National Museum of Natural Science, Taiwan, by the National Science Council 99-2621-B-178-001-MY3, Taiwan, and by the Australian Research Council.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: rick.shine{at}sydney.edu.au.
Author contributions: W.-S.H., H.W.G., and T.-J.C. designed research; W.-S.H. performed research; W.-S.H., T.-J.C., and R.S. analyzed data; and W.-S.H., H.W.G., and R.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Freely available online through the PNAS open access option.
References
Territorial behavior in Taiwanese kukrisnakes (Oligodon formosanus)
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