Territorial behavior in Taiwanese kukrisnakes ( formosanus)

Wen-San Huanga,b, Harry W. Greeneb, Tien-Jye Changc, and Richard Shined,1 aDepartment of Zoology, National Museum of Natural Science, Taichung 404, ; bDepartment of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853-2701; cDepartment of Veterinary Medicine, National Chung Hsing University, Taichung 402, Taiwan; and dBiological Sciences A08, University of Sydney, Sydney, NSW 2006, Australia

Edited by David B. Wake, University of California, Berkeley, CA, and approved March 22, 2011 (received for review January 31, 2011) The independent evolutionary origin of a complex trait, within a repel rivals; empirical measures of such costs and benefits in ter- lineage otherwise lacking it, provides a powerful opportunity to ritorial species generally support that conceptual framework (7, 8). test hypotheses on selective forces. Territorial defense of an area Territorial defense of sites containing critical resources has containing resources (such as food or shelter) is widespread in evolved independently in many phylogenetic lineages of organ- lizards but not . Our studies on an insular population of isms, ranging from invertebrates to mammals (9, 10). However, Taiwanese kukrisnakes (Oligodon formosanus) show that females territoriality is rare or absent in some types of . For ex- of this species actively defend sea turtle nests by repelling con- ample, among the major lineages of terrestrial vertebrates, terri- fi speci cs for long periods (weeks) until the turtle eggs hatch or are torial social systems are common in many birds, mammals, lizards, consumed. A clutch of turtle eggs comprises a large, long-lasting frogs, and salamanders, but they have never been reported in food resource, unlike the prey types exploited by other types of snakes (11). Although males of some species fight for access snakes. Snakes of this species have formidable weaponry (mas- to receptive females, territoriality in the sense of prolonged area sively enlarged teeth that are used for slitting eggshells), and defense is unknown among ≈2,700 species of living serpents (11– when threatened, these snakes wave their tails toward the ag- gressor (an apparent case of head-tail mimicry). Bites to the tail 14). A likely reason for this striking disparity between lizards and during intraspecific combat bouts thus can have high fitness costs snakes involves their trophic ecology; most lizards consume small for males (because the hemipenes are housed in the tail). In com- prey (and, thus, a defensibly sized area may contain enough bination, unusual features of the species (ability to inflict severe resources to support an individual predator), whereas most snakes damage to male conspecifics) and the local environment (a persis- take relatively large prey and feed infrequently (and, thus, may tent prey resource, large relative to the snakes consuming it) ren- have to move extensively to locate enough edible items). Theory der resource defense both feasible and advantageous for female also suggests that when only a subset of individuals within a pop- kukrisnakes. The (apparently unique) evolution of territorial be- ulation exhibits territoriality, the identity of that group will be havior in this snake species thus provides strong support for the determined by their territory-holding potential, for example, their hypothesis that resource defensibility is critical to the evolution ability to defeat rivals in combat (15). of territoriality. In the course of fieldwork on a tropical Asian island, one of us (W.-S.H.) discovered territorial behavior in a snake species. The | sociality | economic defensibility | social system apparent lack of territoriality in other snake species means that this case provides a robust opportunity to test predictions about ne of the primary tasks of evolutionary biology is to identify the environmental features (notably, a defensible food resource) Othe selective forces and environmental circumstances that and species attributes (notably, intraspecific variation in re- promote the evolution of specific traits. Paradoxically, widespread source-holding potential) thought to facilitate the evolution of traits can be among the most difficult to interpret in terms of territoriality. selective forces, because the current distribution of such a trait Results may provide little insight into the conditions under which it arose. In such cases, we may learn more from looking at the trait in Sequence of Arrival of Snakes at Turtle Nests. We observed 105 lineages where it is rare than in ones where it is ubiquitous. For green sea turtle nests being laid and captured 413 kukrisnakes example, the selective forces responsible for the evolution of vi- (274 adult males, 139 adult females) a total of 819 times. Marked viparity (live-bearing) and parental care in mammals are obscure, snakes searched for nests at dawn and at sunset, continuing after because the virtual ubiquity of these traits in living mammals dark. Nests on which we conducted focal observations were lo- ECOLOGY likely results from a single ancient evolutionary origin of the trait cated by snakes 0.5–8.5 h (n = 17) after the female turtle had in each case (1). Squamate offer more robust opportu- finished covering the nest (Table 1). Male snakes were the first to nities for analysis of the initial selective forces favoring these arrive at all 17 nests (Table 1; against a null hypothesis of equal traits, because both viviparity and parental care are the exception numbers of each sex, χ2 = 17.0, 1 df, P < 0.0001). This trend for rather than the rule among reptiles, and there have been many males to arrive first cannot be due simply to male snakes out- independent evolutionary origins of both traits (2, 3). numbering females in the overall beach population [see above, A similar situation arises when we attempt to identify the cir- sex of first arriver against a null hypothesis of 66% male (as in cumstances surrounding evolutionary shifts in social systems. One our capture sample), χ2 = 8.76, 1 df, P < 0.001]. 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 Author contributions: W.-S.H., H.W.G., and T.-J.C. designed research; W.-S.H. performed around critical resources such as food supply, shelter, or mating research; W.-S.H., T.-J.C., and R.S. analyzed data; and W.-S.H., H.W.G., and R.S. wrote the opportunities (5). Territoriality can enhance fitness of an indi- paper. vidual by providing more-or-less exclusive access to the resource in The authors declare no conflict of interest. question (6). Mathematical models suggest that territoriality This article is a PNAS Direct Submission. should evolve when the benefits of exclusive access to the resource Freely available online through the PNAS open access option. outweigh the costs (risks, energy, time) required to detect and 1To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1101804108 PNAS | May 3, 2011 | vol. 108 | no. 18 | 7455–7459 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 snakes were present in the nest (20 of 25 = 80%; χ2 = 23.6, 1 df, hatched 50–60 d after deposition (n = 62 nests). When we dug into P < 0.0001). nests soon after most hatchlings had left, we always found a single female snake and several unfertilized turtle eggs (mean ± SE = Forced Introduction Trials. Of 26 trials in which we added snakes 10.2 ± 2.0 eggs, n = 12 nests). After we recovered those nests, the forcefully to nests containing 1–5 females, the probability that the female snakes dug burrows to the surface (mean length = 46 cm) snakes we added would remain inside the nest for at least 30 min and were seen with their heads protruding from the resulting holes was high in the case of juveniles and adult females (23 of 26 trials, (3.4 ± 0.4 cm in diameter; occupancy duration 8–22 d, mean = in both cases) but 0 of 26 for adult male snakes. That is, juveniles 12 d, n = 30). After those females left, we confirmed that all and other females, but not males, often were able to remain in the unfertilized eggs had been consumed. nest despite the presence of a resident female snake (χ2 = 40.9, 1 df, P < 0.0001). These experiments also provided direct ob- Behavior of Snakes After Arrival at the Nest. The behavior of kuk- servations of snakes attacking each other. Because threatened risnakes arriving at a turtle nest differed between the sexes and kukrisnakes present a coiled tail toward an adversary, the tail is depended on order of arrival. When all snakes arriving at a nest often bitten by the other snake during intraspecific encounters were male, they entered the nest and remained within it, pre- (Fig. 1A). We observed snakes emerge from turtle nests with fresh sumably feeding on eggs (time between arrival of the first snake cuts on their tails (Fig. 1D). and final abandonment of the nest by all snakes: range 5–24 h, mean = 7 h, n = 35 nests). When males arrived first, and out- Field-Enclosure Trials. Our field-enclosure experiment provided numbered females, all of the turtle eggs in a nest were consumed further evidence that female kukrisnakes repel males. In 14 trials rapidly (in three nests where we had accurate records of snake that began with one male plus one female, the male left the nest arrival and departure, all snakes departed within 5 d, no new in all 14 cases. In contrast, only two snakes left the nest in 14 snakes entered the nest after that time, and excavation of these trials involving two female snakes, and only five snakes departed nests confirmed that all eggs had been consumed). in 14 trials involving two male snakes (χ2 = 17.5, 2 df, P < 0.001). As soon as female snakes arrived at a nest, we saw other snakes being forcefully expelled (as inferred by rapid retreat, Correlates of Tail Injury. The potential effects of tail injury on sometimes with fresh wounds). Males that had been expelled fitness are greater for male snakes than for females. Not only are often remained nearby and tried to reenter nests (n = 82 of 105 the hemipenes housed within the tail (taking up the anterior- that were watched). The probability that a late-arriving male most 21% of the tail length, based on dissections of eight mu- would remain within a nest was lower if a female snake was al- seum specimens), but these structures may be at particular risk ready present in the nest (2 of 22, = 9%) than if no female because male kukrisnakes evert their hemipenes during the de-

7456 | www.pnas.org/cgi/doi/10.1073/pnas.1101804108 Huang et al. 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. fensive tail display (16). In keeping with this putative sex dif- Tail injuries were more frequent in snakes from Orchid Island ference in vulnerability, loss of >45% of the tail was more (52 females and 69 males, totaling 121 of 413 individuals) than in common in female kukrisnakes than in males (52 of 139 = 38% conspecific specimens from Taiwan and mainland Asia examined vs. 69 of 274 = 25%, Wald χ2 from logistic regression = 15.06, in museum collections (3 of 48; Wald χ2 = 9.09, 1 df, P=0.003). P < 0.001; Fig. 2). Severe truncation of the tail was especially Moreover, most tail injuries in snakes from the mainland com- common in very large females, but not males (main effect of SVL prised relatively minor scarring, whereas tail injuries were often χ2 = 1.56, P = 0.21; interaction sex × SVL χ2 = 12.44, P < severe in Orchid Island snakes. 0.001). In 14 cases, large female snakes had lost almost all of Discussion their tails (Fig. 2); a male snake losing so much of its tail would have lost its hemipenes (and, thus, reproductive capacity) also. Females in an island population of Taiwan kukrisnakes vigor- ously 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 psammo- phines (17, 18) suggest that other snake taxa also may exhibit ECOLOGY territorial behavior; such possibilities warrant further investi- gation. Pending confirmation of other cases of territoriality in snakes (and even allowing for alternative phylogenetic hypothe- ses), 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). 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 ex- ample, we attribute the higher incidence of tail injuries on Orchid Island snakes to intraspecific agonistic encounters, rather than to fl Fig. 2. Patterns of tail loss due to injury in kukrisnakes, O. formosanus, from injuries in icted by other kinds of predators. In support of that a field study on Orchid Island. The graph shows data for tail length relative to inference, there were no nocturnal snake predators in our study snout-vent length separately for the two sexes and for individuals with intact area, so that the presence of snakes emerging from turtle nests tails versus tails that have been truncated by injury. F-TSL, female, tail trun- with fresh injuries to their tails provides strong evidence that cated; F-n, female, tail intact; M-TSL, male, tail truncated; T-n, male, tail intact. those injuries were obtained from territory defenders. The higher

Huang et al. PNAS | May 3, 2011 | vol. 108 | no. 18 | 7457 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 ex- clude 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 nu- merous 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 cir- Fig. 3. Evolution of territoriality mapped on a conventional phylogeny of cumstances thus have favored this surprising evolution of terri- lizards and snakes (modified from refs. 30 and 31); recent novel topologies torial behavior (Fig. 3), such that only females can defend a long- mainly differ in placing iguanians as sister to anguimorphs plus snakes (19) lasting and abundant supply of food with little additional cost. and, thus, do not affect our conclusions about the loss and gain of territo- The apparent inability of males to remain in nests with territorial riality in this group; number of species in parentheses). Bars show presence females may have favored active searching by males for newly and origin (dark), the occurrence of territorial social systems (hatched), and laid (and hence unoccupied) nests, resulting in a strong trend for the absence and loss (open) of territoriality, as inferred by MacClade (32). males to find nests before females. On a more general note, the occurrence of territoriality in a ≈ incidence of tail injuries in Orchid Island snakes (the only ones single population of snakes, within a clade of 2,700 species known to eat turtle eggs) also fits with this interpretation, as do of otherwise nonterritorial serpents (Fig. 3), underscores the our observations of combat bouts between snakes during the trials fragility of current generalizations about social systems, even in where we induced snakes to enter already-occupied turtle nests. well-studied taxa such as terrestrial vertebrates. Future studies, The apparently unique occurrence of territorial site defense in especially on the species-rich biota of tropical regions, un- female kukrisnakes accords well with predictions of theoretical doubtedly will reveal yet more examples of behavioral and social models based on (i) the economic defensibility of resources and diversity. Species such as the kukrisnakes of Orchid Island, where (ii) the ability to repel conspecific competitors. Below, we con- a single taxon within a diverse taxonomic group displays the in- sider these two issues in turn. For Taiwanese kukrisnakes, a sea dependent evolution of a complex trait, provide robust opportu- turtle nest comprises a massive prey resource that can be nities to test the validity of existing explanatory schemes for accessed for weeks after its initial discovery. At one nest that we such traits. opened before and after snake predation, five snakes consumed Methods 102 eggs in 5 d. Even allowing 50% loss for shells and spillage, an fi Study Area and Species. Orchid (Lanyu) Island lies off the southeastern coast average nest of 105 45-g eggs (20) would allow ve snakes (av- of Taiwan and experiences a tropical climate (20). The study beach is bor- eraging 117 g each) to consume four times their own mass. The dered by a sand dune that is vegetated by patches of mixed false pineapple relatively small area of the nest facilitates surveillance and de- (Pandanus odoratissimus) interspersed with silver-grass (Miscanthus flo- terrence of conspecific intruders. We are not aware of any other ridulus) and saddle vine (Ipomoea pescaprae). Nesting green sea turtles snake species whose feeding ecology would provide such a direct (Chelonia mydas) lay their eggs between the dune and the open beach from energetic reward for expulsion of rival conspecifics. Turtle eggs May to October, with female turtles digging relatively deep nests (mean = 65 are (i) large food items, (ii) highly clumped in occurrence, (iii) cm from ground surface to uppermost egg, 130 cm to lowermost egg: T-H. sedentary, (iv) not maternally defended, and (v) remain edible 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. for long periods of time. Plant material frequently satisfies all of 20). The eggs are laid at a very early stage of embryogenesis, and incubation these criteria (e.g., one could imagine an herbivorous iguana requires ≈8 wk at an average temperature of 29.2 °C (27). defending a tree with edible leaves), but all snakes are carnivores A snake (the Taiwanese kukrisnake, O. formosanus) enters these turtle (11). The only snake prey types that would provide a continuing nests (often, soon after the eggs are laid) and consumes the contents of food resource are clutches of eggs, but although eggs are com- eggs, using its elongated rear teeth (which give it the name “kukri” snake, monly eaten by snakes (21), a single clutch generally contains too after the distinctively shaped knife used by Nepalese Gurkha soldiers; ref. 28) little food to support a snake for a long period. to slit the shell and provide access to the yolk (29). Taiwanese kukrisnakes The eggs and larvae of social insects meet most of the criteria are medium-sized [females to 48.9 ± 0.6 cm snout-vent length (SVL), males ± outlined above and are used by “blindsnakes” (Scolecophidians), to 51.8 0.4 cm SVL; ref. 20] with a broad geographic distribution over a fossorial taxon with reduced eyes and highly specialized mouth- southern and northern ; however, consumption of sea turtle eggs has been reported only in the Orchid Island population (20). parts for ingestion of these tiny prey items (11, 22). However, those trophic specializations mean that blindsnakes lack the second Data Collection. We conducted a behavioral study on a 1,800-m2 section of precondition for the evolution of resource defense: weaponry ca- beach on the island (22°03′N, 121°33′E) between May and October (the pable of repelling intraspecific competitors. It is difficult to imagine turtle nesting season on the beach) from 1997 to 2007. The study site was a scolecophidian inflicting any kind of injury on another snake. In visited three to eight times per day from May to August, with briefer visits

7458 | www.pnas.org/cgi/doi/10.1073/pnas.1101804108 Huang et al. (7 d per month) in September and October. On each visit, we captured snakes and conspecifics from other parts of the species’ range, we examined snakes and recorded their sex by hemipenial eversion and tail shape (to preserved specimens in collections of the American Museum of Natural accommodate the paired hemipenes, males have longer and stouter tails History, the California Academy of Sciences, the Museum of Vertebrate than females at the same body length; ref. 20). Body size (snout-vent length Zoology at the University of California Berkeley, the National Taiwan Mu- and tail length) was determined with a tape measure (±1 mm). Tails were seum, and the Taiwan Endemic Species Research Institute. examined for injuries; these snakes wave their tails at conspecifics during combat bouts (Fig. 1A) and intense combat can result in major slashing Statistical Analyses. We used goodness-of-fit analyses to evaluate differences 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 in arrival time to turtle nests between male and female snakes and to evaluate weighed with an electronic balance (±0.01 g), and then released at their whether the prior presence of either a male or female snake affected the sites of capture. probability of a later-arriving snake (either male or female) leaving the nest Our frequent visits meant that we were present when many turtles were soon after it entered (presumably as a result of territorial defense by resident nesting and, thus, were able to record the timing and sequence of arrival of snakes). To test the hypothesis that the presence of a female snake deterred snakes at those nests during and after the turtle oviposition period. Typically, other snakes from entering a turtle nest, χ2 statistics from a test of in- arriving snakes immediately began to burrow down into the nest chamber dependence were used to compare the number of snakes leaving a freshly (Fig. 1C); later-arriving conspecifics that also attempted to enter the nest laid turtle nest in equivalent periods (of 30 min each) immediately after fe- (using burrows dug by earlier-arriving animals) often were repelled by res- male snakes had arrived, versus at other times when no females had arrived. ident snakes (as indicated by rapid retreat from the burrow, sometimes with fi fresh tail-wounds; Fig. 1D). We continued to monitor the turtle nests until A goodness-of- t test was also used to test the hypothesis of territorial ex- fi turtle hatchlings had left, and then we dug into the nest, recorded the total clusion by females in eld-enclosure trials. We used logistic regression (based number of unfertilized eggs, and examined any remaining snakes. We then on the binomial distribution and logic link function) with SVL and sex as in- recovered the nest and observed it until the snakes dug their way out from dependent variables, and tail damage as the dependent variable, to test the the nest. We recorded the depth of each sea turtle nest and snake burrow, hypothesis that the incidence of tail damage was influenced by an interaction as well as the number of snakes in each burrow. between a snake’s sex and its body size. We also used logistic regression to fi To con rm that the apparent repulsion of later-arriving snakes was due to compare the incidence of tail injuries among kukrisnakes from Taiwan, the presence of earlier-arriving conspecifics (especially females, see below), mainland China, and Orchid Island populations and to compare the fre- we conducted experimental trials (n = 26 burrows) by introducing 1–4 males, quency of tail loss between sexes. females, or juveniles into burrows already inhabited by females, then re- cording 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 × 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 1 m, with one sea turtle egg buried within a chamber 10 cm below the sand K. R. Zamudio for assistance with the manuscript; and C. J. Cole, R. Drews, surface) and released combinations of snakes (14 cages in each treatment: 1 J. Vindum, and J. T. Lin for permission to examine specimens in their care. The male plus 1 female, 2 males, or 2 females) into the cage to test the hy- work was conducted under ethics permit NMNSHP97-001 and was pothesis of territorial exclusion by females. supported by the Kuo Wu Hsiu Luan Culture and Education Foundation and To compare the incidence of tail injuries (likely sustained during in- the National Museum of Natural Science, Taiwan, by the National Science traspecific combat bouts; see Fig. 1B and below) between Orchid Island Council 99-2621-B-178-001-MY3, Taiwan, and by the Australian Research Council.

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Huang et al. PNAS | May 3, 2011 | vol. 108 | no. 18 | 7459