Local Enhancement in Mud-Puddling Swallowtail Butterflies (Battus philenor and Papilio glaucus)

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1 Journal of Insect Behavior, Vol. 19, No. 6, November 2006 ( C 2006) DOI: /s Local Enhancement in Mud-Puddling Swallowtail Butterflies (Battus philenor and Papilio glaucus) G.W. Otis, 1,2 B. Locke, 1 N.G. McKenzie, 1 D. Cheung, 1 E. MacLeod, 1 P. Careless, 1 and A. Kwoon 1 Revised June 26, 2006; accepted December 22, 2006 Published online: December 2, 2006 Male butterflies aggregate at moist soil to acquire nutrients, a phenomenon termed mud-puddling. We studied the attraction of free-flying Papilio glaucus and Battus philenor swallowtails to dead decoys of those two species at artificial puddles moistened with NaCl solution. Both species landed preferentially at puddles with a decoy present rather than at unbaited puddles, demonstrating very strong local enhancement, a form of social facilitation. Papilio glaucus were attracted only to intraspecific decoys, whereas Battus philenor exhibited both intraspecific and interspecific attraction. Circular discs cut from the hindwings of male Battus were highly attractive to male Battus but completely unattractive to Papilio glaucus. The visual cues attractive to males in their search for salts differ between these two swallowtail species for unexplained reasons. KEY WORDS: local enhancement; social facilitation; butterfly ecology; puddling; sodium. INTRODUCTION Social facilitation is a phenomenon by which the behavior of an organism is initiated, or increased in frequency or intensity, due to the presence of others performing the same behavior (Clayton, 1978). The principle benefits of socially facilitated behavior in group-living animals are efficient exploita- 1 Department of Environmental Biology, University of Guelph, Guelph, Ontario, N1G 2W1 Canada. 2 To whome correspondence should be addressed. gotis@uoguelph.ca /06/ /1 C 2006 Springer Science+Business Media, LLC

2 686 Otis et al. tion of food resources, protection from predators through the formation of aggregations, and synchronization of breeding (Clayton, 1978). In insects, local enhancement, a form of social facilitation in which an individual is attracted to a specific location by the presence or actions of other organisms, often increases the fitness of the individual exhibiting the behavior. This occurs most frequently by enhancing the rate of finding and/or acquiring resources, but has also been documented to increase predator avoidance by both increased vigilance and a dilution effect, to decrease the susceptibility to dehydration, and to increase the strength of the warning signal from aposematic insects (Thorpe, 1964; Prokopy et al., 2000; see review by Prokopy and Roitberg, 2001 and citations therein). This phenomenon has been reported in several insect taxa, including flies (Ceratitis capitata: Prokopy et al., 2000; Rull et al., 2003; Musca domestica: Collins and Bell, 1996; Rhagoletis pomonella: Prokopy and Reynolds, 1998), some meliponine bees (Slaa et al., 2003), cockroaches (reviewed by Rust and Appel, 1985; Dambach and Goehlen, 1999) and wasps (Vespula germanica: D Adamo et al., 2000, 2003), but not in all species examined (e.g., the tephritid flies Anastrepha ludens, Diaz-Fleischer and Aluja, 2003, and Bactrocera tryoni, Prokopy et al., 1999). The concept of local enhancement has been extended to embrace the selection of habitat based on visual, chemical, and/or acoustical cues from same or opposite sex conspecifics (Prokopy et al., 2000; D Adamo et al., 2000). Our study is designed to quantify the strength of local enhancement in two species of butterflies, by testing their use of stimuli from pinned butterfly decoys to locate sodium resources. Many species of adult Lepidoptera, particularly males, aggregate at moist ground, perspiration, tears, excrement, and animal carcasses, to ingest essential nutrients, particularly sodium (Arms et al., 1974; Adler, 1982; Boggs and Dau, 2004) and protein (e.g., albumin; Beck et al., 1999). This behavior is conventionally termed mud-puddling (Arms et al., 1974; Adler and Pearson, 1982; Smedley and Eisner, 1996; Beck et al., 1999) or simply puddling (Sculley and Boggs, 1996, Boggs and Dau, 2004). In part, this behavior appears to have evolved due to a shortage of sodium in the diets of many Lepidopterans. Insects with herbaceous diets, such as caterpillars, are often sodium-deficient due to the low levels of sodium ions produced in photosynthetic pathways of terrestrial plants (Adler and Pearson, 1982). Sodium gathered by an adult male butterfly while mud-puddling is transferred to his mate in the spermatophore during copulation, which can result in an increase in egg production (Boggs, 1986) and sometimes in offspring fitness (Pivnick and McNeil, 1987). Therefore, mud-puddling not only benefits the male nutritionally but also the female and in some cases their offspring (Adler and Pearson, 1982; Smedley and Eisner, 1996), and sodium therefore constitutes a nuptial gift from the male to the female

3 Local Enhancement in Mud-Puddling Butterflies 687 (Vahed, 1998). The importance of sodium to Lepidoptera is suggested by the widespread occurrence of receptors for sodium ions on the tarsi of adults of many species (Pivnick and McNeil, 1987). The study on nutrient acquisition by mud-puddling butterflies performed by Arms et al. (1974) proved that mud-puddling in temperate butterflies is largely driven by a need for sodium. In that experiment, they used experimental trays containing various solutions, each baited with a pinned Tiger Swallowtail (Papilio glaucus) specimen to make it more attractive to butterflies seeking ions. Their positive results suggest that patrolling Tiger Swallowtails are attracted by the visual cues of the butterfly decoy, thereby using social facilitation as a mechanism to enhance their success in finding sources of sodium. Other reports also suggest that swallowtails are attracted to other butterflies engaged in puddling behavior (Scudder, 1889; Clark, 1932; Beck et al., 1999). The only experimental test documenting the attraction of swallowtails to other puddling butterflies was conducted by Beck et al. (1999) in Borneo. We report on the attraction of butterflies to artificial mud-puddling sites baited with dead decoy butterflies as a way of investigating the influence of local enhancement on mud-puddling behavior. The test subjects used for our study were Pipevine Swallowtails (Battus philenor) and Tiger Swallowtails (Papilio glaucus). Additionally, we studied the extent to which this phenomenon is based on interspecific and intraspecific attraction and whether a small piece of a Battus wing, instead of an actual butterfly specimen, provides sufficient visual stimulus to stimulate mud-puddling by freeflying butterflies. METHODS All our experiments were performed at the Cascades Recreational Area, Jefferson National Forest, Virginia, USA, in May, 2001 and May, Each test site consisted of two cleared patches of soil approximately one meter apart moistened with 0.1 M NaCl solution (sensu Arms et al., 1974). These artificial puddles were set up in several locations including a clearing on a path in deciduous forest, near the forest edge in a large clearing, and on a raised grassy hilltop. Data were collected under sunny conditions with temperatures between C. In 2001 we performed only one experiment. A pinned male Battus philenor with wings in open position was placed as a decoy in one of the two puddles at each test site. In 2003 we used the same methodology for the second experiment but a pinned male Papilio glaucus served as a decoy while the other puddle was left unbaited to serve as a control puddle. Each

4 688 Otis et al. observer sat approximately two meters away from a test site to observe the behavior of butterflies passing near (< 8 m) the test sites. Both those flying over with no apparent interest to mud-puddle and those that landed on either puddle were recorded. Detailed observations were restricted to Battus or Papilio swallowtails; other butterflies were noted when seen and their behavior recorded. After observing and recording a butterfly feeding at a test site, it was captured and held alive in a glassine envelope to prevent repeated observation of the same butterfly. Furthermore, the decoy s position was switched to the alternate puddle after each butterfly landing in order to eliminate location preferences. Sex determination of all butterflies was accomplished by examining the genitalia of the butterflies after capture. In the third experiment, we simultaneously placed a Battus decoy at one puddle and a Papilio decoy at the other, to provide free-flying butterflies with a choice between the two decoy species. Therefore no empty control puddle was used. The positions of the butterflies were switched every fifteen minutes to eliminate location effects. Only butterflies that landed were recorded. Again, the butterflies attracted to the decoys were captured and held alive until the end of the day s observations. The iridescent blue-green-colored hind wings of three male Battus butterflies were glued dorsal side up to index cards, then trimmed to 2 cm diameter discs for the fourth experiment. A single wing-disc was placed randomly on one of the puddles at each test site while the other puddle served as the unbaited control. The positions of the wing-discs were switched every fifteen minutes. This methodology closely resembles the procedures of experiment three. Sample sizes for each experiment are presented in the figures. All results were analyzed using χ 2 tests. RESULTS There were hundreds of Battus philenor ( Battus ) at the study site; Papilio glaucus ( Papilio ) were common but less abundant that Battus. In the first two experiments, free-flying butterflies had a choice of a puddle with a decoy or an empty puddle. In Experiment 1, 20 Battus males approached the puddles. They had a strong preference to land at puddles baited with pinned Battus decoys compared to unbaited puddles (Fig. 1; χ 2 = 10.71, P < 0.001). No Papilio were attracted to the Battus decoys in this experiment. Similarly, in Experiment 2, of the 149 Papilio that flew near our artificial puddles, all but one of those that approached the puddles (n = 61)

5 Local Enhancement in Mud-Puddling Butterflies 689 Fig. 1. Experiment 1: Comparison between the number of individuals of each species that landed on experimental puddles either baited with a dead male Battus decoy or unbaited. The number of passing Battus butterflies was not recorded but approximately 30 Papilio butterflies passed the sites without landing. landed at the puddles baited with Papilio decoys (Fig. 2; χ 2 = 56.06, P ). Furthermore, male Battus butterflies that approached the puddles (n = 34) exhibited interspecific attraction to the puddles baited with the Papilio decoys compared to the unbaited puddles (Fig. 2; χ 2 = 11.76, P<0.001). When given a choice between Battus and Papilio decoys in Experiment 3, male Battus butterflies landed at both, but more frequently on the conspecific decoy than on the interspecific Papilio decoy (Fig. 3; χ 2 = 14.08, P < ). In the choice situation, Papilio butterflies exhibited no attraction to the Battus decoy and only landed on the conspecific decoy (Fig. 3; χ 2 = 44.00, P ). Male Battus butterflies were strongly attracted to puddles baited with a circular disc cut from the iridescent blue-green hindwings of male Battus compared to unbaited puddles (Fig. 4; χ 2 = 12.46, P < ). No Papilio males were attracted to the Battus-wing-discs. When they approached a baited puddle, both Battus philenor and Papilio glaucus landed either directly on or within wing length of the decoy. The butterflies generally held their wings in a partially open position when drinking, occasionally opening and closing them slightly. In one instance,

6 690 Otis et al. Fig. 2. Comparison between the number of individuals of each species that landed on experimental puddles either baited with a dead male Papilio decoy or unbaited. Many Battus butterflies (n = 308) and 88 Papilio butterflies (n = 88) passed the sites without landing. a Battus that was flying directly towards the conspecific decoy landed on the unbaited puddle it reached first. After being disturbed, it flew directly towards and landed next to the Battus decoy, abandoning the puddle from which it had begun to imbibe fluid. This further demonstrates the attraction of the butterflies to the decoys. Only one female butterfly (Battus) was observed at the salted mudpuddles during our experiments. We observed several other butterfly species during our study. Two spicebush swallowtails (P. troilus) approached and landed next to a Papilio decoy. Duskywing skippers (Hesperidae: Erynnis spp.) landed at puddles baited both with Battus and Papilio decoys as well as other unbaited sites in the study area. They failed to demonstrate a clear attraction to either the sodium enriched puddles or the pinned decoys. Azures (Lycaenidae: Celastrina ladon, C. neglectamajor) were less frequently observed mudpuddling. They exhibited no preference for the baited and unbaited salt licks, suggesting that they were not attracted by the presence of the butterfly decoys. Two Morning Cloaks (Nymphalis antiopa) and several angle wings (Polygonia sp.) were seen; none landed at the artificial mud-puddles.

7 Local Enhancement in Mud-Puddling Butterflies 691 Fig. 3. Comparison between the number of individuals of each species that landed on experimental puddles either baited with a dead male Battus decoy or a dead male Papilio decoy. Passing butterflies were not recorded. DISCUSSION Both Battus philenor and Papilio glaucus showed very strong preferences to land on puddles baited with decoys rather than on unbaited puddles. Our findings indicate that mud-puddling by males of these two species, and consequently their rate of finding sodium, is positively enhanced through social facilitation, specifically through local enhancement. Although it has been observed that a dead Papilio decoy can apparently induce aggregations of Papilio species (Scudder, 1889; Clark, 1932; Arms et al., 1974; Denton, 1989), it has previously not been investigated experimentally in temperate swallowtails. The cues for local enhancement can be visual, chemical, and/or acoustical (D Adamo et al., 2000). In our experiments we believe that visual cues were most extensively used because the butterflies were attracted to dead decoys over relatively large distances and from different directions. This was the conclusion reached by Beck et al. (1999) for brightly colored butterflies in the families Pieridae and Papilionidae in Borneo that were attracted interspecifically to yellow Eurema (Pieridae) decoys. Furthermore, Beck

8 692 Otis et al. Fig. 4. Comparison between the number of individuals of each species that landed on experimental puddles either baited with the Battus hind-wing disc decoy or unbaited. Many Battus butterflies (n = 94) and Papilio butterflies (n = 11) passed the sited without landing. et al. (1999) found that groups of five Eurema decoys attracted more swallowtails and pierids than did single decoys, providing additional evidence of the importance of visual cues in these taxa. However, we cannot completely rule out attraction to chemical cues from the dead butterfly decoys we used because we did not attempt to quantify chemicals emitted from the decoys, nor did we record wind direction and the precise direction from which the butterflies approached. Acoustical cues can be ruled out because the decoys were dead. In other studies concerning insects, chemical cues have generally have a minor role in local enhancement. Prokopy et al. (2000) placed their decoy Ceratitis capitata (Tephritidae) on scented and scentless fruit. Their results showed that scents from the fruit did not contribute to local enhancement. Another experiment, designed to test socially facilitated oviposition behavior in Rhagoletis pomonella (also Tephritidae), determined that both hostmarking pheromones and the odors on recently laid eggs failed to attract conspecifics (Prokopy and Reynolds, 1998), allowing them to conclude that scent did not contribute to socially facilitated behavior in that species. However, in the social wasp Vespula germanica, local enhancement was greatly

9 Local Enhancement in Mud-Puddling Butterflies 693 increased when both odors and visual cues were presented together in contrast to either cue alone (D Adamo et al., 2003). In a study in which albumin proved to be attractive to some mud-puddling butterflies, Beck et al. (1999) suggested that lycaenids and nymphalids seemed to rely predominantly on olfactory cues emitted from dung, carrion, and other proteinaceous resources. Collectively these results further suggest that chemical cues, although extremely important in insect behavior (especially in mate attraction), generally play a relatively minor role in local enhancement of insects to resources; however, in specific instances they may serve as the primary cue. Color reflected from small circular discs cut from dorsal hind-wings of male Battus also elicited conspecific attraction. The attractiveness of these dorsal wing discs (Fig. 4) was strong (compare to results obtained with intact butterflies, Fig. 1), and further supports the conclusion that visual cues are very important to local enhancement in these swallowtail butterflies. It has been reported that aggregations of tropical swallowtails can be attracted to a small square of white paper that serves as a decoy at sites baited with salts or nitrogenous compounds (Tyler et al., 1994). Clearly the complete shape of the butterfly is not required for some attraction to occur. There may be other visual cues that facilitate intraspecific attraction. For example, swallowtails often flutter their wings weakly when mudpuddling (Opler and Krizek, 1984), a behavior we observed in both Battus and Papilio. Regardless of the various explanations for this behavior (eg., thermoregulation, Douglas, 1986; enhanced exposure to warning coloration on the ventral wing surface in unpalatable species such as Battus philenor, Codella and Lederhouse, 1990; intrasexual communication, Silberglied, 1984), wing fluttering should make puddling butterflies more visible to other butterflies seeking sodium or other resources. In studies of Ceratitis capitata (Mediterranean fruit fly), wing-waving by live flies was initially believed to be a primary stimulus for social facilitation (Prokopy and Duan, 1998). However, when re-examining the Ceratitis capitata system using dead decoys (i.e., without the wing waving stimulus), local enhancement was still observed at the same intensity (Prokopy et al., 2000). The strong attraction to the dead butterfly decoys we experimented with indicated that wing-fluttering, although it may serve as an active signal for the attraction of other butterflies to sources of sodium, is not necessary for the phenomenon to occur. Local enhancement may evolve because the presence of other organisms, especially conspecifics, frequently indicates the presence of a resource (e.g., mineral-enriched puddle, food, oviposition site). Movement towards those individuals increases the probability of accessing the desired resource (Prokopy and Duan, 1998; Prokopy and Reynolds, 1998; Prokopy et al.,

10 694 Otis et al. 2000; Prokopy and Roitberg, 2001). Mud-puddling is highly dependent on the specific resource requirements of different taxa (Beck et al., 1999; Sculley and Boggs, 1996; Boggs and Dau, 2004). For species that have low sodium or protein requirements as adults, the selection pressure for local enhancement to other mud-puddling individuals would be nonexistent. However, for taxa such as swallowtails in which males frequently exhibit mud-puddling behavior, in which females are polyandrous (Sculley and Boggs, 1996), and that respond strongly to the presence of sodium, there should be strong selection for individual males to move towards other mudpuddling butterflies as they seek to acquire the sodium they require to transfer to females. The results of our study with respect to strong attraction to conspecific models matches this prediction. The most surprising result of our study was the striking contrast in interspecific attraction by the two species we studied. In Experiment 3, approximately one third of the Battus were attracted to the Papilio decoys when given a choice between decoys of the two species. In contrast, Papilio were never attracted to Battus decoys or Battus wing-discs in any of our experiments. Additionally, on one occasion we observed a Papilio fly over a cluster of three puddling Battus and land on a puddle by itself several meters away. This highly significant difference in interspecific attraction between Battus and Papilio indicates that the two species respond to different visual cues. It is interesting that naïve Battus philenor have an innate preference for yellow over blue and purple in the absence of rewards (Weiss,1997). Although it is unclear what selective forces may have shaped this innate behavior, the preference for yellow may explain the attraction of B. philenor to the matte yellow wing surfaces of the Papilio decoys. If P. glaucus has a similar innate color preference, it might translate into the behaviour we observed attraction to yellow-colored decoys only. However, given that the visible spectrum for butterflies is one of the broadest in the animal kingdom and extends from ultraviolet into red (Silberglied, 1984), it is highly likely that Papilio glaucus males are capable of seeing the blue-green color of Battus males, especially since dark morphs of female P. glaucus are believed to mimic Battus philenor. Why tiger-patterned Papilio failed to be attracted to mud-puddling Battus butterflies and Battus decoys, despite their apparent need to acquire sodium from environmental sources through mud-puddling, remains unclear. The relatively scare Spicebush Swallowtail (P. troilus) was attracted to Papilio glaucus decoys in this study, indicating that some Papilio species do exhibit interspecific social facilitation. If there is generally greater attraction to conspecifics than to butterflies of other species, this could account for the emergence of groups of conspecifics or butterflies of similar appearance in large multispecies aggregations (Larsen, 1991).

11 Local Enhancement in Mud-Puddling Butterflies 695 Only one female butterfly, a Battus philenor, was observed at our experimental puddles; it was attracted to a male Battus decoy. Female Papilio glaucus only rarely have been recorded to mud-puddle (reviewed by Scriber, 2002). Beck et al. (1999) caught only one female (a nymphalid) out of 255 individuals checked. In contrast, Sculley and Boggs (1996) recorded females at mud-puddles more frequently, and particularly in species in which females mate only once. In general, the few female butterflies that mud-puddle tend to be older individuals (Adler and Pearson, 1982; Berger and Lederhouse, 1985; Scriber, 1987; Scriber and Ayres, 1988; Launer et al., 1996; Sculley and Boggs, 1996; Scriber, 2002). Puddling by females may also occur more frequently in environments deficient in sources of sodium. In swallowtails (Papilionidae), the extensive puddling of males and general absence of puddling by females suggests that the males are foraging for most of the sodium required by females, especially in multiple-mating species where the spermatophore and the sodium contained in it constitute a nuptial gift (Molleman et al., 2005). After mating, it is highly likely that males have reduced their stores of sodium, as has been demonstrated experimentally in Pieris (Adler and Pearson, 1982). Mating by males, and especially multiple mating, may cause them to become nutritionally stressed, which in turn may affect their ability to mate again and sire additional offspring (Lederhouse and Scriber, 1987; Sculley and Boggs, 1996) or to sire offspring with high fitness (Pivnick and McNeil, 1987). Males that are successful in finding sources of sodium presumably experience greater reproductive success. A recent test of this idea failed to detect differences in sperm numbers, but did discover that spermatophores of males were larger when they had imbibed a saline solution of low concentration (Watanabe and Makikubo, 2005). Being a member of an aggregation reduces the predation risk for each individual in the group (Hamilton, 1971; Clayton, 1978; Wilson, 1975; Beck et al., 1999; Prokopy and Roitberg, 2001). For mud-puddling butterflies, the benefits of joining an aggregation increase as the number of butterflies in the group increase. In the tropics, relatively high predation rates on butterflies (Srygley and Chai, 1990) provide an additional strong selective force for both interspecific and intraspecific local enhancement to sodium sources, particularly for highly colorful and visible species that may be more easily seen by predators. Consequently, predation intensity may be a factor underlying the large multi-species aggregations of mud-puddling butterflies in the tropics (Tyler et al., 1994; Beck et al., 1999). Conversely, the much lower risk of predation in temperate regions reduces the selective force for interspecific local enhancement by temperate swallowtails. Our results with Battus philenor and Papilio glaucus provide strong evidence of local enhancement in butterflies. Although there is anecdo-

12 696 Otis et al. tal evidence that many butterflies are attracted to mudpuddling butterflies, both intra- and interspecifically, the phenomenon has not been previously interpreted as a form of social facilitation. We have begun to investigate the specific visual cues that attract butterflies to aggregate and have extended our knowledge of inter- and intraspecific attraction of butterflies seeking sodium resources. Our methodology could be employed to elucidate the various mechanisms underlying the phenomenon of local enhancement by mud-puddling butterflies. Variables that could be manipulated, using both real butterfly specimens and artificial decoys, include: sex of the butterfly; wing coloration, size, and iridescence; wing position (i.e., open vs. closed wings) and wing movement; and magnitude of stimuli (numbers of decoys). Beck et al. (1999) suggested that there are complex interactions between resource requirements of particular taxa perhaps resulting from evolutionary constraints, butterfly longevity, geographical factors (tropical vs. temperate conditions), and predation risk Our methodology could be extended to other butterfly species and to other geographical environments to determine the generality of our results across taxa, habitats and latitudes in which selective forces differ. ACKNOWLEDGMENTS We appreciate the superb facilities of the Mountain Lake Biological Station, our base of operations for this study, and the contributions from the director, Dr. Henry Wilbur. Jefferson National Forest personnel in Blacksburg, Virginia, provided permission to conduct entomological studies at the Cascades Recreation Area. This study was conducted by students and faculty in the Field Entomology course offered by the University of Guelph and the University of Virginia. Students who conducted Experiment 1 in 2001 were Nicole McKenzie, Philip Careless, Joel Anderson, Kelly LeBrun, Owen Lonsdale, and Alison Malcolm. Suggestions from four anonymous reviewers greatly improved the study and resulting manuscript. REFERENCES Adler, P. H. (1982). Soil- and puddle-visiting habits of moths. J. Lepidop. Soc. 36: Adler, P. H., and Pearson, D. L. (1982). Why do male butterflies visit mud puddles? Can. J. Zool. 60: Arms, K., Feeny, P., and Lederhouse, R. C. (1974). Sodium: stimulus for puddling behavior by tiger swallowtail butterflies. Papilio Glaucus. Sci. 185: Beck, J., Muhlenberg, E., and Fiedler, K. (1999). Mud-puddling behavior in tropical butterflies: in search of proteins or minerals? Oecologia. 119:

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