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Two heads are better than one:false head allows Calycopis cecrops(Lycaenidae) to escape predationby a Jumping Spider, Phidippuspulcherrimus (Salticidae)Andrei Sourakov aa McGuire Center for Lepidoptera and Biodiversity, FloridaMuseum of Natural History, University of Florida, Gainesville, FL,32611, USAVersion of record first published: 08 Mar 2013.

To cite this article: Andrei Sourakov (2013): Two heads are better than one: false head allowsCalycopis cecrops (Lycaenidae) to escape predation by a Jumping Spider, Phidippus pulcherrimus(Salticidae), Journal of Natural History, DOI:10.1080/00222933.2012.759288

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Journal of Natural History, 2013http://dx.doi.org/10.1080/00222933.2012.759288

Two heads are better than one: false head allows Calycopis cecrops(Lycaenidae) to escape predation by a Jumping Spider, Phidippuspulcherrimus (Salticidae)

Andrei Sourakov*

McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History,University of Florida, Gainesville, FL, 32611 USA

(Received 13 April 2012; final version received 17 October 2012)

The deflection of attack from vital organs to the wing margin is regarded as animportant adaptation in hairstreak butterflies. However, this “lose-little-to-save-much” strategy akin to the detachable lizard’s tail had never been tested experimen-tally. The present study tests the “false head” hypothesis by exposing a hairstreakbutterfly, Calycopis cecrops, as well as many other Lepidoptera species as controls,to the attacks of the jumping spider, Phidippus pulcherrimus. The results unam-biguously indicate that the “false head” is a very efficient strategy in deflectingattacks from the vital centres of the hairstreak butterfly whereas other similar-sizedLepidoptera fall easy prey. Predator fatigue resulting from unsuccessful attacks wasalso observed, suggesting that jumping spiders can learn to avoid attacking preythey cannot capture, which would increase the efficiency of the “false head” as adefensive mechanism.

Keywords: avoidance; butterfly; deception; predator; prey

Introduction

Markings resembling vertebrate eyes are found throughout Insecta and are verycommon in adult butterflies. They are widely believed to serve an important func-tion in defence. However, experimental evidence for such a defensive function islimited. Experiments that involved masking the eyespots of Aglais io (Linnaeus,1758) nymphalid butterflies suggested that the presence of eyespots on the dorsal wingsdoes indeed increase survival from attacks by blue tits, Parus caeruleus (Linnaeus,1758) (Vallin et al. 2005, 2006). In such species as A. io, behaviour can enable wing pat-terns to serve dual cryptic and aposematic functions, because wings are flicked openwhen a predator approaches, often scaring it away (Vallin et al. 2006). Most experimen-tal studies have been conducted using birds as predators because they were assumedto be the main driving force behind the evolution of cryptic and aposematic col-oration in Lepidoptera ever since the classical peppered moth experiments (Kettlewell1961), which suggested the presence of natural selection by birds against non-crypticphenotypes. The innate fleeing response in birds to a sudden encounter with the eye-spot pattern has been proposed to be responsible for a “huge and pervasive mimicrycomplex” that exists in the tropics (Janzen et al. 2010).

*Email: asourakov@flmnh.ufl.edu

© 2013 Taylor & Francis

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Eyespots on the ventral marginal areas of butterfly wings may serve an alterna-tive defensive function in deflecting attack from vital organs to the wing margin,the loss of which is insignificant to a butterfly, akin to the lizard’s tail (Wourmsand Wasserman 1985). An even more striking apparent deflective adaptation is theso-called “false head” coloration found in the diverse butterfly subfamily Theclinae(Lycaenidae) (Cordero 2001; Robbins 1980), which includes numerous species (over1000 species in the Neotropics alone (Robbins 2004)). The common name of the sub-family, “hairstreaks”, refers to thin white lines on the ventral surface which convergeat the tip of the hindwing furthest from the head; the hindwing also usually has one toseveral conspicuous red eyespots surrounded by white and black rings, in addition tothin filamentous black tails with white tips, which strongly resemble the insect’s anten-nae. The influence of eyespot presence on predation has been tested experimentally(Lyytinen et al. 2003a, 2003b; Stevens 2005, 2007; Stevens et al. 2008), but the con-clusions that arise from these studies are controversial. The effectiveness of the “falsehead” as an anti-predatory device has never been tested, and the present study is thefirst to attempt to do so.

Recently, it has also been shown that in encounters between Lepidoptera mimics(the metalmark moth, Brenthia hexaselena Meyrick, 1909) and its model [the salti-cid jumping spider, Phiale formosa (Banks, 1909)] the moth convincingly poses as thespider and so is able to avoid attack (Rota and Wagner 2006). Instead of attackingits prey, the spider reacted with a display behaviour normally observed during anencounter with a conspecific spider. Based on this study, the authors concluded thatjumping spiders “can be regarded as important drivers in the evolution of diurnalinsect phenotypes and behaviours.”

Equipped with excellent vision, jumping spiders are capable of distinguishing var-ious types of threats and altering their behaviour accordingly (Nagata et al. 2012).For example, it was shown that the presence of wings in ants stimulates attackingbehaviour in a jumping spider, Plexippus paykulli (Audouin, 1826) (Edwards 1980).This spider recognized alate ants as palatable (even if they were workers with fakewings), but avoided attacking wingless ants (even alate ones from which the wingswere artificially removed), presumably interpreting these as workers that are equippedto defend themselves. Among some 4000 jumping spider species, there are specialistand generalist predators, many of which have a remarkable ability for learning andeven problem-solving (Jackson and Pollard 1996). Easy to maintain in captivity, jump-ing spiders provide a unique opportunity to test hypotheses regarding predator–preyinteractions.

In the present study, the efficiency of “false head” colour patterns as anti-predator defence mechanisms was tested using a hairstreak butterfly, Calycopis cecrops(Fabricius, 1793) (Lepidoptera: Lycaenidae), as a model prey and Phidippus pulcher-rimus Keyserling, 1885 (Araneae: Salticidae) as a model predator. Calycopis cecrops(Figure 1A) is a common woodland species in the eastern USA and is a typicalhairstreak representative. The insect normally forages or perches with its wings closed,moving its hindwings up and down almost non-stop, especially when threatened,whereas the blue coloration of the upper wing surface is exposed only during its fastflight. This movement adds to the human perception of a second (and more promi-nent) head located on the rear side of the insect. As the movement plays a large rolein triggering predator attacks, it has been proposed that the insect would be targetedfrom this side (Robbins 1980). Perhaps not coincidently, this region of the wing is very

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Figure 1. False head in hairstreak butterflies: (A, B) Calycopis cecrops: (A) perching; (B) thedisturbed butterfly turns its “false head” toward the perceived danger and initiates movement ofhind wings. (C, D) Parhassius m-album: (C) intact freshly emerged; (D) wild specimen that haslost its “false head” in a predator attack.

soft and can easily be ripped off, allowing the butterfly to escape. Indeed, this idea issupported by occasionally finding butterflies with beak marks, which supposedly haveresulted from predator attacks (personal observation, Figure 1C, D). Nevertheless,an alternative hypothesis has been proposed about how the “false head” functions(Cordero 2001). Cordero suggested that some predators normally approach their preyfrom behind so as to be out of the prey’s sight and not alarm it. He suggested thatsuch predators would interpret the “false head” as the side that carries the eyes andas a result would attack a hairstreak from its real head, which would allow it todetect the attacker and escape. Neither of the above theories has been tested, and thepresent study is aimed at rectifying this. Phidippus pulcherrimus (Figure 2) was cho-sen as a predator for the test because this open woodland species lives in the foliage

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Figure 2. In captivity, attacks by Phidippus pulcherrimus almost inevitably result in bites to thebase of the wing, followed by immediate paralysis of the prey and prolonged feeding by thepredator.

of understorey plants where C. cecrops flies and is distributed in the same region ofthe south-eastern USA (Edwards 2004). Their predator–prey interaction in the wild,therefore, is quite likely. Also, P. pulcherrimus, unlike some other smaller Salticidae thatwere tried, proved able to successfully attack small Lepidoptera species in captivity.

Material and methods

A female P. pulcherrimus was collected on the University of Florida campus on20 September 2011 and was kept in a 0.5-litre plastic container for 3 months. SmallLepidoptera of different species were released into the container approximately oncea week, and the interaction was recorded on video with a Canon Powershot SX10IScamera. The spider was normally allowed to feed on the captured prey. In additionto C. cecrops (a butterfly with a 26-mm wing span), which was offered to the spideron two occasions, among Lepidoptera offered were butterflies and moths of differ-ent families ranging from 15 to 40 mm in wing span: e.g. Eurema daira (Godart,1819) (Pieridae); Phyciodes phaon (W. H. Edwards, 1864) (Nymphalidae); Pyrgusoileus (Linnaeus, 1767), Cymaenes tripunctus (Herrich-Schaffer, 1865) (Hesperiidae);Terastia meticulosalis Guenee, 1854, Samea ecclesialis Guenée, 1854, Herpetogrammasp. (Pyralidae); Mocis latipes (Guenée, 1852), Leucania sp., Renia fraternalis J.B.Smith, 1895 (Noctuidae); and Disclisioprocta stellata (Guenée, 1858) (Geometridae).Individuals of C. cecrops were offered to the spider in the middle of the trials (on14 and 19 October). Other species were tested before and after C. cecrops to ensurethat the spider’s ability to successfully attack prey was consistent. The resulting data

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on number of trials resulting in attacks on prey with and without a “false head” wereanalysed using a χ2-test, PAST software (Hammer et al. 2001).

Results and discussion

The results are conclusive in demonstrating that C. cecrops is successful at avoidingattacks by the spider predator unlike the other Lepidoptera tested, and observationssuggest that this is probably a result of its possession of “false head” markings on thehindwing. Among 15 individual butterflies and moths belonging to 12 different speciesthat were offered to the spider, 13 were successfully captured as prey (Table 1). OnlyC. cecrops repeatedly escaped the attacks. From the 14 attacks that were performed byP. pulcherrimus on C. cecrops during 52 minutes of the first exposure (14 October), andthe two attacks that occurred during the second exposure (19 October), none resultedin capture of the prey. Even without considering the outcome for the individual species,but rather treating each attack as a separate event, the observed difference between thesuccess rates of attacks on C. cecrops and the attacks on other prey was significant(p < 0.0004).

A notable decline in the frequency of attacks was observed during the firstC. cecrops trial, in which half of the attacks occurred in the first 10 minutes, andno attacks occurred during the last 10 minutes (Figure 3). In contrast, attacks on allother prey resulted in capture, sometimes on the second or third attempt, but morefrequently on the first attempt (Video 1, see Supplementary materials).

While the attacks on C. cecrops occurred in the “false head” region, as can beclearly observed (Video 1, Supplementary materials, minutes: 1:50; 2:03; 2:21; 2:34;2:46 and in slow motion 3:04), the attacks on other prey always occurred in the

Table 1. Number of attacks until capture (1) or termination of effort(0) on individual Lepidoptera prey by jumping spider, Phidippus pulcher-rimus in captivity.

Prey species No. of attacks(no. of captures)

Eurema daira, ind. 1 1 (1)Eurema daira, ind. 2 2 (1)Phyciodes phaon 1 (1)Pyrgus oileus 2 (1)Cymaenes tripunctus 3 (1)Terastia meticulosalis, ind. 1 1 (1)Terastia meticulosalis, ind. 2 2 (1)Samea ecclesialis 1 (1)Herpetogramma sp. 1 (1)Mocis latipes 1 (1)Leucania sp. 4 (1)Renia fraternalis 2 (1)Disclisioprocta stellata 2 (1)Calycopis cecrops, ind. 1 14 (0)Calycopis cecrops, ind. 2 2 (0)

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Figure 3. Change in frequency of attacks on Calycopis cecrops hairstreak by jumping spider,Phidippus pulcherrimus, during continuous exposure in the laboratory for c.1 hour. “x” shows ahypothetical frequency if the trend had been linear.

head region, with the bite delivered to the thorax at the base of the wing (Figure 2).It appeared that the failure to capture C. cecrops largely resulted not from the abilityof the butterfly to evade the attacker, but from the “false head” being a target. Withno part of the body available for the spider to seize adjacent to the “false head”, thespider appeared to be unable to capture the butterfly through its attacks directed at thisregion. In all other cases, P. pulcherrimus was normally capable of recognizing the exactposition of the head before the attack. For instance, when introduced to D. stellata, itcircled it from one end to the other before delivering the attack into the head region(Figure 4).

The behaviour of the prey in response to exposure to the spider also differed.Whereas most non-C. cecrops prey species became still in the presence of the spi-der, C. cecrops continued moving, as if deliberately exposing itself to the attacks. Theother notable exception was Phyciodes phaon, which was also constantly in motion.Though P. pulcherrimus was able to kill Phyciodes phaon, it did not feed on it. This lat-ter species is chemically protected by iridoid glycosides (Wahlberg 2001) and is brightlycoloured, so exposing itself to the predator may enhance its aposematism. Consideringthe negative (for P. pulcherrimus) outcome of the attacks on C. cecrops, it is reason-able to suppose that this “predator teasing” behaviour may be an innate part of thehairstreaks’ defence specifically targeting small predators such as jumping spiders. Thepresence of perceived danger appears to stimulate the “teasing” behaviour in a restingbutterfly. For instance, I also observed C. cecrops initiating the hind wing movementand crawling behaviours as I approached to take a photograph in the wild. Hence, Iconclude that the deflection of attack to the rear part of the wings is the reason for

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Figure 4. In captivity, Phidippus pulcherrimus almost always (with the exception of Calycopiscecrops) approached the prey from the head region and delivered the attack head-on. Thissequence of frames “grabbed” from a video, shows P. pulcherrimus manoeuvring upon encoun-tering its prey, Disclisioprocta stellata (Geometridae).

“false head” colour and associated behaviour in hairstreaks. A possible alternativeexplanation for the results of the present experiments is that hairstreaks are simplytoo fast for the spiders to catch, and that the motion of the tails has an alternativefunction, perhaps related to the intraspecific communication. However, hairstreaks arefrequently found with their tails ripped off, most likely by predators – their wings inthis region are thinner, which should facilitate them tearing under attack – and P. pul-cherrimus almost invariably attacked the “false head” of C. cecrops, despite attackingthe head of all control species. Skippers (Hesperiidae) are notorious for their quickreflexes, which surpass those of other butterflies (e.g., Sourakov 2009), and two rep-resentatives of this family, Cymaenes tripunctus and Pyrgus oileus, were successfullycaptured by the spider in the present study. These observations support the hypothesisthat the “false head” strategy sensu Robbins (1980) is the most likely explanation forthe observed results.

If escape is the most common outcome of attacks by stalking predators, such asP. pulcherrimus, each failed attempt to capture this or similar prey should imprint thefutility of attacking such prey into the predators’ memory and hence reduce the risk offuture attacks for C. cecrops and similar looking species. In this respect, all hairstreaksshare not only common behavioural responses, but also have very similar ventral pat-terns, and might represent a large, diffused mimicry complex directed to discouragepredators from attacking them. Further studies that involve other species of predatorsand other species of hairstreaks would be of great value to understanding the efficiencyof the “false head” as a predator defence mechanism.

Acknowledgements

I thank Keith Willmott, Alexandra Sourakov, Julieta Brambila and anonymous reviewers whokindly reviewed the manuscript and offered many useful suggestions. I also thank G. B. Edwardswho kindly identified the species of spider.

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References

Cordero C. 2001. A different look at the false head of butterflies. Ecol Entomol. 26:106–108.Edwards GB. 1980. Experimental demonstration of the importance of wings to prey evaluation

by a salticid spider. Peckhamia. 42(1):6–9.Edwards GB. 2004. Revision of the jumping spiders of the genus Phidippus (Araneae:

Salticidae). Occasional Papers of the State Collection of Arthropods. 11:1–156.Hammer Ø, Harper DAT, Ryan PD. 2001. PAST: Paleontological statistics software package

for education and data analysis. Palaeontol Electron. 4(1):1–9.Jackson RR, Pollard SD. 1996. Predatory behavior of jumping spiders. Annu Rev Entomol.

41:287–308.Janzen DH, Hallwachs W, Burns JM. 2010. A tropical horde of counterfeit predator eyes. Proc

Nat Acad Sci USA. 107(26):11659–11665.Kettlewell HBD. 1961. The phenomenon of industrial melanism in Lepidoptera. Annu Rev

Entomol. 6:245–262.Lyytinen A, Brakefield PM, Lindstrom L, Mappes J. 2003a. Does predation maintain eyespot

plasticity in Bicyclus anynana? Proc Biol Sci. 271(1536):279–283.Lyytinen A, Brakefield PM, Mappes J. 2003b. Significance of butterfly eyespots as an anti-

predator device in ground-based and aerial attacks. Oikos. 100(2):373–379.Nagata T, Koyanagi M, Tsukamoto H, Saeki S, Isono K, Shichida Y, Tokunaga F, Kinoshita

M, Arikawa K, Terakita A. 2012. Depth perception from image defocus in a jumpingspider. Science. 335(6067):469–471.

Robbins RK. 1980. The lycaenid “false head” hypothesis: historical review and quantitativeanalysis. J Lep Soc. 34:194–208.

Robbins RK. 2004. Tribe Eumaeini. In: Lamas, G, editors. Atlas of neotropical lepidoptera:checklist: Part 4A. Hesperioidea – Papilionoidea. Gainesville: Scientific Publishers.p. 118–137.

Rota J, Wagner DL. 2006. Predator mimicry: metalmark moths mimic their jumping spiderpredators. PLoS One. 1:e45.

Sourakov A. 2009. Extraordinarily quick visual startle reflexes of skipper butterflies(Lepidoptera: Hesperiidae) are among the fastest in the animal kingdom. Florida Entomol.92(4):653–655.

Stevens M. 2005. The role of eyespots as anti-predator mechanisms, principally demonstratedin the Lepidoptera. Biol Rev Cambridge Philosophical Soc. 80(4):573–588.

Stevens M. 2007. Predator perception and the interrelation between different forms of protectivecoloration. Proc Biol Sci. 274(1617):1457–1464.

Stevens M, Hardman CJ, Stubbin SL. 2008. Conspicuousness, not eye mimicry, makes“eyespots” effective antipredator signals. Behav Ecol. 19:525–553.

Vallin A, Jakobsson S, Lind J, Wiklund C. 2005. Prey survival by predator intimidation:an experimental study of peacock butterfly defence against blue tits. Proc Biol Sci.272(1569):1203–1207.

Vallin A, Jakobsson S, Lind J, Wiklund C. 2006. Crypsis versus intimidation – anti-predationdefence in three closely related butterflies. Behav Ecol Sociobiol. 59:455–459.

Wahlberg N. 2001. The phylogenetics and biochemistry of host-plant specialization inMelitaeine butterflies (Lepidoptera: Nymphalidae). Evolution. 55(3):522–537.

Wourms MK, Wasserman FE. 1985. Butterfly wing markings are more advantageous duringhandling than during the initial strike of an avian predator. Evolution. 39:845–851.

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