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Entomophagy, Behavior, and Elongated Thoracic Legs in The BIOTROPICA 32(4a): 712-721 2000 Ento OphagylBehavior,and Elongated 丁hoLaCic Legs ln the My 丁 " ・ eCophIlou 巳 INeotropicalButterfly A ヰ eSa 甘 " ， eSfSs (Riodini<aey p・ J ・ [LV 刀 o8 ， and C・ ぬ ・ pen 寸 2 Department of Biology, University of Oregon, Eugene, Oregon 97403, U.S.A. ABSTRACT Entomophagy in the riodinid butterHy tribe Eurybiini is demonstratedfor the first time. Alesa amesis caterpillarsand adults possess behavioraland morphological traits for feeding on Homoprera nymphs, and oviposition by A. amesis females is mediated by the combined presence of Camponotusfemoratus ants and homopteran nymphs. Caterpillars are entirely entomophagous,and do not eat plant tissues. Alesa amesis caterpillars have distinct behaviors for feeding on their prey, and for soliciting and drinking honeydew secretions from homopteran nymphs. The leg lengths of entomophagous Alesa caterpillars are shown to be longer than phytophagousrelatives. The legs of Alesa are used for prey handling and soliciting honeydew secretions. W@esuggest that elongation of the thoracic legs has been a general consequence of enromophagyin butterfly caterpillars. This study clarifies our understanding of A. amesis and its interactions with multiple species, and points to behavioral and morphological trails important to interpreting the evolution of entomophagy among caterpillars. Our observations establish the likelihood that other members of Eur- ybnnim 、 ybe 。 n[ 。 mophagous ・， nd ， u毘刃 tha[ 。 ntom 。 ph， ぽ mayh ， "e 。 " 。 l"edind 。 pen 止nt@yamo 。 g 山 eNymphi- diini and Eurybiini RESUMEN Nuesrro esmdio presenta la primera documentaciondc entomofagia en la tribu Eurybiini. Las larvas y adultos de Alesa amesis tienen caracrerfsticas morfo16gicas y de comportamientoque faciliton su alimentaci6n dc ninfas de Homoptera %eneStaesp 。 む。，lc,Ia 。 "ipo 祉卜nF 。 肝。 tuab ， J。 l， p， 卜印Ci ， COnJu。 [ad<h 。， mig払 mP 川。 ヰmo ，如川 ynin 卜止 homopteros. Las larvas dc A. amesis son entom6faeasy no comen materia vegeta1. Ademas, las larvas tienen compor- tamientos distintos para alimentarse dc su presa y para solicitar y beber secreciones producidas por las ninfas dc h。 m。 pt し 0，・ D。 mon ， t，， mosqu 。 卜 p@。，。ぴ [O ， aCi 。 Ld 。 l， s l， wぬ 。 n[ 。 m6 卜甲 ， d。 Alesd ，。 n mLl ， ， gぴ qu 。 卜 d。 卜 F 。 卜斤 6卜伊 ， ぽ，。，。ぬ ・レ ， 卜 w， ， d。 Q[ ，ぽ p。 。 卜 M， n ， " ， @，， 甲， pi 。， nぴ p，， ， m， n。，。， ， y ， Oh 。 ぬ， seC ， 。 。 ione: d。 homopteros. Proponemos que el alargamiento de las piernas coracicas es una consecuenciageneral dc la entomofagia en larvas dc mariposas. Nuestro estudio clarifica el conocimiento dc la interacci6n entre A. amesis y otras especies de insectos. Ademas, discucimos caracceristicasmorfo16gicas y de comportamiento imporcantes para el estudio de la evoluci6n de la entomofagia en larvasde mariposas. Se establece la posibilidad que otras especies dc Eurybiini pueden ser entomofagasy se sugere que especies de Eurybiini y Nymphidiini evoluiran hibitos entom6fagosindependiente- mente ぬヴ 山川山 川。 ，， ; 切のぬ 叫ぬ灯，ぬ ワ &//"L 叱 んば f/" 川 @wfwbra，ぱり砕 わ M収ば ぼり 仏叫お仇，ク m。お 。 " ヰ， dfpF Af 。 必ぬ ぬむヴ mF" ，，，・ アコ Entoi nophagy･ in Myrmecophilous Alesa Caterpillars 713 trast, entomophagy(the habit of feeding on insects) Eurybia, our previous understandingof Alesa cat ﾂ by butterfly caterpillars is rare, and well known erpillars was that they are myrmecophilous and only among the myrmecophilous lycaenids, partic ﾂ phytophagous(e.g., Harvey 1987, Brown 1993). ularly the Liphyrinae and Miletinae of the Old During a long-terminvestigation of butterfly World tropics(Cottrell 1984, Ackery 1990, Pierce diversity in a lowland Ecuadorian forest, we studied 1995). A. amesis in some detai1, and in contrast to previous 1nsightsinto the complexity of entomophagous suggestions, found that the caterpillars were entire ﾂ lycaenid life cycles began with the basic observaﾂ ly aphytophagous.We present the first documen ﾂ tions ofLamborn (1915), Farquarson (1922), Jack ﾂ tation of entomophagy in the Eurybiini, and show son (1937), and Cripps and Jackson (1940) on Af- that A. amesis caterpillars and adults possess behavﾂ rican Milerinae,and recently reached an elegant ioraland morphological traits thatfacilitate feeding benchmark with studies on European Maculinea on Homoptera. First, we summarize our field obﾂ (Polyommatinae) and ants in the genus Myrmica servations on A. amesis to provide a narrative per ﾂ (Thomas et a1. 1989, Elmes & Thomas 1992, tinent to understanding this butterfly in the con ﾂ Thomas & Wardlaw 1992, Akino et a1. 1999). Al ﾂ text of myrmecophily and entomophagy. Second, though complex multispecies interactions likely oc ﾂ we compare A. amesis with other riodinid species cur in a variety ofentomophagous lycaenids (Owen using comparativeallometric data to determine the 1971, Henning 1983, Cottrell 1984, Johnson & effect entomophagy has had on caterpillarleg Valentine 1986, Kitching 1987, Maschwkz et a1. lengths, and discuss our findings to make several 1988, Banno 1990, Pierce 1995), the majority have predictionsregarding the evolution ofentomopha- not been studied in detai1. In contrast to the ly- gy in butterflycaterpillars. caenids, only one species of riodinid has been docﾂ umented as beingentomophagous; the caterpillars METHODS of Setabis lagus feed on the nymphs of Homoptera (DeVries 1997). In sum, relatively little is known Field observations were conducted intermittently about the complexity of interactions between most on A. amesis from July 1994 through July 1998 at entomophagousbutterfly caterpillars and other spe- the La Selva Lodge, Garaa Cocha, Sucumbios, Ecﾂ cies uador (hereafter LSL), where dominant habitat The riodinid tribe Eurybiini currently includes types included intact lowland f100dplain forest, ar ﾂ 24-31 species in three genera; Eurybia (20-25 spe ﾂ eas of riparian forest,and small patches of second- cies),Alesa (4-5 species), and the monobasic Mim- growth vegetation occurring around human habi ﾂ ocastnia (Harvey 1987, Bridges 1994, Banner tation. A more detailed description of the field site 1998). Based on the close relationship among gen- is found in DeVries, Walla et at. (1999). era and rearing records from one genus, all Eury- 0viposition, interactions with ants, and larval biini are considered to be myrmecophilous(Harvey feeding behaviors were observed in the field, or on 1987). The number of observations on Eurybiini field-collected individuals that were brought to a caterpillars, however, is relatively smal1. Of 20 or laboratory and confined in plastic containers or on more Eurybia species, only 8 have been confirmed potted plants at ambient temperatures. Early instars as herbivores on flowers of Marantaceaeor Zingi- were placed in Quinter's solution, transferred to 70 beraceae (e.g., Horvitz et a1. 1987; DeVries et a1. percent alcohol for storage (protocol in DeVries 1994; DeVries 1997; DeVries, pers. obs.); the rest 1997), and subsequentlyexamined with light miﾂ are unknown. croscopy. Terminology for caterpillar morphology The butterfly Alesa amesis (Cramer) is a wideﾂ pertinent to myrmecophilyfollows Cottrell (1984). spreadand often common species of Eurybiini The calls of A amesis caterpillars were detected ranging from Colombia, Venezuela, the Guianas, and recorded with a Bennet-Clark (1984) particle Ecuador, and Peru south through the Amazon ba ﾂ " 山口 7 而 C，。 ph 。 ne ming the m。 山O 小 d。 5田 b。 d sin of Brazi1. The only information on the early in DeVries (1991c). Subsequently, calls were char- stages of Alesa has come from Harvey (1987), who acterizedusing the sound analysis program Canary cited J. Mallet (pers. comm.) as having found an version 1.2 undeterminedAlesa caterpillar tended by Crema- Field observations suggested that the thoracic togaster sp. (Myrmicinae) anrs on Solatium sp. (S0- legs of A amesis caterpillarswere relativelylonger lanaceae). Based on well established patterns of than those of other riodinid genera. To test this host plant association in butterflies (Ehrlich & Ra ﾂ hypothesis,we compared leg lengths of A. amesis ven 1964) and host records from its sister genus caterpillars to those of 31 riodinid caterpillars rep- 714 DeVries and Penz IesenIlng 2I ， p。。ぬ ， 18 g。 n;era,。， and 8 田b ぴ，ぴ de66ned by Hawey (1987) and R"zand D。 V， ぬ (1999).F 。 I 。、 。 h ， p。 Hm 切 ， thekng[h 。 ftheLmu ，， tibia, and [arsu 。 f 。 n。 kg 。 " 。、 。 h th 。 ，， 。 iC 肛g- m。 m， and headwidth weIemeasuIedu5tngan 。 。 - ， r ，。 ・ 。 。 mp ，， e ， 。 田 mL m可汀 % kg k" 叩 tx ，， Iheh 。， d wid[h of ぬ。 h ， p。 。 而 。 " w， Sm 。 d ぴ astandard m。 ， ， u， e 。 f ， ぬ ， and thesum 。 f 。， 。 h leg kngIh (m 卜uS 。 hw) wぁ pl 。 北 d 甥寸n ， [ h。 ， d width. F。， %。 h 山可，。 k kg ， ，， 。 8，。 田 。 n hnew ぬ fitted through points representing 21 riodinid speﾂ cies, and then points representing A. amesis were overlaid on the graphs. RESULTS ADULTS.ﾑ Alesa amesis adults were present during the 48-m 。 "[h 。 b，。 wation P。 ， i。 d， but ， bundm 。 e wasl 。 w。 ， tin thed ， i[estmon[hs,aPatt。， 。 ， " 。 。 mm 。 " in m， ny 。 th" ， buT[。 ， 町 ， p 。 。 卜 (D 。 V， ぬ がぬ 1997; DeVries, Lande et a1. 1999; DeVries, Walla et a1. 1999; DeVries, pers. obs.). On sunny days, A. amesis males (N = >100 observations) perched FIGURE 1. Early stages of Ali-sa amesis. (a) Egg laid in light gaps and along streams and trails 0.5-3.0 directly on a membracid nymph (arrow). An individual m above the ground between 0800 and 1620 h, Camponotusfemoratus ant is tending this group ofmem- with peak perching activity from 1000 and 1500 bracids. (b) Close-up of a mature A. amesis caterpillar h. Females flew between 0900 and 1420 h, but about to drink a drop of honeydew(arrow) produced by a membracid nymph. Note that the caterpillar legs were oviposition behavior was observed only between used to solicit the drop of honeydew. An individual C. 1130 and 1420 h on sunny days. Between 0800 femoratus ant is visible to the left and behind the cater ﾂ and 1000 h, both males and females were frequent- pillar. ly seen visitingflowers of Psiguria sp. (Cucurbita- ceae)that occurred in light gaps and along edges, but never visiting the flowers of any other plant.
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