Downloaded By: [Naskrecki, Piotr] At: 18:21 4 December 2007 ( ora fNtrlHistory Natural of Journal O:10.1080/00222930701633570 online DOI: 1464-5262 print/ISSN 02138, MA 0022-2933 Cambridge, ISSN St., Oxford 26 University, [email protected] Harvard Zoology, Email: Comparative USA. of Museum Naskrecki, Piotr Correspondence: ‘‘Homoptera’’ most Like 2002). (O’Brien forests tropical humid (often large (Auchenorrhyncha in are (Fulgoridae) diverse bugs Lantern Introduction we Here trophobiosis. directly. gastropod–insect it organisms, of on other case feed Keywords: by to first honeydew from able the bugs’ be far knowledge lantern to our eject on known to feeding forcefully been direct snails, they of have including which occurrence organisms widespread no honeydew, a date, of document to amounts and, copious bodies, produce their They forests. (often large tropical are (Fulgoridae) bugs Lantern Abstract 1 NASKRECKI PIOTR (Insecta: bugs Fulgoridae) lantern Auchenorrhyncha: in interactions trophobiotic Novel n rgros(eai 01.Terhnye srlae lwy n a ecollected be can and slowly, released other is sedentary, honeydew mm), in (1–15 1999), Their small 2001). documented Corke are (Delabie insects 1986; gregarious honeydew-producing been and (Fu trophobiosis, (Nishio geckos of and also 2005), Lepidoptera cases (Endersby most birds direct 2002), 2005), has al. such Pedro et (Dobson (Ho trophobiosis While mammals and ants 1999). (Camargo ‘‘homopteran’’ among Dixon Hymenoptera known honeydew- 2001), and This between best (Stadler 1991). relationships Delabie are mechanically (Bristow organisms trophobiotic relationships predators to other of of trophobiotic need and origins attraction the multiple contamination, insects or fungal to in producing avoid 1997), led to resulting (Gullan order has in hour, insect apparently insects the per feeding several the of produce honeydew of drowning vicinity can of the insects from contains and mass Phloem-feeding it auxins, also eliminate 2004). body alcohols, Honeydew al. amides, their honeydew. et phloem), times Woodring of than 2001; form higher (Delabie concentrations the salts in in (often carbohydrates acids and amino water excess the A S,and USA, MA, cetd1Jl 2007) July 1 Accepted osrainItrainla uemo oprtv olg,HradUiest,Cambridge, University, Harvard Zoology, Comparative of Museum at International Conservation ulnia ugrde netmlucitrcin,Trophobiosis interactions, insect–mollusc Fulgoridae, Euglandina, 2 sul eBiologı de Escuela + troryca,lnenbg edo homo lns n excrete and plants, of phloem on feed bugs lantern Sternorrhyncha), 07 13–0:2397–2402 41(37–40): 2007; , 1 EJ NISHIDA KENJI & a nvria eCsaRc,SnJose San Rica, Costa de Universidad ´a, # 07Tyo Francis & Taylor 2007 . 5m) homfeigiscs otdvrei humid in diverse most insects, phloem-feeding mm), 35 . 5m) homfeigiscs most insects, phloem-feeding mm), 35 2 ldbe n isn1990; Wilson and ¨lldobler ,CsaRica Costa ´, lige l 01.In 2001). al. et ¨lling Downloaded By: [Naskrecki, Piotr] At: 18:21 4 December 2007 fCsaRc.Tefrtst a oae ihntebreso aSlaBooia Station Biological Selva La of borders the within located forest was Atlantic the site in first (10 sites The two at Rica. organisms 2005 Costa other December with and of 1994 interactions March their and between phloem conducted on were feeding bugs lantern of Observations by been waxes methods yet and cuticular Materials have of interactions ingestion trophobiotic possible no 2001), the bugs. lantern Naskrecki and in recorded and 2000), honeydew (Roth eject Linsenmair of cockroaches forcefully the ejection With and ant, that it. high-speed giant collecting (Pfeiffer insects This from the ants, mobile away. of as In such meters exception solitary, trophobionts, foragers. fall small-bodied usually honeydew precludes often to apparently large, that resource are droplets renewable stable, bugs honeydew a lantern providing insects, contrast, the off directly ail ainlPr erE eb agrsain(10 station Braulio ranger within located Ceibo was site El second near The Park it. to National leading trails Carillo and arboretum station’s the o eido – s, 3–5 of period a for 2398 uig15rcre bevtoso edn atr usvstn rpoinswere trophobionts of of visiting species bugs species five lantern one recorded feeding and We of Tortricidae), 1). fast. observations (Figure honeydew and of similarly recorded streams (Noctuidae intercept 145 be to bugs moths During to lantern visiting of presumed regularly snail species pulmonate is six it cockroaches, but measured, not s, 5–6 of period cernua Fulgoridae: of species season four rainy the of during observations only visited feeding was 145 Ceibo El guttata made while Copidocephala during seasons, year, We the rainy throughout (November). opportunistically and done dry were Selva both La at Observations m). 560 h pe feetddolt fhnye for honeydew of droplets ejected of speed The Results pulses. and the photograph between to in droplets us allowed individual honeydew This by Hz). ejected traveled (199 pulses distance of light the of speed calculate frequency known the a of measured 580EX) We tergite. sanguinea abdominal 11th modified and Steud. quinquepartitus Phrictus otr18) n efudte rmrl ntrees and on (Johnson primarily oligophagous are them bugs found between Lantern folded body. we insect’s and and the trunk, 1986), of day the the side from Foster During ventral withdrawn trees. the host were the on species observed of legs canopy nocturnal Other the bark, of in periods. loose mouthparts high under both presumably, the hid or, day during trunks, the tree feeding during on and observed patterns crevices foraging were nocturnal strictly species showed this species was only activity of The foraging males) h. diurnal 02:00 (only and and 19:00 nocturnal between both night with at species primarily made were observations nocturnal, atr useethnye hog h nltb n lc niiuldolt sn a using droplets individual flick and tube anal the through honeydew eject bugs Lantern u 26 9 Ne)Mez. (Nees) ,84 N, .Nsrci&K Nishida K. & Naskrecki P. and iaob amara Simarouba u 1 .quinquepartitus P. 9 n ,eeain10m,adosrain hr eemd rmrl within primarily made were there observations and m), 150 elevation W, 5 0.Tesedo h oedweeto ftermiigseiswas species remaining the of ejection honeydew the of speed The 10). n (White), 5 itn.Bcuems pce flnenbg r exclusively are bugs lantern of species most Because Distant. 0,adfor and 20), apntsgigas Camponotus ul,adocsoal on occasionally and Aubl., nhpoasanguinea Enchophora ypoorpigi ihasrbsoi ls (Canon flash stroboscopic a with it photographing by .quinquepartitus P. .sanguinea E. Ltele,psil edn nhoneydew on feeding possibly (Latreille), .9 s m 1.695 , emnlaoblonga Terminalia Distant, u atlaelastica Castilla 19 a .9 s m 0.796 was 9 .sanguinea E. 40 0 ,84 N, .stillifera E. 2 1 eey56mnfra for min 5–6 (every u 4 2 Sesse 9 n individuals and , 43 1 Ri Pav.) & (Ruiz eey3–0s 30–60 (every 0 ,elevation W, and ´ (Sta l,and ˚l), Ocotea E. Downloaded By: [Naskrecki, Piotr] At: 18:21 4 December 2007 oedw(e ro)eetdby ejected arrow) (red honeydew snail, nhpoasanguinea Enchophora qitn oedwti htgahsosasnl rpe xoe utpetmswt toocpcflash. stroboscopic a with times multiple exposed droplet single a shows photograph honeydew—this squirting aurantiaca Euglandina nhpoasanguinea Enchophora iue1 rpoitcitrcin flnenbg Floia)wt net n nis a atr bug, Lantern (a) snails. and insects with (Fulgoridae) bugs lantern of interactions sanguinea Enchophora Trophobiotic 1. Figure ulniaaurantiaca Euglandina ihtosmlaeu ohget (small guests moth simultaneous two with , ihisatna,wiheiisimdaehnye rdcin h atr bug lantern (h) production; honeydew immediate elicits which antennae, its with n lporpoitcant, kleptotrophobiotic and , eddb cockroach, by tended ihlnenbug lantern with , nhpoasanguinea Enchophora Eurycotis oe rpoitcitrcin nlnenbugs lantern in interactions trophobiotic Novel hitsquinquepartitus Phrictus Camponotus e moth, (e) ; p ;(c) 1; sp. p . d snail, (d) n.; sp. ulsi proba Euclystis Platynota nhpoasanguinea Enchophora g moth, (g) ; p n larger and sp. atn o temo oedw (f) honeydew; of stream a for waiting , .aurantiaca E. legah argyritis Elaeognatha ihatohboi snail, trophobiotic a with legah argyritis Elaeognatha acigadoltof droplet a catching , .sanguinea E. tapping 2399 ;(b) ); Downloaded By: [Naskrecki, Piotr] At: 18:21 4 December 2007 ausaeidpnetosrain ftohboi interactions. trophobiotic of observations independent are Values oedwol ntepeec fasnail. a of presence the in only honeydew niswr bet eettepsto falnenbgo h re n olwdwhenever followed and The tree, it. the catch on bug to lantern position a its of adapted position the the changed quickly droplets. insect detect snail the honeydew to If the able of bug. stream, were the stream snails and honeydew the snail the the the catch above of between the to hood contact direction wide of snail physical a a the side forming never allowed the was foot, There the This on of apex. or portion abdominal behind anterior bug’s the either extended themselves and positioned bug, feeding snails The 1987). (Thompson genus the we occasion by one On either ( bug. the the cockroaches on bug, from of legs response the front species any its congeneric and elicit resting to two by cockroach appear observed or not the palps, did contact maxillary ( between This with abdomen wings. or wings contact bug’s bug’s the behind physical the of from palpating tip a cockroach bug the was above the mouthparts often approached their Cockroaches There positioned and I). (Table side, cases the from (33.1%) 48 in present Hymenoptera Lepidoptera Blattodea Visitors trophobionts. by bugs lantern of Visitation I. Table 2400 edn uigtedy(prxmtl 00 )wsrpael iie yanymphalid a by visited repeatedly was of individual h) 10:00 an (approximately occasion resumed one day moth butterfly On the proboscis The s. extended 30–60 during partially stream. within its feeding honeydew on usually accumulated imbibed, a honeydew fully of seen of droplet was moth the production were bug as the immediate soon a moth occasions, as an of tapping of four in wings On species the resulted time. two tapping which same seen Sometimes the was bugs. at Hampson lantern feed to and partially attempting their moths ( positioning droplets between side, flying the contact catch from to bugs the proboscis approached expanded usually Moths bugs. lantern utrl ol o eosre u otepsto fteiscso h retrunk. tree the on insects the of position the to due observed be not could butterfly ulniaaurantiaca Euglandina Gastropoda ne.Trrcde1 7 Camponotus acesta Tigridia Tortricidae Undet. Noctuidae Undet. Platynota proba Euclystis argyritis Elaeognatha Macrophyllodromia Macrophyllodromia maximiliani Macrophyllodromia Eurycotis Eurycotis omnvstrt atr uswsasnail, a was bugs lantern to visitor common A Euglandina p 1 1 2 sp. 1 sp. p 3 sp. .Nsrci&K Nishida K. & Naskrecki P. irdaacesta Tigridia p .(JTL-005) n. sp. p 1 1 2 sp. 1 sp. Siaia)icue rdcossal edn nohrgastropods other on feeding snails predaceous includes (Spiraxidae) a L) lhuhteitreto fhnye rpesb the by droplets honeydew of interception the although (L.), 1 guttata Copidocephala n 5 Enchophora ulniaaurantiaca Euglandina sanguinea 0.I otcssteewsn physical no was there cases most In 20). Eurycotis nhpoasanguinea Enchophora 315 1 13 83 1 4 5 atr bugs Lantern a iiain yat eutdi edn on feeding in resulted ants by Visitations edn h aeidvda of individual same the tending ) Enchophora stillifera legah argyritis Elaeognatha na ( Angas ihisantennae, its with quinquepartitus .sanguinea E. n Phrictus 5 9.The 19). n 5 5). Downloaded By: [Naskrecki, Piotr] At: 18:21 4 December 2007 otne edn o pt .Teewr ee oeta w nsvstn atr bug lantern a visiting be ants ants ant, may two the of than behavior species present, more (this Another never and was time. were ants, body given There the snail its any by h. 4 perturbed at the from to be up if to honeydew for appear Instead, licked feeding not did continued and stream. snails The snail the kleptotrophobiosis). the as reach described of to head small the too climbed were ants the a s hs olct hm eas bevdants observed also We them. snails ( but the locate bugs bugs, and lantern to lantern observations), find (personal these to signals use use vibrational snails producing may the of cues capable which are unclear bugs is the It itself. repositioned insect the aag M,PdoSM 02 uulsi soito ewe iyAaoinsigesbeadawax- a and bee stingless Amazonian tiny a between association interactions. plant Mutualistic Ant 2002. editors. SRM. DF, Cutler Pedro CR, JMF, Huxley In: Camargo tended? ant aphids few so are Why 1991. CM. Bristow lantern between interaction trophic possible ( a ants manuscript and slugs, this bugs, of preparation the During been has 1999). honeydew mechanism Dixon Endnote and a scraping (Stadler Such interactions snails cues. ant–homopteran the tactile of with following or origin eventually olfactory originated the and gustatory, explain have bugs, to using proposed lantern source might feeding the evolutionary behavior the to the honeydew- trail below a that this between vegetation likely on to is of relationship on feed It accumulated they led trophobiotic recorded. case where been direct that 2005) ever no first al. has path et but gastropods intercepting Eguchi the and prey, 2002; known insects of al. ants’ also are producing et species the capable (Witte snail is of colonies few trophobionts ant A remnants This in insect. guest an inquilines Auchenorrhyncha. and be of gastropod to a in case between interaction honeydew American known trophobiotic Central ejected first in trophobiosis the forcefully widespread of and evidence first Fulgoridae, the are observations never These but bug, lantern Discussion feeding bugs. the the approach below to trunk vegetation the climb on to accumulated attempted honeydew on h nomto npsil rpoitcitrcin nlnenbg nPpaNew Papua in bugs References lantern in sharing for interactions Jose Janda for Milan moth, trophobiotic and tortricid (deceased) possible moths, the noctuid Roth Guinea. on of of Louis specimens information identification to snails, access the for the for Brown INBio of during at John observed identification Montero bugs cockroaches, for lantern of of Baldinger identification identification Adam for O’Brien study, Lois personal thank this to Janda, wish authors (M. The widespread more Acknowledgements even be may above described communication). behavior the rdcn cl net itoia34:446–451. Biotropica insect. scale producing p. 601 Press. University Oxford Oxford: n 5 1,btte ee e rmtesra fhnye,ms ieybecause likely most honeydew, of stream the from fed never they but 11), Leptothorax p)wsosre nPpaNwGie,idctn that indicating Guinea, New Papua in observed was sp.) oe rpoitcitrcin nlnenbugs lantern in interactions trophobiotic Novel caom ruidum Ectatomma Camponotus Rgr,wsas enfeeding seen also was (Roger), p .(T-0)visit (JTL-005) n. sp. 2401 Downloaded By: [Naskrecki, Piotr] At: 18:21 4 December 2007 ohL akek .20.Tohboi ewe lteldccrah( cockroach blattellid ant a giant between Malaysian Trophobiosis the 2001. of P. history Naskrecki L, life leafhoppers, Roth the Zikaden: to editor. Contributions W, 2000. Holzinger KE. In: Linsenmair Fulgoromorpha. M, 139:220–223. of Pfeiffer Journal world Heterocerists’ wonderful Japan wild moths. The for resources 2002. food L. tropical as a O’Brien in Honeydew trees 1986. and N. Cicadidae) and Nishio (Fulgoridae Homoptera large of Associations 1986. biology, RB. insects—their Foster LL, scale Johnson Soft editors. CJ, Hodgson Ho Y, Ben-Dov In: ants. with Relationships 1997. PJ. Gullan Fu lorikeets Rainbow 2005. I. Endersby tde ,DxnAG 99 n tednei pis h ifrn ere fmreohl?Ecological myrmecophily? of degrees different why aphids: in attendance Ant 1999. AFG. Dixon B, Stadler odigJ idmn ,FshrM,Hfmn H Vo KH, Hoffmann MK, Fischer R, Wiedemann J, Woodring Florida the 2002. of U. Bulletin Maschwitz America. A, Eppenstein Central R, and Janssen Mexico V, Witte from snails land carnivorous Giant 1987. FD. Thompson osnM odna L hreD.20.Feigbhvoro h qirlgie nrmathbttin habitat Subulinidae) remnant Pulmonata: and in Pupinidae, glider (Prosobranchia: guests squirrel Gastropod the 2005. R. of Janssen behaviour TV, Feeding Bui K, 2005. Eguchi DJ. Sharpe RL, Goldingay Auchenorrhyncha): and M, (Sternorrhyncha air- Dobson Hemiptera particulate and Formicidae by between affected Trophobiosis Rhopalocera) 2001. JHC. (Lepidoptera: Delabie butterflies honeydew/sap-feeding Are 1999. D. Corke 2402 ligM ngeC Bo C, Knogge M, ¨lling ldbe ,Wlo O 90 h ns eln pigr 3 p. 732 Springer. Berlin: ants. The 1990. EO. Wilson B, ¨lldobler Hmnpea omcde.Isce oiu 47:123–132. Sociaux Insectes Formicidae). (Hymenoptera, 4:83–102. Denisia Auchenorrhyncha. Hemiptera: (Insecta: cicadas and planthoppers, 59:415–422. Society Entomological Kansas the of Journal forest. 351–373. p Science. Elsevier Amsterdam: control. and enemies natural 35:279–284. History Natural of Journal ( 22:42–45. 45:307–315. Sociobiology uasadterrl nteetbiheto n-tedneheacyi ih pce fahd edn on feeding aphids of species eight in hierarchy ant-attendance of establishment the ( in tansy role their and sugars 49:301–305. Sociaux Insectes Ponerinae). 30:29–52. Sciences) (Biological Museum State 24:363–369. Entomology ymcpiosmluclvn nclne ftepnrn ryant army ponerine the of colonies in living mollusc myrmecophilous soitdwt h oeieant ponerine the with associated 27:27–35. Mammalogy Australian Brisbane. 30:501–516. Entomology Neotropical overview. an 3:5–14. Conservation Insect of Journal pollution? Enchophora .Nsrci&K Nishida K. & Naskrecki P. aaeu vulgare Tanacetum and Copidocephala heW 01 eksaemlighnye-rdcn lnhpesi Madagascar. in planthoppers honeydew-producing milking are Geckos 2001. W. ¨hme .PyilgclEtmlg 29:311–319. Entomology Physiological ). rcolsu haematodus Trichoglossus p. nCsaRc.Junlo rhpeaRsac 10:189–194. Research Orthoptera of Journal Rica. Costa in spp.) icmasculpturatum Diacamma loesmyrmekophilos Allopeas edn npyldlrs utainFedOrnithology Field Australian lerps. psyllid on feeding llW 04 oedwaioaisi eainto relation in acids amino Honeydew 2004. W. ¨lkl ope Isca yeotr:Formicidae). Hymenoptera: (Insecta: complex Macrophyllodromia etgnsdistinguenda Leptogenys Gsrpd,Ploaa,tefirst the Pulmonata), (Gastropoda, p. n fulgorids and spp.) apntsgigas Camponotus (Formicidae,