Journal of The Lepidopterists' Society Volume 57 2003 Number 1 JournaloftheLepidopterists'Society 57(1),2003,1-16 ANT-ASSOCIATION AMONG SOUTHERN AFRICAN LYCAENIDAE Alan Heath1 DepartmentofZoology,UniversityofCapeTown,Rondebosch7700, SouthAfrica AND Andre M. Claassens J. 203,HighLevelRoad,SeaPoint8005,SouthAfrica ABSTRACT. Knownlifehistorydata, ant-associationsandlarval feedinghabitsforsouthernAfricanlycaenidsaresummarizedanddis- cussedwithafocusonrecentlyacquiredknowledge. Ofthe392Iycaenidspecies representedinsouthernAfrica,overthreequartersareant- associated,twothirdsofwhichareobligate.The Poritiinaeisrepresentedbytwotribesofalgae/lichen feedersthatarenotant-associated. Of theMiletinae,threequartersareobligatelyant-associated,andallarebelievedtopreyonHomopteraortheirsecretionsduringtheirlarvalstage. WithintheLycaeninae,thetribeThecliniareallbelievedtobefacultative.ThetribeAphnaeiniconstitutesonethirdofalllycaenids,almostall obligatelyant-associated.ThetribePolyommatiniaccountsforathirdofalllycaenidsandis95%ant-associated,containingsimilarproportions offacultative andobligate associations. Thepresence, absence andfunction ofmyrmecophilous organs atvarious larval stages is discussed. Ovipositingbelowthesoiloronsandsurfaceisrecordedforthefirsttime.Thevarioustrophicstrategiesoflarvaearediscussed.Crematogaster (Myrmicinae)andAnoplolepis(Formicinae)antstogetheraccountforalmost80%ofobligaterelationships.Itissuggestedthatmanysynonymies existamongobligatelyant-associatedtaxa. Additionalkeywords: evolution, myrmecophily,trophallaxis,aphytophagy,entomophagy,detritus,acoustics,SouthAfrica. Of3607 Afrotropical butterfly species, 42% are in head protected beneath a tough carapace. Many such the family Lycaenidae (Ackery et al. 1995), a similar larvaehaveorgans thatserve specific functions intheir figure (47%) isgivenforsouthernAfrica2byPringle et association with ants. A dorsal nectary organ (DNO), al. (1994). Ofthe397Australianbutterflies, 36% arein present on the seventh abdominal segment of some thefamilyLycaenidae (Braby2000). Thesefiguresim- larvae provides honeydewforants toimbibe. Apairof plythatahigherlevelofdiversificationhasoccurredin tentacleorgans (TOs) locatedontheeighthabdominal the Lycaenidae than in other families, and Pierce segment and several minute perforated cupola organs (1984) suggested that this may have been caused by (PCOs) are present on the larva's cuticle which all se- ant-association (myrmecophily). Many species of ly- crete substances that can influence antbehavior (Cot- caenids are ant-associated in the earlystages (Fiedler trell 1984). Notethatant-organsfoundinant-associated 1991), ants being among the leading predators ofin- Riodininae differ from those in other lycaenids; see sects (Holldobler&Wilson 1990). Lycaenidlarvae are DeVries (1991, 1997) foracomparison. Byusingthese vulnerable to predatory ant species, hence various organs, free-living mutualistic caterpillars provide strategies have evolved to prevent or reduce attack. nutritious secretions and emit chemical signals (Hen- Dense and long hair serves as one effective strategy, ning 1983b) that can manipulate ant behavior to re- endophagy (feeding inside plant material) is another. duce aggression and obtain protection from predators Otherlycaenids possess an extra-thickcuticlewith the and parasitoids (Lenz 1917, Hinton 1951, Pierce & 1Addressforcorrespondence: 1TheClose, Limekiln Lane Bal- Mead 1981, Pierce 1984, Pierce et al. 1987, DeVries dock,Herts,SG76PJU.K. (Email:[email protected]). 1988, 1991, Fiedler 1991). In somecases this manipu- 2 Southern Africa: Countries south ofAngola, Zambia and the lation is extended to inducing regurgitations from ZBoatmsbweaznia,RZiivemrbaibnweM,ozSaomutbhiqAufrei.ca,ThSweazrielgainodn, LienscolutdheosanNdamsiobuitah,- adult ants (trophallaxis) or enabling the larva to prey ernMozambique. directlyontheantbrood(parasitism) (Henning 1983b, . Journalofthe Lepidopterists' Society Pierce 1995, Heath 1998, Elmes et al. 1991, Thomas Ourclassificationhere follows Scott (1985), Eliot (in 1983, Thomas &Wardlaw 1992). Corbet et al. 1992), Ackeryet al. (1999) andPierce et The DNO was first described by Guenee (1867), al. (2002), who treat Biodininae3 as a subfamilywithin subsequentlymoreknowledgewas gatheredaboutthe Lycaenidae, alongwith Poritiinae (including Pentilini myrmecophilous organs (Newcomer 1912, Ehrhardt and Liptenini), Miletinae (Miletini, Liphyrini and 1914, Hinton 1951, Clark & Dickson 1956). Their Spalgini) and Lycaeninae (Theclini, Aphnaeini, Ly- structure andfunctionwas studiedin greaterdetailby caenini and Polyommatini). Examples of adult ly- Malicky (1969, 1970). More recently, secretions from caenids from the region are illustrated (Figs. 1-20). these organs were chemically analyzed (Maschwitz et al. 1975, Pierce 1983, DeVries & Baker 1989). Many, Methods Used for Studying Lycaenids in the Fieldand Laboratory but not all ant-associated lycaenids possess these or- gans, whose presence and possibly function can vary Inducing oviposition. Inducing oviposition facili- throughout the larval stage (Cottrell 1984). Some ly- tates life historystudies in the laboratory. The method caenid tribes and genera are known to be more forinducingovipositionamongChnjsoritis Butleristo strongly ant-associated than others, but even within a place not more than three known or 'suspected' host single genus, the type ofassociation can be quitevar- ants togetherwith some stems preferably ofa known ied (Pierce 1989). larvalfoodplant, insideanopenplasticcontainerabout Ant-associated lycaenid larvae are known to pro- 130 x 100 mm and 70 mm deep covered tightlywith duce a substrate borne call to recruit ants (DeVries finenetting(e.g., ladies' stockings) andkeptwarm,but 1988, 1990, 1991, Travassos & Pierce 2000). Southern not hot, or in the sun. A female Chnjsoritis is added African aphnaeine larvae also produce sounds (Heath oncethe ants have settleddown. More thanthree ants 1998), as dopupae (Schlosz 1991, Claassens 1991). often results in an escape hole chewed in the netting. Numerous field and laboratory studies have con- The female butterflyis fed dailywith a small lump of tributed to our knowledge ofAfrican ant-lycaenid as- tissuepapersoakedinweaksugarwaterplacedon the sociations. One ofthe earliest accounts detailing ant- netting. Eggs areoften laidonthenetting. Attemptsto association in African lycaenids was Lamborn (1914) induce oviposition among Aloeides Hubner in this who recorded observations on early stages of 27 manner have been unsuccessful, but oviposition species (14 genera) from southern Nigeria. Nine of among captive Thestor Hubner occurred on almost these genera are also represented in southern Africa. any surface without either ants or vegetation present Observations in Kenya and Uganda byJackson (1937) (Heath & Claassens 2000) described obligate ant-associations in seven species Obtaining early stages in the field. Methods for anddiscussed25 facultative associations. The first ma- finding early stages in the field vary with life history jorstudyon SouthAfricanlycaenidearlystageswasby characteristics. Many myrmecophilous species spend Clark and Dickson (1971), who described and illus- partoralloftheirjuvenilephasesinorclosetosubter- trated 125 species at different stages oftheir develop- ranean ant nests which makes them difficult to dis- ment, including myrmecophilous organs. Behavioral coverandstudy. Others are foundunderrocks and as- studies under laboratory conditions were done subse- sociated with a particular plant or ant nest. The quentlyby Claassens (1972, 1976) and Claassens and methodusedto findChnjsoritis larvae is tosearchthe Dickson (1977). Onaglobalscale, lycaenid-antassoci- debris beneath potential food plants where ants are ations have been reviewedby Cottrell (1984), Fiedler present. On occasions, the larvae are foundinsmallfi- (1991) and Pierce et al. (2002). brous sheltersbuiltontheplantstemsbytheants,pre- This paper summarizes and discusses our under- sumably intended for Homoptera. For Aloeides we standing of myrmecophilous lycaenids in southern search in the soil beneath potential foodplants orbe- & Africa during the past ten years. Becent accounts in- neath nearby rocks. In Trimenia Tite Dickson, the clude: Schlosz and Brinkman (1991), Williams and early stages are sought by digging in the gravel or by Joannou (1996), Heath and Brinkman (1995a, b), prizingopencracks inbedrockwherenestsofthehost Heath (1997a, b, 1998), Claassens and Heath (1997), ants occur (Heath & Brinkman 1995b). For Phasis EdgeandPringle (1996), HeathandClaassens (2000), Hubner, hollowed out stems ofthe foodplants are ex- Lu and Samways (2001). The number of species for amined where ants are present. For Thestor and Ty- each genus follows Pringle et al. (1994), Ackery et al. lopaedia Tite & Dickson, we search beneath large (1995), Williams (1999) and Heath (2001). A compre- boulders covering ant nests in areas where the adults hensivelistoffoodplants andant-associates forsouth- ernAfrican Lepidopterais foundin Kroon (1999). 3Riodininaeisnotrepresentedin southernAfrica. Volume 57, Number 1 earlystages canbe studiedinthe naturalenvironment. It is nevertheless possible to rear these in captivity with orwithout the host ant. Categories ofAnt-Association and Feeding Strategies There have been manyattempts to categorize feed- ingstrategies and relationships between lycaenids and ants; e.g., Fiedler (1991), DeVries (1991), Pierce (1995), Eastwood and Fraser (1999), Heath and Claassens (2000) and Pierce et al. (2002). The follow- ingthree broad categories ofant-association are used here: (1) 'Notant-associated' (directandcloseinterac- tion with ants is absent or rare, even ifants are pres- ent). (2) 'Facultative' (intermittentlyattended byants but notwholly dependent on them for survival under field conditions). (3) 'Obligate' (dependent on one species ofantforsurvivalunderfield conditions). Threecategories oflarvalfeedingstrategyusedhere 17 18 19 20 are 'algae/lichen-feeding', 'herbivorous' and 'ento- Figs. 1-20. Lycaenidae from southern Africa. 1, Iolaus (Io- mophagous'. The latter term being re-defined by laphilous)trimeniWallengren. 2,Phasistherothero (Linnaeus) fe- Pierce et al. (2002) to mean dependant upon anyin- pmarloet.um3,nuMsyri(Lniansnialeaunsu)sfifceemdaullea.T5r,imAelnoemiadlees.a4,raTnhdeasto(rWpalrloetnugmrneuns) sect-derived resource, and may include homopteran male.6,AloeidespallidagrandisTite&Dicksonmale. 7,Erikssonia secretions, ant regurgitations and/orthe insects them- acraeinaTrimenmale.8,Pentilatropicalistropicalis(DeBoisduval) selves (carnivory). More than one ofthese categories tmiasle.na9t,alTeynlsoipsaed(iWaesstawrodoodny)xsmaarldeo.nyx11(,TrLimeepni)dofcehmraylse.op1s0,tCriigmaerni-i maybe employedduringthe larvalphase. (Bethune-Baker)male. 12,LepidochrysopsoreasoreasTitefemale. 13, Chrysoritis brooksi brooksi (Riley) female. 14, Chrysoritis Genera, Life HistoryandAnt-Associations thysbethysbe(Linnaeus)female. 15,Chrysoritisnigricansnigricans (Aurivillius)male. 16,Chrysoritispalmuspalmus(Stoll)female. 17, For completeness, all 64 lycaenid genera occurring Lycaena orus Stoll male. 18, Lepidochrysops robertsoni Cottrell in southern Africa are included here, whatever their male. 19,Lachnocnemabibulus (Fabricius) female. 20,Axiocerces ant-association. More specific details are shown in amanga(Westwood)male. Table 1 and summarizedin Table2. are known to fly. Rocks underwhichjuvenile Thestor PORITIINAE: Larvae of Pentilini and Liptenini species are found, are often turned over by baboons (together including 13 genera) are clothed with long lookingforThestorlarvae andpupae, and scorpions. hairs and not directly ant-associated; they possess no Study ofbehavior in captivity. Due to the sub- DNO or TOs. Larval food is mostly algae or lichen terranean habits ofmanyjuveniles, close studyofthe (Bampton 1995), butDeloneurawere recordedtaking interactions between ants and larvae in nature is not honeydew from Homoptera in the company of ants feasible. Hence, for taxa like Aloeides, Thestor, Lepi- (Pringle et al. 1994), although ants ignore the larvae dochrysops, Orachnjsops and Trimenia, where a (Jackson 1937). formicarium similar to that described by Claassens Pentilini (three genera): Alaena De Boisduval, (1972, 1974)is required, anestofhostantswitiibrood 1847; Pentila Westwood, 1852; Orniplwlidotos and queen is installedwithin the formicarium. Before Bethune-Baker, 1914. beingintroducedintothenestsectionofthe formicar- Liptenini (ten genera): Durbania Trimen, 1862; ium, larvae areleftamongthe antbroodforabouttwo Durbaniella van Son, 1959; Durbaniopsis van Son, hours. This is to acquire the scent ofthe ant colony 1959; Cooksonia H. H. Druce, 1905; Mimacraea and avoid subsequent attack by ants, but also to see Butler, 1872; Euthecta Bennett, 1954; Teriomima what interaction takes place between larvae and Kirby, 1887; Baliochila Stempffer & Bennett, 1953; brood. Piecesofsuspectedfoodplantarekeptinwater Cnodontes Stempffer & Bennett, 1953; Deloneura within the arena, as describedbyClaassens and Dick- Trimen, 1868. son (1977). Chrysoritis species do not generallyenter MILETINAE: Larval food can be regurgitations antnests butare constantlyattendedwhile feedingon from antsbutis mostlyHomopteraortheirsecretions. thefoodplantandrestinginthedebrisbeneathit;their Homopteraare almostalways attendedbyants butdi- Journalofthe Lepidopterists' Society Table1. LifehistorydetailsforallknownSouthernAfricanlycaenids,showingpresenceofDNOorTOs,larvalfeedingcategory"andant-as- sociation.Abbreviations: * = probablebutunconfirmed. DNO,TOs: + =yes;-=no;Feedingcategory:A= AlgaeorLichenfeeder; H = Her- bivorous;E = Entomophagous.Ant-association: N =none;F=facultative;O=obligate; ?=unknown.Principalsources: 1=ClarkandDickson (1971);2=Pringleetal. (1994);3=Jackson(1937);4= HeathandClaassens(2000);5= Heath(1997);6=BamptonandCongdon(pers.com.); 7 = Stempffer(1967);8 = Henning(1983a,b);9 = Claassens (1976); 10 = EdgeandPringle (1996); 11 = SchloszandBrinkmann(1991); 12= Heath(pers.obs.); 13 = Kroon (1999); 14= Lambom(1914); 15 = HeathandBrinkmann(1995b); 16 =WilliamsandJoannou(1996); 17= Lu andSamways(2001); 18= Larsen(1991); 19= Pennington(1956);20=Atsatt(1981);21= BrabyandWoodger(1994);22= HenningandHen- ning(1982);23= Henning(1984a);24=AckeryandBajan(1990);25=vanSomeren(1974);26=ClaassensandDickson(1977);27=Claassens andDickson(1980);28=FiedlerandHagemann(1992);29ClarkandDickson(1956);30=CongdonandBampton(1995);31 =Edge(1990). Feeding Ant- Principal Genus Species DNO TOs category' association Ant sources PORITIINAE Pentilini(8) Alaena amazoula A 1,29 brainei A 2,6 nyassa A 2,6 margaritacea A 2,6 Pentila pauli A tt swynnertoni A 2,6 tropicalis A 2,6 Ornipholidotos peucetia A 2,12,18 Liptenini(22) Durbania amakosa A 1,12,29 limbata A 2, 12 Durbaniella clarki A 2, 12 Durbaniopsis saga A 2,12 Cooksonia neavei A 2 Mimacraea marshalli A 2 neokoton A 2 Euthecta cooksoni A* 2 Teriomima puellaris A 2 puella A 2 zuluana A 2 Baliochila aslanga A 2 barnesi A 2 neavei A 2 lipara A 2 singlaris A 2 Cnodontes 3species A* It Deloneura sheppardi A 1 mitlari A 2,3,19 subfusca A 2,3,6, 19 MILETINAE Spalgini(1) Spalgis lemolea 3,8,14 Lachnocnemini(32) Lachnocnema bibulus E N 1,8, 14,29 durbani E N 1,2,29 brimo E N* 2 Thestor basutus E O A. custodiens 1,4,16,29 brachycerus E O A. custodiens 12 pictus E O A. custodiens 12 protumnus E A.custodiens 1,12 rileyi E A. custodiens 12 rossouivi E A.custodiens 12 strutti E A.custodiens 4 yildizae E A.custodiens 4 dlcksoni E A.custodiens 1,2,29 +20species E* 0* A. custodiens* 2 Liphyrini(3) Aslauga 3species E* N* 3,6,7, 14 LYCAENINAE Aphnaeini(131) Aphnaeus erikssoni H* o Crematogastersp. 2 hutchinsonii H o Crematogastersp. 1,3,29,31 marshalli H* o* Crematogastersp.* 2 Ciearitis natalensis H o C.castanea 1,2,6,29 ella H o C. castanea 1,2,6, 18 namaqua H o Crematogastersp. 8,6 phanes H o C.castanea 8,6 H o Crematogastersp. 2,6 +5species H* o* Crematogastersp.* 2,6 Lipaphnaeus aderna H o* Crematogastersp.* 6,30 Chloroselas pseudozeritis H o C.gerstaeckeri 2,6,3 argentea H o Crematogastersp. 2,6 mazoensis H o Crematogastersp. 2,6, 19 Volume 57, Number 1 Table 1. Continued. Feeding Ant- Principal Genus Species DNO TOs category' association Ant Zeritis sorhageni ? 2 Axiocerses tjoane H F 1,6,29b H F' 3,6 H F 2,6 Phasis braueri H O C.peringueyi 1,4 clavum H O* Crematogastersp.* 2 pringlei H O C.peringueyi 12,13 thero H C.peringueyi 1,4, 12,29 Tylopaedia sardonyx H C. melanogaster 11,29 Argyraspodes argyraspis H ? Trimenia argyroplaga H O A. custodiens 12 malagrida ? o A.custodiens 15 +3species '? o* A.custodiens* 2 Aloeides apicalis H Monomoriumfridae 4 aranda H o Pheidolecapensis 1.4,29 clarki H 0* Unidentifiedsp.* 1.2 damarensis H o* Unidentifiedsp.* 1.2 dentatis H o L. capensis 2,4,8 depicta H 0* Unidentifiedsp.* 1,2 govoani H 0* Unidentifiedsp.* 1 pallida H,Eh o L.capensis 4 pierus H o L.capensis 4,29 thyra H o L.capensis 2,4,26 trimeni H L.capensis 1,2 rossouivi H o Lepisiotasp. 22 taikosama H o* Unidentifiedsp.* 2,29 almeida H 0* Unidentifiedsp.* 2,29 +39species H o* Unidentifiedsp.* 2 Erikssonia acraeina H Lepisiotasp. 2,23 Chrysoritis adonis H o C. liengmei 5 aethon H o C.liengmei 5 aridus H o Crematogastersp. 5 aureus H C. liengmei 5 azurius H o C. liengmei 5 beaufortia H o C.peringueyi 5 beulah H o Crematogastersp. 5 blencathra H o Crematogastersp. 5 braueri H o C. liengmei 5 brooksi H o C.peringueyi 5 chrysantas H o C. melanogaster 5 chrysaor H o C. liengmei 5,29 daphne H o C.liengmei 5 dicksoni E o C.peringuey 5 endymion H o C.peringuey 5 feltnami H o C.peringuey 5,29 irene H o Crematogastersp. 5 lycegenes H o C.liengmei 5 lyncurium H o C. liengmei 5 midas H o C.peringueyi 5 natalensis H o* Crematogastersp.* 5 nigricans H o Crematogastersp. 5 oreas H o Myrmicarianigra 5 orientalis H o C. liengmei 5 pahnus H o C.liengmei 5,29 pan H o C. liengmei 5 pelion H o* Crematogastersp.* 5 penningtoni H o Crematogastersp. 5 perseus H o C. melanogaster 5 phosphor H* 0* Crematogastersp.* 5 plutus H o C.peringueyi 5 pyramus H o C.peringueyi 5 pyroeis H o Mi/rmicarianigra 5,29 rueyi H o C.peringueyi 5 swanepoeli H o C. liengmei 5 thysbe H o C.peringueyi 5,29 trimeni H o C.peringueyi 5 turneri H o C. liengmei 5 warms H o C. liengmei 5 violescens H o C.peringueyi 5 zeuxo H o C. liengmei 5 zonarius H o C.peringueyi 5 Cnidaria leroma H o A. custodiens 1.5. 12.29 wykehami H o A.custodiens 12 capensis H* o* A.custodiens* 12 Lycaenini(2) Lycaena clarki H N 1. 12 orus H N 1. 12 Journalofthe Lepidopterists' Society Table 1. Continued. Feeding Ant- Principal Genus Species DNO TOs category11 association Ant sources Theclini(47) Amblypodiiti[2 Myrina silenus H F 1,3,14,29 dermaptera H F 1,29 Iolaiti[21] lolaus aemulus H F* 1,2,29 alienus H F 1,2,29 aphnaeoides H p* 2 australis H p* 2 bakeri H p* 2 bowkeri H F 1,2, 12,29 diametra H p* 2 lalos H p* 2 luhia H p* 2 mirnosae H F 1,2, 12,29 nasisii H p* 2,12 obscurus H p* 2 pallene H p* 2,12 penningtoni H p* 2 poultoni H p* 2 sidus H p* 1,2, 12,29 silarus H F 2,12 silas H F 1,2, 12,29 subinfuscata H F 2,12 trimeni H p* 2,8, 12 uiolacea H p* 2,12 Hypolycaeniti(9) Hypolycaena philippus H F 1,3,14,29 lochmophila H p* 2 caeculus H F 2,6 +2species H* p* 2 Leptomyrina liinindo H F 1,2 lara H F 1,2,27,29 pprgias H F 1,2 henningi H F* 2 Deudorigiti[15] 15 Deudorix antalus H F 1,2,29 dariaves H F* 2 dinochares H F 1,2,24 dinomenes H F* 2 diodes H F 1,2,29 lorisona H F* 2 magda H F* 2 penningtoni H p* 2 vansoni H p* 2 caendea H* p* 2 zeloides H* p* 2 Capys alphaeus H F 1,27,29 penningtoni H F 2,12 disjunctus H F 1,2, 12 connexivus H F 2,12 Polyommatini(146) Lycaenesthiti[26] Anthene amarah H F 1,3,29 butleri H p* 1,29 contrastata H p* 2 crawshayi H p* 3 definita H F 1,27,29 kersteni H F P lernnos H p* 1,29 liodes H p* 2,14 lunulata H F 3 wihoni ? O Unidentifiedsp. 3 otacilia H F 1,6,25,29 talboti H p* 1 nigeriae H O Unidentifiedsp. 3 +13species H* p* 2 Polyommatiti[120] Cupidopsis cissus H p.* 1,3 jobates H p* 1 Pseudonacaduba sichela H ? 2 Lampides boeticus H F 1,3,27,29 Uranothaunia antinorii H N* 2 poggei H N 2,6 Volume 57, Number 1 Table 1. Continued. Feeding Ant- Principal Genus Species DNO TOs category" association Ant sources nubifer - - H N 2,3 vansomereni _* H N* 2 Cacyreus dicksoni - - H N 1,2,27 lingeus + - H N 1,3,27,29 marshalli - - H N 1,2,27,29 tespis - - H N 1,2,27,29J virilis + - H N 1,2,27 Harpendyreus notoba + - H F* 1 tsomo + _* H F* 2 noquasa + _* H F* 2 Leptotes pirithous + + H F* 1,3.27,29k brevidentatus + + H F* 1 jeanneli + + H F* 2,29 babaulti + +* H F* 2 pulcher + +* H p* 2 Tuxentius calice + + H F* 1,2 melaena + + H F* 1,2,291 hesperis + +* H F* 2 Tarucus sthyebsapriiss ++ ++ HH FF* 21,27,29 bowkeri + + H F* 1,29 Zintha hintza + + H F 1,2,3 Zizina antanossa + + H F* 1 Zizeeria knysna + + H F 1, 12,28,29 Actizera lucida + + H F* 1,29 stellata + + H F* 1,29 Zizula hylax + + H F* 1,21 Brephidium metophis + + H F* 1,20 Oraidium barberae V ? H F* 1,2 Azanus ubaldus + + H F* 1,29 jesous + + H F* 1,3,29 natalensis + + H F 1,3 monqua + + H F* 1,29 mirza + +* H F* 2 Eicochnjsops messapus + + H F* 1,29 eicotrochilus + +* H F* 2 Hippocrates + + H F* 1 Euchrysops osins + + H F 1,3 barker + H F 1 malathana + H F 1,3, 14 dolorosa + H F 1,2,29 subpallida +* H F* 2 Lepidochnjsops asteris - H,E*'" O* Camponotussp.* 1,2,29" bacchus - H,E* O* Camponotussp.* 1,2,29 ignota - H,E O C. niveosetus 2,8 ketsi - H,E* O* Camponotussp.* 1,2 methymnd - H.E C. maculatus 1,2,29 oreas - H,E C. maculatus 1,2 patricia - H,E O C. maculatus 1,2,29 puncticilia - H,E* O* Camponotussp.* 1,2 trimeni - H,E O C. niveosetus 1,2 variablis - H,E C. niveosetus 1,2 +49species _* H,E* O* Camponotussp.* 2 Orachrysops lacrimosa + H* F* 1,2,29 niobe + H* F*° 10,2 ariadne + H* O C. natalensis 17,2 +7species +* H* F* 2 Oberonia bueronica ? H F 2 Chilades trochylus + H F* 1 Thermoniplias micyfus ? H N 2,6 •'ForFeedingcategory,andAnt-association,seesection"Categoriesofant-associationandfeedingstrategies"above. bAsA.bambana(misidentified). CA.amangaisattendedonlybyPheidolespeciesbutoftenfoundunattended(Bamptonpers.com.). dP.therohasDNObutnotinfinalinstar. eHasDNObutabsentinfinalinstar(alsoA.depicta,A.pallidaandA. thyra). 'DNOpresentinfinalinstar(alsoA.pierus). gDNOabsentinfinalinmstar(Henning1983)butearlierinstarsunknown. ''Herbivorousbutinfinalinstar,feedssolelyonanteggs. 'AsA.larydas(misidentified). JAsC.palemon (misidentified). kAsSyntarucustelicanus(misidentified). 'AsCastaliusmelaena(misidentified). mLepidochnjsopsareherbivorousforfirsttwoinstars,thereaftermainlycarnivorousonantbrood,supplementedbytrophallaxis. "AsLepidochnjsopscaffrariae(mis—identified). "Currentlyregardedasfacultative itcanberearedwithoutants. Journalofthe Lepidopterists' Society Table2. Summaryofant-association: Conf. = basedonpublishedandconfirmedobservations. Predict. = confirmed+ predictedbutun- confirmedassociations. Obigate Ficultative None Unknown Taxon Totalspecies Conf. Predic. Conf. Predic. Conf. Predic. Conf. Predic. PORITIINAE 30 Pentilini 8 8 8 Liptenini 22 18 22 4 MILETINAE 36 Spalgini 1 1 1 Lachnocnemini 32 9 29 2 3 21 Liphyrini 3 3 3 LYCAENINAE 326 Aphnaeini 131 66 126 3 3 62 2 Lycaenini 2 2 2 Theclini 47 20 47 27 Polyommatini 146 9 62 15 73 8 10 114 1 TOTALS 392 84 217 38 123 39 49 231 4 rect interaction between ant and larva maynot neces- SouthAfrica. EarlyinstarlarvaeofLachnocnemabibu- sarilyoccur. lus feed on young psyllids (Homoptera) and their Liphyrini (one genus): Aslauga Kirby 1890 (14 droppings. Mature larvae creep up behind adult psyl- Afrotropicalspecies, three insouthernAfrica). Scarce, lids, seizetheirwings, anddevourthem. Larvaedonot arboreal butterflies with a distinctive wingshape. Vir- associatewith ants directlybutants are always present tuallynothing is known ofthe earlystages ofsouthern tendingthe Homoptera. AfricanAslauga species but suspected to be the same Thestor Hiibner, 1819 (29 species, all endemic to as those observed by Jackson (1937) and Lamborn southern Africa). Medium-size, moth-like, with stout (1914). Larval skin is leathery, the carapace being ex- bodies, and either blackish oryellow and brown; they traordinarily heavy; head small and carried on an ex- always settle on the ground or rocks. Adults possess a tendable neck which can be retracted under a cara- vestigial proboscis and do not nectar. Most Thestor pace; TOs present, but DNO absent. Although the species are univoltine. All species appear to associate presence ofTOs is unique in this subfamily they are with Anoplolepis (Formicinae) ants (Claassens & small anddo not evert. Larvae feed on Coccidae (Ho- Dickson 1980, Cottrell 1984, Claassens & Heath moptera) tendedbyCrematogasterantsthatdonotin- 1997). During the first three instars ofT. protumnus teract directlywith the larvae. ariclus Van Son and T. basutus (Wallengren), larvae Spalgini (one genus): Spalgis Moore, 1879 (four feed on Homoptera (Clark & Dickson 1960, 1971, Afrotropical species, one in southern Africa). Larvae Williams & Joannou 1996). In T. yildizae Kocak, T. pic- feed on Coccidae (Homoptera), do not associate with tusVan Sonand T. basutus foodofthe finaltwoinstars the ants directly, but ants are always present tending is regurgitated food from ants (Fig. 21). We suspect Homoptera. Larvae cover themselves with awaxy se- that all Thestor are entomophagous but only in T ba- cretion produced by the Homoptera and lack both sutus is the life history fully known. The remarkable DNO andTOs (see Lamborn 1914, Jackson 1937). Thestorlarva (Fig. 22) lacks both DNO andTOs, and Lachnocnemini (twogenera): Inthese genera,lar- possesses an extremely small headwith an extendable vae lack DNO and TOs. Lachnocnema Trimen & fleshy "neck". Larval antennae are elongate and pro- Bowker, 1887 (38 Afrotropical species, 3 in southern ject forward; each with a long terminal seta. In Africa). Feeding habits ofL. bibulus Fab. have been T yildizae these antennae remain in contact with the describedby South African authors, but byadifferent ant's mandibles duringexchange offood. It is possible account ofLachnocnema from Kenya (Cripps &Jack- these antennae simulate the ants mandibles, facilitat- son 1940), larvae were carried by ants down to their ingthelarva's acceptanceas anestmateand/ortostim- nest, and trophallaxis occured. The genus was revised ulate the ant to regurgitate. by Libert (1996a-c) who described 25 new species, Williams and Joannou (1996) observed females of hencethelifehistoryaccounts from Kenyamostprob- Thestor basutus capeneri (Dickson) ovipositing on ably apply to what are now considered different blades ofgrass infestedbygrass-feedingcoccids Pulvi- species. Accounts are given by Clark and Dickson naria iceryi (Signoret) (Homoptera: Coccidae) which (1971) of L. bibulus and L. durbani Trimen from in turn were tendedbyAnoplolepis custodiens Smith Volume 57, Number 1 !•.-"-ft* ,.| O-V Fig.21. FinalinstarlarvaofThestoryildizaeKogakbeingfedre- gurgitationsfroma"Pugnaciousant"AnoplolepiscustodiensF.Smith. ants. Theywere observedto oviposit on awidevariety ofvegetation, oftenwithout ants or Homopterabeing present. In thewild and in captivitythe first three in- stars were predaceous on coceids, the ants taking no interestinthelarvae. Aftermoulting, fourthinstarlar- vae in captivity refused to feed on coceids and were 1 cm left in the formicarywhere they entered the artificial Fig. 22. FinalinstarlarvaofThestoryildizae, lateralview(up- ant nest. While in the ant nest, they were ignored by per),dorsalviewwithheadextended(lower). Scalebar= 1cm. the ants but subsequently died, presumably ofstarva- tion (Williams &Joannou 1996). Similar observations The behavior of T. basutus differed from the ob- were recorded by Clark and Dickson (1960, 1972) for served behavior of T. yildizae and T. pictus larvae which solicited regurgitations from individual passing T. basutus basutus. In November2002 fourfinalinstarlarvaofT. basu- ants. The ant species associated with Thestorhave so tus basutus (Wallengren) were taken from an farbeen recordedasA. custodiens butthisiscurrently Anoplolepiscustodiens antnestin KwaZulu-Natal and believed to constitute a species complex. A prelimi- narymolecular studyofA. custodiens at Harvard Uni- studied in captivity together with Anoplolepis ants from anearbylocality(AH, AJMC, S. P. Quek). Alarva versitysuggests that at least three distinct clades exist was often seen to approach two ants engaged in (S.P. Quekunpublished). trophallaxis and insert its headbetween theirs. It pro- LYCAENINAE: Some ant-association occurs in all ceededtoimbibe regurgitations passedbetweenthem tribes except Lycaenini. Almost all species have a DNO andmosthave TOs. andcontinuedtoacceptregurgitations fromthe donor antafterthe otheranthaddeparted. Thelarvawas oc- Theclini (six genera):DTNheOnumber oflarval instars casionallyseento'pull'onanteggs andlarvaeanddrag is normallyfourandthe first appears in the sec- them beneath its carapace; it is assumed these were ond or third instar, the TOs appearing in the second eaten. Thelarvaalso appearedtoscavenge fordetritus instarexceptinendophyticfeeders,wheretheyareab- on the nest substrate. Although T. basutus appears to sentin all instars. utilize four food sources in its larval stage, during the Myrina Fabricius, 1807 (five Afrotropical species, weekitwas studied (priortopupation) the majorfood two in southern Africa); Iolaus Hiibner, [1819] (116 was obtained by trophallaxis. An earlier study in cap- Afrotropical species, 21 in southern Africa); Hypoly- caena Felder, 1862 (extralimital4 28 Afrotropical tivityofT. basutus larvae from KwaZulu-Natalwith an : antspecies from CapeTownresultedinthelarvafeed- species, five in southern Africa); Leptomyrina Butler, ing on detritus only and then dying after almost four 1898 (nine Afrotropical species, four in southern weeks without anytrophallaxis having been observed Africa); Capys Hewitson, 1965 (14 Afrotropical (Heath & Claassens 2000). This would indicate larvae species, fourin southern Africa); Deudorix Hewitson, 1863 (extralimital: 89 Afrotropical species, nine in arehighlyspecific to certainAnoplolepis ants. The larva occasionally 'groomed' an ant, the latter southern Africa). All sixgeneraare regarded as having remaining motionless while the former mayhave de- a facultative association with ants. Ants (often Cre- rived some form of detritus from the process (AH, matogasterspecies) maybe presentbut do not attend AJMC unpublishedobs.). This groomingbehaviorwas the larvae permanently, and larvae do not depend on a(lPsoolyroemcmoartdiendi)inatnhde citasseanotf-aLsespoicdiaotcehryCsaomppsonloartvuase gaennyesrpaecpioessseosfsanDtNfoOrsaunrvdivTaOl.sLbaurtvatehoosfedioefLfierpstttohmrye-e maculatus Fab. (Formicidae) (Claassens 1976). 4Extralimital:GenusalsorepresentedoutsideAfrica. — 10 Journalofthe Lepidopterists' Society rina, Capys and Deudorix are endophytic and lack bythe host ant. The DNO was present in the second TOs (Clark& Dickson 1971). Leptomyrina larvae feed instar, but secreted no honeydew, however, when inside the fleshy leaves of Crassuleaceae (Jackson, everted it attracted, but stupified nearby ants. When 1937). Capys larvae feed inside Protea flower buds offered a red Homopteranjuvenile, the second instar (Proteaceae) (Murray 1935, Clark & Dickson 1971); larva ate it andhalfa second one, but died the follow- the hollowed out buds are later often occupied by ing day. The final instar also fed on ant regurgitations Crematogaster ants (AH pers. obs.). Deudorix larvae living andpupatingwithin the carton nest ofthe host feed inside pods and immature fruit of a variety of ant Crematogaster peringueiji Emery. It is assumed trees (Pinhey 1965, Clark& Dickson 1971). thattheinterveningthreeinstarshadthesamefeeding Aphnaeini (14 genera): All known life histories of behavior as first and last instars. In areas where C. theAphnaeiniindicate anobligateant-association. The dicksoni flies, armored scale insects (Homoptera) are number oflarval instars is normallysix, the DNO first always nearby and maysomehowbe necessaryforthe appearing in second orthird instars, but TOs occurin survival ofthe larva (Heath 1998). The DNO was still all instars. presentin the sixth (final) instar, although itwas infre- Chrysoritis Butler, 1898 (42 species, all endemic to quently visited by ants. The final instar also had spe- southern Africa). A revision and molecularphytogeny cialized setae on each segment that frequently at- ofChrysoritis canbe foundin Heath (2001) andRand tracted the host ant who seemed to nibble at them. et al. (2000). The genus comprises small to medium- Thesesetae appearedasacurvedstructureresembling sized robust butterflies, associated with open veld, a bottle-brush, and are illustrated by Heath (1998). coastal and montane fynbos5 Most Chrysoritis are Heathand Brinkman (1997b) inferredthatinthewild, . multivoltine, except in montane areas, but C. dicksoni females are only stimulated to ovipositbyants attend- (Gabriel) which flies in non-montane localities, is en- ingthis unidentifiedspeciesofscaleinsect. Colonies of tomophagous and univoltine. With this one exception, C. dicksoni adults occupy small areas, seldom larger Chrysoritis are allherbivorous feedingon awidevari- than a tennis court, and where females oviposit on a ety ofplants (see Heath 1997a) and can be reared in widevarietyofplants nearthe hostantnest. captivity without ants. They are nevertheless consid- Aloeides Butler, 1819 (58Afrotropical species, 53 in ered obligate, as larvae are continuously attended by southern Africa). A large genus ofsmall to medium- ants andovipositiononlyoccurs inthepresence ofthe size brown or orange butterflies obligately associated correctantspecies (Heath 1997a). Crematogasterants with ants. All species are found in open or grassland are the most common associates for Chrysoritis, but habitat. The genus is in need oftaxonomic revision, as one species ofMyrmicaria (Myrmicinae) is known to webelieveitcontains manytaxaofdubious status. Un- associate in two species ofthis genus (Heath 1997a). til recently, the onlyant genus known tobe associated Excepting C. dicksoni, larvae in nature rest in a corral with Aloeides larvae was Lepisiota (=Acantholepis) (or byre) beneath the food plant and are tended by (Formicinae). However, two additional ant hosts have three or more ants. Larvae were often found singlyor recentlybeen discovered (Heath &Claassens 2000) inpairs butas manyas five orsixofvaryingsizes could Monomoriumfridae Forel (Myrmicinae) andPheidole be foundtogetherwithin acorral (Heath 1997a). capensis Mayr (Myrmicinae). Larval food plants are In Chrysoritis the DNO appears in the second in- species ofAspalathus (Fabaceae), Hermannia (Stercu- star, a feature shared onlywith Crudaria Wallengren. liaceae), Sida (Malvaceae) (Kroon 1999), and Gnidia The larva's DNO is frequently visited and stimulated (Thymelaeaceae) (A. Gardiner pers. com.). Aloeides bytheant'santennaeandthesecretionis eagerlytaken larvae have TOs in all instars but the DNO first ap- bythe ant. TheTOs are active, everted quicklyand as pears in the third. In some species, e.g., A. apicalis quicklywithrawn; this happens whenever the larvais Tite & Dickson, A. pallida grandis Tite & Dickson, disturbed. When ants are over-eagerto access honey- A. thyra (Linnaeus) and A. dentatis (Swierstra), the dew, the larvawill evertits TOs causingthem to jump DNO is absent in the final instar (Heath & Claassens in alarm. Among this large and otherwise herbivorous 2000, Henning 1983a, b). However, in at least four genus, C. dicksoni larvaeare entomophagous andwere species,A. pierus (Cramer)A. gowani Tite & Dickson, observed in the field and laboratoryby Heath (1998). A. trimeni southeyae Tite & Dickson and A. aranda DNO The first two instars fed on ant regurgitations but (Wallengren), larvae retain their until pupation stayed on the plant close to scale insects, also tended (Clark& Dickson 1971, Heath & Claassens 2000). EarlyinstarlarvaeofA. pallidagrandis are assumed 5 Fynbos: Characteristic treeless shrubland vegetation of the to feed on species ofAspalathus always found close to southernandsouth-westernCapeofSouthAfrica. wheredielarvaearefound. HeadiandClaassens (2000)