Myrmecophilous and Apidophilous Soft Scale of the New World (Hemiptera: Sternorrhyncha: ) TAKUMASA KONDO Department of Entomology, University of California, INTRODUCTION Soft scales belonging to the Myzolecaniinae are often called myrmecophilous, however, there may be other One Shields Avenue, Davis, CA 95616 Toumeyella virginiana coccids in different subfamilies not included in this study that are closely associated with . The Myzolecaniinae has a worldwide distribution and contains the most derived insects in the Coccidae. Morphological features have evolved in such a way that these coccids can no longer survive without attendance Pseudophilippia quaintancii by their symbiotic (rarely bees; the term apidophilous has been herein used to referred to the stingless bee- associated species). However, there are some exceptions, i.e. Toumeyella erythrinae has been well studied but no hymenopterans have ever been observed attending them; Cryptostigma silveirai and Cryptostigma sp. 10 are hypogeal in habit feeding on the roots of its host and are not associated with Hymenoptera. The original descriptions of many of the species included in the Myzolecaniinae lack information on their biology, thus their T. liriodendri association with Hymenoptera remains unknown. Neolecanium Toumeyella cornuparvum The Myzolecaniinae in the New World is represented by the following genera: Akermes , Aztecalecanium, sp. 1 Cryptostigma , Cyclolecanium , Megasaissetia , Neolecanium , Octolecanium , Pseudophilippia and Toumeyella . T. liriodendri The Myzolecaniinae are thought to be composed of several non-related genera which share common features such as: the reduction in size of legs, antennae and anal tube; the increase in size of spiracles; lack of eyespots; Toumeyella pinicola T. quadrifasciata Toumeyella pini and other shared characters that could be a result of parallel evolution in the adult female morphology. Several scale insects treated in the present study are known to be agricultural pests. For example, Cryptostigma silveirai Toumeyella mirabilis Toumeyella is a serious pest of grape vines in Brazil, and Toumeyella erythrinae is a pest of erythrina trees in Mexico. parvicornis Toumeyella turgida Interestingly the two species are not closely-associated with ants. In the USA, T. parvicornis often causes serious damage to pine trees. The hosts of Cryptostigma sp. 10. is a species with a potential of becoming an Toumeyella lignumvitae agricultural pest since its hosts includes oil palms, bananas, Manila hemp, orchids and pineapples. This study presents our current understanding of New World - and bee-coccid relationships, their ecology and Cryptostigma biogeography. inquilina Photo courtesy of Penny Gullan Toumeyella Aztecalecanium T. cubensis Toumeyella sallei Biology of a stingless-bee-associated coccid in Brazil cerifera colimae Neolecanium Neolecanium Neolecanium derameliae tuberculatum chilaspidis T. erythrinae

Octolecanium Neolecanium guatemalensis herrerae Akermes Cryptostigma punctatus Neolecanium Akermes Neolecanium Cryptostigma Cryptsotigma Cryptostigma biorbiculus manzanillense imbricatum townsendi sp. 1 sp. 3 sp.5 Cyclolecanium Cryptostigma Neolecanium Neolecanium hyperbaterum sp.7 leucaenae plebeium

Ant trail of Crematogaster sp. Cryptostigma sp.4 Harvesting Scales!? Cryptostigma Cryptostigma C. reticulolaminae Akermes Cryptostigma Most species of the New World Cryptostigma and the Australasian Cryptostigma quinquepori sp. 2 cordiae Akermes colombiensis sp. 8 genus Myzolecanium have only been collected from hollow branches, twigs sp. 10 or tree trunks and tended by ants and rarely stingless bees. Mr. Stuart Donaldson in charge of plantings at the Australian Natl Botanic Gardens in Canberra shown here chain-sawing an Eucalyptus tree. Myzolecanium endoeucalyptus found inside tree trunk (inset).

Comparison of a non-ant-specialized coccid with an ant-specialized coccid New World Myzolecaniinae: Distribution, Hosts and Notes Cryptostigma sp. 9

Spe cies Known Distribution Hosts Associated Hymenoptera Remarks Akermes bruneri Cockerell Megasaissetia Argentina, Paraguay, Uruguay Celtis tala Azteca sp. Type species of the genus Cryptostigma brasiliensis Akermes colombiensisKondo & Williams Colombia avocado;guava;Ocotea ;Melastomataceae Azteca ; Crematogaster; Myrmelachista Congeneric withA. bruneri Ak ermes cordiae Morrison Panama Cordia alliodora Cryptocerus sp. Doubtly congeneric guadua Mesolecanium Akermes monilis (Cockerell) Brazil Megasaissetia undetermined host None reported Not congeneric argaformis Akermes punctatus (Cockerell) Grenada inflata Citrus medica v. acida None reported Congeneric withA. bruneri Akermes riograndensis Hempel Brazil Schinus dependens None reported Congeneric withA. bruneri Akermes townsendi (Cockerell) Mexico Citrus sp. None reported CongenericA. with bruneri Ak ermes verrucosus (Signoret) Uruguay undetermined host None reported Incertae sedis. ialMater missing. A. xylosma Granara de Willink Argentina Citrus sp.; Astrapaeae sp. None reported IdenticalMallococcus to lanigerus Neolecanium Aztecalecanium colimae (Cockerell) Mexico undetermined host Azteca sp. Monotypic genus amazonensis Cryptostigma biorbiculus Morrison Colombia, Costa Rica, Panama Cordia ; Croton ; Tetrathylacium Aztecaspp.; Pseudomyrma sericea Congeneric withC . inquilina Cryptostigma Mesolecanium Cryptostigma inquilina (Newstead) Widespread in and polyphagous 4 ant species in 4 subfamilies Type iesspec of the genus marmoratum Cryptostigma quinquepori (Newstead) Colombia, Brazil, Grenada, Guyana, Suriname, T.Tobago. sp. 6 polyphagous 4 ant species in 3 subfamilies Congeneric with C. inquilina C. silveirai Cryptostigma reticulolaminae Morrison Costa Rica, Panama, Mexico Cordia ; Triplaris americana Pseudomyrmex triplaris Congeneric withC. inquilina C. saundersi T. paulista Cryptostigma saundersi Laing Mexico undetermined host Azteca sp. Congeneric with C. inquilina Cryptostigma silveirai (Hempel) Brazil roots of Vitis uvifera None reported Pest of grapes; congeneric Cryptostigma sp. 1 Mexico Sambucus sp. None reported only collectedex wooden crates Cryptostigma sp. 2 Ecuador Sapium utile Pseudomyrmex viduus Congeneric withC. inquilina Akermes bruneri Cryptostigma sp. 3 Costa Rica Cecropia spp.; Triplaris sp. 3 species of Azteca Congeneric withC. inquilina Cryptostigma sp. 4 Costa Rica, Ecuador, Panama "cedrus tree" Crematogaster stolli Congeneric withC. inquilina Cryptostigma sp. 5 Guatemala Enterolobium cyclocarpum Pseudomyrmexsp. Congeneric with C. inquilina Cryptostigma sp. 6 Bolivia Caesalpinia paraguariensis Schwarzula timida; Pleb eia sp. *Associated with stingless bees Neolecanium A. Hemilecanium mangiferae , B. Cryptostigma sp. 4, Cryptostigma sp. 7 Colombia Avicennia germinans Pseudomyrmex sp. cf. fortis . Congeneric withC. inquilina craspeditae Akermes a typical non-ant-associated coccid a typical ant-associated coccid Cryptostigma sp. 8 Venezuela Citrus sp. None reported CongenericC. with inquilina Octolecanium Akermes Cryptostigma sp. 9 Brazil Campsiandra angustifolia Schwarzula coccidophila *Associated with stingless bees riograndensis monilis Cryptostigma sp. 10 Colombia, Costa Rica, Ecuador, Panama roots numerous of plants None reported Hypogeal in habit;ential pot pest perconvexum -Symbiotic association with tending -Symbiotic association with tending Cyclolecanium hyperb aterum Morrison Panama Cordia alliodora Pseudomyrma;Camponotus;Azteca;Cremat. Monotypic genus Megasaissetia brasiliensis Hempel Brazil Hymenoptera facultative or absent Hymenoptera facultative or obligate undetermined host None reported Not congenericM. with inflata Akermes Megasaissetia inflata Cockerell Mexico -Eyes present -Eyes absent tree named "laurel" None reported Type species ofgenus the xylosma Megasaissetia nectandrae Hempel Brazil -Anal plates with few 3 or 4 setae -Anal plates with 4 to 21 setae Nectandra sp. None reported Incertae sedis. Material missing. -Anal tube well developed -Anal tube reduced or absent Mesolecanium argaformis Hempel Brazil plant named "canela poca" None reported Congenericth Toumeyella wi -Dorsal setae usually present -Dorsal setae present or absent Neolecanium derameliae (Morrison) Panama undetermined host Azteca sp. Not congeneric N.w/ imbricatum Mesolecanium marmoratum Hempel Brazil -Spiracles rather small -Spiracles rather large ex "canella branca & c. poca" None reported Congenericwith Toumeyella Neolecanium amazonensis Foldi Brazil, Colombia Pourouma cecropiaefoliae found in ant shelters Not congenericN. w/ imbricatum Inside view of a nest of a stingless bee, -Spiracular sclerotization absent -Spiracular sclerotization often present Neolecanium chilaspidis (Cockerell) Mexico Chilopsis linearis, Chilopsissp. None reported Congeneric with Toumeyella Schwarzula timida (Apidae: Meliponini) -Antennae long, segments distinct -Antennae short, segments indistinct Neolecanium cornuparvum (Thro) USA Magnolia spp. None reported Not congenericN. w/imbricatum associated with Cryptostigma sp. 6 -Legs normal, segments distinct -Legs reduced, segments indistinct Neolecanium craspeditae Morrison Panama, Trinidad & Tobago Cordia ; Mangifera indica Azteca trigona Not congeneric w/N. imbricatum Neolecanium derameliae Morrison Panama - Usually found on leaves or externally on -Rarely found on leaves. Often found with ants undetermined host Azteca sp. Not congeneric N.w/ imbricatum Neolecanium herreraeCockerell Mexico Agave sp. None reported Congeneric Toumeyellawith its host. Not found inside woody domatia inside woody domatia, hollow stems, twigs or Neolecanium imbricatum (Cockerell) USA Mimosa sp. None reported Type species of the genus Honey pots Neolecanium leucaenae (Cockerell) Mexico nor hollow stems, twigs or branches branches Leucaena sp. None reported Not congenericN. w/ imbricatum Neolecanium manzanillense Cockerell Mexico Mimosa sp. None reported Congeneric Toumeyellawith Neolecanium plebeium Cockerell Mexico ACKNOWLEDGEMENTS Ficus sp. None reported CongenericToumeyella with Neolecanium subterraneum Hempel Brazil roots of undetermined host None reported Incertaeis. sed Material missing. Many thanks to João Camargo for allowing me to use his photos and for sending me material of Cryptostigma Neolecanium tuberculatum (Town. & Ckll) Mexico Soft scales plant named "cafetillo" None reported Congeneric Toumeyella with sp. 10., to David Roubik for the photo and material of Cryptostigma sp. 6, to Mike Williams for his assistance in Neolecanium urichi (Cockerell) See Cryptostigma quinquepori See Cryptostigma quinquepori See Cryptostigma quinquepori Identical to C. quinquepori collecting Toumeyella parvicornis and Toumeyella sp. 1, and for the loan of material, to Douglass Miller for the Octolecanium guatemalensisKondo & Williams Guatemala undetermined host None reported Genus closeToumeyella to loan of material, to Penny Gullan for photos and loan of material, to Deborah Gordon and Rodolfo Dirzo for Octolecanium perconvexum(Cockerell) Brazil Nectandra sp. None reported Genus close Toumeyella to Photo courtesy sending me material of Aztecalecanium and Cryptostigma reticulolaminae , to Jon Martin for the loan of Pseudophilippia quaintancii Cockerell USA David Roubik Pinus spp. None reported Genus close Toumeyella to BOLIVIA Toumeyella cerifera Ferris Mexico material, and to Cory Unruh for assistance in designing the poster. Many of the undescribed species of Albizzia occidentalis None reported Not congeneric withT. mirab ilis Toumeyella cubensisHeidel & Kohler Cuba Cryptostigma were collected by Jack Longino and Phil Ward, many thanks to them, and all who have help me Citrus spp. None reported (But see remarks) T. lignumvitae junior synonym? Toumeyella erythrinaeKondo & Williams Mexico gather material for this study. This research was supported by grant DEB-0118718 from the U.S. National Erythrina coralloides None reported Pest of street trees in Mexico city Toumeyella lignumvitaeWilliams USA Science Foundation (Partnerships for Enhancing Expertise in program) to P.J. Gullan Guaiacum sanctum Camponotus abdominalis floridanus Identical to Toumeyella cubensis Toumeyella liriodendri(Gmelin) USA Liriodendron tulipifera , Magnolia ants pretect them against predators Known as a pestof its hosts Toumeyella mirabilis (Cockerell) Mexico, USA LITERATURE CITED Prosopis juliflora v. glandulosa Crematogaster sp. (see photo) Type species of the genus Toumeyella nectandraeHempel Brazil Camargo, J.M.F. & Pedro, S.R.M. 2002. Mutualistic association between a tiny Amazonian stingless bee and a Nectandra grandiflora None reported Congeneric with T. mirabilis wax-producing scale . Biotropica 34(3): 446-451.