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PROC. ENTOMOL. SOC. WASH. 105(1), 2003. pp. 186-194

A GREGARIOUS, MYCOPHAGOUS, MYRMECOPHILOUS , AMYDRIA ANCEPS WALSINGHAM (: ), LIVING IN ATTA MEXICANA (F. SMITH) (HYMENOPTERA: FORMICIDAE) SPENT FUNGAL CULTURE ACCUMULATIONS

Sergio R. Sanchez-Pena, Don.ald R. Davis, and Ulrich G. Mueller

(SRS-P. UGM) School of Biological Sciences. University of Texas. Austin. TX 78712, U.S.A.; (DRD) Department of Systematic Biology, Entomology Section, National Mu- seum of Natural History. Smithsonian Institution. Washington. DC 20560-0127. U.S.A. (e-mail: [email protected])

Abstract. —The lepidopteran Ainydria aiiccps Walsingham (Acrolophidae) is reported for the first time as a myrmecophile. Its gregarious larvae feed on the exhausted fungal substrate accumulations outside mature colonies of the Mexican leaf-cutting ant. Atta vie.xicana (Smith), a fungus-growing ant in Mexico. This constitutes the second report of an acrolophid myrmecophile. Morphology of the principal life stages of A. anceps are described, as well as its general natural history. No interactions were observed between Ainydria larvae and A. nie.xicaiui, although the larvae of A. anceps are attacked by ich- neumonid and tachinid parasitoids. Chalcids (primary or secondary parasitoids) also are associated with A. anceps larvae. Thus, there are potentially five trophic levels in this system: fresh plant material Atta fungal symbiont Aniydria anceps—ichneumonid and tachinid parasitoids—chalcid hypeiparasitoids.

Kev Words: Acrolophidae. Aniydria. Atta. biology. Formicidae. leaf-cutting ant. Mexico, mycophagous, myrmecophile

The attine leaf-cutting, fungus-growing strate consists mainly of fungal and plant ants, Atta and Acromyrmex spp., utilize cell walls and is disposed of by the ants. large amounts of plant biomass for the sub- The different species of attine fungus-grow- tenanean cultivation of the fungal symbi- ing ants show at least two strategies for dis- onts (Basidiomycetes: Agaricales: Lepiota- posal of the exhausted fungal substrate: ceae) they use as food (Waller and Moser some species (most Atta species, such as

1990, Mueller et al. 1998). The fungal Atta texana (Buckley) and A. cephalotes L.) strains cultivated by Atta and Acromyrmex create special subterranean galleries where have been identified as species of the mush- the used up fungal substrate is stored (Wal- room genus Leiicoagariciis. principally ler and Moser 1990); other species take this

Leucoagariciis gongylophorus (Mciller), as substrate to the outside and dump it in well as similar species as L. weberi Mucho- "garbage piles" at variable distances from vej, Delia Lucia and Muchovej (Bononi et the nest. Species such as Atta mexicana al. 1981. Fisher et al. 1994. Pagnocca et al. (Smith), Trachymyrmex turrifex (Wheeler) 2001). After overgrowth by the fungus and (S. Sanchez-Pena, personal observation), subsequent harvesting of fungal biomass by and A. colonihica Guerin (Anderson and the ants, the manured, compostlike sub- Ratnieks 2000, Hart and Ratnieks 2001, U. VOLUME 105. NUMBER I

Fiy. I. A mature colony of ,4/;(( iin-\iciiihi in the urban area ol Monterrey. Mexico. The substrate accu-

mulalions on the .street by the curb (a) consist ol the spent lunyal material (dump.s) characteristic of this leaf- cutter ant.

G. Miiellef. personal observation) fVeqiient- were collected at several localities in Mex- ly deposit tiie piles adjacent to the nest. The ico. During June and September 2(XX), gre- Ana substrate dumps, whether subterranean garious larvae of Aiuydria aiucps Wal- or exposed, constitute an accumulation of singham were discovered living in these ex- organic matter that attracts an abundant and ternal dumps in Monterrey, Santiago, and diverse community of invertebrates (Waller Guadalupe, in the State of Nuevo Leon, as and Moser 1990) and microorganisms well as in Queretaro, in the State of Que-

(Rogers et al. 1995. Hart and Ratnieks retaro. Queretaro is approximately 800 km 2001, Sanchez-Pena, unpublished observa- from the other localities. Beutelspacher tions). (1977) previously had reared Aniydria an- Atra nu'xictinii (Smith), the Mexican leaf- ceps (which he redescribed as a new spe- cutting ant, is a widespread fungus-grower cies, Acrolophus socialis) without noting its in Mexico and parts of Central America. association with leaf cutting ants. Larvae of This species eliminates the exhausted, com- this species were reported by Beutelspacher

postlike, fungal substrate by dumping it on as living in tubes within a compact mass or

a garbage heap outside the nest (Fig. 1). "colony," resembling a termite nest. Beu-

The exhausted fungal substrate is made up telspacher's specimens were collected at the of particles or granules up to a few milli- Estacidn de Bitilogia Chamela, Jalisco, meters in diameter. In both Attn coloinbica Mexico.

and A. niexicana, these external dumps can Walter et al. ( 1938) reported another, but

be more than two feet tall and have a vol- not congeneric acrolophid, "Ainyciha" coii- ume of several gallons. fiisella Dietz, from the subterranean cham- In May-September 2000, samples of as- bers where the Texas leaf-cutting ant, Atta sociated biota found on A. iiicxiciiiui dumps tcxuiui (Buckley), accumulates the spent PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON fungal substrate. This appears be the only- Thorax: Light brown dorsally and ventral- previous record of an acrolophid myrme- ly, heavily iiTorated with dark brown dor- cophile. Walter et al. (1^)38) collected lar- sally. Forewing length: d, 4.5-1 1.0 mm; 9,

\ ae and adults from these subterranean 6.5-13.0 mm. Forewing light brown, vari- waste chambers. The utilization of the sub- ably irrorated with dark brown scales until teiranean chambers of .4. texcma (some of often appearing generally dark brown; a which are more than 2 m below ground sur- more or less distinct pattern of dark brown face) probably requires adaptations, behav- markings along costa, with largest forming iors, and cues different from those required an inegular, broadly U-shaped band from to exploit the exposed heaps of A. me.xi- basal third of costa to apical third: base of cana. The present deposition of Walter's wing with an oblique, dark basal band; an- specimens is unknown and, consequently, other large band extending Va-Vi across dis- the identification of the moth could not be tal 'A of wing; fringe light brown, irrorated verified. Larvae of both Amydria and Ptil- with dark brown. Hindwing uniformly light opsaltis. the allied genus which includes grayish brown to dark brown; 6 frenulum confuselki. are known to be scavengers on a simple, stout spine; 9 usually with 4 plant debris as well as guanophiles in caves smaller spines. Foreleg without epiphysis;

(Davis 2000, Davis et al. 1986, Davis and light brown, heavily inxirated with dark Robinson 1998). brown over coxa and femur; tibia mostly dark brown with two light brown rings at AiiiyJrici cinccps Walsingham middle and apex; tarsomeres dark brown, with basal and apical light brown rings; Amydria anccps Walsingham Amydria aii- ceps Walsingham 1914: 363. — Davis midleg similar to foreleg in color; spurs light brown; hindleg uniformly light brown 1984: 20: 2000: 481. except for suffusion of darker scales dor- Acrolophus socialis Beutelspacher 1977: sally. Abdomen: Varying from uniformly 145. —Davis 1984: 20 (synonym o^ Amy- light in paler specimens to dark dria anceps). brown brown dorsally and light brown ventrally in Adult (Figs. 2-?).—Head: Pale buff darker forms. with darker brown scales concentrated near Male genitalia (Figs. 4-8): Uncus deep- vertex and lateral over occipital tufts, to al- ly bifid. Tegumen an elongate niinow dorsal most entirely dark brown. Vertex and oc- ring. Vinculum shoit, broadly U-shaped, cipital areas rough with semi-erect scales; with a slight median indentation (Fig. 4). frons usually less rough: scales slender with Gnathos fused apically into a nanow U- mostly bidentate, sometimes tridentate api- shaped sclerite. Vaha simple, nearly as ces. Antenna filiform, —0.4 length of fore- long as genital capsule, slender, tapering to wing: scape smooth, buff to dark brown: even more slender cucullus (Fig. 6). Ae- flagellum buff to brown, with a single an- doeagus —0.8 the length of valva. moder- nulus of slender scales per segment. Haus- ately broad and flat to apex; apical third lat- tellum and maxillary palpus vestigial, nor- erally separated into a larger, more mem- mally not visible on uncleared head. Labial branous dorsal half and a sclerotized. acute palpus slightly upcurved, with a strong ven- ventral half (Fig. 8); cornuti absent. tral scale brush, especially prominent on Female genitalia (Fig. 9): Posterior segment IL palpus buff, variably marked apophysis short, approximately as long as with dark brown, especially laterally; 2-3 the eighth abdominal segment. Lamella an- dark bristles arising laterally from 111, and tevaginalis — smoothly cur\ed. Ductus bur- up to 7 bristles from II; segment III elon- sae thickened, short, less than half the gate, slender, smooth, sometimes with a length of posterior apophysis, gradually en- dark median rins of dark brown scales. larging to mostly membranous corpus bur- VOLUME 105. NUMBER 1

^:'^*^

'- , e^t . \

Fies. 2-3. Adults at' AniYclria , Male, forcwine Icti'jth S.."! mm. .^. Female, forewing leimlh II

sae which extends about 3X length of along caudal half of corpus anterior to junc- apophysis; a small accessory bursa branch- tion of accessory bursa; anterior margin of ing off caudal end of corpus bursae at com- spinule patch deeply excavated. Ductus mon juncture with ductus bursae; basal, seminalis joined to corpus bursae from cau- ventral half of accessory bursae wall with dal end of cornutal excavatii>n. an elongate-oval ring of thickened tissue; Egg.—Upright, cylindrical, with IX lon- corpus bursae with an elongate, dense, gitudinal ridges evenly dispersed and con- coarse patch of small, irregularly shaped, verging toward either pole; length 0.46 mm, short spicules extending a short distance diameter 0.3 mm (Beuteispacher 1977). PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Figs. 4-9. Genitalia of .4//iy

10

a »# %«

11

12

Figs. 10-12. Larva and larval tubes o{ Airiyilriii iinci'iis. 10. Larva, lateral view; length 21 mm; maximum diameter 2 mm. 1 1. Dorsal view of fig. 10. 12. Larval tubes; longest tube 1.5 cm in length and 5 mm in diameter

Larva (Fig.s. 10-11).—Length of largest A3-6; anal proleg with 17-18 crochets ar- larva 22 mm; maximum diameter 2 mm. ranged in a slightly curved line; all prolegs Head width 1.5 mm; dark reddish brown, with 2-3 scattered rows of spines immedi- with a prominent lateral dark brown to ately anterior to crochets. black streak through stemmatal area; streak Larval case (Figs. 12-13).—An elongate becoming slightly broader toward rear mar- silken tube, up to 15 cm in length. 5 mm gin of head. Six stemmata present; 3-5 in diameter, densely covered with small aligned in a contiguous, vertical, anterior plant fragments. series. Integument cream to buff with dark Pupa (Fig. 14).—Length of largest pupa reddish-brown plates and pinacula. Prespi- 10.2 mm. Head smooth. Abdomen with racular pinaculum of prothorax partially dorsum of A2-6 with an anterior row of fused to pronotum and bearing all three L numerous minute spines and a smooth pos- setae together with spiracle. Thoracic legs terior ridge which continue nearly % around well developed; coxal plates well separated. each segment; A7-8 with anterior row of Prolegs on A3-6 and A 10; crochets 25-28 dorsal spines more reduced and continuing in number, arranged in a uniserial ellipse on around each segment as a ventral ridse; PROCHFDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

i i i

Figs. U^-14. L;ii\.il iiilic ,iikI pupae o\ Aniydria anceps. 13, Dump mound of ,4m( ine.xicana colonized by

Amyclria larva; tubes (tl with active larvae are visible on dump's surface. Erosion has removed some of the substrate that normally completely covers the tubes. White 33 mm Him container included for scale. 14. Five pupal exuviae (arrows) after adult emergence, on dump surface, protruding nearly peipendicular 7-10 mm from substrate. The exuviae remain attached to the buried larval tubes, which open to the surface.

posterior ridge also reduced on 7—8 and inent pair of stout dorsal spines and a much completely encircling each segment. Cre- shorter pair of stout ventral spines. master of A 10 consisting of a large, prom- Material examined.—MEXICO: Chia- 1

VOLUME ins. NUMBER I 193

pas: El ChoiTeadero, Chiapa de Corzo: 1 9 . Two emergence events were observed dur-

1 Aug 1967, O. S. Flint Jr. (USNM). Guer- ing the summer of 2000, within two days rero: Amula. 6.000 ft: 1 6 (holotype). 18 after heavy precipitation.

Sep, H. H. Smith (BMNH). Tonalapa: I 9 Larvae inside cases were collected in the (paratype). Jun. H. H. Smith (USNM). Mo- field and reared to adults. Larvae were in- relos: Cuernavaca: 1 (5, 22 May 1949. J. cubated at room temperature in plastic con-

McKelvey (USNM); 1 9, Nov 14, R. Miill- tainers, using the spent fungal substrate as er (USNM). Nuevo Leon: Anegada Arroyo. food. Adult emerged in these con-

16 mi S. Linares, 1.250 ft: 2 6, 2 9. D. R. tainers. Hymenopteran (Ichneumonoidea Davis & W. D. Duckworth, 9 Jul 1963. and Chalcididae) and dipteran (Tachinidae: slides USNM 32413 (USNM). Monterrey: Pseudochaeta sp.) parasites also emerged 4 3. 14 9,4 larvae, pupal exuviae, S. R. from some of these field-collected larvae Sanchez-Pena, reared from Atta mound, during rearing. In the field, ichneumonid slide USNM 32394 (USNM, UTA); 1 <5 , 3 and chalcid parasitoids have been observed 9, 20 Jun, 2000, S. R. Sanchez-Pena, engaged in host searching behavior over reared from Atta mound, slide USNM Amydria larval cases, on dumps heavily

32340 (USNM, UTA). Puebia: Tehuacan: 1 colonized by Amydria larvae. The chalcids

9, Sep 1937, C. Hoffmann, (USNM); I 9, could be either primary parasitoids or hy- 12 Sep, R. Miiller (USNM). Smaloa: Ven- perparasitoids. The trophic levels of this adio: 3 9, B. Clark (USNM). Tamaulipas: system are thus potentially five: plant ma-

4 mi S. Ciudad Victoria: 19,5 Aug 1963, terial —> symbiotic fungus —> Amydria -^

D. R. Davis & W. D. Duckworth (USNM). ichiifumonids and tachinids —> chalcids. Distribution. —Known only from sub- Amydria larvae are the largest colonizers tropical and semiarid areas of northern of the upper layers of the fungal dumps ex- Mexico, from Nuevo Leon south to Chia- amined. Further research is wananted to de- pas. Beutelspacher (1977) also reported this termine the actual nutritional needs of lar- species from Estacion de Biologia Chame- vae, and their level of dietary specialization ia, Jalisco, Mexico. Atta ine.xicana is known on fungi. No antagonistic interaction was to occur at every locality reported for Ainy- observed between moth larvae and Atta dria anceps. mexicana. The workers do not dig or tunnel Biology.—The larvae were found to bur- into the dump material to any significant row into the fungal substrate heap and to extent. The predaceous ponerine ant, Pa- spin a tough, leathery tube covered with chycondyla villosa (Fabricius), which was substrate particles. They live within these very common at the collection localities, tubes through the larval cycle, probably was observed digging a few millimeters protruding only the head outside the tube to into the Atta dumps in what appeared to be eat while immersed in the substrate. Empty attempts to reach Amydria larvae. tubes (Fig. 13) become very visible after Acknowledgments heavy rains that wash away loose particles. Immediately prior to adult emergence, the We are indebted to Vichai Malikul and moth pupae force their way % their length George Venable. Department of Systematic out of the open upper end of the tubes at Biology. Entomology Section, Smithsonian the dump surface. Pupae are exposed for Institution, and John Chung for the illustra- only a brief period after the rains (perhaps tions, John Steiner of the Smithsonian Pho- one day). Following a mass emergence, pu- tographic Services assisted with the photo- pal exuviae may be observed in large num- graphs. Norman Woodley, Systematic En- bers projecting perpendicularly from the tomology Laboratory, U.S. Department of surface of the dump area (Fig. 14). Adult Agriculture, identified the tachinid para- emergence apparently is triggered by rain. sitoid. Specimens examined are deposited 1

PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

and Gracillarioidea. 91-1 17 //; Kristensen. N. in the following institutions: The Natural pp. P. ed. Lepidoptera, Moths and Butterflies. Hand- History Museum, London, England buch der Zoologie. Vol. IV. Arthropoda: . National of Natural His- (BMNH): Museum Part 35: 91-1 17. Walter de Gniyter & Co.. Berlin, tory. Smithsonian Institution, Washington, New York. DC, USA (USNM); and the University of Fisher. R J.. D. J. Stradling. and D. N. Pegler. 1994. Texas, Austin, TX, USA (UTA). Leucoagaricus basidiomata from a live nest of the leaf-cutting ant Atta cephalotes. Mycological Re- Literature Cited search 98: 884-888. Hart. A. G. ;uid E L. W. Rattiieks. 2001. Task partitioning, Anderson, C. and F L. W. Ratnieks. 2000. Task parti- division of labour and nest compartmentalisation col- tioning in societies: novel situations. Insectes lectively isolate hazardous waste in the leafcutting Sociaux 47; 198-199. ant Atla cephalotes. Behavioral Ecology and Socio- Beutelspacher, C. R. 1977. Una nueva especie de Ac- biology online. http://link.springer-ny.com/liMky roloplnis Poey, 1932. de Chamela, Jalisco. Mexico service/joumals/00265/contents/00/003 21. (Lepidoptera: Acrolophidae). Anales Instituto Mueller. U. G., S. A. Rehner. and T D. Schultz. 1998. Biologi'a. Universidad Nacional Autonoma de The evolution of agriculture in ants. Science 281: Mexico. 48. Serie Zoologi'a (1): 145-150. 2034-2038. Bononi, V.. M. Autori. and M. Rocha. 1981. Leiico- Pagnocca. E. M. Bacci. Jr.. M. H. Fungaro. O. C.

coprinus gongylophonts (MoUer) Heim. o fungo Bueno, M. J. Hebling. A. Sant'anna. and M. Ca- do formigueiro de Atta sexdens rubropilosa Forel. pelari. 2001. RAPD analysis of the sexual state Rickia 9: 93-97. and sterile mycelium of the fungus cultivated by Davis. D. R. 1984. Neopseustidae, Nepticulidae. Opos- the leaf-cutting ant Acromynne.x hispidu.'i falla.x. tegidae. Tischeriidae. Incurvariidae. Cecidosidae, Mycological Research 105: 173-176.

Adelidae. Prodoxidae, Tineidae. Psychidae. Ar- Rogers. J. D.. Y-M. Ju. and F San Martin-Gonzalez. rhenophanidae. pp. 16-25. In Heppner. J. B.. ed. 1995. Disco.xylaria myrmecophila and its Hypo-

Atlas of Neotropical Lepidoptera. 1 (Checklist, pt. creodendron anamorph. Mycologia 87: 41-45.

1). Dr. W. Junk, The Hague. Waller. D. and J. C. Moser. 1990. Invertebrate enemies te.x- . 2000. Tineoidea and Gracillarioidea, pp. 469- and nest associates of the leaf-cutting ant Atta

482, figs 25.1-25.21. In Bousquets, J. L. et al.. ana (Buckley) (Formicidae. Attini). pp. 225-273. eds. Biodiversidad. Taxonomia. y Biogeografi'a de In Vandcr Meer. R. K.. K. Jaffe. and A. Cedeno, Artropodos de Mexico: Hacia una Sintesis de su eds. Applied Myrmecology: A World Perspective. Concocimiento. Vol. 2. Westview Press, Boulder. Colorado. Davis. D. R., D. H. Clayton. D. H. Janzen. and A. R Walsingham. Lord (Thomas De Grey). 1913-14. 42 Brooke. 1986. Neotropical Tineidae. II: biological (Lepidoptera-Heterocera. 4). pp. 225-392. In notes and descriptions of two moths phorectic on Godman. F D. and O. Salvin. Biologia Centrali- spiny pocket mice in Costa Rica (Lepidoptera: Ti- Americana. neoidea). Proceedings of the Entomological So- Walter. C. 1938. The Texas leaf-cutting ant and its con- ciety of Washington 88: 98-109. trol. United States Department of Agriculture Cir- Davis. D. R. and G. S. Robinson. 1998. The Tineoidea cular 494. 18 pp.