lnsecles Sociaux, Paris. 1976, T o m e 23, n ~ 2, pp . 99-108.

BEHAVIORAL OBSERVATIONS ON AETHALION RETICULATUM

(HEM., AETHALIONIDAE) AND ASSOCIATED ANTS

By RICHARD L. B R O W N

Department of Entomology, Cornell University, Ithaca, New York, U.S.A.

Requ lc 28 novembre 1975. Accept6 ie 22 d6cembre 1975.

SUMMAR Y

Aethalion reticulatum n y m p h s and adul t s were found feeding on Piper umbellatum in Costa Riea. Adult females protected the i r egg m a s s e s by s i t t ing atop the ma sse s and scraping the i r h ind legs along the sides. Two paras i to ids , Gonatocerus sp. and Pterygo- gramma sp. were reared f rom egg masses . N y m p h s and adul t s were regula r ly tended by Camponotus sericeiventris and Camponotus (Tanaemyrmex) sp. Camponotas sericei- ventris tended only dur ing the day l igh t hour s and aggress ively protected the hemip te rans . Camponolus (Tanaemyrmex) sp. was compet i t ive ly displaced by the fo rme r species.

RESUMEN

Observaciones de conducta de Aethalion reti~ulatum (L.) (Hem., Aethalionidae) y hormigas asociados.

Las n in f a s y adu l tos de Aethalion reticulatum fue ron encont rados a l imen tandose de Piper umbellatam en Costa Rica. Las h e m b r a s p ro teg ian sus huevos scn tados encima de ellos y f ro tundo los m iembros pos ter iores con los lados de las m a s a s de huevos. Dos paras i tos fue ron criados en los huevos , Gonatocerus sp. y Pterygogramma sp. Ninfas y adul tos eran protegidos r egu la rmen te por los Camponotas sericeiventris y Camponotus (l'anaemyrmex) sp. Los C. sericeiventris cu idahan a l a s he mip t c r a s du ra n t e las ho ras del dia so lamen te y las protegian agres ivamente . Los Camponotlts (Tanaemyrmex) sp. fue ron desa lo jados en competencia por las especies p r imar i a s .

100 RICHARD L. BROWN

RESUME

Observations sur le comportement de Aethalion reticulatum (Hemiptera, Aethalionidae)

et les Fourmis vivont en association avec lui.

Nous avons trouv4 des nymphes et des imagos de Aethalion reticulatum qui se nourrissaient sur Piper umbellatum ~ Costa Rica. Les femelles prot6geaient leur amas d'ceufs en se tenant h leur sommet et en frottant leurs pattes arri6res sur les e6t~s de l'amas. Deux parasitoides, Gonatocerus sp. et Pterygogramma sp., furent 61ev6s au sein des amas d'ceufs. Camponotus sericeioentris et Camponotus (Tanaemyrmex) sp. prenaient r~guli6rement soin des nymphes et des imagos. C'est seulement le jour que Camponotus sericeiuentris s'occupait des H4mipt6res et les prot~geait de fa~on agressive. Camponotus (Tanaemyrmex) sp. 6talt supplant6e par l'esp6ce pr4c6dente, plus comp6titive.

I N T R O D U C T I O N

Aethalion reticulatum (L.) is d is t r ibuted from Costa Rica to Brazil at alti- tudes ranging from 10 to 900 meters. The species is polyphagous, the recorded hosts inc lud ing Cajanus cajun (L.) Hutch (pigeon pea), Mangi[era indica L. (mango), Eriobotrya japonica (Thunberg) Lindley (Japanese plum), Morus alba L. (nmlberry) , Hibiscus tiliaceus L. (Linden hibiscus) , and various species of Citrus L. The species, at times, has been an agr icul tural pest wi th host plants dying unde r

�9 heavy infestat ions (AzEvEDO MAROUES, 1928). The biology of this hemip te ran has been described by AZEVEDO MARQUES

(1925, 1928). Approximate ly 100 eggs are deposited in 3 to 4 rows in a ver t ical to inc l ined posi t ion 15 to 30 days after mating. A viscous material is secreted over the eggs resul t ing in a mass 3 to 5 mm high, 6 to 10 mm long, and 6 to 8 mm wide. The eggs hatch 25 to 30 days after deposi t ion and the nympha l stage extends up to 75 days. The female general ly does not abandon the eggs nor the offspring. Two generat ions or more may feed upon the same plant.

Several insect species have been observed in t rophic associations wi th Aethalion. Aethalion reticalatum is tended by tile ant Ctrmponotas crassus Mayer in Brazil. In addi t ion to obta in ing honeydew, the stingless bee, Melipona ru[icras Latreille, has been observed us ing its mandib les to cut off port ions of the egg mass covering wi thout apparent harm to the eggs themselves (Az~vEr~o MAn0.UES, 1928).

Recorded natura l enemies of A. reticulatum are egg par,~sites. The eggs are parasit ized bv Abbelloides marqae.,'i Brethes (Tr ichogrammatidae) in Brazil (AzE- rEDO MARQUES, 1928). Lathromerella sp. (Tr ichogralnmat idae) has been found parasi t iz ing eggs in Guyana (MEvEns, 1931).

Aethalion reticulatum and its associates were studied from Feb rua ry 28 to March 10, 1972, at the Tropical Science Center near Rinc6n, Osa Peninsu la .

AETHALION RETICULATUM 101

Costa Rica. Observations were l imi ted to indiv iduals found on Piper umbella- tam L. (Piperaceae) along the Aguabuerta ravine. At the beg inn ing of the s tudy 28 egg masses, each wi th an adult female, and two nympha l broods were found on plants ranging from two to five meters in height. The Aethalion n y m p h s were counted daily and numbers of associated ant a t tendants were recorded perio- dically throughout each day. Nine females guarding egg masses were removed and the masses were moni tored for predat ion. Several egg masses from the study area, as well as from Piper in other areas near Rinc6n, were collected and

re ta ined for evidence of parasi t ism.

RESULTS

Although A. reticulatum is cons idered polyphagous, P. umbellatum was the only plant found in the study area wh ich hosted Aethalion. In addi t ion to Aethalion, 24 other species of Auchenor rhyncha (Homoptera) were collected from this plant. A second species of Piper was present along the s t ream but was not host to Aethalion nor a wide range of other hemipterans .

The number of eggs per egg mass ranged from 17 to 140, averaging 76 for 10 masses. The egg masses were s imilar to those described from Brazil by Az~.vEoo MARQtrES (1925, 1928). The hardened mater ial covering the eggs was thicker laterallv, than dorsally. All e~,~,-- masses were guarded by adult females, as descr ibed below. As indicated in fig. 2 and 3, two or more egg masses were often situated together. In most cases, however, egg masses were single.

The first ins tar nymphs fed wi th the female on the stem near the egg mass (fig. 1). Later ins tar nymphs did not remain wi th the female, but moved to various branches of the host p lant dur ing day and night, always congregat ing to feed.

Dur ing daytime, the nymphs ' h i n d legs were generally held close to the body; however, at dusk the legs were raised and held vert ical ly over the body. Two observat ions were made at dusk in which flies approaching an un tended brood evoked a sudden response of leg waving. Artificial d is turbances in the form of movement or loud sound resulted s imilary in this leg wav ing response. The nymphs ' legs were lowered when ants were tending at night.

Adult females were relatively non-mobi le and hesi tant to leave either a feeding site or an egg mass, even when disturbed. Four of five females, t rans- p lanted from egg masses on one tree to another tree host ing a brood of nymphs, remained and fed for at least six days, after which observat ions were terminated. Most females were found s t raddl ing egg masses, cover ing the tops, but occasional ly leaving the h ind port ions exposed. Females fed whi le guarding the egg masses and sporadical ly scraped the sides of the masses wi th quick lateral and downward spurr ings of the h ind legs. Durin~ a 10 minute period, one adult scraped the sides of the egg mass 36 times, whi le another female on a nearby mass remained motionless for the same period. Most egg masses were guarded by females which

1 0 2 R I C H A R D L. B R O W N

Fio. 1. - - Camponotus sericeiventr is t e n d i n g an a d u l t f e m a l e and n e w l y h a t c h e d Aetha- lion re t icula lum.

Fro. 1. - - Camponotus sericeioentris p r e n a n t so in d ' u n e f e m e l l e a d u l t e e t d ' u n i n d i v l d u v e n a n t d 'dc lore de l ' esp~ce Aethal ion re t icu la tum.

Fro. 1. - - Camponotus sericeioentris a t e n d i e n d o u n a h e m b r a a d u l t a y su n u e v a c r i a de Aethal ion re t icu la lum.

AETHALION RETICULATUM 103

showed active leg spurr ing causing the lateral marg ins of the masses to become

dark b rown and glazed. The lack of spur r ing by females left the masses pale

and rough sided, as they were when first deposi ted (fig. 2). The paras i to ids Pterygogramma sp. and Gonatocerus sp. were observed several t imes being

knocked off the egg mass by the female 's spurr ing.

Six of the nine unguarded egg masses were p reyed upon w i t h i n 48 hours

after the females were removed. In all six, the p reda to r ate th rough the dorsal,

th innest por t ion of the mass to get to the eggs. All eggs were eaten, leaving only

the outer cover ing of the masses. In two of the masses the ants, Solenopsis geminata (Fabricius) , were seen w i th in the mass eating eggs. None of the female-

guarded egg masses showed ev idence of p reda t ion dur ing the s tudy per iod.

The two paras i to id species men t ioned above emerged f rom egg masses brought to the laboratory . F rom six egg masses 119 Gonatocerns sp. (Myrmaridae) and

23 Pter~tgogramma sp. (Tr ichogrammat idae) emerged. Dissect ion of the egg

masses revea led two and three mymar id s but no more than one t r i chog rammat id

per egg. Paras i t i sm appeared to be heavies t in the pos ter ior mid -por t ion of the

e--~ mass. This area was often left exposed as the female moved sl ightly fo rward

to feed. Paras i te emergence left cha rac te r i s t i c round holes in the top of the mass (fig. 3).

Three ant species and one vespid wasp were observed obta in ing h o n e y d e w from Aethalion nymphs and adults. Tile ant Monacis bispinosus (Olivier) and the polybi ine wasp Pseudopoiybia compressa Saussure w e r e in te rmi t t en t visi tors

to one small group of Aethal ion nymphs . This group decreased f rom 56 to 10 nymphs after 10 days.

Camponolus sericeivenlris (Guerin) was present on five of 10 Piper plants host ing Aethalion. This ant t ended only dur ing the dayl ich t hours (fig. 1 and 2),

and was never present before 5.30 am nor after 6.00 pm. Throughou t the study

per iod, three to 15 indiv iduals of C. sericeiventris w e r e present dur ing the day-

light hours at the largest brood of nymphs . This brood numbered 116 at the

beginn~.ng of the study per iod and decreased to 113 after 12 days. At no t ime

dur ing the daylight hours was this pa r t i cu la r brood found wi thou t attendants.

Fro. 2. - - Contrasting egg masses of Aethalion reticulatum. Female Aethalion sitting on mass has active leg spurring. Female (removed) on second mass did not exhibit leg spurring, evidence by pale and rough margins of egg mass. Attendant ant is Camponotus sericeiventris.

Fro. 2. - - Masses d'ceufs de Aethalion reticulatum. La femelle d'AethaIion assise sur son amas d'~ufs frotte activement sos pattes le long de l'amas. La femelle qui se tenait sur l 'autre amas d'~3eufs ue pr6sentait pas ce comportement, comme le montre l'aspect grossier et peu color6 des bords de l'amas. La Fourmi soigneuse appartient h l'esp~ce Camponotus sericeiventris.

FI6. 2, - - Contraste de las masas de huevos de Aethalion reticulatum en la cual la hcmbra Aethalion esta sentada sobre los huevos aguijoneando la pata. La hembra (no aparace en la figura) en la segunda masa no mostro senales de aguijonear los huevos con la patas como se observa por el color palido y aspero de las orillas la masa. La hormiga es Camponotus sericeiventris.

104 R I C H A R D L . B R O W N

FIG. 3. - - A e t h a l i o n r e t i c u l a t u m tended by me l ipon ine bees in Brazil . P a r a s i t e emer - gence ho les indica ted hy a r row .

Fro. 3. - - A e t h a l i o n r e t i c u l a t u m soign6s p a r des M61ipones au Br6sil. La fl6che ind ique les orifices de sor t ie de paras i t es .

Fro. 3. - - A e t h a l i o n r e t i c u l a t u m a tendidos p o r abe ja s en Brasi l , Los p a r a s i t o s que emergen de los agu j e ro s es tan sena lados p o r n n a flecha.

AETHALION RETICULATUM 105

Camponotus ser ice iventr i s was very aggressive when t e nd i ng the nymphs , rush ing to confront any object b rough t close to the brood. The defensive posture of si t t ing up wi th the tip of the gaster directed forward was always assumed. This behavior was also exhibi ted when other insects approached the brood. Ind iv idua l s of C. ser iceioentr is found vis i t ing extrafloral nectar ies of Pithecolo- bium sp. (Leguminosea) were only mi ld ly aggressive on this food source, fre- quently d ropp ing from the leaves if confronted wi th a hand-he ld stick. Indi- viduals foraging on the ground were not aggressive when thus confronted.

A second species of Camponotus, in the T a n a e m y r m e x group, t ended Aethal ion on eight of the 10 trees in the study area (fig. 4). This species vis i ted A. reti- culatum dur ing the day and night, in equal numbers , but never in the presence of C. ser iceiventr is . Broods tended by the d iurnal C. ser ice iven tr i s were tended only at night by the second species. At the above-ment ioned brood of 115 nymphs, ind iv idua ls of this species were never present before 5.55 pm and after 5.15 am.

Camponolus ( 'Tanaemyrmex) sp. was non-agressive at all t imes. If confron- ted wi th a hand-beld object, the ant would try to escape, often d ropp ing from the leaves. This species of Camponotus was not found at any other food source.

DISCUSSION

The known na tura l enemies of A. ret iculatum attack the egg stage. A high degree of paras i t i sm is evident in spite of the behavior of the female Aethal ion and associated a t tendant species. Solenopsis may be cons idered a potent ia l egg predator in the absence of guarding females. The one brood of nymphs un tended by aggressive ants was reduced considerably in numbers , suggesting that predators might be involved.

Although the female remains wi th both eggs and nymphs , protec t ion appears to be chiefly for the eggs. The females are probably a greater deterrent to pre- dation than paras i t i sm when covering the dorsal th innes t por t ion of the egg mass. The study showed parasi t ism in the female-guarded masses, but "predation only in those unguarded . The leg spur r ing is no doubt a deter rent to parasi tes as well as predators. This spur r ing is apparent ly not a localized behaviora l trait, as the margins of e,,~,,,~ masses in Brazil also show dark marg ins wh ich are a resu!t of the spur r ing (fig. 3).

Fie,. 4. - - Camponotus (Tanaem.tlrmex) sp. tending brood of last instar and recently metamorphosed adult Aelhalion reticulalum.

Fro. 4 . - Camponotus (Tanaemyrmex) sp. s'oeeupant de rtymphes du dernier stade de Aethalion reliculalum ainsi que d'adultes venant de se m6tamorphoser.

Fn;, 4. - - Camponotus (Tanaemyrmex) sp. atendiendo la eria en el ultimo estado y la del nuevo adulto.

Ir~SECTES SOCIAUX, 1976, T. 93, N ~ 2. 8

106 RICHARD L. BROWN

The curious leg waving by nymphs at night deserved addi t ional at tent ion. The st imuli for in i t i a t ing such behavior are unclear . The combined effect of a large group of n y m p h s waving legs may serve as a deter rent to cer ta in paras i tes

or predators. WHEELE~ (1910) listed modificat ions in s t ructure and behavior of aphids

wh ich showed adaptat ions to associations with ants. One such modif icat ions was the group of setae su r round ing the anal opening, which funct ioned in ho ld ing the honeydew droplet whi le the ant imbibed it. Aethalion nymphs have a s imilar group of setae s u r r o u n d i n g the dorsally directed anal opening.

Publ ished observat ions differ over the ants ' recogni t ion and host i l i ty toward na tura l enemies of homopterans and consequent ly over the value of such protec- t ion to homopterans (HERzm, 1937; EL-ZIADY and KENNEDY, 1956; WAY, 1963). HE,ZIG (1937) concluded that three species of LaMas reacted to swif t -moving bodies and behaved as though the attack were being directed against themelves, inc identa l ly p ro tec t ing aphids coining wi th in the orbit of their defensive acti- vities. He found that these ants seldom interfered wi th the s low-moving larvae and adults of coccinel l id beetles whi le they were feeding on aphids. Obser- vations on I r idomyrmex humilis Mayr (SMITH and AR~XTAGE, 1931) and Oeco- phgIla longinoda (Latreille) (WAY, 1954) showed that the ants ' a lertness and host i l i ty decreased wi th distance from the nest as well as wi th greater numbers of homopterans . The observat ions of several workers, summarized by BnIA.~ (1955), confirm that ants monopol iz ing a food resource, such as honeydew-produ- cing Homoptera, definitely show ownersh ip behavior and are usual ly aggressive towards in t ruders tolerated away from~the food source. Such defensive owner- ship appears to be character is t ic of C. sericeit, entri~ in the presence of Aethalion.

The resource pa r t i t ion ing between the two species of Camponotas in this s tudy has been accomplished bv var ious means by other ants. In West Africa, crematogastr ine ants compete with OecophyIla longinoda for s imi lar te r r i tor ia l requirements , but avoid competi t ion for food by tending different species of scale (STRICKLAND, 1951). Such resource par t i t ion ing of honcvdew by other ants has also been recorded by WAY (1953, 1954). A common food resource may also be par t i t ioned temporal ly , as wi th cases of changeover of ant species at dusk in Australia (WILSON, 1971). The Aethalion honeydew resource appears to be part i- t ioned in a different m a n n e r from the above examples. Time of day does not appear to be a factor in the activities of the oppor tunis t ic Camponotus (Tonae- myrmex) sp. Although the Tanaemyrmex group is considered to be p r inc ipa l ly noc turna l (BnowN, pers. com.), this species is behavioral ly adapted to feed day or night. It is res t r ic ted by the presence of C. sericeiventris, whose activities are regulated temporal ly . Where both species utiIize the same resource, a very precise changeover of species occurs at dusk and dawn. s imilar to the cases in Australia.

ACKNOWLEDGMENTS. - - Thanks are due to the Organization for Tropical Studies which sponsored the Tropical Biology Course during which this study was made; Orley << Chip >> Taylor, course coordinator, for his advice and assistance: the Griswold Committee of

A E T H A L I O N R E T I C U L A T U M 107

Cornell Unive r s i ty for covering the cost of p la t e s ; W. L. BROWN, George EICKWORT, J. G. FRA.~CLE.~IONT and E. Richard HOEBm;E for the i r c r i t ic ism and ass i s t ance in pape r p r e p a r a t i o n ; Lucy Mona de Bricefio fo r the Span i sh t r ans l a t ion . F o r the p h o t o g r a p h s 1 am especial ly gra te fu l to Rudo l f JaNDEn (figs. 1, 2 and 4) and E d w a r d S. R o s s (fig. 3). Species d e t e r m i n a t i o n s made by R. C. FROESCn,~ER, B. D. BunKS, A. S. MENKE, and D. R. SMITH.

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Az~vzoo Man~uEs (L. A. D~), 1928. - - C iga r r inha nociva a va r ias cspecies de vegetaes. Bolm. I n s t . biol. Def. agric., Rio de J., 6, 1-27.

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