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Influence of Azteca Alfari Ants on the Exploitation of Cecropia Trees by a Leaf-Cutting Ant’

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Influence of Azteca Alfari Ants on the Exploitation of Cecropia Trees by a Leaf-Cutting Ant’ BlOTROPlCA 29(1): 84-92 1997 Influence of Azteca alfari Ants on the Exploitation of Cecropia Trees by a Leaf-Cutting Ant’ Heraldo L. Vasconcelos and Antonio B. Casimiro Coordenadoria de Pesquisas em Ecologia, lnstituto Nacional de Pesquisas da AmazBnia (INPA), Cx. Postal 478, 6901 1-970 Manaus, AM, Brazil ABSTRACT The foraging activity of the leaf-cutting ant Ana laevigata in an early successional area near Manaus, Brazil, was monitored over a period of 18 mo. Four Cecropia species were growing in that area and all were associated with the ant Azteca alfari. Unoccupied trees (those in which there was no ant response to mechanical disturbance of the stem) were attacked by leaf-cutting ants more often than were trees occupied by A. alfari colonies. Cecropia ulei was the most frequently attacked species. However, leaves of C. ulei were the least preferred ones during assays in which detached leaves of the four Cecropia species were placed alongside the foraging trails of leaf- cutting ant colonies. C. ulei had the largest number of unoccupied trees compared to the other species. In addition, A. arfari colonies associated with C. ulei were smaller than those associated with C. distacbyu. These data suggest that A. alfari was influencing the selection of Cecropia species by A. laevigata, which harvested more from species that were less defended by the ants (with a higher proportion of unoccupied trees or trees hosting smaller ant colonies), although these were less preferred. RESUMO A atividade forrageira da saliva Ana laevigata foi rnonitorada por 18 rneses em uma Area pr6xima a Manaus. Quatro esptcies de embaliba (Cecropia), associadas a formiga Aztecu ulfari, ocorriam nesta Area. Embalibas n5o ocupadas por A. alfari (aquelas em que nenhuma formiga emergiu do tronco da planta quando este foi sacudido) foram mais atacadas pelas salivas do que as embalibas ocupadas. Cecropia uki foi a esptcie mais atacada pelas salivas. Entretanto as folhas de C. uki foram menos preferidas pelas salivas em ensaios de campo nos quais folhas das quatro espkcies foram simultaneamente colocadas ao longo das trilhas das salivas. Urn nhmero maior de C. ulei nlo tinha colbnias de A. ufuri, comparativamente is outras espkcies. AItm disto, as colbnias de A. alfari em C. uki eram menores que aquelas de ao menos uma outra espkcie, C. distuchya. Estes dados sugerem que A. afuri afetou a escolha das espkcies de Cecropia por A. laevigatu, a qua1 atacou mais a esptcie que era menos defendida por A. uyuri (que tinha menos plantas colonizadas e que abrigava colBnias menores) memo que esta tinha folhas pouco palativeis. Kty word: Amazonia; ant-plant interactions; Atta laevigata; Azteca alfari; Cecropia; herbivory. TREESOF THE GENUS Cecropia (Cecropiaceae) are It has been suggested that Azteca also protect characteristic and important elements of many for- Cecropia against herbivory by leaf-cutting ants of est successional sites in the Neotropics. Most Cec- the genus Atta (Jolivet 1987, 1990), based on ob- ropia species are associated with ants, which live in servations that leaf-cutting ants rarely attack Cec- their hollow stems and feed on glycogen-rich, food ropia, in contrast to their attacks on surrounding bodies provided by the plant on a special organ at tree species, which are not associated with ants (Jo- the base of the petiole (Rickson 1971). Azteca spp. livet 1990). Several ant species are known, or are are the most common ant associates of Cecropia strongly suspected of protecting plants against leaf- (Wheeler 1942, Harada & Benson 1988, Longino cutting ants (Janzen 1967; Eberhard & ffiry 1991), particularly in more open habitats. In return 1974; Leston 1978; Jutsum et al. 1981; Cherrett for food and nesting space, some species of Azteca & Jutsum 1983; Dejean et al. 1992, 1995; Farji are known to protect their host-plants against en- Brener et al. 1992; Morawetz et al. 1992; Wetterer croaching vines (Janzen 1969, Schupp 1986, Da- 1994), and most of these species are similar to Rz- vidson et al. 1988) and Coleopteran herbivores teca of Cecropia in being arboreal and having ter- (Schupp 1986, Rocha & Bergallo 1992). ritorial habits. However, it is possible that the lower rate of leaf-cutting ant attack on Cecropia, as noted I Received 6 February 1995; revision accepted 11 Octo- by Jolivet (1990), is not associated with the pres- ber 1995. ence of defensive Azteca ants, but simply with the 84 Influence of Azteca on Leaf-cutting Ant Herbivory 85 lower palatability of Cecropia leaves compared to (height of the apical leaf attachment site) and re- other plants. This paper analyzes the effects Azteca ceived an uniquely numbered tag. Additional mea- have on herbivory by leaf-cutting ants on Cecropia. surements of height were conducted 8 and 16 mo later. Plant growth rates were calculated as: lnHl STUDY SITE AND SPECIES - InHO, where HO is tree height (m) at the begin- ning of the study and H1 is tree height 16 mo The study was conducted in a small (ca. 2 ha), later. abandoned farm, 7 km north of Manaus, Amazo- At intervals of approximately 14 days, over a to- ns, Brazil (3”05’S,60°00’W), where four species tal period of 18 mo, all trees were examined for of Cecropia were found growing sympatrically. The attack by leaf-cutting ants. At least three A. kzeui- site, on flat terrain at an elevation of 50 m, receives gata colonies were foraging in the study area, but an average of 2105 mm of rain annually (mean for we did not attempt to determine which trees were 1910 to 1979; Ribeiro & Adis 1984), which is attacked by which colony. A. kzeuigata builds un- seasonally distributed, with a distinct drier season derground foraging galleries radiating out from the between June and October. nest, and from the entrance to these, superficial This farm was used for several years to grow foraging trails extend to the plants being cut. This cassava and later as a plantation of Brazil nut trees. greatly increases the difficulty of determining the It was bulldozed in 1990, and has been abandoned foraging range and territories of individual colo- since then. In 1992, when this study was initiated, nies, as it is not always clear which entrance be- grasses and forbs had invaded and were dominating longs to which nest. the abandoned area. Trees, mostly Cecropia, oc- Trees attacked by A. kzeuigata were easy to rec- curred at relatively low densities. ognize as this species causes characteristic damage All four Cecropia species, Cecropia concolor Wild, by cutting through the petiole and removing whole Cecropia distachya Huber, Cecropia pulpurascens C. leaves, so that trees look as they have been pruned. C. Berg and Cecropia ulei Snethlage, were associ- In addition, scars are generally left on the basal part ated with a single ant species, Azteca alfari Emery of petioles, where the ants have attempted to cut (sensu stricto; Longino 1989). Previous studies in but have failed. A tree was recorded as being re-at- Manaus (Harada & Benson 1988) have also found tacked only after it had produced new leaves. A. alfari to be the most common associate of these four species, with only two of 61 plants being as- ASSAYS OF LEAF PREFERENCE.-kld assays were de- sociated with Azteca schimperi. The latter is easily signed to assess possible differences in preference to distinguished from A. a@i, both morphologically leaf-cutting ants among the leaves of the four Cec- (Longino 1991) and behaviourally (Benson 1988; ropia species. During the assays detached leaves A. Y. Harada, pers. comm.), as it builds external were placed alongside an active leaf-cutting ant for- carton nests. These were never found on plants of aging trail. Leaves of the four species (one per spe- our study site. Two leaf-cutting ant species, Atta cies) were presented simultaneously. The position higata Fr. Smith and Acromyrmex latireps nigro- of leaves from different species beside the trail was setosus Forel, were found in the study area, but A. chosen at random. Tracings were made of each leaf laticeps was never observed cutting Cecropia. before and 30 min after presentation. The total leaf area removed (cm2) was determined using a leaf METHODS area meter (Delta-T Devices, Burwell, Cambridge). Assays were performed with three A. kzeuigata col- LMF-CUTTINGANT FORAGING PATTEFWS.-AIIarea of onies and leaves from different trees were used for 0.39 ha, where evidence of leaf-cutting ant activity each assay. The leaves from the different species existed (as judged by the presence of damaged were collected from nearby plants of similar size. plants and foraging trails) was delimited. The area In an attempt to control for differences in leafage was divided in 10 x 10 m quadrats and all Cec- among leaves to be used in the assays, we always ropia growing within these quadrats were located collected the second or third leaf below the ter- and mapped. Only five new Cecropia emerged after minal meristem. This method of selection, how- this survey and these were not included in the anal- ever, presupposes that leaves from different Cecro- yses performed for this study. Each tree (including pia species develop at a similar rate, and this may 18 individuals that were protected from leaf-cut- not be the case. Nevertheless, all leaves collected ting ants within exclosure plots as part of another presented the coloration and the size of a fully ex- study; Vasconcelos 1994) was measured for height panded, mature leaf of its respective species. Data 86 Vasconcelos and Casimiro (cm2 removed from each tree species) were trans- TABLE 1. Number of kaf-cutting ant attacks per indi- formed to In (x + 1) and were analyzed using a vidual tree, over a period of 18 mo, in jur randomized block analysis of variance, which con- Cecropia Ipecies and tbc percentage of tbc total sidered each replicated assay as a block.
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