Element and Energy Flows Through Colonies of the Leaf-Cutting Ant, Atta colombica, in Panama

The total annual flows of elements and energy in tree leaf litter fall and in leaf materials harvested from trees by the leafcutting ant Atta colombica Guerin are compared in order to estimate the fractions of the flows controlled by the ants. Flows of mineral elements through colonies were estimated by determining mineral element content of organic refuse from the colonies which had accumulated during a five month dry season. Because the ants are less active during the dry season than in the wet season, estimates of annual nutrient flow based on dry season refuse accumulations are probably underestimates. The annual flows of 13 elements in tree leaves and in tree reproductive parts processed by the ant colonies were calculated. Expressed per area of forest, flows ranged between 0.5 and 3.1 percent of the nutrient flows in the annual leaf litter fall. When expressed per m2 of ant refuse dump, flows ranged from 16 to 98 times the flows in annual leaf litter. This amplification of element flow through the refuse dumps resulted in a 4-fold increase in the amount of fine roots ( < 2 mm dia) present in the dump compared to the general forest floor. Amount of fine roots in the top 20 cm of the dump was 10 times greater than the amount at the 50-70 cm depth, suggesting that elements flowing to refuse dumps are recycled to the trees from within the dump rather than leached downward through the soil profile. Annual energy flows were 1.7 percent of energy flow in leaf litter fall when calculated per area of forest. When calculated per area of an ant nest, energy flows in leaf material funneled through nests by the ants were 11 times the energy flows in leaf litter falling on the nests. Ant colonies (ants + fungus) were estimated to assimilate about 22 percent of the energy which flowed through them. PLANT-HARVESTING INSECTS obviously process some fraction of ecosystem energy and nutrient flow, though the magnitude of their effects on these flows is often difficult o assess because of insufficient knowledge of the insects and of their host plants, and from the problems of quantifying insect effects (Franklin 1970). The organic refuse dumping of leaf-cutting ants and the seasonal pattern of tree-root growth into the organic refuse facilitate the estimation of nutrient and energy flow rates through these populations of insects. Leaf-cutting ants harvest leaf, flower, and fruit materials from vascular plants and transport hese materials to underground fungus gardens (Mariconi 1970, Weber 1972). Organic materials which no longer support growth of the fungus, along with dead ants, are removed from the fungus gardens to refuse disposal areas. Among the fourteen presently known species of Atta (Hymenoptera: Formicidae), which range from 32? N latitude to 330 S latitude in the Americas (Borgmeier 1959), A. colombica Guerin is the only species known to dispose of organic refuse above ground. Atta cephalotes, A. sexdens, and A. texana dispose of organic refuse in underground chambers pecially excavated for this purpose (Stahel and Geijskes 1939, Cartwright 1967, Moser 1963). Atta colombica carries organic wastes downhill from the nest site and onto a rock, tree trunk, or vine from which it is dropped either into the ground, where it accumulates in heaps, or into running water. During the wet season, tree roots grow into and consolidate the organic refuse (Haines 1971, 1975) (consolidated refuse is defined as that occupied by roots to the extent that the refuse could not be scraped from the dump with bare hands). Root growth in refuse dumps ceases during the dry season, when water potentials in the refuse dump become more negative than -15 atmospheres (Haines 1971), which is the "wilting point" for many plants. Refuse deposited during the dry season remains unconsolidated and is therefore readily quantifiable. Organic refuse production was measured during the dry season in the Panama Canal Zone as an incidental part of a study of interactions between A. colombica, soil, and tree seedlings (Haines 1971, 1975). The mineral nutrient fluxes through colonies of this ant in conjunction with nutrient and energy flows in leaf litter for the forest on nearby Barro Colorado Island (Haines and Foster 1977a, b) permit the assessment of the magnitudes of energy and nutrient flow through the ant populations in relation to flows in forest leaf litter fall. These preliminary estimates of annual nutrient and energy flows through the ant colonies are probably underestimates, for they are based on estimates of organic refuse production during the dry season when the ant colonies are least active. STUDY AREA AND METHODS Field work was conducted in a semi-evergreen seasonal forest (Beard 1944, 1955) at 790 44' W long., 270 BIOTROPICA 10(4): 270-277 1978 This content downloaded from 131.94.192.65 on Mon, 12 May 2014 17:34:53 PM All use subject to JSTOR Terms and Conditions 9? 9' N lat., elevation 50-70 m, 6 km northwest of Gamboa, in the Panama Canal Zone, Central America. The forest developed from a pasture cleared in 1917 and then abandoned in 1936 (records, Canal Zone Civil Affairs Office, Balboa); thus the forest was 42 years old at the time samples were collected for this study. Within the forest, an 850 m long portion of a ridge about 300 m wide, bounded by streams on two sides, and having a total area of 28 ha was selected for detailed study. The forest can be characterized as having a mean canopy height of 16 m, 22 M2 of basal area, and 290 stems per ha (Haines 1971). Of the 43 leaf-cutting ant nests encountered in the study area, colonies of Atta colombica occupied 21, Atta cephalotes 2, and Acromyrmex species 1. Among the 19 vacant nests, 5 were identified from the remains of organic refuse dumps as abandoned Atta colombica nests. The excavators of the other 14 vacant nests could not be identified. Ten of the A. colombica colonies were designated by use of a random numbers table for detailed study. This study was conceived during the dry season when refuse was accumulating but was not being consolidated by roots. When root growth stopped is uncertain. The beginning of the dry season was chosen as 20 December. During the 10 days previous to this date, a daily average of 0.32 cm of rain had fallen, while no rain fell during the following 20 days. Total rainfall in January was 0.22 cm. When rains began again in May, organic refuse that accumulated uring the dry season (since 20 December) was weighed in the field and sub-sampled to determine dry weight:wet weight ratios. This procedure was performed for nine of the ten nests before root growth resumed and consolidated the unmeasured refuse at the tenth nest. Each of the ten colony sites was further characterized with respect to roots and refuse. Smaller diameter roots are presumably the most active in nutrient uptake. The roots were quantified by diameter classes in order to compare the amounts of roots found in soils in the general forest floor, the ant nest, and in the ant organic refuse dump. Root weights in the soil were determined by removing pairs of 18 cm dia x 20 cm deep cores of soil from the undisturbed forest floor near each nest, from the nest proper, and from the consolidated portion of the refuse dump. Cores were taken at the surface and at 50 cm at the same locations. Roots were washed from cores, sorted into diameter classes, dried to constant weight at 100?C, and the weights ubjected to analysis of variance. Least significant differences (LSD) values were also calculated (Service 1972). Approximate area covered by the refuse dump was determined with a meter stick at nine of the colony sites. Refuse samples were dried to a constant weight at 100?C and dassified into those with and those without observable soil contamination. Among those without contamination, ten were randomly designated for chemical analysis. Samples were sent to the Soil Testing and Plant Analysis Laboratory of the Cooperative Extension Service, Athens, Georgia, where 1 g samples were combusted for four hours at 5000C in porcelain crucibles. Ash was taken up in 5 ml of buffer consisting of 0.676 M Li2CO3 + 3.2 M HNO3 and sparked in a direct reading emission spectrograph (Jones 1976). Nitrogen was determined by Kjehldahl digestion where nitrogen in the digest was determined colorimetrically with a Technicon autoanalyzer. Sulfur was determined with a Leco sulfur analyzer (Jones and Isaac 1972). For each colony sampled, the amount of accumulated refuse was divided by the number of weeks (20 or 21) during which accumulation had occurred. The 12 colonies for which refuse was not sampled varied in nest diameter from 1.8 to 6.7 (X_ 5.0, S.D. 1.31) m while those nine sampled ranged from 3.0 to 6.9 (X=4.9, S.D. 1.10)m in diameter, thus an effort was made to use regression to estimate size specific refuse production rates for the nests not sampled. Because the coefficient of determination (r2) of refuse production versus nest diameter was only 0.07 this approach was abandoned. Instead, the weekly mean accumulation rate for the nine randomly designated colonies was simply multiplied by the total population of 21 colonies to estimate total flow through all colonies of A. colombica. Element flows through A. colombica colonies were compared to available data on element flows in leaf litter in a forest 10 km to the west on Barro Colorado Island. This forest may also be classified as a secondary semi-evergreen seasonal forest (Beard 1944, 1955), perhaps 100 to 200 years old (Knight 1975), and having an average canopy height of between 30 and 40 m. Litter was collected weekly on Barro Colorado Island, from August 1969 to August 1970, using a network of 312 plastic litter traps (Haines and Foster 1977a). Element contents of leaf litter and of ant organic refuse were determined simultaneously in the same laboratory. Estimates of annual element flow in leaf, in twig and bark, and in nondescript, small litter fractions are based on element content of 14 sets of samples evenly distributed through the year and are reported elsewhere (Haines and Foster 1977b). Estimates of annual element flow used in Element and Energy Flows through Atta 271 This content downloaded from 131.94.192.65 on Mon, 12 May 2014 17:34:53 PM All use subject to JSTOR Terms and Conditions this paper are based on values from the same data set corresponding to the same five months of the dry season in which the ant refuse analyzed in this study accumulated. Element content data from ant organic refuse and from leaf litter were subjected to analysis of variance. Energy flow through A. colombica colonies was estimated using element content data from this study in conjunction with element and energy content data for freshly fallen leaf litter from Barro Colorado Island. Ratios for energy to nutrient content were calculated. The Barro Colorado Island leaf litter had an energy content of 4772 (SD= 180.0, n -42) cal/g (Haines and Foster 1977a) and 55.133 mg of the elements/g (Haines and Foster 1977b and this study, table 1). Ant organic refuse had 67.110 mg of element/g (table 1). If tree leaves at the study site had the same ash content as did tree leaves on nearby Barro Colorado Island, then, by proportion, each gram of organic refuse represents the remains TABLE 1. Element content and flux in refuse of the leaf-cutting ant, Atta colombica, and in forest leaf litter. Element content Annual element fluxes Mg/Kg dry weight (S.D.) Forest, Kg/Ha Dump, g/m2 refuse leaves refuse refusea leavesb refused refuse leaves refuse Element n= 10 n= 10 leaves leaves leaves S 3143 2212 1.42 0.25 12.88 1.96 80.24 1.28 62.68 (469) (320) P<.0019C N 30600 17,800 1.72 2.46 103.7 2.37 781.18 10.37 75.33 (4427.1) (836) P<.0001 P 259