The Impact of the Leaf Cutter Colombica on the Energy Flow of a Tropical West Forest Author(s): Ariel E. Lugo, Edward G. Farnworth, Douglas Pool, Patricio Jerez and Glen Kaufman Source: Ecology, Vol. 54, No. 6 (Nov., 1973), pp. 1292-1301 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1934191 Accessed: 02-09-2015 18:53 UTC

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This content downloaded from 134.173.140.65 on Wed, 02 Sep 2015 18:53:39 UTC All use subject to JSTOR Terms and Conditions THE IMPACT OF THE LEAF CUTTER ANT A TTA COLOMBICA ON THE ENERGY FLOW OF A TROPICAL WET FOREST' ARIEL E. LUGO Department of Botany, Universityof Florida, Gainesville, FL 32601 EDWARD G. FARNWORTH Department of Entomology and Nematology, Universityof Florida DOUGLAS POOL Department of Agronomy, Universityof Florida PATRICIO JEREZ Department of Botany, Universityof Florida and GLEN KAUFMAN Universal Plant Breeding Services, Ltd., Box 50, Caistor, London, England

Abstract. The patterns,quantity, and activities associated with the leaf-cuttingof Atta colombica were studiedAugust 20-27, 1971, in a lowland tropicalwet forestat Osa Peninsula, Costa Rica (Lat. 08'42'N Long. 83029'W). The study nest had an area of 44.8 m2 and covered1.4 ha of forestfloor. Daily, on a m2of forestfloor, the studynest had inputs of 10.17 leaf fragmentswith an area of 0.0108 M2, a weightof 0.0813 g, an ash content of 0.0039 g, and a potentialenergy of 0.3455 Kcalories. The returnto the forestfloor 0.0525 g of refusewith a potentialenergy of 0.0764 Kcalories and an ash contentof 0.0212 g/m2 day. It was calculatedthat the leaf-cuttingactivity of ants reducedthe grossproduction of the forestby 1.76 Kcal/m2*day but acceleratednet productionby at least 1.80 Kcal/m2. day throughthe returnof ash rich in phosphorusto the forestfloor. The size of the Atta nest may be determinedby the balance of the energyinput to the nest and the cost of ob- taining,carrying (concentrating), and distributingthe potentialenergy into the nest. Of a workforce of 12,000 ants/M2of trail,75% were not carryingleaves and were assumedto be doingtrail maintenancework. Rainfalland litterfall were the main obstaclesof leaf trans- port,which was about70% efficient. The ant's energyallocation for maintenance,which limitsgrowth, and the establishment of reward feedbacksto theirenergy producers have implicationsfor man's urban system development.

INTRODUCTION (Weber 1966) and the foraging activities of ants Scatteredon the floor of many tropical forestsone (Cherrett 1968a, Harris 1969, Rockwood 1971). E. 0. frequentlyfinds trails teeming with traffic,reminis- Wilson (1971) has reviewed the literature on social . cent of the freewaysof our major cities. The traffic This study that one observes, however, is not of cars but of a involves the quantificationof the im- pact of leaf multitude of ant and termite species, working and cuttingon the energy flow of the sur- rounding survivingin the forest. One of these species is the forest,and observationsrelated to activities associated leaf cutterant Atta colombica, which belongs to the withleaf cuttingand transport.An energy flow tribe Attini,a group of fungus-growingants of the diagram is presentedin the discussion, showing the major new world (Weber 1966, 1969). Because of their energy relations of an Atta nest. It is hoped that this conspicuous trails covered with ants carryinggreen study will encourage investigatorsin leaf fragments,these ants have attracted the atten- this field to perfectand quantifythe energydiagram tion of many biologists. Studies have been oriented for this important component of the forest com- towardbehavior and plant-animalinteractions (Mark- munity. ham 1966, Hodgson 1955, Parsons 1968, Martin METHODS 1970, Martin and associates 1969a-b, Martin and Martin 1970), the natural history of leaf cutters Study area '-ReceivedFebruary 10, 1972; acceptedFebruary 14, The study took place on the Osa Peninsula, 1973. Puntarenas Province, in southwestCosta Rica, C.A.

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we collected 200 leaf fragmentsfrom ants on the trails and made the following determinations: leaf area, wet and dry weight, ash content, and caloric value. The caloric values were determined with a Parr Bomb CalorimeterModel 1241. We obtained the total nest input by plottingthe VR-f rate of leaf-fragmentflow over the study period,

2 determiningthe area under that curve, and multi- plying the total number of fragmentsentering the nest by their mean weight, ash weight, and caloric value. Results were expressed on an area basis (Fig. 1).

Efficiencyof transportand program of leaf cutting An estimate of the efficiencyof leaf transporton the lengthytrails leading to the nest was made on the morningof 25 August. Counts were made of frag- ment-carryingants leaving the treesand those arriving FIG. 1. Scale drawingof the studynest and other at the nest. All trees along a discretetrail were moni- ant activitiesin the vicinity.Trail areas in m2: Trail tored, so that all the trafficof ants could be ac- I-130.9, Trail II-244.0, Trail III-307.3, Trail IV- counted for. The ratio of ants arrivingat the nest 179.8, Trail V-72.3. These values include the canopy area of treesbeing cut; the total area of trailswithout to ants leaving the tree was considered a measure the canopies was 32.3 m2. The centralnest areas was of leaf transportsuccess. 10.0 m2and the total refusepile 2.5 M2. The total area We investigated the cycles of leaf cutting by whereants were active was 946.8 m2and the surrounding examiningtrees periodically during the day for cutting area of forestconsidered as the ant's immediatehabitat activity. In addition, the morningwave of workers (enclosedby the solid line) was 14,025M2. Solid dots = abandonedant nest; the X = an activenest. Tree identifi- leaving the nest and moving into trees was followed cations: 1 = Trema micrantha (capulin blanco); 2 = Inga and timed for rate of movementand commencement sp. (guavo); 3 = Brosimum tiles (baco); 4 = Brosium of leaf cutting. sapiifolium (morillo); 5 = Goethalsia meiantha (guacimo blanco); 6 = Sapium jamaicenses (olive); 7 = Virola sp. Ratio of non-carryingto leaf-carryingants and (frutadorada); questionmarks = two treesof the same speciesthat could not be identifiedand one treeon Trail ant biomass IV that was overlooked. The tree at the nest was A 5 X 10 cm framewas used for countingthe ants Terminalia lucida (guayabon). All trees, except the with and without leaves traveling along Trail 2 on nest tree,were softwoods. 26 August. We conducted the inventoryby placing the frame over 10 spots along a transectevery hour (lat. 08'42'N long. 83029'W). This area is a tropical between 0730 and 1600. At the end of the experi- wet forest characterized by an annual rainfall of ment 400 ants were collected for biomass deter- minations. 4200 mm, an annual mean temperatureof 26.30 C, and a brief dry season from January to March Rate of refuse deposition (Holdridge et al. 1971). A large Atta nest (Fig. 1) was observed for 7 days (20-27 Aug. 1971) while Refuse from the nest's internalprocesses was de- the ants on the to side the authors participated in the summer tropical posited by forestfloor one of the nest (Fig. 1). We measured the rate of deposi- biology course (No. 71-6) sponsored by the Or- tion by placing a plastic sheet under this area, and ganization of Tropical Studies, Inc. collecting and weighing the refuse accumulation at various time intervals. Leaf imports into the nest To estimate the amount of leaf fragmentsenter- Other observations ing the nest,we monitoredthe five trailscoming into Throughoutthe studyall authorsspent many hours the nest for a 50-hour period for 1/2-hintervals dur- observing and measuring the behavior and ac- ing the day and at hourly intervals at night, since tivitiesof ants on the trails,nest, and trees. In addi- leaf cutting was essentiallyzero at night. All leaf tion, the observationsand experiences of other OTS fragmentscarried during a 5-minute interval were studentsaided us in clarifyingsome of the mecha- counted. Every 3 hours duringperiods of leaf cutting, nisms operatingin this nest.

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Trail. Aug.2123,1971 600 57 6 600As 516 Trail2 Aug21 23.1911 480 410 400 38X 84 g/hr 288 28.8g/hr. 200 19.2 EL 19?2 E. 20

96 9.6

12 6 12 6 12 6 12 6 12 12 6 12 6 12 6 1? 6 12 PM AM PM AM PM AM PM AM Timeof Day Timeof Day

the TraiI3.AUg.2123,12 AUT.2Ti23219T1Trail4.

Trail 56 Tcnrte dttgm 5hmtlecb009gel480 fa e;toa

4050 ,384mliy 384 288 g/hr.288V r Eg/r 280 1 200 21 200 1 1-r 128 600~~~~~~~~~~1 626 ~~~~57~~~~~19 60 127C ~~96 .1999 ______~~~~ ~ ~~~ ~~~~ 12 6 12 6 12 6 12 6 12 12 6 12 6 12 6 6 12 PM AM PM AM PM AM PM AM limeof Day TimeofDay 5 000 TraH5. AUg. 21.24,oi

12 6 12 6 12 6 12 6 12 PM AM PM AM limooi Day

FIG. 2. Diurnal ratesof leaf-fragmentflows into the studynest throughindividual trails. Data expressed as numbersof leaf fragmentsimported during a 5-mmnperiod and in g/h. Total flowof leaf fragmentsinto the nest/in2 of trailduring the 50 h of observation:Trail 1-883, Trail 2-273, Trail 3-160, Trail 4-391, Trail 5-65. To convertthese data to g/m250 h, multiplyeach by 0.00079 g/leaffragment; to obtainKcal/ m2 50 h, multiplythe above figuresby 4.25 Kcal/g.

Miscellaneous measurementsincluded air tempera- season. As the shower frequency and intensityin- ture, meteorological observations, counts of ants creases it is expected that the leaf input rates are carryingobjects other than leaves, and identification reduced, even approachingzero at times,as observed of the trees fromwhich the ants were cutting. for various hours on subsequent days. Table 1 contains data from the literatureon leaf RESULTS AND DISCUSSION inputs into nests of differentA tta species, at various Leaf imports into nest locations and times of year. Comparisons are diffi- cult because of the variabilityin the samplingperiods The diurnal variation of leaf fragmentflow into and the lack of informationabout the size of the the nest is shown in Fig. 2 and 3. Dramatic changes nest. However, most values are similar (x~= 62g/h). in activityoccurred early in the morning,when the Measurements made only during the peak of the firstwave of leaf-carryingants arrived at the nest, leaf cutting activityor in agricultural areas (Gara and in the late afternoon,when significantinputs 1970) showed high input values. On the other into the nest stopped. Throughout the day a high extreme,low values may be due to the size of the level of cutting was maintained as long as heavy nest (Lutz 1929) or the time of year (Cherrett rainfallor other disturbancessuch as trail blockages 1968a). Our study nest had inputs comparable to by litter fall did not occur. For example, on 25 many of those reported in Table 1 (Harris 1969, Markham 1966, Emmel 1967, Hodgson 1955). Aug. at 1300 h a heavy shower caused all activityto Leaf input into the nest pulses around midnight cease on all trails. On 21 Aug. Trail 3 was blocked on most trails. Since no significantleaf cuttingwas by leaf fall, causing a considerable reduction in leaf observed at this time, these surges may represent fragmentflow along that trail. Observationsof trail the returnof leaves that were dropped on the trails interruptionwere verified many times during the during the day. Many times during the study ants period of study. Because the study period was rela- were observed picking up dropped leaves and carry- tively rain-free,these results must approximate the ing them into the nest, as also reported by Emmel upper limitsof leaf input into the nest for the rainy (1967).

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16 00- 153.6 TABLE Alltrails 2. Standingcrop of recentlycut leaves dropped AUg.21-23,1971 .134.4 along Trails 1 and 4 1200 .115.2 Biomassof "leafdrops" ZE ~~~~~~~~~~~~~~~~~~~~~~~~~~~96.0 g/m2of Kcal/m2 800 71 g/hr. Trail Time trail? SD of nest E 51.6 1 0700 1.499 ? 1.696 0.0004 400 38.4 1 1900 1.473 + 1.329 0.0004 4 0700 1.743 ? 2.006 0.0005 112 4 1900 2.660 ? 1.539 0.0008

12 6 12 6 12 6 12 6 12 MEAN 1.843 + 0.5575 0.0005 PM AM PM AM Timeof Day TABLE 3. Leaf fragmenttransport efficiency along Trails 1 and 2 duringactive cutting

80ArTmeaieAUg.21-23,19ul 126.1 Leaf fragments Inputof F | >/ t 13 cutfrom fragments Efficiency 75 ~~~~~~~~~~~~~~~~~~~~~~~~~~23.9Time treesa intonesta (%) 12 6 12 6 12 6 12 6 12 0930 1,181 770 65.19 PM AM PM AM 1000 1,309 820 62.64 Timeof Day 1100 1,054 810 76.85 FIG. 3. Diurnal ratesof totalleaf fragmentflow into x 68.23 the studynest. Data expressedas numberof leaf frag- mentsimported during 5 min and as g/h. Also shown a 5 min intervals. b Assume is the ambienttemperature at 1.0 m above the ground 70% efficiency. duringthe studyperiod.

the trails. Many more leaf drops were observed at Leaf transport the base of the trees from which ants were cutting. The many interruptionsto leaf transportthat occur These data were verified by purposely blocking a along trails are counteractedby changes in the ant's trail and observing the ensuing events. First there leaf-carryingbehavior. For example, Table 2 con- was a massive confusion of ants carryingleaves and tains data on the standingcrop of leaf droppings in a convergence of unladen ants arriving from the

TABLE 1. Rates of leaf fragmentinput into various leaf-cutterant nests as reported in the literature

Leaf input Time Species Location Date Nest size g/hra period Author

Atta sp. Costa Rica Jul-Aug Med.-large 80.0 0700-2200 h Harris 1969 1969 Atta sexdens Brazil Feb-Mar - 47.7 77 months Autuori 1940b 1966 Atta ceplialotes Costa Rica Feb-Nov 37.8m2 64.0 24 h Markham 1966 1966 Atta cephlalotes Costa Rica Dec 1969 4 trails 290.0 Gara 1970 Mar 1970 Atta cephlalotes Guyana 10 weeks 56 m2 13.1 24 h Cherrett pers. comm. 1963 Atta colombica Costa Rica Feb-Mar 3 trails 41.8 0830-1230 h Emmel 1967 1967 A tta cephalotes Panama Jul-Aug 2 trails 85.2 0700-1800 h Hodgson 1955 1955 Atta sp. Costa Rica Jun-Jul - 118.0 0700-1500 h Lloyd 1967C 1967 Atta sp. Costa Rica - 42.0 0230-2400 h Ferrand 1966C Atta sp. Costa Rica - - 16.5 0730-2230 h Wood 1966C Costa Rica Jul-Aug Various nests 17.2 0530-1300 h Parsons 1968 Atta cephalotes Guyana 10 weeks 56 m2 10.9 0100-2400 h Cherrett 1968 1963 Atta colombica Costa Rica Aug 1971 44.8m2 47.5 50 h This study Assumed 45% dry weight and/or 8.0 mg dry weight per leaf fragmentof 1 cm2 As cited by Weber 1966. As cited by Harris 1969.

This content downloaded from 134.173.140.65 on Wed, 02 Sep 2015 18:53:39 UTC All use subject to JSTOR Terms and Conditions 1296 ARIEL E. LUGO ET AL. Ecology,Vol. 54, No. 6 nest. Second, leaves were dropped while the trail 1200Miscellaneous inputall trails. Aug.2123,1971 was being cleared of debris. Finally, as trafficre- sumed, ants picked up dropped leaves and carried 900 them to the nest. Leaf drops were more frequent as the distance from the nest increased and were -~600 particularly numerous during rain. Laden ants finishedtheir journey when they were close to the 300 nest, but they dropped theirleaves and sought cover in holes and crevices when furtheraway from the 12 6 12 6 12 6 12 6 12 AM nest. Increases in the ants' speed of travel along PM AM PM TimeofDay trails due to rainfall stimuli support these observa- tions and have been reported by Hodgson (1955). FIG. 4. Numberof miscellaneousitems carriedinto The efficiencyof leaf transport,i.e., the percentage the nest. These are minimalestimates since no special made to countall miscellaneousimports into of laden ants arrivingat the nest of those laden ants effortwas the nest. coming down the tree, is approximately 70% (Table 3). The length of the trails and the frequency of moving along trails carryingmiscellaneous items and obstructionsalong them suggestthat a large amount picking up leaves (Fig. 4). Figure 5 also shows of labor must be divertedto trail maintenance (Wil- reported ratios of empty ants to leaf-carryingants. son 1971). Table 4 shows ratios of ants without Notice that except for those hours of intense leaf- leaves to ants with leaves along Trail 2. If one cuttingthis ratio is always greaterthan one. Ratios assumes that ants without leaves are available to of 100:1 have been observed (Parsons 1968). With cope with trail maintenance requirements,the data regard to the ant force in the trails, Table 4 shows on Table 3 would support the contentionof a large a surprisinglyuniform number of ants on the trails diversionof energyto maintenance (75% of ants on (12,000 ants/M2? 2,600) if there is no rain. Rain- the trail). Observations of ant movement towards fall, however,can lower this figureby 50%. various trees early in the morningbefore the cutting It is possible that the size of the maintenanceforce activitystarts showed that a large proportionof the in a given nest becomes one of the determinantsof ants that go up a tree return within 10 minutes nest size and lengthof trails and a measure of access without any leaves. Cherrett (personal communica- to leaves. We know from observations with cities tion) reportsthat over 50% of the workersreturn to and ecosystems, that as structureis created large the nest without leaves. We believe these ants to amounts of energy are required for maintenance. representthe fractionof ants reponsible for daytime In a steady state forest,for example, 100% of the maintenance of trails. At night, when leaf cutting gross production is respired (Odum 1970). Failure is negligible, we counted large numbers of ants to divert an adequate portion of the energy budget

TABLE 4. Ratios of non-carryingto leaf-carryingants and totalnumber of antsin Trail 2 at differentdistances from the nestand/or different times of day

Time of day Distance fromnest 0730 0830 0930 103Oa 1130a 1400 1500 1600 Meand

1.5 m b 3.6 4.5 6.0 11.0 1.4 5.15 7.5 m 9.0 2.0 4.0 4.0 1.6 10.0 4.84 8.5 m 3.0 0.5 1.5 2.0 2.0 2.5 2.40 18.0 m 0.6 4.0 0.2 1.3 1.2 0.7 1.45 27.0 m 1.4 1.2 2.0 3.0 1.2 1.99 38.0 me 2.0 2.0 4.0 1.2 3.50 44.0 m 3.5 0.3 2.0 4.0 3.56 46.0 m 2.0 1.0 5.0 2.5 4.15 61.5 m 0.6 1.0 1.0 2.0 1.0 2.0 7.0 1.64 78.0 m 1.5 1.3 0.5 1.28 mean 10.04 4.07 1.30 3.28 3.87 2.18 2.84 2.17 2.81 Numberof ants on thetrail/m2 of trail 11,400 14,200 12,000 6,000 7,800 14,000 13,800 14,600 11,950 a Hard rainfall. b One of the two measurementswas zero. e South branch of trail. d Means calculated fromthe sum of all counts of leaf carryingand non-carryingants.

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soL

0 Parsons,1968 200, 0 Cherret,1968 a Hodgson,1955(west trail, 15 July) 100, A (westtrail, 19 July) V (northtrail, 15 July) 50. v (northtrail, 19 July)

.,20-

10-

02201- _of

0200 0400 0600 0800 1000 1200 1400 1600 1800 2000 2200 2400 Timeof Day FIG. 5. Summaryof reporteddata on the diurnalpattern of emptyants/ants carry- ing leaves. into maintenance results in operative inefficiency (3) the role of ant refuse piles as energy sources and a decrease in overall power output and competi- and habitat for symbionts. tive survivalof the system. The lack of maintenance, (4) the acceleration of energy as a result of the for example, is one of the reasons for breakdown in ants' role as a grazer and "mineral cycling machines and buildings, and is analogous to no pump."~ respirationin organisms. Using these ant nests as Fig. 6 summarizes the energy flows associated with analogues of heterotrophicsystems, one could calcu- late the energeticcost of maintenance as related to the study nest and Tables 5, 6, and 7 contain esti- nest size and imports. These calculations may have mates of some of the energyflows and storages. importantimplications for other heterotrophicsys- Fig. 6 is an energy flow diagram showing the tems, such as cities. relationshipbetween the Atta nest and the rest of the forest ecosystem. The model shows input of young Energetic considerations leaves and miscellaneous plant parts into the nest Intrinsicto ecological studies of individual species where they are decomposed by the fungus,which is is the assessmentof the species impact in its system. cultured by the fungus attendants. The fungus is Structurally,plant ecologists use the importance value as a measure of a species impact on its eco- TABLE 5. Rate of refuse deposition during the study systems. Energetically,the importance value of a period species is its impact on the overall energyflow of the Time be- Rate of system. With literature values, assumptions, and tween Wet Dry deposi- our data we can make some estimatesof the energetic collec- weight weight' tion tions h Date g g g/hr importancevalue of the Atta nest in terms of four roles: 7.75 21 August 1971 1,354 406 52.4 15.41 21 August 1971 1,336 400 25.9 (1) the total standingcrop of leaves ants remove 15.82 22 August 1971 1,590 477 30.5 29.33 23 August 1971 1,354 406 13.9 fromthe forest. x =30.7= (2) the reduction in potential production of the 0.0525 g/m2*day forestas a result of ant foragingactivity. a Using 30% wet to dry weight conversion.

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Grazingeffects -Fastmineralization //~~~ , ~Environmentalclues

Sun~~~~~~~

te~~~~~~~~~~~~~~~~~~~~s

Totalnest R FIG. 6. Energy diagram showing some of the interactions of the study nest and the surrounding forest. Some details of the nest function are taken from Martin (1970). The work of fungus attendants include 1- cleaning and scraping of fragments,2 cutting of fragmentsinto very small pieces, 3-application of saliva, 4-deposition of liquid fecal droplet rich in proteolytic enzymes, 5-transport of fragmentsto the matrix of the fungus gardens, 6-planting of mycelium on the fragment,7-further application of fecal material. Sym- bols follow the energy language of Odum (1967, 197(0). eaten by all ants. The refuse,composed of old fungus nest, the ants respired a minimum of 0.0012 parts,dead ants, soil particles,and debris is deposited Kcal/m2*day or 0.33% of the input. The rest is outside of the nestby maintenanceants as refusestor- accounted for by ant turnover and growth,fungus age. This refuse is shown to have three roles: (1) respiration,and refuse output. The latter accounted food source, (2) habitatfor associated fauna, some of for 21% of the potential energy input to the nest. which eat ants, and (3) a mechanism for fast min- The ratio of ant respirationto nest input is a measure eralization of the forest. Carrying leaves from the of the amplifyingvalue of the ants' work, which in tree to the decomposer by-passes the normal cycling this study was very high. For example, assuming of the forest. The normal mineralization,shown in ant respirationof 0.0012 Kcal/m2-day of work, ants the lower left corner of the diagram, involves old bringinto the nest 0.3655 Kcal/m2, or an amplifica- leaves fallinginto the litter,decomposition, and re-use tion of 304. It is proposed that when the potential of mineralsby plants. The excavation of the nest by energy is diluted, e.g., young leaves scattered in the maintenance ants yields minerals which accumulate forest,the amplificationof the ants' work is limited in the refuse storage. by the cost of concentratingthe diluted energy into Also shown in Fig. 6 are the cutter ants which the nest. However, when the potential energy is respond to environmentalclues for the initiationof already concentrated (as with agriculturalmonocul- leaf cutting. Such clues are now shown for mainte- tures) the magnificationof the ants' work probably nance ants, since the work of maintenance is con- increases because concentrationis no longer a major tinuous. Cuttingand carryingleaves into the nest is work allocation, maintenancedecreases, and a larger facilitated by trail maintenance, but is interrupted surplus of energy is possible. For example, to cite by rain and by trail obstructions. Trail obstructions an extreme,if maintenance was reduced by 50%o in increase maintenance work, which in turn aids in our study nest, the amplificationof the ants' work the restorationof leaf transportinto the nest. We would be 487, an increase of 183 (60%) in potential have evaluated some of the energyflows, utilizing the input for a decrease of 50%oin cost. literature,reports, our data, and several assumptions. It is significantfor a single species such as Atta Tables 6, and 7 summarizethe calculations,which colombica to control so much energy in a system must be consideredpreliminary estimates. Of the ob- as diverse as this tropical wet forest (Table 7). If served net input of 0.3655 Kcal/m2* day into the one assumes that 10%o of the primary productivity

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TABLE 6. Some estimatesof the energeticsof the study TABLE 7. The impactof Atta colombica on the tropical nest wet forest

Category Kcal/m2 Kcal/m2day Impactper m' of forestbased Total leaf cuta 0.4935 Category on 1 nest/1.4haa Actual inputinto nest as leaves 0.3455 Input as miscellaneous 0.0200 Number of leaf fragmentscarried 10.17/day Total input into nest - 0.3655 into the nest Exportas refuses 0.0764 Area of leaves carriedinto the nest 0.0108 m2/day Nest'snet daily gain of potentialenergy 0.2891 Weight of leaves carried into the 0.0813 g/day Ants in trailand their nest respiration' 0.0045 0.00012 Potential energy carried into the 0.3455 Kcal/day Ants carryingleaves and their nest respiration 0.0011 0.00003 Ash carriedinto the nest in the form 0.0039 g/day Ants withoutleaves and their of leaves. (4.87% ash) respiration' 0.0034 0.00009 Weight of refuse deposition 0.0525 g/day Total ant respiration 0.0012 (Table 5) Assumed 70% efficiencyof transport(Table 6). Ash returnedto the forest floor 0.0212 g/day b A low estimate; assumed 10 mg/piece and 4.25 Kcal/g. Input by the refuse. (40.39%o ash) from Fig. 4 was 0.459 pieces/m2of forest day. c The caloric value of the refuse was 2.5 Kcal/g. Potential decrease of gross photo- 1.4158 Kcal/day d The respirationof ants estimated with the following equation syntheticrate based on a metabolism derived for tropical termites(Weigert 1970): for the forestof 131 Kcal/m2*day Y = 1.3X(.84 y = respiration in microliters02/min and X = the dry weightper individual in mg. A value of 1 mg/ant Potentialacceleration of metabolism 1.80 Kcal/day was used. Actually, our measurementshowed average weights of by the ash returnedto the forest 1.28 and 0.58 mg/ant for two 200-ant samples. One liter of 0, = assumingthat 1 g of ash equals 85 4.8 Kcal (Golley and Gentry 1964). The above equation reflects Kcal of net photosynthesis low respirationin comparison to other reported values for insects (Weigert 1970). Thus, our respiration estimates may be low. Potentialacceleration of metabolism ? e Used the mean ratio of non-carrying/leaf-carryingants = 2.81 and otherroles (Table 4). throughgrazing f Assumed an ant population in the nest 10 times the number a Amounts arrivingat the nest. At 70% efficiencyof transport, in the trails (Golley and Gentry 1964). the actual figures are higher.

as leaves. The input of ash as miscellaneous plant is grazed by all species, and thatthis amounts to 13.1 parts was not measured but an estimateof its weight Kcal/m2 -day (Odum and Ruiz 1970), one then finds input (Fig. 4, Table 6) suggests that it does not that our study nest consumed 2.6%o of the total account for the increase in ash contentof the refuse grazingor 0.2%'oof the total gross productivityof the pile. This "extra" ash mightoriginate from soil over- forest (Table 7). More surprising,however, is the turned by the ants during nest construction. There- impact of the ants on the photosyntheticpotential fore,if one assumes that 1 g of ash is equal to 85 Kcal of the forest. With a forestgross productivityof 131 of net photosynthesis(1 g of leaf tissue is 5% ash Kcal/m2-day (Odum 1970) and the observed grazing and contains 4.25 Kcal), then, by multiplication, by the ants of 0.0108 m2 of leaf tissue/m2day, the the 0.0212 g of ash/m2-day returnedto the forest ant's removal of leaf area reduces the potentialpro- floor by the ants has a potential value of 1.80 Kcal ductivityof the forestby 1.415 Kcal/m2-day. This to the forest. This balances the two "negative" im- is a larger value than the stored potential energy in pacts of the leaf cutters on the forest which were the leaves grazed by the ants. However, one might estimatedas 1.76 (Table 7). This value, however,is argue that grazinghas a positive effectand increases an underestimateof the positive work of the leaf primary production. The energetic impact of the cutters because the quality of the ash is the key positive effectsof grazingand the effectsof the ants' determinantof its energeticrole in the forest. Harris selectivegrazing need evaluation. (1969), for example, analyzed the refuse pile and The ants accelerate the metabolism of the forest found 200 ppm of available phosphorus,whereas he by means of several mechanisms. Grazing is one, detected less than 0.05 ppm of available phosphorus the ant's influence in soil structureand aeration is in the forestfloor away from the nest. This means another (Harris 1969). Ant refuse piles serve as that the actual energeticvalue of the refuse to the habitat and food source for many species of insects forest is the increased forest productivityresulting in theirearly stages of and are development(Fig. 6) from the concentratedavailability of phosphorus in visitedby many birds and mammals (Weber 1966). the vicinity of the refuse pile. Harris failed to These positive benefits need study and quantifica- recognize this importantfeedback role and suggested tion. One of the most importantimpacts of ants is that ants caused an annual loss of 7% of the forest's their mineral cycling work, which also influences total ash budget. Such loss, however, would be energyflow in the forest. Table 7 shows that more intolerablefor any length of time in a tropical wet ash is returnedto the forestfloor than is carried in forest. His proposed negative role of ants is not

This content downloaded from 134.173.140.65 on Wed, 02 Sep 2015 18:53:39 UTC All use subject to JSTOR Terms and Conditions 1300 ARIEL E. LUGO ET AL. Ecology,Vol. 54, No. 6 competitiveor conducive for long-termsurvival of Veno aided in laboratorydeterminations in Gainesville. eitherforest or ants. S. C. Snedakerand W. Smithcritized the manuscriptand Alma Lugo did the art work. To all we are grateful. Implications LITERATURE CITED As discussed earlier, data from leaf-cutter ant Cherrett,J. M. 1968a. The foragingbehavior of Atta nests may be extrapolatedto other heterotrophicsys- ceplhalotesL. (,Formicidae) 1. Foraging tems, such as urban systems. Atta nests resemble patternand plant species attacked in tropical rain cities in their dependence on external sources for forest.J. Anim. Ecol. 37: 387-403. aspects of the distributionof theirfuel supplies. It is importantto both to keep a 1968b. Some pest speciesof leaf-cuttingants in the Caribbean. Am. proper balance between availability of energy Soc. Hort. Sci., Trop. Reg. 12: 295-310. sources, energyuse, and the size of the heterotrophic Emmel,T. C. 1967. Ecologyand activityof leaf-cutting system. ants (Atta sp.), p. 125-131. In Advanced zoology: The leaf-cutters,although limited by their selec- ecology in the tropics,winter 1967. Organi- zation for Tropical Studies,San Jose, Costa Rica. tive grazing (Cherrett, personal communication), Gara, R. I. 1970. Report of forestentomology con- have large amounts of fresh leaves available but sultant (UNDP project 80) IICA, Turrialba,Costa do not overgraze. When the food is concentrated,as Rica. Mimeo. with agriculture,the ants proliferate and become Golley,F. B., and J. B. Gentry. 1964. Bioenergeticsof pests to man (Cherrett1968b). Is the ants' prolifera- the southern harvester ant, Pogonomyremex badius. Ecology 45: 217-225. tion limitedby the amount of food or by the energetic Harris, L. D. 1969. A considerationof the nutrient cost of obtainingfood? Man, like the Atta, prolifer- "sumping"activities of leaf-cutterants (Atta sp.) in ates in proportion to cheap concentrated energy the new worldtropics. Research report. In Advanced sources (Odum 1971), but like the Atta in the nat- population biology, July-August.Organization for Rica. ural forest, the size of the urban system should Tropical Studies,San Jose,Costa Hodgson, E. S. 1955. An ecological studyof the be- eventuallybe limited by the cost of obtaining and haviorof the leaf-cuttingant A tta cephalotes.Ecology distributingfuels, and of maintainingthe complexity 36: 293-304. created. When the energy cost of maintenance Holdridge,L. R., W. C. Grenke,W. H. Hatheway,T. exceeds the energyavailability in fuels,growth should Liant, and J. A. Tosi, Jr. 1971. Forest environments in Tropical Life Zones: A pilot study. Pergamon be limited. Press. 'vYVeber(1966), has suggested that the size of an Lutz, F. E. 1929. Observationson leaf-cuttingants. ant colony is controlled by the size of the fungus Am. Mus. Novit. 388: 1-21. gardens. However, the data presented (Tables 1, 4, Markham,C. P. 1966. The surfaceactivity, behavior and 6) suggest that in order to maintain the flow and energyinflux rhythms of leaf-cuttingants, Acro- sp. and Atta cephalotes. Research Report of energy into the nest and the gardens, 75% or myrinex Summaryin Tropicalbiology: An ecologicalapproach, more of the ant work force must be allocated to Feb.-March, 1966. Organizationfor Tropical Studies. maintenance. As with modern agriculture,fungus San Jose,Costa Rica. monoculture is energeticallyexpensive. Leaf-cutter Martin,J. S., and M. M. Martin. 1970. The presence ants have evolved a stable system of survival by of proteaseactivity in the rectal fluid of attineants. 16: 227-232. growing in concentric rings in proportion to their J. InsectPhysiol. Martin, M. M. 1970. The biochemicalbasis of the capability to obtain leaves (Cherrett personal com- fungus-attineant symbiosis. Science 169: 16-20. munication) and by establishinga net positive feed- Martin,M. M., R. M. Carman,and J. G. MacConnell. back with the primaryproducers. This positive work 1969a. Nutrientsderived from the funguscultured by acceleratesprimary production and thus the potential the fungus-growingant Atta colombica tonsipes. Ann. food for the ants. In thisstrategy growth is secondary Entomol. Soc. Am. 62: 11-13. Martin,M. M., J. G. MacConnell, and G. R. Gale. to maintenance and in proportionto surplus energy 1969b. The chemicalbasis for the attineant-fungus supplies when available on a continuingbasis. We symbiosis.Absence of antibiotics.Ann. Entomol.Soc. believe that the developmentof urban systemsstands Am. 62: 386-388. to gain new strategiesas the energeticsof Atta nests Odum, H. T. 1967. Work circuitsand systemsstress, on and other social insects become known. p. 81-138. In H. E. Young [ed.] Symposium primaryproductivity and mineralcycling in natural ecosystems.Univ. Maine Press, Orono. ACKNOWLEDGMENTS 1970. Summary,an emergingview of the We thank L. Perez and E. Murillo for their help ecologicalsystems at El Verde. Chap. 1-10. In H. T. duringthe courseof our work. The studentparticipants Odum and R. F. Pigeon [ed.] A tropicalrain forest. in the OTS summer Tropical Biology course 71-6 A study of irradiationand ecology at El Verde, offeredmany ideas and intellectualstimuli. J. Down- Puerto Rico. Div. Tech. Inf., U.S. A. E. C. howerprovided many insightsinto the ecology of Atta 1971. Environment,power, and society. John in otherregions of the tropics.Trees were identifiedby Wiley & Sons, N.Y. 331 p. G. B. Picado and the ants by I. Lieberburg. Patricia Odum,H. T., and J. Ruiz. 1970. Holes in leaves and the

This content downloaded from 134.173.140.65 on Wed, 02 Sep 2015 18:53:39 UTC All use subject to JSTOR Terms and Conditions Autumn 1973 LEAF CUTTER ANTS AFFECT ENERGY FLOW 1301

grazing control mechanisms,Chap. 1-6. In H. T. Weber,N. A. 1966. Fungus-growingants. Science 153: Odum and R. F. Pigeon [ed.] A tropicalrain forest. 587-604. A study of irradiationand ecology at El Verde, 1969. Ecological relationsof the Atta species PuertoRico. Div. Tech. Inf.,U.S. A. E. C. in Panama. Ecology 50: 141-147. Parsons,L. R. 1968. Aspectsof leaf cutterant behavior: Weigert,R. G. 1970. Energeticsof the nest-building Acromyrmex octospinosa and Atta cephalotes. Re- termite,Nasutitermes costalis (Holmgren), in a Puerto searchReport In Tropical biology: An ecologicalap- Rican forest,Chap. 1-4 In H. T. Odum and R. F. proach. July-Aug.Organization for Tropical Studies, Pigeon [ed.] A tropicalrain forest. A studyof ir- San Jose,Costa Rica. radiationand ecologyof El Verde,Puerto Rico. Div. Rockwood, L. L. 1971. Population ecology of leaf- Tech. Inf. U.S. A.E.C. cutterants in Guanacaste. Organizationfor Tropical Wilson,E. 0. 1971. The insectsocieties. BelknapPress StudiesNews 71-5: 4-5. of Harvard Univ. Press, Cambridge,Mass.

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