and ¸osa, MG ¸osa, MG ¸osa, Vic ¸osa, Vic Polymorphism, 4,5 b The leaf-cutting 1 ¸osa, MG 36570-000, Brazil. 2013 Society of Chemical Industry ¸osa, Vic c This structure allows efficient division of labor 6 2,3 . and Raul NC Guedes b Departamento de Entomologia, Universidade36570-000, Federal Brazil de Vic 36570-000, Brazil Correspondence to: Terezinha Maria C DellaAnimal, Lucia, Departamento de Universidade Biologia FederalE-mail: [email protected] de Vic Departamento de Biologia , Universidade Federal de Vic Leaf-cutting ants are eusocial or ‘truly’ social , and are ∗ a b certification requirements, andtechniques to a keep lack thesethese pests issues of motivated below this review. economic control thresholds. agents All and 1.1 andThe defining traits membersFormicidae) of exhibit a unique the trait among the antsof Myrmicine, fungi – as the a cultivation food tribe source. Whereas the lowervaried Attini genera substrates of the for tribe (: use this cultivation,fungi on the freshly cut higher vegetation, which genera explains why cultivate theyreferred are widely to as leaf-cutting antsthe and apogee of are instinct thought through to agriculture. have reached Acromyrmex characterized by threereproductive division traits: of (1) labor,of cooperative and stages (3) brood overlapping that care, generations contribute (2) to colony labor. within the colony,in thereby addition including to brood fungus-cultivation, care among and other hygiene behaviors, and are native to the Neotropics and belong to two genera: polyphenism andillustrating polyethism the complexity exist ofA within their colony colony’s is leaf-cutting socialmales formed organization. and ants, by females the (occurringand queen at workers. (which discreet is reproductive wingless), periods) winged ; 1928), who Lailla C Gandra ıma ´ ∗ a ˜ ao Paulo (Brazil) in the Macuna ; control; control shortcomings; management problems ) where leaf-cutting ants are Atta ; Fable II, Book I) illustrates one little health, lots of leaf-cutting ants, ’. In fact, public health in Brazil has Eucalyptus ...... ; baits; ´ ario de Andrade ( : 14–23 www.soci.org 70 explores a different aspect, which emphasizes their 2014; Acromyrmex La Cigale et la Fourmi

ıma, the Brazilian (anti-)hero deprived of any character ´

2013 Society of Chemical Industry The problems with leaf-cutting ants have been aggravated The abundance and economic importance of leaf-cutting ants c key pests. Forestry companies face problems such as restrictive the banes of Brazil are in planted forestof ecosystems. monocultures These (mainly sites are huge extensions mockingly stated that ‘ experienced much improvement since thecutting 1920s; ants however, are leaf- still aentire concern, Neotropical not region. only Their inmuch management Brazil, and has but currently not also faces advanced in tryingin the scenarios all not only other inColombia, countries Peru Brazil, and but Venezuela. where they occur, including, Argentina, Pest Manag Sci 1 LEAF-CUTTINGTO ANTS: SAINT-HILAIRE FROM AND LA BEYOND FONTAINE Ants aredevelopments widely that are knownfables, frequently for aphorisms portrayedFontaine in and their ( popular films. remarkable tales, The evolutionary frugal ant of Jean de la 19th century, during which he stated thatthe ‘either leaf-cutting Brazil ants, annihilates or the leaf-cuttingThis ants will statement annihilate became Brazil’. athe benchmark leaf-cutting for ants Brazilians and toenemies allowed metaphorically of embody other thepoliticians. eventual This country perception and andleaf-cutting the ants its unsavory in Brazil reputation people,Macuna (and of elsewhere) including the are domestic alsocreated illustrated by the by writer M Abstract Leaf-cutting ants are generallyexhibit social recognized organization, foraging, as fungus-cultivation, hygiene important and a pestnotoriously complex nest species structure, difficult. which render in their A management Neotropicalmanagement America. lack of They leaf-cutting of ants; are such economic eusocialthe management insects would thresholds use facilitate that of and their controlchallenges insecticidal sampling and for lessen baits. the plans insecticide management Recent overuse, focused ofare particularly restrictions leaf-cutting addressed on herein, ants. on but Considerable the which the effort also main remain has use challenges been that pest of exerted are regarding yet synthetic species to these compounds be preclude challenges, conquered. which for the such purposesKeywords: impose additional trends and challenges Terezinha MC Della Lucia, Managing leaf-cutting ants: peculiarities, (wileyonlinelibrary.com) DOI 10.1002/ps.3660 Review Received: 6 May 2013 Revised: 22 August 2013 Accepted article published: 1 October 2013 Published online in Wiley Online Library: 30 October 2013 were well recognized by theHilaire French in naturalist his visit Auguste to de the Saint- then Province of S characterization as ‘thieves’ (or pests). of these characteristics:that evolved labor are culminatingstorage. analogous in Although practices describing to agriculture-like cultivationAesop’s modern Fables by ants, human agriculture, such as

14 15 Atta 7,35,36 , 1945) and and 35 species Atta Animal Farm 27,38 . wileyonlinelibrary.com/journal/ps Acromyrmex with their many subspecies, only some 9 or 10 Other control methods, including queen removal and 27,28,37 Acromyrmex Control agents, either biological or chemical, face a different we may allude to George Orwell’s pigs ( of species have broad economic importance as pests (Table 1). mention that all leaf-cuttingequal ants than are others. equal, Among but the some 15 are species of more colonies and some of physical destruction of the colony,to are ants limited to with small small areas and and superficial colonies such as young 2.2 Foraging andAnother fungus cultivation importantforaging peculiarity for of thefungus-cultivated leaf-cutting garden. provision Regarding of ants herbivory, fresh these involves ants leaves are to be used in a Therefore, concern regardingshould leaf-cutting focus on a ants limited number as ofeconomic species loss and pest on indeed fields occurs. species in which 2 LEAF-CUTTINGAND ANT MANAGEMENT PECULIARITIES LIMITATIONS Leaf-cutting ants exhibit aorganization, foraging, fungus-cultivation, series hygiene and of a complex adaptations,nest namely structure social thatadaptations make render these theiradaptations, insects control unique management and, methods difficult.distinct from because for those usually Such of required for their these pestagriculture, management management in cultivated forests are and pastures. also address We will these subsequently general adaptationslimitations. and emphasize their control 2.1 Social organization The social organization andlargely responsible complexity for the of high colony leaf-cutting efficiencythese observed insects. ants among The colony acts are as a superorganism withqueen: a long-living the key individual that isstructure both responsible and for viability, the colony’s whichoutput. are The sustained remaining byher members its progeny, of reproductive including the theeventually colony winged leave males are the and colony formed(in females to by their that form will distinct new ones, subdivisions),within and which the the colony perform workers (e.g. thecolony brood various defense care, tasks and queen waste attendance,that disposal). are foraging, targeted Therefore, at individuals control other than practices the queenchance have a of smaller success unless their suppressiona or strong impairment: and (1) direct has (negative)(2) impact is on sufficiently the great queen’s tocompromising hinder survival, colony replacement sustainability. or by the queen, thus requirement in the controltypes, of high leaf-cutting direct ants.high mortality In mortality both is of control foraging usuallysuppression. workers the Therefore, is objective, unlikely biological tothat and but achieve chemical even target colony control theassociated agents queen with herself broodare care or and more substantially queen likely impactobtain (or to a fungus) and succeed. caste attendance also Suchagainst explain leaf-cutting agents ants. the A are limited lack portfoliois more of of insecticide difficult used options applied to against biologicalsulfluramid and these control fipronil, species, although chlorpyrifos,even which deltamethrin diflubenzuron, and are among mainlyused. a restricted few to other compounds, are also The More 26,27 25 7,8 sp. 2013 Society of Chemical Industry c Cyathea The end result is Annual consumption 29,30 31 24 can reduce tree diameter The virtually continuous , a grass-cutter, is estimated Their activity modifies soil 32 13 – and pine. 9 and their symbiotic relationships In addition, successive defoliations Eucalyptus 28 20,21 In addition, leaf-cutting ant colonies are Secondary seed dispersal and improved Atta bisphaerica Eucalyptus :14–23 22,23 19 70 – 14 2014; 33,34 3 tons of sugarcane, totaling 450 kg of sugar or 300 L of ∼ Leaf-cutting ants may have various benefits and/or losses. Single defoliation events in The notoriety of leaf-cutting ants as pests is in startling alcohol, and a loss of US$ 60 million. Regarding losses and the status of these ants as pests, however, contrast to theirapparent environmental importance paradox andwhere benefits. is leaf-cutting This ants notants are are difficult native, recognized however,(e.g. to as given agriculture pests that understand andenvironments; of these such in reforestation human-altered recognition fields), environments areas isthat they pose rooted but to an in investment not (namely the thator involving forest agriculture of alleged production), threat which natural may(equivalent surpass an to economic control threshold in costs). areas By where contrast,Guadeloupe leaf-cutting there (French ants is West Indies), no arespread leaf-cutting after paradox invasive. ants failures For in were controlthe widely example, attempts island. soon in Now after they theyareas,inparticularrainforestarborescentfernsof are reached threatening plant species in protected Pest Manag Sci 1.2 Importance: hero,Leaf-cutting villain or ants in between? are thehuman-disturbed dominant settings species where they in occur,to both and natural are be and considered aenvironment; keystone these species antsdiversity, because contribute productivity, of largely and their nutrient to influence and environmental on energy the flow. Managing leaf-cutting antsdemands structural nest complexity and social interaction tothe allow coexistence of upcolony. to millions of individuals within a single www.soci.org considered to bemanagement for models sustainable production. for designing improved agricultural properties by improving aeration, drainage andand root penetration, by increasingand organic availability. matter and nutrient mineralization that an estimated 30%devoted of to plantation the control management of leaf-cutting expenses ants. are germination by manipulation have alsoactivity been associated of with leaf-cutting the ants, by a mature colony of to be recently, leaf-cutting antsengineers because they have modulate, directly and been indirectly, resource availability regarded to as other ecosystem of species biotic and by abiotic changing materials. the physical state availability of suitable foodwhere sources they for occur leaf-cutting further ants emphasizesThese in their examples status areas involve as direct pest costs; however, species. as indirect costs, increased such likelihoodnest, of potential damage erosion to cattle due anddamage machinery, to and due construction clearing to aroundneglected. nest the excavation and foraging, should not be compromise tree growth andtree shape, species and the such yield as of cultivated by 11 mm and height by 0.7 m,at causing the a 13% end loss of in wood a volume 7-year cycle. have led toand recent dentigerumicin. antibiotic discoveries, including candicidin overallmagnitudeofthelossescausedbytheants’foragingactivity supports their pest status within agricultureforests and man-established ineconomic the losses Neotropics. causeddollars, Approximate and by these estimates leaf-cutting global are deemed ants to estimates be conservative. reach of billions of 63,64 :14–23 is not the 70 , a specialized 2014; 69 Escovopsis ), (3) waste disposal ) cultured on the ants’ Escovopsis Recent findings indicate that Pest Manag Sci However, In addition, fungus-cultivation 73 Paraguay, Peru, Suriname, Venezuela Venezuela Mexico, Venezuela Peru Guiana, Guyana, Mexico, Nicaragua, Peru, Suriname, Venezuela – ) 63,65 Brazil, Colombia, French Guiana, Brazil, Colombia, Ecuador, French Acromyrmex 71 74,75 Distribution Pseudonocardia Acromyrmex Leaf-cutting ants are able to maintain and are usually regarded as narrow-spectrum 60 – prevail in larger colonies of leaf-cutting ants, thus 57 Atta 70 – South America 57,61 Pathogens are not the only threat to the fungus garden, and a The metabolites produced by the ant mutualistic bacteria multiple microorganism interactions (not only withfungus) the cultivated and high levelsmetropolises). of hygiene (worthy models for human suitable microclimate is also necessaryand for the yield; desired leaf-cutting cultivation antssuitable are nest chambers able and to to heavily relocate investand maintaining their in nest building, structure. gardens repairing to Pseudonocardia antimicrobials, which are active against andoccasionallyvirulentfungusthatisabletoattackanddevastate species of cultivated ant fungus. continuous monocultural fungus-cultivation without perceivable production disasters –accomplishes with a frequent threats feat and disaster. thatapparently These been modern ants able have to human accomplishability agriculture such to a feat associate becauseinvolving: of hygienic (1) their the strategies use(mainly with of the social mixed metapleural chemicals complexity from from glands), mutualistic exocrine bacteria (2) glands ( theexoskeleton use (as of observed antimicrobials in compartmentalization and management, and (4) communication and nestmate (and even fungus)society. recognition within a structured Such a threat is managed withants, exocrine primarily gland from secretions their metapleural from glands, the which exhibit broad- spectrum antimicrobial activity. generates large amountsare frequently of contaminated with degradedmicroorganisms fungal competitors that plant and are material, other potentially which detrimental to the garden elaborate metapleural gland secretions andPseudonocardia reduced reliance on emphasizing the difficulties of efficiently managing disease in large societies with general chemical mixturesantimicrobials versus as specific potential tools bacterial for such tasks. only threat to the fungusalso attack garden, both the and symbiont fungus generalist and pathogens the leaf-cutting may ants. 45 – 11,39 11,40 Dicots South America Argentina, Brazil and Paraguay Dicots South America Brazil and Peru Dicots North, Central and Dicots South America Argentina, Brazil, French Guiana, Dicots North, Central and Dicots South America Argentina, Bolivia, Brazil, Paraguay, Monocots South America Argentina, Bolivia, Brazil, Paraguay, Monocots South America Brazil 2013 Society of Chemical Industry (Agaricaceae: c Monocots and dicots South America Brazil Monocots and dicots South America Brazil and Venezuela www.soci.org TMC Della Lucia, LC Gandra, RNC Guedes Leucocoprinus The integrity of the fungus The fungus is the main food 50 – 54 – and 53,56 39,46 1,51 A. sexdens Ac. rugosus A. laevigata A. cephalotes Ac. octospinosus The ‘superior agriculture’ developed by 51 Fungal transmission is colony-dependent for Ac. subterraneus brunneus Ac. subterraneus molestans Ac. subterraneus subterraneus Leucoagaricus 51,55 Foraging substrate and distribution of the main pest species of leaf-cutting ants ( The history of agriculture in Attini ants most likely had a single Acromyrmex Ac. balzani Atta A. capiguara Genus Species Foraging substrate Continent Main countries Table 1. origin some 50 millionAmerica years from ago, after Africa. the separation of South wileyonlinelibrary.com/journal/ps Some consequences of such foraging habits includeforaging the increased area of individualfields colonies, away which from threatenshomogeneous cultivated the plantations, colony and nest, thepathogen-contaminated rejection the baits. of higher insecticidal risk and of attack in among the most polyphagous andCuriously, voracious however, insects they known. exhibitharvesting unexpected choices selectivity to inappear their provision to manage the their leaf fungusnoticeable behavioral sources plasticity garden. while in their foraging, foraging The and decisions. exhibit ants its clonal propagationformation (within of the newduring colonies colony the via ants’ itself) nuptial dispersion and flight. by for winged the females the higher Attiniuse (i.e., of freshly the cutfungus, leaf-cutting which leaves was ants) to the cultivate is targettheir the of mutualistic based highly association. various on adaptations ‘domesticated’ that the led to 2.3 Hygiene The intricaciesdensity of in farming leaf-cutting and ants living are under rather high complex, colony involving garden is paramount toto colony colony survival, and suppressioncutting its and, ants, jeopardy therefore, which leads the poses to colonies and fungus a the garden contamination challenge. are control possibilitiescontrol, for Physical particularly of in destruction small leaf- of the and shallow physical ant destruction colonies.the However, of fungus the garden with colonycontaminant a (e.g. is a contaminant, pathogen or costly, particularly competitor), is and asocial difficult due structure biological to reaching the and hygiene practicesants when performed securing by their leaf-cutting garden maintenance and yield. source for thebasidiomycetes: ants, and theseLeucocoprinae). fungi belong to two genera of

16 17 108 (Balsamo) Myrmosicarius The efficacy of 27 Furthermore, crop 98 – plantations and/or the 96 spp. antagonizing ant- This lack of effectiveness (Disney) and 26,38,39,41 Beauveria bassiana 27,111 The phorid parasitoid flies that Eucalyptus However, the ants are not passive wileyonlinelibrary.com/journal/ps 27 However, the promising laboratory Trichoderma 108 – efficacy range also reached with thermal 103,104 105 (Metsch.) and Eibesfeldtphora 94 – 27,109,110 92 (Brown), Nonetheless, the chemical control of leaf-cutting ants 102 – 95 99 Phoridae flies compose the main group of biological control The diversification of crop systems, such as the conservation The use of pathogens against leaf-cutting ants seems to (Disney). These parasitoids lay their eggs either in foragingtransporting workers leaves along thecutting leaf trail fragments. or while these workers are efficacy data, however,sulfluramid are (insecticidal) available baits for(ranging providing chemical from high control 83.3 to levels with 100.0%) of againstbroad-leaf species, leaf-cutting efficacy ants attacking maintenance of stripsa of wider native variety vegetation ofof in foraging attack the plants, field, to therebyattractive allows the minimizing alternatives the main are risk plant available. species, especially if well-known agents under scrutiny. of undergrowth vegetation in frequently attack leaf-cutting ants primarily belongApocephalus to the genera 3.2 Biological control Natural biological control of leaf-cuttingally ants favored seems to by be the gener- discussed. diversification In of addition, the crop use systems, ofally applied as encouraged biological because previously control of is its usu- perceivedand rationality, sustainability environmental friendliness; unfortunately,ical however, control biolog- agentsshould do be carefully have studied before eventual potential recommendationuse, and environmental particularly risks in cases and ofefforts. exotic species in classical biocontrol In addition, thesuppress attack the by colony, such whichother is biocontrol natural the agents enemies of same leaf-cutting isone shortcoming ants; of shared unlikely this the by main phenomenon to reasons is such why control little programs. progress has been achieved in be a moretarget promising of biocontrolMetarhizium anisopliae tactic, more which investigation has and been the use with emphasis on infecting the ants, and results that are usuallytranslated obtained into field with effectiveness. these pathogens are not system diversification allowsenemies for that increased diversity areestablishment of of higher likely density natural colonies. to limit colony expansion and the hosts and exhibit a generalized response to phorid attacks. also faces several constraints, which will be addressed. 3.1 Environmental manipulationPhysical, of mechanical the cultivated and field cultural controldiscussed methods independent of are one another, frequently and such methods are used at different levels againstareas that leaf-cutting are attacked ants, by small particularly coloniesexamples in in of superficial control nests. small Some practices within theseremoval categories of include queens, the composta treatments mix (i.e. nest of coverage organicnest with and inorganic top ingredients soil) after and removal of physical the nest destruction. such methods, however, is dubiousrigorous and testing. not By always contrast, subjectedsuggests the to that the cumulative diversification of evidence crop systems gathered potential has against management these ants. fogging. cultivated fungus. that These Nestmate Prompted 90,91 2013 Society of Chemical Industry c 88,89 exhibiting larger, Acromyrmex 57,67,78,79 seem to be the focus Atta Eucalyptus of nest (based on the number and -1 ha 2 However, the levels of nest complexity The containment of these waste products Consequently, the management practice of :14–23 77 80 . 87 – 70 – Furthermore, nest construction and maintenance 22,75 75,84 The high levels of care and sanitation exhibited by 83 2014; – 81 Daily Mail levels by opening new nest ventilation orifices, to prevent 2 61,66,68 The management tactics (or control methods) under recent deeper andinvolve myriad more underground tunnels, deposits and interconnected intricatechambers. designs than 2.4 Nest structure The nesttheir structure fungus-cultivation habits ofsometimes and leaf-cutting reaches socialarchitectural ants extremely organization, achievements which rivaling high is thosethis of levels phenomenon a was China’s recently of Great reflection exploredfrom Wall; in complexity the a of newspaper in section leaf-cutting ants cause constraints ineither pathogens the or insecticides, use thereby of preventing these a control agents from substrate reaching with key castes or the entire colony. noxious gas from spreading byto shutting recycle down tunnels, waste and materials even toand necessary. repair nest damage when feasible are dynamic, and leaf-cutting antsproblems by are raising able chambers above to risk levels, minimize tohigh counterbalance flooding CO Pest Manag Sci The history of leaf-cutting ant controlof encompasses methods a broad ranging array frombiological domestic control techniques methods, toof including physical the chemicals and use fromlime, of to inorganic a old compounds, diverse chlorinateddodecachlor), set fumigants, such compounds traditional (e.g. organosynthetic as compounds aldrin,of sulfur chlordane broad use and (e.g. and organophosphate, carbamates andto pyrethroids) moreCuriously modern though, control, substances andants not (e.g., is management, generally sulfluramid the of goal, leaf-cutting andmanagement and a of basic these economic fipronil). species threshold for isdecisions the usually noticeably based lacking, on with empirical control observations. 3 TRENDSMANAGEMENT IN LEAF-CUTTING ANT Managing leaf-cutting antsand the colony. www.soci.org vary among species, with species of area of nests in a given field) have been suggested. the physical destruction of large leaf-cuttingto failure; ant fumigation nests and/or thermal is fogging doomed require sufficientdistribution gas and careful dosing to achieve the desired effect. scrutiny will be emphasized with their potential practical suitability against leaf-cutting ants. Regretably,alternative efficacy to data insecticide on use methods are scarce and variable. Reliable thresholds will provide a foundationof for the leaf-cutting proper ants management rathercontrol-making decision. than the current prevailing empirical in isolated internal nestthe chambers fungus or garden, aided externaland by piles, strict hygienic labor away behaviors division from to (e.g.guarantees high minimize levels grooming of hygiene contact and minimizes with the potential contaminants) to risks the fungus garden and to colony survival. and even fungus recognitioncolony. further aid in such efforts by the by increased concern and studies aimed atinjury determining economic levels of leaf-cutting ants,seems to a be welcome occurring. Cultivated change inof approach attention regarding thisthe effort, range of and 13.4–39.2 economic m injury levels in 124 – 129,130 119,120 :14–23 121 70 However, 2014; 27,111,117 9 weeks) prevents its ∼ However, their potential from Paraguay from the Another approach against 131 Pest Manag Sci – 129,131 39,42,122 123,127 -eudesmol, a bioactive compound -eudesmol among workers of leaf-cutting – Atta sexdens β β 121 show promise against leaf-cutting ants 124 insecticides or as chemical backbones for new clone effective against leaf-cutting ants, 117,118 ). per se Representative pattern of nestmate aggression with mutilated Eucalyptus 125,126 Atta sexdens Compoundsthatmodulatebehaviorarealsoobjectsofattention Among the new pesticides under development, biopesticides or Natural products have had and continue to have crop protection commercial use. against leaf-cutting ants,show and, among promise. these,recognized Some natural in repellents plants theMedicine and Programme in of the plant Caribbean Applied (TRAMIL),repellence extracts, Research initiated to leaf-cutting in ants to as 1982, and may do Popular provewith exhibit useful recently in cultivated association plants, therebyminimizing diversifying the the crop risk system of and attack. biorational pesticides have received considerable attention. value both as insecticide molecules, but these productssame concerns are and still shortcomings as limited synthetic bynatural compounds. compounds, the particularly Some from plant extracts (unlike others, such as lime stone), Again, these compounds’problems presumed of environmental the evolution safetyhave of and resistance attracted to attention. syntheticcurrent insecticides Plant research on insecticidal extracts compounds for are use inCuriously, baits. at the it forefront isand of frequently not neglected originphysical–chemical that (either properties chemical and naturala consequently structure, or given the synthetic), toxicity compound,recorded of problems determines and of the insecticide thatof resistance one doubtful leaf-cutting with account the in ants1960s. exception notably lack precludes such use despite itsrecognition; potent interference with such nestmate interferencemortality among nestmates leads (Fig. 1). to aggression and high Figure 1. ants and body parts sparked by ants ( and a few other compounds are also employed. in laboratory experiments, eitheror affecting their cultivated the fungus. ants themselves for field use stillvapor deserves pressure attention because, asfrom for an in example, the high the mechanisms of colony suppressionpoorly by known. these Some alternatives, compounds such are asto abamectin, be also proved effective inqueen’s colony fertility, suppression but by directly its impairing slow the activity ( leaf-cutting ants thatthe was mid-1970s developed and and late explored 1980s between was to increase bait pick-up The Sulfluramid 37,114,115 2013 Society of Chemical Industry The baits are c 116 www.soci.org TMC Della Lucia, LC Gandra, RNC Guedes 111,113 of surface diameter), , are not amenable to 2 Atta Deep and complex nest structures, Thermal foggers have been the target Therefore, methyl bromide is no longer 111 33,37 The wholesale death of this caste affects 112 116 – 114 Thermal fogging of insecticides is another management The use of fumigants (i.e. gas insecticide), primarily methyl Toxic baits containing attractants to leaf-cutting ants have fungus-cultivation, resulting in colony starvation. wileyonlinelibrary.com/journal/ps 3.3 Insecticides, repellentsInsecticide and application pheromones prevails against leaf-cuttingout ants through- their areapractices of – occurrenceand powder as toxic application, pest baiting. fumigation, speciesis The achieved thermal application in by pumping of fogging four theopening dry insecticide and distinct into powder active the orifices. nest formulations Organophosphates, viaparticularly carbamates pyrethroids its have and main been used asefficient dry control powder under to provide dry environmentalsmall conditions and and against shallow nests. might be due to a wide rangethe of pathogen possibilities, formulation including and stability the of efficacybut of the the delivery system, remarkablepathogens resilience is of more ants likelydefend to and against recover be the from due their usewhich to exposure are greatly of to their limited these in field capacity control laboratory settings. agents, to detect, alternative used againstthermal these foggers to pests. heat This‘fog’ up in diesel involves which the or insecticide the mineral is suspendedTo oil use and suppress to thus large of disseminated. generate colonies the (with over 10 m an option against leaf-cutting ants,available. and no substitute is currently bromide, was often previously employed against leaf-cutting ants. The compound was directlyand applied active to orifices), the passing nestof from (again pressure. via liquid As a open to gas, gas thethe compound upon is nest, the able thereby release to spread causingto throughout its its suppression. high However, mammaldepleting in toxicity, substance addition methyl that bromide is being isthe phased Montreal an Protocol. out ozone as layer- agreed upon in this practice because thechambers powder will housing not the reach queen, morethat its look protected after brood these insects, and thus the failing to minor suppress workers the colony. as usually observed in mature nests of widespread use,compounds and currently sulfluramid under large-scale and use. fipronil are the main of improvement, and theirremains useful, application although granular against toxic baits leaf-cutting areof the ants insecticide main use method because of their relativelyand low cost, generally high low efficacy environmentalIn impact addition, (when fog properlypotentially used). dispersion allowing in tunnel complex blockingfog-applied by nests insecticide the from is reaching ants key relatively preventing nest chambers. the slow, distributed near the ant trailsbait and is based nest on the openings; nest the size, andintroduce quantity the them ants into of pick the nest. up Until the its granules prohibition, and dodecachlor was the compound of choice in the early use of toxic baits. such a technique requires fog application into active nest openings until the nest is saturated. has largely replaced dodecachlor in toxic baits, although fipronil high persistence of this organochlorideto and foraging its workers are low the likely acute causes toxicity ofThe its success harvested in toxic baits baits. arethe taken fungus garden into and allegedly the also the nest, minor workersare thus when handling they the contaminating fungus, which causes their eventualfour death to within five days.

18 19 - α 43,138,139 and have L.) showed 146 ,thusopening Atta capiguara The challenge here is A. bisphaerica 139,140 27 139 Saccharum officinarum (Forel). wileyonlinelibrary.com/journal/ps bisphaerica . Therefore, to secure their FSC certification status, A This European organization for the certification of 145 However, leaves of jaragua grass ( 144 143 – however, it demands time, money and joint work between 141 27 ¸alves) and . ., Thesearchfornewantagonisticmoleculesoriginatingfromtoxic different nests, directing theeconomic control thresholds effort under and developmentsubjected eventual to for use attack forest by of leaf-cutting plantations Atta ants, particularly of the genus 4.2 New attractantsThe for success toxic of baits a toxic baitdependent used on against its leaf-cutting ants attractant, is andchoice largely citrus in currently extracts marketed are baits; the however,the common the bait granules mass are and also size important of variables to consider. (Nees) Stapf) and sugarpromisingresultsasbaitattractantsfor cane ( up relevant possibilitiesremains to for be explored grass-cuttingwith not pathogen-contaminated only ant baits. with insecticidal species, baits, which but also cypermethrin and deltamethrin) against leaf-cutting antsenvironments. in these forest products promotes integrated pest management andtermmonitoringofhealthandenvironmentalimpactsincultivated long- forests and, consequently, is(including restricting sulfluramid, synthetic fipronil, fenitrothion insecticide and the use pyrehtroids the large reforestation companies andof principle insecticidal large-scale users baits areand increasingly monitoring interested in addition in to pestsynthetic seeking compounds sampling alternatives under to use. the current or repellent plants is on thehave increase. Since been the studying 1980s researchers dodecachlor these the plants studies but havethat it been after can intensified the be up saidphytochemicals. prohibition to that The there of the literature is is point aA very real abundant summary ‘race’ on in of this theet these al search subject. of studies new can be found in Montoya-Lerma 4.3 Naturalcompounds insecticides as a replacement for synthetic The use ofbaits for organo-synthetic leaf-cutting ants without insecticides any naturalavailable. is alternative currently Old pervasive synthetic compounds inset such toxic as the dodecachlor, which standardunderstandably been for banned efficacy ororganic highly pollutants. against restricted Successful leaf-cutting ashowever, successors have persistent ants, been to targeted have by such(FSC) the in compounds, Forest its Stewardship policy Council onplantations. the management and certification of forest Improved bait granuleants, mass which and may vary size withbaits can retain the a improve species standardized granule targeted, and pick-up but attractantwhich are (citrus by commercial not extracts), suitable for grass-cutting ants such(Gonc as the development of toxicalternatives baits have already for been recognized, grass-cutting although some ants; of these alternatives promising did not performbaits. as desired when incorporated into biologists and chemists. Theparticularly search natural continues, alternatives, but arewithout alternatives, difficult risks to and find restrictions, andcomplex as are previously phytochemical not discussed. However, mixturesextracts) usually (e.g. have reduced from risks and restrictions, unpurified plant been successfully subjected toleaf-cutting ant small-scale management tactic. use as an important nests Atta Eucalyptus 2013 Society of Chemical Industry The problem 132,134 c 137 can be considered a per se All alternative methods to the 27 .). The development of sampling plans et al 90,91 Brood, trail and alarm pheromones were 135,136 :14–23 70 134 – 132 2014; Among reforestation companies in Brazil, for instance, empirical Physical, mechanical and cultural control strategies against Thesamplingfocusofeitherinjuryorneststillrequiresdefinition. tend to be easierof to potentially locate allowing and the quantifyand recognition with of minimum the their added spacing area benefit betweendistanceinterpolationusingspatialanalysis.Thisprocedureshould of nests influence with georeferencingallow and us to delimit the range and distribution of injury from methods prevail, and the so-calledmost popular. ‘worst In this focus technique, a technique’ visual survey is ofleaf-cutting the the occurrence ant of nests and their damage isthe worst performed sites, to which recognize are used in decision-making. Pest Manag Sci leaf-cutting ants are limitedwith and restriction generally usedfound (a in in Montoya-Lerma good small areas, review on these methods can be 4 CHALLENGESLEAF-CUTTING FOR ANTS MANAGING The management of leaf-cuttingsome ants of is which not were short previouslypeculiarities of addressed challenges, and while discussing their their addressing management the current limitations trends in and leaf-cutting ant also management. while Managing leaf-cutting ants(bait contaminated withimprove pathogens their orexposure field of toxic the efficacy bait compounds) to dueattractiveness. environmental to conditions to and improved the potentially reduced www.soci.org suitable for decision-making, however, lagslimited research far effort. behind with very Although injury samplingmaking is (since it usually directly preferred incurs when in decision economical loss), is the extrapolation of the worst scenario andof not the identification the sites underlevels, justifiable which control leads basedof to on what insecticide economic should injury (insecticidedevelopment be of avoided baits sampling – inneeded and plans presents the a particular). for challenge, overuse demanding procedures leaf-cutting Therefore,distinct that from are ants those the usually is applied torequiring sorely agriculture a pest strong insects spatial and analysis component. tested by beinggranulated baits, but impregnated the results were into disappointing. small sachets containing 4.1 Applyingants integrated pest management to leaf-cutting The basicintegration tenets of a ofpopulation range levels integrated below of the economic practices pest injuryof level, (or where the the control management tactics) cost tactic to equals areinfestation. the Although contain economic the integration loss of pest the control caused tactics by against leaf- cutting the pest ants requires improvement,injury the levels against availability these of species is economic lacking.sampling Experimentally procedures based and schemes to assess antto population allow levels decision-making with suchexistent.Theestablishmentofeconomicinjurylevelsfor thresholds are virtually non- chemical control of leaf-cuttingchallenge ants because much still hasrecommended to for be large-scale done use. before Infour they this specific can section, be the challenges focusdiscussed. that is on have an impact on those already plantations has recently been the target of attention, andseems the effort to be advancing. of Pest Anim ´ uva, as :19–34 :14–23 :250–253 32 J Trop Ecol 70 Herbivory of :1946–1957 27 ´ oria de vida 78 Environ Manag Acromyrmex 2014; and Biotropica Ecology ¨ olldobler B, Atta ˆ ancia e hist Formigas-cortadeiras – da ´ uva no cerrado. A sa Deutsch Entomol Z :143–156 (1980). Pest Manag Sci 7 ˜ ao com a ciclagem de nutrientes ¸ in a tropical rain forest in Costa Rica. Formigas-cortadeiras – da biologia ao :315–321 (2007). . Harvard University Press, Cambridge, :1–9 (1984). The Ecology and Evolution of Ant–Plant :13367–13371 (2005). ´ 8 ogicos da sa 274 ıvel relac ´ 102 :1265–1276 (2003). :373–386 (1994). . Vol. 1, ed. by Della Lucia TMC. Editora UFV, 84 for the invitation to prepare this review ´ e-Nunes AJ and Sanhudo CED, Taxonomia e 69 . Springer-Verlag, Berlin (2003). ¨ olldobler B, Eusociality: origin and consequences. Atta cephalotes Behav Ecol Sociobiol :316–321 (1993). :170–178 (1998). . . University of Chicago Press, Chicago (2007). Ecology Oikos 25 30 :219–227 (2000). Biol Zool da USP :343–349 (2010). The Insect Societies 3 . Vol. 1, ed. by Della Lucia TMC. Editora UFV, Brazil, pp. 79 Proc R Soc Lond B , Information transfer in head-on encounters between leaf- ˜ ao CR, Mayh :639–646 (2008). :671–675 (1989). et al queimadas e sua poss minerais. (1985). MA (1971). Proc Natl Acad Sci USA (1997). Leaf-cutting Ants das formigas-cortadeiras, in manejo 13–26 (2011). filogenia das formigas-cortadeiras,biologia in ao manejo Brazil, pp. 27–48 (2011). Paraguay (Hymenoptera Formicidae). well-drained savanna in western Venezuela. (1995). up gaps’ in Neotropical rain forest? aEcol critical review Lett of the evidence. ant nests onAmazonia. secondary forest growth andHerre EA, Plants soil use macronutrient accumulated properties innests. leaf-cutting ant in (Hymenoptera: Formicidae:Atta sexdens Atta). I. The overall pattern in Biotropica engineers. organismsasphysicalecosystemengineers. Interactions I, cutting ant workers: food, trail conditionBehav or orientation cues? and soil nutrient availability: the negative24 impact of fire. (Attini), fruits and seeds inBiotropica Cerrado vegetation in Southeast Brazil. Vasconcelos HL, A pest is acutting pest? ants: The keystone dilemma taxa of of Neotropical13 leaf- natural ecosystems. population of 4 Wilson EO, 5 Wilson EO and H 2Brand 3 Fowler HG, Leaf-cuttings ants of the genera 6 Wilson EO, Caste and division of labor in leaf-cutter ants 9 Jones CG, Lawton JH and Shachak M, Organisms as ecosystem 1 Della Lucia TMC and de Souza DJ, Import 7 Fowler HG, Pagani MI, Silva AO, Forti LC, Pereira-da-Silva8 V Perfect and I and Vandermeer J, Distribution and turnover rate of a 11 Wirth R, Herz H, Ryel RJ, Beyschlag W and H 14 Coutinho JM, Aspectos ecol 15 Farji-Brener AG and Silva J, Leaf-cutting ant nests and soil fertility in a 16 Farji-Brener AG and Illes AE, Do leaf-cutting ant nests make ‘bottom- 17 Moutinho P, Nepstad DC and Davidson EA. Influence of leaf-cutting 18 Sternberg L da SL, Pinzon MC, Moreira MZ, Moutinho P, Rojas EI and 10 Jones CG, Lawton JH and Shachak M, Positive and negative effects of 12 Rico-Gray V and Oliveira PS, 13 Farji-Brener AG, Amador S, Chinchillaa F, Escobar S, Cabrera S, Herrera 19 Sousa-Souto L, Shoereder JH, Schaefer CEG and Silva WL, Ant20 nests Leal IR and Oliveira PS, Interactions between fungus growing ants ACKNOWLEDGEMENTS The authors wouldManagement like Science toand thank A Carrick the for thecomments Editorial guidance provided. and Board The suggestions thought-provoking of providedanonymous by reviewers Dr were Rsupport greatly Wilkins provided and appreciated. two byTechnological The financial the Development National(Brazilian (CNPq), Ministry Council the of ofFoundation of Education), CAPES Research Scientific Aid (FAPEMIG) and is Foundation and and also acknowledged the greatly here. appreciated Minas Gerais State REFERENCES 150 (found ,provided 2013 Society of Chemical Industry c www.soci.org TMC Della Lucia, LC Gandra, RNC Guedes ants, is a tripartite Pseudonorcadia may further potentiate ant Beauveria bassiana spp). Usually a single target is Acromyrmex Acromyrmex despite their susceptibility in laboratory Acromyrmex 147 strains in The defensive hygienic behavior of the leaf-cutting 148 149 Another largely neglected management possibility against The prospective use of pathogenic fungi against leaf-cutting emphasizedinmanagingleaf-cuttingants,eithertheantitselforitscultivated fungus. However, the simultaneous useexhibiting of insecticidal compounds and fungicidalinsecticide activity, and a or fungicide, a may provide mixture synergic effectthecontrolefficacy.Thepossibilityofalsosimultaneouslytargeting of increasing an Pseudonocardia management (targeted at the ant and its fungus) compromisingimportant an component of the colonyits vulnerability hygiene to strategy insecticidal and increasing fungicidal agents. Thismanagement tripartite approach deserves future consideration. in the exoskeleton of approach simultaneously combining tacticscultivated fungus against and mutualistic the bacteria ant, its leaf-cutting ants, particularly appealing results andof indicated the the insecticide, predicted whichcombination is synergic in worthy action attractive ofallow baits additional the could attention. introduction This be ofapproach promising should the be and further pathogen explored. could into the nest. Such an ants has potential,a but challenge. itsfungal An effective conidia interesting field with utilization possibility low remains doses is of to neurotoxic associate insecticides. the wileyonlinelibrary.com/journal/ps 5 CONCLUDINGLeaf-cutting ants COMMENTS remain dominant species in Neotropical America, with some species havingefforts recognized should pest be status. directed Management indeedofeconomicconcern.Suchrecognitionisusuallyneglected, against these speciesleading when to they the overuse are ofare predominantly under insecticidal scrutiny and baits, use restriction which in cultivatedcontrol forests. Suitable alternatives for large-scaleare use sorely against needed, leaf-cuttinginsecticides ants but aided recent byfields plant advances are species with promising diversification tactics. pathogens Thefor in development leaf-cutting and cultivated ants of and sampling suitable plans consistent economic decision-making thresholds will regarding allow to ant control lead and todevelopments is are judicious likely more insecticide comprehensivecurrent synthetic than use. insecticides the without We restrictionalternatives suitable are alternatives; of difficult believe (and such expensive) to that find,compounds given should that these natural also be subjectsafety to scrutiny because health origin and is environmental notand a risk. true determinant of toxicity The reasoning behind suchbehavioral alteration an sparked by approach the neurotoxic involves insecticide,might which the potential impair thecontamination. ants’ A defensiveacethylcholine behavior preliminary receptor against attemptwith pathogen agonist the entomopatogenic using imidacloprid, fungus the in association nicotinic 4.4 Pathogen-insecticide associatedNatural use attack of entomopathogenicseems fungi rather on rare leaf-cutting ants tests. ants, including self-antimicrobial and secretions, allo-grooming certainly contributes thatleads to to spreads this the the disappointing effect resultsthe ants’ and that use of are even usually high obtained concentrationsants. of with fungal conidia against the

20 21 , Atta Proc from ,ed.by Evolution :387–392 :169–197 Am J Agric Insect Soc :4053–4056 49 76 Social Insects (Hymenoptera: 108 ˆ onias de formigas- :7998–8002 (1999). ¨ auser Verlag, Basel, pp. Braz Arch Biol Technol 96 :128–131 (1994). JHygCamb 8 :1033–1039 (2001). :349–354 (2011). :427–437 (2008). :5435–5440 (2008). (Forel, 1908) (Hymenoptera: 268 21 52 ˜ ao de sauveiros externos em ¸ 105 Behav Ecol Sociobiol ¸osa, Brazil, pp. 226–235 (2011). . :91–102 (2003). :29–36 (2001). (3):1–12 (2010). Mycologist :224–231 (2002). (Hymenoptera, Formicidae, Attini): . 5 Cien Flor 11 101 13 ´ arias do lixo das col wileyonlinelibrary.com/journal/ps Proc Natl Acad Sci USA Acromyrmex subterraneus molestans Oikos Proc Natl Acad Sci USA Proc R Soc Lond B PLoS ONE , Phylogeny of leafcutter ants in the genus :2034–2038 (1998). Mol Phylogenet Evol :2263–2269 (2009). Atta cephalotes Behav Ecol . et al Formigas-cortadeiras – da biologia ao manejo ` ezard A, Malosse C, Della Lucia TMC, Errard C 281 Chemoecology Atta sexdens rubropilosa ın H, Zimmerman JK, Nash DR, Boomsma JJ and ´ 276 Acromyrmex subterraneus subterraneus Proc Natl Acad Sci USA :701–704 (1999). :1067–1076 (1984). :27–35 (2006). 65 1 389 ´ ez-Martin H, Zimmerman JK and Wcislo WT, Nest-funding Science , Evolution of cold-tolerant fungal symbionts permits winter Acromyrmex octopinosus :277–285 (2006). :2894–2912 (2008). :304–308 (2003). ´ andez-Mar between workers of monogynous and polygynous49 colonies. Atta cephalotes Wcislo WT, Reducedpest biological management in control the evolution and ofRSocLondB enhanced fungus farming chemical in ants. (2001). Attini ants and62 actinomycete bacteria a reevaluation. et al fungi culture by leafcutter ants at theant–fungus northern frontier of a symbiosis. tropical (2011). comportamental das oper cortadeiras, in Della Lucia TMC. Editora UFV, Vic and the colonialrepresentation indentity concept in in information processing, ants: in the emergence of the social ed. by Deneubourg JL and Pasteels J. Birkh ants use antibiotic-producing bacteria to control garden-parasites. Nature agriculture by ants. tripartite mutualism: bacteriaspecialized protect parasites. ant fungus gardens from and Lenoir A,growingant Colonial recognitionFormicidae). of the fungus in fungus- their fungusLeucoagaricus gongylophorus gardens and formation of basidiomata of Microbial community structure ofand refuse leafcutter dumps. ant fungus gardens compartimentalization collectively isolate hazardous wasteleaf-cutting in ant the 219–237 (1999). ant fungus gardens. in demography and50 putative prophylactic behaviors. ant workers an attine ant: seasonal distributionEcology among potential host species. (2001). Carvalho AOR, Fabricius (Formicidae: Attini) based onDNA mitochondrial sequences. and nuclear Formicidae) focusing the ultrastructural cytochemistry. Biol Sci eucaliptais de Minas Gerais. agriculture. ants., origin of the Attini ant fungus mutualism. 68 De Souza DJ, Della Lucia TMC and Barbosa LCA, Discrimination 69 Fern 67 Hart A and Ratnieks F, Waste management in leaf-cutting ant 58 MuellerUG,DashD,RabelingCandRodriguesA,Coevolutionbetween 59 Mueller UG, Mikheyev AS, Hong E, Sen R, Warren DL, Solomon SE, 60 Lacerda FG, Della Lucia TMC and de Souza DJ, Biologia 61 Lenoir A, Fresneau D, Errard C and Hefetz A, The individuality 63 Currie CR, Scott JA, Summerbele RC and Malloch D, Fungus-growing 64 Currie CR and Stuart AE,65 Weeding and Currie grooming CR, of Bot pathogens ANM in and Boomsma JJ, Experimental66 evidence of Viana a AMM, Fr 55 Fisher PJ, Stradling DJ and Pegler DN, Leaf-cutting ants, 56 Scott JJ, Budsberg KJ, Suen G, Wixon DL,57 Balser TC Hart and A Currie and CR, Ratnieks F, Task partitioning, division of labor and nest 62 Currie CR, Mueller UG and Malloch D, The agricultural pathology of 49 Pavon L and Camargo M, Study of the mandibular glands of 47 Hubbell SP, Howard JJ and Wiemer D, Chemical48 leaf repellency Fernand to 54 Bacci M Jr, Solomon EE, Silva-Pinhati ACO, Mueller UG, Martins VG, 50 Magistrali IC and dos Anjos N, Avaliac 51 Schultz TR and Brady52 SG, Mueller UG, Rehner Major SA and evolutionary Schultz TR, The transitions evolution53 of agriculture in in Mueller ant UG, Schultz TR, Currie CR, Adams RMM and Malloch D, The , ´ ´ on on ˜ oes Atta ¸ :55–61 Naturalia :391–393 74 ´ 5 atico sobre Sustainable BiolInvasions 2013 Society of Chemical Industry Pinus caribaea .s/e.Folheto Proc Natl Acad ´ on Neotropical . ´ ecnicas da Pains c :677–688 (2005). :952–957 (2010). Guia pr 21 45 :253–263 (1983). Oecologia 2 Ann Soc Entomol Bras ˜ oes de ¸ :25–41 (1980). . Springer, Berlin (2011). Normas t Formigas-cortadeiras – da . Graffcor ltda. Ponte Nova 5 Escovopsis Nat Chem Biol ˆ omica (1970). :e22340 (2011). ´ a, Colombia, pp. 337–349 . Harvard University Press, 6 et al ¸as, pragas e plantas daninhas J Trop Ecol ´ e-Nunes J, ˆ ancia economica em la regi ˆ omico causado por populac ¸osa, pp. 245–273 (2000). Ecol Manag :225–247 (2012). :121–159 (1976). em plantac 7 spp.). : uma ilustre desconhecida. :1181–1183 (1990). The Ants 53 PLoS ONE Sociobiology . 40 Bol Mus Entomol Universidad del Valle Atta ´ on a las hormigas de la regi Pesqui Agropecu Bras ˜ ao Paulo Agron , Crescimento de eucalipto sob efeito de (Hymenoptera: Formicidae) and seeds of .S ´ ujo MS,. Formigas-cortadeiras: atualidades no ´ eK,Danoecon :489–495 (2007). . Vol. 1, ed. by Della Lucia TMC. Editora UFV, et al Controle de formigas-cortadeiras ´ uvas (Hymenoptera: ) a La remoci (Euphorbiaceae) a pioneer tree species in Brazil. 39 :14–23 ´ omo responde la hormiga cortadora de hojas :597–603 (2003). Introducci Anim Behav Atta laevigata support leaf-cutting ants to protect their fungus ´ Atta bisphaerica 70 ujo MS, Marinho CGS, Ribeiro MMR and Della Lucia 42 Int J Pest Manag ´ andez F. Instituto. Bogot As sa Atta colombica Manejo integrado – doenc Annu Rev Ecol Syst :4742–4746 (2009). in tropical rain forest. ,vol2,ed.byE.Lichtfouse ´ ujo Jr MV, Leal IR and Wirth R, Cutting more from cut Acromyrmex , 8 pp. (1989). 2014; 106 Biotropica and ˆ anica de sus nidos? :287–298 (1995). :53–59 (1999). :467–473 (2008). ´ andez JV and Jaff :1–8 (2007). TMC, Manejo de formigas-cortadeiras, in biologia ao manejo Brazil, pp. 400–419 (2011). Mor. elementos para24 o manejo da praga. AFN, Costa JMFM, desfolhamento artificial. Florestal (1998). de formigas herbivores. mec (1987). from the nest. permanence and plasticity of foragingleaf-cutting trails ant colonies in ( young and mature 24 formigas-cortadeiras em reflorestamentos (1998). ed. by Zambolin L. Editora UFV, Vic ed. by Fern Ropero MC, ¿C Atta cephalotes Cambridge, MA (1990). Calle Z, Leaf-cutting ants revisited:and towards control. rational management cephalotes optimal foraging in a tropical leaf-cutting ant. forests: edge effects onBrazil. foraging herbivory of leaf-cutting ants in leaf-cutting ants? Theenvironmental role patchiness. of foraging territories and trails, and Testing the effectdecisions in of ant-induced plant defences on foraging 8 Neotropical, in (2003). combate, in Borges EE,Atta The interactionMabea fistulifera amongSociobiology workers of theStreptomyces genera garden against the pathogenicSci fungus USA mediator of an(2009). ant-fungus symbiosis. Agriculture introduction a case study of the Guadeloupe invasion. 10 ¨ olldobler B and Wilson EO, 29 Hern 30 Matrangolo CAR, Castro RVO, Della Lucia TMC, Della Lucia RM, Mendes 31 Alipio S, Controle de formigas-cortadeiras. 32 Dow Agrosciences, 33 Mariconi FAM, 28 Oliveira MA, Ara 46 Levin DA, The chemical defenses of plants to pathogens and 43 Roces F, Leaf-cutting ants cut fragment sizes in relation to the distance 44 Kost C, de Oliveira EG, Knoch TA and Wirth R, Spatio-temporal 35 Anjos N, Della Lucia TMC and Mayh 34 Della Lucia TMC, 36 Della Lucia TMC, Hormigas de import 38 Montoya-Correa M, Montoya-Lerma J, Armbrecht I and Gallego- 27 Montoya-Lerma J, Giraldo-Echeverri C, Armbrecht I, Farji-Brener A and 42 Rockwood LL and Hubbell SP, Host plant selection, diet, diversity, and 40 Fowler HG and Stiles EW, Conservative resource41 management by Cherrett JM, Resource conservation by the leaf-cutting ant 45 Kost C, Tremmel M and Wirth R, Do leaf cutting ants cut undetected? 39 Urbas P, Ara 37 Della Lucia TMC and Ara 21 Peternelli EFO, Della Lucia TMC, Peternelli LA, Martins SV and 26 H 22 Haeder S, Wirth R, Herz H and Spiteller D, Candicinin-producing 24 Benckiser G, Ants25 and Mikheyev AS, History, sustainable genetics and agriculture, pathology of in a leaf-cutting ant 23 Oh DC, Poulsen M, Currie CR and Clardy J, Dentigerumicin a bacterial Pest Manag Sci Managing leaf-cutting ants www.soci.org ´ uva :135 Serie spp.). J Appl ısticas ´ ´ 12 umido. :14–23 ˆ encia da ˆ enc Rural :600–606 Formigas- ˜ Atta ao regular 70 ıgenos no ˜ ´ ao do sub- ¸ Ci ¸ 53 ´ opico . ˜ aode madeira caused by the Acta Amazon ˆ encia de iscas ¸ Biochem Eng J Atta cephalotes Atta cephalotes ´ uvas ( 2014; JInsectSci ¸o M, Insecticide Montreal Protocol ´ os no controle de :305–311 (1998). ¸a LA, Mattos JOS Rev Colom Entomol 89 eadistribuic Eucalyptus Environmental Impact of Neodohrniphora elongata :105–117 (2000). Atta sexdens . 1995 assessment, Nairobi, 29 ˆ es dosagens. . Vol. 1, ed. by Della Lucia TMC. Pest Manag Sci (Stal) (Het.: Pentatomidae) and its Rev Bras Entomol :32–40 (2011). (Smith) (Hymenoptera: Formicidae). :1313–1316 (2008). (J.E. Smith) (Lep.: Noctuidae). infectando reinas de 32 Entomol Exp Appl (Hymenoptera: Formicidae) em plantio 104 ız A and Orduz S, Primer registro ´ Forel. sp. Eucalyptus urophyla :185–192 (1996). ˆ encia de produtos termonebul :365–396 (2003). :485–509 (1991). 78 (Hymenoptera:Formicidae),notr :241–244 (2002). leaf-cutter ants (Hymenoptera: Formicidae) in 48 36 , pp. 321–343 (2011). (Hymenoptera: Formicidae) com iscas Landrin- 31 :145–150 (1996). Atta laevigata Ann Soc Entomol Bras ˆ enc Agrotec :31–46 (1997). Ci 26 spp.: panoply of biological control. Supputius cincticeps Brazil :457–460 (1998). :142–144 (1983). Atta laevigata ´ ` 11 e K, Vilela EF, Zanuncio JC and Leite HG, Efeito da a base de sulfluramida e de clopirif 8 . CABI, Wallingford, UK (2006). J Econ Entomol 122 Biol Conserv ´ Neodohrniphora area anteriormente coberta com Spodoptera frugiperada ¸a MAL, Tonhasca A Jr and Della Lucia TMC, Reduction in the ¸a MAL, Tonhasca AJ and Moreira DDO, Parasitism ¸a MAL, Parasitoides de formigas-cortadeiras, in ¸a MAL, Tonhasca AJ and Della Lucia TMC, Caracter ´ ogicas e comportamentais de Metarhizium anisopliae Atta laevigata :49–56 (1999). :1–20 (2007). :573–576 (1999). :115–120 (1996). ´ ecnica IPEF rates of fourAtta vollenweideri phorid speciesArgentina. (Diptera: Phoridae), parasitoids of cortadeiras – da biologia aoEditora manejo UFV, foraging activity of the leaf-cutting ant phorid characteristics of two phorid fly species inleaf-cutting relation ant to their host, the (2012). Invertebrates for Biological Control ofAssessment : Methods and Risk Neotrop Entomol (2009). and responses of their hosts, the leaf-cutting ants. effects – theanalyses Achilles’ to reduce heel risk ofAnnu associated Rev Entomol biological with biocontrol control? introductions. Retrospective de 25 Trichoderma Atta sexdens rubropilosa (Hymenoptera: Formicidae) em Colombia. biol Brown (Diptera: Phoridae), um parasitoide da sa on Sustances that Deplete the Ozone Layer.Bromide 1994 Report Technical of the Options Methyl Committee Kenya (1995). experimentos com iscas granuladas para formigas cortadeiras, control. 37 t Annu Rev Entomol densidade e dotamanhode sauveiros sobre a produc em eucaliptais. selectivity to prey Entomol granuladas 29 isca Mirex-S (sulfluramida(Hymenoptera: 0,3%) no Formicidae) controle26 em de tr de F, em and Rizental MS, Efici bosque em florestas de de portas-isca, visando o controle preventivo deSilvicultura sa Atta sexdens sexdens Acta Amazon controle de de eucalipto. ´ opez E, Romero M, Ort 99 Howarth FG, Environmental impacts of classical biological control. 97 Zanuncio JC, Batalha VC, Guedes RNC and Picanc 98 Zanetti R, Jaff 92 Cruz AP, Zanuncio JC, Zanetti R and Gomes OS, Efici 95 Zanetti R, Zanuncio JC, Souza-Silva A, Mendonc 94 Zanuncio JC, Zanuncio TV, Pereira JMM and Oliveira HN, Controle 96 Almeida AF, Alves JEM and Mendes Filho JMA, Manutenc 93 Zanuncio JC, Cruz AP, Santos DF and Oliveira MA, Efici 104 Guillade A and Folgarait PJ, Life history traits and parasitism 105 Braganc 106 Braganc 109 L 102 Bigler F, Babendreier D and Kuhlmann U, 103 Braganc 107 Braganc 108 Elizalde L and Folgarait PJ, Behavioral strategies of phorid parasitoids 101 Louda SM, Pemberton RW, Johnson MT and Follett PA, Nontarget 110 Verma M, Brar SK, Tyagi RD and Vaerol JR. Antagonistic fungi, 112 United Nations Environmental Programme (UNEP), 113 Forti LC, Della Lucia TMC and Wassu WK, Metodologias para 100 Simberloff D and Stiling P, Risks of species introduced for biological 111 Boareto MAC and Forti LC, Perspectiva de formigas-cortadeiras. ´ otola Insect Insect ,and Behav ˆ ´ ´ omico Arvore Arvore . Neotrop ˆ encia de :165–175 :287–298 Rev Rev JChemEcol 158 243 2013 Society of Chemical Industry J Insect Behav ˆ antica. c :99–103 (2010). ınimo. ´ . Vol. 1, ed. by Della Atta cephalotes 109 , www.soci.org TMC Della Lucia, LC Gandra, RNC Guedes Pesqu Agropecu Bras Atta wollenveideri :267–273 (2010). Oecologia ındice de produtividade ´ J Theor Biol ıvel de dano econ ´ 57 :S92–S102 (2006). ın H, Nash DR and Boomsma ´ :229–236 (2010). ˜ ao de mata atl 42 ˜ ˜ ao JE, Secon DR, Souza LM ao do : divisions of labor, aggressive :225–237 (2001). 60 ¸ 13 ´ atico de formigas-cortadeiras com ´ , UFOP, Ouro Preto (MG, Brazil), p. e-Nunes AJ, Medeiros AGB and Insect Soc workers in contact with colony waste Bull Entomol Res (Hymenoptera: Formicidae). ´ andez-Mar (Hymenoptera: Formicidae). Anim Biol leaf-cutting ants. . Eur J Soil Biol Fire Ants and Leaf-cutting Ants: Biology and ˜ ao’ para combate a formigas cortadeiras, in :1689–1695 (2006). Atta sexdens rubropilosa , Plant compounds insecticide activity against ¨ ens T, Chemical variations in the biostructures Ethol Ecol Evol 273 ¸o MC, Barbosa LCD, Guedes RNC, de Campos Atta sexdens et al , ed. by Lofgren CS and Vander Meer RK. Westview ın H, Zimmerman JK, Rehner SA and Wcislo WT, Active ´ Acromyrmex lobicornis :1791–1799 (2011). :483–488 (2011). Acromyrmex ´ , Feb 2 (2012). 65 osio de Mirmecologia ˜ 40 ao e arquitetura de ninhos de formigas-cortadeiras, in: ¸ :1195–1202 (2012). :241–248 (2000). :363–370 (2002). 23 47 49 Atta sexdens rubropilosa :407–410 (2003). :87–98 (2007). :387–392 (2003). :909–915 (2007). :987–1000 (1996). ´ andez-Mar ´ enez J and Deca isca formicida aplicadade sobre o monte27 de terra solta de ninhos Formigas-cortadeiras – da biologiaLucia ao TMC. manejo Editora UFV, Brazil, pp. 102–125 (2011). Souza-Silva A, Combate sistem 21st Simp cutting ant behavior, and location20 of external refuse dumps. city that rivals the Great Wall ofDaily China‘ Mail with a labyrinth of highways. produced byNeotropical savannas. soil ecosystem engineers.behavior, Examples and the adaptive from value ofspecies nest the of depth in South American 101 (2009). leaf-cutting ants. (2008). Nidificac iscas granuladas em eucaliptais com cultivo m MR, Mortality of from different plant sources. and Deof Souza workers DJ,Atta engaged sexdens rubropilosa Morphometry in of different behavioral the tasks metapleural in gland the ant 27 grass-cutting ants, in Management Press, Boulder, CO, pp. 28–35 (1986). and form of tunneling networks in ants. Soc use of metapleural glands byProc R ants Soc Lond in B controlling fungal infection. behavior in leaf-cutting ants. nest-mound damage by recyclingEcol refuse dump materials. (2006). MR, Silva GA, Coleoptera pests42 of stored products, ventilation in nests of the leaf-cutting ant para formigas-cortadeiras em func J, Immune defense in leaf-cutting antsEvolution a cross-fostering approach. Acromyrmex octospinosus 22 JJ, Variableproduced sensitivity by of the metapleural fungi glands of and leaf-cutting bacteria ants. to compounds Stradling DJ,three Chemistry attine of ants, metapleural gland secretions of Soc florestal de eucaliptais em uma regi Entomol 89 Anjos N, Sistema ‘Arrast 88 Zanetti R, Zanuncio JC, Souza-Silva A and Abreu LG de, Efici 80 Gavaghan J, The bug society: scientists excavate underground ant 85 Jim 79 Ballari S, Farji-Brener AG and Tadey M, Waste management in the leaf- 86 Bollazzi M, Kronenbitter J and Roces F, Soil temperature, digging 76 Lacerda FG, Della Lucia TMC, Pereira OL, Peternelli ELA and T 90 Zanetti R, Zanuncio JC, Mahy 78 Bot A, Currie CR, Hart AG and Boomsma JJ, Waste management in 87 Forti LC, Moreira AA, Andrade APP, Castellani MA and Cadalto N, 77 Lacerda FG, Della Lucia TMC, Serr 91 Souza A, Zanetti R and Calegario N, N 82 Buhl J, Gautrais J, Deneubourg J, Kuntz P and Theraulaz G, The growth 81 Fowler HG, Forti LC, Pereira-da-Silva V and Saes NB, Economics of 73 Fern 84 Kleineidam C and Roces F, Carbon dioxide concentrations and nest 74 Bollazzi M and Roces F, Control of nest75 water losses through Farji-Brener building AG and Tadey M, Trash to treasure: leaf-cutting ants repair 83 Moreira MD, Picanc 72 Bot ANM, Ortius-Lechner D, Finster K, Maile R and Boomsma 71 do Nascimento RR, Schoeters E, Morgan ED, Billen J and 70 Armitage SAO, Broch JF, Fern wileyonlinelibrary.com/journal/ps

22 23 ´ e- ´ ecies Forel ıneas ´ :85–187 ˆ anicos de 24 Forel, 1908 BullEntomol As formigas ´ areas de pr Atta capiguara (Hymenoptera: ¸osa, Brazil, pp. . :337–344 (2004). :179–181 (1999). :497–501 (2003). ıneas ´ Ann Soc Entom Bras ˆ Forel (Hymenoptera: anicos de gram 44 Naturalia Atta bisphaerica 24 32 Forel, 1908, por extratos :321–328 (2002). ´ orio. Atta bisphaerica spp. control (Hymenoptera: 49 :281–285 (1993). avse ¸alves :385–390 (2006). :107–113(1993). 22 Naturalia 36 27 Sociobiology Gonc ˜ ao de substratos, na forma de isca Forel (Hymenoptera: Formicidae). ¸ Forel (Hymenoptera: Formicidae). :1–13 (2013). Rev Ceres Atta bisphaerica 26 wileyonlinelibrary.com/journal/ps Neotrop Entomol Acromyrmex RecommendationsRegardingDerogations (Hym: Formicidae). Atta bisphaerica :175–177 (1999). Forel (Hymenoptera: Formicidae) e sua ˆ enc Rural for 24 Ci ´ arias. :233–240 (2007). ıneas, em laborat ´ avse ¸alves spp. 163 Atta capiguara spp. (Hymenoptera: Formicidae) em :214–220 (2009). (L) as a component in an attractive bait. Gonc Atta bisphaerica 34 J Insect Behav Ann Soc Entomol Bras :249–251 (1999). Acromyrmex subterraneus subterraneus Naturalia plantations in Brazil. , ed. by Della Lucia TMC. Folha de Vic Pinus Recent Adv Phytochem 24 , Seletividade e ˜ ao pelas oper , Insecticides in tropical plants with non-neurotoxic modes :519–529 (1974). ¸ Atta bisphaerica ıneas forrageiras em campo. ´ Atta sexdens rubropilosa ¸alves e et al ˆ 63 anicos de gram Acromyrmex :107–124 (1988). Beauveria bassiana et al Samuels RI, Imidacloprid inhibitscutting behavioral ant defenses of theFormicidae). leaf- of action. (1999). derogations for use of ‘highly hazardous’ pesticides. FSC (2010). to Use Alpha-Cypermethrin, Deltamethrin, Fenitrothion, FipronilSulfluramid in and FSC Certified Forests in Brazil (2010) P, SAO, Novel fungal diseaseEcol Entomol in complex leaf-cutting ant societies. fungi forimidacloprid: perspectives useant for in the control combination of the with leaf-cutting sublethal doses of Mycopathologia of Formicidae). OC, hex forrageiras preferidas para o corte(Hymenoptera: por Formicidae). 212–241 (1993). Desenvolvimento de iscas granuladaspara com atraentes alternativos aceitac components inAtta baits sexdens rubropilosa for17 the control of theFialho leaf-cutting MCQ, Sampling ant methodsof for monitoring colonies the number ofEucalyptus area leaf-cutting ants (Hymenoptera: Formicidae) in de granulada, para formigas cortadeiras de gram Gonc Seletividade de Atta capiguara Formicidae) por iscas granuladas contendogram extratos org Atta cephalotes Res plantio de de formigas-cortadeirascortadeiras em reflorestamentos, in Naturalia (Hymenoptera: Formicidae) por extratosem org campo. 150 Galvanho JP, Carrera MP, Moreira DDO, Erthal M Jr, Silva CP and 144 Forest Stewardship Council, FSC-GUI-30-001145 a VI-0 IsenringRandNeumeisterL, EN, Approved 146 Arnason JT, MacKinnon S, Durst A, Philogene BJR, Hasbun C, Sanchez 147 Hughes DP, Evans HC, Hywel-Jones N, Boomsma JJ148 and Santos Armitage AV, Lorenz B and Samuels RI, Selection of entomopathogenic 149 Diehl-Fleig E, Silva ME da, Specht A and Valim-Labres ME, Efficiency 143 Santos JL, Moreira AA, Boaretto MAC, Andrade APP, Forti LC, Bueno 138 Oliveira MC, Della Lucia TMC, Nascimento D Jr and Lima CA, Esp 139 Lima CA, Della Lucia TMC, Guedes RNC and Veiga CE, 134 Vilela EF and Howse PE, Pheromone performance as an attractive 135 Zanuncio JC, Lopes ET, Leite HG, Zanetti R, Sediyama CS and 140 Forti LC and Boaretto MAC, Selec 136 Cantarelli EB, Costa EC, Zanetti R and Pezzutti R, Plano de amostragem 141 Boaretto MAC, Forti LC, Moreira AA, Bueno OC and Fernandes JB, 142 Boaretto MAC, Forti LC, Bueno OC and Fernandes JB, Seteletividade de 137 Anjos N, Moreira DDO and Della Lucia TMC, Manejo integrado ¸osa, ˜ ao Paulo, Annu Rev -eudesmol ˜ ao JE, Sub- β Bull Entomol 2013 Society of Chemical Industry Pest Manag Sci . ˜ aes STV, Guedes c ˜ Annu Rev Entomol ao JE, Abamectin- :89–93 (2005). :445–454 (2006). :313–320 (2012). ´ :1771–1780 (2004). esn-Robineau L, Des- 117 47 68 -eudesmol in nestmate Acromyrmex octospinosus Acromyrmex octospinosus elicited by caryophyllene. , ed. by Della Lucia TMC. 30 :79–82 (2012). , 2nd ed. Ceres, S β :1224–1233 (2012). (Hymenoptera: Formicidae). (Hymenoptera: Formicidae). 42 :325–347 (2012). ´ 105 etodos atuais de controle e ıcola ´ 10 :103–121 (2008). 33 induced by chemical compounds of Sociobiology JChemEcol Pest Manag Sci :5–6 (1962). , ed. by Della Lucia TMC. Folha de Vic Entomol Exp Appl Crop Protect . . 18 leaves. J Econ Entomol J Pestic Sci :467–473 (2008). As formigas cortadeiras :14–23 :1–13 (2000). 98 Environ Chem Lett Atta sexdens rubropilosa :163–172 (2005). Atta sexdens rubropilosa 13 70 45 Bol Campo Acromyrmex subterraneus subterraneus :489–515 (1994). ¸osa, Brazil, p. 190 (1993). -Eudesmol induced aggression in the leaf-cutting ant β 39 2014; Manual de Entomologia Agr :159–170 (1978). , Atta sexdens rubropilosa 68 :1059–1064 (2000). :45–66 (2006). As formigas cortadeiras et al Lima ER, perspectivas, in Folha de Vic E, Brazil (1988). http://www.pesticideresistance.com/display.php?page-species& arld-472 [accessed 19 April 2013]. leaf-cutting ant the possible use of brood pheromones of the leaf-cutting ant Eucalyptus maculata Atta sexdens rubropilosa J Insect Behav and Vieira PC, Behavioralants changes in workers of the leaf-cutting C, Aurela L(Hymenoptera:formicidae)management.Part1:effectsofTRAMIL‘s and Loranger-Mercirisinsecticidal plant G, extracts. fontaines L and(Hymenoptera:formicidae)management:effectsofTRAMIL’sfungi- Loranger-Merciris G, cidal plant extracts. 56 lethal effects ofcutting ant abamectin suppressing colonies of the leaf- RNC, Aggressive response of pest ant species to carboxilate,ananttrailpheromone,asacomponentofanimprovedbait for leaf-cutting antRes (Hymenoptera: Formicidae). Entomol (Hymenoptera: Formicidae). Brazil, pp. 191–211 (1993). granuladas. lime stone treatment asAtta pest sexdens rubropilosa control fails for the leaf-cutting ant driven alterationsAcromymex on subterraneus subterraneus queenSociobiology ovaries of the leaf-cuttingagriculture and an increasingly ant regulated world. 51 pest management. Merciris G, Insecticidalplants a and review. antifungal chemicals produced by recognition in Bull Entomol Res RNC and Jham GN, Interference of in 129 Marinho CGS, Della Lucia TMC, Guedes RNC, Ribeiro MMR and 116 Gallo D, Nakano O, Silveira Neto S, Carvalho RPL, Batista GC, Berti Filho 117 Antunes EC, Guedes RNC, Della Lucia TMC and Serr 133 Robinson SW and Cherrett JM, Laboratory investigations to evaluate 126 Pesticide Resistance127 North RD, Database, Howse PE and Search Jackson CW, Agonistic (2013) behavior on the 115 Della Lucia TMC and Vilela EF, M 123 Boulogne I, Ozier-Lafontaine H, Germon 128 Marsaro AL Jr, Souza RC, Della Lucia TMC, Fernandes JB, Silva MFGF 122 Boulogne I, Germonsen-Robineau L, Ozier-Lafontaine H, Jacoby-Koaly 118 Antunes AC, Della Lucia TMC, Guedes RNC and Serr 132 Robinson SW and Cherrett JM. The possible use of methylpirrole-2- 130 Marinho CGS, Ribeiro MMR, Della Lucia TMC and Guedes 125 Coats JR, Risk from natural versus synthetic insecticides. 131 Marinho CGS, Della Lucia TMC, Ribeiro MMR, Magalh 114 Souza LF, As formigas cortadeiras e o seu combate por meio de iscas 124 Schoereder JH, Silva HMM, Carvalho AF and Muscardi DC, Proposed 119 Isman MB, Botanical insecticides, deterrents, and repellents in modern 120 Rosell G, Quero C, Coll J and Guerrero A, Biorational insecticides in 121 Boulogne I, Petit P, Ozier-Lafontaine H, Desfontaines L and Loranger- Pest Manag Sci Managing leaf-cutting ants www.soci.org