An. Soc. Entomol. Brasil 29(3) 507Setembro, 2000

BIOLOGICAL CONTROL

Predators Impairing the Natural Biological Control of Parasitoids

RONALDO REIS JR, OG DESOUZA AND EVALDO F. VILELA

Depto Biologia Animal, Universidade Federal de Viçosa,36571-000, Viçosa, MG.

An. Soc. Entomol. Brasil 29(3): 507-514 (2000)

Predadores Prejudicando Parasitóides no Controle Biológico Natural

RESUMO - Foi analisado um caso bem conhecido de insucesso técnico nocontrole biológico natural: a coexistência enigmática do bicho-mineiro-do-cafeeiro, Leucoptera coffeellum (Guérin-Mèneville), e seus inimigos naturais.Apesar de ser uma presa adequada a oito espécies de parasitóides e três espéciesde vespas predadoras, todas ocorrendo simultaneamente, o bicho-mineiro-do-cafeeiro apresenta, muito frequentemente, populações acima do nível de danoeconômico para o cafezal. Foi demonstrado que vespas predadoras e parasitóidesinteragem negativamente, possivelmente porque vespas matam as lagartas debicho-mineiro-do-cafeeiro parasitadas. Fazendo assim, vespas predadoras matamparasitóides indiretamente, prejudicando a eficiência do controle biológico natu-ral. Conclui-se que programas de controle biológico deveriam estar baseadosem conhecimentos de interações tróficas, ao invés de simplesmente se basearemem estratégias que envolvam a introdução de inimigos naturais exóticos.

PALAVRAS-CHAVE: Insecta, Interação intraguilda, Leucoptera coffeellum,café.

ABSTRACT - A well known case of ineffective natural biological control: thepuzzling coexistence of the coffee leaf miner, Leucoptera coffeellum (Guérin-Mèneville), and its natural enemies was analyzed. Despite being a suitable preyto eight parasitoid species and three wasp species, all occurring simultaneously,the coffee leaf miner too often presents populations far above the damaginglevel for the coffee plantation. It is demonstrated that predatory wasps andparasitoids interact negatively, possibly because predatory wasps kill parasitizedminer’s larvae. In doing so, predatory wasps indirectly kill parasitoids, therebyimpairing the efficacy of the natural biological control. It is warned that biologi-cal control programs should be based on knowledge of food web interactions,rather than simply on strategies involving introduction of exotic natural enemies.

KEY WORDS: Insecta, Interguild interaction, Leucoptera coffeellum, coffee.

There are many situations in which strate-gies of the natural biological control are noteffective, failing to keep insect pest

populations below damaging levels. For suchcases, the critics often recommend a completeswitch to “more reliable” strategies, such as

508

chemical control. More ecologically con-cerned professionals, on the other hand, wouldrecommend some kind of improvement to thesystem at hand, aiming to hopefully correctthe faults. Solutions, apparently, tend to bebased on a general assumption that when bio-logical control fails, it happens simply becausethe natural enemies are not killing the pest.Ideas such as those are so deeply rooted, thatimportation of natural enemies have too of-ten been regarded as trivial. That is, sincenative natural enemies are assumed to be in-effective, the easiest solution would be tobring along some “effective” ones. The sce-nario is somewhat more complex, however.Whether they attack or not a prey population,natural enemies may fail to keep pests at ac-ceptable levels (Fig. 1).

This paper analyses a well known case ofagronomic lack of success in biological con-trol: the puzzling coexistence of the coffee leafminer, Leucoptera coffeellum (Guérin-Mèneville), and its natural enemies. Despitebeing a suitable prey of nine species ofparasitoids and two species of predatorywasps, all occurring simultaneously (Avilés1991), the coffee leaf miner too often presentspopulations far above the damaging level.This fact has generated much controversy re-garding the real role of natural enemies ascontrollers of the coffee leaf miner. Some au-thors (e.g. Souza 1979) consider that preda-tory wasps, rather than parasitoids, play thesignificant role in the natural biological con-trol of the coffee leaf miner. Others(Konnorova 1985, Konnorova 1986, Camposet al. 1989, Avilés 1991) believe thatparasitoids do play an important role, but theireffect is overlooked by the current samplingprocedures. Shedding lighting on this issue,Avilés (1991) observes that predatory waspsoften do not kill all larvae in the attacked mine,and hypothesizes that these wasps may be at-tacking only parasitized larvae.

We present a test for such an hypothesis,which conforms to one branch of Fig. 1: byattacking parasitized larvae, predatory waspslimit the population of parasitoids by preyingindirectly on them.

Theoretical Considerations. Natural en-emies may not attack the prey when they arenot adapted to it (Fig. 1; box A); this is thesimplest reason for the failure of biologicalcontrol programs. On the other hand, naturalenemies may fail to kill the prey when theyare not able to locate, fight, or subdue it (Fig.1; box B). This may happen when the naturalenemy does not fulfil all phases of a preda-tor’s foraging dynamics, which include search,pursuit, and domain of the prey (Griffiths1980). Accomplishing these phases is not onlya matter of how finely tuned are the biologiesof the natural enemy and the prey, but alsodepends on the idiosyncrasies of the environ-ment in which biocontrol agents are intro-duced. Since conventional agroecosystems donot resemble natural systems, failing naturalenemies are not at all surprising because thedynamics of predation (sensu latu) may beeasily impaired by the novel plant commu-nity composition and spatio-temporal arrange-ment (Altieri et al. 1993).

Natural enemies may also fail to keep pestsat acceptable levels when they promote amoderate attack to the pest population, kill-ing fewer individuals than would be neededfor a successful biological control program.This may happen when several species of suit-able prey coexist in the same area, therebydiverting the natural enemy from the target ofthe biological control program (Fig. 1, boxC). Sometimes, even though when the pest isthe primary prey available, the success is notachieved (Fig. 1, box D). Firstly, if the popu-lation of natural enemies oscillates tooasynchronically relative to that of the prey,chances are increased that not enough naturalenemies will be present at appropriate timesto suppress populations prey. Normally, onewould assign such fluctuations to climatic fac-tors (Villacorta 1980, Campos et al. 1989,Nestel et al. 1994). Mostly overseen, and per-haps more important than climate, are the os-cillations which are originated intrinsically, asthe consequence of a reproductive rate “r”greater than 3.0. A population presenting suchvalues of “r” will most likely show a fluctua-tion pattern that, although absolutely similar

Reis Jr. et al.

An. Soc. Entomol. Brasil 29(3) 509Setembro, 2000

to climatic effects, obey a chaotic dynamicswhich does not depend on external factors(Miramontes & Rohani 1998). Therefore, ifeither natural enemies or pest present high “r”values, their population will fluctuate in achaotic manner, establishing thereby anasynchrony deleterious to any biological con-trol program. Therefore, reproductive rateshould be one of the first traits to be exam-ined when deciding whether or not a given

natural enemy is suitable as a biological con-trol agent.

Secondly, natural enemies may not achievepopulation numbers high enough to signifi-cantly lower the pest population. Low num-bers of natural enemies can be a consequenceof low “r” which arise from genetic and/orenvironmental factors. In such cases, massalrearing and releasing of natural enemies mayimprove the success of biological control pro-

natural enemies failto keep pestpopulation at

acceptable levels

natural enemies arenot killing the

prey

few pestindividuals are

killed

(C)other prey are used

simultaneously

(A)enemies do notprefer the prey

(B)prey is preferred

but is not located

(D)only the concerned

prey is used

too few naturalenemies

asynchrony ofpopulation

numbers of nat.enem. & pests

low rbiological

interactions(competition,

predation)

intrinsical environmental (eg,climatic)

too high r leadingto chaotic

fluctuations ofpest, natural

enemies, or both

dynamics ofsearch-pursuit-

dominate isimpaired becausepest/natural enem.was imported to anew environment

Figure 1. Theoretical reasons for technical failure in biological control programs. Boxesrepresent hypothetical biological mechanisms/processes which prevent natural enemies to keeppest population at technical acceptable levels. Boxes are kept apart for the sake of reasoningonly, but several of these processes may occur simultaneously.

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grams. However, when the population of natu-ral enemies is limited by biological interac-tions, low numbers of natural enemies maynot be totally overcome by mass rearing andreleasing. For instance, when natural enemiesare under severe predation pressure. There-fore, before recommending a given naturalenemy as a biological control agent, it is im-perative to verify the occurrence of potentialnegative biological interactions in the envi-ronment into which the organism is going tobe inserted.

Thus, when biological control programsfail, the assumption that native natural enemiesneed to be replaced (or other natural enemyspecies must be added to the system) mayprove to be an oversimplified, if not a naïve,approach. There are many theoretical reasons,other than unsuitability of the natural enemy,for the lack of success of pest managementprograms based on biological control strate-gies.

Material and Methods

The system under study was composed ofthe coffee plants (Coffea arabica L), its leafminer (L. coffeellum), and its set of naturalenemies: predaceous wasps (Protonectarinasylveirae (de Saussure), Polybia scutellaris(White) and Brachygastra lecheguana(Latreille); and parasitoids (Mirax sp.,Colastes sp., Horismenus sp., Closterocerussp., Proacrias sp., Eubadizon sp., Cirrospilussp. and Tetrastichus spp.) (Zucchi et al. 1979,Avilés 1991).

Leaves of coffee plants, containing minesof the coffee leaf miner, were marked in thefield, prior to the beginning of the experiment.Leaves were chosen so as to contain onlymines which presented no sign of attack bypredatory wasps. Mines which have been at-tacked by predatory wasps are easily distin-guishable by their torn lower surface (Souza1979). Twenty of those leaves were collectedin a 100 m long row of contiguous trees, onfour occasions, 4, 8, 12, and 16 days aftermarking them; thus totaling 80 leaves per row.Leaves were taken to the laboratory, individu-

alized in plastic bags previously perforatedwith a micropin, and kept for 30 days, or un-til the emergence of parasitoids. The techniqueto keep coffee leaves viable in the laboratoryis described by Reis Jr. et al. (in press). Per-cent of predation was defined as the numberof leaves containing torn mines divided by thetotal number of leaves collected, either in arow or for the whole experiment. Similarly,percent of parasitoidism was defined as thenumber of leaves from which parasitoidsemerged, divided by the total number of leavescollected. The area of all mines was estimatedas the area of an ellipse, using the formulapr1r2 where r1 and r2 are the biggest and thesmallest diameter.

The experiment was carried out in threecommercial coffee plantations in the regionof Viçosa County, state of Minas Gerais,Southeastern Brazil. The coffee leaf miner hadnot been subjected to any non-natural kind ofcontrol in these plantations for the last 10years. A total of 13 (100m) rows of continu-ous coffee plants were chosen within the se-lected plantations, so that three rows werelocated in the smaller plantation and the othertwo plantations held five rows each. Rowswere chosen so as to cover the widest spatialrange within each plantation, observing aminimum inter-row distance of 100m alonglines of coffee plants, and 50m across lines.

Statistical analyses inspected the relation-ship between presence of predators and pres-ence of parasitoids, at the local scale, and thepattern of resource exploitation by predatorsand parasitoids. Regression lines were fittedto the data, along with control variables, asappropriate.

Results and Discussion

Predation upon coffee leaf miner is in-versely related to parasitoidism: low levels ofparasitoidism are detected in places present-ing high rates of predation, and vice-versa(F[1;11] = 7.98; P= 0.0165; Fig. 2); and thisphenomenon does not depend on the planta-tion where the data were collected (F[2;9]= 1.41;P=0.29). This suggests some kind of nega-

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An. Soc. Entomol. Brasil 29(3) 511Setembro, 2000

tive interaction between predatory wasps andparasitoids regarding their action upon cof-fee leaf miner. Patterns of resource exploita-tion by predators and parasitoids overlap par-tially, with predators exploiting mines whichare slightly larger than the mines attacked bythe parasitoids (Predators: F[1;6]= 43.99; P=0.0006; r2= 0.88. Parasitoids: F[1;6]= 1165.18;P< 0.0001; r2= 0.99. Fig. 3).

Biological control programs are not nec-essarily improved by assuring the coexistenceof several species of natural enemies. The

notion that natural enemies sum their effectsupon a prey species population is shown tobe false, at least for the case of the coffee leafminer (Figs. 2 and 3).

In fact, in such a system, predators seemto be impairing the action of parasitoids. Suchan idea is based on three facts: (i) predatorsand parasitoids are inversely related (Fig. 2);(ii) predators and parasitoids partially over-lap in their resource exploitation (Fig. 3); and(iii) predators prey on larvae in mines whichare slightly larger than those attacked by

Percentage of Predation

0 10 20 30 40 50 60

Perc

enta

ge o

f Par

asiti

sm

0

10

20

30

40

50

60

70

80

y = 52.3395 - 0.7384xF(1,11) = 7.98, p=0.0165

r2 = 0.42

Figure 2. Local inverse relationship between predation and parasitism of L. coffeellumattacking coffee plantations. Each dot represents one 100m long row of contiguous coffeeplants. Percents of predation and parasitism are defined as the number of leaves containingtorn mines (predation), or the number of leaves from whose mines parasitoids emerged, di-vided by the total of leaves inspected. Data were collected within three disjunct plantations.Statistical analysis included plantations as a blocking factor (F[2;9]= 1.41; P= 0.29), therebyextracting such effects from the observed trend.

Percentage of predation

Perc

enta

ge o

f par

asiti

sm

512

parasitoids (Fig. 3). The picture that emergesis rather simple: by attacking a larvae in amine, a predator makes it unavailable toparasitoids because the larvae is removed. Theopposite is not true, however: larvae attackedby parasitoids remain in the mine, being there-fore potentially available to predators. Thus,predators may kill both parasitoids and theleaf miner. We are not in position to statewhether or not predators look for parasitizedmines, but our data allow the suspicion thatwhen predators attack their “preferred” mines(Fig. 3), many of these mines have been pre-viously parasitized (otherwise Fig. 2 would

not present the inverse pattern). Similar re-sults have already been reported by Moreira& Becker (1986, 1987), working with Nezaraviridula (Linnaeus) attacking soybean. In sucha system, parasitized eggs of N. viridula suf-fer higher predation rate than non-parasitizedones, but the authors refrain from stating thatthe predators prefer such eggs. Rather, theyshowed that parasitized eggs are available topredators longer than are healthy eggs, whichtherefore increases their chances of being at-tacked.

For the coffee leaf miner, when a predatorattacks parasitized mines, the parasitoid is

Mines' size category (mm2) of L. coffeella

0 20 40 60 80 100 120 140 160

Freq

uenc

y

0

10

20

30

40

50

60

70

PredaçãoParasitismo

y = 43.1739e(-0.0197x)

F = 43.9972, p = 0.0006, r2 = 0.88

y = 107.8924e(-0.0530x)

F = 1165.1815, p < 0.0001, r2 = 0.99

Figure 3. Resource partitioning among predators and parasitoids of the coffee leaf miner(L. coffeellum). Mines have been categorized in arbitrary classes of size. Frequency of occur-rence of predators and parasitoids is defined as the number of leaves containing torn mines(predation), or the number of leaves from whose mines parasitoids emerged, divided by thetotal of leaves inspected (n= 1040) in three commercial coffee plantations.

Mines' size category (mm2) of L. coffeellum

Reis Jr. et al.

PredationParasitism

An. Soc. Entomol. Brasil 29(3) 513Setembro, 2000

consequently killed, which weakens the re-productive success of the latter. Onlyparasitoids escaping such a fate would con-tribute to the next generation. Therefore, thenext generation of parasitoids would be guar-anteed if (i) remaining parasitoids present rela-tively high reproductive rate, (ii) predators arenot too abundant, or (iii) coffee leaf minerpopulations are so large that many parasitizedminers are not preyed upon. In fact, despitethe pressure from predatory wasps on theseparasitoids, the system remains relatively sta-ble: predatory wasps, parasitoids and the cof-fee leaf miner coexist in the field (Le Pelley1973, Parra et al. 1981, Reis & Souza 1996).Apparently, such a stability is sustained by acombination of the above three reasons. Thecoffee leaf miner is known to present lowabundance during summer (Nestel et al. 1994,Souza et al. 1998), when predatory wasps ingeneral tend to present higher activity. In thisscenario, the probability of a parasitized lar-vae being attacked is very high, which sup-presses the population of parasitoids in thesummer. As the winter approaches, the abun-dance of the coffee leaf miner reaches itsmaximum (Souza op.cit.), far beyond dam-aging levels for coffee plants (Villacorta &Tornero 1982, Souza et al. 1998). Because ofthe heavy losses suffered by parasitoids in thesummer, their attack upon the miner is notsevere enough to control this pest in the win-ter, but at least the population of parasitoidsis able to rebound in the next generation.

Success of biological control programs ofthe coffee leaf miner would, thus, depend oncorrect manipulations of the impacts fromsome of the above items. It is important torealize that importation of new species is notamong such strategies. Perhaps, the most ef-fective strategy would be getting the best ofthe complete suite of natural enemies. Firstly,parasitoid abundance’s should be increasedright in the beginning of the miner’s infesta-tion, when mostly small mines are present (asshown in Fig. 3, small mines are attacked moreintensely by parasitoids than by predators).As time elapses and mines get bigger, theabundance of predatory wasps need to be in-

creased in large proportions, so that there areenough predators to attack healthy andparasitized mines. Specific techniques forsuch releases are yet to be developed, whichcould certainly open up several lines of re-search.

Specifically for such a system, introduc-ing new highly specific parasitoid species mayprove ineffective, unless such parasitoidspresent explicit strategies to avoid the attackby predatory wasps.

Acknowledgements

This work is part of the first author’s MScdissertation on Entomology presented to Fed-eral University of Viçosa.

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Accepted 28/VI/2000.

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