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Ant-Herbivore Interactions: Reasons for the Absence of Benefits to a Fern with Foliar

Nectaries Vanessa K. RashbrookAuthor(s): Stephen G. Compton and John H. LawtonSource: Ecology, Vol. 73, No. 6 (Dec., 1992), pp. 2167-2174Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1941464 .

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Ecology, 73(6), 1992, pp. 2167-2174c 1992 by the Ecological Society of Amenrica

ANT-HERBIVORE INTERACTIONS: REASONS FOR THEABSENCE OF BENEFITS TO A FERN WITH

FOLIAR NECTARIES1VANESSA K. RASHBROOK2 AND STEPHEN G. COMPTONDepartmentof ZoologyandEntomology,RhodesUniversity,Grahamstown 140, SouthAfrica

JOHN H. LAWTONNERC Centre or PopulationBiology,ImperialCollege,SilwoodPark, Ascot,Berks SL5 7PY,EnglandAbstract. We tested the hypothesis that ants, attracted to the foliar nectaries of brackenfern (Pteridium aquilinum), confer protection to the plant in South Africa. Using ant-exclusion experiments with unmanipulated and artificially augmented ant densities, wewere unable to detect a positive effect of ants on bracken, as neither the number of herbivoresnor the level of herbivory was significantly greater on ant-free fronds. We then examined

possible explanations for these results by performing a number of laboratory experimentsusing the ant Crematogaster peringueyi and two lepidopteran species, the major bracken-feeding herbivores. We showed that their eggs were susceptible to ant predation, but gainedprotection from their oviposition sites. We also demonstrated that bracken can benefitwhen densities of ants are high, such as when fronds are infested with honeydew-producinghomopterans, as the lepidopteran larvae were more vulnerable to attack under these con-ditions. We propose that low ant density on the fronds is the primary factor limiting theoccurrence of mutualism between bracken and ants in nature.Keywords: ants; bracken;CapeProvince,SouthAfrica; xtrafloral/foliar ectaries;homopterans;lepidopterans;mutualism;predation.

INTRODUCTIONThe role of extrafloral nectaries (EFNs) as a mech-anism of plant defense continues to be the subject ofspeculation and debate. Experimental studies of a di-verse range of plant species often show that nectar-collecting ants remove herbivores and thus benefitplants (see reviews by Bentley 1977a, Buckley 1982,Beattie 1985, Keeler 1989). However, as discussed byBecerra and Venable (1989), almost half the studies ofant-EFN associations fail to demonstrate that plantsbenefit from the interaction. This is perhaps not un-expected, given the increasing recognition that inter-actions involving mutualism are often variable in spaceand time (Keeler 1981, Thompson 1982, 1988, Herrera1988, Cushman and Whitham 1989, Cushman andAddicott 1991). For example, variable outcomes inant-EFN systems may be a function of ant density,which is determined by a number of factors, includingelevation (Inouye and Taylor 1979, Koptur 1985), andthe availability of alternative, more lucrative foodsources such as homopteran honeydew (Buckley 1983,Sudd and Sudd 1985).

' Manuscriptreceived 15 April 1991;revised 16 January1992;accepted28 January1992.2Address for correspondence:% Center for ConservationBiology,School of Biological Sciences,StanfordUniversity,Stanford,California94305 USA.

An additional explanation for the variable resultsobtained from ant-EFN systems may be that someherbivores possess specializations that render thempartially or entirely immune to ants. This can occur ina number of ways. Herbivores may avoid ants by meansof a size refuge (Tilman 1978, Barton 1986), behavioralstrategies, or chemical defenses (Koptur 1984, Headsand Lawton 1985, Barton 1986, Koptur and Lawton1988), such that ant-related benefits to plants are di-minished or absent.

Herbivores can also circumvent attack by providingants with nutritious secretions or excretions. While thedirect effects of ant-tended herbivores (homopteransand lepidopterans) are detrimental to the fitness of theirhost plants (Strong et al. 1984), increased ant densitieson EFN-plants as a result of these herbivores may beof indirect benefit to the plant (Carroll and Janzen1973, Messina 1981, Beattie 1985, Compton and Rob-ertson 1988, 1991). However, this situation is com-plicated if ants also deter the natural enemies of otherherbivores (Fritz 1983).Brackenfern,Pteridium aquilinum, is one plant wherebenefits from foliar nectaries (the equivalent of EFNsin flowering plants) have never been documented. Ex-clusion experiments in the U.S. and England have con-sistently failed to provide evidence that ants visitingfoliar nectaries influence herbivore abundance or levelsof herbivory (Tempel 1983, Heads and Lawton 1984,

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VANESSAK. RASHBROOKET AL.Heads 1986). Nevertheless, Heads (1986) did find thata large and aggressive ant species was capable of re-moving certain bracken herbivores in short-term in-troduction experiments, suggesting that the potentialfor benefits to bracken may vary, depending upon theant and herbivore species involved.

Given the variable nature of multispecies interac-tions (see Thompson 1988), it is important to repeatant-exclusion experiments in different places and, wherepossible, manipulate the system in order to elucidatethe mechanisms determining the outcome of the in-teraction. Our aim was not simply to extend ant-ex-clusion experiments to bracken in another region, butalso to address the hypothesis that bracken fails tobenefit because ant densities are too low. We attemptedthis using augmented densities of ants visiting the nec-taries, a technique that has not been feasible in mostother systems. In addition, we manipulated the con-ditions under which interactions between ants and her-bivores take place in order to address two questions:(1) Are the herbivores of bracken susceptible to antsduring different life history stages? and (2) Does thepresence of ant-tended homopterans influence the out-come of interactions between ants and other herbi-vores?

THE STUDY SYSTEMOur experiments focused on the ant Crematogaster

peringueyi, which is widespread throughout the geo-graphical range of bracken in South Africa and locallyabundant at our sites in the eastern Cape Province(Rashbrook 1989). Colonies nest in hollow stems andtree stumps or construct cartons from plant fibers gluedtogether with maxillary gland secretions (Skaife 1961).This species is ideally suited for our study because,unlike previously studied systems, carton nests can beeasily transferred into the laboratory and the densityof ant colonies can be manipulated in the field. Wealso noted two other less abundant ant species andoccasional dipterans and coleopterans at the foliar nec-taries, but never parasitic hymenopterans.Our investigations involved two lepidopteran spe-cies, the noctuid Appana (=Conservula) cinisigna, andthe pyralid Panotima sp. near angularis. These are themost widespread and abundant herbivores on brackenin South Africa and the ones that appear most vul-nerable to ant attack (Compton et al. 1989, Rashbrook1989). The life histories of the moths have been de-scribed by Lawton et al. (1988). The eggs of both spe-cies are found on young fronds in the spring. Appanacinisigna lays batches of eggs in the curled frond tips.The larvae feed externally and pupate in the soil at theend of their fifth instar. Eggs of Panotima sp. are laidon the underside of unfurling and opened fronds. First-to-third instar larvae produce discrete grazing areas onthe lower epidermis, and often feed under a web ofsilk. They then descend and mine the rachis (stem),

remaining there until the fifth instar when they pupatein the soil.Both lepidopteran species show instar-related re-

sponses when confronted by C. peringueyi (Rashbrook1989). Early-instar A. cinisigna larvae commonly falloff the frond, suspended by a silk thread, or writhe andregurgitate a repellent fluid. Larger larvae flick theirbody away from the ants or simply ignore them. AllPanotima sp. larvae writhe when attacked, but onlythe repellent fluid produced by the larger larvae pro-vides an effective defense.

Our observations suggest that the two other com-monly occurring arthropods are less susceptible to ants.The eriophyid mite Eriophyes sp. near helicantyx isminute and gains protection from living in galls. Acicadellid, Eupteryx maigudoi, is generally found onolder fronds where ant activity is low, and its mobilityensures escape from ants. This homopteran is not anttended, unlike an unidentified bracken-feeding coccidand pseudococcid. Although these tended herbivoreswere relatively rare in the field, they were abundant onplants kept in shade houses (Rashbrook 1989).

METHODSAnt-exclusion and augmentation experiments

We carried out field studies at two farms near Gra-hamstown (33o19' S, 2632' E) during November andDecember of 1987. This represented the period whenthe potential impact of ants on herbivores was greatest(Rashbrook 1989). In our first experiment at "Fara-way" farm (site -200 m2), we matched 10 pairs offronds at the unfurling stage, based on the initial num-ber of eggs of Panotima sp. present. Appana cinisignawas not monitored because it was too scarce. We useda sticky ant repellent (Formex; Ciba Geigy) to excludeants from the experimental fronds.At the second farm, "Glenthorpe" (site 300 m2),we arbitrarilydesignated one-half of the site as the highant density (HAD) area and the other half as the lowant density (LAD) area. We then increased the densityof ants visiting control fronds in the HAD area by (1)creating two artificial "super" nectaries using pieces ofcotton wool soaked in honey, pinned onto each rachisand (2) transferring 12 C. peringueyi carton nests fromthe surrounding area. Prior to setting up the ant-ex-clusion experiments in each half of the site, we assessedant densities in the HAD and LAD areas by makingcounts of ants on haphazardly chosen fronds. We thenlabeled 40 unfurling fronds in each area, half of whichhad ants experimentally excluded. In all experiments,we recorded the numbers of ants and herbivores onthe fronds at regular intervals (weekly or twice weekly)as a function of treatment. Afterwards, we collectedthe senescing fronds in order to record the number ofPanotima sp. grazing areas on the pinnae and minesin the rachis. Chewing damage by A. cinisigna was notscored because we could not confidently identify its

2168 Ecology, Vol. 73, No. 6



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INTERACTIONSBETWEENANTS AND BRACKENdamage on senescent fronds. We assessed the effectsof ants in these experiments by comparing experimen-tal (ant-excluded) and control fronds within the HADor the LAD area, but made no statistical comparisonsbetween HAD and LAD areas because they were notreplicated.We performed permutation tests (see Edgington 1987,Manly 1991) on the ant-exclusion data, which is equiv-alent to using a one-way repeated-measures ANOVA,but does not require that the data are normally dis-tributed. For example, in the experiment involving in-creased ant densities in the HAD area, the five repeatedmeasures of larval abundance for each treatment wererepresented as a vector in five-dimensional space (20vectors per treatment). The pooled observations in eachrepeated measure of these vectors were rescaled to havea variance of 1, so that differences in each measurewere equally represented. We performed 10 000 ran-dom assortments of the 40 vectors into two samplesof 20 and determined the P value as the proportion ofthese permutations for which the distance between thesample means was equal to or greater than the meansobtained from the experiment.

Maintenance of laboratory ant coloniesWe collected four C. peringueyi carton nests fromthe Grahamstown area and maintained each colony inthe laboratory on separate foraging tables (50 x 30cm). They were fed sugar solution and chopped Tri-bolium sp. larvae, but were starved during the exper-iments to encourage ants to forage on the potted brack-

en plants, accessible by a bridge. We used a singlecolony at any one time, and rotated randomly amongthe four colonies.Interactions between ants and

lepidopteran eggsWe tested the palatability of A. cinisigna and Panoti-ma sp. eggs to ants by first removing them from thefronds and exposing them singly to C. peringueyi on

damp filter paper. The moisture ensured that the eggsdid not desiccate and also served to attract ants to thearea. We exposed a total of 50 eggs (10 replicates offive) for each lepidopteran species to ants on the for-aging table. We scored A. cinisigna eggs after a maxi-mum of 5 h, but because of lower predation rates,scored Panotima sp. up to 36 h after exposure.We repeated the experiments using eggs still attachedto the plant tissue to determine whether they gainedprotection from their oviposition sites. Since A. cini-signa oviposits in the tightly curled frond tips, we usedsmall pieces of bracken containing an egg batch ratherthan individual eggs. We presented sections of frondwith Panotima sp. eggs facing up (a procedure that willenhance their accessibility to ants). We tested and scored21 (seven replicates of three) A. cinisigna batches and50 (five replicates of 10) Panotima sp. eggs 8-24 h afterbeing offered to the ants.

Interactions between ants andlepidopteran larvae

We carried out short-term ant-exclusion experi-ments in the laboratory in order to assess the effec-tiveness of escape strategies used by A. cinisigna larvaewhen confronted by ants. Using first-, second-, or third-instar larvae, the most vulnerable stages (Rashbrook1989), we placed 10 larvae on each of two pots ofbracken. One of the pots was connected to an ant col-ony while the other was without ants. We comparedthe number of larvae remaining on fronds after 4-6 d(depending on the instar), as a function of the presenceor absence of ants. In total, we tested 40 larvae perinstar per treatment, using different ant colonies andpreviously unused pots of bracken for each replicateof 10 larvae.To determine the vulnerability of grazing Panotimasp. larvae to ants, we used field-collected fronds oc-cupied by first-, second- and third-instar larvae, somefeeding under a covering of silk, others naturally moreexposed. We positioned pieces of frond in damp blocksof "Oasis" (a water-retaining material) on the ant for-aging table and left them for up to 18 h. We also sim-ulated the period when the transition from frond graz-ing to stem mining occurs by placing 20 third-instarPanotima sp. larvae on the rachis in the path of on-coming ants.

Interactions among homopterans, ants, andlepidopteran larvae

We performed laboratory experiments to monitorthe effects of honeydew-producing homopterans (coc-cids and pseudococcids) on ant visitation rates andlepidopteran disappearances on bracken. The presenceof homopterans served to increase the nutrient rewardsavailable to ants, making the fronds potentially moreattractive to foraging workers. We placed 10 second-instar A. cinisigna larvae on each of two potted brackenplants. One of the plants had fronds that were infestedwith homopterans while the other did not. Both potswere accessible to a single ant colony. We monitoredthe number of ants visiting each potted plant 3 timesa day (0900, 1500, and 2100) to generate daily meantending levels. After 2 d, we compared the number oflarvae remaining on each set of fronds. This procedurewas repeated 6 times using different potted plants andant colonies. In order to correct for different-sized antcolonies among replicates, we used the ratio of ants (orlarvae) per homopteran-infested frond vs. numbers pernoninfested frond in the t test analyses.

RESULTSAnt-exclusion and augmentation experiments

In the first experiment with unmanipulated ant den-sities, Panotima sp. abundance on fronds with antsexcluded was not significantly different from frondswith ants present (Fig. 1A, grazing larvae P = .567;

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VANESSA K. RASHBROOK ET AL.

B. STEM-MINING ARVAE

/

- - 9 - - II I I I I

z0

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13 23 3 13SAMPLINGATENOV/DEC 987)FIG. 1. Comparison of Panotima sp. abundance on frondswith ants present or excluded (means + 1 SE). (A) Frond-grazing larvae. (B) Stem-mining larvae. (C) Areas of frondgrazing damage. In all cases the sample size is 10 fronds pertreatment.

Fig. lB, mining larvae P = .371). We also found thatthe difference in levels of Panotima sp. damage wasnot significant between treatments (Fig. 1C, grazingareas P = .331).

As expected, at the ant-manipulated site, we record-ed higher densities of C. peringueyi on bracken in theHAD area immediately after the colonies were relo-cated there (HAD mean = 1.45 ants/frond; LAD mean= 0.31 ants/frond). During the course of the experi-ment, numbers of ants declined in both the LAD andHAD experimental areas, although significantly morecontinued to visit control fronds in the latter (Fig. 2A,P = .0148). However, the presence of ants did notreduce A. cinisigna larval abundance in either the LADor HAD area (Fig. 2B, LAD P = 0.512; Fig. 2C, HADP = .312). Although not appropriate to analyze statis-tically, visual inspection shows that A. cinisigna was

not more abundant on control fronds in the LAD areacompared with the HAD area.

We only considered fronds that had evidence of lar-val grazing in the comparisons of damage due to Pano-tima sp. rachis mining. The proportions of fronds withmines were not significantly different between treat-ments within either the LAD or HAD areas (Fig. 3,Mann-Whitney U test: LAD P > .05; HAD P > .05).Again, visual inspection of the data suggests that therewere no differences in mine densities between the LADand HAD areas (Fig. 3).

Interactions between ants andlepidopteran eggs

We detected significant differences in the removal oflepidopteran eggs that had been left exposed comparedwith those left on the frond (Fig. 4). Ants readily re-

z0r-U)LL.-0W-mz

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7 12 17 22SAMPLINGATENOVEMBER987)FIG. 2. Densities of ants and Appana cinisigna larvae(means + 1 SE) on fronds during ant-exclusion experimentswith manipulated ant densities. (A) Ant densities on control

fronds. Appana cinisigna abundance on fronds in the (B) lowant density area and (C) high ant density area. In all cases thesample size is 20 fronds per treatment.

2.0-

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INTERACTIONSBETWEENANTS AND BRACKEN0z0n,' I---1= ANTS PRESENT

1.5-- E = ANTSABSENTV)Li n=14z - n=19n=16< 1.0- n=14 n=16

0z - -

ID.0z HIGHANTDENSITY LOWANTDENSITYFIG.3. Comparisonof stemmining damageby Panotimasp. larvae on fronds with ants present or excluded (means +1 SE)within the high ant density and low ant density areas.Only those fronds with evidence of previous larval grazingwere used.

moved exposed A. cinisigna eggs, but had difficultywith eggs naturally positioned in the curled pinna tip(X2= 54.95, df= 1, P < .001); those that were takenfrom fronds disappeared late in the experiment whenthe plant tissue had dried out and revealed the eggs.Similarly, exposed Panotima sp. eggs were taken byants, but those presented on the fronds remained un-disturbed (x2 = 53.85, df= 1, P < .001), despite beingpresented with the fronds upside down, thereby facil-itating access to ants.

Interactions between ants andlepidopteran larvae

The results of our laboratory ant-exclusion experi-ments using first-to-third instar A. cinisigna larvae onpotted bracken plants show that ants had a significantinfluence on the disappearance of this herbivore (Fig.5). Although we did not directly measure ant densitieson fronds during the experiment, the numbers wereappreciably higher than on fronds at our study sites

m2 10z>- 8mrnJ6

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0 - n=50 1-1 = EXPERIMENTALLYXPOSED EGGSS = UNMANIPULATEDGGS0- n=21

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FIG.4. Lepidopteran egg removal by ants on the foragingtable. Experimentally exposed eggs were removed from thefrond and offered singly, while unmanipulated eggs were leftin their natural positions. In the case of Appana cinisigna, 21egg batches were used (mean + SD= 3.4 + 1.8 eggs per batch,based on measurements of 148 batches).

0 2 2zzL0i 1

1

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= = ANTS PRESENT~5- E9 = ANTSABSENT

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FIG. 5. The laboratory ant-exclusion experiments usingAppanacinisigna arvae on fronds withants presentand ab-sent. Each treatment used 40 individuals at each larval instar(histogram bars show means, vertical lines indicate + SE).

(V. K. Rashbrook, personal observation). All the larvalstages we tested were vulnerable to disturbance and/or predation by ants (first-instar larvae, x2 = 36.84, df= 3, P < .001; second-instar larvae, x2 = 19.52, df=3, P < .001; third-instar larvae, x2 = 11.56, df = 3, P< .01).

Similarly, we found that frond-grazing Panotima sp.larvae (instars one to three) were highly susceptible toforaging C. peringueyi. Ants were undeterred by thecovering of silk under which the larvae often feed, andrapidly removed 94% of the larvae tested (n = 50),irrespective of the instar. In confrontations on the ra-chis between ants and third-instar Panotima sp. larvae,75% (n = 20) of the larvae attempted some form ofdefense (usually producing a repellent fluid) before theywere eventually immobilized and carried back to thenest. Thus, under laboratory conditions, it appears thatants are capable of subduing herbivores, thereby de-fending the plant.

Interactions among homopterans, ants, andlepidopteran larvae

Our experiments using plants with and without ho-mopteran-infested fronds demonstrate the vulnerabil-ity of second-instar A. cinisigna larvae to C. peringueyi(Fig. 6). Ant densities were significantly higher on frondswith coccids and pseudococcids (t test, P < .00001),and consistently more larvae disappeared on thesefronds (t test, P = .0003). Honeydew-producing ho-mopterans therefore complemented the bracken nec-taries in terms of defending the plant against herbi-vores.

DISCUSSIONBoth ant-exclusion and ant-enhancement experi-ments indicated that bracken at our South African fieldsites did not benefit from attracting ants via foliar nec-taries. Ants did not influence the number of lepidop-teran larvae feeding on fronds or reduce the amount

December 1992 2171



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VANESSA K. RASHBROOKET AL.

0C3z0LL_'I-zLL.0LJm:z

25 1UU

15- -60

10- -40

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PRESENT ABSENT PRESENT ABSENTHOMOPTERANS N FRONDS

00

z

FIG.6. A comparisonof ant densities and Appanacini-signa larvaldisappearances means+ 1 SE) n the laboratoryon fronds nfestedwithand withoutant-tendedhomopterans.

of damage they caused (Figs. 1-3). Our results add tothe growing number of studies that show that manyplants with EFNs and foliar nectaries, including brack-en on other continents, do not gain protection fromvisiting ants (O'Dowd and Catchpole 1983, Boecklen1984, Heads and Lawton 1984, Heads 1986, Whalenand Mackay 1988, Becerra and Venable 1989, Mackayand Whalen 1991).Our laboratory experiments pin-point both the im-munity and susceptibility of the two major herbivoresto ant predation at different stages of their life history.Appana cinisigna eggs were extremely palatable, butgained protection from their oviposition sites. Simi-larly, the exposed Panotima sp. eggs were taken byforaging ants, but under natural conditions the eggs arefirmly attached to the pinna undersurface and ants areunable to remove them (Fig. 4).The disappearance of young A. cinisigna larvae onant-visited fronds in our laboratory experiments in-dicated that their escape methods (Rashbrook 1989)were not completely effective (Fig. 5). We also observedthat the survivors were considerably smaller than theircounterparts on the control fronds, suggesting that theirfeeding had been disrupted. Ants could therefore con-tribute to reducing levels of herbivory by harassing A.cinisigna larvae (Bentley 1977a).

Grazing Panotima sp. larvae were easy prey for C.peringueyi, both on the fronds and on the rachis. Thethird-instar larvae appear especially vulnerable, as theyspend several hours burrowing into the rachis, and ourfield observations indicate that they do not reduce therisk of exposure to diurnal ant species by mining ex-clusively at night.Several studies have shown that homopterans canindirectly benefit their host plants by attracting antsthat deter other herbivores (Messina 1981, Comptonand Robertson 1988, 1991, but see Fritz 1983). Ourlaboratory data support this finding, as bracken frondsinfested with honeydew-producing homopterans haveboth significantly increased ant densities and reducedabundances of lepidopteran herbivores compared with

fronds without homopterans (Fig. 6). Although we didnot quantitatively document the behavior of ants be-tween treatments, we observed no increase in theiraggressiveness on fronds occupied by homopterans,and attribute the disappearance of larvae to increasednumbers of ants.

Our experiment with homopterans also tests a majorassumption of Becerra and Venable's (1989) ant-dis-traction hypothesis. They propose that EFNs may en-tice ants away from homopterans, which, without theirant guards, succumb to natural enemies. While reducedtending levels can adversely affect homopteran fitness(Cushman and Addicott 1989, Cushman and Whitham1991), there is no evidence that the nectaries of brackencause such reductions, since we observed that antsstrongly prefer homopteran honeydew to foliar nectar.Similar findings have been reported for other systems(Buckley 1983) as well as bracken in England (Suddand Sudd 1985).

Ants will be most effective plant bodyguards if oneor more of the following conditions are met: (1) periodsof ant activity on plants with EFNs correspond to thoseof the major herbivores (Lawton and Heads 1984,Rashbrook 1989); (2) ants are sufficiently aggressive tosuccessfully deter herbivores (Bentley 1977a, b,Schemske 1980, Horvitz and Schemske 1984, Koptur1984); (3) ants are able to circumvent herbivore escapestrategies (Heads and Lawton 1985, Heads 1986); and(4) ants occur at sufficiently high densities to maximizetheir encounter rates with herbivores (Boecklen 1984,Barton 1986). Although the first three conditions aremet in our system, ants failed to deter lepidopteranherbivores in field experiments, and we suggest thatlow ant densities on the fronds were instrumental ingenerating these negative results. In the laboratory,densities of ants on the potted plants regularlyexceededthose found under natural conditions: the maximummean recorded was 3.5 ants/potted bracken frond,reaching 17.5 ants/frond on plants with homopterans,compared with a mean of generally less than two antsper frond in the field. Although homopterans can belocally common on bracken in the field (V. K. Rash-brook and S. G. Compton, personal observations), con-sistently high ant densities are less likely to occur.Comparative measurements on different continentsshow that ant densities on bracken are generally low,and have never been recorded above a mean of 3ants/frond (Rashbrook et al. 1991). Ants and herbi-vores were present together on < 1% of the fronds inthe U.S. (Tempel 1983), with little opportunity forsignificant interactions between the two. Furthermore,even the relatively high densities recorded in Englandmay not translate into high encounter rates (Heads1986).The benefits arising from mutualisms are inherentlyvariable (Thompson 1982, 1988, O'Dowd and Catch-pole 1983, Schemske and Horvitz 1984, Barton 1986,Koptur and Lawton 1988, Cushman and Whitham




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INTERACTIONSBETWEENANTS AND BRACKEN1989, Cushman and Addicott 1991). Nevertheless, theoutcome of interactions may be relatively predictable,given a knowledge of the conditions under which theytake place. Despite the implications of our ant-exclu-sion experiments, results in the laboratory demonstratethat the dominant bracken herbivores in South Africaare vulnerable to ant attack, especially in their earlylarval stages and when ants are abundant. The lownutritional quality of bracken foliar nectar relative toother resources (Sudd and Sudd 1985) may explain whyhigh ant densities rarely occur in the field. This factor,coupled with the tendency for bracken to form mono-cultures, leads us to predict that the plant is unlikelyto commonly sustain sufficient numbers of ants forbenefits to occur.

ACKNOWLEDGMENTSOur research was supported by an AFRC grant to J. H.

Lawton. We are grateful to Hamish Robertson for identifyingthe ants, M. V. Swain and C. B. Cottrell for identifying Appanacinisigna, and M. Schaeffer for taxonomic information onPanotima sp. We thank Amy Jacot Guillarmod and PatrickGrant for unlimited hospitality during work at Faraway andGlenthorpe Farms, Andrew Beattie for comments on themanuscript, and the late Ross Talent for writing the permu-tation test program and statistical help. We especially thankHall Cushman for invaluable advice, discussion, and com-ments on the manuscript.LITERATUREITED

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