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Agrawal, A.A Ecology 1998
Agrawal, A.A Ecology 1998
2100–2112
q 1998 by the Ecological Society of America
Abstract. Induced chemical responses following herbivory are common in plants. Plant
responses that change the level of physical or biotic defense are less well documented and
poorly understood. Many Azteca spp. ants are obligate inhabitants of Cecropia spp. trees.
In such ant–plant associations the ants are thought to be analogous to chemical defenses;
previous experiments have demonstrated that ant occupation of C. obtusifolia reduced
herbivory and plant competition and increased growth. Experiments, conducted over two
years, on the dynamics of ant defense demonstrate that leaf damage caused a fivefold
increase in the number of Azteca spp. ants on damaged leaves of C. obtusifolia compared
to that on disturbed but undamaged control leaves. Ant activity peaked 8–12 min after
damage, and differences between damaged and control leaves remained evident for 24 h.
Such rapid induction of ant recruitment is likely to be particularly effective against un-
predictable and mobile herbivores. The magnitude of the induced ant response to damage
was strongly correlated with the number of ants patrolling the leaves before damage oc-
curred. Ant responses to disturbance were not influenced by the presence of damage that
had been applied 24 h previously. However, ant responses to subsequent damage, 24 h after
initial damage, resulted in greater recruitment than to previously undamaged leaves.
Ant recruitment to several other cues associated with herbivory was also tested. Presence
of pyralid caterpillars that naturally feed on C. obtusifolia induced a low level of ant
recruitment, and most larvae were removed from leaves by the ants within 10 min. Exposure
to plant sap collected from damaged conspecifics and a commercially available green leaf
volatile (hexanal) commonly released by plants after damage, both resulted in a doubling
of ant numbers relative to controls. However, the levels of recruitment in response to these
stimuli were insufficient to account for the high numbers of ants and persistence of re-
cruitment observed on experimentally damaged leaves. Experimental wounding of leaves
with minimal leaf tissue removal (using pin pricks) revealed that leaf wounds per se can
only partially explain the induced ant recruitment following leaf damage. The type of
herbivory and size of leaf wounds may be important cues for ant recruitment. Severed C.
obtusifolia leaves that were freshly damaged failed to elicit an induced ant response when
held adjacent to conspecific leaves with ants. However, induction of ant recruitment on
damaged plants did significantly induce a low level of ant recruitment on neighboring
conspecifics, providing evidence for interplant communication. Induced ant responses in
the Cecropia–Azteca system are the result of multiple physical and chemical cues associated
with herbivory. Ant responses to herbivory, although not previously studied in detail, are
likely to be common among myrmecophytic plants and are likely to be an important com-
ponent of antiherbivore defense in such systems.
Key words: Antiherbivore defense; ant-plant interactions; ant recruitment; Azteca; Cecropia;
Costa Rica; hexanal; induced resistance; interplant communication; mutualism; plant–insect inter-
actions; plant cues.
syndrome in tightly evolved ant-plant systems, es- example, rapidly induced localized responses may serve
pecially where herbivory is unpredictable (see Zangerl to make the herbivore flee the plant or at least disperse
and Rutledge 1996). I tested this prediction for the herbivore damage over different portions of the plant
well-known mutualism between Cecropia obtusifolia (Marquis 1996). Systemic responses may serve to pro-
(Moraceae) trees and ants in the genus Azteca. tect the whole plant, but may be more delayed in nature,
Defense by ants in ant-plant systems has largely been and if delayed they are also dependent on the predict-
viewed as a static process (but see Tilman 1978, Le- ability of future herbivory (Karban and Adler 1996).
tourneau 1983, Cronin 1998; A. A. Agrawal and M. T. Localized and systemic responses are not mutually ex-
Rutter, unpublished manuscript). Defense of plants by clusive and are often found in the same system (Clausen
ants has been studied most often by one of two meth- et al. 1991, Haukioja 1991).
ods: (1) ant removal experiments (e.g., Janzen 1966, Several cues could be responsible for rapidly induced
Schupp 1986, Vasconcelos 1991, Fisher 1992, Fonseca responses in biotically and chemically defended plants.
1994), and (2) study of the production of ant rewards Leaf damage alone does not always simulate herbivory
(e.g., Risch and Rickson 1981, Steward and Keeler (Baldwin 1990, Turlings et al. 1990). Cues associated
1988, Koptur 1989, 1992, Smith et al. 1990, Davidson with the herbivores, including disturbance, pattern of
and Fisher 1991, Folgarait et al. 1994, Folgarait and feeding, and saliva may influence the plant response.
Davidson 1995, Frias and Dirzo 1996). This body of Similarly, different aspects of plant damage, including
work has demonstrated that ants often defend plants emission of volatiles (Takabayashi and Dicke 1996), ex-
and have the potential to increase plant fitness. Al- udation of plant sap (Naganuma and Hespenheide 1988,
though few studies have tested the dynamic nature of Dussourd and Denno 1994, McCloud et al. 1995, Jolivet
ant defense, some authors have speculated that ant re- 1996), and visual signs of herbivory (Niemela and
sponses are inducible (Koptur 1989, Smith et al. 1990; Tuomi 1987) may directly or indirectly affect subsequent
A. A. Agrawal and M. T. Rutter, unpublished manu- preference or performance of herbivores. In addition,
script). Previous studies, however, have focused on po- plant cues may affect the defensive phenotype and re-
tential mechanisms for induced responses, such as in- sponse of neighboring plants (Baldwin and Schultz
creased attractiveness or additional production of 1983, Rhoades 1983, Farmer and Ryan 1990, Bruin et
extrafloral nectar; previous studies have not focused on al. 1995, Shonle and Bergelson 1995, Shulaev et al.
induction of defending ants patrolling near damaged 1997). Studies of interplant communication are rarely
sites (but see Fiala and Maschwitz 1990). There are conducted in the field and have not been repeatable.
many biotic and abiotic components of the ant’s and Cues associated with herbivory are likely to be es-
the plant’s environment that can have important con- pecially important for biotically defended plants be-
sequences for the induction and persistence of patrol- cause the plant defenders must recognize and recruit
ling by ants (reviewed by A. A. Agrawal and M. T. to the damage site. Previous damage itself may be a
Rutter, unpublished manuscript). I speculate that ant- cue for rapid recruitment of biotic defenders; for ex-
plants often employ ants as induced defenses. Defend- ample, ants may be poised to recruit more strongly to
ing ants are ideal inducible defenses because of their previously damaged plants than to undamaged plants.
mobile, rapidly deployable, and recoverable nature. Such an association could facilitate ‘‘memory’’ as a
The significance of ants as an induced biotic defense component of the induced response. Memory is an im-
is manifold. Induced chemical response systems include portant component of animal immune responses and
rapidly induced responses, operating over minutes to has been recently reported in an induced plant chemical
hours, and delayed induced responses, operating over response (Baldwin and Schmelz 1996). In biotically
weeks to years (Clausen et al. 1991, Haukioja 1991, defended plants the mechanism of memory could be a
Tallamy and McCloud 1991). Many induced ant re- more rapidly induced emission of plant cues, or could
sponses in ant-plant systems may be analogous to rapidly be based within the ants themselves (i.e., existing pher-
induced chemical responses, and effective against mo- omonal trails or alarm motivation). In either case, mem-
bile herbivores that can damage plants over a short pe- ory could be important, even in systems with mobile
riod. Alternatively, delayed induced responses may also and ephemeral herbivores, if certain parts of the plant
be common, influencing the longer term growth of an will be predictably attacked or if dispersion of herbiv-
ant colony (see Passera et al. 1996). Ant-plants may also ory is beneficial to the plant (see Marquis 1996).
employ other delayed induced responses (chemical or In this paper I report the results of experiments con-
otherwise) that are more effective against predictable ducted over two years that tested the hypothesis that ant
subsequent attackers (see Karban and Adler 1996; A. A. defense of host plants in the Cecropia–Azteca system is
Agrawal and M. T. Rutter, unpublished manuscript). In- induced by cues associated with herbivory. Specifically
duced chemical responses can be highly localized (Olson I asked: (1) Does simulated herbivore damage induce
and Roseland 1991, Zangerl and Berenbaum 1994/5) or localized ant recruitment to the leaves with damage; (2)
systemic, changing throughout the whole plant (Baldwin What is the time course of induction of ant recruitment
1994, Pare and Tumlinson 1997). Such responses po- and relaxation of patrolling following foliar damage; (3)
tentially have different consequences for the plant. For Does ant recruitment result after fresh damage only, rath-
2102 ANURAG A. AGRAWAL Ecology, Vol. 79, No. 6
Statistical analysis
All analyses were conducted using the MGLH rou-
tine in Systat (Wilkinson et al. 1992). All experiments
were conducted with a paired design, where each tree
or experimental unit had both treatments, with no rep-
FIG. 2. Schematic diagram of the experimental design lication within each unit. Repeated measures analysis
used to test for evidence of interplant communication. Leaf of variance procedures were used to test for treatment
A was disturbed (not damaged), and leaf C was damaged. effects in all experiments except in the ant response to
Ant responses were then measured and compared on the ‘‘lis-
ten leaves’’ B and D. disturbance experiment in which a paired t test was
used. Treatments were considered fixed effects and tree
was considered a random effect. In such designs, the
at the base of the petiole. All ants were picked off the between-subjects (remainder) mean square and degrees
leaves by hand. I then took these leaves to an assay C. of freedom are used in the denominator to calculate the
obtusifolia tree and simultaneously held the cut leaves F statistic (Zar 1996:267). In all ant recruitment trials
as close as possible (without touching, but no farther the first census (time 0) was conducted immediately
than 5 cm) next to two unmanipulated assay leaves. prior to treatment and was strictly used to verify that
Ants were censused before the experiment began and
at 4 and 8 min after starting to hold experimental leaves
next to assay leaves. Cut leaves were only used once.
The experiment was replicated with 15 assay trees.
Visual and tactile cues.—To test whether the per-
sistent ant recruitment induced by foliar damage was
due to visual or tactile cues, I attempted to damage
leaves without a detectable loss of leaf area. By lodging
50 insect pins through a small block of styrofoam, I
constructed a device to deliver a large number of tiny
foliar wounds. On each of 24 plants I randomly as-
signed two undamaged leaves to receive either: (1) one
pin press per lobe (7–12 lobes, ;500 pin holes total)
or (2) undamaged controls that were disturbed by clap-
ping the leaf with the styrofoam side of the pin press.
Ants were censused prior to manipulation and at 4, 8,
12, 16, and 20 min afterwards.
Interplant communication and ant-borne signals
Here I tested the hypothesis that cues emanating from
a damaged plant induce biotic defenses in undamaged
neighbors. To test if induced ant recruitment on one
tree would cause closely neighboring trees to have el-
evated ant activity, I selected 15 pairs of trees growing
together with leaves that were within 5 cm of each
other. Two pairs of touching or nearly touching leaves
were selected for each pair of plants (Fig. 2). Because
ant recruitment is very localized in this system (see
Fig. 3), each pair of leaves was considered independent.
The first pair (A, B) was randomly chosen to serve as FIG. 3. Time course of ant recruitment to leaves damaged
the control pair: leaf A was disturbed but not damaged by punching holes vs. undamaged (disturbed) controls for
and ants were censused on both leaves before and 4, experiments conducted over two years.
September 1998 INDUCED ANT RECRUITMENT IN AN ANT-PLANT 2105
TABLE 1. Repeated-measures ANOVAs for the effects of induction treatments on ant recruitment.
there were not differences between leaves prior to treat- cruitment was rapid and localized. The ant recruitment
ment. Similar analyses using MANOVA and profile seen in these experiments demonstrates the importance
analysis yielded the same conclusions. Only repeated- of leaf damage per se, as disturbance without damage
measures analysis of variance are reported (Table 1). elicited minimal change in ant activity (Fig. 3). In both
All error bars shown in the graphs are standard errors years, ant recruitment peaked between 8 and 12 min
of the mean. Data were transformed if necessary to after leaves were damaged. Up to 150 ants per leaf
meet the assumptions of normality and equal variances. were counted during peak recruitment. After 24 h ant
levels relaxed to nearly premanipulation levels.
RESULTS
The number of ants patrolling leaves before damage
Ant responses to damage was a good predictor of ant recruitment following dam-
Ant recruitment to artificially damaged leaves was age (Fig. 4). Plants with high levels of ants before
much greater than to control leaves on the same tree damage had higher subsequent ant recruitment than
in both years of this study (Fig. 3). Induction of re- plants that started out with lower numbers of ants. This
2106 ANURAG A. AGRAWAL Ecology, Vol. 79, No. 6
is consistent with the observation of lower average Induced ant recruitment to previously damaged
peak recruitment in 1996 (35 ants/leaf) vs. 1995 (45 leaves was greater than that to previously undamaged
ants/leaf) because ant numbers before damage were leaves (Fig. 6). Although ant recruitment was higher
lower in 1996 than 1995. on previously damaged plants, initial levels of ant pa-
trolling had not fully relaxed in previously damaged
Disturbance and memory
plants.
Disturbance (without damage) to the petioles of
leaves that had been damaged 24 h earlier did not cause Ant recruitment to herbivores
higher or more rapid ant recruitment than did similar There was a marginally significant effect of ant re-
disturbance to control leaves not receiving prior dam- cruitment to the presence of a pyralid caterpillar (Fig.
age (Fig. 5). Surprisingly, fewer than 15 ants per leaf 7). Control leaves that were disturbed with a small twig
were observed following the disturbances, suggesting of the same size as a caterpillar did not accumulate
that even severe disturbance does not induce the mag- ants. In 2 of the 19 trials, the caterpillars sewed leaf
nitude of recruitment observed after foliar damage. In rolls and subsequently were not bothered by Azteca
addition, this trial shows that ants do not recruit to the ants. In all other trials the ants attacked the caterpillar
presence of damage unless it is fresh, suggesting that as soon as they recognized it and drove it to the edge
only cues associated with fresh leaf damage induce of the leaf until it dropped off the plant. In none of the
recruitment.
FIG. 5. Recruitment of ants to paired leaves that were FIG. 7. Recruitment of ants to the presence of a pyralid
heavily disturbed; one leaf was previously undamaged, and moth caterpillar. Control leaves had a caterpillar-sized twig.
the other was damaged 24 h previously (t test: t 5 20.688, The average time to eviction of the caterpillars was 7.24 6
df 5 10, P 5 0.51). 2.27 min.
September 1998 INDUCED ANT RECRUITMENT IN AN ANT-PLANT 2107
DISCUSSION
Ant responses to damage
Experiments conducted over two years indicate that
Azteca ants rapidly recruit to localized sites of foliar
FIG. 8. Recruitment of ants to extracted plant sap, green damage on C. obtusifolia. This is the first detailed study
leaf volatiles (hexanal), and volatiles emitted from a damaged
severed conspecific leaf.
dividual leaves can affect the level to which the ants sociations, ants do not consume herbivores found at
will recruit. Karban and Niiho (1995) failed to find the wounds, but rather attack and discard them (A. A.
evidence of plant memory for induced resistance of Agrawal, personal observation; J. Longino, personal
cotton seedlings against spider mites. However, Bald- communication). As discussed, plants may not have to
win and Schmelz (1996) did find that induction of nic- entice their ant inhabitants to damaged leaves in in-
otine accumulation was faster in previously damaged creasingly obligate systems.
wild tobacco plants than in undamaged plants. Memory Puncturing C. obtusifolia leaves with pin holes re-
in an induced defense might not only minimize overall sulted in elevated ant levels, although the magnitude
herbivory, but may also reduce areas of concentrated of response was less than a twofold increase compared
damage. Because spatial patterns of herbivory may to disturbed but undamaged controls (Fig. 9). This re-
have differential fitness effects for plants (Lowman sult underscores the conclusion that chemicals asso-
1982, Marquis 1992, 1996, Mauricio et al. 1993, Cole- ciated with leaf damage can induce recruitment, but
man and Leonard 1995), memory could serve the im- that leaf wounds alone, especially when made by small
portant function of dispersing herbivore damage. pins, are insufficient to explain induced ant recruitment
to larger leaf wounds seen in this system (Fig. 3). I
Mechanisms of the induced response predict that visual and tactile cues associated with larg-
Ants are likely recruiting to cues associated with leaf er leaf wounds contribute significantly to the induction
damage, such as the volatile constituents of plant sap of high and persistent levels of ant recruitment.
and green leaf volatiles. Ants must be able to recognize Results of the experiment to test for interplant com-
host plants when colonizing the plants and especially munication are contrary to the results of experiments
when pruning encroaching vines (reviewed by David- using severed leaves, suggesting that cues from other
son and McKey 1993). This identification may largely ants may be more important than cues from plants in
be based in perceptions of volatile plant constituents some aspects of ant recruitment. When both damaged
and leaf damage may release many of these compounds leaves and induced ant recruitment were considered
(Fiala and Maschwitz 1990). I did not observe Azteca (interplant communication experiment), ants on neigh-
ants drinking plant sap at sites of damage, although boring control leaves increased in numbers. However,
this has been observed in other systems (Jolivet 1996; when damaged severed leaves (with ants removed)
J. Longino and A. Fraser, personal communication). were held near control leaves, no induced recruitment
Although I tested for ant recruitment following expo- was detected. Other work on interplant communication
sure to one green leaf volatile (hexanal), many different under field conditions is lacking, and it remains un-
volatiles and mixtures may be released following dam- known whether plants commonly have an altered de-
age. It is unlikely, however, that chemical cues asso- fensive phenotype because of signals from neighboring
ciated with leaf damage are solely responsible for the plants.
high magnitude and persistence of ant recruitment seen
after leaf damage. Cut leaves did not induce ant re- CONCLUSION
cruitment when held next to intact plants with ants. Leaf damage to C. obtusifolia and associated cues
In non-ant-plant systems there is mounting evidence induce significant recruitment of Azteca ants. The in-
that cues released following damage are associated duction of ant recruitment is rapid and localized to
with recruitment of predators of herbivores (Dicke et damaged leaves. Demonstration of this phenomenon
al. 1990, Turlings et al. 1990, Whitman and Eller 1990, indicates that plant defense in myrmecophytic plants
Takabayashi and Dicke 1996). For example, number of is dynamic and not simply a function of ant presence
foraging formicine ants, Formica lasioides, increased in the general vicinity or the level of production of
significantly within 24 h on artificially damaged bush food bodies and nectar. Demonstration of induced re-
lupine, Lupinus arboreus, compared to undamaged sponses in non-ant-plant systems has led to consider-
controls (Wilcox 1996). Recent evidence demonstrates able insight into the constraints and selection pressures
that some of these cues are volatiles produced de novo on plant defense (Parker 1992, Simms 1992, Agrawal
by the plant, suggesting that plants may play an active and Karban 1998). Similarly, cost–benefit analyses of
part in recruiting protectors (Pare and Tumlinson 1997). ant protection should consider the dynamic behavior
In addition, insect damage on Baccharis can produce of ants. Future studies should also consider additional
nectary-like wounds that attract natural enemies of her- cues, including the amount and spatial spread of leaf
bivores who drink the exuding sap (Naganuma and damage, and how these cues are employed by plants
Hespenheide 1988). In these systems, it is presumed and ants in the induction process.
that the predators additionally benefit by finding prey Induced responses to herbivory that attract predators
items at wound sites. Such signals may also be im- have been described from many non-ant-plant systems
portant cues in more facultative ant-plant systems and mechanisms whereby damaged plants attract pred-
where the ants consume the herbivores attacking the ators of herbivores are accumulating. In the Cecropia–
host plant. In obligate systems such as the Acacia– Azteca system, multiple factors are involved in induc-
Pseudomyrmex (Janzen 1966) and Cecropia–Azteca as- ing ant recruitment, including: disturbance, presence of
2110 ANURAG A. AGRAWAL Ecology, Vol. 79, No. 6
herbivores, volatile constituents released from dam- SOS signals from their infested neighbours? Trends in Ecol-
aged leaves, plant sap, and wound size. It appears that ogy and Evolution 10:167–170.
Clausen, T. P., P. B. Reichardt, J. P. Bryant, and R. A. Werner.
wound size may be one of the most important factors 1991. Long-term and short-term induction in quaking as-
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provide its mutualist ants with a direct or immediate bivores. Wiley, New York, New York, USA.
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where on a leaf a folivore feeds. Oecologia (Berlin) 101:
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ACKNOWLEDGMENTS and identification of volatile kairomone that affects acarine
predator–prey interactions: involvement of host plant in its
I am grateful for the numerous contributions of Mathew T. production. Journal of Chemical Ecology 16:381–396.
Rutter during the inception and initial stages of field work of Dussourd, D. E., and R. F. Denno. 1994. Host range of gen-
this project. I also thank Rick Karban for encouraging me to eralist caterpillars: trenching permits feeding on plants with
continue the work and for subsequently improving many of secretory canals. Ecology 75:69–78.
the manuscript drafts. Beth Braker, Deborah Clark, Phyllis Farmer, E. E., and C. A. Ryan. 1990. Interplant communi-
Coley, Sean Duffey, Lee Dyer, Brigitte Fiala, Walter Federle, cation: airborne methyl jasmonate induces synthesis of pro-
Brian Fisher, Martin Heil, Bert Hölldobler, Marcel Holyoak, teinase inhibitors in plant leaves. Proceedings of the Na-
Steven Juliano, Louis LaPierre, Sharon Lawler, Deborah Le- tional Academy of Sciences (USA) 87:7713–7716.
tourneau, Bob Marquis, Chris Nice, Eric Olson, Matt Orr, Fiala, B., and U. Maschwitz. 1990. Studies on the South East
Eugene Schupp, Peggy Stern, Jennifer Thaler, James Um- Asian ant-plant association Crematogaster borneensis/Ma-
banhowar, and Phil Ward contributed assistance, ideas and/
caranga: Adaptations of the ant partner. Insectes Sociaux
or comments on earlier versions of the manuscript. Many
37:212–231.
thanks to all of you. Several anonymous reviewers also im-
Fisher, B. L. 1992. Facultative ant association benefits a
proved the manuscript. Jack Longino kindly helped with iden-
neotropical orchid. Journal of Tropical Ecology 8:109–114.
tification of the ants. Funding for this study was provided by
a Graduate Fellowship from the Organization for Tropical Folgarait, P. J., and D. W. Davidson. 1995. Myrmecophytic
Studies and grants from the Center for Population Biology at Cecropia—antiherbivore defenses under different nutrient
the University of California–Davis, the Jastro Shields Re- treatments. Oecologia (Berlin) 104:189–206.
search Awards Program (U.C. Davis), the Northern California Folgarait, P. J., H. L. Johnson, and D. W. Davidson. 1994.
Chapter of Phi Beta Kappa, and National Science Foundation Responses of Cecropia to experimental removal of Mül-
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