Interspecific and Intraspecific Interactions Via Plant Responses to Folivory: An Experimental Field Test

Interspecific and Intraspecific Interactions Via Plant Responses to Folivory: An ExperimentalField TestAuthor(s): Stanley H. FaethReviewed work(s):Source: Ecology, Vol. 73, No. 5 (Oct., 1992), pp. 1802-1813Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/1940031 .

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Eco/oigy, 73(5), 1992. pp. 1802-1813 (c 1992 by, the Ecological Society of America

INTERSPECIFIC AND INTRASPECIFIC INTERACTIONS VIA PLANT RESPONSES TO FOLIVORY: AN

EXPERIMENTAL FIELD TEST'

STANLEY H. FAETH Department of Zoology, Ari-ona State University, Temnpe, 1 rriona 85287-1501 USA

Abstract. I tested the hypothesis that phytophagous insect species compete interspecifically on shared host plants by inducing chemical, physical, and phonological changes in the plant that either directly reduce insect growth and survival or indirectly alter attack by natural enemies. I manipulated levels of simulated folivory on branches within eight trees of Qiiercus emor vi in a complete randomized block design. Survival and causes of mortality, including attack by natural enemies, of a dominant leafminer, Catneraria sp. nov., were monitored over two growing seasons.

Survival varied significantly among trees but not among treatments. Causes of mortality also varied significantly among trees. Death from premature leaf abscission increased significantly with increasing levels of branch damage, while mortality from other causes, including death from bacterial and fungal attack, declined significantly with increasing levels of damage. However, neither of these changes in mortality was sufficient to cause changes in overall survival. Leaf damage did not influence attack by macroscopic natural enemies (hymenopteran parasitoids or vertebrate and invertebrate predators). By far, the most important factor affecting survival and causes of mortality within trees was the presence of co-occurring larvae on leaves (i.e., intraspecific competition).

Simulated folivory in the first growing season did not affect folivory by Cameraria or other folivorous arthropods in the next season. Colonization, survival, rate of attack by natural enemies, and amount of herbivory by other arthropods in the second growing season were not affected by levels of leaf damage in the first one. Neither survival nor causes of mortality of Cameraria in the second growing season were associated with folivory by endemic leafchewing arthropods. Simulated folivory in the first growing season did, however, reduce leaf production in the second season.

These results do not support the hypothesis that insect species compete interspecifically via induced plant responses and their effects on the third trophic level (natural enemies of the herbivores). The effects of simulated (first growing season) and insect (second growing season) folivory via induced plant responses on the Cameraria population was negligible relative to intraspecific interactions. Further, my results do not support the notion that folivore-induced responses are defensive and that plants have evolved these responses to manipulate the third trophic level. In natural settings, other factors that influence population dynamics of phytophagous insects, such as intraspecific competition and interactions with microparasites, may obscure any negative effects of herbivore-induced plant responses on interactions among herbivore species and their macroscopic natural enemies.

Kei iiords: .A ri-ona, Cameraria; competition, Emory oak, herbivory;inducedresponses, leafnniners, natural enemies; population dynamics; tritrophic level interactions.

INTRODUCTION

Most theories of community organization and population dynamics have traditionally centered on interspecific competition as a key organizing factor. The role of interspecific competition in phytophagous insect communities, however, has been questioned (Hairston et al. 1960, Lawton and Strong 1981, Strong et al. 1984) and many now consider interspecific competition as less important in these insect communities than other communities (see Price 1983, Strong 1983, Faeth 1987 for general reviews). Interest in interspecific competition among phytophagous insect species has

I Manuscript received 24 June 1991; revised 21 October 1991: accepted 12 November 199 1.

recently resurged with accumulating evidence that herbivory by one species can induce changes in host plants that alter resources for other species that feed concur- rently or subsequently on the same host plant (for reviews see Schultz 1988, Karban and Myers 1989). Induced changes in chemical, morphological, or phenological properties of plants are thought to deter herbivores by killing them or reducing their growth and fecundity, although the generality of these effects are debated (e.g., Schultz 1988, Spencer 1988, Karban and Myers 1989, Tallamy and Raupp 1991).

Induced responses may also affect survival of herbivorous insects by altering attack by their macroscopic natural enemies (Price et al. 1980, Faeth 1986, Price 1986, Niemelk and Tuomi 1987, Schultz 1988, Spen- cer 1988). Herbivory can cause chemical or physical



October 1992 INSECT COMPETITION VIA PLANT RESPONSES 1803

changes, which (1) slow development and thus increase exposure time of herbivorous insects to natural enemies (Clancy and Price 1987), (2) increase movement and thus make herbivorous insects more apparent to natural enemies (Schultz 1983, Bergelson and Lawton 1988). or (3) provide natural enemies with cues for locating insect hosts (Vinson 1976, Weseloh 198 1, Heinrich and Collins 1983, Dicke et al. 1990). Thus, phytophagous insect species may compete indirectly and subtly by altering the host plant and, consequently, attack by mutual natural enemies.

If phytophagous insect species compete directly via induced changes on quality of resources and indirectly via changes in the third trophic level, natural enemies, then interspecific competition may be more important than acknowledged in prevailing concepts of population dynamics and community organization of phytophagous insects. Further, the outcome of such inter- specifc interactions may defy conventional expectations of interspecific competition. For example, complete defoliation of trees by one insect species may result in production of new leaves that are of higher quality to other insect species (e.g., Auerbach and Simberloff 1985, Faeth 1987), while partial consumption of individual leaves results in poor quality, damaged leaves (e.g., Haukioja and Niemeli 1979, Faeth 1987). Further, natural enemies may effectively use cues associated with plant damage only at relatively low levels of herbivory (Faeth 1987). Interspecific interactions among insect species via changes in the host plant need not be an increasing, monotonic function of density as usually envisioned for classical interspecific competition.

Despite the important implications of interspecific competition among phytophagous insects via induced responses and their effects on the third trophic level to community and population ecology, there have been few experimental field tests of this type of interspecific competition. Experiments that control herbivory levels and consider the relative importance of interspecific interactions to other factors affecting populations of phytophagous insects, such as intraspecific competition. are particularly scarce. Here, I tested the hypothesis that folivory causes plant-mediated changes in colonization and survival of a leafmining insect, Caineraria sp. nov. (Davis) (Lepidoptera: Gracillariidae, agrifoli- ella group), with a field manipulation. I tested the effects of different levels of folivory on Cameraria survival and causes of mortality, including attack by natural enemies. relative to effects of intraspecific competition. I also examined long-term effects of folivory on colonization and survival of Cameraria and feeding patterns of other arthropod herbivores.

METHODS

Studio' site

All experiments and observations were conducted from April 1988 to April 1990 at the Oak Flat recre-

ational area (Tonto National Forest), 15 km east of Superior, Arizona (1292 m elevation) in Pinal County. The general habitat in this area is chaparral-oak wood- land dominated by Quercus einorv 'i Torr. (Emory oak), Q. turbinella (Greene) (shrub live oak), Jrctostaph vlos pungens H.B.K. (point-leaf manzanita), Juniperus os- teospermna Torr. (Utah juniper), and J. mnonospernia Engelm. (one-seed juniper).

Host plant and leaf[miner Quercus ernori'i is an evergreen oak that produces

new leaves in late April at the study site and retains them for 1 yr until budbreak the following year.

Cameraria sp. nov. is a univoltine leafminer whose phenology is closely tied to that of Q. emnorvi, its sole host plant. Shortly after budbreak and leaf expansion, females oviposit on upper leaf surfaces. Larvae emerge in -10 d, complete 3-4 instars by September. and apparently enter larval diapause or greatly reduce feeding until March of the following year. Larvae then feed and grow rapidly, consume the majority of upper epi- dermal areas and complete the last 4-5 instarsjust prior to leaf abscission in late March to early April (Bultman and Faeth 1986). Larvae whose mines have coalesced on the leaf may kill and cannibalize other larvae, especially in the first four instars when mouthparts pro- ject forward (Faeth 1 990a, 1991 a). Pupation occurs in the mine about the time of leaf abscission, and emergence of adults is synchronous with budburst. Larvae are the only feeding stage of this leafminer. Faeth (I1986, 1990a, 199 lb) provides further details of the biology of Cameraria and its host plant, Emory oak.

Natural enemies of Cameraria

Cameraria is attacked by >20 species of hymenopteran parasitoids (Faeth 1990b). The majority of parasitism is caused by Paraleurocerus bicoloripes Girault (Encyrtidae), several species of Svmpiesis (S. conica Provancher, S. stigmata Girault, and S. acrohasidis Miller), Closterocerus trifasciatus Westwood, Clostero- cerus sp. near cinctipennis Ashmead, Pnigalio meta- comet Crawford, Chrvsonotoin via sp. (Eulophidae), and Chelonus (Microchelonus) sp. and Pholetesor ornigis (Braconidae). All of the known species are generalist parasitoids of leafminers, barkminers, casebearers, gallformers, or strictly free-feeding insects. Biology of closely related species of the unknown parasitoids sug- gests that they are also generalists. All of the parasitoid species attack Cameraria in larval stages although at least one (P. ornigis) usually emerges from pupae.

Most predation occurs from two sources, the arboreal ant Pseudoinvyrmex apache (Faeth 1990b) and host feeding by adult parasitoids listed above. Other occa- sional predators include both invertebrates (hemipter- ans, dipterans, and hymenopterans) and vertebrates (birds and lizards).



1804 STANLEY H. FAETH Ecology, Vol. 73, No. 5

Manipulation of herbivory levels

To test the hypothesis that folivory affects survival and causes of mortality of the leafminer, Cameraria sp. nov., I manipulated levels of simulated herbivory. Four branches were selected within eight Emory oak trees on the basis of similar number of leaves and similar height and aspect within the canopy. Each branch within the trees randomly received one of four treatments, either 0, 25, 50, or 75% of leaves damaged. Simulated leaf damage was accomplished with a hole- punch. Three or four 5 mm diameter holes were punched on individual leaves until -0, 25, 50, or 75% of the total number of leaves on a branch were damaged. Leaves were artificially damaged between 30 May and 2 June 1988, just after appearance of first-instar CaIlneraria mines and just after most herbivory by leafchewing insects occurs (Faeth 1985). Hole-punching removed - 20% of the leaf area of each leaf. The levels of simulated herbivory are within the range of endemic herbivore levels encountered on Emory oak (Faeth 1985).

It was impossible to control leafchewing damage by endemic arthropods after hole-punching without in- terfering with activity of either leafminers or their natural enemies. All leaves, however, were scored for arthropod and artificial damage to ensure conformity to assigned treatment levels. All abscised leaves from each branch were collected once every 2 wk from beneath trees. Abscised leaves from each treatment were iden- tified by small dots of different colors of latex paint placed near the petiole of mined leaves at the time of simulated damage. Study trees are isolated from other Emory trees at the study site so that abscised, marked leaves can be readily located beneath the trees and are not confused with other treatments from other trees. All remaining leaves were collected from branches in April 1989. A leaf was considered "damaged" if > 5% of leaf area had been consumed by leafchewing arthropods. Relative levels of leaf damage conformed to originally assigned treatments for each block. Final ef- fective treatment levels corresponding to 0, 25, 50, and 75% artificial damage were 18.4 + 5.6% (mean + 1 SD), 44.6 ? 7.4%, 59.5 ? 5.8%, and 75.3 ? 2.4%, respectively.

I used simulated, partial herbivory of individual leaves within branches for several reasons. Herbivory in the form of partial leaf damage is much more common generally in nature (Edwards and Wratten 1983) and specifically on Emory oak (Faeth 1985, 1987) than complete consumption of leaves (defoliation). Partially damaged leaves also purportedly provide chemical and physical cues for searching natural enemies of folivorous insects (Whitman 1988a, Turlings et al. 1990). I used simulated herbivory because previous studies in this system have shown that partial insect and artificial damage of individual leaves of Q. emoryi produce very similar photochemical and phonological changes (Faeth

1986, 1991 a), although these similarities may not hold in other insect-plant systems (Baldwin 1990). Simu- lated herbivory allowed controlled levels of damage. Furthermore, branches were used as experimental units because previous studies (Faeth 1986, 199 la) indicate that phytochemical and phonological changes associated with simulated and insect herbivory are localized within branches in Q. emorYi (i.e., there are no systemic responses). Finally, natural enemies of leafminers in this system (Faeth 1986, 1990b, Faeth and Bultman 1986) and others (e.g., Sugimoto et al. 1988) respond at the branch or leaf level to chemical and physical cues associated with plant damage to locate hosts.

Effects offolivory on Cameraria To test the effects of simulated herbivory on Camer-

aria, all leaves from each branch were returned to the laboratory in April 1989 and all mines were examined to determine larval and pupal survival rates and causes of mortality. Survival is easily determined by the presence of a characteristic emergence hole in the mine and an empty pupal case (Faeth 1986). Leaves with dead leafminers were dissected and causes of mortality cat- egorized as follows: (1) parasitized, i.e., presence of characteristic emergence holes or pupal remnants of parasitoids within mines; (2) preyed upon, i.e., mines torn open and larvae or pupae missing or early instars (1-4) flattened and attached to the floor or roof of the mine (the latter indicates host feeding by adult parasitoids); (3) premature abscission, i.e., desiccated larvae in leaves collected beneath trees before the typical onset of leaf abscission; (4) cannibalism, i.e., dead larvae, especially in early instars (1-4), with ruptured ab- domens in coalesced mines within multiply mined leaves; (5) other causes, i.e., dead, early-instar larvae with no other apparent cause of mortality. This category includes leafminers dying presumably from nutritional causes or secondary phytochemistry, abiotic factors, or attack by microorganisms. Designation of survival and causes of mortality have been standard- ized and reliably used in past studies of Cameraria (Faeth 1986, 1988, 1991 a). Survival and mortality of leafminers in singly and multiply mined leaves were recorded separately. I also determined mean density of leafminers and proportion of multiply mined leaves within each branch by examining all leaves for the presence and numbers of Cameraria (Table 1).

Long-term effects of o/ivor' on Cameraria and other arthropods

To test the long-term effects of folivory on Camer- aria, survival and causes of mortality were determined for leafminers on the same branches after the second growing season (1989-1990). No experimental damage was inflicted in the 2nd yr so only damage from native phytophagous arthropods was present. Cameraria densities were generally much lower on study (Table 1) and nonstudy trees in the second season at Oak Flat,




TABLE 1. Densities of the leaf miner, (ameraria sp. nov., on experimental branches of Quercus einorvi that were subjected to simulated folivorv in 1988-1989 and were untreated in 1989-1990.

Branch 1988-1989 (the treatment year) 1989-1990

treatment Density Ratio* Density Ratio* (% Of leaves (mines/LOG Total no. mult./sing. (mines/LOG Total no. mult./sing.

Tree damaged) leaves) leaves mined lvs. leaves) leaves mined lvs.

1 0 48.4 219 1.29 7.2 838 0.10 25 69.4 284 0.86 8.6 100 0.33 50 36.8 95 0.20 5.0 463 0.06 75 47.8 368 0.75 5.7 420 0.11 0 67.7 248 1.00 10.8 562 0.26

25 33.9 537 0.65 0.1 534 0 50 91.7 192 1.00 4.3 328 0 75 46.5 411 0.49 2.6 765 0.12

3 0 46.2 260 0.72 4.7 1086 0.06 25 26.6 493 0.45 6.6 693 0.18 50 49.3 444 0.53 8.6 567 0.07 75 18.7 630 0.19 3.1 880 0

4 0 15.7 432 0.48 10.3 774 0.53 25 7.6 406 0.17 7.3 593 0.16 50 43.8 210 0.57 5.6 285 0.17 75 20.4 636 0.38 2.0 951 0.23

5 0 57.0 279 0.73 5.9 490 0.50 25 26.7 883 0.29 3.7 893 0.29 50 35.7 911 0.54 1.7 944 0.18 75 46.1 297 1.03 14.3 63 0.14

6 0 106.3 351 0.85 20.0 167 0.18 25 125.4 571 1.68 8.5 692 0.08 50 96.5 311 1.10 8.9 493 0.02 75 56.3 349 0.57 7.4 530 0.26

7 0 69.2 302 1.06 6.6 605 0.06 25 39.8 630 0.90 6.9 980 0.31 50 38.4 232 0.29 6.5 368 0.18 75 74.4 321 0.65 4.3 585 0.10

8 0 41.1 521 1.40 6.9 849 0.06 25 27.8 273 0.32 17.9 385 0.09 50 43.8 664 0.52 5.4 1100 0.08 75 26.7 382 0.28 12.0 474 0.14

* The ratio of multiply mined to singly mined leaves.

so I could only analyze data for survival, attack by natural enemies, and all other causes of mortality. The latter category is pooled mortality from cannibalism, premature leaf abscission, and other causes.

To determine whether colonization by leafminers and damage by leafchewers were affected by different levels of folivory in the previous season, I determined mean densities of leafminers on each branch (Table 1) and the amount of arthropod damage by examining all leaves from each branch.

Effects of to/iv ory on host trees

The effects of past bouts of herbivory on growth and phonology of the host trees in the next season were also tested by determining the percent increase in number of leaves on branches in 1989-1990 relative to the 1988-1989 growing season. Since premature leaf abscission can be an important factor in leafminer survival (e.g., Faeth et al. 1981, Faeth 1986), I tested the hypothesis that herbivory in one season affects the pro- pensity of leaves to abscise in the next season. On 11 January 1990, 25 leaves were selected randomly and

marked on each study branch. The number of marked leaves remaining on each of the branches was determined 4 February and 7 March, and all marked leaves were collected on 31 March 1991 when normal abscission typically begins.

Statistical analyses

I used complete randomized block ANOVA with trees as blocks, damage levels as treatments within blocks and branches as replicates. Number of mines within each leaf (1 or > 1 mine) was used as a nested factor within each branch, except for rate of cannibalism because cannibalism can only occur in multiply mined leaves. Percent survival and percent mortality from various sources (arcsine transformed) were used as separate dependent variables in univariate ANO- VA. In ANOVA involving sources of mortality other than cannibalism, percent mortality on multiply mined leaves was calculated after removing the cannibalized larvae since cannibalism occurs in early instars before other mortality factors act and only in multiply mined leaves. In the ANOVA using percent cannibalism as



1806 STANLEY H. FAETH Ecology. Vol. 73, No. 5

TABLE 2. Univariate analyses of variance of the effects of block (tree), treatment (level of simulated herbivore damage). and number of mines per leaf (1 or > 1 mine per leaf) on rates of survival and causes of mortality (arcsine transformed) of the leaf miner Cameraria on Qwercus emor'i in 1988-1989.

Dependent variable Source of variation ss df MS F P

Survival Block (tree) 0.27 7 0.04 3.89 .002 Treatment 0.02 3 0.01 0.65 .585 Mines per leaf 0.18 1 0.18 18.08 .0001 Error 0.51 52 0.01

Parasitism Block (tree) 0.55 7 0.08 5.11 .001 Treatment 0.06 3 0.02 1.35 .269 Mines per leaf 0.10 1 0.10 6.22 .016 Error 0.81 52 0.02

Predation Block (tree) 0.16 7 0.02 2.04 .067 Treatment 0.04 3 0.01 1.32 .276 Mines per leaf 0.26 1 0.26 23.30 .001 Error 0.57 52 0.01

Natural enemies Block (tree) 0.52 7 0.07 5.67 .001 Treatment 0.01 3 0.00 0.29 .834 Mines per leaf 0.41 1 0.41 31.81 .001 Error 0.68 52 0.01

Cannibalism* Block (tree) 0.20 7 0.03 2.22 .074 Treatment 0.03 3 0.01 0.79 .514 Error 0.27 21 0.01

Abscission Block (tree) 0.31 7 0.04 3.11 .008 mortality Treatment 0.22 3 0.07 5.22 .003

Mines per leaf 0.40 1 0.40 27.89 .001 Error 0.74 52 0.01

Other mortality Block (tree) 0.71 7 0.10 7.51 .001 Treatment 0.11 3 0.04 2.83 .047 Mines per leaf 0.02 1 0.02 1.56 .217 Error 0.70 52 0.01

* The effect of number of mines per leaf was not analyzed for cannibalism, and singly mined leaves were excluded from analyses since cannibalism occurs only in multiply mined leaves.

the dependent variable, only block (tree) and treatment effects were tested and singly mined leaves were excluded. Randomized block design assumes no interaction between blocks (trees) and treatments (levels of simulated folivory). All assumptions of homogeneity of variances and normality were appropriately tested and met.

In the second growing season, percent survival, attack from natural enemies, and other causes of mortality were used as dependent variables in an incom- plete block ANOVA. Four branches were excluded from analysis because there were too few leafminers (<15) to assess percent survival and mortality accurately. The effect of number of mines within leaves on the other 28 branches could not be tested due to a general decline in Caweraria densities (Table 1). Branches were grouped into the same treatment levels as in the previous growing season, although the branches were not damaged experimentally in 1989-1990 since the ob- jective was to test the carry-over effects of herbivory from the previous season. To determine the effect of herbivory in the previous season on colonization by Cameraria and folivory by leafchewing arthropods in the next, I used change in Cameraria densities relative to the first season and amount of leafchewing damage in the second season as separate dependent variables.

I also used percent leaf abscission and percent change in leaf number as dependent variables to assess the effect of folivory in the previous season on growth and phenology in the following season. All percentages were arcsine transformed, and all assumptions of ANOVA were tested and met.

To test the effect of folivory by endemic arthropods in the 1989-1990 season on Carneraria survival and sources of mortality, I regressed endemic levels of leafchewing damage from each branch against survival, rates of natural enemy attack, and other causes of mortality (arcsine transformed) for that branch. The four branches with insufficient numbers of leafminers were excluded from the regressions.

RESULTS

Efkects offolivory on Cameraria Degree of simulated folivory did not significantly

affect overall survival of Cameraria (Table 2; 6.35 ? 2.61% survival at 0% leaf damage, 7.61 + 8.13% survival at 25% leaf damage, 6.01 ? 3.51% survival at 50% leaf damage, and 6.89 ? 3.26% survival at 75% leaf damage [means ? I SE]), although survival rates did vary significantly among trees (Table 2). All factors causing mortality varied among trees (Table 2), but




40 I 35 1988 - 1989

35- 3

0 30

0 25 - VI) C) 20- VI)

15 1 z w 10

w 5- a.- 0

0% 25% 50% 75% PROPORTION OF LEAVES DAMAGED

FIG. 1. Percent mortality of Camneraria larvae from premature abscission of Quercus cinorvi leaves (means plus 1 SE) for the four treatment levels of simulated herbivory in 1988- 1989.

only death resulting from premature abscission and from "other" causes of mortality varied significantly among treatments. Mortality resulting from premature abscission increased (Fig. 1), while death from other causes, including nutritional or secondary chemistry, abiotic factors, or attack by microorganisms decreased (Fig. 2). with increasing levels of simulated folivory. Changes in these mortality factors, however, were not sufficient to alter overall survival (Table 2) perhaps because they compensated for each other.

The degree of simulated folivory did not affect (means + 1 SE in all cases below) hymenopteran parasitoids: 13.56 ? 7.58% parasitism at 0% leaf damage, 18.57 + 8.7/2% parasitism at 255% leaf damage, 1 5.23 ? 8.5 1/% parasitism at 50% leaf damage; 14.43 ? 5.24% at 75% leaf damage; predators: 13.64 ? 7.95% predation at 0% leaf damage, 12.66 ? 4.93 predation at 25% leaf damage, 14.73 ? 6.36% predation at 50% leaf damage, 15.69 ? 4.23% predation at 75% leaf damage; macroscopic natural enemies (i.e., parasitoids plus predators): 27.20 ? 9.75% death from natural enemies at 0% leaf damage, 31.33 ? 9.49% death from natural enemies at 25% leaf damage, 29.96 ? 12.07% death from natural enemies at 50% leaf damage, 30.13 ? 5.28% death from natural enemies at 75% leaf damage; or cannibalism: 19.91 ? 8.4 10% cannibalism at 0% leaf damage. 15.18 ? 8.52% cannibalism at 25% leaf damage. 15.93 ? 5.46% cannibalism at 50% leaf damage, 16.96 ? 7.49% cannibalism at 75% leaf damage.

Survival was significantly lower for leafminers shar- ing leaves than those occupying leaves alone (Table 2, Fig. 3). All categories of mortality except death from other causes were significantly affected by co-occurrence of leafminers on leaves (Table 2, Fig. 3). The decrease in overall survival of co-occurring leafminers relative to those mining alone is caused by cannibalism

and increases in death due to premature leaf abscission, since death from predators and hymenopteran parasitoids is less for larvae in multiply mined leaves than for those mining alone in leaves (Table 2, Fig. 3).

Long-termn efects of folbl ory on Cameraria and other arthropods

There were no significant long-term effects of folivory on Camneraria colonization or performance in the second growing season. Rates of survival varied significantly among trees but not among treatments (Ta- ble 3, treatments performed in the previous year). The two categories of mortality with sufficient numbers to analyze, attack by natural enemies and all other mortality (including mortality from cannibalism, abscission, and other causes), did not vary among either trees or treatments (Table 3). Colonization by Cameraria was not affected by folivory in the previous season. Densities varied among trees, but not among treatments (Table 4). Carneraria densities were generally much lower in 1989-1990 on study trees (Table 1) as well as unmanipulated trees (Faeth 1991 a).

Levels of herbivory by endemic, leafchewing arthropods in 1989-1990 were not related to survival of Cameraria (F = 1.38, df = 1,26, P > .20), rates of attack by natural enemies (F = 0.21, df= 1,26, P > .50), or other causes of mortality (F = 0.64, df = 1,26, P > .50).

Simulated folivory in the previous season did not affect the percentage of leaves damaged by leafchewing arthropods in 1989-1990, although herbivore in 1989- 1990 varied significantly among trees (Table 4).

100 -

90 - 1988 - 1989

80-

Or- 70 - 0 :2 60-

Li 50- T o 40-

Z 30

v

U 20- Of

a_ 10

0% 25% 50% 75%

PROPORTION OF LEAVES DAMAGED FIG. 2. Percent mortality of Cameraria larvae from othc

causes (means plus 1 SE) for the four treatment levels of sirr ulated herbivory of Quercus cinorti leaves in 1988-198' Other causes include mortality from abiotic factors, plain chemistry or physical features, and death by microparasite such as fungi and bacteria.




80 -

1 MINE 1988 1989 70- E > 1 MINE

60-

50-

IL o 40 -

z O30-

LU la_ 20-

10

0 ci ~~~~c/i

FATE OF LEAFMINERS

FIG. 3. Percent survival of Carneraria larvae in Quercus ernorji leaves, and for larvae dying, percent larval mortality from parasitism, predation, natural enemies (parasitism plus predation), premature leaf abscission, cannibalism, and other causes for larvae occurring alone and for those occurring with conspecifics in leaves in 1988-1989 (means plus I SE in all cases). Cannibalism cannot occur in singly mined leaves. All categories of mortality were calculated after removing those dying from cannibalism in early instars.

Effects of folivorv on host trees

In contrast to the effect of folivory on leafminers and leafchewers, past episodes of simulated folivory did marginally reduce the number of leaves in the subse- quent growing season (Table 5, Fig. 4). Simulated folivory in the previous year did not affect rate of premature leaf abscission in the next year (Table 5).

DISCUSSION

My results do not support the idea that interactions among herbivore species via induced chemical or phe-

nological changes are important factors in population dynamics of Cameraria. Simulated folivory did not affect survival of the leafminer, Cameraria sp. nov., in the first growing season, and there is no indication of any relationship between amount of folivory and mean survival. Cameraria survival in the second growing season was also not related to amounts of folivory caused by endemic leafchewing arthropods.

Interspecific competition via alteration of the host plant requires that chemical or physical changes occur in the plant. There is ample evidence for induction ol allelochemicals after herbivory in virtually every plank

TABLE 3. Univariate analyses of variance of the effects of block (tree) and of treatment (level of simulated herbivore damage from the treatment year, 1988-1989, on rates of survival and causes of mortality (arcsine transformed) in the leaf mine Camneraria on Quercus emnorvi, and the amount of leaf damage in the next growing season (1989-1990).


Survival Block (tree) 0.24 7 0.03 3.41 .018 Treatment 0.05 3 0.02 1.82 .181 Error 0.17 17 0.01

Natural enemies Block (tree) 0.31 7 0.04 1.71 .173 Treatment 0.09 3 0.03 1.21 .337 Error 0.45 17 0.03

Other mortality Block (tree) 0.31 7 0.04 1.77 .160 Treatment 0.10 3 0.03 1.28 .312 Error 0.43 17 0.03

* Lower densities of Cameraria in the 1989-1990 growing season prevented statistical analyses of rates of predation ar parasitism separately or separation of mortality from abscission and cannibalism. The former two are joined as "natur enemies" and the latter two are included in "other mortality."




TABLE 4. Univariate analyses of variance of the effects of block (tree) and of treatments (level of simulated herbivore damage) performed in 1988-1989 on relative change in densities of the leaf miner Camneraria on Quercus emorpvi and on the percent of leaf damage (arcsine transformed) by chewing herbivores in the next growing season (1989-1990).


Caweraria densities* Block (tree) 0.51 7 0.07 2.32 .064 Treatment 0.14 3 0.05 1.45 .258 Error 0.66 21 0.03

Leaf damage Block (tree) 0.42 7 0.06 4.22 .005 Treatment 0.01 3 0.00 0.20 .894 Error 0.30 21 0.01

* Relative change in Camneraria density (mines per 100 leaves) was calculated as density on a given branch in 1989-1990 divided by density on the same branch in 1988-1989.

examined (e.g., Barbosa 1988, Schultz 1988, Karban and Myers 1989, Faeth 1991b, Karban 1991), and Emory oak is no exception. Both insect and artificial herbivore produce increases in condensed tannin levels that are sustained for the remainder of the growing season (Faeth 1986, 1987, 1988). Apparently, these changes have no direct negative effect on Cameraria. To the contrary, simulated folivory significantly decreased "other" causes of mortality (Table 2, Fig. 2), the category of mortality that includes death from nutritional deficiencies or allelochemicals. That Camer- aria is not adversely affected by increases in tannin levels is not surprising since Cameraria is a specialist herbivore on Emory oak and likely well adapted to the high tannin content of Emory oak leaves. Indeed, neither oviposition by Cameraria adults nor performance of larval offspring is associated with variation in foliar tannin content (Faeth 1 990a). The question of why mortality in this category is actually reduced for Cam- eraria larvae may be related to attack by microparasites and is discussed below (E~ffcts offolivory on tritrophic interactions).

Morphological and phenological changes also ac- company herbivory, although these changes and their effects on herbivores are not as well studied as phytochemical induction (Haukioja 1980, Tuomi et al. 1989. Faeth 1991 b). Endophagous insects like leafminers and gallformers may be strongly affected by phonological changes because of their sedentary life histories. Caineraria larvae, which require 11 mo to develop, the life-span of Emory oak leaves, may be

particularly susceptible to premature leaf abscission. Phenological and morphological changes, such as premature leaf abscission, have been considered as induced defenses (Williams and Whitham 1986, but see Faeth et al. 1981, Stiling and Simberloff 1989, Faeth 1991b). In this study, simulated folivory did increase death from premature leaf abscission (Fig. 1), but this effect was either not strong enough to decrease overall survival (Table 2) or was offset by decreases in other causes of mortality. It therefore seems unlikely that herbivore-induced changes in either phytochemistry or phonology and morphology of Emory oak affect dynamics of Cameraria populations.

EJ/ects of folivorV on tritrophic interactions

Herbivorous insect species may also compete indirectly via their common natural enemies (Holt 1977, Jeffries and Lawton 1984, Price et al. 1986) if induced responses enhance attack of these natural enemies. Re- cently, some researchers have proposed that plants have evolved to manipulate natural enemies of phytophagous insects through induced responses as another line of defense against herbivores (Price 1986, Niemelk and Tuomi 1987, Whitman 1988a, b, Williams et al. 1988, Dicke et al. 1990, Turlings et al. 1990). This intriguing proposal of induced defense via natural enemies (henceforth, termed IDNE) is supported by evidence that many parasitoids and some predators of phytophagous insects respond to visual (Heinrich and Collins 1983) and olfactory (Flint et al. 1979, Greany and Ha- gen 1981, Aldrich et al. 1985, Barbosa 1988, Whitman

TABLE 5. Univariate analyses of variance of the effects of block (tree) and of treatments (level of simulated herbivore damage) performed in 1988-1989 on percent change in number of leaves in Quercus emoryv and on rate of premature leaf abscission (arcsine transformed) in the next growing season (1989-1990).


Change in number Block (tree) 66 297.90 7 9471.13 1.16 .368 of leaves Treatment 58 006.36 3 19 335.45 2.36 .100

Error 171 906.78 21 8186.04 Premature Block (tree) 0.49 7 0.07 2.11 .088

abscission Treatment 0.11 3 0.04 1.09 .375 Error 0.70 21 0.03




300 -

1988 - 1989

Z 250 - LL.

H 200-

Z 150 -

LI -100

a~ 50-

0 0% 25% 50% 75%

PROPORTION OF LEAVES DAMAGED

FIG. 4. Percent change in number of leaves of Quercus emorvj0' from the treatment year, 1988-1989, to 1989-1990, by treatment levels (means plus 1 SE). Percent change in number of leaves was determined by dividing number of leaves in 1989-1990 by number of leaves in 1988-1989 for each branch.

1988b, Sugimoto et al. 1988, Dicke et al. 1990, Tur- lings et al. 1990, Whitman and Eller 1990) cues pro- duced by herbivore feeding.

I found no evidence that either simulated (1988- 1989) or arthropod (1989-1990) folivory alters attack of Camneraria by macroscopic natural enemies (predators and hymenopteran parasitoids). The failure to detect effects of folivory on the third trophic level is particularly noteworthy because these interactions should be strong. Cameraria has an unusually long larval development time within the leaf (z 11 mo), and larvae are therefore exposed to both the direct and indirect effects of other herbivores for long periods. The major parasitoids and predators of Cameraria are generalists and therefore should respond to nonspecific plant damage (Hawkins 1988, Faeth 1990b). Most of the parasitoids attack the other seven species of leafminers on Emory oak (Faeth 1986), and some attack larvae of Epinotia emarginata (Lepidoptera: Tortrici- dae), a leaftying caterpillar, which is the primary leafchewing herbivore on Emory oak (S. H. Faeth, personal obseri action . The major predator, the arboreal ant Pseudornvrrnex apache, is also a generalist that feeds upon a wide variety of leafchewing species. Other invertebrate and vertebrate predators are also probably generalists. More importantly, previous studies have shown that natural enemies of Cameraria respond to both localized chemical (Faeth and Bultman 1986) and structural changes (Faeth 1990b) associated with leaf damage. Thus, the requisite conditions are present for competition among leafminers and leafchewers via the effects of induced responses on mutual natural enemies.

Direct support of the IDNE hypothesis requires that induced chemical or physical changes and their effect on the natural enemy complex are translated into dis-

cernible effects on population dynamics of the phytophagous insect species. The latter criterion has been rarely tested. In the few tests to date, support for the IDNE hypothesis appears sparse. Fowler and Mac- Garvin (1986) showed that artificial damage to birch leaves caused increases in mortality and decreases in body size of geometrid larvae but no increases in attack by parasites. Bergelson et al. (1986) and Bergelson and Lawton (1988) found that artificial leaf damage increased movement of casebearing larvae on birch trees, but increased movement did not render larvae more susceptible to predation. West (1985) and Hawkins (1988) showed that leaf damage did not increase parasitism of leafminers on oak. Here, the effects of plant- mediated changes in attack by natural enemies are not detectable for this Cameraria population. Convincing support for the IDNE hypothesis remains elusive.

Evolution of plants to manipulate the third trophic level, although an exciting idea, may be unlikely in most plant-insect-natural enemy systems. Williams et al. (1988) concluded that conflicting selective pressures may prevent plants from evolving chemical sub- stances that simultaneously deter or reduce growth and survival of herbivores, the second trophic level, and attract beneficial insects, the third trophic level, without increasing toxicity of their prey or hosts. Similar conflicting pressures may also exist when one considers only the third trophic level. For example, chemical and physical changes induced by herbivory on Emory oak attract macroparasites (wasps) but inhibit growth of microparasites (bacteria and fungi) of Cameraria (Faeth and Bultman 1986). The latter is indicated in the present study. Increasing levels of simulated leaf damage decreased mortality from "other" causes (Fig. 2), which includes attack from microparasites. Such conflicting selective pressures relative to the third trophic level, coupled with overriding influences of intraspecific competition and other biotic and abiotic factors on population dynamics of herbivores may reduce the probability of coevolutionary links between the plants and natural enemies of herbivores via induced responses (Faeth 1988, 199 lb). Accumulating evidence indicates that natural enemies have evolved to use cues associated with herbivory to locate insect hosts, but presently there is little evidence to suggest that plants either benefit from this interaction or have evolved to exploit it.

Interspecific vs. intraspecific competition By far, the most important factor affecting survival

and causes of mortality was whether or not larvae co- occur with other larvae on a leaf (Table 2, Fig. 3). Survival and every category of mortality except mortality from other causes were affected significantly by the presence of co-occurring leafminers (Fig. 3). The decrease in survival of co-occurring larvae was related to an increase in death from premature leaf abscission and the presence of intraspecific aggression, notably



October 1992 INSECT COMPETITION VIA PLANT RESPONSES 181 1

cannibalism (in singly mined leaves, there is obviously no possibility of intraspecific aggression). These two mortality factors outweighed any other benefit of co- occurring with other larvae in a leaf; rates of parasitism, predation, and unknown causes of mortality were all significantly less for larvae co-occurring in leaves com- pared to singly mining larvae (Table 2, Fig. 3). Clearly, intraspecific interactions are potent mortality factors for Cameraria larvae And pupae.

Intraspecific competition, directly through aggression and indirectly through premature leaf abscission, likely obscures any effect of interspecific interactions via the host plant and natural enemies. In general, intraspecific competition tends to be stronger than direct interspecific competition in most studies of competition in phytophagous insects (e.g., Stiling 1980, Connell 1983, Strong et al. 1984). However, indirect interactions via induced changes and natural enemies were envisioned as a novel, and a potentially powerful, way that insects species might compete interspecifically (Holt 1977, Schultz 1983, Faeth 1987, Barbosa and Letourneau 1988). At least in the Cameraria-Emory oak-natural enemy system, interspecific competition, even at intense levels (i.e., >75 /% of leaves damaged), does not appear to be important relative to intraspecific competition. In previous studies of Cameraria where indirect effects of herbivory via changes in attack by natural enemies were shown to be important (Faeth and Bultman 1986, Faeth 1990a), only singly mined leaves were considered, and therefore the relative effects of interspecific and intraspecific competition could not be evaluated.

Long-term c#ffects of folivorv on insects

Delayed chemical or phonological changes in peren- nial plants may function as plant defenses against herbivores in the next growing season (Haukioja 1980, Neuvonen et al. 1987, Myers 1988, Tuomi et al. 1989, Bryant et al. 1991). Similarly, the effects of one herbivore species on others via these induced responses might be delayed until the next growing season. For Emory oak, folivory affects neither colonization by Cameraria nor folivory by other arthropod folivores in the next growing season (Table 4). Further, simulated folivory levels did not affect survival of Camer- aria in the next season or attack by their natural enemies. Folivory in the previous season did, however, reduce tree growth in the next, at least in terms of leaf production (Fig. 4). Emory oak trees clearly do not benefit from folivore-induced responses in either the current season or the next one. Reduction of herbivory is a prerequisite in order to consider induced responses as "defensive" (Schultz 1988). It is therefore unlikely that induced changes in allelochemistry, phenology, or morphology of Q. emorvi are evolved defenses against current or future herbivores, at least within the limits of this study.

ACKNOWLEDGMENTS

I thank Peiling Cheng, Cody Faeth, Carmen Febus, Kyle Hammon, Aneezah Nabee, Suzanne Reeser, and Jeannie Sim- mons for assistance in the field or lab. Mike Auerbach, Laurel Fox, Erkki Haukioja, Rick Karban, Susan Mopper, Dave Pearson, Peter Price, Lisa Schmoetzer, and Peter Stiling made helpful comments on the manuscript. This research was supported by NSF grant BSR 8717543.

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Interspecific and Intraspecific Interactions Via Plant Responses to Folivory: An Experimental Field Test