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0 Department of Biology, Dartmouth College, Hanover, New Hampshire 03755 USA
Received for publication September 1, 1999. Accepted for publication February 11, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Borneo • delayed greening • Dipterocarpaceae • Gunung Palung National Park • Indonesia • immature leaves • premature leaf loss • Shorea hopeifolia • tropical rain forest tree
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Damaged leaves are often shed more rapidly than undamaged ones and, for many plant species, the rate of abscission increases with the area damaged (Table 1). Thus, premature abscission of damaged leaves can increase the degree of defoliation beyond that imposed directly by herbivores. Severe defoliation can decrease plant growth and ultimately decrease plant fitness (Lowman, 1982
; Becker, 1983
; Crawley, 1983
; Krischik and Denno, 1983
; Wright, Hall, and Peacock, 1989
).
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; Coley and Barone, 1996
). Furthermore, some models (Kikuzawa, 1991, 1995
) suggest that abscission following damage should be more likely for immature than for mature leaves, because immature leaves require future investment in carbohydrates and nitrogen. If abscission is especially sensitive to damage for immature leaves, then existing studies that focus on mature leaves only (Table 1) may underestimate the overall effect of herbivory on plants.
However, any tendency to abscise damaged immature leaves may depend on species' life history traits. Juveniles of fast-growing tropical pioneer species, found primarily in gaps, invest in photosynthates high in nitrogen early in leaf development, whereas shade-tolerant persistent species tend to delay provisioning until expansion is nearly complete ("delayed greening"; Coley and Barone, 1996
). Thus, early greening species may be less likely than delayed greening species to abscise leaves that are damaged during the expansion phase (J. Barone, Smithsonian Tropical Research Institute, personal communication).
Shade-tolerant seedlings form a "seedling bank" of individuals growing slowly in the low-light conditions of the understory (Connell, 1989
); most of these species are delayed greeners (Kursar and Coley, 1991
). Loss of leaves can increase the risk of mortality for juveniles in the shaded understory (Clark and Clark, 1985
). We tested the effects of leaf age on abscission after herbivore damage in an abundant, shade-tolerant, delayed-greening species, Shorea hopeifolia (Heim.) Sym, a member of the species-rich family Dipterocarpaceae, which dominates much of the Southeast Asian rain forest canopy (Whitmore, 1984
) and accounts for >95% of Indonesia's timber production (Ashton, 1988
). We compared the effects of partial tissue loss on abscission, between mature and immature leaves, on seedlings in the understory.
We addressed the following questions: (1) How much tissue is removed by herbivores from the youngest leaf of S. hopeifolia seedlings under natural conditions? (2) For artificially damaged leaves, how does the probability of abscission depend on the proportion of leaf tissue removed? (3) For a given proportion of leaf tissue removed, how does the probability of abscission depend on the stage of leaf development?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), on sandstone-derived soils in the lowlands of the Cabang Panti Research Station, Gunung Palung National Park (1.13° S, 110.7° E), in Kalimantan Barat (Indonesian West Borneo). At Cabang Panti, dipterocarps comprise >80% of stems 
30 cm diameter at breast height (dbh; C. Cannon, Duke University, and M. Leighton, Harvard University, unpublished data). Most dipterocarp species produce fruit during "masts," at irregular, supra-annual intervals cued by weather patterns associated with El Niño and La Niña events (Ashton, Givnish, and Appanah, 1988
; Yasuda et al., 1999
; mean mast interval for West Borneo 
4 yr [Curran, 1994
]). Their wind-dispersed seeds produce concentrations of seedlings near parents (Appanah and Rasol, 1995
; Itoh et al., 1995
). We chose a species, S. hopeifolia, that is the third most abundant tree species at the study site (mean density of adults = 2.3 individuals/ha; Curran, 1994
), and has been the subject of related studies on the spatial pattern of seedlings, herbivory, and juvenile plant condition (Blundell and Peart, 1998
).
At the time of this study, S. hopeifolia seedlings (
25 cm tall) were at least 3 yr old and no longer reliant on maternal reserves from the seed. Like most canopy species, Dipterocarpaceae seedlings typically occur in the extremely low light of the rain forest understory. Growing slowly, seedlings may remain suppressed for decades before a canopy gap opens (Brown and Whitmore, 1992
). During this period, they experience repeated bouts of herbivory, which may have little effect on the already negligible growth of the seedlings, but may reduce plant survival (Blundell, 1999
).
The study site is aseasonal (mean annual rainfall of 4.5 m), and herbivory and leaf production are continuous throughout the year (A. Blundell, Dartmouth College, personal observation). Most herbivory on S. hopeifolia was caused by caterpillars and grasshoppers. Leaf rollers, gall-forming insects, leaf miners, and mammalian herbivores were also present, but were the main cause of damage on <5% of juveniles. Further, we found no evidence of pathogens causing leaf or juvenile mortality (Blundell, 1999
).
Measurement of naturally occurring herbivore damage
We measured the amount of partial tissue loss caused by herbivores that had accumulated on the youngest mature leaf of 270 S. hopeifolia seedlings. We used the youngest leaf because differences in retention time for individual leaves (Kikuzawa, 1995
) suggest that older leaves may be less comparable in age than the youngest. Seedlings were located around five focal adults (>75 cm dbh), randomly chosen except that adults had no conspecific reproductive trees within 40 m (Blundell and Peart, 1998
). We divided the area around each adult into four 90° sectors, and randomly placed one transect within each sector. On each transect, we placed a 10-m2 plot at each of three distances (5, 15, and 35 m), and sampled the five seedlings closest to each plot center. On each seedling, at each leaf node, we determined whether a leaf was present or absent (i.e., whether the leaf had abscised). If a mature leaf was present on the youngest node, we visually estimated the percentage of tissue lost to herbivory.
Prior to data collection, visual estimates were calibrated to more precise measurements made from leaf tracings on graph paper. Estimates of leaf tissue loss were consistently within ±2% of measured levels when the partial leaf loss was <20%, and within ±5% when >20% of the leaf was missing. For consistency, all estimates were made by AGB. In addition, a random subsample of 60 leaves was taken during data collection, and percentage tissue loss measured using graph paper to check for accuracy. Estimates were closely correlated (r2 = 0.95) with measured values.
Simulated herbivory: partial leaf loss and premature abscission
Developmental stages
To test whether the effects of tissue removal on abscission depend on leaf development, we compared the abscission rates of leaves in five successive stages: (1) bud (leaf furled and enclosed in stipules); (2) expanding (unfurled, but less than full size); (3) red (fully expanded, but with red pigments not yet masked by chlorophyll); (4) green (fully expanded, the color of mature leaves, but not yet toughened); and, (5) mature (lignified). Leaves in the first four categories will be referred to collectively as immature.
We conducted two field experiments. In the first, we compared the abscission rates of artificially damaged mature leaves to those of similarly damaged immature leaves (categories 1–4 above, combined), over a 9-wk period. Then, because we found an unexpectedly large difference in the rate of abscission between immature and mature leaves, a second experiment was conducted, concurrently with the final 4 wk of experiment 1, to examine in more detail the relation between leaf development and abscission. In each experiment, we used seedlings near a conspecific "focal" adult that due to localized wind dispersal of seeds, were likely to be siblings. This approach thus minimized variance in genetic and habitat differences among seedlings within an experiment. While progeny of different adults could plausibly differ in their responses, the emphasis in these artificial herbivory experiments was on the differences in response among treatments within an experiment.
Experiment 1
We tagged 314 S. hopeifolia seedlings in five transects (1 x 30 m) on random azimuths from a single conspecific adult. These fell into two groups—those on which the youngest leaf was mature, and those on which it was immature (categories 1–4, above). From each group, seedlings were randomly chosen for artificial herbivory treatments, in which part of the foliage was removed from the youngest leaf. The remaining seedlings served as controls in each group. From mature leaves, we removed either 25% of the tissue (N = 48 seedlings), 50% (N = 50), or 75% (N = 49), to simulate a wide range of herbivore damage levels. From immature leaves, we removed 50% of leaf tissue (N = 48 seedlings). Using chi-square tests, abscission rates on treated plants were compared to those on controls (N = 50 seedlings for mature and N = 69 seedlings for immature leaves).
Herbivory was simulated by cutting leaves with scissors, in two ways. One-half of the seedlings in each treatment were randomly selected and the appropriate proportion of the leaf was removed at the distal end using a transverse cut, severing the mid-rib. For the other half of the seedling sample, tissue was removed from both sides of the leaf, with a longitudinal cut parallel to the midrib. Control leaves were handled similarly to those in the treatments, except that they were not cut. Because there was no significant difference in abscission rate between transverse (6% shed) and longitudinal cuts (3% shed; 
2 = 1.27, P = 0.26), leaves within a treatment were pooled over cutting methods in the analyses presented below.
The fate of each leaf was checked after 2, 4, and 9 wk, except for control immature leaves, which were followed for 2 wk only (after 2 wk, most control immature leaves had developed into mature leaves).
Experiment 2
To obtain a sufficient sample of seedlings with immature leaves, this experiment was located around a second focal S. hopeifolia adult, 150 m from that used in experiment 1. Seedlings were selected as in experiment 1. We removed 50% of the tissue from randomly selected seedlings whose youngest leaf was in one of the following developmental stages: bud (N = 26 seedlings); expanding (N = 42); red (N = 31); or green (N = 24). We recorded leaf abscission after 1 mo and compared leaf abscission using a chi-square test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 46.53, N = 117, df = 1, P < 0.0001; Fig. 3). Furthermore, after 2 wk a greater proportion of control mature leaves remained than control immature leaves (100 vs. 84%; chi-square: 2 = 8.78, N = 119, P = 0.003; Fig. 3). Finally, after 9 wk, mature leaves missing 50% of their tissue were approximately four times more likely to survive than similarly damaged immature leaves (93 vs. 25%; chi-square: 2 = 55.07, N = 98, df = 1, P < 0.001; Fig. 3).
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2 = 83.47, N = 123, df = 3, P < 0.001; Fig. 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), so we cannot conclude that herbivore damage has no effect on abscission in nature. However, the experimental results show clearly that there is a brief window of time during leaf expansion when abscission is highly responsive to partial tissue loss. Herbivore damage to expanding leaves, and consequent high abscission rates, may explain why the most recently produced leaf was missing from 49% of S. hopeifolia seedlings in the field.
There are several plausible factors that may favor abscission of damaged, expanding leaves. The abscission of immature leaves may be inevitable if damage removes differentiating cells required for development (Coleman and Leonard, 1995
). Damage may cause high water loss (Ostlie and Pedigo, 1984
). Immature leaves also lack lignin, an important defense against pathogens (van Loon, 1993
), and thus may be vulnerable to infection. Abscission may be triggered directly by infection, or plants may have been subject to selection for early abscission of damaged leaves, reducing infection risk. The plant may actually gain more carbon by cutting its losses and flushing a new leaf rather than retaining and expanding a damaged leaf (Harper, 1989
).
Nevertheless, there is evidence that the loss of young leaves may detract from plant growth and/or reproduction more than the loss of older leaves, at least for some temperate trees (O'Neil, 1962
; Kulman, 1965
), a tropical palm (Mendoza, Piñero, and Sarukhán 1987
), and some agricultural crops (Sackston, 1959
; Stickler and Pauli, 1961
; Krisckik and Denno, 1983
; Jurik and Chabot, 1986
; Brown, Cooper, and Blaser, 1966
). Young leaves have a higher expected lifetime photosynthetic contribution (Mooney and Gulmon, 1982
; Harper, 1989
), while older leaves have lower nitrogen concentration, stomatal conductance, and photosynthetic capacity (Aide, 1993
). Furthermore, the capacity for leaf initiation may be limited (Spurr and Barnes, 1980
), restricting the replacement of prematurely abscised leaves, even though their abscission represents less of an investment loss than abscission of fully expanded, lignified leaves (Harper, 1989
; Kikuzawa, 1991, 1995
).
Thus our major finding, that premature abscission can be triggered by tissue loss from expanding leaves, may explain the large number of new leaves missing from S. hopeifolia seedlings and may have strong implications for the photosynthetic capacities of whole plants. However, the capacities of plants to replace early leaf loss, and the impact of losses on plant fitness, need further investigation; S. hopeifolia is apparently the only species for which abscission of immature leaves has been studied to date. The short duration of the leaf expansion phase and the potentially high rate of loss make precise observations difficult, especially under natural conditions. These considerations point to the use of experimental methods (exclosures, enclosures, insecticide treatments, simulated and real herbivory). Studies of leaf demography over entire plants in an experimental setting are needed to clarify both the patterns of leaf demography and the ecological impact of herbivores on growth and survival.
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FOOTNOTES |
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2 Current address: National Center for Environmental Assessment, American Association for the Advancement of Science—Science and Engineering Fellow, U.S. Environmental Protection Agency, 1200 Pennsylvania Ave., NW Mail Stop 8601 D, Washington, D.C. 20460 USA.
3 Author for reprint requests (e-mail: art.blundell{at}alum.dartmouth.org
, Fax: 202-565-0059)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
) were retained than undamaged immature leaves (•; 
) remained than equally damaged immature leaves (
; 