Journal of Ecology 2014, 102, 873–881
doi: 10.1111/1365-2745.12252
SPECIAL FEATURE – STANDARD PAPER
META-ANALYSIS IN PLANT ECOLOGY
Effects of herbivory on leaf life span in woody plants:
a meta-analysis
Elena L. Zvereva* and Mikhail V. Kozlov
Department of Biology, Section of Ecology, University of Turku, 20014 Turku, Finland
Summary
1. Premature abscission of leaves damaged by herbivores can increase the degree of defoliation
beyond that imposed directly by insect feeding. Our aim was to explore the general patterns and
sources of variation in the effects of insect herbivory on leaf life span in woody plants.
2. Meta-analysis of published data demonstrated that herbivory significantly reduced the life span of
damaged leaves; insect feeding had a greater effect than the same level of herbivory simulated by
mechanical wounding. The effects of both natural and simulated herbivory became stronger with
increase in the proportion of damaged leaf area. Damage to young leaves and to plant species with
higher specific leaf area resulted in a greater reduction in leaf life span than damage to mature
leaves and to species with lower specific leaf area.
3. Herbivores differed in the magnitude of their effects on leaf life span, but this variation was not
explained by herbivore feeding guilds or specialization.
4. Natural herbivory similarly reduced leaf life span in deciduous and evergreen trees, thereby questioning the hypothesis that premature abscission as a defence response is primarily a characteristic
of evergreen trees. However, simulated herbivory imposed stronger effects on evergreens, suggesting
that they are more sensitive to non-specific wound-induced elicitors than deciduous trees.
5. Synthesis. We demonstrated that, in spite of pronounced variation between study systems, herbivory in general reduces the life span of the damaged leaves of woody plants. Our results suggest that
variability in plant responses to herbivory may be linked with the leaf economic spectrum. Premature abscission of damaged leaves can be seen as a tolerance strategy that reduces the negative consequences of local damage on the whole plant. This phenomenon should be accounted for in
estimation of losses of net primary production caused by herbivory.
Key-words: abscission, insect herbivores, leaf age, plant traits, plant–herbivore interactions,
research bias, simulated herbivory, timing of damage, tolerance
Introduction
Studies addressing the effects of herbivores on plant communities have generally focused on the removed plant biomass
(Cyr & Pace 1993; Schowalter & Lowman 1999). However,
in addition to direct consumption of foliar tissues or photosynthates, insect feeding selectively impairs the remaining leaf
tissue by altering leaf physiology, including the suppression
of photosynthesis (Nabity, Zavala & DeLucia 2009). Some of
these changes may lead to premature abscission of damaged
leaves, which increases the degree of defoliation beyond that
imposed directly by insect feeding (Blundell & Peart 2000).
In some ecosystems, the loss of plant material via the
*Correspondence author. E-mail: elezve@utu.fi
premature abscission of insect-damaged leaves is greater, or
at least equal, to the leaf biomass consumed by insect herbivores (Burrows 2003; Mazıa et al. 2012). Therefore, losses
from herbivore-induced abscission need to be accounted for
to correctly estimate the effects of herbivory on plant communities. Furthermore, premature leaf abscission, by modifying
nutrient cycles, may have important consequences for ecosystem functioning (Risley 1993; Hunter 2001).
Although the phenomenon of premature abscission of damaged leaves has been recognized for decades, the number of
case studies reporting quantitative data is surprisingly low
(see Appendices S1–S2 in Supporting Information). Furthermore, most of the studies tested the hypothesis that damaged
leaves abscise earlier than intact leaves, whereas the actual
reduction in leaf life span has been measured only rarely. Thus,
although the existence of the effect has been demonstrated in a
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society
874 E. L. Zvereva & M. V. Kozlov
number of studies, its magnitude and potential consequences
for plant fitness remain poorly documented. Furthermore,
almost half of the data on the effects of herbivory on leaf
abscission were obtained from experiments involving mechanically damaged leaves. Plant responses to damage, particularly
growth and defensive responses, can greatly differ between natural herbivory and mechanical wounding (Baldwin 1990; Koo
& Howe 2009; Zvereva & Kozlov 2012), but the direct comparison of the effects of simulated and natural herbivory on leaf
life span has been performed only once (Kozlov & Zvereva
2014). Therefore, the extent to which the impacts of mechanical
damage on leaf life span mimic the impacts of natural herbivory
is unclear.
Other sources of variation in the effects of herbivory on
leaf life span have not been explored either, although several
hypotheses have been proposed. In particular, these effects
were hypothesized to depend on plant life-history traits (Blundell & Peart 2000; Burrows 2003), with the principal difference existing between evergreen and deciduous species
(Bultman & Faeth 1986; Karban & Baldwin 1997). Several
case studies demonstrated the importance of the timing of
damage (Pritchard & James 1984) and of co-occurring abiotic
stressors, for example drought (Abbott et al. 1993; Stone &
Bacon 1994), as well as the dependence of the effect on the
intensity of the damage (Blundell & Peart 2000); however,
the generality of these patterns remains unknown.
Another gap in our current knowledge concerns the effects
of herbivory on needle/scale abscission in conifers. Several
publications that reported premature foliar abscission in gymnosperms either did not provide quantitative data (Silver
1957; Habermann 2000) or did not discriminate between different causes of abscission (Chapman et al. 2003). Considering the ecological and economical importance of conifers, this
research bias requires urgent attention.
Finally, earlier studies addressing the consequences of natural herbivory for leaf life span usually described the effects of
the single herbivore species (or the single feeding guild) and
did not compare different herbivore guilds (but see Kozlov &
Zvereva 2014). However, several studies demonstrated dissimilar impacts of insects from different feeding guilds on
photosynthesis and growth of plants (Welter 1989; Zvereva,
Lanta & Kozlov 2010), and therefore, their differential effects
on leaf abscission are likely.
The aim of the present work was to explore the general
patterns and sources of variation in the effects of leaf damage
on leaf life span in woody plants. We used a meta-analysis
summarizing the published research findings to test the following hypotheses: (i) both natural and simulated insect herbivory causes premature abscission of damaged leaves, (ii)
natural herbivory has stronger effects on leaf life span than
simulated herbivory, (iii) the effect of herbivory on leaf life
span is stronger in evergreen plants than in deciduous plants,
(iv) the effect of herbivory on leaf life span differs among
insect feeding guilds, (v) the effect of herbivory on leaf life
span depends on plant and leaf traits and the timing of the
damage, and (vi) the effect of herbivory on leaf life span
depends on the damaged leaf area.
Materials and methods
DATA COLLECTION
To be included in our meta-analysis, a study had to fit the following
criteria:
1. Changes in the life span of woody plant leaves were measured at
a leaf-specific or plant-specific level in terms of: (i) life span (or
the date of abscission) of damaged vs. undamaged leaves; (ii)
proportions of damaged vs. undamaged leaves abscised/retained
on a tree by a certain date; or c) difference in herbivore damage
between abscised and retained leaves;
2. Localized damage was imposed by either insect feeding (in terms
of leaf area removed, mined or transformed to a gall; feeding by
sucking insects that did not result in the formation of galls was
not considered) or herbivory simulated by mechanical wounding;
3. Damage was imposed to the leaf lamina (i.e. petiole damage was
not considered); and
4. Means, variances and sample sizes or numbers (percentages) were
reported for damaged and undamaged leaves or could be obtained
from the authors, or it was possible to estimate missing data from
the test statistics.
We searched for publications that met these criteria in the ISI Web
of Science data base and Google Scholar using several keywords
(‘abscission’, ‘leaf longevity’, ‘leaf life span’ or ‘shedding’ in combination with ‘herbivor*’, ‘insect’ or ‘damag*’) and further examined
the reference lists of the identified papers. The search was completed
on 15 October 2012.
DATA SELECTION, RESPONSE VARIABLES
AND CLASSIFICATORY VARIABLES
As a rule, we extracted the means, variances and sample sizes (or numbers/percentages of damaged vs. undamaged leaves) from the publications or obtained these data from the authors directly (one study: Mazıa
et al. 2012). For several publications, we approximated the variances of
the control and treatment groups using the reported means, sample sizes
and test statistics, as described by Zvereva, Lanta & Kozlov (2010). For
studies that reported the temporal dynamics of leaf fall (i.e. numbers or
proportions of leaves abscised by several sequential dates), we calculated the average date of leaf fall for damaged and intact leaves. The
authors of several studies did not provide information on the proportions of leaf tissue removed/damaged by each treatment or herbivore
(Appendix S1). For six of these studies, we were able to recover this
information from the leaf area and/or the mine size of a certain species.
Herbivores were classified by feeding guild (defoliators, miners
and gallers) and by the level of specialization to their host plants
(high: feed on plants from one genus; low: feed on plants from two
or more genera); these moderator variables were independent from
each other (v2 = 4.13, df = 2, P = 0.13). The studies that reported
effects caused by groups of herbivores (e.g., by all miners or all defoliators) were excluded from the latter analysis. The levels of damage
(proportion of damaged leaf area) were divided into three groups: low
(<10%), moderate (11–49%) and high (>50%). Plants were classified
by life-form (evergreen or deciduous), growth rate (slow, moderate or
high), shade tolerance (tolerant, moderate or intolerant), ontogenetic
stage (mature, i.e. reproductive age, or young) and by leaf traits (type,
size, longevity and specific leaf area, SLA). Leaves were classified as
simple and compound and divided into 3 groups by maximum leaf
length: small (<7 cm), medium (7–20 cm) and large (>20 cm) and
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 873–881
Herbivory and leaf life span in woody plants 875
into two groups by SLA: low (<10 mm2 mg 1) and high
(>10 mm2 mg 1). Species-specific data on leaf traits were extracted
either from original studies or from various publications. However,
data for some plant species were unavailable, which resulted in smaller sample sizes in some of analyses. In particular, leaf longevity for
deciduous plants is reported only rarely, and therefore, our analysis of
this source of variation was conducted for evergreens only.
All plant characteristics used as moderators in our meta-analysis
varied among the investigated species of woody plants independently
from each other (P > 0.05), with the exception of SLA which was
lower in evergreen plants than in deciduous plants (v2 = 11.8,
d.f. = 1, P = 0.0006). Therefore, we searched for the effect of SLA
on leaf life span separately within evergreen and deciduous species.
Hedge’s d, a measure of effect size (ES), was calculated as the difference between the mean values of (i) leaf life spans or dates of leaf
fall of damaged and intact leaves, (ii) the proportions of damaged and
intact leaves retained on a plant or abscised or (iii) the levels of damage in leaves collected from a plant and from the ground under the
plant, divided by the pooled standard deviation and weighted by the
sample size. A negative ES indicated that damaged leaves abscised
earlier than intact leaves.
When the results were reported as numbers (or percentages) of intact
and damaged leaves abscised by a certain date, and no estimates of variation among trees were provided (or if there was a single tree under
study), we calculated the ESs as odd ratios using MetaWin 2.0 (Rosenberg, Adams & Gurevitch 2000) and converted the odds ratios to
Hedge’s d using an Excel spreadsheet (available at www.stat-help.com/
spreadsheets.html) based on formulas from Borenstein et al. (2009).
The mean ESs were computed and compared using the MetaWin
2.0 program. The herbivory was considered to have a statistically significant effect if the 95% confidence interval (CI) of the mean ES did
not include zero. All analyses (both categorical and continuous, i.e.
meta-regression) were performed using random effects models,
assuming that the studies differed not only by sampling error but also
by a random component of the ES. The variation in the ESs within
and among the classes of categorical variables was explored by calculating the heterogeneity indices (QT and QB, respectively) and testing
these against the chi-square distribution. The temporal changes in
effect size were searched for by calculating Pearson correlation
between the ES and the year of publication.
We tested for publication bias using the funnel plot method: in the
absence of bias, effect size should not correlate with sample size. The
studies for which the ESs have been calculated as odd ratios were
excluded from this analysis. We also calculated the Rosenthal’s failsafe numbers (nfs) to check how robust our conclusions were against
the non-published results. Finally, we checked our meta-analysis
against the quality criteria coined by Koricheva and Gurevitch (2014).
Importantly, we did not find any published data on conifers that
were suitable for meta-analysis and therefore had to use the
results of a specifically arranged field study of Norway spruce
and Scots pine (Appendix S3); the remaining 22 evergreen species included in our data base were broadleaved.
VARIATIONS RELATED TO METHODOLOGY
AND THE LEVEL OF DAMAGE
The overall effect of herbivory on leaf life span was negative
(d = 0.84, CI = 0.96 to 0.71) and highly heterogeneous
(QT = 290.6, d.f. = 144, P < 0.0001). This heterogeneity was
not related to the diversity of indices used to measure the
effect: we found no differences between studies that compared life span of damaged and intact leaves, percentages of
retained/abscised leaves, and differences in herbivory between
retained and abscised leaves (QB = 5.33, d.f. = 2, P = 0.07).
Papers reporting leaf-specific and plant-specific levels of damage also did not differ in the magnitude of the effects
(QB = 2.02, d.f. = 1, P = 0.15). All of these studies were
therefore combined for subsequent analyses.
The authors of 20 of 42 publications compared between 2
and 7 different treatments (median value = 3) to the same
control. However, the random removal of non-independent
ESs did not change our estimate of the overall effect of herbivory on leaf life span (d = 0.86, CI = 1.00 to 0.73).
Similarly, exclusion of data on oaks, which were overrepresented in the data base, did not change the mean ES value
(d = 0.85, CI = 0.99 to 0.71).
The negative impact of both simulated and natural herbivory varied between low, moderate and high levels of damage
(natural herbivory: QB = 15.7, d.f. = 2, P = 0.0004; simulated herbivory: QB = 22.1, d.f. = 2, P < 0.0001). Natural
herbivory had a stronger effect on leaf life span than simulated herbivory at all levels of damage (Fig. 1). Low (<10%)
levels of simulated herbivory did not have a statistically significant effect on leaf life span (Fig. 1).
Studies of a single herbivore species yielded greater reduction in leaf life span than studies considering the effects of a
multiple-herbivore community (d = 1.11, CI = 1.31 to
0.91 and d = 0.61, CI = 0.90 to 0.32 respectively,
QB = 8.42, d.f. = 1, P = 0.004).
VARIATIONS RELATED TO HERBIVORES
Results
DATA BASE
A total of 145 ESs were calculated from 42 papers (Appendices
S1–S2) and from 1 unpublished study (Appendix S3). The magnitude of the reported effects did not change with publication year
(r = 0.03, n = 26 years, P = 0.88). Experiments simulating
herbivore damage yielded 66 ESs, whereas the remaining 79 ESs
reflected effects imposed by insect herbivores, among which 43
ESs were calculated for mining insects. These effects were studied in 47 species of woody plants, among which oaks (Quercus
spp.) were the best represented (11 species, 21 ESs).
The effects of damage on leaf life span varied among herbivore species (those for which we obtained at least two ESs:
QB = 39.2, d.f. = 16, P = 0.001), but this variation was not
explained by herbivore feeding guilds or the level of herbivore specialization (Fig. 2). Galling aphids and gall midges
did not differ in their effects on leaf life span (QB = 1.05,
d.f. = 1, P = 0.31).
VARIATIONS RELATED TO PLANTS
Herbivory caused a greater decrease in leaf life span in evergreen trees than in deciduous trees (Fig. 3). However, these
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 873–881
876 E. L. Zvereva & M. V. Kozlov
Fig. 1. Effects (mean Hedges’ d effect sizes) of natural (Nat) and
simulated (Sim) herbivory on leaf life span of woody plants at three
levels of damage (low, <10%; moderate, 11–49%; high, >50% of the
leaf area). Horizontal lines denote 95% confidence intervals; sample
sizes are shown in brackets. The effect is significant if the 95% confidence interval does not include zero. Significant (P < 0.05) QB values
indicate between-group heterogeneity.
Fig. 3. Effects (mean Hedges’ d effect sizes) of natural and simulated
herbivory on leaf life span of evergreen (eve) and deciduous (dec)
plants. For explanations, see Fig. 1.
Fig. 2. Effects (mean Hedges’ d effect sizes) of damage by different
groups of herbivores on leaf life span of woody plants. For explanations, see Fig. 1.
Fig. 4. Variation in the effects (mean Hedges’ d effect sizes) of herbivory on leaf life span of woody plants related to plant characteristics. Variation related to plant and leaf age refers to pooled data
including both natural and simulated herbivory, while variation
related to leaf size (small, <7 cm; medium, 7–20 cm; large, >20 cm)
and specific leaf area (low, <10 mm2 mg 1; high, >10 mm2 mg 1)
refers to natural herbivory only. For explanations, see Fig. 1.
differences were due to significantly stronger effects of simulated herbivory on evergreens than on deciduous plants,
whereas natural herbivory caused similar effects on leaf
abscission in evergreen and deciduous trees (Fig. 3). Consequently, in deciduous plants, natural herbivory resulted in a
significantly higher reduction in leaf life span than simulated
herbivory (QB = 8.19, d.f. = 1, P = 0.004), whereas in evergreen plants, the effects of natural and simulated herbivory
were similar (QB = 0.04, d.f. = 1, P = 0.85).
The highly significant (QB = 72.7, d.f. = 26, P < 0.0001)
variation among plant species (those for which we calculated
at least two ESs) in their responses to herbivory was not
explained by their family (QB = 30.5, d.f. = 18, P = 0.40),
growth rate (QB = 1.18, d.f. = 2, P = 0.71), shade tolerance
(QB = 3.09, d.f. = 2, P = 0.42) or biome (QB = 7.21,
d.f. = 6, P = 0.58).
The effects of damage were similar between mature and
young plants but depended on leaf age: damage to young
leaves resulted in a larger decrease in life span than damage
to mature leaves (Fig. 4). The effects of natural herbivory
were weaker on plants with larger (>20 cm in length) leaves
compared to plants with smaller leaves (Fig. 4; QB = 3.82,
d.f. = 1, P = 0.05) and on plants with compound leaves compared to plants with simple leaves (QB = 5.07, d.f. = 1,
P = 0.02). The natural herbivory caused greater reduction in
leaf life span in plants with higher (>10 mm2 mg 1) SLA
than in plant with lower SLA (Fig. 4), and this difference
was observed within both evergreen (QB = 8.43, d.f. = 1,
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 873–881
Herbivory and leaf life span in woody plants 877
P = 0.004) and deciduous (QB = 3.46, d.f. = 1, P = 0.06)
trees. In evergreen species, the reduction in leaf life span
decreased with the increase in species-specific leaf longevity (meta-regression, slope, mean SE: 0.0169 0.0072,
n = 35, P = 0.001).
PUBLICATION BIAS
The absolute values of ESs increased with sample size
(sB = 0.28, n = 115, P < 0.0001), hinting at the existence
of publication bias. Examination of the funnel plot
(Appendix S4) suggests possible selection against smallsample studies that demonstrated an increase in life span of
damaged leaves. However, in spite of the detected bias,
Rosental’s fail-safe number (nfs = 34 341) indicates that our
conclusions for pooled data set were robust against the
unpublished results.
Discussion
LEAF ABSCISSION DUE TO HERBIVORY AS A GENERAL
PHENOMENON
All woody plants periodically shed their leaves. Abscission is
controlled at the level of individual leaves, and the timing of
leaf abscission is regulated by a balance between different
hormones, with ethylene acting as an accelerator and auxin as
inhibitor (Roberts, Elliott & Gonzalez-Carranza 2002). Premature abscission of leaves can be induced by a number of environmental signals, including photoperiod, water stress,
invasive stress (including damage by herbivores) and ozone
(reviewed by Taylor & Whitelaw 2001).
The effects of herbivory on leaf life span greatly differ
among the study systems in both the direction and magnitude.
While numerous publications have reported premature abscission of leaves damaged by insects or the experimenter
(Williams & Whitham 1986; Simberloff & Stiling 1987;
Risley 1993; Gripenberg & Roslin 2008), many researchers
found no effects of either natural or simulated herbivory on
leaf life span (Heads & Lawton 1983; Kudo 1996; Hodge
et al. 1998; Wool & Bogen 1999; Hodge, Keesing & Wratten
2000). Some miners were even reported to delay leaf senescence and prevent the host plant from abscising damaged
leaves until the completion of larval development (Oishi &
Sato 2007). In spite of this variation, our meta-analysis
detected strong overall effects of herbivory on leaf life span of
woody plants. However, we also found that studies of a single
herbivore species yielded stronger effects than studies of multispecies assemblages, suggesting the existence of research bias
due to preferential selection of insect species that are known to
impose greater damage or stronger effects on plants. This bias,
along with publication bias, leads to some overestimation of
ecosystem-wide effects of herbivory, but still, premature
abscission of damaged leaves can be viewed as one of the general responses of woody plants to herbivory. The generality of
this phenomenon emphasizes the importance of studying its
ecological and evolutionary consequences.
COMPARISON BETWEEN NATURAL AND SIMULATED
HERBIVORY
It is commonly appreciated that simulated herbivory cannot
recreate the full suite of events that constitute relevant leaf–
insect interactions and chemical exchanges. The experiments
on downy birch (Kozlov & Zvereva 2014) showed that stronger reduction in leaf life span due to natural herbivory compared to simulated herbivory was not related to the temporal
pattern of the damage (gradually accumulating damage or the
single damage event). Therefore, the difference in the magnitude of the effect on leaf abscission observed between natural
and simulated herbivory is most likely a consequence of other
mechanisms.
Many plant defensive responses are elicited only by compounds present in insect oral secretions and thus do not
develop following simulated herbivory; as a result, the nonspecific response to wounding is likely modified by specific
responses to insect-specific elicitors (Kessler & Baldwin
2002). In particular, caterpillar feeding and the application of
their oral secretions to wounds, but not wounding alone,
induce a burst of ethylene (Kahl et al. 2000), which acts as
an accelerator of abscission (Roberts, Elliott & GonzalezCarranza 2002). Thus, it seems likely that premature
abscission in response to damage is considerably enhanced by
insect-specific elicitors, at least in deciduous trees (see
below). However, although mechanical damage may not
faithfully mimic natural damage, simulated herbivory has
many advantages (Baldwin 1990) that justify its use in studies
of plant responses to herbivory, assuming that the limitations
of this method are explicitly appreciated.
The design of studies exploring the consequences of natural
herbivory also poses some limitations on the interpretation of
results. In these studies, the distribution of damage between
trees, shoots and leaves is not random but rather results from
selection by herbivorous insects. The single study explicitly
addressing this problem demonstrated that the observed effect
on leaf life span was directly induced by leaf mining and did
not reflect preferential oviposition on leaves programmed for
early abscission (Preszler & Price 1993). On the other hand,
herbivore species that oviposit late in the season selected for
birch trees with later leaf abscission (most likely using the
absence of the first signs of senescence as a search cue) to
ensure the completion of larval development (Kozlov &
Zvereva 2014). The possibility of selective oviposition with
respect to the potential life span of the leaf requires detailed
investigation and should be taken into account in studies of
the effects of natural herbivory. To date, the causality of the
effects of damage on the date of leaf abscission is primarily
supported by studies employing simulated herbivory.
VARIATION IN THE EFFECTS OF INSECT HERBIVORES
ON LEAF LIFE SPAN
The majority of studies on the effects of natural herbivory on
leaf life span have been conducted with leaf miners: these
insects account for 65% of the guild-specific data in our
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 873–881
878 E. L. Zvereva & M. V. Kozlov
meta-analysis, compared with 12% on defoliators. This preferential exploration of the effects of miners on leaf abscission
can be classified as a research bias because in natural ecosystems, the average background damage imposed by defoliators
is more than 10 times as high as the damage caused by miners (Nuckols & Connor 1995; Paul et al. 2012). In our opinion, this bias can be explained in two ways. First, leaf mines
can usually be attributed to a certain species, in contrast to
the damage imposed by defoliators. Secondly, the fates of
individual larvae can be inferred from examination of their
mines, allowing interpretation of results in terms of plant
defence acting through abscission of mined leaves (Owen
1978; Faeth, Connor & Simberloff 1981).
Based on the meta-analysis, we can conclude, for the first
time, that insect herbivores from three feeding guilds (miners,
defoliators and gallers) do not differ in their effects on leaf
life span. However, this conclusion may be biased by the low
number of studies on defoliators. On the other hand, galling
aphids with piercing mouthparts and gall midges, whose larvae have chewing mouthparts and feed on a nutritive tissue
that internally surrounds the gall chamber, impose similar
effects on leaf life span, although sap-feeders considerably
differ from other feeding guilds in the mechanisms of their
effects on plants (as discussed by Zvereva, Lanta and Kozlov
2010). Considering the importance of defoliators and sapfeeders for ecosystem functioning, the collection of additional
data on their effects on leaf abscission is an urgent task.
Although specialist and generalist herbivores may differentially influence some plant characteristics (Zvereva, Lanta &
Kozlov 2010; Ali & Agrawal 2012), the effects on leaf life
span were not related to the level of host plant specialization
of individual herbivores. The variation among herbivore species detected in our meta-analysis is more likely explained by
the proportion of damaged leaf area (varying from 1.5 to
87.5% in different study systems) and/or the timing of damage (see below) than by the mode of feeding. However, in
the analysis of the data on birch-feeding herbivores, accounting for both the timing and intensity of damage, the effect of
herbivore species on the date of leaf abscission remained significant, suggesting that specific elicitors of individual herbivores may differ in their effects on leaf life span (Kozlov &
Zvereva 2014).
INTENSITY AND TIMING OF DAMAGE
The effects of herbivory on leaf life span were repeatedly
demonstrated to increase with the proportion of damaged leaf
area (reviewed by Blundell & Peart 2000), and our metaanalysis also detected a decrease in leaf life span with
increasing damage intensity. However, in birch, this relationship was observed only when the damage exceeded 15% of
the area of the damaged leaf for natural herbivory and 30%
for simulated herbivory (Kozlov & Zvereva 2014). Several
earlier studies also revealed the existence of thresholds, demonstrating that for miners, it generally lies between 10 and
20% (Hileman & Lieto 1981; Pritchard & James 1984) but
can be as low as 3% (Naruse 1978). For simulated herbivory,
the threshold falls between 60 and 80% of leaf area (Lam &
Dudgeon 1985; Risley 1993). This difference between the
effects of natural and simulated herbivory on leaf life span is
in line with the generally stronger effect of insect feeding relative to mechanical damage (discussed above).
Young and mature leaves are differentially damaged by a
number of herbivore species (Aide & Zimmerman 1990) and
may differ in their responses to herbivory (Ohnmeiss & Baldwin 2000; Chen & Poland 2009). Direct comparisons demonstrated that similar levels of mechanical damage were more
likely to cause premature abscission of younger leaves than
older leaves (Preszler & Price 1993; Risley 1993; Blundell &
Peart 2000; Kostenyuk & Burns 2004; Kozlov & Zvereva
2014). However, we are aware of only two studies comparing
abscission of differently aged leaves in response to natural
damage (Abbott et al. 1993; Kozlov & Zvereva 2014). Our
meta-analysis confirmed the generality of the conclusions of
these two case studies and indicated that insects attacking
host plants early in the season reduce leaf life span to a
greater extent than species that begin damaging leaves later in
the season. Moreover, herbivores that start feeding in late
summer do not influence the date of leaf abscission in birch
at all (Kozlov & Zvereva 2014).
The detected pattern may result from one or more mechanisms that likely differ between study systems. Abscission of
immature leaves is inevitable if the damage removes differentiating cells required for their development (Coleman &
Leonard 1995). In addition, growing tissues are most sensitive
to environmental stress (Heckenberger, Roggatz & Schurr
1998). In particular, damage imposed by both natural and
simulated herbivory causes considerable water loss (Aldea
et al. 2005), thus leading to water stress, which may differentially affect young and mature leaves (Cechin et al. 2006).
Moreover, immature leaves also lack lignin, an important
defence against pathogens, and thus are vulnerable to infections invading through wounds, which may cause premature
abscission (Taylor & Whitelaw 2001). The responses of
young and mature leaves to herbivory may differ in terms of
damage-induced production of ethylene, which stimulates leaf
abscission: for example, aphids feeding on Dendranthema
grandiflora caused greater ethylene production in young
leaves than in mature leaves (Davies et al. 2004). Finally, the
higher sensitivity of growing leaves to herbivore damage may
result from differences in the balance of hormones between
growing and mature leaves. Accumulation of auxin in meristems of developing leaves may deplete the surrounding cells
of auxin (Heisler et al. 2005), thus making the abscission
zone more reactive to ethylene induced by leaf damage (Kahl
et al. 2000; Taylor & Whitelaw 2001). Alternatively, the ability of auxin to promote ethylene synthesis (Taylor & Whitelaw 2001) may accelerate the abscission of young leaves with
high auxin activity.
PLANT TRAITS
Based on studies of leaf miners, Bultman & Faeth (1986)
suggested that the likelihood of premature abscission due to
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 873–881
Herbivory and leaf life span in woody plants 879
herbivory is higher for evergreens than for deciduous trees.
In spite of weak empirical support (four studies of evergreen plants and a single study of a deciduous tree), this
conclusion has served as the basis for further generalizations. Karban and Baldwin (1997) emphasized the differences in mechanisms of induced resistance as the most
important distinction between deciduous trees and evergreens, concluding that premature leaf abscission is one of
the main defensive responses to herbivory in evergreen
plants, whereas in deciduous plants, herbivory commonly
results in the induction of secondary compounds but not in
premature leaf abscission. However, our meta-analysis does
not support this conclusion because the effects of natural
herbivory on leaf life span appeared to be similar in a
comparison of data from 24 evergreen and 23 deciduous
plant species.
On the other hand, simulated herbivory had a significantly
greater effect on evergreens. Consequently, the responses of
deciduous plants to natural herbivory were much stronger
than their responses to simulated herbivory, whereas in evergreens, the responses to these two types of damage were similarly high. This difference in relative sensitivity to herbivore
feeding and mechanical damage may indicate that evergreens
are more responsive to non-specific wound-induced elicitors,
whereas in deciduous plants, herbivore-specific elicitors are
more likely to enhance the response to mechanical wounding.
Consequently, studies simulating herbivory by mechanical
damage (which comprise 51% of the data on deciduous
plants) significantly underestimate the effects of herbivory on
leaf life span in deciduous plants, thus creating a false
impression of their principal difference from evergreen plants.
We conclude that premature leaf abscission cannot be viewed
as a response to herbivory that is primarily characteristic of
evergreen trees.
The reduction in leaf life span in woody plants in response
to herbivory depends considerably on species-specific leaf
traits. Plants with compound leaves and with large leaves
showed weaker responses, which may be explained at least
partly by the generally lower proportion of leaf biomass lost
due to insect feeding. The effect of damage on leaf life span
weakens with the increase in leaf longevity in evergreens and
with the decrease in SLA in both evergreen and deciduous
plants, indicating that plants with long-living and thicker
leaves are less susceptible to damage in terms of reduction in
leaf life span. Both leaf longevity and SLA belong to a suite
of leaf traits that form the leaf economic spectrum (Wright
et al. 2004) and are positively correlated with mass-based leaf
nitrogen, net photosynthetic capacity and a number of other
leaf traits (Reich et al. 1999). Therefore, our results may indicate that species with a quicker return on investment in nutrients and dry mass in leaves (i.e. species with higher nutrient
concentrations, higher rates of photosynthesis and respiration,
shorter leaf longevity and lower dry-mass investment per leaf
area) are, in general, more susceptible to herbivore damage
and the life span of their leaves is reduced to a greater extent
than in plants from the opposite end of the leaf economic
spectrum.
The traits mentioned above that form the leaf economic
spectrum strongly correlate with each other (Reich et al.
1999; Wright et al. 2004), so the differences in the responses
of plants with alternative leaf economics are difficult to
explain by a single plant trait. However, these differences are
in line with the greater life span reduction observed in young
leaves (low SLA, high metabolic rates) compared to mature
leaves (Abbott et al. 1993; Kozlov & Zvereva 2014) and with
the higher susceptibility to herbivory of seedlings (having
higher metabolic rates compared to older plants) (Nyk€anen &
Koricheva 2004; Zvereva, Lanta & Kozlov 2010). Thus, our
results suggest that variability in plant responses to herbivory
may be linked with the leaf economic spectrum.
ADAPTIVE SIGNIFICANCE OF PREMATURE LEAF
ABSCISSION IN RESPONSE TO HERBIVORY
The adaptive significance of early abscission of damaged
leaves has been widely discussed, in particular as a mechanism of the induced plant defence against insect attack (e.g.
Owen 1978; Faeth, Connor & Simberloff 1981; Williams &
Whitham 1986; Waddell et al. 2001). However, premature
abscission of damaged leaves can cause mortality of herbivores only when (i) the development of a herbivore is
restricted to a single leaf (as in mining and galling insects),
(ii) the damaged leaf sheds before the herbivore completes its
development, or (iii) the herbivore’s development cannot be
continued in a shed leaf, or the risk of predation is higher in
shed leaves. This combination rarely occurs in nature; consequently, the effect of early leaf shedding on insect mortality
has been found in only a few studies (Faeth, Connor &
Simberloff 1981; Williams & Whitham 1986; Simberloff &
Stiling 1987; Mopper & Simberloff 1995), and its generality
has been repeatedly questioned (Kahn & Cornell 1983; Stiling
& Simberloff 1989; Preszler & Price 1993).
Although some responses, such as premature abscission of
intact leaves situated next to the damaged leaves (Stiling,
Simberloff & Brodbeck 1991; Kozlov & Zvereva 2014), can
hardly be seen as adaptive, abscising leaves damaged by herbivores may still benefit plants for a number of reasons. First,
wounding can provide entry points for pathogens; therefore, it
is to the plant’s distinct advantage to drop the damaged leaf
to prevent further invasion and spread of infection (Taylor &
Whitelaw 2001). Secondly, herbivory enhances water loss
from cut edges, thus leading to leaf dehydration (Aldea et al.
2005); shedding of these leaves allows the maintenance of a
favourable water balance of the whole plant (Munne-Bosch &
Alegre 2004). In addition, water deficits initiate signalling
related to senescence (Lim, Kim & Nam 2007), which is generally accompanied by export of nutrients from senescent
leaves to young growing tissues or storage organs so that
nutrient utilization is optimized at the whole plant level
(Munne-Bosch & Alegre 2004).
Thus, premature leaf abscission in response to herbivore
damage can only rarely be classified as an induced resistance
strategy. In general, it is a tolerance strategy that reduces the
negative consequences of local damage on the whole plant.
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 873–881
880 E. L. Zvereva & M. V. Kozlov
Conclusions
Testing of the research hypotheses stated in the introduction
led to the following conclusions: (i) both natural and simulated insect herbivory cause premature abscission of damaged
leaves, (ii) natural herbivory has stronger effects on leaf life
span than simulated herbivory, (iii) natural herbivory similarly
reduces leaf life span in deciduous and evergreen plants, but
simulated herbivory imposes stronger effects on evergreens,
(iv) herbivore feeding guilds do not differ in the magnitude of
their effects on leaf life span, (v) the effect of herbivory on
leaf life span depends on plant and leaf traits and the timing
of the damage, and (vi) the effect of herbivory on leaf life
span increases with the damaged leaf area.
Acknowledgements
We are grateful to Dr. C. N. Mazıa, Dr. J. Yukawa and Prof. D. Wool for providing additional information, to V. Zverev for assistance in the field experiment, to J. Koricheva for methodological advices and to two anonymous
referees for their helpful and inspiring comments. The study was supported by
the Academy of Finland (project no. 122133) and a Turku University strategic
research grant.
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Received 8 November 2013; accepted 24 March 2014
Handling Editor: Ignasi Bartomeus
Supporting Information
Additional Supporting Information may be found in the online version of this article:
Appendix S1. Data used in meta-analysis.
Appendix S2. List of publications included in meta-analysis.
Appendix S3. Effects of simulated herbivory on needle abscission in
Norway spruce and Scots pine.
Appendix S4. Funnel plot.
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 873–881