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Article

Decomposition of Herbivore-Damaged Leaves of Understory Species Growing in Oak and Pine Stands

1
Faculty of Forestry and Wood Technology, Poznań University of Life Sciences, Wojska Polskiego 71c, 60-625 Poznań, Poland
2
Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, Poland
3
Faculty of Biological Sciences, University of Zielona Góra, Prof. Z. Szafrana 1, 65-516 Zielona Góra, Poland
*
Author to whom correspondence should be addressed.
Submission received: 23 December 2020 / Revised: 25 February 2021 / Accepted: 3 March 2021 / Published: 6 March 2021
(This article belongs to the Special Issue Impacts of Herbivory on Plant Communities)

Abstract

:
Leaves are the largest component of forest litter. Their decomposition rate depends mainly on plant species, leaf chemical composition, microorganism biodiversity, and habitat conditions. It is known that herbivory by insects can modify the chemical composition of leaves, such as through induction. The aim of this study was to determine whether the rate of leaf decomposition is related to the susceptibility of the plant species to insect feeding and how leaf damage affects this rate. For our research, we chose six species differing in leaf resistance to insect damage: Cornus sanguinea, Frangula alnus, and Sambucus nigra (herbivore resistant), and Corylus avellana, P. padus, and Prunus serotina (herbivore susceptible). The decomposition of these plant leaves was examined in two monoculture forest stands, deciduous (Quercus robur) and coniferous (Pinus sylvestris). Litter decay rate k and change of litter mass, content of defensive metabolites (total phenols (TPh) and condensed tannins), and substances beneficial for organisms decomposing litter (nitrogen (N) and nonstructural carbohydrates (TNC)) were determined. Contrary to our expectations, leaf litter of herbivore-resistant species decomposed faster than that of herbivore-susceptible species, and damaged leaves decayed faster than undamaged leaves. We found that faster decaying leaf litter had a lower content of defensive compounds and a higher content of TNC and N, regardless of the plant species or leaf damage. Leaf litter decomposition caused a large and rapid decrease in the content of defensive compounds and TNC, and an increase in N. In all species, the tannin content was lower in damaged than in undamaged leaves. This pattern was also observed for TPh, except in S. nigra. We interpret this as the main reason for faster decay of damaged leaves. Moreover, the loss of leaf mass was greater under oak than pine stands, indicating that the microorganisms in deciduous stands are more effective at decomposing litter, regardless of leaf damage.

1. Introduction

The understory is a very important forest layer for each biome, and is mainly composed of shrub species. In European countries, such species include common dogwood (Cornus sanguinea L.), glossy buckthorn (Frangula alnus Mill.), black elder (Sambucus nigra L.), common hazel (Corylus avellana L.), bird cherry (Prunus padus L.), and black cherry (P. serotina Ehrh.). There are also trees that grow tall under normal conditions, but under unfavorable conditions, such as under the canopy of fast-growing trees, they experience inhibited growth and development. The understory significantly affects the functioning of the entire forest ecosystem because it protects the soil from erosion, reduces evaporation from the soil surface, and improves the climate relations of the interior of the stand, strongly inhibiting wind penetration into the forest. In addition, understory shrubs shed leaves that vary in terms of structure and chemical composition [1,2], and thus, contribute to faster degradation of dead organic matter accumulated on the soil surface [3,4].
The introduction of understory shrubs into a monoculture forest is a form of forest protection against outbreaks of insect pests, mainly of coniferous species, deprived of the natural regulatory mechanisms of pest populations. However, the understory plants themselves suffer severely due to the large number of associated herbivorous species [5]. This is most easily observed in the case of bird cherry, whose leaves begin to develop very early [6] and are severely damaged by leaf-eating insects of many species [7,8,9]. The leaves of this shrub are eaten by both polyphagous insects, mainly in the genus Gonioctena Kirby [10], and monophagous insects such as Yponomeuta evonymella L. [6,11].
The main reason for the differences in the degree of leaf damage by leaf-eating insects is variation in food quality, which can be analyzed mainly in two ways. The first is the physical barriers associated with the morphological and anatomical structure of the leaves, depending on the plant species and light conditions [12,13,14]. The second is leaf chemistry, affecting the digestibility and palatability of leaves as a food for herbivorous insects. This applies both to compounds that benefit herbivores in terms of growth and development of herbivores, i.e., attractants (nonstructural carbohydrates (TNC), nitrogen (N) compounds, proteins, and fats) [15,16], and to defensive compounds that the plant has to deter and discourage its consumption, i.e., repellents (phenolic compounds, terpenoids, and alkaloids) [17,18,19]. The chemical composition of the leaves affects not only the amount of damage they receive from insects, but also the rate of their decomposition [20,21].
Our research is an attempt to answer the question of whether the rate of leaf decomposition is related to the susceptibility of the plant species to insect feeding and how leaf damage affects this rate. To explain the reason for the differences in the rate of litter leaf decomposition between the chosen understory plant species and between undamaged and insect-damaged leaves, we conducted a number of chemical analyses. We hypothesized that (1) the rate of litter leaf decomposition would be slower in species resistant to feeding by herbivorous insects due to higher amounts of defensive metabolites and lower amounts of substances beneficial for the growth and development of herbivorous insects in the leaves. Some authors point to such a relationship [22,23]. In line with Burghardt et al. [24], we expected that the leaf litter microbial decomposition efficiency would correspond to herbivore resistance. Thus, we expected that the leaf litter of herbivore-resistant species would decompose more slowly than the leaf litter of herbivore-susceptible species. Additionally, we hypothesized that (2) the rate of decomposition of insect-damaged leaves would be slower compared to undamaged leaves. We supposed that damaged leaves would decompose more slowly because they would be devoid of soft tissues, and the tissues around the damage (necrosis) would be characterized by increased phenolic content. The protective function of phenolic compounds against microorganisms should inhibit the rate of litter decomposition, as stated by Gavinet et al. [25]. Similar to the previous hypothesis, we also assumed in this hypothesis that leaves that contain higher amounts of defensive metabolites and fewer beneficial substances for herbivorous insects would decompose more slowly. In our view, this should be a consequence of the following process: herbivore-induced defense reactions change the leaf palatability and these changes can cascade through to either inhibit or promote the decomposability of leaf litter [24]. In both hypotheses, the basis was the assumption that the above-mentioned substances would affect the microfauna and microorganisms that decompose the litter, just as they affect herbivorous insects [24,26].
We also studied the effect of overstory stand conditions on understory plant growth and the decomposition of leaf litter. There were two single-species overstory stands, English oak (Quercus robur L.) and Scots pine (Pinus sylvestris L.). We tested the hypothesis (3) that the leaves of understory plants would decompose faster in deciduous (oak) than in coniferous (pine) stands. We believe that the specific stand conditions, primarily the microfauna participating in the decay of leaves, are more favorable in oak stands than in pine stands, which is consistent with the “home-field advantage” hypothesis [27,28,29].

2. Materials and Methods

2.1. Plant Material

Research, including the collection of litter to determine their chemical composition and decomposition rates, was carried out at the Zwierzyniec Experimental Forest in Kórnik, Poland (52°14′ N, 17°05′ E). Six understory plant species (Sp) were included in the study, differing in susceptibility (Sus) to insect damage. Three species belonged to the resistant group, in which leaf perforation is less than 10%—common dogwood (Cornus sanguinea L.), glossy buckthorn (Frangula alnus Mill.), and black elder (Sambucus nigra L.)—and three belonged to the susceptible group, in which leaf perforation is more than 10%—common hazel (Corylus avellana L.), bird cherry (Prunus padus L.), and black cherry (Prunus serotina Ehrh.). This distinction was made based on results previously published by our research group on the percentage of leaf tissue loss in these species [9,30]. The plants selected for research, all in shrubby form, were from a dozen to several dozen years old. They grew in a mixed forest stand, under a canopy of oak, beech, hornbeam, birch, ash, alder, and pine.
In autumn (mid-November), both undamaged and insect-damaged leaves from the six species of shrubs were collected. The leaves were collected on sheets under the shrubs, after shaking the shrubs gently. Collected leaves were divided into two groups: including undamaged control leaves (C; 0% of the leaf surface damaged) and leaves damaged by herbivorous insects (D; damage > 0%). From the D group, random samples were chosen (20 leaves from each species) to determine the percentage of perforation using the WinFOLIA software (version 2003b, Regent Instruments Inc., Québec, QC, Canada).
After drying for a week at room temperature (approx. 25 °C), the leaves (5 g—except for F. alnus, 4 g) were placed in nylon bags (20 cm × 20 cm) with a 0.3 mm mesh and placed on the ground in two single-species forest stands (St), oak (Quercus robur L.), and pine (Pinus sylvestris L.) A small mesh size was used because of the needle-leaved species stand in the experiment, and to limit organic matter ingress through the litterbag. The chosen stands were characterized by similarly aged trees, about 25 years old. Six bags representing each treatment of the experiment (plant species × leaf damage) were placed on three randomly selected plots of each kind of stand species (n = 6 species × 2 leaf damage × 2 stands × 3 plots within stand × 6 bags = 432 samples). All bags were placed out on 30 November 2006 and were collected on 30 March, 30 June, and 30 September in 2007 and 2008 (always one bag out of six, i.e., three per treatment). An additional portion of leaves of each treatment was used to determine the initial levels of N and metabolites. The periodically collected bags of leaves in two consecutive years were used to determine the mass of remaining (undecomposed) litter and, after drying, to carry out the same analyses as mentioned above. The litterbags were cleaned with precision, and this type of work was done by one, and always the same, person.
The percentage of undecomposed litter was calculated for each time period relative to the initial mass (100%). In addition to determining the percentage of remaining litter mass, litter decay rate k was also calculated using a negative exponential distribution model, after Olson [31] and Hobbie et al. [32]. This calculation used the linear regression equations of the negative natural logarithm of the fraction of residue mass mi in relation to the initial mass mo from time t (year–1), k =ln (mi/mo) t−1.

2.2. Chemical Analyses

Plant material was dried for 3 days at 40 °C using a Memmert ULE 400 dryer (Memmert GmbH & Co. KG, Schwabach, Germany) with forced air circulation, and ground into powder with a Mikro-Feinmühle-Culatti MFC mill (IKA®-Labortechnik Staufen, Janke & Kunkel GmbH & Co. KG, Staufen, Germany). Small amounts of the powder (0.1 g/sample) were separated for later determination of tannins, because these compounds decompose at temperatures above 40 °C. The remaining powdered material was dried at 65 °C and used for the remaining chemical analyses.
The determination of total soluble phenols (TPh), condensed tannins, TNC, and N content was described in by Karolewski et al. [9]. The content of total soluble phenols was measured colorimetrically using Folin and Ciocalteu’s phenol reagent (Sigma F-9252) at λ = 660 nm. Condensed (catechol) tannins were measured using a color reaction with vanillin in an acid medium. Readings of absorption were taken at λ = 500 nm. Results of the phenol measurements were expressed as micromole of chlorogenic acid per gram of dry mass (μM g−1 d.m.), whereas condensed tannins were converted into micromole of catechin per gram (μM g−1 d.m.). N content (% d.m.) was determined using an ECS CHNS-O 4010 analyzer (Costech Instruments, Pioltello, Italy). TNC were assayed in methanol–chloroform–water extract and results were expressed as % d.m. The content of soluble carbohydrates was measured at λ = 625 nm, following a color reaction with anthrone, while content of starch was measured at λ = 450 nm, following the reaction with dianisidine. Absorbance (tannins, phenols, and carbohydrates) was determined with a spectrophotometer (UV-1700 Visible Spectrophotometer; PharmaSpec, Shimadzu, Japan).

2.3. Statistical Analyses

Analysis of variance (ANOVA) was performed to compare the effect of: susceptibility to insect damage (Sus), understory plant species (Sp), stand species (St), leaf damage (Ld), and time of decomposition (T) on the examined features: remaining mass calculated for the whole research period in relation to initial mass (%), TPh, condensed tannins, N, and TNC in the leaf litter. Understory plant species was nested within the susceptibility group. To assess the impact of the studied factors and associated variables, i.e., the initial content of metabolites (TPh, tannins, TNC) and N on the decay rate (k), ANCOVA was used. The Bliss (arcsin) formula was used for statistical analysis of the features, expressed as a percentage. Before all analyses, normal distributions were verified using the Shapiro-Wilk test. The assumption of homogeneity of variances was tested via Bartlett’s test prior to analysis. For the ANOVA, the number of included data was smaller than the established n = 504 (i.e., the sum of bags (n = 432) and samples used immediately before laying in the leaf litter (n = 72)), because in some cases we were limited by the remaining (undecomposed) litter leaf mass to carry out chemical analyses. Moreover, five bags from different experiment treatments were damaged by animals, but since each experimental variable was represented by three replicates, it was still possible to perform statistical analyses. Statistical analyses were conducted using the JMP 14PRO program (SAS Institute Inc., Cary, NC, USA).

3. Results

3.1. Differences in Rate of Litter Decomposition between Plant Species

Our classification of understory shrubs as either herbivore-resistant or herbivore-susceptible was supported by our leaf damage data. The average percentage of damaged leaf surface was as follows: in the resistant group: C. sanguinea, 3.4%; S. nigra, 4.7%; and F. alnus, 7.2%; and in the susceptible group: C. avellana, 16.8%; P. serotina, 19.6%; and P. padus, 24.3%.
Susceptibility and understory plant species had a significant impact on both the rate of litter decomposition, expressed by the decay rate k (Table 1), and the mass of undecomposed leaves, expressed as a percentage of the initial mass taken as 100% (Table 2). This indicates a clear trend of faster leaf decomposition in plant species characterized by low susceptibility to insect feeding (C. sanguinea, F. alnus, and S. nigra) and slower in other plant species (Figure 1). A similar relationship is also noticeable when comparing the mass of undecomposed leaf litter over time (Figure 2).
The content of TPh and tannins in leaf litter was significantly affected by the understory plant species (Table 2). The differences in content of these metabolites for the entire leaf degradation period were mainly due to their initial level. Such high levels of TPh were first characterized for C. sanguinea leaves (Figure 3A), followed by P. serotina (Figure 3F), C. avellana (Figure 3D), and P. padus (Figure 3E). Initially, a higher content of tannins was found in the leaves of susceptible species: P. serotina (Figure 4F), P. padus (Figure 4E), and C. avellana (Figure 4D). An analysis of TPh and tannins indicated a very rapid decline in their content during the first half of the year. Low content was detected irrespective of the differentiated baseline and persisted for two consecutive years.
In the case of substances that may have a potentially beneficial effect on the microorganisms involved in the decomposition of litter, i.e., N and TNC, the impact of the species was significant (Table 2). N content significantly (p < 0.0001) increased with increased time for litter decomposition (Table 2). This increase is particularly evident in species less susceptible to insects (Figure 5). The content of TNC in leaves decreased especially in the first period of decomposition (Figure 6). Differences between susceptible groups were also noted, where the TNC and N content were lower in susceptible species.

3.2. Differences in Rate of Litter Decomposition between Damaged and Undamaged Leaves

There was no significant effect of leaf damage on the rate of litter decomposition, characterized by the decay rate k (Table 1). When analyzing each species separately, it was found that in P. serotina, damaged leaves decomposed significantly faster (higher k) than the controls (Figure 1). However, leaf damage significantly affected the mass of undecomposed leaf litter (Table 2). The mass of damaged leaves was 6.1% lower than that of control leaves. This faster reduction in the mass of damaged leaves was most evident in P. serotina (Figure 2F), and also noticeable in P. padus (Figure 2E) and C. avellana (Figure 2D). There was a significant Sp × Ld interaction, indicating that the impact of damage on the mass of the remaining litter was affected by understory plant species (Sp). The remaining litter mass data (average in both St) showed that, compared to control leaves, the mass loss of damaged leaves was the largest in P. serotina (27.1%), followed by S. nigra (6.1%), and C. avellana (1.7%). The opposite was true in F. alnus and P. padus, where there was more decomposition in the control than damaged leaves by 7.1% and 4.3%, respectively. In C. sanguinea, there was no difference.
Leaf damage significantly differentiated the content of TPh (Table 2). The understory plant species differentiated the content of TPh; however, there were no differences between the herbivore susceptibility groups. The content of TPh throughout the entire decomposition period and for all Sp was lower in damaged than in undamaged leaves.
Leaf damage did not significantly affect average N content for all species, but there was a significant interaction of Ld × Sus (Table 2). The susceptibility affects N and TNC, where resistant species had 62% and 34% higher content of N and TNC respectively, than susceptible species (Table 2). As the results show by the curve representing changes in TNC content with time of decomposition (Figure 6), one of the reasons for the lack of significant differences between control and damaged leaves may be that in all species, the carbohydrate content after the first measurement period (4 months) of leaf decay decreased to a very low level and at later stages remained practically unchanged.

3.3. Rate of Litter Leaf Decomposition and Its Chemical Composition Variation between Stand Species

The stand species did not significantly affect the decay rate k. However, the interaction between Sus and the St in the impact on k was significant. In the oak stand, decomposition was faster in C. sanguinea than in S. nigra, while in the pine stand, the opposite was true (Figure 2A,C). Additionally, decomposition of P. serotina and C. avellana leaves in oak (Figure 1A) was faster than in pine (Figure 1B). The stand species had a significant impact on undecomposed mass. In the oak stand, the leaves decomposed faster. On average, for all plant species and both treatments of Ld, the mass of undamaged control leaves was 14.8% lower in oak than pine. There was no St × Ld interaction, so regardless of damage, the leaves decomposed faster in oak than pine.
The stand species did not significantly differentiate the content of tannin and TPh in the leaves (Table 2). In all plant species, the levels of these compounds were practically the same under both stand species. The initial content of tested metabolites or N did not affect the decay rate (k), which depended primarily on insect susceptibility and understory plant species, and to some extent on the stand species; a significant interaction was noted between susceptibility and stand species (Table 1). The stand species did not affect the differences in average TPh and tannin content between damaged and undamaged leaves determined throughout their decomposition period (Table 2).

4. Discussion

4.1. Differences in Rate of Litter Decomposition between Plant Species

Our prediction was that differences in the rate of litter decomposition would reflect differences in susceptibility to insect damage. We based this assumption on the influence of defensive compounds, soluble phenols, and condensed tannins on herbivorous insects. At the same time, we assumed that these compounds would similarly inhibit the decay of leaf litter by microorganisms, as they impede the feeding of insects on growing leaves [24,26]. However, we found the reverse: herbivore resistant species had a higher decay rate, which means they decomposed faster. Thus, our first hypothesis, regarding faster leaf litter decomposition in plant species more susceptible to herbivorous insects, was not confirmed. This indicates that there is no direct effect of the resistance of growing leaves to insect feeding on the decomposition of fallen leaf litter by microorganisms.
Results different from ours were obtained by Chapman et al. [23], who examined the relationship between resistant and sensitive tree populations of Pinus edulis Engelm. The fallen needles of the resistant population decomposed slower than those of the sensitive trees. Additionally, Cornelissen et al. [22] obtained results that were opposite of ours. Conducting research in two countries (Argentina and Great Britain), Cornelissen et al. [22] concluded that there was a highly significant positive correlation between leaf palatability and litter mass loss and also a negative correlation between leaf thickness/strength and litter mass loss across all tested species. In contrast, research conducted on 14 temperate woody species by Simon et al. [33] indicated that metabolic profiles in the leaves or litter, including phenol content, does not allow simple grouping according to the decomposition rate. In our research, it is also difficult to find an explanation for the faster decomposition of P. serotina leaves than P. padus leaves, with much greater resistance to feeding of insects in the former [9].
We assumed that the decomposition of leaf litter would be slower for plant species in which the leaves contain more defensive metabolites because these substances would adversely affect microorganisms decomposing litter, just as they adversely affect herbivorous insects [24]. The feeding of insects induces the synthesis of defensive compounds [19,34,35,36,37]. The TPh and tannin content also determines constitutive defense, but it can change during the growing season [9]. Gavinet et al. [25] found higher levels of phenolic compounds in aging leaves of Cotinus coggygria Scop. than in growing leaves. In contrast, our results in both the current and previous studies [9] show that the levels of defense compounds at the end of the growing season decrease rapidly, and the differences in TPh content in autumn leaves are smaller than at the beginning or the peak of the growing season.
The results of the influence of TPh (Figure 3) and tannins (Figure 4) on the litter decomposition rate are unclear. There were significant differences between species at the beginning of the experiment, before decomposition. However, in all species, the levels dropped rapidly after a short period of time. We see the greatest need for further research in this time period, possibly taking into account other groups of metabolites. In general, our results are not consistent with data in the literature, which show that leaves with a higher content of defense compounds decompose more slowly. The negative effect of phenols in fallen leaves on microorganisms decomposing litter, and thus, inhibition of the decomposition process, was indicated in a study by Silfver et al. [38] on individual Betula pendula Roth trees and by Jones et al. [39] on Rhododendron ponticum L. shrubs. In the case of tannins, this pattern is indicated in a review by Kraus et al. [40], and for both groups of defensive compounds (TPh and tannins) in other research [24,41,42]. The inhibitory effect of tannins on the decomposition process is also found in decaying roots [43,44]. In general, the content of the studied defensive compounds in leaf litter was lower in species resistant to insect damage. This trend could explain the reason for the faster leaf litter decomposition in plant species resistant to insect damage.
We found a higher content of TNC in the leaf litter of plant species characterized by faster decomposition (Table 2). Kiser et al. [45] reported on the positive effect of elevated TNC content of Pinus taeda L. needles on their decomposition. Additionally, according to Guo et al. [46], Fan and Guo [47], and Goebel et al. [44], a higher content of TNC in roots significantly contributes to their faster decomposition. Castells et al. [48] indicated a large role of carbohydrates in accelerating the decomposition of litter. Moreover, they suggested that TNC cause the release of N from litter, and their interaction can mask the negative effects of phenolic compounds. The effect of N compounds on reducing the content of defensive carbon compounds in living plants is well known [49]. Our results show that increased TNC content, but also N to some extent, affects litter decomposition. The positive effect of N content in fallen leaves on microorganisms decomposing the litter, and thus, accelerating decomposition, was indicated by Silfver et al. [38], referring to reactions occurring in individual trees of B. pendula. A positive effect of N on leaf litter decomposition was also found by Osono et al. [50], but it concerned decomposition by fungi (Xylaria Hill ex Schrank). In some studies, however, the significance of the effect of N on leaf litter decomposition was negated or defined as negligible [51,52]. The increase of N that we observed was most likely related to the change in the proportion of this element in the decomposed litter. Thus, the proportional increase in N over time in dry matter was due to the relatively faster degradation of nitrogen-free compounds (e.g., carbohydrate).

4.2. Differences in Rate of Litter Decomposition between Damaged and Undamaged Leaves

The second tested hypothesis was also not confirmed. We hypothesized that the damaged leaves would decompose slowly because earlier insect damage would deprive them of soft tissues between the veins [23]. On average, in all species and in most of the leaves, damaged leaves decomposed faster than did undamaged leaves. Similar results, i.e., faster decomposition of damaged versus undamaged needles of Pinus edulis Engelm., were obtained by Chapman et al. [23], studying the feeding of Matsucoccus acalyptus Herbert and Dioryctria albovittella Hulst and by Piazza et al. [53], for Nothofagus pumilio Krasser leaves. The largest and most statistically significant differences in the rate of decomposition between damaged and undamaged leaves were for P. serotina (Figure 1). In P. serotina, shade leaves are eaten almost exclusively by herbivorous insects as opposed to sun leaves [9,10]. The two types of leaves differ greatly in their structure [13]. Shade leaves are very thin and soft, while sun leaves are thick, hard, and leathery. Sariyildiz and Anderson [54], who examined freshly fallen leaf litter from sweet chestnut (Castanea sativa Mill.), oak (Q. robur), and beech (Fagus sylvatica L.) trees classified sun, intermediate, and shade leaf types, and found that shade leaves decomposed faster than sun leaves. Shade leaves are characterized by a much higher specific leaf area (SLA) than sun leaves. The faster rate of decomposition for leaves with higher SLA is also indicated in the review by Cornwell et al. [55]. The likely reason for the faster decomposition of damaged leaves may be that they are generally shaded leaves (with a higher SLA, i.e., a larger area per unit of mass than undamaged leaves), and therefore, more accessible to the microorganisms that decay them. In addition to differences in chemical leaf quality, insects can affect physical quality by increasing tissue weakness and causing a pre-decomposition of damaged leaves, stimulating early fungal colonization [56]. These could be the reasons for the significantly faster decomposition of undamaged versus damaged leaves of P. serotina. Similar factors may have influenced differences (although not significant) between damaged and undamaged leaves for the other studied understory plant species.
We assumed that since leaves damaged by insects would have more defensive metabolites (because of phenolic compound induction) and less carbohydrate or N, they would be slower to decompose. Our results indicate that the content of these compounds does not predetermine the rate of the litter decay and does not cause decomposition differences between damaged and undamaged leaves. However, it was surprising to us that damaged leaves decomposed faster than undamaged leaves, although the difference in litter decay rate was not statistically significant. We knew from many of our previous studies that the damaged leaves [6,10,13,57], and especially the tissues around the necroses [58], are characterized by an increased phenol content. Above, we described the results showing that phenolic compounds inhibit the rate of litter decomposition. For the same reason, we thought that damaged leaves would have a higher content of defensive compounds than undamaged leaves. However, according to our current research, and contrary to our assumptions, the phenol content in fallen leaves just before decomposition turned out to be lower in all plant species in damaged leaves than in those undamaged by herbivorous insects.
The average tannin content in all plant species, and TPh in all species except S. nigra, was lower in damaged than undamaged leaves, not only immediately before decomposition but in the entire decomposition period. Thus, the results regarding defensive compounds explain the faster decomposition of damaged versus undamaged leaves. The results of our research indicating the inhibitory effect of defensive compounds on the decomposition of litter are consistent with the results obtained by other authors [24,59]. However, our results clearly show that in a short time (after 4 months), there is a rapid decrease in the content of defensive compounds, both the TPh (Figure 3) and condensed tannins (Figure 4). A very large decrease in the level of phenolic compounds (by almost 75%) in the fallen needles of C. coggygria, after just over 3 months, was indicated by Santonja et al. [60]. Gavinet et al. [61] reported very rapid degradation of phenolic compounds in the leaf litter of six Mediterranean woody species, despite their very high levels immediately before decomposition. A similar scenario, i.e., a rapid decrease in the content in the first period of decomposition, was also observed in other compounds (terpenes).
Unlike defensive compounds, undamaged and damaged leaves did not differ in their N and TNC content (Table 2). However, when they were analyzed separately for each of the studied plant species, significant differences were noted for some species (Figure 5 and Figure 6). Research carried out by Chapman et al. [23] showed that damage in P. edulis needles increased N content in litter and accelerated decomposition. Conrad et al. [62] explained higher levels of N in leaf litter by herbivory-induced desiccation and foliar mortality prior to the translocation of N back into plant reserves. Because high N content in leaves does not limit insect feeding [63], it is likely that litter-decomposing microorganisms are also unperturbed by high N levels, so differences in N levels do not contribute to differences in decomposition between damaged and undamaged leaves.
It is likely that in the case of litter decomposition by microorganisms, the complex composition of secondary defensive metabolites and nutrients may be more decisive. Some of the results of our research showed a tendency toward such patterns, but their lack of significance diminished their use in inference. For example, there was no significant correlation of leaf damage with leaf decomposition rates of litter or with the level of some metabolites. One reason for this may be that the largest leaf damage in some of the understory plant species we studied was caused by insects classified as monophagous (C. avellana), others as polyphagous (C. sanguinea, S. nigra, F. alnus, P. serotina), and others as both (P. padus). The main pest of C. avellana leaves is the monophagous Altica brevicollis coryletorum Král, which is not harmed by a very high phenolic compound content, but prefers elevated levels of TNC [14]. However, leaf damage caused by this insect mainly affects sun leaves. This results not from the nutritional quality of the leaves, but from the insect’s preference for high temperatures, which causes it to feed on the leaves of plants growing in direct sunlight. This example indicates that leaf damage is not always dependent on metabolite content. Other causes, such as the direct influence of external factors, may be more decisive. In contrast, P. padus leaves are severely damaged by polyphagous insects, mainly Gonioctena quinquepunctata F. [10], and the monophagous Yponomeuta evonymella L. [64,65], which tolerates high levels of phenolic compounds in leaves [6,66]. This may be another reason for the difficulties in obtaining an overall understanding of the relationship between leaf damage, metabolite levels, and the rate of leaf litter decomposition.

4.3. Rate of Litter Decomposition between Stand Species

Some authors point to the influence of the litter of one species on the leaf decomposition of other species [25,67]. According to Ristok et al. [67], this effect consists of accelerating the destruction of tannins, which inhibit the decomposition of litter. Others indicate that the fallen leaves of plant species with high levels of phenolic compounds negatively affect springtails (Collembola) decomposing the litter of other plant species. Soil organisms that decompose plant litter were thought to be mostly generalists [29]. Nevertheless, plant–decomposer interactions show a higher level of specificity than has been formerly thought [68]. Therefore, we formulated our third hypothesis regarding the possibility of differences in the decomposition of leaves depending on the stand, deciduous or coniferous. We assumed that leaves of understory plant species would decompose faster in deciduous versus coniferous stands, i.e., deciduous stands are more favorable for decaying organisms than are coniferous stands. Many leaf litter decay studies have suggested that decomposition occurs more rapidly when litter is placed beneath the plant species from which it has been derived (often referred to as a “home-field advantage”) [28,32,69]. This hypothesis was partially confirmed, because the stand species did not alter the decay rate k; however, it had an influence on the remaining mass in relation to the initial mass (%), where the loss of leaf mass was larger under oak than under pine (Table 2). Horodecki and Jagodziński [70] came to a similar conclusion regarding several species of deciduous trees, noting that leaves decomposed significantly faster in home stands than in Scots pine stands. Furthermore, Ayres et al. [71,72] found that aspen litter degraded more rapidly than the pine litter and both litters decomposed more rapidly in the aspen stands than in pine stands. They speculated that “home-field advantage” may have been due to differences in bacterial and fungal community composition, and differences in the abundance of soil organisms such as rotifers, collembolans, nematodes, and mesostigmatid mites between soil communities in the pine and aspen stands [72].

5. Conclusions

Herbivore-resistant species had a higher decay rate, which means they decomposed faster. This indicates no direct effect of the herbivore resistance of growing leaves on the decomposition of leaf litter by microorganisms. We conclude that we cannot sufficiently confirm the negative impact of defensive compounds and the positive impact of TNC and N on the decomposition of leaf litter that is reported in the literature. Instead, we report that these compounds similarly affect the differences in the decomposition of leaf litter between understory plant species and between damaged and undamaged leaves. However, we cannot say that the tested metabolites play a key role in the rate of litter degradation, primarily because the majority of these substances are decomposed quickly (in the first few months). Moreover, when assessing the influence of these compounds on litter decomposition, we could not determine their content as growing leaves, but only as fallen leaves. Finally, it is worth emphasizing that the loss of litter mass was larger under oak than under pine stands, indicating that the microorganisms in deciduous stands are more effective at decomposing leaf litter from the six understory plant species we examined.

Author Contributions

Conceptualization, P.K. and M.J.G.; methodology, P.K. and M.Ż.; formal analysis, M.J.G. and P.K.; investigation, M.Ż. and E.M.; resources, E.M. and M.Ż.; data curation, E.M. and P.K.; writing—original draft preparation, A.Ł., M.Ż., and P.K.; writing—review and editing, M.J.G., E.M., and D.A., visualization, M.Ż., D.A., and A.Ł.; supervision, P.K.; project administration, P.K.; funding acquisition, P.K. and A.Ł. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the National Science Centre, Poland (grant no. N309 002 31/0246), and the statutory activities of the Polish Academy of Sciences Institute of Dendrology in Kórnik, Poznań University of Life Sciences and University of Zielona Góra. The APC was funded by A.Ł. and M.G. The publication is co-financed within the framework of Ministry of Science and Higher Education programme as Regional Initiative Excellence in 2019–2022, project number 005/RID/2018/19.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available from the corresponding author upon request.

Acknowledgments

We would like to thank Michael T. Stevens and the three anonymous reviewers for their comments, which were helpful in improving the final version of the article.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Figure 1. Coefficients of leaf litter decomposition (mean ± SE) of six understory plant species (the three species on the left are resistant and the three on the right are susceptible to herbivory) in two stand species (n = 3; three bags/species in each stand/damage treatment): (A) oak and (B) pine monoculture. Significant differences between control and damaged and leaves within the same plant species are shown with asterisks (* p < 0.05 and ** p < 0.01).
Figure 1. Coefficients of leaf litter decomposition (mean ± SE) of six understory plant species (the three species on the left are resistant and the three on the right are susceptible to herbivory) in two stand species (n = 3; three bags/species in each stand/damage treatment): (A) oak and (B) pine monoculture. Significant differences between control and damaged and leaves within the same plant species are shown with asterisks (* p < 0.05 and ** p < 0.01).
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Figure 2. Dynamics of leaf litter decomposition of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
Figure 2. Dynamics of leaf litter decomposition of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
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Figure 3. Changes in content of total phenols (TPh; expressed as μM of chlorogenic acid g−1 d.m.) in leaf litter of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
Figure 3. Changes in content of total phenols (TPh; expressed as μM of chlorogenic acid g−1 d.m.) in leaf litter of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
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Figure 4. Changes in content of tannins (expressed as μM of catechin g−1 d.m.) in leaf litter of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
Figure 4. Changes in content of tannins (expressed as μM of catechin g−1 d.m.) in leaf litter of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
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Figure 5. Changes in content of nitrogen (% d.m.) in leaf litter of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
Figure 5. Changes in content of nitrogen (% d.m.) in leaf litter of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
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Figure 6. Changes in content of total non-structural carbohydrates (TNC, % d.m.) in leaf litter of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
Figure 6. Changes in content of total non-structural carbohydrates (TNC, % d.m.) in leaf litter of six understory plant species (herbivore resistant species: Cornus sanguinea—(A), Frangula alnus—(B), Sambucus nigra—(C), on the left and herbivore susceptible species: Corylus avellana—(D), Prunus padus—(E), Prunus serotina—(F), on the right), depending on leaf damage (Ld; control (C) and damaged (D)) in two stand species (St; oak and pine monocultures).
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Table 1. Mean litter decay rate (k) with standard errors (SE) are presented in first part of table. In the second part are ANCOVA results for the influence of susceptibility to herbivores (Sus; resistant and susceptible), plant species (Sp) nested in Sus, stand species (St; oak and pine), leaf damage (Ld; C, control; D, damaged), and initial content of nitrogen (N), total phenolic compounds (TPh), tannins, and total nonstructural carbohydrates (TNC) on litter decay rate (k). p-values < 0.05 are indicated in bold.
Table 1. Mean litter decay rate (k) with standard errors (SE) are presented in first part of table. In the second part are ANCOVA results for the influence of susceptibility to herbivores (Sus; resistant and susceptible), plant species (Sp) nested in Sus, stand species (St; oak and pine), leaf damage (Ld; C, control; D, damaged), and initial content of nitrogen (N), total phenolic compounds (TPh), tannins, and total nonstructural carbohydrates (TNC) on litter decay rate (k). p-values < 0.05 are indicated in bold.
Speciesk
CD
ResistantC. sanguinea3.09 (0.29)3.26 (0.29)
F. alnus2.67 (0.20)2.45 (0.17)
S. nigra2.79 (0.25)3.09 (0.19)
SusceptibleC. avellana0.68 (0.07)0.71 (0.09)
P. padus1.90 (0.15)1.81 (0.09)
P. serotina0.87 (0.15)1.60 (0.27)
Stoak2.06 (0.22)2.25 (0.21)
pine1.94 (0.28)2.06 (0.26)
ANCOVAd.f.Fp
Sus111.76500.0011
Sp (Sus)49.3449<0.0001
St10.96310.3306
Ld10.82740.3669
Ld × Sus11.52190.2225
Ld × St10.84640.3615
Sus × St17.52020.0082
Ld × Sus × St10.23380.6306
N10.86360.3567
TPh13.45400.0684
Tannins10.03570.8509
TNC10.59310.4445
df error56
Table 2. Influence of susceptibility (Sus; resistant and susceptible), understory plant species (Sp) nested in Sus, stand species (St; oak and pine), and leaf damage (Ld; C, control; D, damaged) and leaf decomposition time (T), on remaining mass calculated for the whole research period in relation to initial mass (%), content of total phenols (TPh; expressed as μM of chlorogenic acid g−1 d.m.), condensed tannins (Tannins; expressed as μM of catechin g−1 d.m.), nitrogen (N, % d.m.), and total nonstructural carbohydrates (TNC, % d.m.) in leaf litter. For the ANOVA, the results of all seven terms (1) were used to assess the remaining mass, and for other parameters a maximum of six terms (2) (details in Materials and Methods). p-values < 0.05 are indicated in bold.
Table 2. Influence of susceptibility (Sus; resistant and susceptible), understory plant species (Sp) nested in Sus, stand species (St; oak and pine), and leaf damage (Ld; C, control; D, damaged) and leaf decomposition time (T), on remaining mass calculated for the whole research period in relation to initial mass (%), content of total phenols (TPh; expressed as μM of chlorogenic acid g−1 d.m.), condensed tannins (Tannins; expressed as μM of catechin g−1 d.m.), nitrogen (N, % d.m.), and total nonstructural carbohydrates (TNC, % d.m.) in leaf litter. For the ANOVA, the results of all seven terms (1) were used to assess the remaining mass, and for other parameters a maximum of six terms (2) (details in Materials and Methods). p-values < 0.05 are indicated in bold.
FactorMassTPhTanninsNTNC
ANOVADf 1df. 2FpFpFpFpFp
Sus11662.03<0.00010.180.672271.80<0.0001626.05<0.000149.34<0.0001
Sp(Sus)4463.16<0.000117.78<0.000112.18<0.0001150.64<0.000138.65<0.0001
St1140.26<0.00012.100.14790.010.907825.27<0.00010.040.8390
Ld116.030.01444.910.027312.510.00050.090.76170.010.9282
Time651190.20<0.0001224.30<0.000197.27<0.000175.89<0.0001377.03<0.0001
Ld × Sus119.890.00183.630.05778.000.004912.510.00050.360.5478
Ld × St110.120.72850.010.95390.010.95600.770.38110.340.5572
Ld × T651.130.34285.83<0.000113.34<0.00011.220.29800.280.9249
Sus × St1126.07<0.00010.630.42950.100.75220.900.34270.010.9931
T × St652.530.02050.210.96010.130.98651.920.09011.900.0943
T × Sus6526.43<0.00017.74<0.000171.36<0.000111.96<0.00011.230.2937
T × St x Sus652.130.04870.360.87310.050.99880.970.43670.730.6049
T × St x Ld650.500.81020.040.99920.040.99901.490.19380.590.7087
T × Sus x Ld650.430.85943.610.003410.61<0.00012.010.07610.950.4518
St × Sus x Ld110.100.75360.030.86420.010.96300.010.98080.900.3448
T × Sus × St × Ld650.140.99110.100.99260.020.99980.410.84230.400.8464
df error331233247261237
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Łukowski, A.; Giertych, M.J.; Żmuda, M.; Mąderek, E.; Adamczyk, D.; Karolewski, P. Decomposition of Herbivore-Damaged Leaves of Understory Species Growing in Oak and Pine Stands. Forests 2021, 12, 304. https://0-doi-org.brum.beds.ac.uk/10.3390/f12030304

AMA Style

Łukowski A, Giertych MJ, Żmuda M, Mąderek E, Adamczyk D, Karolewski P. Decomposition of Herbivore-Damaged Leaves of Understory Species Growing in Oak and Pine Stands. Forests. 2021; 12(3):304. https://0-doi-org.brum.beds.ac.uk/10.3390/f12030304

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Łukowski, Adrian, Marian J. Giertych, Michał Żmuda, Ewa Mąderek, Dawid Adamczyk, and Piotr Karolewski. 2021. "Decomposition of Herbivore-Damaged Leaves of Understory Species Growing in Oak and Pine Stands" Forests 12, no. 3: 304. https://0-doi-org.brum.beds.ac.uk/10.3390/f12030304

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