TY - JOUR
AU - Kazakou, Elena
AB - Abstract Background and Aims Forage quality for herbivores and litter quality for decomposers are two key plant properties affecting ecosystem carbon and nutrient cycling. Although there is a positive relationship between palatability and decomposition, very few studies have focused on larger vertebrate herbivores while considering links between the digestibility of living leaves and stems and the decomposability of litter and associated traits. The hypothesis tested is that some defences of living organs would reduce their digestibility and, as a consequence, their litter decomposability, through ‘afterlife’ effects. Additionally in high-fertility conditions the presence of intense herbivory would select for communities dominated by fast-growing plants, which are able to compensate for tissue loss by herbivory, producing both highly digestible organs and easily decomposable litter. Methods Relationships between dry matter digestibility and decomposability were quantified in 16 dominant species from Mediterranean rangelands, which are subject to management regimes that differ in grazing intensity and fertilization. The digestibility and decomposability of leaves and stems were estimated at peak standing biomass, in plots that were either fertilized and intensively grazed or unfertilized and moderately grazed. Several traits were measured on living and senesced organs: fibre content, dry matter content and nitrogen, phosphorus and tannin concentrations. Key results Digestibility was positively related to decomposability, both properties being influenced in the same direction by management regime, organ and growth forms. Digestibility of leaves and stems was negatively related to their fibre concentrations, and positively related to their nitrogen concentration. Decomposability was more strongly related to traits measured on living organs than on litter. Digestibility and decomposition were governed by similar structural traits, in particular fibre concentration, affecting both herbivores and micro-organisms through the afterlife effects. Conclusions This study contributes to a better understanding of the interspecific relationships between forage quality and litter decomposition in leaves and stems and demonstrates the key role these traits play in the link between plant and soil via herbivory and decomposition. Fibre concentration and dry matter content can be considered as good predictors of both digestibility and decomposability. Afterlife effect, dry matter digestibility, decomposability, fertilization, grazing, plant traits, litter, leaves, stems, rangeland INTRODUCTION Plant species control carbon and nutrient cycling as they provide the resources for both herbivores and the functioning of the decomposer subsystem (Hobbie, 1992; Berendse, 1994; Aerts and Chapin, 2000). Several comparative studies have demonstrated that functional traits of living leaves persist through senescence and influence both litter quality and decomposition (Cornelissen, 1996; Cornelissen and Thompson, 1997; Pérez-Harguindeguy et al., 2000). Plant species that are preferentially browsed generally grow more rapidly, accumulate higher concentrations of nitrogen in their tissues and contain lower amounts of secondary metabolites than less preferentially eaten species (Coley, 1988; Grime, 1979; Wardle, 2002). According to the ‘afterlife effect hypothesis’ (Grime and Anderson, 1986), more palatable species will produce high-quality litter, which promotes the activity of the decomposer subsystem and thus enhances decomposition rates (Cornelissen et al., 1999). Indeed, at the interspecific level mainly structural traits of living leaves and those of leaf litter tend to be strongly positively correlated (e.g. Kazakou et al., 2009; Freschet et al., 2010). Experimental studies supporting the afterlife effects hypothesis found that high leaf consumption by invertebrate herbivores (snails, insects) was related to both low investment in foliar defence and high litter decomposability (Grime et al., 1996; Wardle et al., 1998; Cornelissen et al., 1999; Pérez-Harguindeguy et al., 2000; Cornelissen et al., 2004). In spite of the recognition of the positive covariation between palatability and decomposition, there is only limited evidence to support the view that the defences against invertebrates also operate against larger vertebrate herbivores and vice versa, reducing leaf digestibility (Bryant et al., 1991). For instance, only one study (Cornelissen et al., 2004) both focused on larger vertebrate herbivores and considered the links between the digestibility of living leaves and leaf litter decomposability and associated traits. Studies conducted separately on these two processes provide evidence that leaf digestibility and leaf litter decomposability are generally governed by the same leaf traits (see Garnier et al., 2016 for a synthesis): fibre content, which can be considered as an anti-herbivore defence (Coley, 1988) is negatively correlated to digestibility (Al Haj Khaled et al., 2006; Bumb et al., 2016) and decomposability at the interspecific level (Cobo et al., 2002; Wardle et al., 2002; White et al., 2004; Kazakou et al., 2009). Leaf nitrogen concentration is positively related to both processes (e.g. Bidlack and Buxton, 1992; Karn et al., 2006 for digestibility; Pérez-Harguindeguy et al., 2000; Cornwell et al., 2008 for decomposability), whereas leaf toughness (Onoda et al., 2011 for digestibility; Kazakou et al., 2009 for decomposability) and leaf dry matter content (e.g. Pontes et al., 2007; Bumb et al., 2016 for digestibility; Kazakou et al., 2006, 2009; Cortez et al., 2007; Bakker et al., 2011 for decomposability) are negatively correlated to both digestibility and decomposability. The relative importance of each of these traits in explaining the relationship between digestibility and decomposability remains to be determined. We test several biochemical and structural traits for their possible predictive power with respect to leaf digestibility and litter decomposability. Another point under debate in the literature is whether the relationship between digestibility and decomposition is consistent across different plant organs other than leaves. To date, only a few studies have focused on the digestibility and decomposability of organs other than leaves, such as stems and whole shoots (but see Louault et al., 2005; Al Haj Khaled et al., 2006; Pontes et al., 2007 for shoot digestibility; Bumb et al., 2016 for stem digestibility; Birouste et al., 2012; Freschet et al., 2012, 2013 for stem and root decomposability). However, leaves often represent a small fraction of the plant, and stems in some species may provide important biomass for herbivores and decomposers. With only a few studies available on interspecific variation in stem digestibility (Bumb et al., 2016) and decomposability (Freschet et al., 2012), we do not know whether the covariation between digestibility and decomposability in stems is comparable with that observed in leaves. We postulate that (1) leaves will present higher digestibility and decomposability than stems, that (2) similar traits will affect the two processes, but (3) the magnitude will be not the same. We assume that leaves contain more easily degradable forms of organic nitrogen than organs with predominant support and transport functions, in which most nitrogen might be in structural or defence-related compounds (e.g. microtubules, phloem proteins). Freschet et al. (2010) proposed that differences between organ structures also affect their degradation and decomposability. For instance, the typically flat structure of leaves should provide a relatively larger surface for microbial attacks and selective feeding by soil fauna compared with cylindrical organs such as stems. Here, we propose to test these hypotheses by measuring several structural and chemical and traits of green and senescent stems and to evaluate their relative importance in predicting stem digestibility and decomposability. Previous studies demonstrated that differences in management regimes pertaining to defoliation or fertilizer supply affect vegetation structure and function, leading to differences in digestibility (Bumb et al., 2016) and related traits (Pontes et al., 2007; Carrère et al., 2010). So far, digestibility–decomposability relationships have mostly been established for species belonging to different functional types and very few studies have explicitly addressed the effects of the intensity of herbivory and resources availability on these relationships (Wardle et al., 2004). The originality of the present study is that we propose to explore dry matter digestibility and decomposability relationships for 16 dominant species from Mediterranean rangelands subject to management regimes differing in intensity of grazing and fertilization. We expect that the high-fertility conditions and the high rates of herbivory jointly (1) cause the dominance of fast-growing plants, which are able to compensate for tissue loss by herbivory, and (2) produce highly digestible organs and litter with high decomposition rates. Figure 1 summarizes the different hypotheses tested: (1) as postulated by the afterlife effect hypothesis, digestibility and decomposability covary positively (bidirectional arrow 1) due to the fact that both are caused by the same traits both across and within management regimes and for all studied organs; (2) digestibility is caused by traits measured only on living organs (arrow 2); (3) traits of living organs cause some traits of litter for all studied organs (arrow 3) and (4) decomposability is caused by traits measured on both living and litter organs (arrows 4 and 5). Fig. 1. View largeDownload slide Scheme showing the putative links between traits of leaves and stems and the two degradation processes studied here: digestibility and decomposition. We tested the hypotheses that (1) digestibility and decomposability covary positively (bidirectional arrow 1); (2) digestibility is affected by traits measured only on living organs (arrow 2); (3) traits of living organs affect some traits of litter for all studied organs (arrow 3) and (4) decomposability is caused by traits measured on both living and litter organs (arrows 4 and 5). Fig. 1. View largeDownload slide Scheme showing the putative links between traits of leaves and stems and the two degradation processes studied here: digestibility and decomposition. We tested the hypotheses that (1) digestibility and decomposability covary positively (bidirectional arrow 1); (2) digestibility is affected by traits measured only on living organs (arrow 2); (3) traits of living organs affect some traits of litter for all studied organs (arrow 3) and (4) decomposability is caused by traits measured on both living and litter organs (arrows 4 and 5). MATERIALS AND METHODS Study site, experimental design and plant species We chose species from dry calcareous rangelands in southern France located on a limestone plateau (Larzac Causse) at the INRA La Fage experimental station (French National Institute for Agricultural Research) (43°55′ N, 3°05′ E, 790 m above sea level). The climate of the plateau is sub-humid with a Mediterranean influence, with cool wet winters and warm dry summers. Mean annual precipitation of 1070 mm occurs mainly during spring and autumn, and mean monthly temperatures vary from 1 °C in January to 19 °C in August (data from 1973–2006). The vegetation is dominated by perennial herbaceous species (Bromopsis erecta), along with loosely scattered shrubs and trees (Buxus sempervirens and Juniperus oxycedrus) (Bernard, 1996). For the past 35 years, these rangelands have been grazed by a sheep flock (Romane breed) raised outdoors year-round for meat production. The experimental station is divided into paddocks that vary between 4.7 and 24.5 ha. We chose six of them, with two different management regimes since 1978. The first regime consists of moderate grazing (G+F− hereafter) of 0.20 kg kg−1 (proportion of total annual biomass produced that is removed by grazing) and no fertilization. The second regime consists of intensive grazing (G++F+ hereafter) of 0.61 kg kg−1 (increased grazing in spring) and fertilization, with additions of mineral nitrogen (65 kg ha−1 year) and phosphorus (40 kg ha−1 every 3 years, stopped in 2005) since 1978. We chose three plots per paddock, which covered 200–500 m2, for the present study (replicates). Based on previous botanical surveys conducted in the paddocks (Bernard-Verdier et al., 2012; Barkaoui et al., 2013; Chollet et al., 2014), we selected 16 species among the most abundant ones: six species were present only in G+F−, six species were present only in the G++F+ and four were present in both treatments (Bromopsis erecta, Pilosella officinarum, Potentilla tabernaemontani and Poterium sanguisorba; Table 1, species names from International Plant Names Index). Table 1. List of species studied, with occurrence in each treatment, taxonomic group, life cycle and growth form (according to Pérez-Harguindeguy et al. 2013) Species  Treatment  Taxonomic group  Life cycle  Growth form  Anthyllis vulneraria  G+F−    Fabaceae  Perennial/annual  Rosette  Brachypodium pinnatum  G+F−    Poaceae  Perennial  Tussock  Carex humilis  G+F−    Cyperaceae  Perennial  Tussock  Helianthemum apenninum  G+F−    Cistaceae  Perennial  Extensive vegetative spread and stemmed herb  Helianthemum canum  G+F−    Cistaceae  Perennial  Extensive vegetative spread and stemmed herb  Stipa pennata  G+F−    Poaceae  Perennial  Tussock  Capsella bursa-pastoris    G++F+  Brassicaceae  Annual  Rosette  Erodium cicutarium    G++F+  Geraniaceae  Annual  Rosette  Geranium molle    G++F+  Geraniaceae  Annual  Extensive vegetative spread and stemmed herb  Plantago lanceolata    G++F+  Plantaginaceae  Perennial  Rosette  Poa bulbosa    G++F+  Poaceae  Perennial  Tussock  Veronica arvensis    G++F+  Plantaginaceae  Annual  Extensive vegetative spread and stemmed herb  Bromopsis erecta  G+F−  G++F+  Poaceae  Perennial  Tussock  Pilosella officinarum  G+F−  G++F+  Asteraceae  Perennial  Rosette  Potentilla tabernaemontani  G+F−  G++F+  Rosaceae  Perennial  Extensive vegetative spread and stemmed herb  Poterium sanguisorba  G+F−  G++F+  Rosaceae  Perennial  Rosette  Species  Treatment  Taxonomic group  Life cycle  Growth form  Anthyllis vulneraria  G+F−    Fabaceae  Perennial/annual  Rosette  Brachypodium pinnatum  G+F−    Poaceae  Perennial  Tussock  Carex humilis  G+F−    Cyperaceae  Perennial  Tussock  Helianthemum apenninum  G+F−    Cistaceae  Perennial  Extensive vegetative spread and stemmed herb  Helianthemum canum  G+F−    Cistaceae  Perennial  Extensive vegetative spread and stemmed herb  Stipa pennata  G+F−    Poaceae  Perennial  Tussock  Capsella bursa-pastoris    G++F+  Brassicaceae  Annual  Rosette  Erodium cicutarium    G++F+  Geraniaceae  Annual  Rosette  Geranium molle    G++F+  Geraniaceae  Annual  Extensive vegetative spread and stemmed herb  Plantago lanceolata    G++F+  Plantaginaceae  Perennial  Rosette  Poa bulbosa    G++F+  Poaceae  Perennial  Tussock  Veronica arvensis    G++F+  Plantaginaceae  Annual  Extensive vegetative spread and stemmed herb  Bromopsis erecta  G+F−  G++F+  Poaceae  Perennial  Tussock  Pilosella officinarum  G+F−  G++F+  Asteraceae  Perennial  Rosette  Potentilla tabernaemontani  G+F−  G++F+  Rosaceae  Perennial  Extensive vegetative spread and stemmed herb  Poterium sanguisorba  G+F−  G++F+  Rosaceae  Perennial  Rosette  View Large Sampling for digestibility of living organs and litter decomposability In spring 2013, we harvested living biomass of these plant species at the period of peak biomass (end of May for G++F+ and mid-June for G+F−). We placed 30–150 healthy individuals per species from each plot into plastic bags with moist tissues (wetted with deionized water) and kept them in a cooler for 24–48 h until further processing in the laboratory. We then sorted each sample into leaves (lamina and sheath) and stems, and dried them at 60 °C for 72 h. We ground them using a ZM100 centrifugal mill through a 1-mm screen. We collected leaf and stem litter at the season of maximum senescence for each species (summer and autumn 2013). We collected dead or senescing leaves and stems directly from the standing plant, carefully cleaned them and then dried them at 60 °C for 72 h and stored them in the laboratory. Dry matter digestibility We measured dry matter digestibility in dried and ground samples of living organs. This was done in two steps. First, we obtained in vitro measurements of a reference subsample using a pepsin-cellulase method of Aufrère et al. (2007); for more details see Bumb et al. (2016). These in vitro measurements come both from previously published values (see Bumb et al., 2016 for details) and from our own samples. Second, we developed calibration curves based on near-infrared reflectance spectroscopy (NIRS) using a FOSS NIRSystems 6500 spectrometer (FOSS NIRSystems, Silver Spring, MD, USA). These calibration curves allowed us to predict the in vitro digestibility of the remaining samples using only the NIRS values. Near infrared reflectance spectroscopy is a non-destructive and highly precise physical method based on selective absorption of near-infrared electromagnetic waves by organic molecules (Birth and Hecht, 1987). NIRS has proved useful to relate the spectra of samples to their laboratory biochemical values in a number of digestibility studies (Aufrère et al., 1996; Stuth et al., 2003; Andrés et al., 2005). Calibration curves were obtained using modified partial least squares regression with WINISI software (version 4, Infrasoft International, Port Matilda, PA, USA). As measured and predicted digestibility were strongly correlated (Bumb et al., 2016), the NIRS method was used to predict digestibility from spectral data. Chemical parameters known to be related to the nutritional value of the samples were also measured in the 24 samples used for calibrations: in vitro dry matter digestibility (g kg−1) was measured by the pepsin-cellulase method of Aufrère et al. (2007); total nitrogen concentration (NC; g kg−1) was measured by the Kjeldahl method and fibre content (neutral detergent fibre, NDF %) was measured by the Van Soest sequential detergent method with an amylase and protease pre-treatment (Van Soest et al., 1991). In total, we analysed 119 samples of leaves and 97 of stems (not enough material was available for Brachypodium pinnatum, Carex humilis and Pilosella officinarum). Litter decomposability Within each of the two management regimes, we collected and pooled litters by species independently of the paddock where there were collected. In total we collected leaf litter of 16 species (in total 18 populations, as two species were found in the two management regimes) and stem litter of 14 species (not enough material was available for Carex humilis and Pilosella officinarum). We incubated leaf and stem litters in microcosms in the laboratory, under controlled temperature and humidity conditions, to measure the potential decomposability of the litter induced by differences in litter quality only. The microcosm type used for this experiment was described by Taylor and Parkinson (1988). Each microcosm chamber, 15 cm high, was made of a 15-cm diameter polyvinylchloride pipe, fitted with a lid and a sealed bottom. We placed 1 kg of standard soil on the grid, 2 cm above the bottom. The soil was a 3:1 mixture of mineral soil and surface organic horizon taken from the CEFE experimental garden in Montpellier. For each of the 16 species, we sealed in nylon litter bags of 1 mm mesh four repetitions of litter samples (between 0.40 and 2.10 ± 0.01 g each) per management regime (Northern Mesh, Oldham, UK). In the microcosm experiment we excluded the mesofauna, and the mass loss observed was the result of microbial decomposition. We weighed each litter sample to get its initial mass. We subsequently moistened the soil to 80 % of field capacity. We kept the microcosms in the dark at 24 °C throughout the experiment and watered them once a week to maintain constant soil moisture during the incubation period. After 8 weeks, we took litter bags out of the microcosms, carefully removed soil particles from the litter bags, dried the litter samples for 48 h at 60 °C and weighed them. Traits of living and litter organs: sampling and measurements We assessed living leaf and stem dry matter content (DMC) [calculated as the ratio between the dry mass of the organ and its water-saturated fresh mass (Garnier et al., 2001)] on at least 12 individuals per species in each management regime during spring 2013, collected at the same time as those used for digestibility measurements (more details are given in Bumb et al., 2016). We conducted chemical analyses on living organs and their litter at the peak period of growth and senescence, respectively, for both leaves and stems. For living leaves and stems, we estimated NC and fibre content (NDF %) by the NIRS method on the same material as that used for digestibility measurement. We based calibrations on NC measured by the Kjeldahl method (Bradstreet, 1954) and fibre content measured by the Van Soest sequential detergent method (Van Soest et al., 1991). We determined the NC of litter leaves and stems with an elemental analyser (model EA 1108; Carlo Erba Instruments, Milan, Italy) while we predicted their NDF by NIRS. We measured phosphorus concentration (PC) colorimetrically with an autoanalyser (Evolution II; Alliance instruments, Frépillon, France), using the molybdenum blue method following digestion with sulphuric acid (Grimshaw et al., 1989) on living leaves and stems, as well as on leaf litter. We measured condensed tannins according to the acid butanol method (Waterman and Mole, 1994). Phosphorus and tannin concentrations were not available for living stems due to insufficient material. Data analysis We performed statistical analyses with the R software (R Development Core Team, 2010). To test the influence of management regime, growth form, species (nested in growth form) and their interactions with digestibility and decomposability we used linear mixed models (as implement in the lme4 R package; Bates et al., 2015), in which we treated these effects as fixed and paddock as a random effect on the intercept of the relationship. We performed these analyses for each organ (leaf and stem) of the studied species. We used manual backward elimination for covariate selection using conditional F-test P-values to assess the significance of effects (as implemented in the R package pbkrtest; Halekoh and Højsgaard 2014). We verified the normality of the distribution of residuals for each model. When a growth form effect was detected, Tukey tests were used to determine significant differences between them. The same procedure was applied to the four plant species that occurred in both treatments to test the influence of management regime for each plant part. We calculated Pearson and Spearman correlations on data averaged for each species, organ and management regime to test for relationships between digestibility, decomposability and traits. We tested digestibility in relation to traits of living organs only, while for decomposability we tested relationships with traits measured on both living and litter plant material to assess the afterlife effects (Fig. 1). We also tested correlations for each management regime and organ. We estimated intercepts and slopes with ANCOVA to compare the influences of management regime and organ on dependent variables. We performed principal components analysis (PCA) separately for each organ using the adee4 R package (Dray and Dufour, 2007) to determine the relationships among traits across species, considering separately leaves and stems on the one hand, and traits of living plants and litter on the other hand. We addressed differences between growth forms using one-way analysis of variance (ANOVA), followed by a Tukey test. We used multiple regressions to test the relative importance of traits for the prediction of digestibility and decomposability. We used only traits from living plant material to predict digestibility, while we considered traits from living and litter plant material in separate models to predict decomposability. We used a stepwise approach to select the best model and we based this on the corrected Akaike information criterion (package glmulti, function glmulti). We tested the variance inflation factor (VIF) (package car, function vif) in order to avoid collinearity between variables. We considered variables presenting VIF <5 in the model (Kutner et al., 2004). We calculated the partial η2 (package heplots, function etasq) to provide a measure of the relative importance of each variable representing the proportion of the total variability attributable to a given factor. After selection of variables (the AIC criterion was used), we checked and confirmed the homoscedasticity and normality of the residuals of each best model. Finally, we calculated Spearman ranking coefficients between living and litter traits (for nitrogen and phosphorus concentrations, NDF and tannin concentrations) on leaves and stems. RESULTS Variations in digestibility and decomposability Species identity and growth forms influenced digestibility (for leaves F4,93.1 = 1.45**, for stems F2,67.3 = 10.9***, and Fig. 2A) and decomposability (for leaves F3,197 = 5.05**, for stems F3,173 = 3.17*, and Fig. 2B). Rosette plants like Capsella bursa-pastoris and Erodium cicutarium showed higher digestibility (Fig. 2A) and decomposability (Fig. 2B) than tussock plants like Stipa pennata, Bromopsis erecta and Carex humilis. Extensive vegetative spread and stemmed herbs like Potentilla tabernaemontani had digestibility and decomposability similar to rosette plants or intermediate between rosette and tussock plants (Fig. 2). Fig. 2. View largeDownload slide Relationships between (A) dry matter digestibility and (B) litter decomposability of leaves and stems. The r values are Spearman correlation coefficients and F values correspond to ANOVA results. Open symbols represent the G++F+ treatment and solid symbols represent the G+F− treatment. *P < 0.05; **P < 0.01; ***P < 0.001; ns, not significant. Extensive and stemmed herb: extensive vegetative spread and stemmed herb (see Table 1). Fig. 2. View largeDownload slide Relationships between (A) dry matter digestibility and (B) litter decomposability of leaves and stems. The r values are Spearman correlation coefficients and F values correspond to ANOVA results. Open symbols represent the G++F+ treatment and solid symbols represent the G+F− treatment. *P < 0.05; **P < 0.01; ***P < 0.001; ns, not significant. Extensive and stemmed herb: extensive vegetative spread and stemmed herb (see Table 1). For most species, digestibility was higher for leaves than for stems (Fig. 2A, 3A), while decomposability was not significantly different between the two organs (Figs 2B and 3B). Differences between organs (Figs 2 and 3), management regimes and growth forms (Fig. 3) were higher for digestibility than for decomposability. Fig. 3. View largeDownload slide Average values of (A) dry matter digestibility and (B) decomposability for species of the two management regimes and for leaf and stem. Different letters indicate significant differences among management regimes and organs (post hoc Student–Newman–Keuls test). Fig. 3. View largeDownload slide Average values of (A) dry matter digestibility and (B) decomposability for species of the two management regimes and for leaf and stem. Different letters indicate significant differences among management regimes and organs (post hoc Student–Newman–Keuls test). Management regimes influenced digestibility and decomposability of each organ (Fig. 3): species in the G++F+ treatment had higher digestibility and decomposability than those in the G+F− treatment for both leaves and stems (+20.3 % and +26.0 %, respectively, for digestibility; +38.8 % and +20.2 %, respectively, for decomposability). Relationships between digestibility and decomposability Digestibility was positively related to decomposability when all data from the 16 plant species were considered in the analysis, irrespective of the organ or management regime considered (Fig. 4). This relationship was also consistent within each management regime or organ (Fig. 4). Common slopes and intercepts were found when leaves and stems were analysed separately (Fig. 4 and data not shown). Digestibility–decomposability relationships typically showed similar slopes for both management regimes, with slight shifts in intercepts: that of the relationship in the G++F+ treatment was marginally higher than that in the G+F− treatment (legend to Fig. 4). Fig. 4. View largeDownload slide Relationship between dry matter digestibility and litter decomposability. Solid symbols are for the G+F− treatment, while open symbols are for the G++F+ treatment. The r values are Pearson or Spearman correlation coefficients for all data (rtotal), each organ (rleaf and rstem) and management regime (rG+F+ and rG++F−). ANCOVA analyses show that the influences of management regimes and organs on slopes and intercepts of the relationships between the two variables are significant only for the effect of management on the intercept (F = 2.99, P < 0.01). *P < 0.05; ***P < 0.001. Fig. 4. View largeDownload slide Relationship between dry matter digestibility and litter decomposability. Solid symbols are for the G+F− treatment, while open symbols are for the G++F+ treatment. The r values are Pearson or Spearman correlation coefficients for all data (rtotal), each organ (rleaf and rstem) and management regime (rG+F+ and rG++F−). ANCOVA analyses show that the influences of management regimes and organs on slopes and intercepts of the relationships between the two variables are significant only for the effect of management on the intercept (F = 2.99, P < 0.01). *P < 0.05; ***P < 0.001. Relationships between digestibility, decomposability and traits Axis 1 of the PCA on living leaves accounted for 52.4 % of the variation and was primarily positively associated with DMC and NDF was negatively associated with nitrogen concentration (Supplementary Data Appendix S4). Axis 1 of the PCA for living stems accounted for 75.6 % and was determined by similar traits as for the PCA on living leaves (Supplementary Data Appendix S4). Dry matter content was the trait with the highest loading on axis 1 of the PCA (insets in Supplementary Data Appendix S4), explaining 28 % of the variation for leaves and 35 % for stems. The projection of the points on axis 1 was recovered to test correlations with digestibility for traits from living plant material and decomposability for traits from living and litter plant material. Digestibility was negatively related to this axis 1 for both leaves (Fig. 5A) and stems (Fig. 5B) (see Supplementary Data Appendix S3A, D, F, I for bivariate relationships between traits of living organs and digestibility). Decomposability was also strongly and negatively correlated with this first PCA axis for both leaves (Fig. 5C) and stems (Fig. 5D) (see Supplementary Data Appendix S3B, E, G, J for bivariate relationships between traits of living organs and decomposability). For leaf litter and stem litter we found similar results (Supplementary Data Appendix S4) and decomposability was negatively related to this axis for both leaves (Fig. 5E) and stems (Fig. 5F) (see Supplementary Data Appendix S3C, H, K for bivariate relationships between traits of litter and decomposability). Fig. 5. View large Download slide Relationships between axis 1 of the PCA combining traits of living organs and (A) leaf dry matter digestibility, (B) stem dry matter digestibility, (C) leaf decomposability, (D) stem decomposability, and between axis 1 of PCA combining traits of litter and (E) leaf decomposability and (F) stem decomposability. Open symbols correspond to the G++F+ treatment and solid symbols to the G+F− treatment. The r values are Pearson correlation coefficients for all data. Relationships between individual traits and digestibility and litter decomposability are given in Supplementary Data Appendix 3. *P < 0.05; **P < 0.01; ***P < 0.001. Extensive and stemmed herb: see Table 1. Fig. 5. View large Download slide Relationships between axis 1 of the PCA combining traits of living organs and (A) leaf dry matter digestibility, (B) stem dry matter digestibility, (C) leaf decomposability, (D) stem decomposability, and between axis 1 of PCA combining traits of litter and (E) leaf decomposability and (F) stem decomposability. Open symbols correspond to the G++F+ treatment and solid symbols to the G+F− treatment. The r values are Pearson correlation coefficients for all data. Relationships between individual traits and digestibility and litter decomposability are given in Supplementary Data Appendix 3. *P < 0.05; **P < 0.01; ***P < 0.001. Extensive and stemmed herb: see Table 1. Loading of species on axis 1 varied significantly among growth forms. Tussock plants had higher living leaf NDF and DMC and lower NC than rosette plants and extensive and stemmed herbs (F = 11.4***; Fig. 5A, C and Supplementary Data Appendix S4); the PC of their leaf litter was also lower than that of rosette plants and extensive and stemmed herbs (F = 15.9***; Fig. 5E and Supplementary Data Appendix S4). Extensive and stemmed herbs were intermediate for living stems (F = 5.66*; Fig. 5B, D and Supplementary Data Appendix S4). Finally, the litter stems of tussock and rosette plants generally had higher NDF and lower NC than extensive and stemmed herb litter stems (F = 10.1**; Fig. 5F and Supplementary Data Appendix S4). There was a strong relationship between NDF of leaves and NDF of stems, indicating that fibres were more conserved across the senescing process than nutrients (Supplementary Data Appendix S2). Relative influence of traits on digestibility and decomposability The regression model showed that the digestibility of leaves was mainly explained by NDF (negative relationship) and nitrogen concentration (positive relationship) (Table 2). NDF was also the most important variable explaining the digestibility of stems, with marginal effects of NC (Table 2). For the two organs, DMC was excluded from the regression models due to the collinearity with several other traits, in particular NDF (Fig. 4, and see Discussion section). Table 2. Effects of functional traits on dry matter digestibility and decomposability for leaves and stems. The table shows t values from multiple linear regression models, and with their relative importance in dry matter digestibility or decomposability variation (%). The R2 adjusted results shown are from best model after traits selection.     Dry matter digestibility  Decomposability      Leaf  Stem  Leaf  Stem      Effect  Relative importance  Effect  Relative importance  Effect  Relative importance  Effect  Relative importance  Green trait  DMC          2.80*  17.1      N  3.23**  32.8      4.23***  26.6      NDF  −7.77***  67.2  −3.03**  92.5  −4.37***  27.4  −4.12***  100  P          4.65  28.8        Adjusted R2  0.91  0.42  0.85  0.48  Litter trait  N                  NDF          3.65**  100  −4.12***  100  P                  Tannins                    Adjusted R2      0.42  0.50      Dry matter digestibility  Decomposability      Leaf  Stem  Leaf  Stem      Effect  Relative importance  Effect  Relative importance  Effect  Relative importance  Effect  Relative importance  Green trait  DMC          2.80*  17.1      N  3.23**  32.8      4.23***  26.6      NDF  −7.77***  67.2  −3.03**  92.5  −4.37***  27.4  −4.12***  100  P          4.65  28.8        Adjusted R2  0.91  0.42  0.85  0.48  Litter trait  N                  NDF          3.65**  100  −4.12***  100  P                  Tannins                    Adjusted R2      0.42  0.50  *P < 0.05; **P < 0.01; ***P < 0.001; ns, not significant. View Large For litter, the regression model showed that nitrogen was the most important variable explaining the decomposability of leaves (Table 2). When traits of living leaves were considered to explain the decomposability of the corresponding litter, PC, NDF and nitrogen presented higher relative importance than DMC (Table 2). Decomposability of stems was more tightly related to NDF in both regression models considering the traits of litter or living organs (Table 2). DISCUSSION Digestibility–decomposability relationships The first objective of our study was to test the afterlife effect hypothesis (Grime and Anderson, 1986) across different organs for rangeland species found in contrasted management regimes. The strong positive relationship between the two degradation processes supported this hypothesis, which postulates that highly defended leaves have low digestibility and produce more recalcitrant litter, leading to low decomposition rates (Melillo et al., 1982; Grime et al., 1996; Cornelissen et al., 1999, 2004; Hättenschwiler and Vitousek, 2000). This hypothesis had only been tested in two studies in the context of vertebrate herbivores (Cornelissen et al., 2004; White et al., 2004) and only on leaves. Here we found a single general relationship between the two processes for both leaves and stems, and across management regimes, suggesting that afterlife effects are maintained whatever the source of variation inducing differences in the quality of plant material. The range of variation observed in our study conducted on 16 species from Mediterranean rangelands was comparable to that observed in the study by Cornelissen et al. (2004) on 32 subarctic plant species (≈300–872 versus 350–800 g kg−1 for leaf digestibility, respectively; ≈8.13–41.3 % in microcosm versus 20–80 % in situ for leaf litter mass loss, respectively). Our results were in line with previous studies showing that dicotyledons, composed mainly of rosettes and extensive and stemmed herbs, presented higher digestibility (Duru, 1997) and decomposability than monocotyledons (Cornelissen et al., 1999, 2004; Pérez-Harguindeguy et al., 2000; Cornwell et al., 2008; Pálková and Lepš, 2008). In a simultaneous multi-species comparison of decomposition rates of leaf litters in a temperate flora, graminoid monocots showed on average lower litter decomposition rates than herbaceous dicots (Cornelissen, 1996). Graminoid monocots have generally physically tougher leaves with greater silicon contents than herbaceous dicots, and this corresponds with the lesser decomposability of the former (Cornelissen and Thompson, 1997). Our results showed that digestibility of leaves was 1.2 times higher than that of stems, in agreement with previous studies (Duru, 1997; Bidlack et al., 1999; Arzani et al., 2004; Karn et al., 2006; Duru et al., 2008; Beecher et al., 2013): leaves are rich in nitrogen and soluble compounds that are easily degradable, while stems contained more fibre and structural tissue (Poorter and Bergkotte, 1992; Duru et al., 2000; Duru, 2003). However, decomposability was similar for both organs (8.13–41.3 % for leaves and 13.5–35.2 % for stems), whereas we expected leaves to decompose faster than stems (Semmartin and Ghersa, 2006; Freschet et al., 2012, 2013). In stems, there is an increase in cell-wall concentration and a decrease in soluble cells during development (Buxton, 1996), making basal segments more digestible than upper segments (Pritchard et al., 1963). High grazing and fertilization in the G++F+ treatment induced a modification in species composition over time in these rangelands (Chollet et al., 2014), resulting in species with higher digestibility and decomposability in the G++F+ than in the G+F− treatment. We hypothesized that more intensive management practices hastened plant development in relation to faster growth and in relation to changes in chemical composition, such as an increase in nitrogen concentration (Pontes et al., 2007; Carrère et al., 2010; Lavorel and Grigulis, 2012) and a decrease in fibre content (Duru and Ducrocq, 2002; Carrère et al., 2010; Lavorel and Grigulis, 2012). This hypothesis was confirmed here: the G++F+ treatment was dominated by exploitative species with high nitrogen concentration and low fibre content, likely to allow compensatory growth after grazing (Herms and Mattson, 1992); conversely, the G+F− treatment was dominated by conservative species with high leaf DMC (see also Pontes et al., 2007), tannin concentration and fibre content (see also De Bello et al., 2010), protecting plants from herbivory via efficient defence mechanisms (Herms and Mattson, 1992). Thus, the response of plant traits to grazing and fertilization induced changes both in the digestibility of living organs and in the decomposability of litter whose quality was dependent on these traits. Traits related to digestibility or decomposability The second objective of this study was to determine which traits explained variations in digestibility and decomposability. Dry matter content was the trait contributing most to explaining variation of the first axis of the PCA analysis for living leaves and stems. This axis was strongly correlated to both digestibility and decomposability. However, DMC was excluded from the regression model as it was strongly correlated to NDF. Among the measured traits, NC and NDF had strong explanatory power: high NC represents high nutritional quality and has been shown to influence digestibility (Al Haj Khaled et al., 2006; Karn et al., 2006; Pontes et al., 2007; Lavorel and Grigulis, 2012) and decomposability (Pérez-Harguindeguy et al., 2000; Bakker et al., 2011; Dias et al., 2013); conversely, NDF is effective for anti-herbivore defence (Coley, 1988), affecting negatively both digestibility (Al Haj Khaled et al., 2006; Bumb et al., 2016) and decomposability (Cobo et al., 2002; Wardle et al., 2002; White et al., 2004). Digestibility was more strongly related to traits of living leaves (NC, PC and NDF) than decomposability, which was expected since digestibility is a property of living material. Changes in the properties of plant material during the senescence process (Supplementary Data Appendix S2) probably explain the weaker relationships with decomposability. Surprisingly, we also found that the decomposability of litter was more tightly related to the traits of living leaves (NDF, nitrogen and phosphorus concentrations) than to those of litter, which was unexpected. We currently do not have any convincing explanation for this, especially since NDF of litter would logically have a more direct effect on litter decomposition (Supplementary Data Appendix S2). A possible explanation for this may be that decomposition is affected by traits of living organs, as these traits control the phyllosphere/microbiota on organs and hence control, at least, the beginning of decomposition. Dry matter content as a functional marker of degradation processes Traits related to the morpho-anatomy of living organs, such as NDF and DMC, were tightly correlated and were good predictors of differences in digestibility and decomposability. Other studies further confirm the good association between NDF and DMC in a range of temperate grassland species (Al Haj Khaled et al., 2006; Pontes et al., 2007) (Fig. 6). However, in our analysis DMC of plant organs was excluded from the regression model used to assess the relative effects of the different traits on the two degradation processes studied, due to the collinearity between DMC and several other traits, including NDF. Fig. 6. View largeDownload slide Relationship between dry matter content and fibre concentration of (A) leaves – combination of data from this study (open circles) and from Al Haj Khaled et al. (2006) obtained for 15 grass species from temperate permanent grasslands grown under two nitrogen levels (solid circles) – and (B) stems (this study). The inset in (B) shows the relationship between dry matter content measured on leaves and fibre concentration measured on whole shoots for 14 grass species from temperate permanent grasslands grown under two nitrogen levels and cutting frequencies (Pontes et al. 2007). The number of data points (n) and the values of Pearson’s correlation coefficients (r) are given for each relationship. ***P < 0.001. Fig. 6. View largeDownload slide Relationship between dry matter content and fibre concentration of (A) leaves – combination of data from this study (open circles) and from Al Haj Khaled et al. (2006) obtained for 15 grass species from temperate permanent grasslands grown under two nitrogen levels (solid circles) – and (B) stems (this study). The inset in (B) shows the relationship between dry matter content measured on leaves and fibre concentration measured on whole shoots for 14 grass species from temperate permanent grasslands grown under two nitrogen levels and cutting frequencies (Pontes et al. 2007). The number of data points (n) and the values of Pearson’s correlation coefficients (r) are given for each relationship. ***P < 0.001. A high DMC of leaves indicates a high proportion of dense tissues (sclerenchyma and vascular bundles) in the leaf volume (Garnier and Laurent, 1994), which is probably the reason for the low digestibility and decomposability of such leaves. Leaf DMC has recurrently been found to relate to digestibility on the one hand (Al Haj Khaled et al., 2006; Pontes et al., 2007; Ansquer et al., 2009; Gardarin et al., 2014) and to decomposability on the other hand (Cornelissen et al., 2004; Kazakou et al., 2006), both at the species and the community level. Therefore, and even if NDF exerts a strong control on digestibility and decomposability, we suggest that DMC, which is far easier and quicker to determine, can safely be used as an efficient marker of both degradation processes. CONCLUSIONS The broad scope of this work allows us to demonstrate a strong positive relationship between digestibility and decomposability across species, organs and management regimes, thereby widening the generality of the afterlife effects hypothesis. Our findings provide further support for the key role played by foliar traits in the link between plant and soil via the decomposition pathway. Traits measured on living organs can be used to predict both digestibility and decomposability, and these two degradation processes are governed by similar traits describing the structural composition of organs, fibres in particular. We also demonstrated the importance of stems for nutrient and carbon cycling and thus ecosystem functioning. Finally, we showed that fertile habitats support high herbivory and cause positive feedbacks in such ecosystems because species typical of such habitats have high crude protein content, are more digestible and produce litter that decomposes faster. Infertile habitats support low herbivory and cause negative feedbacks because species typical of such infertile habitats have high amounts of structural carbohydrates and more persistent and less digestible organs, and produce recalcitrant litters with low decomposition. SUPPLEMENTARY DATA Supplementary data are available at https://academic.oup.com/aob and consist of the following. Supplementary Data Appendix S1: correlations between dry matter digestibility and decomposability with functional traits (dry matter, nitrogen, phosphorus, NDF and tannin contents) measured on green and litter material. Appendix S2: Spearman ranking coefficients between green and litter traits (for nitrogen and phosphorus concentrations, NDF and tannin concentration) measured on leaves and stems. An empty cell indicates that the correlation was not tested due to absence of measurements on green or litter plant material. Appendix S3: relationships between dry matter digestibility and (A) green NDF, (D) green DMC, (F) green nitrogen content and (I) green phosphorus content; between decomposability and (B) green NDF, (E) green DMC, (G) green nitrogen content and (J) green phosphorus content; and between decomposability and (C) litter NDF, (H) litter nitrogen content and (K) litter phosphorus content. The r values are Pearson or Spearman correlation coefficients for all data. Appendix S4: PCA between functional traits (NDF and dry matter, nitrogen, phosphorus and tannin concentrations) measured (A) on living leaves, (B) leaf litter, (C) living stems and (D) stem litter. ACKNOWLEDGEMENTS We thank J. Richarte for his help in the field and laboratory. All digestibility measurements were conducted in collaboration with D. Bastianelli, and with technical help from L. Bonnal and E. Baby (UMR SELMET, CIRAD of Montpellier). Chemical analyses were conducted at the Plateforme d’Analyses Chimiques en Ecologie (PACE) and the decomposition experiment was carried out in the Terrain d’Expériences (TE) facilities, both at the Centre d’Ecologie Fonctionnelle et Evolutive (CEFE-CNRS), Montpellier, France. J. Devaux helped prepare the microcosms and conduct the controlled chamber decomposition experiment. We thank the technical staff of the experimental station INRA La Fage for access to facilities. This work was funded by the EC2CO CASCADE (INSU CNRS) project. I.B. was supported by a doctoral fellowship from Montpellier Supagro. LITERATURE CITED Aerts R, Chapin FSIII. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. 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TI - Traits determining the digestibility–decomposability relationships in species from Mediterranean rangelands
JF - Annals of Botany
DO - 10.1093/aob/mcx175
DA - 2018-01-06
UR - https://www.deepdyve.com/lp/oxford-university-press/traits-determining-the-digestibility-decomposability-relationships-in-CUleBAC23V
SP - 459
EP - 469
VL - 121
IS - 3
DP - DeepDyve
ER -