Abstract
Herbivorous insect assemblages are functionally diverse, with each species exploiting plant tissues in different ways. Availability and palatability of plant tissues influence the diversity and composition of herbivorous insect assemblages. However, few studies have compared herbivorous insect assemblages and their ecological correlates across multiple plant species within the same plant community. Here, we sampled insect assemblages from the canopies of 1060 plants belonging to 36 woody species in two mixed Mediterranean forest stands. 401 insect species were classified as herbivores and grouped into sucker or chewer guilds. We explored differences in the diversity and composition of each insect guild across plant species, and tested their relationships with plant leaf traits, abundance or phylogeny, and explored whether the structures of plant-herbivorous insect networks depended on any of the studied plant traits. Plant identity accounted for the highest proportion of variation in the composition of each insect guild. Plant species abundance showed a positive effect on both insect guilds’ diversity. Suckers’ diversity was higher in plant species with deciduous leaves and low SLA, while the composition was more similar between phylogenetically closer plant species. Chewers diversity increased with the leaf area, while plants with similar LA, leaf nitrogen, SLA and distinct leaf habit showed more similar assemblages. Similarly, closely related angiosperms showed similar chewer assemblages. Plant–insect interaction networks present a modular structure, in which plants belonging to the same module tend to be related and share more sucker species. We add to the evidence supporting the role of plant species features as filters for structuring their associated herbivore insect assemblages.
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Introduction
Plants and herbivorous insects share a long history of coadaptation and coevolution with consequences on individual plant fitness, population-level processes, and community assembly (Coley et al. 1985; Crawley 1989; Agrawal 2007). Plants, to avoid or limit insect herbivory, have evolved physical (e.g. leaf indumenta, spines, tough leaves) and chemical (e.g. wax, resins, secondary metabolites or volatile compounds) traits acting as defensive, deterrent mechanisms or defensive mutualisms (Peeters 2002a, b; Peeters et al. 2007; Agrawal 2007; Clissold et al. 2009; Carmona et al. 2011; Pereira et al. 2020). Other plant traits, such as leaf phenology or leaf nutrient content, can control insect development, fecundity, and performance (Southwood et al. 2004; Wetzel et al. 2016; Barton et al. 2019). On their part, herbivorous insects have also developed multiple adaptations to feed on plant tissues of different qualities (War et al. 2018). Herbivorous insects can be grouped into feeding guilds, i.e. groups of species exploiting the same resources in a similar way (Simberloff and Dayan 1991), typically defined by the combination of one or various features as: feeding mode (e.g. sucking–piercing or chewing mouthparts), feeding habit (e.g. endophagous or exophagous), behavior (e.g. sessile or mobile) or developmental (e.g. larvae or adults) (Peeters 2002a, b; Southwood et al. 2004; Peeters et al. 2007; Novotny et al. 2010).
Plant-herbivorous insect interactions do not occur randomly, but are strongly determined by plants’ phenotypes (Ibanez et al 2016), i.e. interactions are functionally or phylogenetically conserved. Despite that, the richness and composition of plant-herbivorous insect assemblages vary widely within and between plant species (Basset and Novotny 1999; Southwood et al. 2004; Novotny et al. 2010; Wardhaugh 2014; Harrison et al. 2018; Rego et al. 2019; Tielens and Gruner 2020). Such variation has been frequently linked to the quality and quantity of resources offered by distinct plant species (Robinson et al. 2012; Harrison et al. 2018; Wang et al. 2020; Tielens and Gruner 2020; Lu et al. 2021; Keith et al. 2023), abundance effects (Cornell and Kahn 1989; Basset and Novotny 1999) or host plant phylogeny (Ødegaard et al. 2005; Grandez-Rios et al. 2015). However, most studies lack a community-level approach, focusing on one or few plant species and a particular insect guild or a single taxonomic group, what can limit our understanding of what determines the richness and composition of herbivorous insect assemblages associated with different plant species in a community, and how these associations translate into a network of plant-herbivorous insect interactions.
The quality and quantity of resources provided by plants are determinants of which kind of insect herbivores interact with a particular plant species. In general, herbivorous insects prefer young, tender and soft plant tissues of high nutritive quality (Clissold et al. 2009; Carmona et al. 2011), but this resource is temporary and spatially scarce (Barton et al. 2019). In turn, more available mature or perennial leaves may provide more abundant and stable resources and, consequently, could support richer insect communities. The effects of plant traits on insects probably depend on their feeding behaviors, physiology and ability to solve and manage direct and indirect plant-imposed barriers. As a result, each feeding guild can respond differently to the same plant traits (Basset and Novotny 1999; Peeters 2002a, b; Peeters et al. 2007; Novotny et al. 2010; Harrison et al. 2018; Caldwell et al. 2016; Tielens and Gruner 2020). Even, within the same feeding guild, species might react differently to plant traits, because of spatiotemporal partitioning of resources used by distinct insect species or because of different degrees of specialization (Novotny et al. 2010; Pimentel et al. 2023).
Several plant traits related to leaves quality and quantity have been found to be functional for herbivorous insect communities affecting their abundance, richness and composition. While biochemical traits are known to be poor predictors (Carmona et al. 2011; Harrison et al. 2018), leaf physical and nutritional-related traits seem to widely affect the richness and composition of herbivorous insect assemblages (Peeters 2002a, b; Dial et al. 2006; Robinson et al. 2012; Caldwell et al. 2016; Harrison et al. 2018; Tielens and Gruner 2020; Lu et al. 2021; Keith et al. 2023). According to the resource availability hypothesis (Coley et al. 1985), leaf size, palatability and nutritive value can be strong predictors of arthropod richness and composition (Basset and Novotny 1999; Peeters et al. 2007; Harrison et al. 2018; Tielens and Gruner 2020; Wang et al. 2020; Lu et al. 2021; Keith et al. 2023). For example, the richness and composition of chewers tends to correlated positively with leaf area, SLA and nitrogen content (Kagata and Ohgushi 2011; Peeters 2002a, b; Dial et al. 2006; Caldwell et al. 2016; Lu et al. 2021; Schön et al. 2023). This is explained because chewing insects ingest entire plant tissues, and are therefore more exposed to secondary and structural compounds (Clissold et al. 2009). While in the suckers’ guild, although would be expected a similar trend, evidences are contradictory, especially for the SLA and nitrogen content (Whitham 1978; Peeters 2002a, b; Dial et al. 2006; Caldwell et al. 2016; Lu et al. 2021). In the case of the suckers’ guild is assumed to be less constrained by structural or nutritional of leaf traits since they ingest fluids from different plant tissues, e.g. phloem, xylem or mesophyll cells (Peeters 2002a, b; Peeters et al. 2007; Caldwell et al. 2016). In addition, as expected by Root`s (1973) resource concentration hypothesis, abundant or dominant plant species that provide much of the vegetative tissues should support richer insect assemblages than rare plant species (Cornell and Kahn 1989; Basset and Novotny 1999; Southwood et al. 2004; Lewinsohn et al. 2005).
Plant phylogeny synthesizes the shared evolutionary history of a set of species, including multiple traits potentially affecting herbivorous insects (Kraft et al. 2007), many of which are not feasible to measure. To circumvent this limitation, phylogenetic distance has been used as a surrogate for trait dissimilarity and specialization (Ødegaard et al. 2005; Lewinsohn et al. 2005; Grandez-Rios et al. 2015). Because most traits are more or less evolutionarily conserved, trait dissimilarity is expected to increase with phylogenetic distance. If dissimilarity in functional traits between two plants involves extreme or unique combinations of traits, it may be difficult for herbivorous insects to exploit both (Hill and Kotanen 2009). This led to the prediction, that an increase in phylogenetic distance is associated with a high dissimilarity of herbivorous insect assemblages and a decrease in species richness hosted (taxonomic isolation hypothesis, Kennedy and Southwood 1984; Vialatte et al. 2010; Grandez-Rios et al. 2015).
Due to this tight ecological and evolutionary history, and in contrast with mutualistic networks that tend towards generalization, antagonistic plant-herbivorous insect interactions are more specialized and structured, with groups of species interacting intensively with each other, while maintaining few interactions with other groups (Lewinsohn et al. 2006; Cirtwill et al. 2020). Therefore, is expected that plant species with similar traits, i.e. traits with a functional role for herbivorous insects, or phylogenetically related tend to share partners and potentially structure the plant-herbivorous insect interaction networks (Ibanez et al. 2016; Cirtwill et al. 2020). Nevertheless, within antagonistic networks, the degree of specialization and modularity depends on the interacting guild, being highly specialized in the case of endophagous insects (galling insects), but less specialized in the case of free living (suckers and chewers) with sucker tending to be more specialized than chewers (Novotny et al. 2010; Oliveira et al. 2020). Also, variation in the proportion of generalist and specialist species within a guild might have effects on the structure and specialization of plant-herbivorous insect interaction networks (Araújo and Oliveira 2021).
The main goal of our study is to understand the differentiation of herbivorous insect assemblages across woody plant species of Mediterranean mixed forests. We hypothesize that, (1) given the interspecific differences among plant species in their trait profiles and abundances, their associated herbivorous insect communities should differ. In such case, (2) some specific plant features should be behind such differentiation, probably affecting differently to each guild. According to the different evolutionary history of plants and feeding mode of each guild (i.e. suckers and chewers), we expect for both guilds that (2.1) closely related plant species should show similar insect assemblages and (2.2) abundant plant species should have richer insect assemblages. Additionally, (2.3) suckers should be mainly affected by leaf quantity related traits; while, (2.4) chewers should be mainly affected by leaf quality and quantity. Finally, (3) such differentiation should influence the structure of plant–insect interaction networks.
Material and methods
Study sites and dominant plant species
This work was carried out in two Mediterranean pine-oak mixed forest communities of the south-eastern Iberian Peninsula: Sierra Sur de Jaén and Sierra de Segura (Jaén and Segura, hereafter). The study area at Jaén is characterized by mixed forests of Pinus halepensis, Quercus ilex, and Q. faginea while Segura is characterized by mixed forests of P. nigra subsp. salzmanii, Q. faginea, and Q. pyrenaica. Both areas have calcareous soils and Mediterranean climate. Jaén has a mean annual temperature of 14.1 °C, a mean annual rainfall of 715 mm, and a mean altitude of 1010 m, and Segura has a mean annual temperature of 11.6 °C, a mean annual rainfall of 890.5 mm, and a mean altitude of 1338 m. We chose for this study the dominant woody species (trees and shrubs) in each community: 22 species in Jaén and 14 species in Segura (Table S1).
Arthropod sampling and characterization of herbivorous insect assemblages
Arthropod communities are inherently variable at multiple scales. To address as many as possible sources of variation we sampled 36 plant species, with 26 to 31 individuals sampled per species, across two sites, over two seasons (spring and summer) and three consecutive years (2016–2018), which resulted in a total effort of 1060 samples (Table S1). In this way, we addressed the multiple sources of variation at spatial, inter-annual, intra-annual, between-species, and within-species. Arthropod sampling was carried out by the beating method. This is a standard method for sampling foliage and is frequently used to sample arthropods associated with the canopies of shrubs and trees (e.g. caterpillars, aphids, scale insects, other hemipterans, some beetles, and other plant-feeding or plant-dwelling arthropods (Montgomery et al. 2021).
Individual plants were sampled in the four cardinal directions using beating trays (40 cm × 50 cm or 20 cm × 30 cm depending to plant size) with soapy water to reduce the loss by escape of the collected arthropods (Ballare et al. 2019). Beating trays were placed under the canopy of the sampled individual and branches hitted until no more arthropods fell into the trays. Due to sampling plant species of contrasting canopy sizes, we adjusted the number of the trays to the sampled plant canopy to avoid sampling bias. In the case of trees, we sampled individuals which were able to beat completely from the lower to the upper canopy layer.
Samples were taken to the lab, where specimens were sorted under the stereomicroscope and identified to morphospecies or at the lower taxonomic level possible (specimens are preserved in 75% ethanol at the Department of Animal and Plant Biology and Ecology in the University of Jaén, Spain). Arthropod species were classified into trophic groups: phytophagous, zoophagous (including active predators, parasites, parasitoids, scavengers and sarcophagous), saprophagous, mycophagous and omnivorous. The trophic group was ascribed based on mouthparts and considering the available information at the species level or from close relatives (see Table S2).
Here, we focused on insects that feed on vegetative plant tissues. Pollinivores, nectarivores and florivores were excluded unless their larvae feed on vegetative plant tissues. Gall-forming insects also were excluded since our sampling was not properly designed for them. We classified phytophagous insects into feeding guilds (Table S2), according to whether their mouthparts are adapted to suck-pierce vascular fluids (external, mobile and sessile phloem, mesophyll or xylem suckers), suckers hereafter, or to chew plant tissues (external and internal chewers including boring and mining insects, and rostrum chewers), chewers hereafter.
Diversity of herbivorous insect assemblages
To estimate insect diversity of each guild, we used both rarefaction/extrapolation curves and Hill numbers, as a way to get more robust and meaningful comparisons (Chao et al. 2014; Roswell et al. 2021). Diversity indices were calculated from incidence data (0/1) to avoid abundance biases caused by differences in the gregarious behaviour between insect species (e.g. aphids vs. leafhoppers). Diversity was approximated by using Hill numbers, the computation was performed for three increasing values of the order parameter q, corresponding to increasing weight on the species relative abundances: q = 0, counts interacting species equally, irrespective of their relative abundances, correspond to richness; q = 1, counts interactions equally, thus representing species proportional to their frequency of interaction, correspond to the Hill-Shannon index; q = 2, exclusively pertains to the dominant interactions across the surveys, correspond to the Hill-Simpson index. While richness tends to be sensitive to rare species since it uses an arithmetic rarity scale. The Hill-Shannon index uses a logarithmic scale and the Hill-Simpson index uses a reciprocal scale which emphasizes the abundant species (Chao et al. 2014; Hsieh et al. 2016; Roswell et al. 2021).
To avoid estimation bias, plant species with extremely low number of recorded insects were excluded: Thymus mastichina and Daphne laureola, in the sucker guild, and Phillyrea angustifolia, P. latifolia, Phlomis purpurea, Pistacia lentiscus, P. terebinthus and Acer granatensis in the chewer guild.
Plant leaf traits and abundance
We used leaf plant traits frequently found to affect herbivorous insect assemblages. Namely, specific leaf area (SLA, mm2/mg) and leaf nitrogen content (LN, %) as measures of leaf quality; and leaf area (LA, mm2) as a proxy for resource quantity (Basset and Novotny 1999; Peeters 2002a, b; Harrison et al. 2018; Wang et al. 2020). In addition, we included the mean cover (m2) of each plant species at each site (evaluated through vegetation surveys), as a proxy for the resource concentration (Cornell and Kahn 1989; Basset and Novotny 1999). Leaf habit (evergreen vs. deciduous) was included as a life history trait related to plant phenology, with potential effects on insects’ development and degree of specialization (Southwood et al. 2004; Barton et al. 2019). In each site we choose 10 adult individuals per plant species for sampling leaf traits. We collected 5 healthy and mature leaves from each individual. These leaves were collected 2–3 h after sunrise and 3–4 h before the sunset, and were placed individually into plastic zip-bags. These bags were placed inside a portable fridge to avoid water loss. We used the average of the five collected leaves to estimate the leaf traits. Leaf area was measured by taking a picture of the leaves of each individual with a reference scale and processing with the image analysis software ImageJ (Abràmoff et al. 2004). To obtain the SLA, the leaf area was divided by the oven-dried mass. Leaf Nitrogen content was obtained from 0.2 g of homogenized oven-dried leaves for each sample, and analyzed on an automated CHNS elemental analyzer (Thermo Fisher). However, some species like Thymus mastichina or Juniperus oxycedrus show relatively small leaves, so several leaves were taken and weighted until a minimum of 2 gr of leaf fresh weight was reached, and leaf traits averaged by the number of leaves. It also should be noted that other species like Juniperus phoenicea or Ulex parviflorus present photosynthetic stems with small modified leaves, so we used 5 cm of the stem tip to calculate the traits. All the protocols followed for the measurement of functional traits follow Cornelissen et al. (2003), and are described in detail in Perea et al. (2021). Plant traits are available and described in detail in Perea et al. (2021). Since environmental conditions and soil properties are similar at both sites (Perea et al. 2021), we assumed that traits do not differ within species in these two communities (Zhao et al. 2022).
Plant phylogenetic relatedness metrics
To incorporate in the analyses phylogenetic information from plant species, we used an in situ time-calibrated barcoded phylogeny from the same study sites (Alcántara et al. 2019). Depending on the analysis nature, the phylogenetic information must be provided on a species or on a pairwise basis. Thus, the phylogenetic distance of a given plant species relative to a whole plant community was estimated using the “evolutionary distinctiveness” index (Isaac et al. 2007), which informs about how isolated or distant a species is within a given phylogeny. It was calculated using the evol.distinct function from the picante package in R (version 1.8.2) (Kembel et al. 2010). Pairwise distances were calculated using the cophenetic function from the vegan package in R (version 2.5–7) (Oksanen et al. 2022).
Data analysis
Differentiation of herbivorous insect assemblages across plant species
To explore the variation in herbivorous insect assemblages among plant species, we used the total β diversity based on the Sørensen index (Baselga 2010; Baselga et al. 2022). We used the matrices of insect presence-absence separately for each site (Jaén and Segura) and feeding guild (suckers and chewers).
Differences in β diversity of insect assemblages were tested by means of PERMANOVA (Anderson 2001), including as factors, plant species identity, and also sampling year and month, to account for a possible temporal variation across samplings. To estimate p values, we run 999 permutations randomizing individuals only between samples taken on the same date. β diversity matrices were computed using the betapart package in R (version 1.5.4) (Baselga et al. 2022).
Plant traits and diversity of herbivorous insect assemblages
To test for the effect of plant traits on the diversity of herbivorous insect communities, we fitted a generalized linear model separately for each insect’s guild and diversity index. All diversity estimates (i.e. q0, q1, q2) were modelled with Gaussian family distribution, while q1 for the chewers guild was modeled with tweedie family distribution. The model included, as a dependent variable, each diversity index per plant species, and, as explanatory variables, leaf area (LA), specific leaf area (SLA), leaf nitrogen content (LN), mean plant cover, plant evolutionary distinctiveness, and site (Jaén and Segura). All models were checked for residuals diagnostics.
Plant traits and composition of herbivorous insect assemblages
To test whether plant species differences in the composition of their associated insect assemblages were related to plant differences in ecological and functional leaf traits, and/or phylogenetic distances, we fitted a generalized linear mixed model separately for each feeding guild.
Betadiversity was modelled with Beta family distribution (suckers) and Gamma family distribution (chewers). All models were checked for residuals diagnostics.
Pairwise β diversity was estimated from a plant–insect matrix of the mean incidence of insect species among samples. β diversity was calculated based on the Bray–Curtis index using the betapart package in R (version 1.5.4) (Baselga et al. 2022). Distances for each plant trait were calculated using Gower distance (Gower 1971) using the FD package in R (version 1.0–12) (Laliberté and Legendre 2010). This metric yields a standardized distance between 0 and 1, which is recommended because it facilitates interpretations of dissimilarity and allows comparisons between traits with different units (de Bello et al. 2021).
The model included, as a dependent variable, the pairwise β diversity. As explanatory variables: Gower distances in leaf area (LA), specific leaf area (SLA), leaf Nitrogen content (LN), and mean plant cover, similarity in leaf habit (same (0) or different (1)), phylogenetic distances (squared-root transformed) and site (Jaén and Segura). Since every plant species appears in multiple pairwise distances with all other species, data from those pairs sharing plant species are not independent. To account for this non-independence, we included two random factors coding the identity of each species in a pair, considering their site provenance. To control for phylogenetic autocorrelation, we included in our models the squared-root of the phylogenetic distances as a covariable. However, the correlation between betadiversity and phylogenetic distances can be mainly driven by the differences between gymnosperms and angiosperms (for example, see Brändle and Brandl 2006). Therefore, we analysed also our data including only distances within angiosperms.
Plant traits and structure of plant–insect interaction networks
We explored whether plant ecological and functional leaf traits, and phylogenetic relatedness can leave an imprint on the structure of plant-herbivorous insect interaction networks. Thus, we built a weighted bipartite network for each site and feeding guild using bipartite package in R (version 2.17) (Dormann et al. 2008). Modularity was assessed with the meta Compute Modules function of the bipartite package in R (version 2.17) (Dormann et al. 2008) with the Beckett algorithm (Beckett 2016). To test for modularity significance, we used 999 permutations of a non-sequential algorithm for quantitative matrices that preserves column sums and cells within each column are shuffled, using the c0_samp option of the nullmaker function of the metacom package in R (version 1.5.3) (Dallas 2014).
Once the plant–insect networks were built and their modularity calculated, we tested the influence of plant ecological and functional leaf traits, and phylogenetic distances on the belonging of each plant species pairs to the same or different module. For that, we used as a dependent variable, a binary variable coding whether two plant species belonged to the same or different module (0 and 1, respectively). Leaf functional traits and mean plant cover dissimilarities (i.e. Gower distances as in the previous section), leaf habit similarity (same (0) or different (1)), phylogenetic distances (squared-root transformed) and site (Jaén and Segura) were included as explanatory variables. We used generalized linear mixed model with binomial family distribution, and included the identity of both plant species in the pair as a random factor.
All analyses were performed in R (R Core Team 2021). PERMANOVAs were run using the vegan package in R (version 2.5–7) (Oksanen et al. 2022). Models were performed using the glmmTMB package (version 1.1.2.3) (Brooks et al. 2017). Model residuals diagnostics were checked with the DHARMa package (version 0.4.5) (Hartig 2022). Model predictions were evaluated with the ggeffects package (version 1.1.1) (Lüdecke 2018) and the stats package (R Core Team 2021). All graphics were done with ggplot2 package (version 3.3.5) (Wickham 2016).
Results
A total of 6635 individual arthropod specimens were collected, of which 2176 were classified as herbivorous insects and involved 401 species. The taxonomic composition was dominated by Hemiptera (66.33%) followed by Coleoptera (20.45%), Diptera (4.49%), Orthoptera (4.74%), Hymenoptera (2.00%), Lepidoptera (1.50%) and Phasmatodea (0.50%) (Fig. 1, see Table S2). Regarding feeding guilds, suckers represented 66.33% (all Hemipterans), while chewers represented 33.67%, mainly including exophagous species from Coleoptera, Orthoptera and Phasmatodea (76.3%), and some species from Diptera, Hymenoptera and Lepidoptera whose larvae feed on plant tissues (23.7%).
Differentiation of herbivorous insect assemblages across plant species
Plant species differed in their associated herbivorous insect assemblages, accounting significantly for the largest proportion of variation in each insect feeding guild. In the case of sucker insects, plant identity explained 19.30% of the variation in Jaén, and 15.60% in Segura (Table 1). In the case of chewer insects, plant identity explained 17.54% of the variation in Jaén, and 8.13% in Segura (Table 1). The explained variation by plant species identity was much more than that explained by year or month (Table 1).
Plant traits and diversity of herbivorous insect assemblages
Regarding suckers’ guild, both the Hill-Shannon and Hill-Simpson diversity indexes indicated that plants with low SLA and deciduous leaves hosted more diverse sucker assemblages, in terms of common and dominant insect species, respectively (Table 2; Fig. 2). In the chewers’ guild, the Hill-Simpson index (that takes into account dominant species) indicated that plants with large leaf areas can support more diverse assemblages and mainly composed by dominant chewer species (Table 3; Fig. 3). In addition, independently of the estimator considered, mean plant cover showed a general significant positive relationship with the diversity of sucking and chewing insects (Tables 2, 3; Figs. 2, 3). Evolutionary distinctiveness did not show any effects on herbivorous insect diversity.
Plant traits and composition of herbivorous insect assemblages
Plant traits did not show any effect on the variation in composition of suckers’ assemblages. Phylogenetic distance revealed that closely related plants hosted more similar suckers’ assemblages (Table 4, Fig. 4a). This relationship was held when we analysed exclusively distances between angiosperms (Table S1, Fig. 4b). Regarding chewers, the dissimilarity of their assemblages between plant species pairs was higher in Jaén than in Segura. We showed that betadiversity of chewing insect assemblages (dissimilarity) increases with differences in plant leaf traits. That is, plants with similar leaf functional traits, i.e. leaf area, SLA and nitrogen content, tend to host similar chewing insect assemblages (Table 4, Fig. 5a–c). However, when we analysed the chewing insect associated exclusively to angiosperm species, we showed that betadiversity increases with differences in leaf area and phylogenetic distances (Table 4, Fig. 5d, f). By contrast, betadiversity was higher in plant species with the same leaf habit (Fig. 5e). That is, angiosperm species with similar leaf area, phylogenetically close and with different leaf habit tend to show similar chewing insect assemblages.
Plant traits and structure of plant-herbivorous insect interaction networks
Interaction networks showed a modular structure for both feeding guilds (Fig. S1-2): plant-sucker insect networks were composed by 12 modules in Jaén (modularity score = 0.47, p < 0.01) and 9 in Segura (modularity score = 0.47, p < 0.01). On the other hand, plant-chewer insect networks consisted of 12 modules in Jaén (modularity score = 0.46, p < 0.05) and 8 in Segura (modularity score = 0.35, p < 0.05).
GLMMs performed to assess the relationships of plant leaf traits, abundance and phylogenetic distance with the modular structure of plant-herbivorous insect networks found significant influences of plant phylogenetic distances on the probability of two plant species belong to the same module (Table 5, Fig. 6). Plant species from the same modules tended to be phylogenetically closer. In contrast, GLMMs did not detect any traits related to the modular structure of the plant-chewer network (Table 5).
Discussion
Herbivorous insect assemblages are highly diverse and variable across multiple scales (Southwood et al. 2004; Lewinsohn et al. 2005; Wardhaugh 2014). To understand how this variability is structured within local plant communities, we identified plant features acting as potential biotic filters for regional herbivorous insect pools and explored their effects on plant-herbivorous insect interaction networks. In the present study, herbivorous insect assemblages were much more variable at fine than at large spatial and temporal scales, and a relevant part of their variability could be attributed to host plant species.
Variability of insect assemblages between samples mostly reflects small-scale spatial variation among samples taken throughout the study sites, since temporal variation explained a very small fraction of the variance. Despite the wide variability of herbivorous insect assemblages among samples, those taken from the same plant species tended to be more similar than those taken from different species. These results concur with many other studies reporting distinct plant species to harbour different associated herbivorous insect assemblages (Cornell and Kahn 1989; Basset and Novotny 1999; Peeters 2002a, b; Peeters et al. 2007; Southwood et al. 2004, 2005; Lewinsohn et al. 2005; Rego et al. 2019). Such differentiation can reflect the effect of plant traits and evolutionary features. For example, variation in herbivorous insect composition has been found to be mainly related to traits that directly or indirectly reduce herbivory, such as leaf toughness, leaf indumenta, SLA, leaf nitrogen content or leaf area (Lawton and Price 1979; Peeters 2002a, b; Peeters et al. 2007; Hanley et al. 2007; Clissold et al. 2009; Carmona et al. 2011). Moreover, there is increasing evidence that certain insect guilds vary between and within plant species depending on their ecological and functional traits. For example, suckers are negatively related to leaf water content and positively related to leaf nitrogen content (in Australian species Peeters 2002a, b; Lewinsohn et al. 2005; or within Metrosideros polymorpha Tielens and Gruner 2020); while chewers are positively related to leaf area or leaf nitrogen content and negatively by the leaf indumenta (in Australian species Peeters 2002a, b; Lewinsohn et al. 2005; or within Metrosideros polymorpha Tielens and Gruner 2020).
Plant traits and diversity of herbivore insect assemblages
The diversity of sucker and chewer assemblages was related to different plant features. In the sucker guild, diversity decreased with SLA and was lower in evergreen than in deciduous plants. On the one hand, species with low SLA (e.g. Juniperus phoenicea, J. communis, Pinus halepensis, P. nigra or Quercus ilex), that is, strong and tough leaves, supported more diverse sucker assemblages than plants with soft and thin leaves, high SLA (e.g. Sorbus torminalis, Berberis hispanica, Daphne gnidium or Cistus albidus). A similar trend was found by Caldwell et al. (2016), who showed that the density of sucker species was negatively correlated with the specific leaf area (i.e. SLA), although others have found the opposite trend (Peeters 2002a, b a, b; Peeters et al. 2007; Lu et al. 2021). On the other hand, deciduous plants (e.g. Pistacia terebinthus, Quercus_faginea, Crataegus monogyna or Rosa spp.) supported more diverse sucker assemblages than perennials (e.g. Cistus albidus, Phillyrea spp. or Phlomis purpurea). This result is supported by studies on different tree species from the British islands (Cornell and Kahn 1989) and for Quercus species (Southwood et al. 2004, 2005) where deciduous species supported higher diversity of sucker species. Jointly, these traits can be interpreted as mechanical and temporal constraints to the sucker guild. First, plants with tough and thick leaves with large lifespan can provide more resistance and for longer times to damage by suckers, which only need to pierce the cuticle; but also provide resources for long time, and, in this way, they could support more diverse assemblages along seasons (Peeters 2002a, b; Peeters et al. 2007; Hanley et al. 2007; Caldwell et al. 2016). Indeed, the feeding behaviour of suckers (e.g. the use of enzymatic secretions to facilitate penetration, the reuse of stylet tracks or the use of stomata to penetrate) do not remove leaf tissues, therefore, it would be less harmful and costly in species with low SLA leaves (Peeters et al. 2007; Hanley et al. 2007; Caldwell et al. 2016). Second, deciduous species can have high photosynthetic rates during bud break resulting in a faster translocation of sap, and probably more nutritive, which may make new and young tissues or growing meristems more attractive for suckers (Coley 1983; Peeters 2002a, b; Peeters et al. 2007; Barton et al. 2019). Besides, like plants, sucker life cycles show seasonality and synchrony with the development of new plant structures (Awmack and Leather 2002; Southwood et al. 2004; Barton et al. 2019).
In turn, in the chewer guild, plants providing large leaves (e.g. S. torminalis or Q. pyrenaica) harboured more diverse chewer assemblages than those with small leaves (e.g. Genista cinerea, D. gnidium, Juniperus spp. or Thymus mastichina), as expected by the resource availability hypothesis (Coley 1983; Coley et al. 1985). Other authors also reported similar trends; for example, in the Australian flora, Peeters (2002a, b) and Peeters et al. (2007) found densities of total chewer species positively related to leaf area. While, in the British flora, Umbellifera species (Lawton and Price 1979) and trees (Moran and Southwood 1982; Kennedy and Southwood 1984) with large leaf areas and less divided supported more diverse insect communities.
The diversity of both insect guilds was positively affected by mean plant cover, as expected by the resource concentration hypothesis (Root 1973). Species providing most of the resources in our community (e.g. P. halepensis, P. nigra, Q. ilex, Q. faginea or Q. pyrenaica) supported richer and more diverse herbivorous insect assemblages. Similar results have been reported for the British arboreal insects, where sucker and chewer richness increased with host abundance (Cornell and Kahn 1989; Kelly and Southwood 1999) or for sucker assemblages on Ficus species (Basset and Novotny 1999). Besides, some of the more abundant species co-occur with phylogenetically close relatives which would facilitate host shifts by insects, especially for specialist insects (Hill and Kotanen 2009; Vialatte et al. 2010). At the same time, the fact that some of the most abundant species are gymnosperms (e.g. P. halepensis or P. nigra), which are phylogenetically distant with respect to the rest of co-occurring plant species, may explain the lack of a phylogenetic effect on the richness and diversity of each assemblage.
Plant traits, assemblage composition and interaction network structure
We found that insect assemblages were more different with increasing functional or phylogenetic distances between co-occurring plant species (Lewinsohn et al. 2005; Ødegaard et al. 2005; Grandez-Rios et al. 2015). In the sucker guild, variation in composition was related to phylogenetic distance between pairs of plant species. Moreover, the analysis of the interaction network structure reveals a clustering of plant species into modules with similar sucker assemblage composition, and that this clustering also reflects the signal of the phylogenetic distance between plants. By contrast, the variation in the composition of chewers was related to resource availability-palatability leaf traits (LA, LN and SLA) when consider angiosperms and gymnosperms together. However, when consider only angiosperm pairs, chewer’s composition was related to the LA and leaf habit, both traits related to resource availability, and the phylogenetic distance. The phylogenetic distance effect may be indicating two non-mutually exclusive processes contributing to the assembly of both herbivorous insect guilds. On the one hand, it seems likely that phylogenetically conserved traits not included in this study (e.g. leaf indumenta, spines, waxes, resins, secondary metabolites or volatile compounds) are contributing to the assembly of the studied communities (Ødegaard et al. 2005; Kraft et al. 2007; Ibanez et al. 2016). On the other hand, it is also possible that the evolution of sucker and chewer lineages has occurred in concert with the diversification of plant lineages (Agrawal 2007; Lewinsohn et al. 2005). Plant functional traits seems to be important for chewers, species with similar LA, SLA, LN showed more similar assemblages of chewers. For example, Wang et al. (2020) found that the composition of Lepidopteran caterpillars was affected by SLA; while Tielsen and Gruner (2020) and Whitfeld et al. (2012) found positive effects of LN on the abundance of chewers species (including caterpillars and leaf miners); and Pitteloud et al. (2020) found a relationship between Orthopteran species composition and changes in SLA and LDMC. Indeed, chewer insects, unlike suckers, tend to consume whole leaves and are directly exposed to leaf material secondary compounds and toxins. Therefore, variation in some of these traits could represent filters to the composition of chewers. However, despite the clustering of host species into modules with similar chewer composition, such interaction structure was not related to any of the studied plant traits. These results can reflect the heterogeneous composition of our chewer guild, which includes several Orders of insects, and also the more generalist feeding behaviour of chewers in comparison with suckers (Ødegaard et al. 2005; Novotny et al. 2010; Oliveira et al. 2020). Alternatively, other traits correlated with the SLA, LA, LN or deciduousness can be involved in the patterns detected here for the diversity and composition. For example, SLA is positively related to photosynthetic rates (Reich et al. 1991; Wright et al. 2001) and relative growth rates (Poorter and Remkes 1990), and negatively with leaf life span (Reich et al. 1991). Besides, the reduction in SLA is accompanied by an increase in lignin and fibres, and consequently, a dilution of leaf nitrogen content (Clissold et al. 2009). In addition, other plant features such as size and branch density patterns (Lawton 1983) or symbiosis with mycorrhizas (Koricheva et al. 2009) and N-fixing organisms (Lewinsohn et al. 2005) can be involved.
Conclusions
Based on a wide sampling of herbivore insect communities associated with the most important woody species dominating Mediterranean mixed forests, we show that the diversity and compositional variation of sucker and chewer insect assemblages are strongly determined by plant species identity and are structured by plant features that act as biotic filters of the insect species pool. The effects of such plant features vary with respect to the guild considered, so they are guild-specific. The sucker’s assemblage was affected by the SLA, leaf habit and plant abundance, while chewers were affected by the SLA, LA, LN and plant abundance. The effect of plant phylogenetic distance only was important for the sucker guild. Both plant-sucker and plant-chewer interaction networks showed a modular structure. Plant-sucker network modularity is related to plant phylogenetic distance, where more closely related plants tend to share more suckers with each other, than with distantly related plants from different modules. Exploring the causes and consequences of plant features over their associated—herbivore insect assemblages within local plant communities may provide insights to understand their role in multiple community processes and ecological functions.
Data availability
The data are publicly available in Zenodo https://doi.org/https://doi.org/10.5281/zenodo.10611074
References
Abràmoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11(7):36–42
Agrawal AA (2007) Macroevolution of plant defense strategies. Trends Ecol Evol 22:103–109
Alcántara JM, Garrido JL, Rey PJ (2019) Plant species abundance and phylogeny explain the structure of recruitment networks. New Phytol 223(1):366–376. https://doi.org/10.1111/nph.15774
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. https://doi.org/10.1146/annurev.ento.47.091201.145300
Ballare KM, Pope NS, Castilla AR, Cusser S, Metz RP, Jha S (2019) Utilizing field collected insects for next generating sequencing: effects of sampling, storage, and DNA extraction methods. Ecol Evol 9:13690–13705. https://doi.org/10.1002/ece3.5756
Barton KE, Edwards KF, Koricheva J (2019) Shifts in woody plant defence syndromes during leaf development. Func Ecol 33(11):2095–2104. https://doi.org/10.1111/1365-2435.13435
Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Global Ecol Biogeogr 19(1):134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x
Baselga A, Orme D, Villeger S, De Bortoli J, Leprieur F, Logez M (2022) Betapart: partitioning beta diversity into turnover and nestedness components. R package version 1.5.6. https://CRAN.R-project.org/package=betapart
Basset Y, Novotny V (1999) Species richness of insect herbivore communities on Ficus in Papua New Guinea. Biol J Linn Soc 67(4):477–499
Beckett SJ (2016) Improved community detection in weighted bipartite networks. Roy Soc Open Sci 3:140536. https://doi.org/10.1098/rsos.140536
Brändle M, Brandl R (2006) Is the composition of phytophagous insects and parasitic fungi among trees predictable? Oikos 113(2):296–304. https://doi.org/10.1111/j.2006.0030-1299.14418.x
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9(2):378–400
Caldwell E, Read J, Sanson GD (2016) Which leaf mechanical traits correlate with insect herbivory among feeding guilds? Ann Bot 117(2):349–361. https://doi.org/10.1093/aob/mcv178
Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367. https://doi.org/10.1111/j.1365-2435.2010.01794.x
Chao A, Gotelli N, Hsieh T, Sander E, Ma K, Colwell R, Ellison AM (2014) Rarefaction and extrapolation with hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84(1):45–67. https://doi.org/10.1890/13-0133.1
Cirtwill AR, Dalla Riva GV, Baker NJ, Ohlsson M, Norström I, Wohlfarth IM, Tia JA, Stouffer DB (2020) Related plants tend to share pollinators and herbivores, but strength of phylogenetic signal varies among plant families. New Phytol 226(3):909–920. https://doi.org/10.1111/nph.16420
Clissold FJ, Sanson GD, Read J, Simpson SJ (2009) Gross vs. net income: How plant toughness affects performance of an insect herbivore. Ecology 90:3393–3405. https://doi.org/10.1890/09-0130.1
Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53(2):209–234. https://doi.org/10.2307/1942495
Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230(4728):895–899. https://doi.org/10.1126/science.230.4728.895
Cornelissen JH, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE et al (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51(4):335–380
Cornell HV, Kahn DM (1989) Guild structure in the British arboreal arthropods: is it stable and predictable? J Anim Ecol. https://doi.org/10.2307/5138
Crawley MJ (1989) Insect herbivores and plant population dynamics. Annu Rev Entomol 34(1):531–562. https://doi.org/10.1146/annurev.en.34.010189.002531
Dallas T (2014) metacom: an R package for the analysis of metacommunity structure. Ecography. https://doi.org/10.1111/j.1600-0587.2013.00695.x
de Araújo WS, Oliveira JB (2021) Plant–herbivore assemblages composed of endophagous and exophagous insects have different patterns of diversity and specialization in Brazilian savannas. Biotropica 53(4):1013–1020
de Bello F, Carmona CP, Dias ATC, Götzenberger L, Moretti M, Berg MP (2021) Handbook of Trait-Based Ecology From Theory to R Tools. Cambridge University Press, Cambridge. https://doi.org/10.1017/9781108628426
Dial RJ, Ellwood MDF, Turner EC, Foster WA (2006) Arthropod abundance, canopy structure, and microclimate in a Bornean lowland tropical rain forest. Biotropica 38:643–652
Dormann CF, Gruber B, Fruend J (2008) Introducing the bipartite package: analysing ecological networks. R News 8(2):8–11
Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27(4):857–871. https://doi.org/10.2307/2528823
Grandez-Rios JM, Lima Bergamini L, Santos de Araújo W, Villalobos F, Almeida-Neto M (2015) The effect of host-plant phylogenetic isolation on species richness, composition and specialization of insect herbivores: a comparison between native and exotic hosts. PLoS ONE 10(9):e0138031. https://doi.org/10.1371/journal.pone.0138031
Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect. Plant Ecol Evol Syst 8(4):157–178. https://doi.org/10.1016/j.ppees.2007.01.001
Harrison JG, Philbin CS, Gompert Z, Forister GW, Hernandez-Espinoza L, Sullivan BW, Forister ML (2018) Deconstruction of a plant-arthropod community reveals influential plant traits with nonlinear effects on arthropod assemblages. Func. Ecol. 32(5):1317–1328. https://doi.org/10.1111/1365-2435.13060
Hartig F (2022) DHARMa: residual diagnostics for hierarchical (Multi-Level/Mixed) regression models. R package version 0.4.5 https://CRAN.R-project.org/package=DHARMa
Hill SB, Kotanen PM (2009) Evidence that phylogenetically novel non-indigenous plants experience less herbivory. Oecologia 161:581–590. https://doi.org/10.1007/s00442-009-1403-0
Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7(12):1451–1456. https://doi.org/10.1111/2041-210X.12613
Ibanez S, Arène F, Lavergne S (2016) How phylogeny shapes the taxonomic and functional structure of plant—insect networks. Oecologia 180(4):989–1000. https://doi.org/10.1007/s00442-016-3552-2
Isaac NJB, Turvey ST, Collen B, Waterman C, Baillie JEM (2007) Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS ONE 2:e296. https://doi.org/10.1371/journal.pone.0000296
Kagata H, Ohgushi T (2011) Ecosystem consequences of selective feeding of an insect herbivore: palatability–decomposability relationship revisited. Ecol Entomol 36(6):768–775
Keith AR, Bailey JK, Whitham TG (2023) Assisted migration experiments along a distance/elevation gradient show limits to supporting home site communities. PLOS Clim 2(5):e0000137
Kelly CK, Southwood TRE (1999) Species richness and resource availability: a phylogenetic analysis of insects associated with trees. P Natl Acad Sci 96(14):8013–8016. https://doi.org/10.1073/pnas.96.14.801
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26(11):1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Kennedy CEJ, Southwood TRE (1984) The number of species of insects associated with British trees: a re-analysis. J Anim Ecol 455–478:1984. https://doi.org/10.2307/4528
Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90(8):2088–2097. https://doi.org/10.1890/08-1555.1
Kraft NJB, Cornwell WK, Webb CO, Ackerly DD (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170:271–283. https://doi.org/10.1086/519400
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1
Lawton JH (1983) Plant architecture and the diversity of phytophagous insects. Annu Rev Entomol 28(1):23–39. https://doi.org/10.1146/annurev.en.28.010183.000323
Lawton JH, Price PW (1979) Species richness of parasites on hosts: agromyzid flies on the British Umbelliferae. J Anim Ecol. https://doi.org/10.2307/4183
Lewinsohn TM, Novotny V, Basset Y (2005) Insects on plants: diversity of herbivore assemblages revisited. Annu Rev Ecol Evol S. https://doi.org/10.1146/annurev.ecolsys.36.091704.175520
Lewinsohn TM, Prado PI, Jordano P, Bascompte J, Olesen JM (2006) Structure in plant—animal interaction assemblages. Oikos 113(1):174–184. https://doi.org/10.1111/j.0030-1299.2006.14583.x
Lu X, Zhao X, Tachibana T, Uchida K, Sasaki T, Bai Y (2021) Plant quantity and quality regulate the diversity of arthropod communities in a semi-arid grassland. Funct Ecol 35(3):601–613
Lüdecke D (2018) Ggeffects: tidy data frames of marginal effects from regression models. J Open Sour Softw 3(26):772. https://doi.org/10.21105/joss.00772
Montgomery GA, Belitz MW, Guralnick RP, Tingley MW (2021) Standards and best practices for monitoring and benchmarking insects. Front Ecol Evol. https://doi.org/10.3389/fevo.2020.579193
Moran VC, Southwood TRE (1982) The guild composition of arthropod communities in trees. J Anim Ecol. https://doi.org/10.2307/4325
Novotny V, Miller SE, Baje L, Balagawi S, Basset Y, Cizek L, Craft KJ, Dem F, Drew RAI, Hulcr J, Leps J, Lewis OT, Pokon R, Stewart AJA, Allan Samuelson G, Weiblen GD (2010) Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. J Anim Ecol 79(6):1193–1203. https://doi.org/10.1111/j.1365-2656.2010.01728.x
Ødegaard F, Diserud OH, Østbye K (2005) The importance of plant relatedness for host utilization among phytophagous insects. Ecol Lett 8(6):612–617. https://doi.org/10.1111/j.1461-0248.2005.00758.x
Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB et al.: Vegan: community ecology package (2022) R package version 2.6-2. https://CRAN.Rproject.org/package=vegan.
Oliveira JBBS, Faria ML, Borges MA, Fagundes M, de Araújo WS (2020) Comparing the plant—herbivore network topology of different insect guilds in Neotropical savannas. Ecol Entomol 45(3):406–415. https://doi.org/10.1111/een.12808
Peeters PJ (2002a) Correlations between leaf constituent levels and the densities of herbivorous insect guilds in an Australian forest. Austral Ecol 27(6):658–671. https://doi.org/10.1046/j.1442-9993.2002.01227.x
Peeters PJ (2002b) Correlations between leaf structural traits and the densities of herbivorous insect guilds. Biol J Linn Soc 77(1):43–65. https://doi.org/10.1046/j.1095-8312.2002.00091.x
Peeters PJ, Sanson G, Read J (2007) Leaf biomechanical properties and the densities of herbivorous insect guilds. Funct Ecol. https://doi.org/10.1111/j.1365-2435.2006.01223.x
Perea AJ, Garrido JL, Alcántara JM (2021) Plant functional traits involved in the assembly of canopy—recruit interactions. J Veg Sci 32(1):e12991. https://doi.org/10.1111/jvs.12991
Pereira CC, Boaventura MG, De Castro GC, Cornelissen T (2020) Are extrafloral nectaries efficient against herbivores? Herbivory and plant defenses in contrasting tropical species. J Plant Ecol 13:423–430. https://doi.org/10.1093/jpe/rtaa029
Pimentel CS, Firmino PN, Almeida RP, Lombardero MJ, Ayres MP, Calvão T (2023) Coexistence of insect species in a phloem feeding guild: deterministic and stochastic processes. Ecol Entomol 48(6):658–668. https://doi.org/10.1111/een.13263
Pitteloud C, Descombes P, Sànchez-Moreno S, Kergunteuil A, Ibanez S, Rasmann S, Pellissier L (2020) Contrasting responses of above-and below-ground herbivore communities along elevation. Oecologia 194(3):515–528. https://doi.org/10.1007/s00442-020-04778-7
Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83:553–559. https://doi.org/10.1007/BF00317209
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
Rego C, Boieiro M, Rigal F, Ribeiro SP, Cardoso P, Borges PA (2019) Taxonomic and functional diversity of insect herbivore assemblages associated with the canopy-dominant trees of the Azorean native forest. PLoS ONE 14(7):e0219493
Reich PB, Uhl C, Walters MB, Ellsworth DS (1991) Leaf lifespan as a determinant of leaf structure and function among 23 Amazonian tree species. Oecologia 86:16–24
Robinson KM, Ingvarsson PK, Jansson S, Albrectsen BR (2012) Genetic variation in functional traits influences arthropod community composition in aspen (Populus tremula L.). PLoS ONE 7(5):e37679
Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica Oleracea). Ecol Monogr 43(95–124):1973. https://doi.org/10.2307/1942161
Roswell M, Dushoff J, Winfree R (2021) A conceptual guide to measuring species diversity. Oikos 130(3):321–338. https://doi.org/10.1111/oik.07202
Schön JE, Tiede Y, Becker M, Donoso DA, Homeier J, Limberger O et al (2023) Effects of leaf traits of tropical trees on the abundance and body mass of herbivorous arthropod communities. PLoS ONE 18(11):e0288276. https://doi.org/10.1371/journal.pone.0288276
Simberloff D, Dayan T (1991) The guild concept and the structure of ecological communities. Annu Rev Ecol Syst 22:115–143. https://doi.org/10.1146/annurev.es.22.110191.000555
Southwood TRE, Wint GW, Kennedy CE, Greenwood SR (2004) Seasonality abundance, species richness and specificity of the phytophagous guild of insects on oak (Quercus) canopies. Eur J Entomol 101(1):43–50
Southwood TRE, Wint GW, Kennedy CE, Greenwood SR (2005) The composition of the arthropod fauna of the canopies of some species of oak (Quercus). Eur J Entomol 102(1):65–72. https://doi.org/10.14411/eje.2005.009
Tielens EK, Gruner DS (2020) Intraspecific variation in host plant traits mediates taxonomic and functional composition of local insect herbivore communities. Ecol Entomol 45(6):1382–1395. https://doi.org/10.1111/een.12923
Vialatte A, Bailey RI, Vasseur C, Matocq A, Gossner MM, Everhart D et al (2010) Phylogenetic isolation of host trees affects assembly of local Heteroptera communities. Proc R Soc B Biol Sciences 277:2227–2236. https://doi.org/10.1098/rspb.2010.0365
Wang MQ, Li YI, Chesters D, Bruelheide H, Ma K, Guo PF, Schuldt A (2020) Host functional and phylogenetic composition rather than host diversity structure plant—herbivore networks. Mol Ecol 29(14):2747–2762. https://doi.org/10.1111/mec.15518
War AR, Taggar GK, Hussain B, Taggar MS, Nair RM, Sharma HC (2018) Plant defence against herbivory and insect adaptations. AoB Plants 10:1–19. https://doi.org/10.1093/aobpla/ply037
Wardhaugh CW (2014) The spatial and temporal distributions of arthropods in forest canopies: uniting disparate patterns with hypotheses for specialisation. Biol Rev 89(4):1021–1041. https://doi.org/10.1111/brv.12094
Wetzel WC, Kharouba HM, Robinson M, Holyoak M, Karban R (2016) Variability in plant nutrients reduces insect herbivore performance. Nature 539:425–427. https://doi.org/10.1038/nature20140
Whitfeld TJS, Kress WJ, Erickson DL, Weiblen GD (2012) Change in community phylogenetic structure during tropical forest succession: evidence from New Guinea. Ecography 35(9):821–830. https://doi.org/10.1111/j.1600-0587.2011.07181.x
Whitham TG (1978) Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 6:1164–1176
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Func Ecol 15:423–434. https://doi.org/10.1046/j.0269-8463.2001.00542.x
Zhao N, Yu G, Wang Q, Wang R, Zhang J, Liu C, He N (2022) Conservative allocation strategy of multiple nutrients among major plant organs: From species to community. J Ecol 108(1):267–278. https://doi.org/10.1111/1365-2745.13256
Acknowledgements
JMB was supported by FEDER SUMHAL-Sustainability for Mediterraean Hospost in Andalusia integrating LifeWatch ERIC [Work Package 5. Task 5.1.2. Development of the data standard. Repository development.] (LifeWatch ERIC—FEDER, POPE 2014-2020; Ministerio de Ciencia e Innovación, Spain).
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Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. COEXMED II: Especificidad de las interacciones adulto-juvenil durante el reclutamiento de plantas leñosas: complementariedad de caracteres funcionales e interacciones plant-antagonista (CGL2015-69118-C2-1-P, FEDER y Ministerio de Economia y Competitividad, Spain); REPNETS-Redes de reemplazamiento en bosques: variación ecogeográfica e influencia de las comunidades de hongos de la filosfera y de las interacciones planta-suelo (PGC2018-100966-B-I00, FEDER—Agencia Estatal de Investigación, Ministerio de Ciencia e Innovación, Spain); and FEDER SUMHAL-Sustainability for Mediterraean Hospost in Andalusia integrating LifeWatch ERIC [Work Package 5. Task 5.1.2. Development of the data standard. Repository development.] (LifeWatch ERIC—FEDER, POPE 2014–2020; Ministerio de Ciencia e Innovación, Spain).
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All authors have contributed to this study. JMA and JLG designed this study and carried out the field sampling. LCP and DC-S carried out the taxonomy of insects. AJP provided plant functional traits. JMB carried out statistical analyses and wrote the draft, all co-authors contribute to the final version.
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Bastida, J.M., Garrido, J.L., Cano-Sáez, D. et al. Effects of plant leaf traits, abundance and phylogeny on differentiation of herbivorous insect assemblages in Mediterranean mixed forest. Eur J Forest Res (2024). https://doi.org/10.1007/s10342-024-01676-y
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DOI: https://doi.org/10.1007/s10342-024-01676-y