Genetic variation in foundation species governs the dynamics of trophic interactions

Genetic variation in foundation species governs the dynamics of trophic interactions Various studies have demonstrated that the foundation species genetic diversity can have direct ef- fects that extend beyond the individual or population level, affecting the dependent communities. Additionally, these effects may be indirectly extended to higher trophic levels throughout the entire community. Quercus castanea is an oak species with characteristics of foundation species beyond pre- senting a wide geographical distribution and being a dominant element of Mexican temperate forests. In this study, we analyzed the influence of population (He) and individual (HL) genetic diversity of Q. castanea on its canopy endophagous insect community and associated parasitoids. Specifically, we studied the composition, richness (S) and density of leaf-mining moths (Lepidoptera: Tischeridae, Citheraniidae), gall-forming wasps (Hymenoptera: Cynipidae), and canopy parasitoids of Q. castanea. We sampled 120 trees belonging to six populations (20/site) through the previously recognized gradi- ent of genetic diversity. In total, 22 endophagous insect species belonging to three orders (Hymenoptera, Lepidoptera, and Diptera) and 20 parasitoid species belonging to 13 families were identified. In general, we observed that the individual genetic diversity of the host plant (HL) has a sig- nificant positive effect on the S and density of the canopy endophagous insect communities. In con- trast, He has a significant negative effect on the S of endophagous insects. Additionally, indirect ef- fects of HL were observed, affecting the S and density of parasitoid insects. Our results suggest that genetic variation in foundation species can be one of the most important factors governing the dy- namics of tritrophic interactions that involve oaks, herbivores, and parasitoids. Key words: community structure, introgressive hybridization, red oaks, tritrophic interactions. An important question in modern ecology is how genetic variation Hughes et al. 2008). In this sense, an increasing number of reports within dominant species can be an important driver of ecological have documented the effect of intra-specific genetic variation within processes (Whitham et al. 2006; Johnson and Stinchcombe 2007; foundation species on their associated communities. There is an V C The Author (2017). Published by Oxford University Press. 13 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 14 Current Zoology, 2018, Vol. 64, No. 1 emphasis on foundation species, which are a small subset of the total However, information about the effects of the foundation host plant species in an ecosystem, because it has been suggested that they genetic diversity on this trophic level is scarce. Understanding the should capture most of the variation in the community structure and processes for structuring host–parasitoid communities is important ecosystem processes. Additionally, it could be nearly impossible to because parasitoids and their insect hosts comprise approximately perform the studies of all species in the system had to be studied one-third of the animal species and more than 50% of the terrestrial (Whitham et al. 2003, 2006). Studies performed with this perspec- animal species (May 1988). Parasitoids also play a major role in reg- tive suggest that the genetics of the foundation species can have ulating their insect host populations. Scientific evidence has demonstrated that predators depend on strong organizational effects at the community and ecosystem levels (see review Whitham et al. 2012). The effect of the host plants’ gen- herbivores. The distribution, abundance, and performance of para- etic characteristics on the associated communities has focused on sitoids and predators should also somewhat depend on the quality specific genotypes within a species (e.g., Oenothera, Johnson and of their host plants (Giles et al. 2002; Harvey et al. 2003). If there is Agrawal 2005; Populus, Shuster et al. 2006; Schweitzer et al. 2008; high variation among plant genotypes for predation (Fritz 1995), Solidago, Crutsinger et al. 2008) or hybrid systems (e.g., there could be a heritable plant trait that is subject to natural selec- Eucalyptus, Dungey et al. 2000; Salix, Hochwender and Fritz 2004, tion (Hare 2002). In this sense, Whitham et al. (2003) proposed that Quercus, Tovar-S anchez and Oyama 2006). In the latter systems, associated communities can change in response to natural selection, the genetic diversity levels of host plants involved in hybridization which acts on plants if there are genetic correlations between the events may be increased (Tovar-S anchez et al. 2008; Ortego et al. plant traits and their associated communities. Therefore, tritrophic- 2014; Valencia-Cuevas et al. 2014). level interactions represent a good model for examining the interact- Canopy arthropod communities have been widely used to ing species and ecosystem processes in which the direct and indirect evaluate the influence of the genetic diversity of host plants on their effects of plant genetics are analyzable (Price 1997). Considering associated communities (Wimp et al. 2004; Bangert et al. 2006; that natural communities are complex ecological systems with struc- Tovar-S anchez et al. 2013). In particular, endophagous insects in- tures and functions based on the interaction of different factors clude gall-forming wasps (Cynipidae) and leaf mining moths (Wimp (Bailey and Whitham 2007), multifactorial studies that include gen- et al. 2007). This preference is probably because they are species etic factors and at least one ecological factor may be useful. with specific organ and tissue specialization (Stone et al. 2002), sug- Oaks are dominant elements of forest canopies. These trees have gesting that this group represents a good model to evaluate the influ- a wide geographical distribution and are involved in important eco- ence of host plant genetic diversity on associated communities. system processes, such as nutrient recycling and water balance To date, most the studies in the field of community genetics have (Madritch and Hunter 2002). This information inspires us to think analyzed the influence of genetic diversity and similarity on host that most oak species have attributes of foundation species. A foun- plant communities. In particular, these studies have reported that dation species has been defined as “those that structure a commu- species diversity increases as the genetic diversity of host plant popu- nity by creating locally stable conditions for other species, and by lations increases (Dungey et al. 2000; Wimp et al. 2004, 2005; modulating and stabilizing fundamental ecosystem processes” Tovar-S anchez and Oyama 2006; Crawford and Rudgers 2013), (Dayton 1972; Ellison et al. 2005). Moreover, oaks have high gen- and genetically similar host plants support similar communities etic diversity levels as a result of their life-history characteristics (Bangert et al. 2005, 2008; Barbour et al. 2009). Several studies (e.g., Tovar-S anchez et al. 2008; Lorenzo et al. 2009). However, have demonstrated that an increase in the host plant genetic diver- few studies have evaluated the influence of the host oak species gen- sity can generate changes in their morphology (Lambert et al. 1995; etic diversity on canopy arthropod communities. In addition, the re- Gonz alez-Rodr ıguez et al. 2004; Tovar-S anchez and Oyama 2004) sults of these studies differ (Tovar-S anchez and Oyama 2006; Tack and phenological traits (Hunter et al. 1997) as well as their second- et al. 2010, 2012; Castagneyrol et al. 2012; Tovar-Sanchez et al. ary chemistry (Fritz 1999; Wimp et al. 2004). These characteristics 2013). Furthermore, it is unknown whether the oak genetic diversity constitute a wider array of resources and conditions that can be used may indirectly extend to higher trophic levels throughout the by their associated communities. On the other hand, similarities in community. host plant communities have been explained as due to genetically In addition, the associated insect communities have been con- similar host plants expressing similar physical, chemical, and pheno- sidered complex systems with structures and functions that are logical characteristics (Bangert and Whitham 2007), suggesting that determined by the interaction of both genetic and ecological factors genetic differentiation through the geographic distribution of host (Tovar-S anchez et al. 2015a). One important ecological factor for plants can result in variation in the associated communities (Bangert oak canopy insect communities is the habitat heterogeneity et al. 2005, 2006, 2008; Barbour et al. 2009). In addition, it has (Valencia-Cuevas and Tovar-S anchez 2015). In habitats like oak for- been suggested that the ecological relevance of host plant intra- ests, tree communities define the physical structure. For example, specific genetic diversity can have a cascading effect (Abrahamson the forest canopy can be structurally more complex when it consists 1997; Whitham et al. 2003; Johnson and Stinchcombe 2007; of more than one tree species or more host plant species individuals Crutsinger 2016), extending throughout the community (Crutsinger (Sobek et al. 2009). This complexity may result in greater availabil- et al. 2006; Whitham et al. 2006; Moreira and Mooney 2013). ity of resources and conditions for insect communities. In particular, galls induced by cynipid wasps are structures that Our previous studies showed that Quercus castanea is an oak have extraordinary ecological value because the host communities species involved in hybridization events with other red oaks are structured in several trophic levels. These communities some- (Valencia-Cuevas et al. 2015), which promotes an increase in its times form very complex networks that consist of gall inductor, genetic diversity levels (Valencia-Cuevas et al. 2014). In addition, parasitoid, and inquiline insects (Askew 1984). Particularly, gall Q. castanea possesses characteristics of foundation tree species wasps are frequently associated with a diverse parasitoid commu- (Ellison et al. 2005). In this study, we characterized the canopy nity. In these communities, the majority of the associated parasitoids endophagous insect community (gall and miner insects) and associ- only attack oak gall wasps (Askew 1980; Stone et al. 2002). ated parasitoids to Q. castanea while addressing the following Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Valencia-Cuevas et al.  Dynamics of trophic interactions 15 hypotheses: (1) if more genetically diverse host plants offer a wider array of resources and conditions to be exploited by insects, then an increase of Q. castanea genetic diversity will favor more diverse endophagous insect communities; 2) if parasitoids depend on herbi- vores, and the herbivore species richness directly depends on the genetic attributes of the plant, an increase in the host plant genetic diversity will have indirect positive effects on the parasitoid commu- nity richness; and 3) if associated oak insect communities are com- plex systems whose structure and function are determined by the interaction of several factors, the structure of the canopy endopha- gous community insects and associated parasitoids can be shaped by both genetic and ecological factors. Materials and Methods Species description Quercus castanea Nee´(Lobatae: red oaks) includes trees from 5 to Figure 1. Spatial localization of six Q. castanea populations showing a natural 15 m in height with a trunk diameter of 30–60 cm. These trees can gradient of nuclear genetic diversity in the central part of the Transmexican be easily recognized in the field by their leaf characteristics. The Volcanic Belt, according to Valencia-Cuevas et al. (2014). 1) Parque Ecologico flowering season is from April to May and fruiting is from August El Huixteco (PEH, He: 0.873a); 2) Parque Las Penas ~ (PLP, He: 0.611d); 3) Parque Barranca de Tarango (PBT, He: 0.765b); 4) Parque Ecologico de la to December (Valencia 1995; V azquez 2006). The trees are located Ciudad de Me´ xico (PECM, He: 0.832c); 5) Parque Nacional El Tepozteco (PNT, between 1,180 and 2,600 m a.s.l., and they are distributed along all He: 0.611d); and 6) Corredor Biologico  Ajusco Chichinautzin (CBACh, He: major Mexican mountain ranges (Valencia 2004). They are fre- 0.621d). Different letters show that the mean values for each locality differ at quently found in perturbed areas with a xerophytic shrub type of a¼ 0.05 (Tukey’s test). vegetation, which is also localized in mountain cloud forests (Rzedowski and Rzedowski 2001). Furthermore, Q. castanea is a (PEH: 366.3). Three transects of 1,000 m in each locality were cre- red oak species that possesses characteristics associated with a foun- ated. At each 50 m, the nearest individual morphologically recog- dation tree species (Ellison et al. 2005). For example, Q. castanea is nized pure “Q. castanea” was sampled. the most widely distributed species within the red oak group in Mexico (Valencia 2004); it is a dominant element of the temperate Molecular data forests where it resides (Valencia-Cuevas et al. 2014) and it acts as The 120 individuals (20 individuals per site) that were morphologic- the habitat for different species (Tovar-S anchez et al. 2013). ally recognized as pure Q. castanea were previously analyzed by 14 microsatellite (SSRs) primers (six nSSRs and eight cpSSRs). We Study sites and sampling found an increase in the individual and population genetic diversity Trees that are morphologically recognized as “pure” Q. castanea of Q. castanea populations analyzed here (Valencia-Cuevas et al. were sampled from six populations (20 trees/site), one allopatric 2014) as a result of the interspecific gene flow with other red oaks population of Q. castanea (population 1) and five sympatric stands species (Valencia-Cuevas et al. 2015). between Q. castanea and other red oak species (populations 2–6, Figure 1) through the central part of the TVB. All chosen sites share Canopy endophagous insect communities and the following common traits: geological history [all localities belong associated parasitoids to the central portion of TVB with a formation process that occurred The endophagous insect and parasitoid community structure associ- in a single geological event that began during the Quaternary– ated with Q. castanea was analyzed in the same 120 individuals as Pliocene (Challenger 1998)], weather (sub-humid temperate), alti- in Valencia-Cuevas et al. (2014). These individuals were 8–10 m tude (between 1,800 and 2,500 m), vegetation type (mature oak), (9.126 SE 0.17 m) in height and accounted for 18.3–20.1 m and soil type (volcanic origin or derived from igneous and sediment- 2 2 (19.20 m 6 SE 0.17 m ) of canopy cover. Tree canopies selected for ary rocks). Additionally, these areas present almost no local disturb- sampling were, as far as possible, spatially delimited from others by ance inside the forest because they are under Mexican protection avoiding overlaps. Insect communities were sampled using four ran- standards. This homogeneity among study sites could be useful to domly selected branches (50 leaves per branch) in the middle part of minimize the influence of environmental and spatial factors on in- the crown. Galls and mining leaves collected in each host tree were sect endophagous and parasitoid communities that are associated separated into the morphospecies level, placed in previously vou- with the Q. castanea canopy. chered plastic containers (e.g., locality, host category, etc.) and In addition, the number of associated species with Q. castanea in transported to the laboratory where the insects emerged. Wasps and each sympatric locality ranged from one to five. These species were their parasitoids were identified to the finest taxonomic level. as follows: Q. candicans, Q. crassifolia, Q. crassipes, Q. laurina, Q. mexicana, Q. scytophyla, and Q. urbanii (Appendix 1). The Q. castanea local density (ind/ha) in each site was as follows: Corredor Statistical analysis Biologico  Ajusco Chichinautzin (CBACh: 51.7), Parque Nacional El Genetic diversity of host plant To evaluate the influence of the Q. castanea genetic diversity on can- Tepozteco (PNT: 56.7), Parque Ecologico de la Ciudad de Me ´ xico (PECM: 149.0), Parque Barranca de Tarango (PBT: 161.6), Parque opy endophagous communities and parasitoids, the parameter He Las Penas ~ (PLP: 186.7) and Parque Nacional El Huixteco (expected heterozygosis) was used to analyze the genetic diversity at Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 16 Current Zoology, 2018, Vol. 64, No. 1 the population level, as reported by Valencia-Cuevas et al. (2014). population (He) genetic diversity, S and density of endophagous and Additionally, the Q. castanea individual genetic diversity was esti- parasitoid insects. The model was performed with the lavaan pack- mated using homozygosity by the loci index (HL), a microsatellite- age for R (Rosseel 2011). derived measure that improves heterozygosity estimates in natural populations by weighting the contribution of each locus to the Results homozygosity value based on the allelic variability (Aparicio et al. 2006). The HL is calculated as follows: HL ¼ (RE )/(RE þRE ), Endophagous and associated parasitoid insect h h j where E and E are the expected heterozygosity of the loci that an h j community composition individual bears in homozygosis (h) and heterozygosis (j), respect- The endophagous insect community associated with Q. castanea ively, forms. This index varies between 0, when all loci are heterozy- consisted of 22 species that belong to the following three orders: gous, and 1, when all loci are homozygous. The HL was estimated Hymenoptera (18 species), Lepidoptera (two species), and Diptera using CERNICALIN, an Excel spreadsheet that is available on re- (two species, Appendix 2). In particular, the gall insect group quest. These parameters (He and HL) were used because they are (Hymenoptera: Cynipidae) was represented by eight genera frequently employed to evaluate the influence of both the population (Appendix 2). In terms of the species richness, the most important and individual genetic diversity on the community structure (e.g., genus was Andricus at 38.8% (seven species, Appendix 2). (Tovar-S anchez and Oyama 2006); Tovar-S anchez et al. 2013). Meanwhile, the leaf mining insect group was represented by two families, Diptera and Lepidoptera (Appendix 2, Figure 2). Infestation levels of endophagous insects The parasitoid community was represented by 13 families The species richness (S) of the canopy arthropod community and (Figure 2). The most important family in terms of the genus and spe- their associated parasitoids was estimated at the morpho-species cies richness was Eulophidae (Appendix 2). In addition, we found one inquiline wasp species was associated with gall inducted with level. Each host tree infestation value was estimated as [(number of galls or miners/200 leaves)  100] over the four branches. Analysis Amphibolips hidalgoensis belonging to Synergus genus (Cynipidae). of variance (ANOVA, Model III; Zar 2010) was used to determine We also found two individuals who belong to Encyrtidae and one to differences in the average infestation levels among Q. castanea Megaspilidae. Both families included hyperparasitoids species. populations. Infestation percentage data were corrected as Hyperparasitoids and inquiline insects were not included in the analysis. X¼ arcsin (%) = , and discontinuous data were transformed as X¼ (x) = þ 0.5 (Zar 2010). Finally, a Tukey test was used to deter- mine significant differences between the infestation mean values Infestation levels among populations (Zar 2010). The software used for statistical The mean infestation levels of endophagous insects were signifi- analysis was STATISTICA 8.0 (Statsoft 2007). cantly different among the Q. castanea populations (F ¼ 5, 114 42.688, P< 0.0001). We did not detect an infestation level pattern over the natural genetic diversity gradient that was previously recog- Influence of Q. castanea genetic diversity, host plant density, and nized in Q. castanea populations. In general, the infestation levels red oak species richness on canopy insects had the following relationship (mean6 SE): PNT (12.986 We used a multiple regression approach to examine whether the 1.92)¼ PECM (14.786 0.74)< PEH (18.616 0.73)¼ CBACh Q. castanea genetic diversity levels [population (He) and individual (HL)] and two ecological factors (Q. castanea density and red oak (24.456 1.22)< PLP (26.236 1.52). Finally, we found that there is species richness) influence the canopy endophagous insect and asso- no relationship between the infestation levels of gall forming insects and the parasitoid density (r ¼ 0.2, r ¼ 0.13, P ¼ 0.17). ciated parasitoids. Specifically, this analysis was useful to determine the relative contribution from each factor on the species richness variation and endophagous and parasitoid insect density. We used a Influence of Q. castanea genetic diversity, host plant density, and standard least squares model with partial (type III sums of squares) red oak species richness on canopy insects error structure and the He, HL, host density, and oak richness as In general, our results showed that the Q. castanea genetic diversity our factors. We excluded the variables that showed a correlation co- levels (population and individual), host tree density, and red oak efficient >0.6 to improve the analysis. Considering that endopha- species richness influence the community structure of endophagous gous insects are resources for parasitoids, we were interested in and parasitoid canopy insects (Table 1). Specifically, we found that determining whether the density and species richness of endopha- the HL and oak richness had a significant positive effect on the S of gous insects can predict the density and species richness of the asso- endophagous insects, explaining 10.7% and 5.6%, respectively, of ciated parasitoids. Therefore, we used simple linear regressions. The the variation of this metric. In contrast, the He had a significant software used for statistical analysis were STATISTICA 8.0 (Statsoft negative effect on the S of endophagous insects, explaining 13.6% 2007) and Species Diversity and Richness version 3.03 (Henderson of the variation in this metric (Table 1). and Seaby 2002). We found that the HL had a significant positive influence on the We constructed one structural equation model (SEM) to estimate endophagous insect density, explaining the 11.1% of the variation. the causal relationships between the host plant genetic diversity (He, In contrast, the host density had a significant negative influence on HL) and ecological (host plant density and red oak species richness) the endophagous insect density, explaining 4.1% of the variation and community (S and density of endophagous and parasitoid in- (Table 1). sects) variables. Based on a previous study (Valencia-Cuevas et al. The species richness of parasitoid insects was significantly posi- 2014) and literature review, we anticipated what causal paths may tively influenced by the HL and host density, explaining 5.6% and be important. For the model, we considered the host plant density 3.5%, respectively, of the variation. In contrast, the species richness and red oak species richness as independent variables. The depend- of parasitoid insects was significantly negatively influenced by the ent variables that we examined were the individual (HL) and oak richness, explaining 9.2% of the variation (Table 1). Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Valencia-Cuevas et al.  Dynamics of trophic interactions 17 Gall-forming wasps genus (Cynipidae) Leaf mining insect families Parasitoid insect families Figure 2. Canopy endophagous insects (gall-forming wasps and leaf mining insects) and parasitoid composition associated to Q. castanea. Table 1. Multiple regression analysis testing the influence of 1.-individual (HL) and population genetic diversity of Q. castanea (He), 2.-host density, and 3.-red oak species local community richness on species richness and density of endophagous insect and associated parasit- oids to Q. castanea in the Transmexican Volcanic Belt Species richness Density df SS FP % Variation df SS FP % Variation Endophagous insects He 1 9.934 11.983 0.000 6.2 1 1.260 0.475 0.490 0.4 HL 1 53.220 64.194 0.000 33.2 1 36.845 13.893 0.000 7.5 Host density 1 0.000 0.007 0.927 0.0 1 31.395 11.838 0.000 5.1 Oak richness 1 4.173 5.034 0.026 2.6 1 10.549 3.977 0.048 7.2 Parasitoid insects He 1 0.004 0.156 0.693 0.1 1 0.207 0.973 0.326 0.9 HL 1 0.328 11.095 0.001 8.6 1 2.219 10.384 0.001 9.6 Host density 1 0.111 3.764 0.055 2.9 1 1.412 6.612 0.011 6.0 Oak richness 1 0.207 7.005 0.009 5.4 1 2.066 9.673 0.002 8.4 We also found that the HL and host density had a significant the S and density of endophagous and parasitoid insects. However, positive influence on the parasitoid insect density. The relative con- the He was negatively correlated with the S of endophagous insects. tributions of the abovementioned factors on the variation in the In contrast, the HL showed a positive influence on the analyzed parasitoid density were 5.1% and 5.9%, respectively. In contrast, community parameters. Similarly, ecological variables had a signifi- the oak richness had a significant negative influence on the parasit- cant influence on the associated endophagous and parasitoid crea- oid insect density, explaining 10.5% of the variation (Table 1). tures (Figure 3; Table 2). In general, the HL was the factor that explained the highest per- Finally, this model explained 25.75% and 16.24% of the S and centage of variation in the analyzed community parameters. density of endophagus insects, respectively. Additionally, 12% and Additionally, the proportion of the total variance explained by the 8.91% of the S and density of parasitoid insects, respectively, were plant genotype was lower for parasitoids than for endophagous in- explained with this model (Figure 3). sects (Table 1). When the relationship between the gall and parasit- oid density was analyzed, there was no significant relationship 2 Discussion (r ¼ 0.02; P ¼ 0.17). In contrast, the gall and parasitoid richness showed a significant positive relationship (r ¼ 0.12; P< 0.0001). In this study, we simultaneously evaluated the influence of genetic Figure 3 shows the partial correlation coefficient for each path. attributes of Q. castanea (individual and population genetic diver- In all cases, the proposed paths were significant. The only exception sity) and two ecological factors (host density and red oak species was the relationship between the host plant density and parasitoid richness) on two different trophic levels of the canopy arthropod density. In particular, the He and HL had a significant influence on community, endophagous insects, and associated parasitoids. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Abundance of arthropods (%) 18 Current Zoology, 2018, Vol. 64, No. 1 Figure 3. Path model. Solid paths are statistically different from 0 (P< 0.05), where dotted path is not. Path widths are proportional to the standardized regression coefficients. Only the coefficients for significant paths are shown. The R of the endogenous variables are inside of the boxes. Table 2. Coefficient value, standard errors, Z scores, and P values host plants, which can influence the abundance, distribution, and di- for the SEM versity of the associated species, in this type of system (Vellend and Geber 2005). Therefore, common garden studies can be a useful ap- Path Estimate SE Z value P proach for comparing the effects of the genetic diversity of Q. casta- He ! S_endophagous 1.249 0.243 5.134 0.000 nea and other ecological variables on the associated arthropods in S_ oaks ! S_endophagous 0.213 0.064 3.351 0.001 both experimental settings and wild populations. HL ! S_endophagous 0.320 0.081 3.970 0.000 In general, we found a significant positive effect of the genetic di- HL ! endophagous density 3.363 0.952 3.531 0.000 versity levels (HL)of Q. castanea on the S and density of endopha- S_oaks ! endophagous density 1.602 0.761 2.106 0.035 gous insects. This result was supported by path analysis. A similar Host plant density ! endophagous 0.010 0.003 3.175 0.001 response has been reported in phytophagous insect communities density that are associated with different foundation species [e.g., poplars HL ! S_parasitoids 0.259 0.102 2.541 0.011 (Whitham et al. 2006); willows (Hochwender and Fritz 2004); euca- S_oaks ! S_parasitoids 0.147 0.041 3.570 0.000 lyptus (Dungey et al. 2000); and oaks (Tovar-S anchez and Oyama S_oaks ! parasitoid density 0.465 0.151 3.082 0.002 2006; Tovar-S anchez et al. 2015a,b)]. For example, Tovar-S anchez Host plant density ! parasitoid 0.001 0.000 1.767 0.077 density et al. (2013) reported that the H variation of the Q. crassipes and HL ! parasitoid density 0.694 0.273 2.543 0.011 Q. castanea arthropod communities was positive and significantly S_oaks ! He 0.225 0.011 20.408 0.000 influenced by the individual genetic diversity of the host. S_oaks ! HL 0.126 0.037 3.440 0.001 Additionally, recent studies in Q. crassifolia (Tovar-Sanchez et al. 2015a) showed that individual genetic diversity had a significant Notes: He, population genetic diversity; HL, individual genetic diversity; positive influence on the S and H of the canopy arthropods during S_oaks, oak species richness; S_endophagous, endophagous species richness; the dry and rainy seasons, respectively. It has been proposed that S_parasitoids, parasitoid species richness. increasing the genetic diversity of the host plant can generate changes in its morphological (Lambert et al. 1995; Gonz alez- The results in this study are in accordance with those in other studies Rodr ıguez et al. 2004; Tovar-S anchez and Oyama 2004), pheno- that have shown the genetic diversity of foundation species has a sig- logical (Hunter et al. 1997), architectural (Whitham et al. 1999; nificant effect on the associated community (Bangert and Whitham Bangert et al. 2005), and chemical (Fritz 1999; Cheng et al. 2011) 2007; Hughes et al. 2008; Whitham et al. 2012; Crutsinger 2016). characteristics. These changes can be translated into a broader mo- Additionally, we found that insect communities associated with Q. saic of resources and conditions that can be beneficial for canopy castanea are determined by both host plant genetic attributes and arthropods. ecological factors, such as the host tree density and local red oak Considering that the arthropod community structure could be species richness. influenced by several factors beyond the host genetic diversity Studies in natural systems, as presented in this report, offer the (Johnson and Stinchcombe 2007; Hughes et al. 2008; Tack et al. realism of the wild; however, it is important to considerer that it is 2012), the approach used in the present study offers a more realistic difficult to control the variables related to the spatial location of scenario than the other studies that only evaluate the role of host Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Valencia-Cuevas et al.  Dynamics of trophic interactions 19 plant genetic attributes on the community structure (Hersch-Green should be easy to find (Sholes 2008). Additionally, a high resource et al. 2011). Although these studies have helped demonstrate that concentration could support both more herbivore species and higher intraspecific genetic variation can have an effect beyond an individ- densities of each herbivore species (Root 1973; Kareiva 1983). ual’s phenotype, they likely do not accurately estimate its effective Additionally, this effect will be the strongest for specialist herbivores size. The most commonly employed method in these approaches has (Stephens and Myers 2012). Under this scenario, we suppose that been the collection of multiple genotypes from diverse and often dis- lower Q. castanea densities promote low resource concentration for tant environments as well as to replicate these genotypes into single endophagous insects; as a result, their densities are less favored, as common environments where the environmental variation is mini- seen in other systems (Ostergard and Ehrle ´ n 2005; Sholes 2008). mized (Tack et al. 2012). As a result, these studies provide little in- This hypothesis is also suggested by our path analysis in which there formation regarding the importance of the plant genotype or genetic was a significant negative relationship between the host plant dens- variation compared with other factors that also influence multi- ity and endophagous insect density. In contrast, the path analysis trophic communities. In our study, we simultaneously evaluated the failed to show that the host density also affects the parasitoid dens- influence of genetic attributes of Q. castanea (individual and popu- ity. In addition, we found that there is no relationship between gall lation genetic diversity) and two ecological factors (host density and forming insects and parasitoid density. Both results led us to think red oak species richness) on canopy insect community in natural that the parasitoid insect densities are not mediated by resource conditions. This experimental design allowed us to more accurately availability (endophagous insect density), but they are probably quantify the influence of the effects of three different variables on related to the host plant or prey quality, as has been reported in community structuring. other studies (e.g., Fritz et al. 1997; Harvey et al. 2003; Sch€ adler In contrast, some studies have not found significant effects of et al. 2010). For example, Harvey et al. (2003) and Fritz et al. plant genetics on associated communities. For example, Tack et al. (1997) demonstrated differences in the performance of parasitoids, (2010) found that genetic diversity had little influence on the which depend on the host plant quality. From this perspective, endophagous insect community structure (gallers, leafminers, and Sch€ adler et al. (2010) reported that parasitoid abundance may be leafrollers) of Q. robur in Finland. Similar results were reported by correlated with the quality of host plants. Considering these state- Castagneyrol et al. (2012), who found that the genetic attributes of ments, it is likely that certain performance traits of parasitoids asso- the host plant had no significant effect on the phytophagous insect ciated with Q. castanea are affected by the quality of the host plant community (endophagous and ectophagous) of Q. robur in France. or endophagous insect prey, suggesting that the host plant’s genetic In the case of Q. castanea, previous studies have shown high gen- attributes can influence parasitoid populations via plant quality or etic diversity levels (Valencia-Cuevas et al. 2014) as a result of inter- prey consumption. It is important to emphasize that we did not specific gene flow with three of its associated red oak species in the measure the host plant or endophagous insect quality in this study; Transmexican Volcanic Belt (Valencia-Cuevas et al. 2015). In this however, addressing this issue in future work could help accept or scenario, it is possible that the Q. castanea genetic diversity levels reject these hypotheses. Moreover, the oak species richness also had are sufficient for the endophagous insect community to have an ob- a significant influence on the endophagous species richness. Previous servable response. studies in Q. crassifolia (Tovar-S anchez et al. 2015a) revealed a phe- It has been proposed that the direct effects of genetically based nomenon known as “associational susceptibility” (Brown and Ewel plant traits on herbivores may also indirectly extend to the next tro- 1987) in which plant species present with greater abundance and di- phic level, impacting predators and parasitoids (Johnson and versity of herbivores when they are spatially associated with hetero- Agrawal 2005; Crutsinger 2016). From this perspective, we ex- specific neighbors. This phenomenon probably occurs in Q. pected that the endophagous insect species richness directly depends castanea. on the genetic attributes of the host plant, which has indirect posi- In this study, we observed significant differences in the endopha- tive effects on the parasitoid community richness. This hypothesis gous insect infestation levels associated with Q. castanea among dif- was supported in this study because we found that the Q. castanea ferent localities. The occurrence of different response patterns has genetic diversity levels influenced the canopy parasitoid insects. been attributed to differences in the host plant genetic characteristics When the relationship between parasitoid species richness and and genetic mechanisms that determine the inheritance of resistance endophagous species richness was examined, we found a significant characteristics (Boecklen and Spellenberg 1990; Fritz et al. 1994; positive relationship (r ¼ 0.12; P< 0.0001). This result demon- Strauss 1994). In a previous study, we revealed the existence of an strates the high degree of specialization between parasitoid species array of homozygous and heterozygous genotypes in the Q. castanea and their host gall inductor species (Sanchez et al. 2013). Finally, we populations that were analyzed in this research (Valencia-Cuevas suggest that the genetic diversity of Q. castanea had an indirect ef- et al. 2014). Therefore, we presumed that different Q. castanea fect on the S of parasitoid insects, which was mediated through the genotypes inherit different mechanisms which, in turn, establish the effects on the S of endophagous insects. These results are consistent different resistance patterns observed here. In addition, it has been with reports by Bailey et al. (2006) and Johnson (2008). Overall, reported that the host plant resistance characteristics may be differ- these results show that genetic variation in plants can be an import- entially expressed in different environments (Fritz 1999). The Q. ant factor governing the herbivore population dynamics and tritro- castanea populations in this study are distributed in the central por- tion of the TVB, whose formation process occurred in a single geolo- phic interactions that involve plants, herbivores, and parasitoids. According to the results obtained in this study, we suggest that Q. gical event that began during the Quaternary–Pliocene (Challenger castanea is a foundation species whose genetic diversity levels have 1998). This observation makes us suppose that these populations direct effects on the endophagous insect community. have had the same evolutionary origin, which has minimized the en- In addition, we found that ecological parameters, such as the vironmental variation among localities and the influence of such host density and red oak species richness, influence the canopy insect variability on the endophagous insect infestation levels among the community. It has been suggested that high host density should pro- study sites. Hence, we suggest that the variation in the expression of vide herbivores with substantial edible biomass and the biomass the resistance characteristics of Q. castanea through the localities Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 20 Current Zoology, 2018, Vol. 64, No. 1 Cheng D, Vrieling K, Klinkhammer PGL, 2011. The effect of hybridization on found in this work is related to the genetic characteristics of the host secondary metabolites and herbivore resistance: implications for the evolu- plant in each population. tion of chemical diversity in plants. Phytochem Rev 10:107–117. In conclusion, the multifactorial approach used in this study Crawford KM, Rudgers JA, 2013. Genetic diversity within a dominant plant helped to determine the influence of genetic and ecological factors outweighs plant species diversity in structuring an arthropod community. on the arthropod community structure associated with Q. castanea, Ecology 94:1025–1035. as well as to obtain a more realistic understanding of natural condi- Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC et al., 2006. tions. Therefore, the results from this study suggest that evaluating Plant genotypic diversity predicts community structure and governs an eco- genetic variation in plant traits may be essential to understanding system process. Science 313:966–968. the ecology of oak–parasite–parasitoid interactions. Crutsinger GM, Souza L, Sanders NJ, 2008. Intraspecific diversity and domin- ant genotypes resist plant invasions. Ecol Lett 11:16–23. Crutsinger GM, 2016. A community genetics perspective: opportunities for Acknowledgments the coming decade. New Phytol 210:65–70. Dayton PK, 1972. Toward an understanding of community resilience and the The authors thank Gabriel Flores, Mauricio Mora, Efra ın Ram ırez, and potential effects of enrichments to the benthos at McMurdo Sound, Guillermo S anchez for their help with the field collection process. We thank Antarctica. In: Parker BC, editor. 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Locality name, state, and red oak species associated to Q. castanea in the Transmexican Volcanic Belt Locality State Oak species Corredor Biologico  Ajusco-Chichinautzin Morelos Q. castanea Parque Nacional El Tepozteco Morelos Q. castanea, Q. crassipes Parque Ecologico  de la Ciudad de Me ´ xico Mexico City Q. castanea, Q. crassipes, Q. laurina Parque Barranca de Tarango Mexico City Q. castanea, Q. crassipes, Q. laurina, Q. mexicana Parque Ecologico  Las Penas ~ Mexico State Q. castanea, Q. crassipes, Q. laurina, Q. mexicana, Q. crassifolia Parque Ecologico  El Huixteco Guerrero Q. castanea, Q. crassifolia, Q. laurina, Q. candicans, Q. urbanii, Q. scytophyla Appendix 2. Community composition of canopy endophagous and parasitoid insects associated to Q. castanea in the Transmexican Volcanic Belt Orden Family Genus Species Endophagous insects Hymenoptera Cynipidae Amphibolips Amphibolips hidalgoensis Andricus Andricus nr sphaericus Disholcaspis A. nievesaldreyi A. linaria group A. tuberoses group A. nr bonansaeai A. sp. 1 A. sp. 2 Disholcaspis nr pallens D. sp 1 Antron Antron sp. Erythres Erythres hastata Kokkocynips Kokkocynips doctorrosae Neuroterus Neuroterus nr junctor N. sp. 1 N. sp. 2 N. sp. 3 Melikaiella Melikaiella amphibolensis Diptera Cecidomyiidae Cecidomyiidae sp.1 Chloropidae Chloropidae sp. 1 Lepidoptera Bedellinae Bedellia sp. Gelechiidae Gelechiidae sp. Parasitoid insects Apidea Apidea sp.1 Bethylidae Bethylidae sp.1 Braconidae Braconidae sp.1 Elasmidae Elasmus Elasmus sp. Eulophidae Cirruspilus Cirruspilus sp. Clostocerus Clostocerus sp. Euplectrus Euplectrus sp. Tetrastichinae Tetrastichinae sp. Eulophidae sp. 1 Eulophidae sp. 2 Eulophidae sp. 3 Eupelmidae Brossema Brossema sp. Eurytomidae Eurytoma Eurytoma sp. Figitidae Figitidae sp. 1 Ormyridae Ormyrus Ormyrus sp. Platygastridae Scelionidae Scelionade sp. Platigastridae sp. 1 Pteromelidae Pteromelidae sp. 1 Sphecidae Sphecidae sp. 1 Torymidae Torymus Torymus sp. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Zoology Oxford University Press

Genetic variation in foundation species governs the dynamics of trophic interactions

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Abstract

Various studies have demonstrated that the foundation species genetic diversity can have direct ef- fects that extend beyond the individual or population level, affecting the dependent communities. Additionally, these effects may be indirectly extended to higher trophic levels throughout the entire community. Quercus castanea is an oak species with characteristics of foundation species beyond pre- senting a wide geographical distribution and being a dominant element of Mexican temperate forests. In this study, we analyzed the influence of population (He) and individual (HL) genetic diversity of Q. castanea on its canopy endophagous insect community and associated parasitoids. Specifically, we studied the composition, richness (S) and density of leaf-mining moths (Lepidoptera: Tischeridae, Citheraniidae), gall-forming wasps (Hymenoptera: Cynipidae), and canopy parasitoids of Q. castanea. We sampled 120 trees belonging to six populations (20/site) through the previously recognized gradi- ent of genetic diversity. In total, 22 endophagous insect species belonging to three orders (Hymenoptera, Lepidoptera, and Diptera) and 20 parasitoid species belonging to 13 families were identified. In general, we observed that the individual genetic diversity of the host plant (HL) has a sig- nificant positive effect on the S and density of the canopy endophagous insect communities. In con- trast, He has a significant negative effect on the S of endophagous insects. Additionally, indirect ef- fects of HL were observed, affecting the S and density of parasitoid insects. Our results suggest that genetic variation in foundation species can be one of the most important factors governing the dy- namics of tritrophic interactions that involve oaks, herbivores, and parasitoids. Key words: community structure, introgressive hybridization, red oaks, tritrophic interactions. An important question in modern ecology is how genetic variation Hughes et al. 2008). In this sense, an increasing number of reports within dominant species can be an important driver of ecological have documented the effect of intra-specific genetic variation within processes (Whitham et al. 2006; Johnson and Stinchcombe 2007; foundation species on their associated communities. There is an V C The Author (2017). Published by Oxford University Press. 13 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 14 Current Zoology, 2018, Vol. 64, No. 1 emphasis on foundation species, which are a small subset of the total However, information about the effects of the foundation host plant species in an ecosystem, because it has been suggested that they genetic diversity on this trophic level is scarce. Understanding the should capture most of the variation in the community structure and processes for structuring host–parasitoid communities is important ecosystem processes. Additionally, it could be nearly impossible to because parasitoids and their insect hosts comprise approximately perform the studies of all species in the system had to be studied one-third of the animal species and more than 50% of the terrestrial (Whitham et al. 2003, 2006). Studies performed with this perspec- animal species (May 1988). Parasitoids also play a major role in reg- tive suggest that the genetics of the foundation species can have ulating their insect host populations. Scientific evidence has demonstrated that predators depend on strong organizational effects at the community and ecosystem levels (see review Whitham et al. 2012). The effect of the host plants’ gen- herbivores. The distribution, abundance, and performance of para- etic characteristics on the associated communities has focused on sitoids and predators should also somewhat depend on the quality specific genotypes within a species (e.g., Oenothera, Johnson and of their host plants (Giles et al. 2002; Harvey et al. 2003). If there is Agrawal 2005; Populus, Shuster et al. 2006; Schweitzer et al. 2008; high variation among plant genotypes for predation (Fritz 1995), Solidago, Crutsinger et al. 2008) or hybrid systems (e.g., there could be a heritable plant trait that is subject to natural selec- Eucalyptus, Dungey et al. 2000; Salix, Hochwender and Fritz 2004, tion (Hare 2002). In this sense, Whitham et al. (2003) proposed that Quercus, Tovar-S anchez and Oyama 2006). In the latter systems, associated communities can change in response to natural selection, the genetic diversity levels of host plants involved in hybridization which acts on plants if there are genetic correlations between the events may be increased (Tovar-S anchez et al. 2008; Ortego et al. plant traits and their associated communities. Therefore, tritrophic- 2014; Valencia-Cuevas et al. 2014). level interactions represent a good model for examining the interact- Canopy arthropod communities have been widely used to ing species and ecosystem processes in which the direct and indirect evaluate the influence of the genetic diversity of host plants on their effects of plant genetics are analyzable (Price 1997). Considering associated communities (Wimp et al. 2004; Bangert et al. 2006; that natural communities are complex ecological systems with struc- Tovar-S anchez et al. 2013). In particular, endophagous insects in- tures and functions based on the interaction of different factors clude gall-forming wasps (Cynipidae) and leaf mining moths (Wimp (Bailey and Whitham 2007), multifactorial studies that include gen- et al. 2007). This preference is probably because they are species etic factors and at least one ecological factor may be useful. with specific organ and tissue specialization (Stone et al. 2002), sug- Oaks are dominant elements of forest canopies. These trees have gesting that this group represents a good model to evaluate the influ- a wide geographical distribution and are involved in important eco- ence of host plant genetic diversity on associated communities. system processes, such as nutrient recycling and water balance To date, most the studies in the field of community genetics have (Madritch and Hunter 2002). This information inspires us to think analyzed the influence of genetic diversity and similarity on host that most oak species have attributes of foundation species. A foun- plant communities. In particular, these studies have reported that dation species has been defined as “those that structure a commu- species diversity increases as the genetic diversity of host plant popu- nity by creating locally stable conditions for other species, and by lations increases (Dungey et al. 2000; Wimp et al. 2004, 2005; modulating and stabilizing fundamental ecosystem processes” Tovar-S anchez and Oyama 2006; Crawford and Rudgers 2013), (Dayton 1972; Ellison et al. 2005). Moreover, oaks have high gen- and genetically similar host plants support similar communities etic diversity levels as a result of their life-history characteristics (Bangert et al. 2005, 2008; Barbour et al. 2009). Several studies (e.g., Tovar-S anchez et al. 2008; Lorenzo et al. 2009). However, have demonstrated that an increase in the host plant genetic diver- few studies have evaluated the influence of the host oak species gen- sity can generate changes in their morphology (Lambert et al. 1995; etic diversity on canopy arthropod communities. In addition, the re- Gonz alez-Rodr ıguez et al. 2004; Tovar-S anchez and Oyama 2004) sults of these studies differ (Tovar-S anchez and Oyama 2006; Tack and phenological traits (Hunter et al. 1997) as well as their second- et al. 2010, 2012; Castagneyrol et al. 2012; Tovar-Sanchez et al. ary chemistry (Fritz 1999; Wimp et al. 2004). These characteristics 2013). Furthermore, it is unknown whether the oak genetic diversity constitute a wider array of resources and conditions that can be used may indirectly extend to higher trophic levels throughout the by their associated communities. On the other hand, similarities in community. host plant communities have been explained as due to genetically In addition, the associated insect communities have been con- similar host plants expressing similar physical, chemical, and pheno- sidered complex systems with structures and functions that are logical characteristics (Bangert and Whitham 2007), suggesting that determined by the interaction of both genetic and ecological factors genetic differentiation through the geographic distribution of host (Tovar-S anchez et al. 2015a). One important ecological factor for plants can result in variation in the associated communities (Bangert oak canopy insect communities is the habitat heterogeneity et al. 2005, 2006, 2008; Barbour et al. 2009). In addition, it has (Valencia-Cuevas and Tovar-S anchez 2015). In habitats like oak for- been suggested that the ecological relevance of host plant intra- ests, tree communities define the physical structure. For example, specific genetic diversity can have a cascading effect (Abrahamson the forest canopy can be structurally more complex when it consists 1997; Whitham et al. 2003; Johnson and Stinchcombe 2007; of more than one tree species or more host plant species individuals Crutsinger 2016), extending throughout the community (Crutsinger (Sobek et al. 2009). This complexity may result in greater availabil- et al. 2006; Whitham et al. 2006; Moreira and Mooney 2013). ity of resources and conditions for insect communities. In particular, galls induced by cynipid wasps are structures that Our previous studies showed that Quercus castanea is an oak have extraordinary ecological value because the host communities species involved in hybridization events with other red oaks are structured in several trophic levels. These communities some- (Valencia-Cuevas et al. 2015), which promotes an increase in its times form very complex networks that consist of gall inductor, genetic diversity levels (Valencia-Cuevas et al. 2014). In addition, parasitoid, and inquiline insects (Askew 1984). Particularly, gall Q. castanea possesses characteristics of foundation tree species wasps are frequently associated with a diverse parasitoid commu- (Ellison et al. 2005). In this study, we characterized the canopy nity. In these communities, the majority of the associated parasitoids endophagous insect community (gall and miner insects) and associ- only attack oak gall wasps (Askew 1980; Stone et al. 2002). ated parasitoids to Q. castanea while addressing the following Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Valencia-Cuevas et al.  Dynamics of trophic interactions 15 hypotheses: (1) if more genetically diverse host plants offer a wider array of resources and conditions to be exploited by insects, then an increase of Q. castanea genetic diversity will favor more diverse endophagous insect communities; 2) if parasitoids depend on herbi- vores, and the herbivore species richness directly depends on the genetic attributes of the plant, an increase in the host plant genetic diversity will have indirect positive effects on the parasitoid commu- nity richness; and 3) if associated oak insect communities are com- plex systems whose structure and function are determined by the interaction of several factors, the structure of the canopy endopha- gous community insects and associated parasitoids can be shaped by both genetic and ecological factors. Materials and Methods Species description Quercus castanea Nee´(Lobatae: red oaks) includes trees from 5 to Figure 1. Spatial localization of six Q. castanea populations showing a natural 15 m in height with a trunk diameter of 30–60 cm. These trees can gradient of nuclear genetic diversity in the central part of the Transmexican be easily recognized in the field by their leaf characteristics. The Volcanic Belt, according to Valencia-Cuevas et al. (2014). 1) Parque Ecologico flowering season is from April to May and fruiting is from August El Huixteco (PEH, He: 0.873a); 2) Parque Las Penas ~ (PLP, He: 0.611d); 3) Parque Barranca de Tarango (PBT, He: 0.765b); 4) Parque Ecologico de la to December (Valencia 1995; V azquez 2006). The trees are located Ciudad de Me´ xico (PECM, He: 0.832c); 5) Parque Nacional El Tepozteco (PNT, between 1,180 and 2,600 m a.s.l., and they are distributed along all He: 0.611d); and 6) Corredor Biologico  Ajusco Chichinautzin (CBACh, He: major Mexican mountain ranges (Valencia 2004). They are fre- 0.621d). Different letters show that the mean values for each locality differ at quently found in perturbed areas with a xerophytic shrub type of a¼ 0.05 (Tukey’s test). vegetation, which is also localized in mountain cloud forests (Rzedowski and Rzedowski 2001). Furthermore, Q. castanea is a (PEH: 366.3). Three transects of 1,000 m in each locality were cre- red oak species that possesses characteristics associated with a foun- ated. At each 50 m, the nearest individual morphologically recog- dation tree species (Ellison et al. 2005). For example, Q. castanea is nized pure “Q. castanea” was sampled. the most widely distributed species within the red oak group in Mexico (Valencia 2004); it is a dominant element of the temperate Molecular data forests where it resides (Valencia-Cuevas et al. 2014) and it acts as The 120 individuals (20 individuals per site) that were morphologic- the habitat for different species (Tovar-S anchez et al. 2013). ally recognized as pure Q. castanea were previously analyzed by 14 microsatellite (SSRs) primers (six nSSRs and eight cpSSRs). We Study sites and sampling found an increase in the individual and population genetic diversity Trees that are morphologically recognized as “pure” Q. castanea of Q. castanea populations analyzed here (Valencia-Cuevas et al. were sampled from six populations (20 trees/site), one allopatric 2014) as a result of the interspecific gene flow with other red oaks population of Q. castanea (population 1) and five sympatric stands species (Valencia-Cuevas et al. 2015). between Q. castanea and other red oak species (populations 2–6, Figure 1) through the central part of the TVB. All chosen sites share Canopy endophagous insect communities and the following common traits: geological history [all localities belong associated parasitoids to the central portion of TVB with a formation process that occurred The endophagous insect and parasitoid community structure associ- in a single geological event that began during the Quaternary– ated with Q. castanea was analyzed in the same 120 individuals as Pliocene (Challenger 1998)], weather (sub-humid temperate), alti- in Valencia-Cuevas et al. (2014). These individuals were 8–10 m tude (between 1,800 and 2,500 m), vegetation type (mature oak), (9.126 SE 0.17 m) in height and accounted for 18.3–20.1 m and soil type (volcanic origin or derived from igneous and sediment- 2 2 (19.20 m 6 SE 0.17 m ) of canopy cover. Tree canopies selected for ary rocks). Additionally, these areas present almost no local disturb- sampling were, as far as possible, spatially delimited from others by ance inside the forest because they are under Mexican protection avoiding overlaps. Insect communities were sampled using four ran- standards. This homogeneity among study sites could be useful to domly selected branches (50 leaves per branch) in the middle part of minimize the influence of environmental and spatial factors on in- the crown. Galls and mining leaves collected in each host tree were sect endophagous and parasitoid communities that are associated separated into the morphospecies level, placed in previously vou- with the Q. castanea canopy. chered plastic containers (e.g., locality, host category, etc.) and In addition, the number of associated species with Q. castanea in transported to the laboratory where the insects emerged. Wasps and each sympatric locality ranged from one to five. These species were their parasitoids were identified to the finest taxonomic level. as follows: Q. candicans, Q. crassifolia, Q. crassipes, Q. laurina, Q. mexicana, Q. scytophyla, and Q. urbanii (Appendix 1). The Q. castanea local density (ind/ha) in each site was as follows: Corredor Statistical analysis Biologico  Ajusco Chichinautzin (CBACh: 51.7), Parque Nacional El Genetic diversity of host plant To evaluate the influence of the Q. castanea genetic diversity on can- Tepozteco (PNT: 56.7), Parque Ecologico de la Ciudad de Me ´ xico (PECM: 149.0), Parque Barranca de Tarango (PBT: 161.6), Parque opy endophagous communities and parasitoids, the parameter He Las Penas ~ (PLP: 186.7) and Parque Nacional El Huixteco (expected heterozygosis) was used to analyze the genetic diversity at Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 16 Current Zoology, 2018, Vol. 64, No. 1 the population level, as reported by Valencia-Cuevas et al. (2014). population (He) genetic diversity, S and density of endophagous and Additionally, the Q. castanea individual genetic diversity was esti- parasitoid insects. The model was performed with the lavaan pack- mated using homozygosity by the loci index (HL), a microsatellite- age for R (Rosseel 2011). derived measure that improves heterozygosity estimates in natural populations by weighting the contribution of each locus to the Results homozygosity value based on the allelic variability (Aparicio et al. 2006). The HL is calculated as follows: HL ¼ (RE )/(RE þRE ), Endophagous and associated parasitoid insect h h j where E and E are the expected heterozygosity of the loci that an h j community composition individual bears in homozygosis (h) and heterozygosis (j), respect- The endophagous insect community associated with Q. castanea ively, forms. This index varies between 0, when all loci are heterozy- consisted of 22 species that belong to the following three orders: gous, and 1, when all loci are homozygous. The HL was estimated Hymenoptera (18 species), Lepidoptera (two species), and Diptera using CERNICALIN, an Excel spreadsheet that is available on re- (two species, Appendix 2). In particular, the gall insect group quest. These parameters (He and HL) were used because they are (Hymenoptera: Cynipidae) was represented by eight genera frequently employed to evaluate the influence of both the population (Appendix 2). In terms of the species richness, the most important and individual genetic diversity on the community structure (e.g., genus was Andricus at 38.8% (seven species, Appendix 2). (Tovar-S anchez and Oyama 2006); Tovar-S anchez et al. 2013). Meanwhile, the leaf mining insect group was represented by two families, Diptera and Lepidoptera (Appendix 2, Figure 2). Infestation levels of endophagous insects The parasitoid community was represented by 13 families The species richness (S) of the canopy arthropod community and (Figure 2). The most important family in terms of the genus and spe- their associated parasitoids was estimated at the morpho-species cies richness was Eulophidae (Appendix 2). In addition, we found one inquiline wasp species was associated with gall inducted with level. Each host tree infestation value was estimated as [(number of galls or miners/200 leaves)  100] over the four branches. Analysis Amphibolips hidalgoensis belonging to Synergus genus (Cynipidae). of variance (ANOVA, Model III; Zar 2010) was used to determine We also found two individuals who belong to Encyrtidae and one to differences in the average infestation levels among Q. castanea Megaspilidae. Both families included hyperparasitoids species. populations. Infestation percentage data were corrected as Hyperparasitoids and inquiline insects were not included in the analysis. X¼ arcsin (%) = , and discontinuous data were transformed as X¼ (x) = þ 0.5 (Zar 2010). Finally, a Tukey test was used to deter- mine significant differences between the infestation mean values Infestation levels among populations (Zar 2010). The software used for statistical The mean infestation levels of endophagous insects were signifi- analysis was STATISTICA 8.0 (Statsoft 2007). cantly different among the Q. castanea populations (F ¼ 5, 114 42.688, P< 0.0001). We did not detect an infestation level pattern over the natural genetic diversity gradient that was previously recog- Influence of Q. castanea genetic diversity, host plant density, and nized in Q. castanea populations. In general, the infestation levels red oak species richness on canopy insects had the following relationship (mean6 SE): PNT (12.986 We used a multiple regression approach to examine whether the 1.92)¼ PECM (14.786 0.74)< PEH (18.616 0.73)¼ CBACh Q. castanea genetic diversity levels [population (He) and individual (HL)] and two ecological factors (Q. castanea density and red oak (24.456 1.22)< PLP (26.236 1.52). Finally, we found that there is species richness) influence the canopy endophagous insect and asso- no relationship between the infestation levels of gall forming insects and the parasitoid density (r ¼ 0.2, r ¼ 0.13, P ¼ 0.17). ciated parasitoids. Specifically, this analysis was useful to determine the relative contribution from each factor on the species richness variation and endophagous and parasitoid insect density. We used a Influence of Q. castanea genetic diversity, host plant density, and standard least squares model with partial (type III sums of squares) red oak species richness on canopy insects error structure and the He, HL, host density, and oak richness as In general, our results showed that the Q. castanea genetic diversity our factors. We excluded the variables that showed a correlation co- levels (population and individual), host tree density, and red oak efficient >0.6 to improve the analysis. Considering that endopha- species richness influence the community structure of endophagous gous insects are resources for parasitoids, we were interested in and parasitoid canopy insects (Table 1). Specifically, we found that determining whether the density and species richness of endopha- the HL and oak richness had a significant positive effect on the S of gous insects can predict the density and species richness of the asso- endophagous insects, explaining 10.7% and 5.6%, respectively, of ciated parasitoids. Therefore, we used simple linear regressions. The the variation of this metric. In contrast, the He had a significant software used for statistical analysis were STATISTICA 8.0 (Statsoft negative effect on the S of endophagous insects, explaining 13.6% 2007) and Species Diversity and Richness version 3.03 (Henderson of the variation in this metric (Table 1). and Seaby 2002). We found that the HL had a significant positive influence on the We constructed one structural equation model (SEM) to estimate endophagous insect density, explaining the 11.1% of the variation. the causal relationships between the host plant genetic diversity (He, In contrast, the host density had a significant negative influence on HL) and ecological (host plant density and red oak species richness) the endophagous insect density, explaining 4.1% of the variation and community (S and density of endophagous and parasitoid in- (Table 1). sects) variables. Based on a previous study (Valencia-Cuevas et al. The species richness of parasitoid insects was significantly posi- 2014) and literature review, we anticipated what causal paths may tively influenced by the HL and host density, explaining 5.6% and be important. For the model, we considered the host plant density 3.5%, respectively, of the variation. In contrast, the species richness and red oak species richness as independent variables. The depend- of parasitoid insects was significantly negatively influenced by the ent variables that we examined were the individual (HL) and oak richness, explaining 9.2% of the variation (Table 1). Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Valencia-Cuevas et al.  Dynamics of trophic interactions 17 Gall-forming wasps genus (Cynipidae) Leaf mining insect families Parasitoid insect families Figure 2. Canopy endophagous insects (gall-forming wasps and leaf mining insects) and parasitoid composition associated to Q. castanea. Table 1. Multiple regression analysis testing the influence of 1.-individual (HL) and population genetic diversity of Q. castanea (He), 2.-host density, and 3.-red oak species local community richness on species richness and density of endophagous insect and associated parasit- oids to Q. castanea in the Transmexican Volcanic Belt Species richness Density df SS FP % Variation df SS FP % Variation Endophagous insects He 1 9.934 11.983 0.000 6.2 1 1.260 0.475 0.490 0.4 HL 1 53.220 64.194 0.000 33.2 1 36.845 13.893 0.000 7.5 Host density 1 0.000 0.007 0.927 0.0 1 31.395 11.838 0.000 5.1 Oak richness 1 4.173 5.034 0.026 2.6 1 10.549 3.977 0.048 7.2 Parasitoid insects He 1 0.004 0.156 0.693 0.1 1 0.207 0.973 0.326 0.9 HL 1 0.328 11.095 0.001 8.6 1 2.219 10.384 0.001 9.6 Host density 1 0.111 3.764 0.055 2.9 1 1.412 6.612 0.011 6.0 Oak richness 1 0.207 7.005 0.009 5.4 1 2.066 9.673 0.002 8.4 We also found that the HL and host density had a significant the S and density of endophagous and parasitoid insects. However, positive influence on the parasitoid insect density. The relative con- the He was negatively correlated with the S of endophagous insects. tributions of the abovementioned factors on the variation in the In contrast, the HL showed a positive influence on the analyzed parasitoid density were 5.1% and 5.9%, respectively. In contrast, community parameters. Similarly, ecological variables had a signifi- the oak richness had a significant negative influence on the parasit- cant influence on the associated endophagous and parasitoid crea- oid insect density, explaining 10.5% of the variation (Table 1). tures (Figure 3; Table 2). In general, the HL was the factor that explained the highest per- Finally, this model explained 25.75% and 16.24% of the S and centage of variation in the analyzed community parameters. density of endophagus insects, respectively. Additionally, 12% and Additionally, the proportion of the total variance explained by the 8.91% of the S and density of parasitoid insects, respectively, were plant genotype was lower for parasitoids than for endophagous in- explained with this model (Figure 3). sects (Table 1). When the relationship between the gall and parasit- oid density was analyzed, there was no significant relationship 2 Discussion (r ¼ 0.02; P ¼ 0.17). In contrast, the gall and parasitoid richness showed a significant positive relationship (r ¼ 0.12; P< 0.0001). In this study, we simultaneously evaluated the influence of genetic Figure 3 shows the partial correlation coefficient for each path. attributes of Q. castanea (individual and population genetic diver- In all cases, the proposed paths were significant. The only exception sity) and two ecological factors (host density and red oak species was the relationship between the host plant density and parasitoid richness) on two different trophic levels of the canopy arthropod density. In particular, the He and HL had a significant influence on community, endophagous insects, and associated parasitoids. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Abundance of arthropods (%) 18 Current Zoology, 2018, Vol. 64, No. 1 Figure 3. Path model. Solid paths are statistically different from 0 (P< 0.05), where dotted path is not. Path widths are proportional to the standardized regression coefficients. Only the coefficients for significant paths are shown. The R of the endogenous variables are inside of the boxes. Table 2. Coefficient value, standard errors, Z scores, and P values host plants, which can influence the abundance, distribution, and di- for the SEM versity of the associated species, in this type of system (Vellend and Geber 2005). Therefore, common garden studies can be a useful ap- Path Estimate SE Z value P proach for comparing the effects of the genetic diversity of Q. casta- He ! S_endophagous 1.249 0.243 5.134 0.000 nea and other ecological variables on the associated arthropods in S_ oaks ! S_endophagous 0.213 0.064 3.351 0.001 both experimental settings and wild populations. HL ! S_endophagous 0.320 0.081 3.970 0.000 In general, we found a significant positive effect of the genetic di- HL ! endophagous density 3.363 0.952 3.531 0.000 versity levels (HL)of Q. castanea on the S and density of endopha- S_oaks ! endophagous density 1.602 0.761 2.106 0.035 gous insects. This result was supported by path analysis. A similar Host plant density ! endophagous 0.010 0.003 3.175 0.001 response has been reported in phytophagous insect communities density that are associated with different foundation species [e.g., poplars HL ! S_parasitoids 0.259 0.102 2.541 0.011 (Whitham et al. 2006); willows (Hochwender and Fritz 2004); euca- S_oaks ! S_parasitoids 0.147 0.041 3.570 0.000 lyptus (Dungey et al. 2000); and oaks (Tovar-S anchez and Oyama S_oaks ! parasitoid density 0.465 0.151 3.082 0.002 2006; Tovar-S anchez et al. 2015a,b)]. For example, Tovar-S anchez Host plant density ! parasitoid 0.001 0.000 1.767 0.077 density et al. (2013) reported that the H variation of the Q. crassipes and HL ! parasitoid density 0.694 0.273 2.543 0.011 Q. castanea arthropod communities was positive and significantly S_oaks ! He 0.225 0.011 20.408 0.000 influenced by the individual genetic diversity of the host. S_oaks ! HL 0.126 0.037 3.440 0.001 Additionally, recent studies in Q. crassifolia (Tovar-Sanchez et al. 2015a) showed that individual genetic diversity had a significant Notes: He, population genetic diversity; HL, individual genetic diversity; positive influence on the S and H of the canopy arthropods during S_oaks, oak species richness; S_endophagous, endophagous species richness; the dry and rainy seasons, respectively. It has been proposed that S_parasitoids, parasitoid species richness. increasing the genetic diversity of the host plant can generate changes in its morphological (Lambert et al. 1995; Gonz alez- The results in this study are in accordance with those in other studies Rodr ıguez et al. 2004; Tovar-S anchez and Oyama 2004), pheno- that have shown the genetic diversity of foundation species has a sig- logical (Hunter et al. 1997), architectural (Whitham et al. 1999; nificant effect on the associated community (Bangert and Whitham Bangert et al. 2005), and chemical (Fritz 1999; Cheng et al. 2011) 2007; Hughes et al. 2008; Whitham et al. 2012; Crutsinger 2016). characteristics. These changes can be translated into a broader mo- Additionally, we found that insect communities associated with Q. saic of resources and conditions that can be beneficial for canopy castanea are determined by both host plant genetic attributes and arthropods. ecological factors, such as the host tree density and local red oak Considering that the arthropod community structure could be species richness. influenced by several factors beyond the host genetic diversity Studies in natural systems, as presented in this report, offer the (Johnson and Stinchcombe 2007; Hughes et al. 2008; Tack et al. realism of the wild; however, it is important to considerer that it is 2012), the approach used in the present study offers a more realistic difficult to control the variables related to the spatial location of scenario than the other studies that only evaluate the role of host Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Valencia-Cuevas et al.  Dynamics of trophic interactions 19 plant genetic attributes on the community structure (Hersch-Green should be easy to find (Sholes 2008). Additionally, a high resource et al. 2011). Although these studies have helped demonstrate that concentration could support both more herbivore species and higher intraspecific genetic variation can have an effect beyond an individ- densities of each herbivore species (Root 1973; Kareiva 1983). ual’s phenotype, they likely do not accurately estimate its effective Additionally, this effect will be the strongest for specialist herbivores size. The most commonly employed method in these approaches has (Stephens and Myers 2012). Under this scenario, we suppose that been the collection of multiple genotypes from diverse and often dis- lower Q. castanea densities promote low resource concentration for tant environments as well as to replicate these genotypes into single endophagous insects; as a result, their densities are less favored, as common environments where the environmental variation is mini- seen in other systems (Ostergard and Ehrle ´ n 2005; Sholes 2008). mized (Tack et al. 2012). As a result, these studies provide little in- This hypothesis is also suggested by our path analysis in which there formation regarding the importance of the plant genotype or genetic was a significant negative relationship between the host plant dens- variation compared with other factors that also influence multi- ity and endophagous insect density. In contrast, the path analysis trophic communities. In our study, we simultaneously evaluated the failed to show that the host density also affects the parasitoid dens- influence of genetic attributes of Q. castanea (individual and popu- ity. In addition, we found that there is no relationship between gall lation genetic diversity) and two ecological factors (host density and forming insects and parasitoid density. Both results led us to think red oak species richness) on canopy insect community in natural that the parasitoid insect densities are not mediated by resource conditions. This experimental design allowed us to more accurately availability (endophagous insect density), but they are probably quantify the influence of the effects of three different variables on related to the host plant or prey quality, as has been reported in community structuring. other studies (e.g., Fritz et al. 1997; Harvey et al. 2003; Sch€ adler In contrast, some studies have not found significant effects of et al. 2010). For example, Harvey et al. (2003) and Fritz et al. plant genetics on associated communities. For example, Tack et al. (1997) demonstrated differences in the performance of parasitoids, (2010) found that genetic diversity had little influence on the which depend on the host plant quality. From this perspective, endophagous insect community structure (gallers, leafminers, and Sch€ adler et al. (2010) reported that parasitoid abundance may be leafrollers) of Q. robur in Finland. Similar results were reported by correlated with the quality of host plants. Considering these state- Castagneyrol et al. (2012), who found that the genetic attributes of ments, it is likely that certain performance traits of parasitoids asso- the host plant had no significant effect on the phytophagous insect ciated with Q. castanea are affected by the quality of the host plant community (endophagous and ectophagous) of Q. robur in France. or endophagous insect prey, suggesting that the host plant’s genetic In the case of Q. castanea, previous studies have shown high gen- attributes can influence parasitoid populations via plant quality or etic diversity levels (Valencia-Cuevas et al. 2014) as a result of inter- prey consumption. It is important to emphasize that we did not specific gene flow with three of its associated red oak species in the measure the host plant or endophagous insect quality in this study; Transmexican Volcanic Belt (Valencia-Cuevas et al. 2015). In this however, addressing this issue in future work could help accept or scenario, it is possible that the Q. castanea genetic diversity levels reject these hypotheses. Moreover, the oak species richness also had are sufficient for the endophagous insect community to have an ob- a significant influence on the endophagous species richness. Previous servable response. studies in Q. crassifolia (Tovar-S anchez et al. 2015a) revealed a phe- It has been proposed that the direct effects of genetically based nomenon known as “associational susceptibility” (Brown and Ewel plant traits on herbivores may also indirectly extend to the next tro- 1987) in which plant species present with greater abundance and di- phic level, impacting predators and parasitoids (Johnson and versity of herbivores when they are spatially associated with hetero- Agrawal 2005; Crutsinger 2016). From this perspective, we ex- specific neighbors. This phenomenon probably occurs in Q. pected that the endophagous insect species richness directly depends castanea. on the genetic attributes of the host plant, which has indirect posi- In this study, we observed significant differences in the endopha- tive effects on the parasitoid community richness. This hypothesis gous insect infestation levels associated with Q. castanea among dif- was supported in this study because we found that the Q. castanea ferent localities. The occurrence of different response patterns has genetic diversity levels influenced the canopy parasitoid insects. been attributed to differences in the host plant genetic characteristics When the relationship between parasitoid species richness and and genetic mechanisms that determine the inheritance of resistance endophagous species richness was examined, we found a significant characteristics (Boecklen and Spellenberg 1990; Fritz et al. 1994; positive relationship (r ¼ 0.12; P< 0.0001). This result demon- Strauss 1994). In a previous study, we revealed the existence of an strates the high degree of specialization between parasitoid species array of homozygous and heterozygous genotypes in the Q. castanea and their host gall inductor species (Sanchez et al. 2013). Finally, we populations that were analyzed in this research (Valencia-Cuevas suggest that the genetic diversity of Q. castanea had an indirect ef- et al. 2014). Therefore, we presumed that different Q. castanea fect on the S of parasitoid insects, which was mediated through the genotypes inherit different mechanisms which, in turn, establish the effects on the S of endophagous insects. These results are consistent different resistance patterns observed here. In addition, it has been with reports by Bailey et al. (2006) and Johnson (2008). Overall, reported that the host plant resistance characteristics may be differ- these results show that genetic variation in plants can be an import- entially expressed in different environments (Fritz 1999). The Q. ant factor governing the herbivore population dynamics and tritro- castanea populations in this study are distributed in the central por- tion of the TVB, whose formation process occurred in a single geolo- phic interactions that involve plants, herbivores, and parasitoids. According to the results obtained in this study, we suggest that Q. gical event that began during the Quaternary–Pliocene (Challenger castanea is a foundation species whose genetic diversity levels have 1998). This observation makes us suppose that these populations direct effects on the endophagous insect community. have had the same evolutionary origin, which has minimized the en- In addition, we found that ecological parameters, such as the vironmental variation among localities and the influence of such host density and red oak species richness, influence the canopy insect variability on the endophagous insect infestation levels among the community. It has been suggested that high host density should pro- study sites. Hence, we suggest that the variation in the expression of vide herbivores with substantial edible biomass and the biomass the resistance characteristics of Q. castanea through the localities Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018 20 Current Zoology, 2018, Vol. 64, No. 1 Cheng D, Vrieling K, Klinkhammer PGL, 2011. The effect of hybridization on found in this work is related to the genetic characteristics of the host secondary metabolites and herbivore resistance: implications for the evolu- plant in each population. tion of chemical diversity in plants. Phytochem Rev 10:107–117. In conclusion, the multifactorial approach used in this study Crawford KM, Rudgers JA, 2013. Genetic diversity within a dominant plant helped to determine the influence of genetic and ecological factors outweighs plant species diversity in structuring an arthropod community. on the arthropod community structure associated with Q. castanea, Ecology 94:1025–1035. as well as to obtain a more realistic understanding of natural condi- Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC et al., 2006. tions. 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Locality name, state, and red oak species associated to Q. castanea in the Transmexican Volcanic Belt Locality State Oak species Corredor Biologico  Ajusco-Chichinautzin Morelos Q. castanea Parque Nacional El Tepozteco Morelos Q. castanea, Q. crassipes Parque Ecologico  de la Ciudad de Me ´ xico Mexico City Q. castanea, Q. crassipes, Q. laurina Parque Barranca de Tarango Mexico City Q. castanea, Q. crassipes, Q. laurina, Q. mexicana Parque Ecologico  Las Penas ~ Mexico State Q. castanea, Q. crassipes, Q. laurina, Q. mexicana, Q. crassifolia Parque Ecologico  El Huixteco Guerrero Q. castanea, Q. crassifolia, Q. laurina, Q. candicans, Q. urbanii, Q. scytophyla Appendix 2. Community composition of canopy endophagous and parasitoid insects associated to Q. castanea in the Transmexican Volcanic Belt Orden Family Genus Species Endophagous insects Hymenoptera Cynipidae Amphibolips Amphibolips hidalgoensis Andricus Andricus nr sphaericus Disholcaspis A. nievesaldreyi A. linaria group A. tuberoses group A. nr bonansaeai A. sp. 1 A. sp. 2 Disholcaspis nr pallens D. sp 1 Antron Antron sp. Erythres Erythres hastata Kokkocynips Kokkocynips doctorrosae Neuroterus Neuroterus nr junctor N. sp. 1 N. sp. 2 N. sp. 3 Melikaiella Melikaiella amphibolensis Diptera Cecidomyiidae Cecidomyiidae sp.1 Chloropidae Chloropidae sp. 1 Lepidoptera Bedellinae Bedellia sp. Gelechiidae Gelechiidae sp. Parasitoid insects Apidea Apidea sp.1 Bethylidae Bethylidae sp.1 Braconidae Braconidae sp.1 Elasmidae Elasmus Elasmus sp. Eulophidae Cirruspilus Cirruspilus sp. Clostocerus Clostocerus sp. Euplectrus Euplectrus sp. Tetrastichinae Tetrastichinae sp. Eulophidae sp. 1 Eulophidae sp. 2 Eulophidae sp. 3 Eupelmidae Brossema Brossema sp. Eurytomidae Eurytoma Eurytoma sp. Figitidae Figitidae sp. 1 Ormyridae Ormyrus Ormyrus sp. Platygastridae Scelionidae Scelionade sp. Platigastridae sp. 1 Pteromelidae Pteromelidae sp. 1 Sphecidae Sphecidae sp. 1 Torymidae Torymus Torymus sp. Downloaded from https://academic.oup.com/cz/article-abstract/64/1/13/3075076 by Ed 'DeepDyve' Gillespie user on 16 March 2018

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