Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus

Abstract. 1. Community level oak–tannin–insect patterns have been largely unexplored since Paul Feeny's ground‐breaking research. Two hypotheses were tested for Quercus velutina and Q. alba in the Missouri Ozarks: abundance and richness of leaf‐chewing herbivores are negatively correlated with foliar condensed tannin concentrations and variation in condensed tannin concentrations explains variation in herbivore community structure. 2. In 2001, foliar condensed tannins in the understorey and canopy of these two oak species were quantified simultaneously with censuses of herbivores in May, during leaf expansion, and in June and August, when leaves were fully expanded. Thirty‐eight of the 134 species encountered had densities sufficient to be analysed individually (n = 10). Of those, Acronicta increta (Noctuidae) and Attelabus sp. (Curculionidae), both oak specialists, were negatively correlated with condensed tannins in the canopy of Q. alba. One additional specialist, Chionodes pereyra (Gelechiidae), was marginally negatively correlated with condensed tannins in the understorey of Q. velutina. Understorey species richness of May Q. velutina herbivores was negatively correlated with condensed tannins, as were total canopy insect density and species richness of August herbivores on Q. alba. 3. Principal component analysis (PCA) of insect abundances indicated that understorey and canopy Q. velutina and Q. alba had different communities of leaf‐chewing insects. Furthermore, condensed tannin levels contributed significantly to variation in PCA scores for Q. velutina, explaining 25% of the total variation. 4. Overall, these results indicate that specialists were more likely than generalists both to correlate negatively with condensed tannins and to occur in lower tannin habitats; abundance and richness of both early and late season fauna correlated negatively with tannins; and species were more likely to correlate negatively with condensed tannins when feeding on Q. alba than on Q. velutina and when feeding in the canopy than in the understorey. Future studies of tannin–insect interactions should manipulate leaf quality in combination with manipulations of other factors that likely influence community structure.     

Discovery of an oak gall wasp (Hymenoptera: Cynipidae) inducing galls on deciduous oak trees in India

We report for the first time the occurrence of an oak gall wasp Andricus mukaigawae (Mukaigawa) (Hymenoptera: Cynipidae) on the deciduous oak Quercus griffithii Hook. F & Thomson ex Miq. in India. Andricus mukaigawae is the only cynipid species that has been observed to induce galls on deciduous oak species in India to date. In addition, this is the first record of a gall wasp species with a distribution extending all the way from the eastern Palearctic region to the Indian subcontinent, suggesting the existence of a close relationship between cynipid faunas on deciduous oak trees in the two regions.     

Differential effects of host plant hybridization on herbivore community structure and grazing pressure on forest canopies

Interspecific hybridization in plants is known to have ecological effects on associated organisms. We examined the differences in insect herbivore community structure and grazing pressure on tree canopy leaves among natural hybrids and their parental oak species. We measured leaf traits, herbivore community structure, and grazing pressure on leaves of two oak species, Quercus crispula and Q. dentata, and their hybrids. The concentration of nitrogen in canopy leaves was greater in hybrids and in Q. dentata than in Q. crispula. The concentration of total phenolics was lower in hybrids than in Q. crispula. The concentration of condensed tannin was greater in hybrids than in Q. crispula. Relative herbivore abundance and species richness were greater on oak hybrids than on either parental species; herbivore species diversity and composition on hybrids were close to those on Q. crispula. Herbivore grazing pressure was lower on hybrids and Q. dentata than on Q. crispula. There was a negative correlation between herbivore grazing pressure and leaf nitrogen, suggesting that interspecific variation among oak taxa in herbivore pressure may be explained by leaf nitrogen; variation in herbivore community structure among oak taxa is likely to be controlled by polygenic leaf traits. Differing responses of (1) herbivore community structure and (2) herbivore grazing pressure to host plant hybridization may play important roles in regulating herbivore biodiversity in cool‐temperate forest canopies.     

Dietary circumvention of acorn tannins by blue jays

Blue jays consume large quantities of acorns to fuel energy-demanding caching flights in the fall. Yet blue jays possess no known physiological adaptation to counter the negative effects of a high tannin diet on protein digestion. Dietary experiments were conducted to determine if blue jays could subsist on an acorn-only diet, and if they could not, to determine whether supplements of acorn weevil larvae (Curculio), present inside acorns, enabled them to maintain their mass. Comparative tannin assays also were conducted on Lepidobalanus (low tannin; white oak) and Erythrobalanus (high tannin; pin oak) acorns using radial diffusion assay. Captive jays consumed considerable acorn material, yet were unable to maintain mass on ad lib. acorn-only diets or on an acorn +1.5 g larvae/day supplement. There were no significant differences in mass loss between high and low tannin diets. In contrast, blue jays were able to stabilize mass on a diet of acorns +5.0 g larvae supplement/day. These results suggest that acorn weevil larvae, or perhaps other insects, counteract the effects of acorn tannins in the jay diet allowing jays to subsist largely on acorns during the fall caching season. Oak demographic processes may be partly regulated by a tri-trophic relationship among plant, insect and bird. Acorn weevil larvae, considered damaging to oak populations, may actually facilitate oak recruitment and population vagility in the long-term.     

The role of leaf defensive traits in oaks on the preference and performance of a polyphagous herbivore,Orgyia vetusta

1. Leaves possess traits that mediate the preference and performance of herbivores. Most evidence for the importance of leaf traits as defences against herbivory comes from studies of few model plant species. 2. In a phylogenetically explicit comparison, I explain the differences in preference and performance of tussock moth (Orgyia vetusta Boisduval) larvae on leaves of 27 oak (Quercus) species using nine putative leaf defences. 3. The preference for an oak species correlated positively with the survival of caterpillars. The correlation between preference and performance did not differ between oak species native to the range of tussock moth versus those from outside the herbivore's range. 4. The first principal component of leaf traits predicted survival of caterpillars on oak leaves but only marginally predicted their preference between oak species. A multiple regression model showed that evergreenness, toughness, and condensed tannin content were the best predictors of caterpillar survival, and leaf toughness was the best predictor of host preference. 5. Generalist caterpillars may accurately assess the value of novel food sources. Moreover, many leaf traits that have been found to affect herbivory within a plant species can also be used to predict the fitness of a generalist herbivore between species.     

Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species

Phytochemical coevolution theory posits that specialist herbivores will be less sensitive than generalists to the defensive compounds of their host. On the other hand, both types of herbivores should allegedly be similarly sensitive to ‘quantitative’ defences, such as tannin compounds. In this paper, we critically examine the biological effects of two types of tannins: vescalagin (a quantitatively dominant hydrolysable tannin of Quercus robur), and a mix of condensed tannins. In a phylogenetically controlled design, we compare the response of two specialist moth species (Dichonia aprilina and Catocala sponsa) and two generalist species (Acronicta psi and Amphipyra pyramidea) to four artificial diets: a control diet, a diet with 50 mg g^?1 vescalagin, a diet with 15 mg/g condensed tannins, and a diet with both 50 mg g^?1 vescalagin and 15 mg g^?1 condensed tannins. Overall, we find drastic effects of vescalagin and pronounced differences in the responses of generalist and specialist herbivores, but no detectable effects of condensed tannins, and no interaction between the two types of compounds. More specifically, vescalagin reduced the growth of generalist species to one‐half of control levels over 72 h. The compound served as a strong feeding deterrent to generalists, reducing ingestion rates by two‐thirds. Vescalagin also reduced the metabolic and growth efficiency of generalist species to between 16% and 56% of control levels – effects which were lacking or even reversed in specialist species. These patterns suggest that vescalagin forms an important part of the oak's defence against herbivores, and that specialist species have adapted to deal with such substances. In terms of biological effects, condensed tannins seem much less important. Given a quantitative dominance of hydrolysable tannins over condensed tannins in oak leaves, and a seasonal decline in overall tannin levels, these findings contradict the previous notion that widespread spring feeding among oak herbivores could be attributed to tannins.     

Environmentally-based maternal effects: a hidden force in insect population dynamics?

Summary The nutritional environment of the parental generation of the polyphagous gypsy moth, Lymantria dispar, can significantly influence the growth and reproductive potential of the next generation through environmentally-based maternal effects. In the first experiment, members of the parental generation were reared on red oak trees (Quercus rubra L.) with known defoliation and phenolic levels. Diet in the offspring generation was homogeneous (synthetic diet). With genetic effects accounted for 1) offspring attained greater pupal weights when their mothers fed on trees with higher leaf damage levels, 2) daughters had a shorter prefeeding stage, a trait associated with dispersal tendency, when their mothers experienced higher condensed tannin levels, and 3) sons had lower pupal weights when their mothers experienced greater condensed tannin levels. In the second experiment, members of the parental generation were reared on either red or black oak (Q. velutina) trees. Offspring of each mother were divided among four diets: red oak, chestnut oak (Q. prinus L.), a standard synthetic diet, and a low-protein synthetic diet. The parental host species accounted for 24% of the variation in daughters' development time; offspring diet accounted for 52%. When mothers were reared on black oak rather than red oak, their offspring developed significantly faster when the F1 diet was chestnut oak. Environmentally-based maternal effects can significantly influence the expression of offspring dispersal potential, growth rate, and offspring fecundity. These traits contribute to natality and survival in natural populations and, hence, to population growth potential. Theoretical models of insect population dynamics demonstrate that the presence of a time delay in a density dependent response can induce destabilization. Maternal effects act on a time delay and may participate in the destabilization characteristic of outbreak species.     

Sources of mortality for a cynipid gall-wasp (Dryocosmus dubiosus (Hymenoptera: Cynipidae)): The importance of the Tannin/Fungus interaction

Summary Emergence success was determined for 1300 galls of the cynipid waspDryocosmus dubiosus. Galls were collected throughout a single host tree (a California coast live oakQuercus agrifolia). Each gall was reared individually in small gelatin capsules. For each gall data was recorded on 17 parameters characterizing hyperparasitism, fungal infestation, leaf tannin levels, inter- and intraspecific competition, and spatial position within the tree. Using contingency table analysis and logistic regression, we determined that the most significant factors influencing the success ofD. dubiosus galls are 1) fungal infestation and 2) chalcid hyperparasitism, both having negative effects. Of the factors investigated we found that leaf tannin level had the strongest influence on the degree of fungal infestation. Fungal infestation, in turn, is lowest in regions of high leaf tannins.     

Differential effects of sugar maple, red oak, and hemlock tannins on carbon and nitrogen cycling in temperate forest soils

Tannins are abundant secondary chemicals in leaf litter that are hypothesized to slow the rate of soil-N cycling by binding protein into recalcitrant polyphenol–protein complexes (PPCs). We studied the effects of tannins purified from sugar maple, red oak, and eastern hemlock leaf litter on microbial activity and N cycling in soils from northern hardwood–conifer forests of the northeastern US. To create ecologically relevant conditions, we applied tannins to soil at a concentration (up to 2 mg g⁻¹ soil) typical of mineral soil horizons. Sugar maple tannins increased microbial respiration significantly more than red oak or hemlock tannins. The addition of sugar maple tannins also decreased gross N mineralization by 130% and, depending upon the rate of application, decreased net rates of N mineralization by 50–290%. At low concentrations, the decrease in mineralization appeared to be driven by greater microbial-N immobilization, while at higher concentrations the decrease in mineralization was consistent with the formation of recalcitrant PPCs. Low concentrations of red oak and hemlock tannins stimulated microbial respiration only slightly, and did not significantly affect fluxes of inorganic N in the soil. When applied to soils containing elevated levels of protein, red oak and hemlock tannins decreased N mineralization without affecting rates of microbial respiration, suggesting that PPC formation decreased substrate availability for microbial immobilization. Our results indicate that tannins from all three species form recalcitrant PPCs, but that the degree of PPC formation and its attendant effect on soil-N cycling depends on tannin concentration and the pool size of available protein in the soil.     

Effects of subsidy quality on reciprocal subsidies: how leaf litter species changes frog biomass export

Spatial subsidies are resources transferred from one ecosystem to another and which can greatly affect recipient systems. Increased subsidy quantity is known to increase these effects, but subsidy quality is likely also important. We examined the effects of leaf litter quality (varying in nutrient and tannin content) in pond mesocosms on gray treefrog (Hyla versicolor) biomass export, as well as water quality and ecosystem processes. We used litter from three different tree species native to Missouri [white oak (Quercus alba), northern red oak (Quercus rubra), and sugar maple (Acer saccharum)], one non-native tree [white pine (Pinus strobus)], and a common aquatic grass [prairie cordgrass (Spartina pectinata)]. We found that leaf litter species affected almost every variable we measured. Gray treefrog biomass export was greatest in mesocosms with grass litter and lowest with white oak litter. Differences in biomass export were affected by high tannin concentrations (or possibly the correlated variable, dissolved oxygen) via their effects on survival, and by primary production, which altered mean body mass. Effects of litter species could often be traced back to the characteristics of the litter itself: leaf nitrogen, phosphorus, and tannin content, which highlights the importance of plant functional traits in affecting aquatic ecosystems. This work and others stress that changes in forest species composition could greatly influence aquatic systems and aquatic–terrestrial linkages.     

Costs and benefits of defense by tannins in a neotropical tree

Summary The costs and benefits of defense by tannins were investigated for a neotropical tree, Cecropia peltata L. (Moraceae). Seedlings of equal age were grown under uniform conditions in a greenhouse for 18 months. Within a plant, leaf tannin concentrations measured in different years were highly correlated. Tannin concentrations differed substantially among individuals; plants with high tannin content had lower damage levels in herbivory experiments. The effects of tannin on herbivory appeared to be dosage dependent. There was, however, a cost associated with tannin production in terms of reduced leaf production.     

The predictability of traits and ecological interactions on 17 different crosses of hybrid oaks

Herbivory on hybrid plants has the potential to affect patterns of plant evolution, such as limiting gene-flow through hybrids, and can also affect herbivore biodiversity. However, few studies have surveyed multiple hybrid species to identify phylogenetic patterns in the inheritance of plant traits that may drive herbivory. We surveyed 15 leaf traits and patterns of chewing, mining, and galling herbivory in a common garden of 17 artificially crossed hybrid oak species and each of their parental species over a 2-year period. Using a phylogeny of oaks, we tested whether hybrids that resulted from more divergent parents received more herbivory than those derived from closely related parents (as would be predicted by a build-up of incompatibilities in defensive systems over evolutionary time) and found only marginal evidence in support of this. We found that chewing damage to hybrids was weakly predicted by the relatedness of a parental species to the single native oak. The levels of chewing and mining herbivory on hybrids were typically intermediate to those of their parental species, though less than the parental mean for chewing damage in 2008. Most leaf traits of hybrids were also intermediate to those of their parental species. There was no clear pattern in terms of an association between 11 species of cynipid gall wasps and hybrids. The patterns of (1) intermediate levels of herbivory on hybrids and (2) no trend in herbivory on hybrids based on the phylogenetic relatedness of parental species suggest that herbivory may not play a general role in limiting hybrid fitness (and thus gene-flow through hybrids) in oaks.     

Different responses to shade of evergreen and deciduous oak seedlings and the effect of acorn size

An evergreen oak species, Cyclobalanopsis multinervis, and a deciduous oak species, Quercus aliena var. acuteserrata were grown from acorns under two light levels (full sunlight and shade at about 18 % of full sunlight, simulating the light intensities in forest clearings and gaps, respectively) for one growing season. Three hypotheses were tested: (i) the deciduous species grows faster than the evergreen species in forest gaps and clearings; (ii) the deciduous species responds more strongly in terms of growth and morphology to variation in light climate than the evergreen species; and (iii) seedling size is positively correlated to acorn size. The results showed: (i) at both light levels, the deciduous seedlings gained significantly more growth in biomass and height than the evergreen seedlings; (ii) both species produced significantly more biomass in full sunlight than in shade, without showing any significant difference in height between treatments. Increase in light intensity improved the growth of the deciduous seedlings more strongly; (iii) at a similar age, the deciduous seedlings showed a greater response in leaf morphology and biomass allocation to variation in light levels, but when compared at a similar size, biomass allocation patterns did not differ significantly between species; (iv) bigger acorns tended to produce larger seedlings, larger leaf sizes and more leaf area, between and within species. These differences demonstrate that the deciduous species is gap-dependent and has the advantage over the evergreen species in forest gaps and clearings.     

Foliage acceptability to browsing ruminants in relation to seasonal changes in the leaf chemistry of woody plants in a South African savanna

Summary We investigated seasonal changes in food selection by hand-reared kudus and impalas in savanna vegetation in northern Transvaal, South Africa. The acceptability of the leaves of woody plants to these animals was compared with leaf concentrations of nutrients, fibre components and old leaf phenophases. No consistently significant correlation was found between acceptability and any single chemical factor. Based on an a priori palatability classification, discriminant function analysis separated relatively palatable species from unpalatable species in terms of a linear combination of protein and condensed tannin concentrations. The high acceptability of certain otherwise unpalatable species during the new leaf phenophase was related to elevation of protein levels relative to condensed tannin contents. Species were added to the diet during the dry season approximately in the order of their relative protein-condensed tannin difference.     

The Ultimate Basis of the Caching Preferences of Rodents, and the Oak-Dispersal Syndrome: Tannins, Insects, and Seed Germination

We have shown that eastern gray squirrels and other animalsconsistently prefer to store intact acorns from the red oakgroup rather than those from the white oak group. We hypothesizedthat the ultimate advantage to this behavior comes from thedormancy of red oak acorns. Acorns of the white oak group germinateearly in the autumn; thus, we hypothesize that avoiding germinationis the primary selective advantage to the preference for cachingred oak acorns. Here, we test two alternative hypotheses toexplain the benefits of this caching preference: 1) storingred oak acorns allows the high tannin concentrations in redoak acorns to decline (making them more palatable), and 2) storingred oak acorns minimizes losses to insects, presuming they areless infested with insects. We also test the effect of germinationschedule on squirrel caching preferences directly, by presentingthem with dormant red oak acorns, and red oak acorns about togerminate. We find no evidence that tannin concentrations inred oak acorns decline, although tannin levels did decline inour white oak acorns. We found high losses to insect infestationsin one white oak species, but a second white oak species lostvery little mass to insects. Finally, we found that germinationschedule directly affects squirrel caching preferences: redoak acorns that are near germination are treated like whiteoak acorns. We conclude that the primary advantage to the preferencefor caching red oak acorns is that they are less perishable,due to their dormancy. We discuss the effects of this preferenceon the dispersal of red and white oak acorns, and the subsequenteffects of differential dispersal on the ecology and evolutionof oaks.     

Elevated CO2 decreases leaf fluctuating asymmetry and herbivory by leaf miners on two oak species

Fluctuating asymmetry (FA) represents small, random variation from symmetry in otherwise bilaterally symmetrical characters. Significant increases in FA have been found for several species of plants and animals in response to various stresses, including environmental and genetic factors. In this study, we investigated the effects of elevated CO₂ on leaf symmetry of two oak species, Quercus geminata and Q. myrtifolia, and the responses of three species of leaf miners and one gall‐making species to random variation in leaf morphology. Leaf FA decreased with an increase in CO₂ concentration. There were fewer asymmetric leaves and lower levels of asymmetry on leaf width and leaf area on elevated CO₂ compared with ambient CO₂. Leaf miners responded to leaf asymmetry, attacking asymmetric leaves more frequently than expected by chance alone. Differences in secondary chemistry and nitrogen (N) content between symmetric and asymmetric leaves may be responsible for these results due to lower levels of tannins and higher levels of N found on asymmetric leaves of Q. myrtifolia and Q. geminata.     

Growth traits of juvenile American chestnut and red oak as adaptations to disturbance

American chestnut (Castanea dentata) was a dominant species in eastern North America prior to the importation of chestnut blight. In light of recent efforts to restore viable populations of chestnut in eastern forests, an increased understanding of its association with other co‐occurring, disturbance‐adapted oak species is necessary. We evaluated crown architecture and leaf morphology in juvenile chestnut and red oak (Quercus rubra) to assess potential differences in establishment strategies of both species. We also investigated differences in nonstructural carbohydrate reserves and whole tree biomass partitioning between species. Seedlings of both species were planted in forest stands treated either with midstory removal or small patch cuts, simulating potential restoration plantings. After 5–7 years, chestnut's allocation to its root system was lower than red oak's, with chestnut saplings instead diverting resources to branches and foliage. Chestnut had lower leaf area index, greater crown projection area, and higher specific leaf area than red oak, indicating the species may have an advantage in shaded understories. There were only minor differences in nonstructural root carbohydrate reserves, between red oak and American chestnut, indicating that chestnut may respond similarly to oak by resprouting after disturbances topkill young saplings. We suggest that American chestnut has morphological and physiological attributes that allow it to function as an opportunistic and plastic species that can utilize gaps to facilitate its canopy recruitment, yet still persist after occasional surface fire. This knowledge can guide restoration strategies for this iconic species of the eastern temperate forest region.     

Gall-inducing insects provide insights into plant systematic relationships

Field surveys of cynipid gall-inducer occurrences on Quercus species were conducted in Florida, North Carolina, and Pennsylvania, USA. All cynipids demonstrated strong host species and organ fidelity. One result of this specialization is effective niche partitioning among cynipids. The host-association patterns of these specialist herbivores should reflect similarities among oaks, thus we clustered oak species according to their cynipid distributions. Cynipids distinguished small differences among their hosts. A dendrogram of oak species based on cynipid distributions was largely congruent with botanical arrangernents. Cynipid occurrences offer information helpful to resolving some aspects of oak systematics. Collaborative efforts between taxonomic botanists and entomologists will be useful in resolving a variety of plant and insect systematic problems.     

Tree resistance to Lymantria dispar caterpillars: importance and limitations of foliar tannin composition

The ability of foliar tannins to increase plant resistance to herbivores is potentially determined by the composition of the tannins; hydrolyzable tannins are much more active as prooxidants in the guts of caterpillars than are condensed tannins. By manipulating the tannin compositions of two contrasting tree species, this work examined: (1) whether increased levels of hydrolyzable tannins increase the resistance of red oak (Quercus rubra L.), a tree with low resistance that produces mainly condensed tannins, and (2) whether increased levels of condensed tannins decrease the resistance of sugar maple (Acer saccharum Marsh.), a tree with relatively high resistance that produces high levels of hydrolyzable tannins. As expected, when Lymantria dispar L. caterpillars ingested oak leaves coated with hydrolyzable tannins, levels of hydrolyzable tannin oxidation increased in their midgut contents. However, increased tannin oxidation had no significant impact on oxidative stress in the surrounding midgut tissues. Although growth efficiencies were decreased by hydrolyzable tannins, growth rates remained unchanged, suggesting that additional hydrolyzable tannins are not sufficient to increase the resistance of oak. In larvae on condensed tannin-coated maple, no antioxidant effects were observed in the midgut, and levels of tannin oxidation remained high. Consequently, neither oxidative stress in midgut tissues nor larval performance were significantly affected by high levels of condensed tannins. Post hoc comparisons of physiological mechanisms related to tree resistance revealed that maple produced not only higher levels of oxidative stress in the midgut lumen and midgut tissues of L. dispar, but also decreased protein utilization efficiency compared with oak. Our results suggest that high levels of hydrolyzable tannins are important for producing oxidative stress, but increased tree resistance to caterpillars may require additional factors, such as those that produce nutritional stress.     

Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes

Little is known about the evolutionary history of most complex multi‐trophic insect communities. Widespread species from different trophic levels might evolve in parallel, showing similar spatial patterns and either congruent temporal patterns (Contemporary Host‐tracking) or later divergence in higher trophic levels (Delayed Host‐tracking). Alternatively, host shifts by natural enemies among communities centred on different host resources could disrupt any common community phylogeographic pattern. We examined these alternative models using two Megastigmus parasitoid morphospecies associated with oak cynipid galls sampled throughout their Western Palaearctic distributions. Based on existing host cynipid data, a parallel evolution model predicts that eastern regions of the Western Palaearctic should contain ancestral populations with range expansions across Europe about 1.6 million years ago and deeper species‐level divergence at both 8–9 and 4–5 million years ago. Sequence data from mitochondrial cytochrome b and multiple nuclear genes showed similar phylogenetic patterns and revealed cryptic genetic species within both morphospecies, indicating greater diversity in these communities than previously thought. Phylogeographic divergence was apparent in most cryptic species between relatively stable, diverse, putatively ancestral populations in Asia Minor and the Middle East, and genetically depauperate, rapidly expanding populations in Europe, paralleling patterns in host gallwasp species. Mitochondrial and nuclear data also suggested that Europe may have been colonized multiple times from eastern source populations since the late Miocene. Temporal patterns of lineage divergence were congruent within and across trophic levels, supporting the Contemporary Host‐tracking Hypothesis for community evolution.