Leaf defenses of subtropical deciduous and evergreen trees to varying intensities of herbivory.

Generally, deciduous and evergreen trees coexist in subtropical forests, and both types of leaves are attacked by numerous insect herbivores. However, trees respond and defend themselves from herbivores in different ways, and these responses may vary between evergreen and deciduous species. We examined both the percentage of leaf area removed by herbivores as well as the percentage of leaves attacked by herbivores to evaluate leaf herbivore damage across 14 subtropical deciduous and evergreen tree species, and quantified plant defenses to varying intensities of herbivory. We found that there was no significant difference in mean percentage of leaf area removed between deciduous and evergreen species, yet a higher mean percentage of deciduous leaves were damaged compared to evergreen leaves (73.7% versus 60.2%). Although percent leaf area removed was mainly influenced by hemicellulose concentrations, there was some evidence that the ratio of non-structural carbohydrates:lignin and the concentration of tannins contribute to herbivory. We also highlight that leaf defenses to varying intensities of herbivory varied greatly among subtropical plant species and there was a stronger response for deciduous trees to leaf herbivore (e.g., increased nitrogen or lignin) attack than that of evergreen trees. This work elucidates how leaves respond to varying intensities of herbivory, and explores some of the underlying relationships between leaf traits and herbivore attack in subtropical forests.

Plant sex influences on riparian communities and ecosystems.

Over the past several decades, we have increased our understanding of the influences of plant genetics on associated communities and ecosystem functions. These influences have been shown at both broad spatial scales and across many plant families, creating an active subdiscipline of ecology research focused on genes-to-ecosystems connections. One complex aspect of plant genetics is the distinction between males and females in dioecious plants. The genetic determinants of plant sex are poorly understood for most plants, but the influences of plant sex on morphological, physiological, and chemical plant traits are well-studied. We argue that these plant traits, controlled by plant sex, may have wide-reaching influences on both terrestrial and aquatic communities and ecosystem processes, particularly for riparian plants. Here we systematically review the influences of plant sex on plant traits, influences of plant traits on terrestrial community members, and how interactions between plant traits and terrestrial community members can influence terrestrial ecosystem functions in riparian forests. We then extend these influences into adjacent aquatic ecosystem functions and aquatic communities to explore how plant sex might influence linked terrestrial-aquatic systems as well as the physical structure of riparian systems. This review highlights data gaps in empirical studies exploring the direct influences of plant sex on communities and ecosystems but draws inference from community and ecosystem genetics. Overall, this review highlights how variation by plant sex has implications for climate change adaptations in riparian habitats, the evolution and range shifts of riparian species and the methods used for conserving and restoring riparian systems.

The influence of weevil herbivory on leaf litter chemistry in dioecious willows.

Leaf litter inputs can influence the structure and function of both terrestrial and adjacent aquatic ecosystems. Dioecy and herbivory are two factors that together have received little attention, yet have the potential to affect the quantity, quality, and timing of riparian litterfall, litter chemistry, and litter decomposition processes. Here, we explore litter chemistry differences for the dioecious Sitka willow (Salix sitchensis Sanson ex. Bong), which is establishing on primary successional habitats at Mount St. Helens (WA, USA) and is heavily infested with a stem-boring weevil (Cryptorhynchus lapathi). Weevil-attacked branches produced summer senesced litter that had significantly higher %N, lower C:N ratios, and lower condensed tannins than litter from branches that were unattacked by the weevil and senesced naturally in the autumn. Weevils more often attack female willows; however, these common litter chemicals did not significantly differ between males and females within the weevil-attacked and -unattacked groups. High-resolution mass spectrometry was used to isolate compounds in litter from 10 Sitka willow individuals with approximately 1500-1600 individual compounds isolated from each sample. There were differences between weevil-attacked litter and green leaf samples, but at this level, there was no clustering of male and female samples. However, further exploration of the isolated compounds determined a suite of compounds present only in either males or females. These findings suggest some variation in more complex litter chemistry between the sexes, and that significant differences in weevil-attacked litter chemistry, coupled with the shift in seasonality of litter inputs to streams, could significantly affect in-stream ecological processes, such as decomposition and detritivore activity.

Synergistic effects: a common theme in mixed-species litter decomposition.

Litter decomposition plays a key role in nutrient cycling across ecosystems, yet to date, we lack a comprehensive understanding of the nonadditive decomposition effects in leaf litter mixing experiments. To fill that gap, we compiled 69 individual studies with the aim to perform two meta-analyses on nonadditive effects. We show that a significant synergistic effect (faster decomposition in mixtures than expected) occurs at a global scale, with an average increase of 3-5% in litter mixtures. In particular, low-quality litter in mixtures shows a significant synergistic effect, while additive effects are observed for high-quality species. Additionally, synergistic effects turn into antagonistic effects when soil fauna are absent or litter is in very late stages of decomposition (near-humus). In contrast to temperate and tropical areas, studies in boreal regions show significant antagonistic effects. Our two meta-analyses provide a systematic evaluation of nonadditive effects in mixed litter decomposition studies and show that litter quality alters the effects of litter mixing. Our results indicate that nutrient transfer, soil fauna and inhibitory secondary compounds can influence mixing effects. We also highlight that synergistic and antagonistic effects occur concurrently, and the final litter mixing effect results from the interplay between them.

Global synthesis of the temperature sensitivity of leaf litter breakdown in streams and rivers.

Streams and rivers are important conduits of terrestrially derived carbon (C) to atmospheric and marine reservoirs. Leaf litter breakdown rates are expected to increase as water temperatures rise in response to climate change. The magnitude of increase in breakdown rates is uncertain, given differences in litter quality and microbial and detritivore community responses to temperature, factors that can influence the apparent temperature sensitivity of breakdown and the relative proportion of C lost to the atmosphere vs. stored or transported downstream. Here, we synthesized 1025 records of litter breakdown in streams and rivers to quantify its temperature sensitivity, as measured by the activation energy (Ea , in eV). Temperature sensitivity of litter breakdown varied among twelve plant genera for which Ea could be calculated. Higher values of Ea were correlated with lower-quality litter, but these correlations were influenced by a single, N-fixing genus (Alnus). Ea values converged when genera were classified into three breakdown rate categories, potentially due to continual water availability in streams and rivers modulating the influence of leaf chemistry on breakdown. Across all data representing 85 plant genera, the Ea was 0.34 ± 0.04 eV, or approximately half the value (0.65 eV) predicted by metabolic theory. Our results indicate that average breakdown rates may increase by 5-21% with a 1-4 °C rise in water temperature, rather than a 10-45% increase expected, according to metabolic theory. Differential warming of tropical and temperate biomes could result in a similar proportional increase in breakdown rates, despite variation in Ea values for these regions (0.75 ± 0.13 eV and 0.27 ± 0.05 eV, respectively). The relative proportions of gaseous C loss and organic matter transport downstream should not change with rising temperature given that Ea values for breakdown mediated by microbes alone and microbes plus detritivores were similar at the global scale.

Testing a 'genes-to-ecosystems' approach to understanding aquatic-terrestrial linkages.

A 'genes-to-ecosystems' approach has been proposed as a novel avenue for integrating the consequences of intraspecific genetic variation with the underlying genetic architecture of a species to shed light on the relationships among hierarchies of ecological organization (genes → individuals → communities → ecosystems). However, attempts to identify genes with major effect on the structure of communities and/or ecosystem processes have been limited and a comprehensive test of this approach has yet to emerge. Here, we present an interdisciplinary field study that integrated a common garden containing different genotypes of a dominant, riparian tree, Populus trichocarpa, and aquatic mesocosms to determine how intraspecific variation in leaf litter alters both terrestrial and aquatic communities and ecosystem functioning. Moreover, we incorporate data from extensive trait screening and genome-wide association studies estimating the heritability and genes associated with litter characteristics. We found that tree genotypes varied considerably in the quality and production of leaf litter, which contributed to variation in phytoplankton abundances, as well as nutrient dynamics and light availability in aquatic mesocosms. These 'after-life' effects of litter from different genotypes were comparable to the responses of terrestrial communities associated with the living foliage. We found that multiple litter traits corresponding with aquatic community and ecosystem responses differed in their heritability. Moreover, the underlying genetic architecture of these traits was complex, and many genes contributed only a small proportion to phenotypic variation. Our results provide further evidence that genetic variation is a key component of aquatic-terrestrial linkages, but challenge the ability to predict community or ecosystem responses based on the actions of one or a few genes.

Increased resistance of Bt aspens to Phratora vitellinae (Coleoptera) leads to increased plant growth under experimental conditions.

One main aim with genetic modification (GM) of trees is to produce plants that are resistant to various types of pests. The effectiveness of GM-introduced toxins against specific pest species on trees has been shown in the laboratory. However, few attempts have been made to determine if the production of these toxins and reduced herbivory will translate into increased tree productivity. We established an experiment with two lines of potted aspens (Populus tremula×Populus tremuloides) which express Bt (Bacillus thuringiensis) toxins and the isogenic wildtype (Wt) in the lab. The goal was to explore how experimentally controlled levels of a targeted leaf beetle Phratora vitellinae (Coleoptera; Chrysomelidae) influenced leaf damage severity, leaf beetle performance and the growth of aspen. Four patterns emerged. Firstly, we found clear evidence that Bt toxins reduce leaf damage. The damage on the Bt lines was significantly lower than for the Wt line in high and low herbivory treatment, respectively. Secondly, Bt toxins had a significant negative effect on leaf beetle survival. Thirdly, the significant decrease in height of the Wt line with increasing herbivory and the relative increase in height of one of the Bt lines compared with the Wt line in the presence of herbivores suggest that this also might translate into increased biomass production of Bt trees. This realized benefit was context-dependent and is likely to be manifested only if herbivore pressure is sufficiently high. However, these herbivore induced patterns did not translate into significant affect on biomass, instead one Bt line overall produced less biomass than the Wt. Fourthly, compiled results suggest that the growth reduction in one Bt line as indicated here is likely due to events in the transformation process and that a hypothesized cost of producing Bt toxins is of subordinate significance.

Incubation time, functional litter diversity, and habitat characteristics predict litter-mixing effects on decomposition.

Plant diversity influences many fundamental ecosystem functions, including carbon and nutrient dynamics, during litter breakdown. Mixing different litter species causes litter mixtures to lose mass at different rates than expected from component species incubated in isolation. Such nonadditive litter-mixing effects on breakdown processes often occur idiosyncratically because their direction and magnitude change with incubation time, litter species composition, and ecosystem characteristics. Taking advantage of results from 18 litter mixture experiments in streams, we examined whether the direction and magnitude of nonadditive mixing effects are randomly determined. Across 171 tested litter mixtures and 510 incubation time-by-mixture combinations, nonadditive effects on breakdown were common and on average resulted in slightly faster decomposition than expected. In addition, we found that the magnitude of nonadditive effects and the relative balance of positive and negative responses in mixtures change predictably over time, and both were related to an index of functional litter diversity and selected environmental characteristics. Based on these, it should be expected that nonadditive effects are stronger for litter mixtures made of functionally dissimilar species especially in smaller streams. Our findings demonstrate that effects of litter diversity on plant mixture breakdown are more predictable than generally thought. We further argue that the consequences of current worldwide homogenization in the composition of plant traits on carbon and nutrient dynamics could be better inferred from long-duration experiments that manipulate both functional litter diversity and ecosystem characteristics in "hotspots of biodiversity effects," such as small streams.

From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization.

Using two genetic approaches and seven different plant systems, we present findings from a meta-analysis examining the strength of the effects of plant genetic introgression and genotypic diversity across individual, community and ecosystem levels with the goal of synthesizing the patterns to date. We found that (i) the strength of plant genetic effects can be quite high; however, the overall strength of genetic effects on most response variables declined as the levels of organization increased. (ii) Plant genetic effects varied such that introgression had a greater impact on individual phenotypes than extended effects on arthropods or microbes/fungi. By contrast, the greatest effects of genotypic diversity were on arthropods. (iii) Plant genetic effects were greater on above-ground versus below-ground processes, but there was no difference between terrestrial and aquatic environments. (iv) The strength of the effects of intraspecific genotypic diversity tended to be weaker than interspecific genetic introgression. (v) Although genetic effects generally decline across levels of organization, in some cases they do not, suggesting that specific organisms and/or processes may respond more than others to underlying genetic variation. Because patterns in the overall impacts of introgression and genotypic diversity were generally consistent across diverse study systems and consistent with theoretical expectations, these results provide generality for understanding the extended consequences of plant genetic variation across levels of organization, with evolutionary implications.

Plant-soil microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms.

Although soil microbial communities are known to play crucial roles in the cycling of nutrients in forest ecosystems and can vary by plant species, how microorganisms respond to the subtle gradients of plant genetic variation is just beginning to be appreciated. Using a model Populus system in a common garden with replicated clones of known genotypes, we evaluated microbial biomass and community composition as quantitative traits. Two main patterns emerged. (1) Plant genotype influenced microbial biomass nitrogen in soils under replicated genotypes of Populus angustifolia, F1, and backcross hybrids, but not P. fremontii. Genotype explained up to 78% of the variation in microbial biomass as indicated by broad-sense heritability estimates (i.e., clonal repeatability). A second estimate of microbial biomass (total phospholipid fatty acid) was more conservative and showed significant genotype effects in P. angustifolia and backcross hybrids. (2) Plant genotype significantly influenced microbial community composition, explaining up to 70% of the variation in community composition within P. angustifolia genotypes alone. These findings suggest that variation in above- and belowground traits of individual plant genotypes can alter soil microbial dynamics, and suggests that further investigations of the evolutionary implications of genetic feedbacks are warranted.

Variation in below-ground carbon fluxes along a Populus hybridization gradient.

Here, soil CO(2) efflux, minirhizotron fine root production (FRP), and estimated total below-ground carbon allocation (TBCA) were examined along an elevation and hybridization gradient between two cottonwood species. FRP was 72% greater under high-elevation Populus angustifolia, but soil CO(2) efflux and TBCA were 62% and 94% greater, respectively, under low-elevation stands dominated by Populus fremontii, with a hybrid stand showing intermediate values. Differences between the responses of FRP, soil CO(2) efflux and TBCA may potentially be explained in terms of genetic controls; while plant species and hybridization explained variance in carbon flux, we found only weak correlations of FRP and TBCA with soil moisture, and no correlations with soil temperature or nitrogen availability. Soil CO(2) efflux and TBCA were uncorrelated with FRP, suggesting that, although below-ground carbon fluxes may change along environmental and genetic gradients, major components of below-ground carbon flux may be decoupled.

A framework for community and ecosystem genetics: from genes to ecosystems.

Can heritable traits in a single species affect an entire ecosystem? Recent studies show that such traits in a common tree have predictable effects on community structure and ecosystem processes. Because these 'community and ecosystem phenotypes' have a genetic basis and are heritable, we can begin to apply the principles of population and quantitative genetics to place the study of complex communities and ecosystems within an evolutionary framework. This framework could allow us to understand, for the first time, the genetic basis of ecosystem processes, and the effect of such phenomena as climate change and introduced transgenic organisms on entire communities.

Plant genes link forests and streams.

Although it is understood that the composition of riparian trees can affect stream function through leaf litter fall, the potential effects of genetic variation within species are less understood. Using a naturally hybridizing cottonwood system, we examined the hypothesis that genetic differences among two parental species (Populus fremontii and P. angustifolia) and two groups of their hybrids (F1 and backcrosses to P. angustifolia) would affect litter decomposition rates and the composition of the aquatic invertebrate community that colonizes leaves. Three major findings emerged: (1) parental and hybrid types differ in litter quality, (2) decomposition differs between two groups, a fast group (P. fremontii and F1 hybrid), and a slow group (P. angustifolia and backcross hybrids), and (3) aquatic invertebrate communities colonizing P. fremontii litter differed significantly in composition from all other cross types, even though P. fremontii and the F1 hybrid decomposed at similar rates. These findings are in agreement with terrestrial arthropod studies in the same cottonwood system. However, the effects are less pronounced aquatically than those observed in the adjacent terrestrial community, which supports a genetic diffusion hypothesis. Importantly, these findings argue that genetic interactions link terrestrial and aquatic communities and may have significant evolutionary and conservation implications.