Attackers gain the upper hand over plants in the face of rapid global change.

Interactions among organisms in natural ecosystems are the foundational underpinnings of nearly all ecological studies. It has never been more important to increase our awareness of how these interactions are altered by human activity, threatening biodiversity and disrupting ecosystem functioning. Much of the historic focus of species conservation has been the preservation of endangered and endemic species at risk from hunting, over-exploitation, and habitat destruction. However, there is increasing evidence that differences between plants and their attacking organisms in the speed and direction of physiological, demographic, and genetic (adaptation) responses to global change are having devastating consequences, resulting in large-scale losses of dominant or abundant plant species, particularly in forest ecosystems. From the elimination in the wild of the American chestnut to the extensive regional damage caused by insect outbreaks in temperate forest ecosystems, these losses of dominant species change the ecological landscape and functioning, and represent important threats to biodiversity at all scales. Introductions due to human activity, range shifts due to climate change, and their combination are the principal drivers behind these profound ecosystem changes. In this Review, we argue that there is an urgent need to increase our recognition and hone our predictive power for how these imbalances may occur. Moreover, we should seek to minimize the consequences of these imbalances in order to ensure the preservation of the structure, function and biodiversity of entire ecosystems, not just rare or highly endangered species.

Termite sensitivity to temperature affects global wood decay rates.

Deadwood is a large global carbon store with its store size partially determined by biotic decay. Microbial wood decay rates are known to respond to changing temperature and precipitation. Termites are also important decomposers in the tropics but are less well studied. An understanding of their climate sensitivities is needed to estimate climate change effects on wood carbon pools. Using data from 133 sites spanning six continents, we found that termite wood discovery and consumption were highly sensitive to temperature (with decay increasing >6.8 times per 10°C increase in temperature)-even more so than microbes. Termite decay effects were greatest in tropical seasonal forests, tropical savannas, and subtropical deserts. With tropicalization (i.e., warming shifts to tropical climates), termite wood decay will likely increase as termites access more of Earth's surface.

Dose-responses for solar radiation exposure reveal high sensitivity of microbial decomposition to changes in plant litter quality that occur during photodegradation.

Plant litter decomposition is a key process for carbon (C) turnover in terrestrial ecosystems. Sunlight has been shown to cause and accelerate C release in semiarid ecosystems, yet the dose-response relationships for these effects have not been evaluated. We conducted a two-phase experiment where plant litter of three species was subjected to a broad range of cumulative solar radiation (CSR) exposures under field conditions. We then evaluated the relationships between CSR exposure and abiotic mass loss, litter quality and the subsequent biotic decomposition and microbial activity in litter. Dose-response relationships demonstrated that CSR exposure was modestly correlated with abiotic mass loss but highly significantly correlated with lignin degradation, saccharification, microbial activity and biotic decay of plant litter across all species. Moreover, a comparison of these dose-response relationships suggested that small reductions in litter lignin due to exposure to sunlight may have large consequences for biotic decay. These results provide strong support for a model that postulates a critical role for lignin photodegradation in the mechanism of photofacilitation and demonstrate that, under natural field conditions, biotic degradation of plant litter is linearly related with the dose of solar radiation received by the material before coming into contact with decomposer microorganisms.

Sunlight Doubles Aboveground Carbon Loss in a Seasonally Dry Woodland in Patagonia.

Photodegradation of aboveground senescent plant material (plant litter) due to exposure to solar radiation has been identified as a dominant control on carbon (C) loss in semi-arid ecosystems [1], upturning traditional models of C cycling based only on available moisture and litter quality. In addition to the photochemical mineralization of organic matter [1, 2], sunlight alters the chemistry of cell walls in plant litter [3, 4], making them more susceptible to subsequent biotic degradation [5-7]. Nevertheless, the interactive effects of sunlight exposure, climate seasonality, and biotic decomposition on C turnover remain unresolved in terrestrial ecosystems. We show here that exposure to sunlight accelerated litter decomposition in a Patagonian woodland with a marked dry summer season. Controls on initial decomposition varied seasonally from direct photochemical mineralization in the dry summer to biotic degradation in the wet winter. By manipulating sunlight received by plant litter using spectral filters that attenuated ultraviolet and short-wave visible light, we demonstrate that direct photodegradation and its legacy, associated with increased microbial access to labile carbohydrates, are responsible for the acceleration of aboveground C turnover in this Mediterranean-type climate. Across plant species and over a 2-year period, litter exposed to the full solar spectrum decomposed twice as fast as litter that received attenuated sunlight. Changes in vegetation cover or biodiversity due to projected increased drought and dry season length [8] will likely exacerbate C losses from aboveground litter due to sunlight exposure, negatively impacting the C balance in ecosystems that are particularly vulnerable to global change [9].

A light-dependent molecular link between competition cues and defence responses in plants.

Growth responses to competition1 and defence responses to the attack of consumer organisms2 are two classic examples of adaptive phenotypic plasticity in plants. However, the mechanistic and functional links between these responses are not well understood. Jasmonates, a family of lipid-derived signals, are potent growth inhibitors and central regulators of plant immunity to herbivores and pathogens3,4, with both roles being evolutionarily conserved from bryophytes5 to angiosperms6. When shade-intolerant plants perceive the proximity of competitors using the photoreceptor phytochrome B, they activate the shade-avoidance syndrome and downregulate jasmonate responses7. Despite the central implications of this light-mediated change in the growth/defence balance for plant adaptation and crop yield8,9, the mechanisms by which photoreceptors relay light cues to the jasmonate signalling pathway remain poorly understood10. Here, we identify a sulfotransferase (ST2a) that is strongly upregulated by plant proximity perceived by phytochrome B via the phytochrome B-phytochrome interacting factor signalling module. By catalysing the formation of a sulfated jasmonate derivative, ST2a acts to reduce the pool of precursors of active forms of jasmonates and represents a direct molecular link between photoreceptors and hormone signalling in plants. The metabolic step defined by this enzyme provides a molecular mechanism for prioritizing shade avoidance over defence under intense plant competition.

Field exclusion of large soil predators impacts lower trophic levels and decreases leaf-litter decomposition in dry forests.

Shifts in densities of apex predators may indirectly affect fundamental ecosystem processes, such as decomposition, by altering patterns of cascading effects propagating through lower trophic levels. These top-down effects may interact with anthropogenic impacts, such as climate change, in largely unknown ways. We investigated how changes in densities of large predatory arthropods in forest leaf-litter communities altered lower trophic levels and litter decomposition. We conducted our experiment in soil communities that had experienced different levels of long-term average precipitation. We hypothesized that altering abundances of apex predators would have stronger effects on soil communities inhabiting dry forests, due to lower secondary productivity and greater resource overexploitation by lower trophic levels compared to wet forests. We experimentally manipulated abundances of the largest arthropod predators (apex predators) in field mesocosms replicated in the leaf-litter community of Iberian beech forests that differed in long-term mean annual precipitation by 25% (three dry forests with MAP < 1,250 mm and four wet forests with MAP > 1,400 mm). After one year, we assessed abundances of soil fauna in lower trophic levels and indirect impacts on leaf-litter decomposition using litter of understorey hazel, Corylus avellana. Reducing densities of large predators had a consistently negative effect on final abundances of the different trophic groups and several taxa within each group. Moreover, large predatory arthropods strongly impacted litter decomposition, and their effect interacted with the long-term annual rainfall experienced by the soil community. In the dry forests, a 50% reduction in the densities of apex predators was associated with a 50% reduction in decomposition. In wet forests, the same reduction in densities of apex soil predators did not alter the rate of litter decomposition. Our results suggest that predators may facilitate lower trophic levels by indirectly reducing competition and resource overexploitation, cascading effects that may be more pronounced in drier forests where conditions have selected for greater competitive ability and more rapid resource utilization. These findings thus provide insights into the functioning of soil invertebrate communities and their role in decomposition, as well as potential consequences of soil community responses to climate change.

A world of co-benefits: Solving the global nitrogen challenge.

Nitrogen is a critical component of the economy, food security, and planetary health. Many of the world's sustainability targets hinge on global nitrogen solutions, which, in turn, contribute lasting benefits for: (i) world hunger; (ii) soil, air and water quality; (iii) climate change mitigation; and (iv) biodiversity conservation. Balancing the projected rise in agricultural nitrogen demands while achieving these 21st century ideals will require policies to coordinate solutions among technologies, consumer choice, and socioeconomic transformation.

Recalculating growth and defense strategies under competition: key roles of photoreceptors and jasmonates.

The growth-defense trade-off in plant biology has gained enormous traction in the last two decades, highlighting the importance of understanding how plants deal with two of the greatest challenges for their survival and reproduction. It has been well established that in response to competition signals perceived by informational photoreceptors, shade-intolerant plants typically activate the shade-avoidance syndrome (SAS). In turn, in response to signals of biotic attack, plants activate a suite of defense responses, many of which are directed to minimize the loss of plant tissue to the attacking agent (broadly defined, the defense syndrome, DS). We argue that components of the SAS, including increased elongation, apical dominance, reduced leaf mass per area (LMA), and allocation to roots, are in direct conflict with configurational changes that plants require to maximize defense. We hypothesize that these configurational trade-offs provide a functional explanation for the suppression of components of the DS in response to competition cues. Based on this premise, we discuss recent advances in the understanding of the mechanisms by which informational photoreceptors, by interacting with jasmonic acid (JA) signaling, help the plant to make intelligent allocation and developmental decisions that optimize its configuration in complex biotic contexts.

Plant, fungal, bacterial, and nitrogen interactions in the litter layer of a native Patagonian forest.

Plant-microbial interactions in the litter layer represent one of the most relevant interactions for biogeochemical cycling as litter decomposition is a key first step in carbon and nitrogen turnover. However, our understanding of these interactions in the litter layer remains elusive. In an old-growth mixed Nothofagus forest in Patagonia, we studied the effects of single tree species identity and the mixture of three tree species on the fungal and bacterial composition in the litter layer. We also evaluated the effects of nitrogen (N) addition on these plant-microbial interactions. In addition, we compared the magnitude of stimulation of litter decomposition due to home field advantage (HFA, decomposition occurs more rapidly when litter is placed beneath the plant species from which it had been derived than beneath a different plant species) and N addition that we previously demonstrated in this same forest, and used microbial information to interpret these results. Tree species identity had a strong and significant effect on the composition of fungal communities but not on the bacterial community of the litter layer. The microbial composition of the litter layer under the tree species mixture show an averaged contribution of each single tree species. N addition did not erase the plant species footprint on the fungal community, and neither altered the bacterial community. N addition stimulated litter decomposition as much as HFA for certain tree species, but the mechanisms behind N and HFA stimulation may have differed. Our results suggest that stimulation of decomposition from N addition might have occurred due to increased microbial activity without large changes in microbial community composition, while HFA may have resulted principally from plant species' effects on the litter fungal community. Together, our results suggest that plant-microbial interactions can be an unconsidered driver of litter decomposition in temperate forests.

Photodegradation alleviates the lignin bottleneck for carbon turnover in terrestrial ecosystems.

A mechanistic understanding of the controls on carbon storage and losses is essential for our capacity to predict and mitigate human impacts on the global carbon cycle. Plant litter decomposition is an important first step for carbon and nutrient turnover, and litter inputs and losses are essential in determining soil organic matter pools and the carbon balance in terrestrial ecosystems. Photodegradation, the photochemical mineralization of organic matter, has been recently identified as a mechanism for previously unexplained high rates of litter mass loss in arid lands; however, the global significance of this process as a control on carbon cycling in terrestrial ecosystems is not known. Here we show that, across a wide range of plant species, photodegradation enhanced subsequent biotic degradation of leaf litter. Moreover, we demonstrate that the mechanism for this enhancement involves increased accessibility to plant litter carbohydrates for microbial enzymes. Photodegradation of plant litter, driven by UV radiation, and especially visible (blue-green) light, reduced the structural and chemical bottleneck imposed by lignin in secondary cell walls. In leaf litter from woody species, specific interactions with UV radiation obscured facilitative effects of solar radiation on biotic decomposition. The generalized effect of sunlight exposure on subsequent microbial activity, mediated by increased accessibility to cell wall polysaccharides, suggests that photodegradation is quantitatively important in determining rates of mass loss, nutrient release, and the carbon balance in a broad range of terrestrial ecosystems.

Effects of stratospheric ozone depletion, solar UV radiation, and climate change on biogeochemical cycling: interactions and feedbacks.

Climate change modulates the effects of solar UV radiation on biogeochemical cycles in terrestrial and aquatic ecosystems, particularly for carbon cycling, resulting in UV-mediated positive or negative feedbacks on climate. Possible positive feedbacks discussed in this assessment include: (i) enhanced UV-induced mineralisation of above ground litter due to aridification; (ii) enhanced UV-induced mineralisation of photoreactive dissolved organic matter (DOM) in aquatic ecosystems due to changes in continental runoff and ice melting; (iii) reduced efficiency of the biological pump due to UV-induced bleaching of coloured dissolved organic matter (CDOM) in stratified aquatic ecosystems, where CDOM protects phytoplankton from the damaging solar UV-B radiation. Mineralisation of organic matter results in the production and release of CO2, whereas the biological pump is the main biological process for CO2 removal by aquatic ecosystems. This paper also assesses the interactive effects of solar UV radiation and climate change on the biogeochemical cycling of aerosols and trace gases other than CO2, as well as of chemical and biological contaminants. Interacting effects of solar UV radiation and climate change on biogeochemical cycles are particularly pronounced at terrestrial-aquatic interfaces.

There's no place like home? An exploration of the mechanisms behind plant litter-decomposer affinity in terrestrial ecosystems.

Litter decomposition in terrestrial ecosystems is an important first step for carbon and nutrient cycling, as senescent plant material is degraded and consequently incorporated, along with microbial products, into soil organic matter. The identification of litter affinity effects, whereby decomposition is accelerated in its home environment (home-field advantage, HFA), highlights the importance of plant-soil interactions that have consequences for biogeochemical cycling. While not universal, these affinity effects have been identified in a range of ecosystems, particularly in forests without disturbance. The optimization of the local decomposer community to degrade a particular combination of litter traits is the most oft-cited explanation for HFA effects, but the ways in which this specialized community can develop are only beginning to be understood. We explore ways in which HFA, or more broadly litter affinity effects, could arise in terrestrial ecosystems. Plant-herbivore interactions, microbial symbiosis, legacies from phyllosphere communities and attractors of specific soil fauna could contribute to spatially defined affinity effects for litter decomposition. Pyrosequencing soil communities and functional linkages of soil fauna provide great promise in advancing our mechanistic understanding of these interactions, and could lead to a greater appreciation of the role of litter-decomposer affinity in the maintenance of soil functional diversity.

Environmental effects of ozone depletion and its interactions with climate change: progress report, 2011.

The parties to the Montreal Protocol are informed by three panels of experts. One of these is the Environmental Effects Assessment Panel (EEAP), which deals with two focal issues. The first focus is the effects of increased UV radiation on human health, animals, plants, biogeochemistry, air quality, and materials. The second focus is on interactions between UV radiation and global climate change and how these may affect humans and the environment. When considering the effects of climate change, it has become clear that processes resulting in changes in stratospheric ozone are more complex than believed previously. As a result of this, human health and environmental problems will be longer-lasting and more regionally variable. Like the other panels, the EEAP produces a detailed report every four years; the most recent was published in 2010 (Photochem. Photobiol. Sci., 2011, 10, 173-300). In the years in between, the EEAP produces less detailed and shorter progress reports, which highlight and assess the significance of developments in key areas of importance to the parties. The next full quadrennial report will be published in 2014-2015.

Do soil organisms affect aboveground litter decomposition in the semiarid Patagonian steppe, Argentina?

Surface litter decomposition in arid and semiarid ecosystems is often faster than predicted by climatic parameters such as annual precipitation or evapotranspiration, or based on standard indices of litter quality such as lignin or nitrogen concentrations. Abiotic photodegradation has been demonstrated to be an important factor controlling aboveground litter decomposition in aridland ecosystems, but soil fauna, particularly macrofauna such as termites and ants, have also been identified as key players affecting litter mass loss in warm deserts. Our objective was to quantify the importance of soil organisms on surface litter decomposition in the Patagonian steppe in the absence of photodegradative effects, to establish the relative importance of soil organisms on rates of mass loss and nitrogen release. We estimated the relative contribution of soil fauna and microbes to litter decomposition of a dominant grass using litterboxes with variable mesh sizes that excluded groups of soil fauna based on size class (10, 2, and 0.01 mm), which were placed beneath shrub canopies. We also employed chemical repellents (naphthalene and fungicide). The exclusion of macro- and mesofauna had no effect on litter mass loss over 3 years (P = 0.36), as litter decomposition was similar in all soil fauna exclusions and naphthalene-treated litter. In contrast, reduction of fungal activity significantly inhibited litter decomposition (P < 0.001). Although soil fauna have been mentioned as a key control of litter decomposition in warm deserts, biogeographic legacies and temperature limitation may constrain the importance of these organisms in temperate aridlands, particularly in the southern hemisphere.

Has water limited our imagination for aridland biogeochemistry?

The classic ecological paradigm for deserts, that all processes are controlled by water availability, has limited our imagination for exploring other controls on the cycling of carbon and nutrients in aridland ecosystems. This review of recent studies identifies alternative mechanisms that challenge the idea that all soil processes in aridlands are proximately water-limited, and highlights the significance of photodegradation of aboveground litter and the overriding importance of spatial heterogeneity as a modulator of biotic responses to water availability. Aridlands currently occupy >30% of the terrestrial land surface and are expanding. It is therefore critical to incorporate these previously unappreciated mechanisms in our understanding of aridland biogeochemistry to mitigate the effects of desertification and global change.

Dual role of lignin in plant litter decomposition in terrestrial ecosystems.

Plant litter decomposition is a critical step in the formation of soil organic matter, the mineralization of organic nutrients, and the carbon balance in terrestrial ecosystems. Biotic decomposition in mesic ecosystems is generally negatively correlated with the concentration of lignin, a group of complex aromatic polymers present in plant cell walls that is recalcitrant to enzymatic degradation and serves as a structural barrier impeding microbial access to labile carbon compounds. Although photochemical mineralization of carbon has recently been shown to be important in semiarid ecosystems, litter chemistry controls on photodegradative losses are not understood. We evaluated the importance of litter chemistry on photodegradation of grass litter and cellulose substrates with varying levels of lignin [cellulose-lignin (CL) substrates] under field conditions. Using wavelength-specific light attenuation filters, we found that light-driven mass loss was promoted by both UV and visible radiation. The spectral dependence of photodegradation correlated with the absorption spectrum of lignin but not of cellulose. Field incubations demonstrated that increasing lignin concentration reduced biotic decomposition, as expected, but linearly increased photodegradation. In addition, lignin content in CL substrates consistently decreased in photodegradative incubations. We conclude that lignin has a dual role affecting litter decomposition, depending on the dominant driver (biotic or abiotic) controlling carbon turnover. Under photodegradative conditions, lignin is preferentially degraded because it acts as an effective light-absorbing compound over a wide range of wavelengths. This mechanistic understanding of the role of lignin in plant litter decomposition will allow for more accurate predictions of carbon dynamics in terrestrial ecosystems.