Leaf mechanical properties strongly influence leaf lifespan, plant-herbivore interactions, litter decomposition and nutrient cycling, but global patterns in their interspecific variation and underlying mechanisms remain poorly understood. We synthesize data across the three major measurement methods, permitting the first global analyses of leaf mechanics and associated traits, for 2819 species from 90 sites worldwide. Key measures of leaf mechanical resistance varied c. 500-800-fold among species. Contrary to a long-standing hypothesis, tropical leaves were not mechanically more resistant than temperate leaves. Leaf mechanical resistance was modestly related to rainfall and local light environment. By partitioning leaf mechanical resistance into three different components we discovered that toughness per density contributed a surprisingly large fraction to variation in mechanical resistance, larger than the fractions contributed by lamina thickness and tissue density. Higher toughness per density was associated with long leaf lifespan especially in forest understory. Seldom appreciated in the past, toughness per density is a key factor in leaf mechanical resistance, which itself influences plantanimal interactions and ecosystem functions across the globe.
Theory on trophic interactions predicts that predators increase plant biomass by feeding on herbivores, an indirect interaction called a trophic cascade. Theory also predicts that predators feeding on predators, or intraguild predation, will weaken trophic cascades. Although past syntheses have confirmed cascading effects of terrestrial arthropod predators, we lack a comprehensive analysis for vertebrate insectivores-which by virtue of their body size and feeding habits are often top predators in these systems-and of how intraguild predation mediates trophic cascade strength. We report here on a meta-analysis of 113 experiments documenting the effects of insectivorous birds, bats, or lizards on predaceous arthropods, herbivorous arthropods, and plants. Although vertebrate insectivores fed as intraguild predators, strongly reducing predaceous arthropods (38%), they nevertheless suppressed herbivores (39%), indirectly reduced plant damage (40%), and increased plant biomass (14%). Furthermore, effects of vertebrate insectivores on predatory and herbivorous arthropods were positively correlated. Effects were strongest on arthropods and plants in communities with abundant predaceous arthropods and strong intraguild predation, but weak in communities depauperate in arthropod predators and intraguild predation. The naturally occurring ratio of arthropod predators relative to herbivores varied tremendously among the studied communities, and the skew to predators increased with site primary productivity and in trees relative to shrubs. Although intraguild predation among arthropod predators has been shown to weaken herbivore suppression, we find this paradigm does not extend to vertebrate insectivores in these communities. Instead, vertebrate intraguild predation is associated with strengthened trophic cascades, and insectivores function as dominant predators in terrestrial plant-arthropod communities.bottom-up and top-down control | intraguild predation | meta-analysis | trophic cascade | vertebrate predator exclusion R esearch demonstrates that predators, by feeding on herbivores, can increase plant biomass via the indirect interaction commonly labeled a trophic cascade (1). In recent years, metaanalyses have quantified trophic cascades separately in terrestrial (2, 3) and aquatic systems (4, 5) and in multiple habitats together to compare the strength of trophic cascades among ecosystem types (6). Although the strengths of trophic cascades vary across ecosystem types, explanations for the significant residual variation within ecosystems remain enigmatic (6-8).Vertebrate insectivores such as birds, bats, and lizards often feed as top predators on terrestrial arthropod communities, but based upon current theory it is unclear whether their effects should cascade down to affect plant biomass. Because of their large body size relative to arthropod prey, vertebrate insectivores can consume both predatory and herbivorous arthropods (9, 10). As a consequence, vertebrate insectivores may feed as so-called intraguild predators ...
Colletotrichum interacts with numerous plant species overtly as symptomatic pathogens and cryptically as asymptomatic endophytes. It is not known whether these contrasting ecological modes are optional strategies expressed by individual Colletotrichum species or whether a species' ecology is explicitly pathogenic or endophytic. We explored this question by inferring relationships among 77 C. gloeosporioides s.l. strains isolated from asymptomatic leaves and from anthracnose lesions on leaves and fruits of Theobroma cacao (cacao) and other plants from Panamá.ITS and 5′-tef1 were used to assess diversity and to delineate operational taxonomic units for multilocus phylogenetic analysis. The ITS and 5′-tef1 screens concordantly resolved four strongly supported lineages, clades A-D: Clade A includes the ex type of C.gloeosporioides, clade B includes the ex type ITS sequence of C. boninense, and clades C and D are unidentified. The ITS yielded limited resolution and support within all clades, in particular the C. gloeosporioides clade (A), the focal lineage dealt with in this study.In contrast the 5′-tef1 screen differentiated nine distinctive haplotype subgroups within the C. gloeosporioides clade that were concordant with phylogenetic terminals resolved in a five-locus nuclear phylogeny. Among these were two phylogenetic species associated with symptomatic infections specific to either cacao or mango and five phylogenetic species isolated principally as asymptomatic infections from cacao and other plant hosts. We formally describe two new species, C. tropicale and C. ignotum, that are frequent asymptomatic associates of cacao and other Neotropical plant species, and epitypify C. theobromicola, which is associated with foliar and fruit anthracnose lesions of cacao. Asymptomatic Colletotrichum strains isolated from cacao plants grown in China included six distinct C. gloeosporioides clade taxa, only one of which is known to occur in the Neotropics. (Bailey and Jeger 1992). The genus is the subject of numerous studies that deal primarily with its role as a plant pathogen as summarized in Bailey and Jeger (1992) and Cannon et al. (2008). In addition to its conspicuous ecology as a plant pathogen Colletotrichum is also a ubiquitous asymptomatic foliar endophyte of a diverse spectrum of plant hosts (e.g. Lodge et al. 1996, Cannon and Simmons 2002, Gamboa and Bayman 2001, Lu et al. 2004, Duran et al. 2005, Morakotkarn et al. 2007, Osono 2008. The ecological significance of endophytism is unclear. Although it has been suggested that endophytic fungi might be quiescent saprobes (Petrini et al. 1995, Whalley 1996, latent pathogens (Stone et al. 2000) or mutualists (Herre et al. 2007, specific examples detailing these hypotheses remain scant.It has been shown that particular Colletotrichum endophytes confer protective benefits to cacao hosts by reducing disease incidence and damage caused by other plant pathogens (Arnold et al. 2003, Herre et al. 2007. Mejía et al. (2008) reported the frequent isolation of C. gloeo...
We discuss studies of foliar endophytic fungi (FEF) and arbuscular mycorrhizal fungi (AMF) associated with Theobroma cacao in Panama. Direct, experimentally controlled comparisons of endophyte free (E−) and endophyte containing (E+) plant tissues in T. cacao show that foliar endophytes (FEF) that commonly occur in healthy host leaves enhance host defenses against foliar damage due to the pathogen (Phytophthora palmivora). Similarly, root inoculations with commonly occurring AMF also reduce foliar damage due to the same pathogen. These results suggest that endophytic fungi can play a potentially important mutualistic role by augmenting host defensive responses against pathogens. There are two broad classes of potential mechanisms by which endophytes could contribute to host protection: (1) inducing or increasing the expression of intrinsic host defense mechanisms and (2) providing additional sources of defense, extrinsic to those of the host (e.g., endophyte‐based chemical antibiosis). The degree to which either of these mechanisms predominates holds distinct consequences for the evolutionary ecology of host–endophyte–pathogen relationships. More generally, the growing recognition that plants are composed of a mosaic of plant and fungal tissues holds a series of implications for the study of plant defense, physiology, and genetics.
Most forest birds include arthropods in their diet, sometimes specializing on arthropods that consume plant foliage. Experimental tests of whether bird predation on arthropods can reduce plant damage, however, are few and restricted to relatively low-diversity systems. Here, we describe an experimental test in a diverse tropical forest of whether birds indirectly defend foliage from arthropod herbivores. We also compare how the indirect effects of bird predation vary with different levels of foliage productivity in the canopy vs. the understory. For three Neotropical tree species, we observed that birds decreased local arthropod densities on canopy branches and reduced consequent damage to leaves. In contrast, we observed no evidence of bird-arthropod limitation on conspecific saplings in the less productive understory of the same forest. Our results support theory that predicts trophic cascades where productivity is high and suggest that birds play an important role in Neotropical communities by means of their indirect defense of some canopy tree species.F or decades, ecologists have debated the circumstances under which a predator limits its prey's consumption of organisms in lower trophic levels (i.e., a predator-driven trophic cascade) (1-4). One body of theory predicts such cascades will occur in terrestrial systems with high plant productivity (5, 6). Opposing theory predicts that cascades will not occur in terrestrial systems and only in low-diversity aquatic or marine systems (7). Proponents of the latter theory suggest that higher diversity in terrestrial systems leads to diffuse food webs, rendering trophic levels nonexistent (7). Field experiments demonstrate that insectivorous birds can limit arthropod abundances and decrease damage to plants, but these tests have been conducted in settings with relatively low tree species diversity such as temperate forests (8-11) or agricultural systems (12, 13). Along with high tree species diversity, tropical forests support a high diversity and biomass of leaf-chewing arthropods (14) as well as a high biomass of birds that consume them (15). In a lowland forest of Panama, we used canopy crane access (16) to test the hypotheses that (i) birds limit arthropod densities and consequent herbivore damage, and (ii) the effects of bird predation are strongest where foliage production rates are high.For one year, we observed how the local density and taxonomic composition of the arthropod community responded to the absence of bird predation and also assessed changes in herbivore damage. We estimated and compared these quantities on control branches͞saplings where birds had access to foliage and on branches͞saplings in experimental exclosures where foliage was inaccessible to birds. A within-site comparison of canopy branches and conspecific understory͞edge saplings allowed us to investigate the effects of bird predation across a 3-fold vertical gradient of foliage production. MethodsA canopy crane provided forest canopy access in a dry, semideciduous lowland tropical for...
Understanding distribution patterns and multitrophic interactions is critical for managing bat‐ and bird‐mediated ecosystem services such as the suppression of pest and non‐pest arthropods. Despite the ecological and economic importance of bats and birds in tropical forests, agroforestry systems, and agricultural systems mixed with natural forest, a systematic review of their impact is still missing. A growing number of bird and bat exclosure experiments has improved our knowledge allowing new conclusions regarding their roles in food webs and associated ecosystem services. Here, we review the distribution patterns of insectivorous birds and bats, their local and landscape drivers, and their effects on trophic cascades in tropical ecosystems. We report that for birds but not bats community composition and relative importance of functional groups changes conspicuously from forests to habitats including both agricultural areas and forests, here termed ‘forest‐agri’ habitats, with reduced representation of insectivores in the latter. In contrast to previous theory regarding trophic cascade strength, we find that birds and bats reduce the density and biomass of arthropods in the tropics with effect sizes similar to those in temperate and boreal communities. The relative importance of birds versus bats in regulating pest abundances varies with season, geography and management. Birds and bats may even suppress tropical arthropod outbreaks, although positive effects on plant growth are not always reported. As both bats and birds are major agents of pest suppression, a better understanding of the local and landscape factors driving the variability of their impact is needed.
It is increasingly recognized that macro-organisms (corals, insects, plants, vertebrates) consist of both host tissues and multiple microbial symbionts that play essential roles in their host's ecological and evolutionary success. Consequently, identifying benefits and costs of symbioses, as well as mechanisms underlying them are research priorities. All plants surveyed under natural conditions harbor foliar endophytic fungi (FEF) in their leaf tissues, often at high densities. Despite producing no visible effects on their hosts, experiments have nonetheless shown that FEF reduce pathogen and herbivore damage. Here, combining results from three genomic, and two physiological experiments, we demonstrate pervasive genetic and phenotypic effects of the apparently asymptomatic endophytes on their hosts. Specifically, inoculation of endophyte-free (E−) Theobroma cacao leaves with Colletotrichum tropicale (E+), the dominant FEF species in healthy T. cacao, induces consistent changes in the expression of hundreds of host genes, including many with known defensive functions. Further, E+ plants exhibited increased lignin and cellulose content, reduced maximum rates of photosynthesis (Amax), and enrichment of nitrogen-15 and carbon-13 isotopes. These phenotypic changes observed in E+ plants correspond to changes in expression of specific functional genes in related pathways. Moreover, a cacao gene (Tc00g04254) highly up-regulated by C. tropicale also confers resistance to pathogen damage in the absence of endophytes or their products in host tissues. Thus, the benefits of increased pathogen resistance in E+ plants are derived in part from up-regulation of intrinsic host defense responses, and appear to be offset by potential costs including reduced photosynthesis, altered host nitrogen metabolism, and endophyte heterotrophy of host tissues. Similar effects are likely in most plant-endophyte interactions, and should be recognized in the design and interpretation of genetic and phenotypic studies of plants.
SignificanceLeaf traits, such as photosynthetic capacity, nitrogen concentration, and leaf mass per area, strongly affect plant growth and nutrient cycles. Understanding relationships among leaf traits is, therefore, a fundamental challenge in plant biology, crop science, and ecology. Different groups of leaves exhibit distinct relationships among pairs of traits. For example, photosynthetic capacity per unit leaf area increases strongly with leaf mass per area from sun to shade within species, but these same traits are only weakly related across global species. Our analysis suggests that divergent trait relationships can be understood by partitioning leaf mass into photosynthetic and structural support components. Our paper clarifies the causes of relationships among traits and why those relationships differ among different groups of plants.
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