Exposing the error hidden in plain sight: A critique of Calder's (1983) group selectionist seed-dispersal hypothesis for mistletoe "mimicry" of host plants.

Some mistletoe species (Loranthaceae) resemble their host plants to a striking degree. Various mechanisms have been proposed for the developmental origins of novel traits that cause mistletoes to appear similar to their hosts, as well as for the adaptive phenotypic evolution of such traits. Calder (1983) proposed a logically flawed group selectionist seed-dispersal hypothesis for mistletoes to resemble their hosts. Calder's (1983) hypothesis does not provide a viable potential explanation for mistletoe resemblance to hosts.

Low sodium availability in hydroponically manipulated host plants promotes cannibalism in a lepidopteran herbivore.

As an abundant element in the Earth's crust, sodium plays an unusual role in food webs. Its availability in terrestrial environments is highly variable, but it is nonessential for most plants, yet essential for animals and most decomposers. Accordingly, sodium requirements are important drivers of various animal behavioural patterns and performance levels. To specifically test whether sodium limitation increases cannibalism in a gregarious lepidopteran herbivore, we hydroponically manipulated Helianthus annuus host plants' tissue-sodium concentrations. Gregarious larvae of the bordered patch butterfly, Chlosyne lacinia, cannibalized siblings when plant-tissue sodium concentrations were low in two separate experiments. Although cannibalism was almost non-existent when sodium concentrations were high, individual mortality rates were also high. Sodium concentration in host plants can have pronounced effects on herbivore behaviour, individual-level performance, and population demographics, all of which are important for understanding the ecology and evolution of plant-animal interactions across a heterogeneous phytochemical landscape.

Provenance of rhizobial symbionts is similar for invasive and noninvasive acacias introduced to California.

Plant-soil interactions can be important drivers of biological invasions. In particular, the symbiotic relationship between legumes and nitrogen-fixing soil bacteria (i.e. rhizobia) may be influential in invasion success. Legumes, including Australian acacias, have been introduced into novel ranges around the world. Our goal was to examine the acacia-rhizobia symbiosis to determine whether cointroduction of non-native mutualists plays a role in invasiveness of introduced legumes. To determine whether acacias were introduced abroad concurrently with native symbionts, we selected four species introduced to California (two invasive and two noninvasive in the region) and identified rhizobial strains associating with each species in their native and novel ranges. We amplified three genes to examine phylogenetic placement (16S rRNA) and provenance (nifD and nodC) of rhizobia associating with acacias in California and Australia. We found that all Acacia species, regardless of invasive status, are associating with rhizobia of Australian origin in their introduced ranges, indicating that concurrent acacia-rhizobia introductions have occurred for all species tested. Our results suggest that cointroduction of rhizobial symbionts may be involved in the establishment of non-native acacias in their introduced ranges, but do not contribute to the differential invasiveness of Acacia species introduced abroad.

Contrasts among cationic phytochemical landscapes in the southern United States.

Understanding the phytochemical landscapes of essential and nonessential chemical elements to plants provides an opportunity to better link biogeochemical cycles to trophic ecology. We investigated the formation and regulation of the cationic phytochemical landscapes of four key elements for biota: Ca, Mg, K, and Na. We collected aboveground tissues of plants in Atriplex, Helianthus, and Opuntia and adjacent soils from 51, 131, and 83 sites, respectively, across the southern United States. We determined the spatial variability of these cations in plants and soils. Also, we quantified the homeostasis coefficient for each cation and genus combination, by using mixed-effect models, with spatially correlated random effects. Additionally, using random forest models, we modeled the influence of bioclimatic, soil, and spatial variables on plant cationic concentrations. Sodium variability and spatial autocorrelation were considerably greater than for Ca, Mg, or K. Calcium, Mg, and K exhibited strongly homeostatic patterns, in striking contrast to non-homeostatic Na. Even so, climatic and soil variables explained a large proportion of plants' cationic concentrations. Essential elements (Ca, Mg, and K) appeared to be homeostatically regulated, which contrasted sharply with Na, a nonessential element for most plants. In addition, we provide evidence for the No-Escape-from-Sodium hypothesis in real-world ecosystems, indicating that plant Na concentrations tend to increase as substrate Na levels increase.

No escape: The influence of substrate sodium on plant growth and tissue sodium responses.

As an essential micronutrient for many organisms, sodium plays an important role in ecological and evolutionary dynamics. Although plants mediate trophic fluxes of sodium, from substrates to higher trophic levels, relatively little comparative research has been published about plant growth and sodium accumulation in response to variation in substrate sodium. Accordingly, we carried out a systematic review of plants' responses to variation in substrate sodium concentrations.We compared biomass and tissue-sodium accumulation among 107 cultivars or populations (67 species in 20 plant families), broadly expanding beyond the agricultural and model taxa for which several generalizations previously had been made. We hypothesized a priori response models for each population's growth and sodium accumulation as a function of increasing substrate NaCl and used Bayesian Information Criterion to choose the best model. Additionally, using a phylogenetic signal analysis, we tested for phylogenetic patterning of responses across taxa.The influence of substrate sodium on growth differed across taxa, with most populations experiencing detrimental effects at high concentrations. Irrespective of growth responses, tissue sodium concentrations for most taxa increased as sodium concentration in the substrate increased. We found no strong associations between the type of growth response and the type of sodium accumulation response across taxa. Although experiments often fail to test plants across a sufficiently broad range of substrate salinities, non-crop species tended toward higher sodium tolerance than domesticated species. Moreover, some phylogenetic conservatism was apparent, in that evolutionary history helped predict the distribution of total-plant growth responses across the phylogeny, but not sodium accumulation responses.Our study reveals that saltier plants in saltier soils proves to be a broadly general pattern for sodium across plant taxa. Regardless of growth responses, sodium accumulation mostly followed an increasing trend as substrate sodium levels increased.

Interactions between all pairs of neighboring trees in 16 forests worldwide reveal details of unique ecological processes in each forest, and provide windows into their evolutionary histories.

When Darwin visited the Galapagos archipelago, he observed that, in spite of the islands' physical similarity, members of species that had dispersed to them recently were beginning to diverge from each other. He postulated that these divergences must have resulted primarily from interactions with sets of other species that had also diverged across these otherwise similar islands. By extrapolation, if Darwin is correct, such complex interactions must be driving species divergences across all ecosystems. However, many current general ecological theories that predict observed distributions of species in ecosystems do not take the details of between-species interactions into account. Here we quantify, in sixteen forest diversity plots (FDPs) worldwide, highly significant negative density-dependent (NDD) components of both conspecific and heterospecific between-tree interactions that affect the trees' distributions, growth, recruitment, and mortality. These interactions decline smoothly in significance with increasing physical distance between trees. They also tend to decline in significance with increasing phylogenetic distance between the trees, but each FDP exhibits its own unique pattern of exceptions to this overall decline. Unique patterns of between-species interactions in ecosystems, of the general type that Darwin postulated, are likely to have contributed to the exceptions. We test the power of our null-model method by using a deliberately modified data set, and show that the method easily identifies the modifications. We examine how some of the exceptions, at the Wind River (USA) FDP, reveal new details of a known allelopathic effect of one of the Wind River gymnosperm species. Finally, we explore how similar analyses can be used to investigate details of many types of interactions in these complex ecosystems, and can provide clues to the evolution of these interactions.

Overdispersed Spatial Patterning of Dominant Bunchgrasses in Southeastern Pine Savannas.

Spatial patterning is a key natural history attribute of sessile organisms that frequently emerges from and dictates potential for interactions among organisms. We tested whether bunchgrasses, the dominant plant functional group in longleaf pine savanna groundcover communities, are nonrandomly patterned by characterizing the spatial dispersion of three bunchgrass species across six sites in Louisiana and Florida. We mapped bunchgrass tussocks of >5.0 cm basal diameter in three [Formula: see text] plots at each site. We modeled tussocks as two-dimensional objects to analyze their spatial relationships while preserving sizes and shapes of individual tussocks. Tussocks were overdispersed (more regularly spaced than random) for all species and sites at the local interaction scale (<0.3 m). This general pattern likely arises from a tussock-centered, distance-dependent mechanism, for example, intertussock competition. Nonrandom spatial patterns of dominant species have implications for community assembly and ecosystem function in tussock-dominated grasslands and savannas, including those characterized by extreme biodiversity.

Plant responses to fertilization experiments in lowland, species-rich, tropical forests.

We present a meta-analysis of plant responses to fertilization experiments conducted in lowland, species-rich, tropical forests. We also update a key result and present the first species-level analyses of tree growth rates for a 15-yr factorial nitrogen (N), phosphorus (P), and potassium (K) experiment conducted in central Panama. The update concerns community-level tree growth rates, which responded significantly to the addition of N and K together after 10 yr of fertilization but not after 15 yr. Our experimental soils are infertile for the region, and species whose regional distributions are strongly associated with low soil P availability dominate the local tree flora. Under these circumstances, we expect muted responses to fertilization, and we predicted species associated with low-P soils would respond most slowly. The data did not support this prediction, species-level tree growth responses to P addition were unrelated to species-level soil P associations. The meta-analysis demonstrated that nutrient limitation is widespread in lowland tropical forests and evaluated two directional hypotheses concerning plant responses to N addition and to P addition. The meta-analysis supported the hypothesis that tree (or biomass) growth rate responses to fertilization are weaker in old growth forests and stronger in secondary forests, where rapid biomass accumulation provides a nutrient sink. The meta-analysis found no support for the long-standing hypothesis that plant responses are stronger for P addition and weaker for N addition. We do not advocate discarding the latter hypothesis. There are only 14 fertilization experiments from lowland, species-rich, tropical forests, 13 of the 14 experiments added nutrients for five or fewer years, and responses vary widely among experiments. Potential fertilization responses should be muted when the species present are well adapted to nutrient-poor soils, as is the case in our experiment, and when pest pressure increases with fertilization, as it does in our experiment. The statistical power and especially the duration of fertilization experiments conducted in old growth, tropical forests might be insufficient to detect the slow, modest growth responses that are to be expected.

The causes of disproportionate non-random mortality among life-cycle stages.

The emergent properties of the collection of species in a natural community, such as diversity and the distribution of relative abundances, are influenced by both niche-based and neutral (stochastic) processes. This pluralistic view of the natural world reconciles theory with empirical observations better than does either a strictly niche- or neutrality-based perspective. Even so, rules (or rules of thumb) that govern the relative contributions that niche-based and stochastic processes make as communities assemble remain only vaguely formulated and incompletely tested. For example, the translation of non-random (non-neutral) ecological processes, which differentially sort among species within a community, into species-compositional patterns may occur more influentially within some demographic subsets of organisms than within others. In other words, the relative contributions of niche vs. neutral processes may vary among age-, size-, or stage-classes. For example, non-random patterns of mortality that occur among seedlings in a rain forest, or among newly settled juveniles in communities of sessile marine communities, could be more influential than non-random mortality during later stages in determining overall community diversity. We propose two alternative, mutually compatible, hypotheses to account for different levels of influence from mortality among life-cycle stages toward producing non-random patterns in organismal communities. The Turnover Model simply posits that those demographic classes characterized by faster rates of turnover contribute greater influence in the short-term as sufficient mortality gives rise to non-random changes to the community, as well as over the longer-term as multiple individuals of a given fast-turnover demographic class transition into later classes compared to each individual that ratchets from a slow-turnover starting class into a later class. The Turnover Model should apply to most communities of organisms. The Niche Model, which posits that niche-based processes are more influential in some demographic classes relative to others, may alternatively or additionally apply to communities. We also propose several alternative mechanisms, especially relevant to forest trees, that could cause dynamics consistent with the Niche Model. These mechanisms depend on differences among demographic classes in the extent of demographic variation that individual organisms experience through their trait values or neighborhood conditions.

Correction: Persistence of Neighborhood Demographic Influences over Long Phylogenetic Distances May Help Drive Post-Speciation Adaptation in Tropical Forests.

[This corrects the article DOI: 10.1371/journal.pone.0156913.].

Differential plant invasiveness is not always driven by host promiscuity with bacterial symbionts.

Identification of mechanisms that allow some species to outcompete others is a fundamental goal in ecology and invasive species management. One useful approach is to examine congeners varying in invasiveness in a comparative framework across native and invaded ranges. Acacia species have been widely introduced outside their native range of Australia, and a subset of these species have become invasive in multiple parts of the world. Within specific regions, the invasive status of these species varies. Our study examined whether a key mechanism in the life history of Acacia species, the legume-rhizobia symbiosis, influences acacia invasiveness on a regional scale. To assess the extent to which species varying in invasiveness correspondingly differ with regard to the diversity of rhizobia they associate with, we grew seven Acacia species ranging in invasiveness in California in multiple soils from both their native (Australia) and introduced (California) ranges. In particular, the aim was to determine whether more invasive species formed symbioses with a wider diversity of rhizobial strains (i.e. are more promiscuous hosts). We measured and compared plant performance, including aboveground biomass, survival, and nodulation response, as well as rhizobial community composition and richness. Host promiscuity did not differ among invasiveness categories. Acacia species that varied in invasiveness differed in aboveground biomass for only one soil and did not differ in survival or nodulation within individual soils. In addition, acacias did not differ in rhizobial richness among invasiveness categories. However, nodulation differed between regions and was generally higher in the native than introduced range. Our results suggest that all Acacia species introduced to California are promiscuous hosts and that host promiscuity per se does not explain the observed differences in invasiveness within this region. Our study also highlights the utility of assessing potential mechanisms of invasion in species' native and introduced ranges.

Persistence of Neighborhood Demographic Influences over Long Phylogenetic Distances May Help Drive Post-Speciation Adaptation in Tropical Forests.

Studies of forest dynamics plots (FDPs) have revealed a variety of negative density-dependent (NDD) demographic interactions, especially among conspecific trees. These interactions can affect growth rate, recruitment and mortality, and they play a central role in the maintenance of species diversity in these complex ecosystems. Here we use an equal area annulus (EAA) point-pattern method to comprehensively analyze data from two tropical FDPs, Barro Colorado Island in Panama and Sinharaja in Sri Lanka. We show that these NDD interactions also influence the continued evolutionary diversification of even distantly related tree species in these FDPs. We examine the details of a wide range of these interactions between individual trees and the trees that surround them. All these interactions, and their cumulative effects, are strongest among conspecific focal and surrounding tree species in both FDPs. They diminish in magnitude with increasing phylogenetic distance between heterospecific focal and surrounding trees, but do not disappear or change the pattern of their dependence on size, density, frequency or physical distance even among the most distantly related trees. The phylogenetic persistence of all these effects provides evidence that interactions between tree species that share an ecosystem may continue to promote adaptive divergence even after the species' gene pools have become separated. Adaptive divergence among taxa would operate in stark contrast to an alternative possibility that has previously been suggested, that distantly related species with dispersal-limited distributions and confronted with unpredictable neighbors will tend to converge on common strategies of resource use. In addition, we have also uncovered a positive density-dependent effect: growth rates of large trees are boosted in the presence of a smaller basal area of surrounding trees. We also show that many of the NDD interactions switch sign rapidly as focal trees grow in size, and that their cumulative effect can strongly influence the distributions and species composition of the trees that surround the focal trees during the focal trees' lifetimes.

Nonrandom, diversifying processes are disproportionately strong in the smallest size classes of a tropical forest.

A variety of ecological processes influence diversity and species composition in natural communities. Most of these processes, whether abiotic or biotic, differentially filter individuals from birth to death, thereby altering species' relative abundances. Nonrandom outcomes could accrue throughout ontogeny, or the processes that generate them could be particularly influential at certain stages. One long-standing paradigm in tropical forest ecology holds that patterns of relative abundance among mature trees are largely set by processes operating at the earliest life cycle stages. Several studies confirm filtering processes at some stages, but the longevity of large trees makes a rigorous comparison across size classes impossible without long-term demographic data. Here, we use one of the world's longest-running, plot-based forest dynamics projects to compare nonrandom outcomes across stage classes. We considered a cohort of 7,977 individuals in 186 species that were alive in 1971 and monitored in 13 mortality censuses over 42 y to 2013. Nonrandom mortality with respect to species identity occurred more often in the smaller rather than the larger size classes. Furthermore, observed nonrandom mortality in the smaller size classes had a diversifying influence; species richness of the survivors was up to 30% greater than expected in the two smallest size classes, but not greater than expected in the larger size classes. These results highlight the importance of early life cycle stages in tropical forest community dynamics. More generally, they add to an accumulating body of evidence for the importance of early-stage nonrandom outcomes to community structure in marine and terrestrial environments.

A taxonomic comparison of local habitat niches of tropical trees.

The integration of ecology and evolutionary biology requires an understanding of the evolutionary lability in species' ecological niches. For tropical trees, specialization for particular soil resource and topographic conditions is an important part of the habitat niche, influencing the distributions of individual species and overall tree community structure at the local scale. However, little is known about how these habitat niches are related to the evolutionary history of species. We assessed the relationship between taxonomic rank and tree species' soil resource and topographic niches in eight large (24-50 ha) tropical forest dynamics plots. Niche overlap values, indicating the similarity of two species' distributions along soil or topographic axes, were calculated for all pairwise combinations of co-occurring tree species at each study site. Congeneric species pairs often showed greater niche overlap (i.e., more similar niches) than non-congeneric pairs along both soil and topographic axes, though significant effects were found for only five sites based on Mantel tests. No evidence for taxonomic effects was found at the family level. Our results indicate that local habitat niches of trees exhibit varying degrees of phylogenetic signal at different sites, which may have important ramifications for the phylogenetic structure of these communities.

Soil resources and topography shape local tree community structure in tropical forests.

Both habitat filtering and dispersal limitation influence the compositional structure of forest communities, but previous studies examining the relative contributions of these processes with variation partitioning have primarily used topography to represent the influence of the environment. Here, we bring together data on both topography and soil resource variation within eight large (24-50 ha) tropical forest plots, and use variation partitioning to decompose community compositional variation into fractions explained by spatial, soil resource and topographic variables. Both soil resources and topography account for significant and approximately equal variation in tree community composition (9-34% and 5-29%, respectively), and all environmental variables together explain 13-39% of compositional variation within a plot. A large fraction of variation (19-37%) was spatially structured, yet unexplained by the environment, suggesting an important role for dispersal processes and unmeasured environmental variables. For the majority of sites, adding soil resource variables to topography nearly doubled the inferred role of habitat filtering, accounting for variation in compositional structure that would previously have been attributable to dispersal. Our results, illustrated using a new graphical depiction of community structure within these plots, demonstrate the importance of small-scale environmental variation in shaping local community structure in diverse tropical forests around the globe.

Small-scale variation in fuel loads differentially affects two co-dominant bunchgrasses in a species-rich pine savanna.

Ecological disturbances frequently control the occurrence and patterning of dominant plants in high-diversity communities like C(4) grasslands and savannas. In such ecosystems disturbance-related processes can have important implications for species, and for whole communities when those species are dominant, yet mechanistic understanding of such processes remains fragmentary. Multiple bunchgrass species commonly co-dominate disturbance-dependent and species-rich pine savannas, where small-scale fuel heterogeneity may influence bunchgrass survival and growth following fires. We quantified how fire in locally varying fuel loads influenced dynamics of dominant C(4) bunchgrasses in a species-rich pine savanna in southeastern Louisiana, USA. We focused on two congeneric, co-dominant species (Schizachyrium scoparium and S. tenerum) with similar growth forms, functional traits and reproductive strategies to highlight effects of fuel heterogeneity during fires. In experimental plots with either reduced or increased fuels versus controls with unmanipulated fuels, we compared: 1) bunchgrass damage and 2) mortality from fires; 3) subsequent growth and 4) flowering. Compared to controls, fire with increased fuels caused greater damage, mortality and subsequent flowering, but did not affect post-fire growth. Fire with reduced fuels had no effect on any of the four measures. The two species responded differently to fire with increased fuels--S. scoparium incurred measurably more damage and mortality than S. tenerum. Logistic regression indicated that the larger average size of S. tenerum tussocks made them resistant to more severe burning where fuels were increased. We speculate that locally increased fuel loading may be important in pine savannas for creating colonization sites because where fuels are light or moderate, dominant bunchgrasses persist through fires. Small-scale heterogeneity in fires, and differences in how species tolerate fire may together promote shared local dominance by different bunchgrasses.

Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest.

We maintained a factorial nitrogen (N), phosphorus (P), and potassium (K) addition experiment for 11 years in a humid lowland forest growing on a relatively fertile soil in Panama to evaluate potential nutrient limitation of tree growth rates, fine-litter production, and fine-root biomass. We replicated the eight factorial treatments four times using 32 plots of 40 x 40 m each. The addition of K was associated with significant decreases in stand-level fine-root biomass and, in a companion study of seedlings, decreases in allocation to roots and increases in height growth rates. The addition of K and N together was associated with significant increases in growth rates of saplings and poles (1-10 cm in diameter at breast height) and a further marginally significant decrease in stand-level fine-root biomass. The addition of P was associated with a marginally significant (P = 0.058) increase in fine-litter production that was consistent across all litter fractions. Our experiment provides evidence that N, P, and K all limit forest plants growing on a relatively fertile soil in the lowland tropics, with the strongest evidence for limitation by K among seedlings, saplings, and poles.

Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis.

Tropical rain forests play a dominant role in global biosphere-atmosphere CO(2) exchange. Although climate and nutrient availability regulate net primary production (NPP) and decomposition in all terrestrial ecosystems, the nature and extent of such controls in tropical forests remain poorly resolved. We conducted a meta-analysis of carbon-nutrient-climate relationships in 113 sites across the tropical forest biome. Our analyses showed that mean annual temperature was the strongest predictor of aboveground NPP (ANPP) across all tropical forests, but this relationship was driven by distinct temperature differences between upland and lowland forests. Within lowland forests (< 1000 m), a regression tree analysis revealed that foliar and soil-based measurements of phosphorus (P) were the only variables that explained a significant proportion of the variation in ANPP, although the relationships were weak. However, foliar P, foliar nitrogen (N), litter decomposition rate (k), soil N and soil respiration were all directly related with total surface (0-10 cm) soil P concentrations. Our analysis provides some evidence that P availability regulates NPP and other ecosystem processes in lowland tropical forests, but more importantly, underscores the need for a series of large-scale nutrient manipulations - especially in lowland forests - to elucidate the most important nutrient interactions and controls.

Seed arrival and ecological filters interact to assemble high-diversity plant communities.

Two prominent mechanisms proposed to structure biodiversity are niche-based ecological filtering and chance arrival of propagules from the species pool. Seed arrival is hypothesized to play a particularly strong role in high-diversity plant communities with large potential species pools and many rare species, but few studies have explored how seed arrival and local ecological filters interactively assemble species-rich communities in space and time. We experimentally manipulated seed arrival and multiple ecological filters in high-diversity, herbaceous-dominated groundcover communities in longleaf pine savannas, which contain the highest small-scale species richness in North America (up to > 40 species/m2). We tested three hypotheses: (1) local communities constitute relatively open-membership assemblages, in which increased seed arrival from the species pool strongly increases species richness; (2) ecological filters imposed by local fire intensity and soil moisture influence recruitment and richness of immigrating species; and (3) ecological filters increase similarity in the composition of immigrating species. In a two-year factorial field experiment, we manipulated local fire intensity by increasing pre-fire fuel loads, soil moisture using rain shelters and irrigation, and seed arrival by adding seeds from the local species pool. Seed arrival increased species richness regardless of fire intensity and soil moisture but interacted with both ecological filters to influence community assembly. High-intensity fire decreased richness of resident species, suggesting an important abiotic filter. In contrast, high-intensity fire increased recruitment and richness of immigrating species, presumably by decreasing effects of other ecological filters (competition and resource limitation) in postfire environments. Drought decreased recruitment and richness of immigrating species, whereas wet soil conditions increased recruitment but decreased or had little effect on richness. Moreover, some ecological filters (wet soil conditions and, to a lesser extent, high-intensity fire) increased similarity in the composition of immigrating species, illustrating conditions that influence deterministic community assembly in species-rich communities. Our experiment provides insights into how dispersal-assembly mechanisms may interact with niche-assembly mechanisms in space (spatial variation in disturbance) and time (temporal variation in resource availability) to structure high-diversity communities and can help guide conservation of threatened longleaf pine ecosystems in the face of habitat fragmentation and environmental change.