Noelle G. Beckman

Rate of tree carbon accumulation increases continuously with tree size

Forests are major components of the global carbon cycle, providing substantial feedback to atmospheric greenhouse gas concentrations. Our ability to understand and predict changes in the forest carbon cycle—particularly net primary productivity and carbon storage—increasingly relies on models that represent biological processes across several scales of biological organization, from tree leaves to forest stands. Yet, despite advances in our understanding of productivity at the scales of leaves and stands, no consensus exists about the nature of productivity at the scale of the individual tree, in part because we lack a broad empirical assessment of whether rates of absolute tree mass growth (and thus carbon accumulation) decrease, remain constant, or increase as trees increase in size and age. Here we present a global analysis of 403 tropical and temperate tree species, showing that for most species mass growth rate increases continuously with tree size. Thus, large, old trees do not act simply as senescent carbon reservoirs but actively fix large amounts of carbon compared to smaller trees; at the extreme, a single big tree can add the same amount of carbon to the forest within a year as is contained in an entire mid-sized tree. The apparent paradoxes of individual tree growth increasing with tree size despite declining leaf-level and stand-level productivity can be explained, respectively, by increases in a tree’s total leaf area that outpace declines in productivity per unit of leaf area and, among other factors, age-related reductions in population density. Our results resolve conflicting assumptions about the nature of tree growth, inform efforts to undertand and model forest carbon dynamics, and have additional implications for theories of resource allocation and plant senescence.

Testing predictions of the Janzen–Connell hypothesis: a meta‐analysis of experimental evidence for distance‐ and density‐dependent seed and seedling survival

The Janzen–Connell hypothesis proposes that specialist natural enemies, such as herbivores and pathogens, maintain diversity in plant communities by reducing survival rates of conspecific seeds and seedlings located close to reproductive adults or in areas of high conspecific density. Variation in the strength of distance- and density-dependent effects is hypothesized to explain variation in plant species richness along climatic gradients, with effects predicted to be stronger in the tropics than the temperate zone and in wetter habitats compared to drier habitats. We conducted a comprehensive literature search to identify peer-reviewed experimental studies published in the 40+ years since the hypothesis was first proposed. Using data from these studies, we conducted a meta-analysis to assess the current weight of evidence for the distance and density predictions of the Janzen–Connell hypothesis. Overall, we found significant support for both the distance- and density-dependent predictions. For all studies combined, survival rates were significantly reduced near conspecifics compared to far from conspecifics, and in areas with high densities of conspecifics compared to areas with low conspecific densities. There was no indication that these results were due to publication bias. The strength of distance and density effects varied widely among studies. Contrary to expectations, this variation was unrelated to latitude, and there was no significant effect of study region. However, we did find a trend for stronger distance and density dependence in wetter sites compared to sites with lower annual precipitation. In addition, effects were significantly stronger at the seedling stage compared to the seed stage. Synthesis. Our study provides support for the idea that distance- and density-dependent mortality occurs in plant communities world-wide. Available evidence suggests that natural enemies are frequently the cause of such patterns, consistent with the Janzen–Connell hypothesis, but additional studies are needed to rule out other mechanisms (e.g. intraspecific competition). With the widespread existence of density and distance dependence clearly established, future research should focus on assessing the degree to which these effects permit species coexistence and contribute to the maintenance of diversity in plant communities.

EFFECTS OF FOREST ROADS ON THE ABUNDANCE AND ACTIVITY OF TERRESTRIAL SALAMANDERS

One of the major effects of deforestation is the creation of numerous edge zones where remaining forest meets nonforest habitat. At this interface, edge effects on forest habitats can include altered abiotic conditions, changes in rates of competition and predation, and altered community structure. While the edge effects resulting from clear- cuts and other open habitats are well-studied, little is known about the comparative edge effects of forest roads. We studied the effects of forest roads on the abundance, surface activity, and body condition of red-backed salamanders (Plethodon cinereus) and slimy salamanders (P. glutinosus and P. cylindraceus) in the Southern Appalachians of Virginia. We conducted surveys for salamanders at 21 sites where gravel roads bisected mature forest. These sites were divided into three data sets based on region and year of survey. We also carried out an enclosure experiment to determine whether road edges influenced the surface activity and detectability of red-backed salamanders. We found fewer red-backed salaman- ders near roads in all three data sets. These edge effects extended ,20 m into the forest in two of the three data sets but increased linearly out to 80 m in the data set collected during an unusually dry period. In contrast, slimy salamanders showed no clear responses to forest-road edges and had significantly different responses than those of red-backed salamanders. Within our experimental enclosures, red-backed salamander detectability did not differ between edge and interior habitats, suggesting that the patterns we observed were not simply due to changes in salamander activity patterns. Like red-backed salamander counts, soil moisture and cover object area also tended to decrease near roads. The steepness of the gradient in soil moisture was a significant predictor of the steepness of the decline in salamander counts, while there was no significant relationship between the decreases in cover object area and decreases in salamander counts. Collectively, these results show that edge effects from forest roads may be comparable to edge effects from clear-cuts or other types of silvicultural edges. Additionally, they suggest that, for terrestrial salamanders, variation in the magnitude of edge effects may be related to variation in soil moisture. Management approaches that minimize soil desiccation associated with road building and maintenance may reduce the impacts of roads on amphibian populations in adjacent forest.

Pollen feeding and fitness in praying mantids: The vegetarian side of a tritrophic predator

Abstract Although the importance of omnivory in food webs has been established, the community niche of generalist arthropod predators such as praying mantids is usually assumed to be at most bitrophic, feeding on herbivores and other carnivores. As with most predators, mantids often are food limited in nature. Flowering plants in their environment offer mantids an opportunity to obtain high-protein pollen, a potential vegetarian alternative to their normal arthropod prey. Although some arthropod predators have been shown to feed occasionally on pollen, the extent to which they gain fitness from this behavior is unclear, and often assumed to be minor. In replicated laboratory tests, Chinese mantids, Tenodera aridifolia sinensis (Saussure), actively fed on pollen just after hatching, and on pollen-laden insects as adults. Pollen feeding enhanced fitness of these mantids by: 1) preventing starvation of nymphs at egg hatch in the absence of normal insect prey; 2) increasing body mass of nymphs fed pollen in addition to normal prey; and 3) allowing adults that were fed both pollen and insects to maintain the same fecundity on fewer insect prey than those fed insects alone. These predators are therefore tritrophic because the extent of their omnivory includes a fitness-enhancing plant product in addition to herbivore and carnivore prey. Pollen feeding may explain higher fecundity of females located on flowers, and also may enable these and other generalist predators to maintain high population densities when animal prey are scarce, which has potential consequences for the rest of the community.

Linking fruit traits to variation in predispersal vertebrate seed predation, insect seed predation, and pathogen attack

The importance of vertebrates, invertebrates, and pathogens for plant communities has long been recognized, but their absolute and relative importance in early recruitment of multiple coexisting tropical plant species has not been quantified. Further, little is known about the relationship of fruit traits to seed mortality due to natural enemies in tropical plants. To investigate the influences of vertebrates, invertebrates, and pathogens on reproduction of seven canopy plant species varying in fruit traits, we quantified reductions in fruit development and seed germination due to vertebrates, invertebrates, and fungal pathogens through experimental removal of these enemies using canopy exclosures, insecticide, and fungicide, respectively. We also measured morphological fruit traits hypothesized to mediate interactions of plants with natural enemies of seeds. Vertebrates, invertebrates, and fungi differentially affected predispersal seed mortality depending on the plant species. Fruit morphology explained some variation among species; species with larger fruit and less physical protection surrounding seeds exhibited greater negative effects of fungi on fruit development and germination and experienced reduced seed survival integrated over fruit development and germination in response to vertebrates. Within species, variation in seed size also contributed to variation in natural enemy effects on seed viability. Further, seedling growth was higher for seeds that developed in vertebrate exclosures for Anacardium excelsum and under the fungicide treatment for Castilla elastica, suggesting that predispersal effects of natural enemies may carry through to the seedling stage. This is the first experimental test of the relative effects of vertebrates, invertebrates, and pathogens on seed survival in the canopy. This study motivates further investigation to determine the generality of our results for plant communities. If there is strong variation in natural enemy attack among species related to differences in fruit morphology, then quantification of fruit traits will aid in predicting the outcomes of interactions between plants and their natural enemies. This is particularly important in tropical forests, where high species diversity makes it logistically impossible to study every plant life history stage of every species.

The Distribution of Fruit and Seed Toxicity during Development for Eleven Neotropical Trees and Vines in Central Panama

Secondary compounds in fruit mediate interactions with natural enemies and seed dispersers, influencing plant survival and species distributions. The functions of secondary metabolites in plant defenses have been well-studied in green tissues, but not in reproductive structures of plants. In this study, the distribution of toxicity within plants was quantified and its influence on seed survival was determined in Central Panama. To investigate patterns of allocation to chemical defenses and shifts in allocation with fruit development, I quantified variation in toxicity between immature and mature fruit and between the seed and pericarp for eleven species. Toxicity of seed and pericarp was compared to leaf toxicity for five species. Toxicity was measured as reduced hyphal growth of two fungal pathogens, Phoma sp. and Fusarium sp., and reduced survivorship of brine shrimp, Artemia franciscana, across a range of concentrations of crude extract. I used these measures of potential toxicity against generalist natural enemies to examine the effect of fruit toxicity on reductions of fruit development and seed survival by vertebrates, invertebrates, and pathogens measured for seven species in a natural enemy removal experiment. The seed or pericarp of all vertebrate- and wind-dispersed species reduced Artemia survivorship and hyphal growth of Fusarium during the immature and mature stages. Only mature fruit of two vertebrate-dispersed species reduced hyphal growth of Phoma. Predispersal seed survival increased with toxicity of immature fruit to Artemia during germination and decreased with toxicity to fungi during fruit development. This study suggests that fruit toxicity against generalist natural enemies may be common in Central Panama. These results support the hypothesis that secondary metabolites in fruit have adaptive value and are important in the evolution of fruit-frugivore interactions.

High Dispersal Ability is Related to Fast Life-History Strategies

Seed dispersal is an essential, yet often overlooked process in plant ecology and evolution, affecting adaptation capacity, population persistence and invasiveness. A species’ ability to disperse is expected to covary with other life-history traits to form dispersal syndromes. Dispersal might be linked to the rate of life history, fecundity or generation time, depending on the relative selection pressures of bet-hedging, kin competition or maintaining gene flow. However, the linkage between dispersal and plant life-history strategies remains unknown because it is difficult to observe, quantify and manipulate the influence of dispersal over large spatiotemporal scales. We integrate datasets describing plant vital rates, dispersal and functional traits to incorporate dispersal explicitly into the rich spectra of plant life-history strategies. For 141 plant species, we estimated dispersal ability by predicting maximum dispersal distances using allometric relationships based on growth form, dispersal mode, terminal velocity and seed mass. We derived life-history traits from matrix population models parameterized with field data from the COMPADRE Plant Matrix Database. We analysed the covariation in dispersal ability and life-history traits using multivariate techniques. We found that three main axes of variation described plant dispersal syndromes: the fast-slow life-history continuum, the dispersal strategy axis and the reproductive strategy axis. On the dispersal strategy axis, species’ dispersal abilities were positively correlated with aspects of fast life histories. Species with a high net reproductive rate, a long window of reproduction, low likelihood of escaping senescence and low shrinkage tendencies disperse their seeds further. The overall phylogenetic signal in our multidimensional analyses was low (Pagels λ < 0.24), implying a high degree of taxonomic generality in our findings. Synthesis. Dispersal has been largely neglected in comparative demographic studies, despite its pivotal importance for populations. Our explicit incorporation of dispersal in a comparative life-history framework provides key insights to bridge the gap between dispersal ecology and life-history traits. Species with fast life-history strategies disperse their seeds further than slow-living plants, suggesting that longer dispersal distances may allow these species to take advantage of habitats varying unpredictably in space and time as a bet-hedging strategy.