Daniel P. Bebber

Rules for Biologically Inspired Adaptive Network Design

Miniature Transport Engineers In its vegetative phase, the slime mold Physarum polycephalum “slimes” its way through the world seeking food. As it explores, it links previously found food sources with tubular structures. Tero et al. (p. 439) report that if food sources are deposited on a plate in a pattern corresponding in miniature to the positions of the cities that surround Tokyo, the resulting network of Physarum tubules that develops is rather similar in structure to the railroad network that connects the Japanese cities. A model was produced that describes the adaptive network development displayed by the slime mold. This biologically inspired model might provide insight into how to implement properties like resistance of transport systems to local failures into similar human-designed systems. Human municipal transportation engineers might learn design strategies from the lowly slime mold. Transport networks are ubiquitous in both social and biological systems. Robust network performance involves a complex trade-off involving cost, transport efficiency, and fault tolerance. Biological networks have been honed by many cycles of evolutionary selection pressure and are likely to yield reasonable solutions to such combinatorial optimization problems. Furthermore, they develop without centralized control and may represent a readily scalable solution for growing networks in general. We show that the slime mold Physarum polycephalum forms networks with comparable efficiency, fault tolerance, and cost to those of real-world infrastructure networks—in this case, the Tokyo rail system. The core mechanisms needed for adaptive network formation can be captured in a biologically inspired mathematical model that may be useful to guide network construction in other domains.

Herbaria are a major frontier for species discovery

Despite the importance of species discovery, the processes including collecting, recognizing, and describing new species are poorly understood. Data are presented for flowering plants, measuring quantitatively the lag between the date a specimen of a new species was collected for the first time and when it was subsequently described and published. The data from our sample of new species published between 1970 and 2010 show that only 16% were described within five years of being collected for the first time. The description of the remaining 84% involved much older specimens, with nearly one-quarter of new species descriptions involving specimens >50 y old. Extrapolation of these results suggest that, of the estimated 70,000 species still to be described, more than half already have been collected and are stored in herbaria. Effort, funding, and research focus should, therefore, be directed as much to examining extant herbarium material as collecting new material in the field.

Scale‐dependent relationships between tree species richness and ecosystem function in forests

1. The relationship between species richness and ecosystem function, as measured by productivity or biomass, is of long-standing theoretical and practical interest in ecology. This is especially true for forests, which represent a majority of global biomass, productivity and biodiversity.

Predicting unknown species numbers using discovery curves

A common approach to estimating the total number of extant species in a taxonomic group is to extrapolate from the temporal pattern of known species descriptions. A formal statistical approach to this problem is provided. The approach is applied to a number of global datasets for birds, ants, mosses, lycophytes, monilophytes (ferns and horsetails), gymnosperms and also to New World grasses and UK flowering plants. Overall, our results suggest that unless the inventory of a group is nearly complete, estimating the total number of species is associated with very large margins of error. The strong influence of unpredictable variations in the discovery process on species accumulation curves makes these data unreliable in estimating total species numbers.

Biological solutions to transport network design

Transport networks are vital components of multicellular organisms, distributing nutrients and removing waste products. Animal and plant transport systems are branching trees whose architecture is linked to universal scaling laws in these organisms. In contrast, many fungi form reticulated mycelia via the branching and fusion of thread-like hyphae that continuously adapt to the environment. Fungal networks have evolved to explore and exploit a patchy environment, rather than ramify through a three-dimensional organism. However, there has been no explicit analysis of the network structures formed, their dynamic behaviour nor how either impact on their ecological function. Using the woodland saprotroph Phanerochaete velutina, we show that fungal networks can display both high transport capacity and robustness to damage. These properties are enhanced as the network grows, while the relative cost of building the network decreases. Thus, mycelia achieve the seemingly competing goals of efficient transport and robustness, with decreasing relative investment, by selective reinforcement and recycling of transport pathways. Fungal networks demonstrate that indeterminate, decentralized systems can yield highly adaptive networks. Understanding how these relatively simple organisms have found effective transport networks through a process of natural selection may inform the design of man-made networks.

Fungi in Biogeochemical Cycles: The role of wood decay fungi in the carbon and nitrogen dynamics of the forest floor

decomposed amino acid that tracks the mycelial free amino acid pool. Its movement can be imaged by counting photon emissions from a scintillant screen in contact with the mycelial system. This method allows real-time imaging at high temporal and spatial resolution, for periods of weeks and areas up to 1 m 2 , in microcosms that mimic the mineral/organic soil interface of the forest floor. The results reveal a hitherto unsuspected dynamism and responsiveness in amino acid flows through mycelial networks of cord-forming, wood-decomposing basidiomycetes. We interpret these in the light of current understanding of the pivotal role of fungi in boreal and temperate forest floor nutrient cycling, and attempt to formulate key questions to investigate the effects of mycelial nitrogen translocation on forest floor decomposition and nitrogen absorption.

Imaging complex nutrient dynamics in mycelial networks

Transport networks are vital components of multi‐cellular organisms, distributing nutrients and removing waste products. Animal cardiovascular and respiratory systems, and plant vasculature, are branching trees whose architecture is thought to determine universal scaling laws in these organisms. In contrast, the transport systems of many multi‐cellular fungi do not fit into this conceptual framework, as they have evolved to explore a patchy environment in search of new resources, rather than ramify through a three‐dimensional organism. These fungi grow as a foraging mycelium, formed by the branching and fusion of threadlike hyphae, that gives rise to a complex network. To function efficiently, the mycelial network must both transport nutrients between spatially separated source and sink regions and also maintain its integrity in the face of continuous attack by mycophagous insects or random damage. Here we review the development of novel imaging approaches and software tools that we have used to characterise nutrient transport and network formation in foraging mycelia over a range of spatial scales. On a millimetre scale, we have used a combination of time‐lapse confocal imaging and fluorescence recovery after photobleaching to quantify the rate of diffusive transport through the unique vacuole system in individual hyphae. These data then form the basis of a simulation model to predict the impact of such diffusion‐based movement on a scale of several millimetres. On a centimetre scale, we have used novel photon‐counting scintillation imaging techniques to visualize radiolabel movement in small microcosms. This approach has revealed novel N‐transport phenomena, including rapid, preferential N‐resource allocation to C‐rich sinks, induction of simultaneous bi‐directional transport, abrupt switching between different pre‐existing transport routes, and a strong pulsatile component to transport in some species. Analysis of the pulsatile transport component using Fourier techniques shows that as the colony forms, it self‐organizes into well demarcated domains that are identifiable by differences in the phase relationship of the pulses. On the centimetre to metre scale, we have begun to use techniques borrowed from graph theory to characterize the development and dynamics of the network, and used these abstracted network models to predict the transport characteristics, resilience, and cost of the network.

Range-Expanding Pests and Pathogens in a Warming World

Crop pests and pathogens (CPPs) present a growing threat to food security and ecosystem management. The interactions between plants and their natural enemies are influenced by environmental conditions and thus global warming and climate change could affect CPP ranges and impact. Observations of changing CPP distributions over the twentieth century suggest that growing agricultural production and trade have been most important in disseminating CPPs, but there is some evidence for a latitudinal bias in range shifts that indicates a global warming signal. Species distribution models using climatic variables as drivers suggest that ranges will shift latitudinally in the future. The rapid spread of the Colorado potato beetle across Eurasia illustrates the importance of evolutionary adaptation, host distribution, and migration patterns in affecting the predictions of climate-based species distribution models. Understanding species range shifts in the framework of ecological niche theory may help to direct future research needs.

Simulated nitrogen deposition affects wood decomposition by cord-forming fungi

Anthropogenic nitrogen (N) deposition affects many natural processes, including forest litter decomposition. Saprotrophic fungi are the only organisms capable of completely decomposing lignocellulosic (woody) litter in temperate ecosystems, and therefore the responses of fungi to N deposition are critical in understanding the effects of global change on the forest carbon cycle. Plant litter decomposition under elevated N has been intensively studied, with varying results. The complexity of forest floor biota and variability in litter quality have obscured N-elevation effects on decomposers. Field experiments often utilize standardized substrates and N-levels, but few studies have controlled the decay organisms. Decomposition of beech (Fagus sylvatica) blocks inoculated with two cord-forming basidiomycete fungi, Hypholoma fasciculare and Phanerochaete velutina, was compared experimentally under realistic levels of simulated N deposition at Wytham Wood, Oxfordshire, UK. Mass loss was greater with P. velutina than with H. fasciculare, and with N treatment than in the control. Decomposition was accompanied by growth of the fungal mycelium and increasing N concentration in the remaining wood. We attribute the N effect on wood decay to the response of cord-forming wood decay fungi to N availability. Previous studies demonstrated the capacity of these fungi to scavenge and import N to decaying wood via a translocating network of mycelium. This study shows that small increases in N availability can increase wood decomposition by these organisms. Dead wood is an important carbon store and habitat. The responses of wood decomposers to anthropogenic N deposition should be considered in models of forest carbon dynamics.

Edge effects on moisture reduce wood decomposition rate in a temperate forest.

Forests around the world are increasingly fragmented, and edge effects on forest microclimates have the potential to affect ecosystem functions such as carbon and nutrient cycling. Edges tend to be drier and warmer due to the effects of insolation, wind, and evapotranspiration and these gradients can penetrate hundreds of metres into the forest. Litter decomposition is a key component of the carbon cycle, which is largely controlled by saprotrophic fungi that respond to variation in temperature and moisture. However, the impact of forest fragmentation on litter decay is poorly understood. Here, we investigate edge effects on the decay of wood in a temperate forest using an experimental approach, whereby mass loss in wood blocks placed along 100 m transects from the forest edge to core was monitored over 2 years. Decomposition rate increased with distance from the edge, and was correlated with increasing humidity and moisture content of the decaying wood, such that the decay constant at 100 m was nearly twice that at the edge. Mean air temperature decreased slightly with distance from the edge. The variation in decay constant due to edge effects was larger than that expected from any reasonable estimates of climatic variation, based on a published regional model. We modelled the influence of edge effects on the decay constant at the landscape scale using functions for forest area within different distances from edge across the UK. We found that taking edge effects into account would decrease the decay rate by nearly one quarter, compared with estimates that assumed no edge effect.