Scott Ferrenberg

Patterns and Processes of Microbial Community Assembly

SUMMARY Recent research has expanded our understanding of microbial community assembly. However, the field of community ecology is inaccessible to many microbial ecologists because of inconsistent and often confusing terminology as well as unnecessarily polarizing debates. Thus, we review recent literature on microbial community assembly, using the framework of Vellend (Q. Rev. Biol. 85:183–206, 2010) in an effort to synthesize and unify these contributions. We begin by discussing patterns in microbial biogeography and then describe four basic processes (diversification, dispersal, selection, and drift) that contribute to community assembly. We also discuss different combinations of these processes and where and when they may be most important for shaping microbial communities. The spatial and temporal scales of microbial community assembly are also discussed in relation to assembly processes. Throughout this review paper, we highlight differences between microbes and macroorganisms and generate hypotheses describing how these differences may be important for community assembly. We end by discussing the implications of microbial assembly processes for ecosystem function and biodiversity.

Changes in assembly processes in soil bacterial communities following a wildfire disturbance

Although recent work has shown that both deterministic and stochastic processes are important in structuring microbial communities, the factors that affect the relative contributions of niche and neutral processes are poorly understood. The macrobiological literature indicates that ecological disturbances can influence assembly processes. Thus, we sampled bacterial communities at 4 and 16 weeks following a wildfire and used null deviation analysis to examine the role that time since disturbance has in community assembly. Fire dramatically altered bacterial community structure and diversity as well as soil chemistry for both time-points. Community structure shifted between 4 and 16 weeks for both burned and unburned communities. Community assembly in burned sites 4 weeks after fire was significantly more stochastic than in unburned sites. After 16 weeks, however, burned communities were significantly less stochastic than unburned communities. Thus, we propose a three-phase model featuring shifts in the relative importance of niche and neutral processes as a function of time since disturbance. Because neutral processes are characterized by a decoupling between environmental parameters and community structure, we hypothesize that a better understanding of community assembly may be important in determining where and when detailed studies of community composition are valuable for predicting ecosystem function.

Mountain pine beetle develops an unprecedented summer generation in response to climate warming.

The mountain pine beetle (MPB; Dendroctonus ponderosae) is native to western North America, attacks most trees of the genus Pinus, and periodically erupts in epidemics. The current epidemic of the MPB is an order of magnitude larger than any previously recorded, reaching trees at higher elevation and latitude than ever before. Here we show that after 2 decades of air-temperature increases in the Colorado Front Range, the MPB flight season begins more than 1 month earlier than and is approximately twice as long as the historically reported season. We also report, for the first time, that the life cycle in some broods has increased from one to two generations per year. Because MPBs do not diapause and their development is controlled by temperature, they are responding to climate change through faster development. The expansion of the MPB into previously inhospitable environments, combined with the measured ability to increase reproductive output in such locations, indicates that the MPB is tracking climate change, exacerbating the current epidemic.

Climate change and physical disturbance cause similar community shifts in biological soil crusts

Significance In drylands worldwide, where plant cover is sparse, large amounts of the ground surface are covered by specialized organisms that form biological soil crusts (biocrusts). Biocrusts fix carbon and nitrogen, stabilize soils, and influence hydrology. Extensive physical disturbance from livestock/human trampling and off-road vehicles is known to destroy biocrusts and alter ecosystem function. More recent work also indicates that climate change can affect biocrust communities. Contrary to our expectations, experimental climate change and physical disturbance had strikingly similar impacts on biocrust communities, with both promoting a shift to degraded, early successional states. These results herald ecological state transitions in drylands as temperatures rise, calling for management strategies that consider risks from both physical disturbances and climate change. Biological soil crusts (biocrusts)—communities of mosses, lichens, cyanobacteria, and heterotrophs living at the soil surface—are fundamental components of drylands worldwide, and destruction of biocrusts dramatically alters biogeochemical processes, hydrology, surface energy balance, and vegetation cover. Although there has been long-standing concern over impacts of physical disturbances on biocrusts (e.g., trampling by livestock, damage from vehicles), there is increasing concern over the potential for climate change to alter biocrust community structure. Using long-term data from the Colorado Plateau, we examined the effects of 10 y of experimental warming and altered precipitation (in full-factorial design) on biocrust communities and compared the effects of altered climate with those of long-term physical disturbance (>10 y of replicated human trampling). Surprisingly, altered climate and physical disturbance treatments had similar effects on biocrust community structure. Warming, altered precipitation frequency [an increase of small (1.2 mm) summer rainfall events], and physical disturbance from trampling all promoted early successional community states marked by dramatic declines in moss cover and increases in cyanobacteria cover, with more variable effects on lichens. Although the pace of community change varied significantly among treatments, our results suggest that multiple aspects of climate change will affect biocrusts to the same degree as physical disturbance. This is particularly disconcerting in the context of warming, as temperatures for drylands are projected to increase beyond those imposed as treatments in our study.

Decreases in average bacterial community rRNA operon copy number during succession

Trait-based studies can help clarify the mechanisms driving patterns of microbial community assembly and coexistence. Here, we use a trait-based approach to explore the importance of rRNA operon copy number in microbial succession, building on prior evidence that organisms with higher copy numbers respond more rapidly to nutrient inputs. We set flasks of heterotrophic media into the environment and examined bacterial community assembly at seven time points. Communities were arrayed along a geographic gradient to introduce stochasticity via dispersal processes and were analyzed using 16 S rRNA gene pyrosequencing, and rRNA operon copy number was modeled using ancestral trait reconstruction. We found that taxonomic composition was similar between communities at the beginning of the experiment and then diverged through time; as well, phylogenetic clustering within communities decreased over time. The average rRNA operon copy number decreased over the experiment, and variance in rRNA operon copy number was lowest both early and late in succession. We then analyzed bacterial community data from other soil and sediment primary and secondary successional sequences from three markedly different ecosystem types. Our results demonstrate that decreases in average copy number are a consistent feature of communities across various drivers of ecological succession. Importantly, our work supports the scaling of the copy number trait over multiple levels of biological organization, ranging from cells to populations and communities, with implications for both microbial ecology and evolution.

Smooth bark surfaces can defend trees against insect attack: resurrecting a ‘slippery’ hypothesis

Summary 1. Smooth bark on trees and shrubs was historically hypothesized to be an anatomical defence against epiphytic vegetation and phytophagous insects. This hypothesis has fallen from favour, yet no clear tests of bark texture as a defence against insects have been published. 2. We tested the smooth bark defence hypothesis using bark beetles specialized in attacking pine trees as model insects, and Pinus flexilis (limber pine) – a widespread tree that can have both smooth and rough bark surfaces on the same stem – as the model tree. We investigated the effects of bark texture on the locations of bark beetle attacks on trees with a combination of field surveys and experiments in the Colorado Rocky Mountains, USA. 3. Bark beetle attacks were overwhelmingly located on rough bark surfaces and virtually absent from smooth bark. Increasing proportional coverage by smooth bark was negatively related to bark beetle attacks per square metre of bark surface. Experimental tests of bark beetles’ ability to grip smooth versus rough bark revealed that bark beetles have difficulty gripping and quickly fell from smooth bark but not from rough bark. 4. Smooth bark was negatively related to increasing tree size, but our models indicated that even partial coverage by smooth bark on a tree’s trunk can significantly reduce total bark beetle attacks – this reduction likely improves tree fitness as bark beetles must aggregate to overcome tree defences. 5. Synthesis. Our results indicate that smooth bark on trees can act as an anatomical defence against insects by reducing their ability to grip a tree’s surface – even for insects specialized in attacking tree stems. Similar to other forms of anti-insect defence (i.e. secondary chemistry, leaf toughness), smooth bark appears to be influenced by plant ontogeny whereby younger trees have greater defences than older trees. Understanding the adaptive significance of bark texture will require continued field and genetic study. Nevertheless, our results revealed that smooth bark texture increases tree resistance to phytophagous insects calling for the resurrection and vetting of the smooth bark defence hypothesis.

Soil bacterial community structure remains stable over a 5-year chronosequence of insect-induced tree mortality

Extensive tree mortality from insect epidemics has raised concern over possible effects on soil biogeochemical processes. Yet despite the importance of microbes in nutrient cycling, how soil bacterial communities respond to insect-induced tree mortality is largely unknown. We examined soil bacterial community structure (via 16S rRNA gene pyrosequencing) and community assembly processes (via null deviation analysis) along a 5-year chronosequence (substituting space for time) of bark beetle-induced tree mortality in the southern Rocky Mountains, USA. We also measured microbial biomass and soil chemistry, and used in situ experiments to assess inorganic nitrogen mineralization rates. We found that bacterial community structure and assembly—which was strongly influenced by stochastic processes—were largely unaffected by tree mortality despite increased soil ammonium (NH4+) pools and reductions in soil nitrate (NO3−) pools and net nitrogen mineralization rates after tree mortality. Linear models suggested that microbial biomass and bacterial phylogenetic diversity are significantly correlated with nitrogen mineralization rates of this forested ecosystem. However, given the overall resistance of the bacterial community to disturbance from tree mortality, soil nitrogen processes likely remained relatively stable following tree mortality when considered at larger spatial and longer temporal scales—a supposition supported by the majority of available studies regarding biogeochemical effects of bark beetle infestations in this region. Our results suggest that soil bacterial community resistance to disturbance helps to explain the relatively weak effects of insect-induced tree mortality on soil N and C pools reported across the Rocky Mountains, USA.

Banking on the past: seed banks as a reservoir for rare and native species in restored vernal pools

We found the belowground community in the soil seed bank of restored vernal pools has been less invaded by exotic plants and is a reservoir for rare and native plant species. We also found that seed bank community structure most closely resembled the aboveground community structure from five to eight years prior to seed bank sampling rather than more recent years. The maintenance of rare and native plant species in soil seed banks, even as aboveground vegetation communities become invaded by exotic plants is an exciting finding with important implications for management and restoration efforts in annual plant communities.

Competition as a factor underlying the abundance of an uncommon phytophagous insect, the salt-marsh planthopper Delphacodes penedetecta

Abstract. 1. Recent reviews of experimental studies provide compelling evidence that competition should be retained as a potential factor influencing the success of phytophagous insects. In this context, the objective of the study was to determine the role of interspecific and intraspecific competition, both contemporaneous and plant mediated (feeding‐induced resistance), in limiting the population density of a consistently rare insect in a guild of abundant potential competitors.

Albedo feedbacks to future climate via climate change impacts on dryland biocrusts

Drylands represent the planet’s largest terrestrial biome and evidence suggests these landscapes have large potential for creating feedbacks to future climate. Recent studies also indicate that dryland ecosystems are responding markedly to climate change. Biological soil crusts (biocrusts) ‒ soil surface communities of lichens, mosses, and/or cyanobacteria ‒ comprise up to 70% of dryland cover and help govern fundamental ecosystem functions, including soil stabilization and carbon uptake. Drylands are expected to experience significant changes in temperature and precipitation regimes, and such alterations may impact biocrust communities by promoting rapid mortality of foundational species. In turn, biocrust community shifts affect land surface cover and roughness—changes that can dramatically alter albedo. We tested this hypothesis in a full-factorial warming (+4 °C above ambient) and altered precipitation (increased frequency of 1.2 mm monsoon-type watering events) experiment on the Colorado Plateau, USA. We quantified changes in shortwave albedo via multi-angle, solar-reflectance measurements. Warming and watering treatments each led to large increases in albedo (>30%). This increase was driven by biophysical factors related to treatment effects on cyanobacteria cover and soil surface roughness following treatment-induced moss and lichen mortality. A rise in dryland surface albedo may represent a previously unidentified feedback to future climate.