Effects of Predator Avoidance Behavior on the Coexistence of Competing Prey

Predator avoidance behavior, in which prey limit foraging activities in the presence of predation threats, affects the dynamics of many ecological communities. Despite the growing theoretical appreciation of the role predation plays in coexistence, predator avoidance behavior has yet to be incorporated into the theory in a general way. We introduce adaptive avoidance behavior to a consumer-resource model with three trophic levels to ask whether the ability of prey-the middle trophic level-to avoid predators alters their ability to coexist. We determine the characteristics of cases in which predator avoidance behavior changes prey coexistence or the order of competitive dominance. The mechanism underlying such changes is the weakening of apparent competition relative to resource competition in determining niche overlap, even with resource intake costs. Avoidance behavior thus generally promotes coexistence if prey partition resources but not predators, whereas it undermines coexistence if prey partition predators but not resources. For any given case, the changes in the average fitness difference between two species resulting from avoidance behavior interact with changes in niche overlap to determine coexistence. These results connect the substantial body of theoretical work on avoidance behavior and population dynamics with the body of theory on competitive coexistence.National Science Foundation [DEB-1353715]12 month embargo; published online: 07 March 2019This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

Island Biogeography of Cryoconite Hole Bacteria in Antarctica's Taylor Valley and Around the World

Cryoconite holes are holes in a glacier's surface caused by sediment melting into the glacier. These holes are self-contained ecosystems that include abundant bacterial life within their sediment and liquid water, and have recently gained the attention of microbial ecologists looking to use cryoconite holes as “natural microcosms” to study microbial community assembly. Here, we explore the idea that cryoconite holes can be viewed as “islands,” in the same sense that an island in the ocean is an area of habitat surrounded by a barrier to entry. In the case of a classic oceanic island, the ocean is a barrier between islands, but in the case of cryoconite holes, the ocean is comprised of impermeable solid ice. We test two hypotheses, born out of island biogeographic theory, that can be readily applied to cryoconite hole bacteria. First, we ask to what extent the size of a cryoconite hole is related to the amount of bacterial diversity found within it. Second, we ask to what extent cryoconite holes exhibit distance decay of similarity, meaning that geographically close holes are expected to harbor similar bacterial communities, and distant holes are expected to harbor more different bacterial communities. To test the island size hypothesis, we measured the sizes of cryoconite holes on three glaciers in Antarctica's Taylor Valley and used DNA sequencing to measure diversity of bacterial communities within them. We found that for two of these glaciers, there is a strong relationship between hole size and bacterial phylogenetic diversity, supporting the idea that cryoconite holes on those glaciers are “islands.” The high biomass dispersing to the third glacier we measured could explain the lack of size-diversity relationship, remaining consistent with island biogeography. To test the distance decay of similarity hypothesis, we used DNA sequence data from several previous studies of cryoconite hole bacteria from across the world. Combined with our Taylor Valley data, those data showed that cryoconite holes have strong spatial structuring at scales of one to several hundred kilometers, also supporting the idea that these dirty holes on glaciers are really islands in the cryosphere

Single-Stranded DNA Viruses in Antarctic Cryoconite Holes

Antarctic cryoconite holes, or small melt-holes in the surfaces of glaciers, create habitable oases for isolated microbial communities with tightly linked microbial population structures. Viruses may influence the dynamics of polar microbial communities, but the viromes of the Antarctic cryoconite holes have yet to be characterized. We characterize single-stranded DNA (ssDNA) viruses from three cryoconite holes in the Taylor Valley, Antarctica, using metagenomics. Half of the assembled metagenomes cluster with those in the viral family Microviridae (n = 7), and the rest with unclassified circular replication associated protein (Rep)-encoding single-stranded (CRESS) DNA viruses (n = 7). An additional 18 virus-like circular molecules encoding either a Rep, a capsid protein gene, or other unidentified but viral-like open reading frames were identified. The samples from which the genomes were identified show a strong gradient in microbial diversity and abundances, and the number of viral genomes detected in each sample mirror that gradient. Additionally, one of the CRESS genomes assembled here shares ~90% genome-wide pairwise identity with a virus identified from a freshwater pond on the McMurdo Ice Shelf (Antarctica). Otherwise, the similarity of these viruses to those previously identified is relatively low. Together, these patterns are consistent with the presence of a unique regional virome present in fresh water host populations of the McMurdo Dry Valley region

Gullies and Moraines Are Islands of Biodiversity in an Arid, Mountain Landscape, Asgard Range, Antarctica

Cold, dry, and nutrient-poor, the McMurdo Dry Valleys of Antarctica are among the most extreme terrestrial environments on Earth. Numerous studies have described microbial communities of low elevation soils and streams below glaciers, while less is known about microbial communities in higher elevation soils above glaciers. We characterized microbial life in four landscape features (habitats) of a mountain in Taylor Valley. These habitats varied significantly in soil moisture and include moist soils of a (1) lateral glacial moraine, (2) gully that terminates at the moraine, and very dry soils on (3) a southeastern slope and (4) dry sites near the gully. Using rRNA gene PCR amplicon sequencing of Bacteria and Archaea (16S SSU) and eukaryotes (18S SSU), we found that all habitat types harbored significantly different bacterial and eukaryotic communities and that these differences were most apparent when comparing habitats that had macroscopically visible soil crusts (gully and moraine) to habitats with no visible crusts (near gully and slope). These differences were driven by a relative predominance of Actinobacteria and a Colpodella sp. in non-crust habitats, and by phototrophic bacteria and eukaryotes (e.g., a moss) and predators (e.g., tardigrades) in habitats with biological soil crusts (gully and moraine). The gully and moraine also had significantly higher 16S and 18S ESV richness than the other two habitat types. We further found that many of the phototrophic bacteria and eukaryotes of the gully and moraine share high sequence identity with phototrophs from moist and wet areas elsewhere in the Dry Valleys and other cold desert ecosystems. These include a Moss (Bryum sp.), several algae (e.g., a Chlorococcum sp.) and cyanobacteria (e.g., Nostoc and Phormidium spp.). Overall, the results reported here broaden the diversity of habitat types that have been studied in the Dry Valleys of Antarctica and suggest future avenues of research to more definitively understand the biogeography and factors controlling microbial diversity in this unique ecosystem

Microbial Species–Area Relationships in Antarctic Cryoconite Holes Depend on Productivity

The island species&ndash;area relationship (ISAR) is a positive association between the number of species and the area of an isolated, island-like habitat. ISARs are ubiquitous across domains of life, yet the processes generating ISARs remain poorly understood, particularly for microbes. Larger and more productive islands are hypothesized to have more species because they support larger populations of each species and thus reduce the probability of stochastic extinctions in small population sizes. Here, we disentangled the effects of &ldquo;island&rdquo; size and productivity on the ISAR of Antarctic cryoconite holes. We compared the species richness of bacteria and microbial eukaryotes on two glaciers that differ in their productivity across varying hole sizes. We found that cryoconite holes on the more productive Canada Glacier gained more species with increasing hole area than holes on the less productive Taylor Glacier. Within each glacier, neither productivity nor community evenness explained additional variation in the ISAR. Our results are, therefore, consistent with productivity shaping microbial ISARs at broad scales. More comparisons of microbial ISARs across environments with limited confounding factors, such as cryoconite holes, and experimental manipulations within these systems will further contribute to our understanding of the processes shaping microbial biogeography.</p

Characterization of a Deglaciated Sediment Chronosequence in the High Arctic Using Near‐Surface Geoelectrical Monitoring Methods

Accelerated climate warming is causing significant reductions in the volume of Arctic glaciers, such that previously ice-capped bare ground is uncovered, harboring soil development. Monitoring the thermal and hydrologic characteristics of soils, which strongly affect microbial activity, is important to understand the evolution of emerging terrestrial landscapes. We instrumented two sites on the forefield of a retreating Svalbard glacier, representing sediment ages of approximately 5 and 60 years since exposure. Our instrumentation included an ERT array complemented by adjacent point sensor measurements of subsurface temperature and water content. Sediments were sampled at each location and at two more additional sites (120 and 2000 years old) along a chronosequence aligned with the direction of glacial retreat. Analysis suggests older sediments have a lower bulk density and contain fewer large minerals, which we interpret to be indicative of sediment reworking over time. Two months of monitoring data recorded during summer 2021 indicate that the 60-year-old sediments are stratified showing more spatially consistent changes in electrical resistivity, whereas the younger sediments show a more irregular structure, with consequences on heat and moisture conductibility. Furthermore, our sensors reveal that young sediments have a higher moisture content, but a lower moisture content variability

Comparison of Microbial Communities in the Sediments and Water Columns of Frozen Cryoconite Holes in the McMurdo Dry Valleys, Antarctica

Although cryoconite holes, sediment-filled melt holes on glacier surfaces, appear small and homogenous, their microbial inhabitants may be spatially partitioned. This partitioning could be particularly important for maintaining biodiversity in holes that remain isolated for many years, such as in Antarctica. We hypothesized that cryoconite holes with greater species richness and biomass should exhibit greater partitioning between the sediments and water, promoting greater biodiversity through spatial niche partitioning. We tested this hypothesis by sampling frozen cryoconite holes along a gradient of biomass and biodiversity in the Taylor Valley, Antarctica, where ice-lidded cryoconite holes are a ubiquitous feature of glaciers. We extracted DNA and chlorophyll a from the sediments and water of these samples to describe biodiversity and quantify proxies for biomass. Contrary to our expectation, we found that cryoconite holes with greater richness and biomass showed less partitioning of phylotypes by the sediments versus the water, perhaps indicating that the probability of sediment microbes being mixed into the water is higher from richer sediments. Another explanation may be that organisms from the water were compressed by freezing down to the sediment layer, leaving primarily relic DNA of dead cells to be detected higher in the frozen water. Further evidence of this explanation is that the dominant sequences unique to water closely matched organisms that do not live in cryoconite holes or the Dry Valleys (e.g., vertebrates); so this cryptic biodiversity could represent unknown microbial animals or DNA from atmospheric deposition of dead biomass in the otherwise low-biomass water. Although we cannot rule out spatial niche partitioning occurring at finer scales or in melted cryoconite holes, we found no evidence of partitioning between the sediments and water in frozen holes. Future work should include more sampling of cryoconite holes at a finer spatial scale, and characterizing the communities of the sediments and water when cryoconite holes are melted and active

Cryoconite – from minerals and organic matter to bioengineeredsediments on glacier's surfaces

Cryoconite is a mixture of mineral and organic material covering glacial ice, playing important roles in biogeochemical cycles and lowering the albedo of a glacier surface. Understanding the differences in structure of cryoconite across the globe can be important in recognizing past and future changes in supraglacial environments and ice-organisms-minerals interactions. Despite the worldwide distribution and over a century of studies, the basic characteristics of cryoconite, including its forms and geochemistry, remain poorly studied. The major purpose of our study is the presentation and description of morphological diversity, chemical and photoautotrophs composition, and organic matter content of cryoconite sampled from 33 polar and mountain glaciers around the globe. Observations revealed that cryoconite is represented by various morphologies including loose and granular forms. Granular cryoconite includes smooth, rounded, or irregularly shaped forms; with some having their surfaces covered by cyanobacteria filaments. The occurrence of granules increased with the organic matter content in cryoconite.Moreover, amajor driver of cryoconite colouringwas the concentration of organicmatter and its interplay with minerals. The structure of cyanobacteria and algae communities in cryoconite differs between glaciers, but representatives of cyanobacteria families Pseudanabaenaceae and Phormidiaceae, and algae families Mesotaeniaceae and Ulotrichaceaewere themost common. Themost of detected cyanobacterial taxa are known to produce polymeric substances (EPS) that may cement granules. Organic matter content in cryoconite varied between glaciers, ranging from 1% to 38%. The geochemistry of all the investigated samples reflected local sediment sources, except of highly concentrated Pb andHg in cryoconite collected fromEuropean glaciers near industrialized regions, corroborating cryoconite as element-specific collector and potential environmental indicator of anthropogenic activity. Our work supports a notion that cryoconite may bemore than just simple sediment and instead exhibits complex structure with relevance for biodiversity and the functioning of glacial ecosystem

Interacting Effects of Predation and Competition in the Field and in Theory

The principle of competitive exclusion holds that the strongest competitor for a single resource can exclude other species. Yet in many systems, more similar species appear to stably coexist than the small number of limiting resources. Understanding how and when similar species can stably coexist has taken on new urgency in managing biological invasions and their ecological impacts. Recent theoretical advances emphasize the importance of predators in determining coexistence. The effects of predators, however, can be mediated by behavioral changes induced in their prey as well as by their lethality. In this dissertation, I ask how considering multiple trophic levels changes our understanding of how a grass invasion (Pennisetum ciliare) affects species diversity and dynamics in southeastern Arizona. In considering interactions with plant consumers, and with the predators of those consumers, this research reveals more general ecological processes that determine species diversity across biological communities. I first present evidence from a grass removal experiment in the field that shows increased emergence and short-term survival of native perennial plants without grass. This is consistent with Pennisetum ciliare causing the observed concurrent decline in native plant abundance following invasion. I then present results from greenhouse and field studies consistent with that suppression of native plants being driven primarily through resource competition rather than increased rodent granivory. Granivorous rodents do not solely function as consumers, however, because they cache their harvested seeds in shallow scatter-hoards, from which seeds can germinate. Rodents thus act also as seed dispersers in a context-dependent mutualism. The primary granivores in areas invaded by Pennisetum ciliare are pocket mice (genus Chaetodipus), which have a well-studied tendency to concentrate their activity under plant cover to avoid predation by owls. Because the dense canopy of the grass may provide safer refuge, I hypothesized the pocket mice may be directly dispersing native seeds closer to the base of the invasive grass. Such a behavior could increase the competitive effect of the grass on native plant species, further driving the impacts of the invasion. By offering experimental seeds dusted in fluorescent powder and tracking where the seeds were cached, I show that rodents do preferentially cache experimental seeds under the grass. This dispersal interaction may be more general to plant interactions with seed-caching rodents across semi-arid regions that are experiencing plant invasions. Finally, I ask how the predator avoidance behavior exhibited by these rodents affects their ability to coexist with one another. Not only could their diversity affect that of the plant community, but the effects of plant invasions can cascade through other trophic levels. Theoretical understanding of how similar predator avoidance strategy alters coexistence had not yet been developed, however. Instead of a field study, therefore, I modified a general consumer-resource model with three trophic levels to ask whether avoidance behavior by the middle trophic level alters the ability of those species to coexist. I found that more effective avoidance behavior, or greater safety for less cost, increased the importance of resource partitioning in determining overall niche overlap. Lowering niche overlap between two species promotes their coexistence in the sense that their average fitness can be more different and still permit coexistence. These results provide novel understanding of behavioral modifications to population dynamics in multi-trophic coexistence theory applicable to this invasion and more broadly

Stage of invasion: How do sensitive seedlings respond to buffelgrass?

Awarded second place in Biological Sciences for GPSC Student ShowcaseThis item is part of the GPSC Student Showcase collection. For more information about the Student Showcase, please email the GPSC (Graduate and Professional Student Council) at [email protected]