FIG 6 - uploaded by Liane Cochran-Stafira
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Interaction web for the Sarracenia purpurea inquilines used in the laboratory microcosms. Solid arrows are direct interactions. Dashed arrows represent indirect effects and are drawn with the arrow head indicating the target organism(s); the tail of the arrow indicates the species that is responsible for producing the indirect effect. Horizontal arrows designate competitive interactions; upward-pointing vertical or diagonal arrows designate predation or indirect effects mediated by predation. Heavy lines represent strong interactions; thin lines represent less intense interactions. Individual bacterial taxa are not represented here since they may vary among pitchers.
Source publication
Using organisms isolated from natural pitchers, we constructed food webs comprising 1–4 consumer species (all possible combinations of the presence and absence of Colpoda, Cyclidium, Bodo, and Wyeomyia larvae) along with a constant bacterial species pool in a factorial design experiment. Bacterial community structure was modified by the direct effe...
Context in source publication
Context 1
... at Cedarburg Bog. Experimental manip- ulation of this relatively simple food web allowed us to dissect the interactions among its four consumer taxa, and analyze their effects on the bacterial assem- blage. As a result, we can now begin to describe the pitcher food web, including the bacterial component, in terms of a complex interaction web (Fig. 6) that involves direct predatory and competitive interactions, interaction chains, and interaction modifications, the effects of which permeate throughout the community. ...
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Citations
... Because intermittent pools are bordered by distinct aquatic-terrestrial habitat boundaries in both space (at their aquatic margins) and time (during pool drying and filling), and because they are excellent experimental systems [1], they are often used as model systems for ecological studies. Insights gained from research on intermittent pools have enhanced our understanding of predation [2][3][4][5], competition [6,7], trophic functionality [8][9][10], metapopulation dynamics [11][12][13], trophic cascades [14,15] and food web dynamics [16][17][18][19][20]. However, the perspective that intermittent pools are temporally and spatially isolated temporary aquatic habitats constrains the range of ecological questions that can be addressed by studying them. ...
Recognition that intermittent pools are a single habitat phase of an intermittent pool bed that cycles between aquatic and terrestrial habitat greatly enhances their usefulness for addressing general questions in ecology. The aquatic phase has served as a model system in many ecological studies, because it has distinct habitat boundaries in space and time and is an excellent experimental system, but the aquatic to terrestrial transition and terrestrial phase remain largely unstudied. We conducted a field experiment within six replicate natural intermittent pool beds to explore macroinvertebrate community dynamics during the transition from aquatic to terrestrial habitat and during the terrestrial phase. We monitored and compared macroinvertebrate communities within leaf packs that i) remained wet, ii) underwent drying (i.e., started wet and then dried), and iii) remained dry. Our results show that i) a diverse macroinvertebrate community inhabits all phases of intermittent pool beds, ii) pool drying involves colonization by an assemblage of macroinvertebrates not recorded in permanently terrestrial leaf packs, iii) the community within dried leaf packs remains distinct from that of permanently terrestrial leaf packs for an extended period following drying (possibly until subsequent refilling), and iv) there are likely to be strong spatial and temporal resource linkages between the aquatic and terrestrial communities. The unique environmental characteristics of intermittent pool beds, which repeatedly cycle from aquatic to terrestrial habitat, should continue to make them valuable study systems.
... Th is system has previously been used to examine the role of trophic cascades ( Kneitel and Miller 2002), omnivory (Kneitel 2007), commensalism (Heard 1994, top -down and bottom -up forces (Cochran-Stafi ra and von Ende 1998, Kneitel and Miller 2002, Gray et al. 2006), competition and evolution (terHorst et al. 2010), food web diversity ( Baiser et al. 2011), and invasion success ( Miller et al. 2002) on community dynamics and structure. Th is background knowledge of community composition, species interactions and community dynamics allow us to investigate mecha- nisms driving establishment success of species with diff erent characteristics in diff erent environments. ...
Understanding whether factors important for species establishment in a local community are predictable or context- dependent is key for determining the features that affect community stability and species coexistence. A major challenge for scientists addressing this question is that natural systems are complex. This makes it difficult to test multiple properties of species and features of the resident community simultaneously to determine what factors are most important for establishment success of a species into a novel community. We used the model aquatic system inside the leaves of the pitcher plant Sarracenia purpurea to test whether properties predicted to be important for establishment success of a species (initial density, competitive ability, body size) are generalizable across communities varying in resource availability and the presence of a top predator. For intermediate trophic-level species, we found that both competitive dominance and initial density were important for establishment success. Although a less competitive species was also able to successfully establish in the communities, high resource availability and high initial density were important for its establishment success. Body size of the introduced species, although correlated with competitive ability, was not an important characteristic for establishment success. The presence of a top predator significantly decreased the densities of the introduced species when resources were low, but did not completely inhibit establishment success. The relative importance of each of these factors, and interactions among them, could not have been discerned through single hypothesis testing. The results from this work show the need for detailed experiments that focus on combinations of factors to understand if mechanisms determining community assembly and species establishment can be generalized across systems.
... Sarracenia purpurea food web Most macroarthropods that enter the leaves drown and are devoured by the plant or specialized, obligate organisms that live in the leaves called inquilines. Inquilines include the larvae of three dipteran species -the midge, Metriocnemus knabi Coquillet, the mosquito, Wyeomyia smithii (Coquillet), and the fl esh fl y, Fletcherimyia ( Blaesoxipha ) fl etcheri Aldrich; the mite Sarraceniopus gibsoni (Nesbitt); the bdelloid rotifer, Habotrocha rosa Donner, as well as various species of bacteria, rotifers and other protozoa, algae, and mites (Fish and Hall, 1978 ;Rymal and Folkerts, 1982 ;Fashing and O'Connor, 1984 ;Heard, 1994 ;Harvey and Miller, 1996 ;Heard, 1997 ;Cochran-Stafi ra and von Ende, 1998 ;Buckley et al., 2003Buckley et al., , 2004Miller and Kneitel, 2005 ) ( Figures 2 and 3 ). Th e omnivorous mosquito is considered the keystone predator. ...
... Th e mite, protists -protozoa and rotifers are considered bacterivores and prey upon the algae, fungi and bacteria occupying the basal trophic positions. Bacteria and algal species feed on the remaining detritus from the drowned arthropods (Fish and Hall, 1978 ;Rymal and Folkerts, 1982 ;Cochran-Stafi ra and von Ende, 1998 ). Species abundance and diversity in the pitcher plant food web is controlled by some combination of predation (top-down), nutrient (prey) availability (bottom-up), and environmental factors (Cochran-Stafi ra and von Ende, 1998 ;Kneitel and Miller, 2003 ;Trzcinski et al., 2005 ;Gotelli and Ellison, 2006 ;Gray et al., 2006 ;Hoekman, 2007 ;Peterson et al., 2008 ;Hoekman et al., 2009) ...
... Bacteria and algal species feed on the remaining detritus from the drowned arthropods (Fish and Hall, 1978 ;Rymal and Folkerts, 1982 ;Cochran-Stafi ra and von Ende, 1998 ). Species abundance and diversity in the pitcher plant food web is controlled by some combination of predation (top-down), nutrient (prey) availability (bottom-up), and environmental factors (Cochran-Stafi ra and von Ende, 1998 ;Kneitel and Miller, 2003 ;Trzcinski et al., 2005 ;Gotelli and Ellison, 2006 ;Gray et al., 2006 ;Hoekman, 2007 ;Peterson et al., 2008 ;Hoekman et al., 2009) ...
A seasonal survey of the abundances of three inquilines species in Sarracenia purpurea L. leaves was con-ducted by sampling 240 leaves from three pitcher plant populations on Beaver Island in Lake Michigan, United States. Leaf characteristics such as fl uid pH, fl uid volume, and keel length were quantifi ed. Th e study focused primarily on the larvae of three dipteran inquiline species – the midge, Metriocnemus knabi Coquillet, the mosquito, Wyeomyia smithii (Coquillet), and the fl esh fl y, Fletcherimyia fl etcheri Aldrich. Dipteran inquiline abundances varied with sampling season. Most pitchers contained one of the three studied inquilines species. Mosquito abundances were low relative to the other inquilines. In samples col-lected soon after new leaves open, a mixture of mosquito and midge larvae was characteristic. We related inquilines abundances to leaf parameters using generalized linear mixed models. Th e midge and mosquito responded diff erently to leaf parameters during diff erent sampling seasons, where as the fl esh fl y showed no response. Th e most important leaf parameters were pH and percent of total leaf volume fi lled with fl uid (relative volume). Th e midge and mosquito were more likely to be present in pitchers with low pH and higher fl uid volume. Our results indicate that pitchers of isolated northern populations of S. purpurea are inhabited by a less diverse insect community than reported elsewhere. Our study also suggests that site isolation may play an important role in the seasonal variation of inquiline community structure. © Koninklijke Brill NV, Leiden, 2011
Understanding microbial roles in ecosystem function requires integrating microscopic processes into food webs. The carnivorous pitcher plant, Sarracenia purpurea, offers a tractable study system where diverse food webs of macroinvertebrates and microbes facilitate digestion of captured insect prey, releasing nutrients supporting the food web and host plant. However, how interactions between these macroinvertebrate and microbial communities contribute to ecosystem functions remains unclear. We examined the role of the pitcher plant mosquito, Wyeomyia smithii, in top-down control of the composition and function of pitcher plant microbial communities. Mosquito larval abundance was enriched or depleted across a natural population of S. purpurea pitchers over a 74-day field experiment. Bacterial community composition and microbial community function were characterized by 16S rRNA amplicon sequencing and profiling of carbon substrate use, bulk metabolic rate, hydrolytic enzyme activity, and macronutrient pools. Bacterial communities changed from pitcher opening to maturation, but larvae exerted minor effects on high-level taxonomic composition. Higher larval abundance was associated with lower diversity communities with distinct functions and elevated nitrogen availability. Treatment-independent clustering also supported roles for larvae in curating pitcher microbial communities through shifts in community diversity and function. These results demonstrate top-down control of microbial functions in an aquatic microecosystem.
The spatial distribution of predators can affect both the distribution and diversity of their prey. Therefore, differences in predator dispersal ability that affect their spatial distribution, could also affect prey communities. Here, we use the microbial communities within pitcher plant leaves as a model system to test the relationship between predator (protozoa) dispersal ability and distribution, and its consequences for prey (bacteria) diversity and composition. We hypothesized that limited predator dispersal results in clustered distributions and heterogeneous patches for prey species, whereas wide predator dispersal and distribution could homogenize prey metacommunities. We analyzed the distribution of two prominent bacterivore protozoans from a 2‐year survey of an intact field of Sarracenia purpurea pitcher plants, and found a clustered distribution of Tetrahymena and homogeneous distribution of Poterioochromonas. We manipulated the sources of protozoan colonists and recorded protozoan recruitment and bacterial diversity in target leaves in a field experiment. We found the large ciliate, Tetrahymena, was dispersal limited and occupied few leaves, whereas the small flagellate Poterioochromonas was widely dispersed. However, the bacterial communities these protozoans feed on was unaffected by clustering of Tetrahymena, but likely influenced by Poterioochromonas and other bacterivores dispersing in the field. We propose that bacterial communities in this system are structured by a combination of well dispersed bacterivores, bacterial dispersal, and bottom‐up mechanisms. Clustered predators could become strong drivers of prey communities if they were specialists or keystone predators, or if they exerted a dominant influence on other predators in top‐down controlled systems. Linking dispersal ability within trophic levels and its consequences for trophic dynamics can lead to a more robust perspective on trophic metacommunities.
The use of ever‐advancing sequencing technologies has revealed incredible biodiversity at the microbial scale, and yet we know little about the ecological interactions in these communities. For example, in the phytotelmic community found in the purple pitcher plant, Sarracenia purpurea, ecologists typically consider the bacteria as a functionally homogenous group. In this food web, bacteria decompose detritus and are consumed by protozoa that are considered generalist consumers. Here, we tested whether a generalist consumer benefits from all bacteria equally. We isolated and identified 22 strains of bacteria, belonging to six genera, from S. purpurea plants. We grew the protozoa, Tetrahymena sp. with single isolates and strain mixtures of bacteria and measured Tetrahymena fitness. We found that different bacterial strains had different effects on protozoan fitness, both in isolation and in mixture. Our results demonstrate that not accounting for the composition of prey communities may affect the predicted outcome of predator–prey interactions. Sarracenia purpurea, the purple pitcher plant, is used as model system for studying ecology and evolution in a constrained natural community. The bacteria that serve as the base of this brown food web are often treated as a functionally similar as the food source for protozoa. Through our experiment, we demonstrate that bacterial strain identity matters for protozoan fitness and that this should be a consideration in future studies looking at bottom‐up effects in this system.
Background
The leaves of carnivorous pitcher plants harbor diverse communities of inquiline species, including bacteria and larvae of the pitcher plant mosquito (Wyeomyia smithii), which aid the plant by processing captured prey. Despite the growing appreciation for this microecosystem as a tractable model in which to study food web dynamics and the moniker of W. smithii as a ‘keystone predator’, very little is known about microbiota acquisition and assembly in W. smithii mosquitoes or the impacts of W. smithii-microbiota interactions on mosquito and/or plant fitness.
Results
In this study, we used high throughput sequencing of bacterial 16S rRNA gene amplicons to characterize and compare microbiota diversity in field- and laboratory-derived W. smithii larvae. We then conducted controlled experiments in the laboratory to better understand the factors shaping microbiota acquisition and persistence across the W. smithii life cycle. Methods were also developed to produce axenic (microbiota-free) W. smithii larvae that can be selectively recolonized with one or more known bacterial species in order to study microbiota function. Our results support a dominant role for the pitcher environment in shaping microbiota diversity in W. smithii larvae, while also indicating that pitcher-associated microbiota can persist in and be dispersed by adult W. smithii mosquitoes. We also demonstrate the successful generation of axenic W. smithii larvae and report variable fitness outcomes in gnotobiotic larvae monocolonized by individual bacterial isolates derived from naturally occurring pitchers in the field.
Conclusions
This study provides the first information on microbiota acquisition and assembly in W. smithii mosquitoes. This study also provides the first evidence for successful microbiota manipulation in this species. Altogether, our results highlight the value of such methods for studying host-microbiota interactions and lay the foundation for future studies to understand how W. smithii-microbiota interactions shape the structure and stability of this important model ecosystem.
https://www.frontiersin.org/articles/10.3389/fmicb.2022.791079/abstract
Suberin, as a lipid polyester barrier, limits the movement of gas, water and solutes, and plays important roles in plant protection and growth. In this study, a CDS encoding glycerol-3-phosphate acyltransferase 5 (GPAT5) was cloned from Sarracenia purpurea to investigate the gene function. SpGPAT5 shares 72% identity and 80% similarity to AtGPAT5 that is required for suberin synthesis. Fluorol Yellow 088 staining showed that the S. purpurea pitcher (specific leaf) tube contained more suberin in the adaxial surface compared to the lid, and SpGPAT5 transcripts were detected in the pitcher. Previous reported Atgpat5-1 phenotypes were complemented with SpGPAT5 showing that the Atgpat5-1 seed coat had increased permeability of tetrazolium red and the mutant was sensitive to salt. We also found that SpGPAT5 was able to revert the hyperhydric phenotype of Atgpat5-1 under high humidity. Thus, this study suggests that SpGPAT5 can functionally replace AtGPAT5 and contributes to plant tolerance to high humidity, which maybe assist in understanding the role of suberin-associated waxes in S. purpurea pitchers for water retention.
The mosquito body hosts highly diverse microbes, which influence different physiological traits of both larvae and adults. The composition of adult mosquito microbiota is tightly linked to that of larvae, which are aquatic and feed on organic detritus, algae and prokaryotic microorganisms present in their breeding sites. Unraveling the ecological features of larval habitats that shape the structure of bacterial communities and their interactions with the mosquito host is still a poorly investigated topic in the Asian tiger mosquito Aedes albopictus, a highly invasive species that is vector of numerous arboviruses, including Dengue, Chikungunya, and Zika viruses. In this study, we investigated the composition of the bacterial community present in the water from a natural larval breeding site in which we separately reared wild-collected larvae and hatched eggs of the Foshan reference laboratory strain. Using sequence analysis of bacterial 16S rRNA gene amplicons, we comparatively analyzed the microbiota of the larvae and that of adult mosquitoes, deriving information about the relative impact of the breeding site water on shaping mosquito microbiota. We observed a higher bacterial diversity in breeding site water than in larvae or adults, irrespective of the origin of the sample. Moreover, larvae displayed a significantly different and most diversified microbial community than newly emerged adults, which appeared to be dominated by Proteobacteria. The microbiota of breeding site water significantly increased its diversity over time, suggesting the presence of a dynamic interaction among bacterial communities, breeding sites and mosquito hosts. The analysis of Wolbachia prevalence in adults from Foshan and five additional strains with different geographic origins confirmed the described pattern of dual wAlbA and wAlbB strain infection. However, differences in Wolbachia prevalence were detected, with one strain from La Reunion Island showing up to 18% uninfected individuals. These findings contribute in further understanding the dynamic interactions between the ecology of larval habitats and the structure of host microbiota, as well as providing additional information relative to the patterns of Wolbachia infection.
