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. 2020 Mar 10;10(1):4431.
doi: 10.1038/s41598-020-61193-x.

Tropical pitcher plants (Nepenthes) act as ecological filters by altering properties of their fluid microenvironments

Kadeem J Gilbert  1 , Leonora S Bittleston  2   3   4 , Wenfei Tong  5 , Naomi E Pierce  2
Affiliations

Tropical pitcher plants (Nepenthes) act as ecological filters by altering properties of their fluid microenvironments

Kadeem J Gilbert et al. Sci Rep. .

Abstract

Characteristics of host species can alter how other, interacting species assemble into communities by acting as ecological filters. Pitchers of tropical pitcher plants (Nepenthes) host diverse communities of aquatic arthropods and microbes in nature. This plant genus exhibits considerable interspecific diversity in morphology and physiology; for example, different species can actively control the pH of their pitcher fluids and some species produce viscoelastic fluids. Our study investigated the extent to which Nepenthes species differentially regulate pitcher fluid traits under common garden conditions, and the effects that these trait differences had on their associated communities. Sixteen species of Nepenthes were reared together in the controlled environment of a glasshouse using commonly-sourced pH 6.5 water. We analyzed their bacterial and eukaryotic communities using metabarcoding techniques, and found that different plant species differentially altered fluid pH, viscosity, and color, and these had strong effects on the community structure of their microbiota. Nepenthes species can therefore act as ecological filters, cultivating distinctive microbial communities despite similar external conditions, and blurring the conceptual line between biotic and abiotic filters.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Illustration of fluid properties and community composition of experimental pitchers. (A) Beanplot representing pH levels of each species. The width of short white lines represents the number of samples at each value; long black lines represent means. Letters above indicate significant differences: species sharing a letter do not have significantly different means from one another. Small barplots represent portion of pitchers per species that exhibited colored fluid. Circles represent portion of pitchers per species that produced viscous fluid. Fly icons represent individual pitcher samples that contained more than 50 visible gnats. Illustrations of pitchers from each species by LSB; illustrations are not to scale and are for representative purposes only. Species are organized by mean pH. Species codes: DUB = Nepenthes dubia, JAC = N. jacquelineae, SAN = N. sanguinea, INE = N. inermis, RAM = N. ramispina, SIN = N. singalana, VEN = N. × “Bill Bailey”, HAM = N. hamata, MAX = N. maxima, TRU = N. truncata, KHA = N. khasiana, EYM = N. eymae, COP = N. copelandii, BOS = N. boschiana, TEN = N. tentaculata, FUS = N. fusca (B) Stacked barplot representing relative abundances of bacterial taxa. Note that “Rhodospirillaceae” here is Rhodosprillaceae sensu lato and also includes Reyranellaceae. (C) Stacked barplot representing relative abundances of eukaryotic taxa.
Figure 2
Figure 2
Non-metric multidimentional scaling (NMDS) plots representing community similarity (UniFrac distances) of bacteria (A,C) and eukaryotes (B,D) by host plant species identity (A,B) and by pH (C,D). Each point represents a sample and distance between points represents degree of similarity in community composition. Lines in A and B connect points belonging to the same species. Grey contour lines in C and D are smooth surfaces calculated based on variation in pH using the ‘ordisurf’ function in the ‘vegan’ package of R. Species codes: BOS = N. boschiana, COP = N. copelandii, EYM = N. eymae, FUS = N. fusca, INE = N. inermis, JAC = N. jacquelineae, KHA = N. khasiana, MAX = N. maxima, RAM = N. ramispina, SAN = N. sanguinea, SIN = N. singalana, TEN = N. tentaculata, TRU = N. truncata. pH levels: 1 = red, 2 = orange, 3 = yellow, 4 = green, 5 = blue, 6 = purple.
Figure 3
Figure 3
Results of analysis of composition of microbiomes (ANCOM) test, showing OTUs that are differentially abundant across pH levels. The points and dotted lines are smooth splines generated to summarize the individual trends in change of mean log relative abundance for each OTU across pH levels. Bars indicate standard deviation.
Figure 4
Figure 4
Results of analysis of composition of microbiomes (ANCOM) test, showing OTUs that are differentially abundant between the two categories of fluid color (clear and colored). The individual OTU taxonomic assignments are as follows: A-B: “Ascomycota: Pezizomycotina: Eurotiomycetes: Chaetothyriales: Capronia”, C: “Basidiomycota: Agaricomycotina: Tremellomycetes: Tremella”, D: “Basidiomycota: Agaricomycotina: Tremellomycetes: Syzygospora”, E: “Basidiomycota: Pucciniomycotina: Microbotryomycetes: Rhodosporidium”, F–W: “Arthropoda: Insecta: Diptera: Sciaridae: Bradysia”.
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