Investigation of an Elevational Gradient Reveals Strong Differences Between Bacterial and Eukaryotic Communities Coinhabiting Nepenthes Phytotelmata

Abstract

Elevation is an important determinant of ecological community composition. It integrates several abiotic features and leads to strong, repeatable patterns of community structure, including changes in the abundance and richness of numerous taxa. However, the influence of elevational gradients on microbes is understudied relative to plants and animals. To compare the influence of elevation on multiple taxa simultaneously, we sampled phytotelm communities within a tropical pitcher plant (Nepenthes mindanaoensis) along a gradient from 400 to 1200 m a.s.l. We use a combination of metabarcoding and physical counts to assess diversity and richness of bacteria, micro-eukaryotes, and arthropods, and compare the effect of elevation on community structure to that of regulation by a number of plant factors. Patterns of community structure differed between bacteria and eukaryotes, despite their living together in the same aquatic microhabitats. Elevation influences community composition of eukaryotes to a significantly greater degree than it does bacteria. When examining pitcher characteristics, pitcher dimorphism has an effect on eukaryotes but not bacteria, while variation in pH levels strongly influences both taxa. Consistent with previous ecological studies, arthropod abundance in phytotelmata decreases with elevation, but some patterns of abundance differ between living inquilines and prey.

Arthropods discovered in lower and upper pitchers of Nepenthes at Rampa-Sitahuis Hill, North Sumatra, Indonesia

“…The extreme condition of the Nepenthes pitchers' fluid renders organisms incapable of survival. This finding corroborates Hidayat (2016) assertion that numerous bacterial species reside in this fluid and participate in the substrate degrading process (Biteau et al 2013;Chou et al 2014;Gilbert et al 2020). The presence of bacteria with a high variety index benefits Nepenthes growth by providing additional nutrients.…”

“…The presence of bacteria with a high variety index benefits Nepenthes growth by providing additional nutrients. Additionally, the presence of bacteria is influenced by a variety of parameters, including the location and growing conditions of Nepenthes, nutrition availability, and the state of the pitchers' fluid (Chou et al 2014;Takeuchi et al 2015;Hidayat 2016;Gilbert et al 2020). The hue of Nepenthes pitchers' liquid is determined by the particles suspended in it, the remains of Arthropod carcasses, and the chemical enzymes involved in the pitchers' symbiotic interaction with these animals.…”

“…In addition to rotting arthropods, the Nepenthes pitchers' fluid contains various species of bacteria (Hidayat 2016). Arthropods and other predatory creatures trapped in Nepenthes pitchers accelerate decomposition and boost the plant's nutritional availability (Takeuchi et al 2015;Hidayat 2016;Gilbert et al 2020). Adlassnig et al (2011) assert that the Arthropod family trapped in Nepenthes pitchers affects the characteristics of the Nepenthes pitchers' bacteria.…”

Evidence of Elevational Speciation in Kerteszia cruzii (Diptera: Culicidae) in the Ribeira Valley, São Paulo, Brazil

“…Accordingly, even small variations, such as 200 m in elevation, can imply differences in the structure of Culicidae bromeliad communities. Similarly, bacterial and eukaryotic communities of phytotelma, on which the larval stages develop, also vary at low and high elevations (Gilbert et al, 2020;Malfatti et al, 2020). Additionally, Culicidae species distribution varies according to bromeliad species; for example, Culex (Microculex) spp.…”

Characterization and Comparison of Convergence Among Cephalotus follicularis Pitcher Plant-Associated Communities With Those of Nepenthes and Sarracenia Found Worldwide

“…Pitcher plants provide an opportunity to examine how hosts with similar morphology and life-history traits that have evolved independently in dramatically different geographic locations, can nevertheless attract and cultivate similar communities within their structures. Pitcher plant-associated communities from the genera Sarracenia (family Sarraceniaceae) and Nepenthes (family Nepenthaceae) have now been characterized across numerous studies ( Peterson et al, 2008 ; Koopman and Carstens, 2011 ; Gray, 2012 ; Gray et al, 2012 ; Kanokratana et al, 2016 ; Bittleston et al, 2018 ; Grothjan and Young, 2019 ; Gilbert et al, 2020a , b ). Many of the same bacterial and eukaryotic taxonomic groups are common in both Sarracenia and Nepenthes communities and their metagenomes show enrichment in specific degradation genes ( Bittleston et al, 2018 ), suggesting that convergent interactions ( Bittleston et al, 2016b ) may exist among these convergently evolved plants and the organisms living in their pitchers.…”