Ontogeny and Anatomy of the Dimorphic Pitchers of Nepenthes rafflesiana Jack

Abstract

An enigmatic feature of tropical pitcher plants belonging to the genus Nepenthes is their dimorphic prey-capturing pitfall traps. In many species, the conspicuously shaped upper and lower pitchers grow from a swollen leaf tendril tip until finally opening as insect-alluring devices. Few have studied the ontogeny of these traps from an anatomical and quantitative morphological perspective. We investigated whether the anatomy and development of lower and upper type pitchers of N. rafflesiana differ or overlap in terms of 3D geometric morphology and microstructure progression and presence. We hypothesized that there is an overlap in the initial, but not all, developmental stages of the two pitcher types and that one pitcher type is suspended in development. We identified four important morphological changes of pitcher ontogeny and defined these as curvation, elongation, inflation and maturation phases. Pitcher length indicated progress through developmental phases, and we propose to use it as a tool for indication of developmental stage. Microstructure development coincided with the developmental phases defined. Additionally, we discovered a new anatomical feature of extrafloral nectariferous peristomal glands between the inner peristome ridges of upper and lower pitchers being hollow and analyze the chemistry of the sugars on the outside of these glands. Ontogenetic shape analysis indicated that upper and lower pitcher types develop with similar phase progression but have no directly overlapping morphology. This means that upper pitchers are not a derived state from lower pitchers. Independent developmental programs evolved to produce distinctly shaped upper and lower pitchers in Nepenthes, likely to exploit different food sources.

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

“…Additionally, these arthropods are prone to falling into plants due to their slippery lips (Bonhomme et al 2011;Buch et al 2013). The lips of N. eustachya, N. ampullaria, N. gracilis, N. rafflesiana, and N. sumatrana pitchers are brighter than the rest of the body, the pitchers' edges are smooth and jagged, and the nectar is found at the gland's top (Buch et al 2015;Chou et al 2015;Bekalu et al 2020;Schwallier et al 2020). Nepenthes pitchers also have a distinct odor caused by extrafloral nectarine glands, which draws land arthropods to the lips of their pitchers (Gorb et al 2013;Schwallier et al 2020).…”

“…The lips of N. eustachya, N. ampullaria, N. gracilis, N. rafflesiana, and N. sumatrana pitchers are brighter than the rest of the body, the pitchers' edges are smooth and jagged, and the nectar is found at the gland's top (Buch et al 2015;Chou et al 2015;Bekalu et al 2020;Schwallier et al 2020). Nepenthes pitchers also have a distinct odor caused by extrafloral nectarine glands, which draws land arthropods to the lips of their pitchers (Gorb et al 2013;Schwallier et al 2020). Arthropods of the family Formicidae were discovered dead in pitchers of N. eustachya, N. ampullaria, N. gracilis, N. rafflesiana, and N. sumatrana, but their remains were found intact in bag fluid.…”

“…Diverse arthropod groups have been observed trapped in their pitchers on numerous occasions (Bauer et al 2015;Biswal et al 2018;Hidayat et al 2018;Rizqiani et al 2018;Setiawan et al 2018;Nainggolan et al 2020). Extrafloral nectarine glands on Nepenthes provide a scent that draws arthropods to the pitcher's lip (Bonhomme et al 2011;Gorb et al 2013;Schwallier et al 2020). In addition, the upper part of the plant contains digestive enzymes referred to as glandular parts that act as digesting sites for trapped prey (Rottloff et al 2016;Ravee et al 2018;Saganová et al 2018;Bekalu et al 2020;Dkhar et al 2020;Schwallier et al 2020).…”

“…Extrafloral nectarine glands on Nepenthes provide a scent that draws arthropods to the pitcher's lip (Bonhomme et al 2011;Gorb et al 2013;Schwallier et al 2020). In addition, the upper part of the plant contains digestive enzymes referred to as glandular parts that act as digesting sites for trapped prey (Rottloff et al 2016;Ravee et al 2018;Saganová et al 2018;Bekalu et al 2020;Dkhar et al 2020;Schwallier et al 2020).…”

How a sticky fluid facilitates prey retention in a carnivorous pitcher plant (Nepenthes rafflesiana)

“…The slippery zone can also contain directional microstructures that make it easier for insects to slip into and impede escape from the pitcher [10]. Finally, the walls of the digestive zone are covered in glands for secretion and absorption, but they are unlikely to serve a role in prey retention [11,12].…”