Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities

Annals of Botany 107: 181 –194, 2011 doi:10.1093/aob/mcq238, available online at www.aob.oxfordjournals.org REVIEW Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities Wolfram Adlassnig*, Marianne Peroutka and Thomas Lendl University of Vienna, Cell Imaging and Ultrastructure Research Unit, Althanstrasse 14, A-1090 Vienna, Austria * For correspondence. E-mail Received: 16 April 2010 Returned for revision: 28 June 2010 Accepted: 8 November 2010 Published electronically: 15 December 2010 Key words: Brocchinia, carnivorous plants, Cephalotus, Heliamphora, pitcher inquilines, mutualism, Nepenthes, phytotelm, Sarracenia, symbiosis. IN T RO DU C T IO N Carnivorous pitcher plants (CPPs) use cone-shaped leaves filled with fluid to trap and digest animals and to absorb their soluble ingredients. However, no species of pitcher plants kills all organisms entering the traps. At least some organisms, ranging from bacteria to vertebrates, are able to survive and propagate in the traps. For some inquilines, pitcher traps are the only habitat the species occupies. This study presents a synopsis of 130 years of research, focusing on (a) the pitcher fluid as the environment of inquilines, (b) the diversity of inquilines on the natural site and (c) the contribution of inquilines in prey degradation and the benefit for the plant. Carnivorous pitcher plants About 500 species of vascular plants trap and digest animals in order to gain additional inorganic nutrients (Juniper et al., 1989; Barthlott et al., 2004). The retention of animals is performed by different mechanisms such as sticky adhesive traps, moveable snap traps, pitchers, suction bladders or eel traps (Lloyd, 1942). The trapped animal usually dies within a short time from drowning or O2 deficiency (Adamec, 2007). The corpse is dissolved by digestive enzymes produced either by the plant itself (carnivorous plants sensu stricto) or by mutualistic organisms ( protocarnivorous plants) (Peroutka et al., 2008). The epidermis of the trap is equipped with glands or a porous cuticle where dissolved nutrients are absorbed. For a complete survey, compare Barthlott et al. (2004), Juniper et al. (1989) and Peroutka et al. (2008). The aim of prey capture is the acquisition of inorganic nutrients, especially N and P; the uptake of organic compounds is negligible in most species (Adamec, 1997; Schulze et al., 1997, 2001). Carnivorous plants are able to colonize habitats with highly oligotrophic soils but are restricted to very specific ecological niches; detailed descriptions of their ecology are given by Benzing (1987), Ellison (2006), Ellison and Gotelli (2001) and Givnish (1989). The net benefit of carnivory seems to be marginal (Karagatzides and Ellison, 2009). CPPs independently developed five times in geographically separated regions. However, the traps are remarkably similar in all species. The trapping process is driven by gravity: the prey falls into a hollow leaf and is unable to climb out. A typical pitcher trap consists of four zones (Fig. 1). (A) The uppermost part of the pitcher is an appendix carrying attraction glands # The Author 2010. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: † Background Carnivorous pitcher plants (CPPs) use cone-shaped leaves to trap animals for nutrient supply but are not able to kill all intruders of their traps. Numerous species, ranging from bacteria to vertrebrates, survive and propagate in the otherwise deadly traps. This paper reviews the literature on phytotelmata of CPPs. † Pitcher Fluid as a Habitat The volumes of pitchers range from 0.2 mL to 1.5 L. In Nepenthes and Cephalotus, the fluid is secreted by the trap; the other genera collect rain water. The fluid is usually acidic, rich in O2 and contains digestive enzymes. In some taxa, toxins or detergents are found, or the fluid is extremely viscous. In Heliamphora or Sarracenia, the fluid differs little from pure water. † Inquiline Diversity Pitcher inquilines comprise bacteria, protozoa, algae, fungi, rotifers, crustaceans, arachnids, insects and amphibia. The dominant groups are protists and Dipteran larvae. The various species of CPPs host different sets of inquilines. Sarracenia purpurea hosts up to 165 species of inquilines, followed by Nepenthes ampullaria with 59 species, compared with only three species from Brocchinia reducta. Reasons for these differences include size, the life span of the pitcher as well as its fluid. † Mutualistic Activities Inquilines closely interact with their host. Some live as parasites, but the vast majority are mutualists. Beneficial activities include secretion of enzymes, feeding on the plant’s prey and successive excretion of inorganic nutrients, mechanical break up of the prey, removal of excessive prey and assimilation of atmospheric N2. † Conclusions There is strong evidence that CPPs influence their phytotelm. Two strategies can be distinguished: (1) Nepenthes and Cephalotus produce acidic, toxic or digestive fluids and host a limited diversity of inquilines. (2) Genera without efficient enzymes such as Sarracenia or Heliamphora host diverse organisms and depend to a large extent on their symbionts for prey utilization. 182 Adlassnig et al. — Traps of carnivorous pitcher plants as a habitat covered by the pitcher fluid (E). The outside of the traps is usually rough and hairy and equipped with longitudinal ridges (F) in order to facilitate the access to the pitcher by animals. About 110 species of CPPs have been described from the plant families shown in Table 1. A B C The phytotelm concept E 2 cm F I G . 1. Longitudinal section through a typical carnivorous pitcher plant, Nepenthes × coccinea. (A) Pitcher hood with attractive glands, (B) smooth pitcher margin, (C) retention zone with loose wax crystals, (D) absorption zone with digestive glands, (E) digestive fluid, (F) hairy longitudinal ledge. Glands are drawn disproportionally large for better visibility. producing nectar and volatiles. The appendix may form a hood to protect the pitcher against precipitation (other functions are discussed by Bauer et al., 2008). (B) The pitcher margin ( peristome) may also be equipped with attractive glands. A wettable, slippery surface or inward-pointing hairs facilitate the stumbling of animals and let them fall into the pitcher. (C) The upper part of the pitcher serves for prey retention. The inner surface is covered with downward-pointing hairs or loose wax crystals that make climbing impossible. (D) The bottom of the pitcher is equipped with a permeable cuticle and absorbs dissolved nutrients. Glands for enzyme production are also located in this zone. The lower part of this zone is TA B L E 1. Diversity of pitcher plants Family Nepenthaceae Sarraceniaceae Cephalotaceae Bromeliaceae Eriocaulaceae Genus Nepenthes Sarracenia Species Heliamp (...truncated)