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A Unique Resource Mutualism Between the Giant Bornean Pitcher Plant, Nepenthes Rajah, and Members of a Small Mammal Community

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A Unique Resource Mutualism Between the Giant Bornean Pitcher Plant, Nepenthes Rajah, and Members of a Small Mammal Community A Unique Resource Mutualism between the Giant Bornean Pitcher Plant, Nepenthes rajah, and Members of a Small Mammal Community Melinda Greenwood1, Charles Clarke2, Ch’ien C. Lee3, Ansou Gunsalam4, Rohan H. Clarke1* 1 School of Biological Sciences, Monash University, Clayton, Victoria, Australia, 2 School of Science, Monash University, Bandar Sunway, Selangor, Malaysia, 3 Kuching, Sarawak, Malaysia, 4 Sabah Parks, Kota Kinabalu, Sabah, Malaysia Abstract The carnivorous pitcher plant genus Nepenthes grows in nutrient-deficient substrates and produce jug-shaped leaf organs (pitchers) that trap arthropods as a source of N and P. A number of Bornean Nepenthes demonstrate novel nutrient acquisition strategies. Notably, three giant montane species are engaged in a mutualistic association with the mountain treeshrew, Tupaia montana, in which the treeshrew defecates into the pitchers while visiting them to feed on nectar secretions on the pitchers’ lids. Although the basis of this resource mutualism has been elucidated, many aspects are yet to be investigated. We sought to provide insights into the value of the mutualism to each participant. During initial observations we discovered that the summit rat, R. baluensis, also feeds on sugary exudates of N. rajah pitchers and defecates into them, and that this behavior appears to be habitual. The scope of the study was therefore expanded to assess to what degree N. rajah interacts with the small mammal community. We found that both T. montana and R. baluensis are engaged in a mutualistic interaction with N. rajah. T .montana visit pitchers more frequently than R. baluensis, but daily scat deposition rates within pitchers do not differ, suggesting that the mutualistic relationships are of a similar strength. This study is the first to demonstrate that a mutualism exists between a carnivorous plant species and multiple members of a small mammal community. Further, the newly discovered mutualism between R. baluensis and N. rajah represents only the second ever example of a multidirectional resource-based mutualism between a mammal and a carnivorous plant. Citation: Greenwood M, Clarke C, Lee CC, Gunsalam A, Clarke RH (2011) A Unique Resource Mutualism between the Giant Bornean Pitcher Plant, Nepenthes rajah, and Members of a Small Mammal Community. PLoS ONE 6(6): e21114. doi:10.1371/journal.pone.0021114 Editor: Sharon Gursky-Doyen, Texas A&M University, United States of America Received March 15, 2011; Accepted May 19, 2011; Published June 14, 2011 Copyright: ß 2011 Greenwood et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The research was funded by an internal research grant from Monash University Sunway Campus. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction in detail. No observation of pitcher visitors or nectar production by pitchers has been attempted at night. We do not know whether The carnivorous pitcher plant genus Nepenthes (Nepenthaceae) individual treeshrews defend valuable pitchers against other consists of ,120 species that are predominantly found in the animals, or whether such resources are shared. There is almost Southeast Asian tropics [1], [2]. Most species grow in nutrient- no quantitative data relating to the frequency, duration and deficient substrates and produce jug-shaped leaf organs that trap interval between visits by T. montana, or the rate of scat deposition arthropods as a supplementary source of N and P which are otherwise into Nepenthes pitchers. scarce in their habitats [3]. Diversity in Nepenthes –intermsofboth In this study, we conducted a series of experiments and species numbers and trap form – is greatest in Borneo, where some of observations designed to provide further insights into the interaction the largest and most unusual species occur [4]. between T. montana and N. rajah on Mount Kinabalu, Sabah, Recently, it has been shown that several Bornean Nepenthes Malaysian Borneo. Our objective was to determine the time of day, species demonstrate specialized nutrient acquisition strategies, frequency, duration, and interval between pitcher visits by T. montana, which differ markedly from the ‘typical’, arthropod-trapping along with rates of scat deposition and preliminary measures of strategy [5], [6]. Clarke et al. [7] and Chin et al. [8] established that diurnal and nocturnal nectar sugar content, to provide the necessary three giant montane pitcher plant species from Borneo, Nepenthes foundations for future experiments designed to quantify the value of lowii Hook.f., N. rajah Hook.f. and N. macrophylla (Marabini) Jebb & the mutualism to each participant. However, during our preliminary Cheek, are engaged in an extraordinary mutualistic association observations, we detected a second mammalian visitor to N. rajah with mountain treeshrews (Tupaia montana Thomas (Scandentia)), pitchers, the summit rat (Rattus baluensis Thomas (Rodentia)). We in which the treeshrews defecate into the Nepenthes’ pitchers while discovered that like T. montana, R. baluensis feeds on the lid gland visiting them to feed on carbohydrate rich secretions produced by exudates of N. rajah pitchers and defecates into them, and that this glands on the pitchers’ lids. behavior appears to be habitual. This raised the possibility that N. Although the basis of this mutualism has been elucidated, many rajah interacts with a community of small mammal species, so we aspects have yet to be investigated [6]. For instance, the behavioral expanded the scope of our study, comparing the visiting behavior of ecology of T. montana with respect to Nepenthes has not been studied T. montana with that of R. baluensis at N. rajah pitchers. PLoS ONE | www.plosone.org 1 June 2011 | Volume 6 | Issue 6 | e21114 A Pitcher Plant/Small Mammal Resource Mutualism Specifically, we investigated what time of day (or night) T. montana Visits by vertebrates to N. rajah pitchers were filmed using digital and R. baluensis visited N. rajah pitchers and whether there was any video cameras and a still camera trap. Several digital video evidence for competition or avoidance between mammalian visitors. cameras were used: Sony HDR-XR550 with Infrared light (HVL- The visitation rate, duration of visits and interval between visits was HIRL), Sony HDR-CX150, Sony DCR-SX44, Sony Corporation, also investigated to explore similarities and differences between the Tokyo, Japan and Panasonic SDR-S7, Panasonic Corporation, two species. Finally, this study sought to document the scat deposition Osaka, Japan) mounted on tripods. rates within pitchers to explore the strength of the mutualistic Filming methods described elsewhere [7], [8] were replicated relationship between each mammal species and N. rajah. with increased effort during daylight hours. Unlike previous work, We found that both T. montana and R. baluensis are engaged in a filming also included nocturnal sampling periods. Total filming mutualistic interaction with N. rajah, that T. montana visits pitchers effort was 515.1 hours between sunrise and sunset, and 44.6 hours more frequently than R. baluensis, but that daily scat deposition between sunset and sunrise. Sunrise occurred between 6:01– rates within pitchers do not differ between the two species. This 6:09am, and sunset between 5:54–6:33pm (Malaysia Time) during study is the first to demonstrate that a mutualism exists between a the filming period [9]. Sixty-nine individual pitchers were filmed single species of carnivorous plant and multiple species of small over the course of the study. facultative mammalian nectarivores. Between 4 and 6 August, 2010 camera trapping was conducted during the hours of darkness at two pitchers such that a total of Materials and Methods 48 hours of nocturnal monitoring was achieved. Each camera was positioned on a tripod approximately 1.5 m from the pitcher Ethics statement (Nikon D90 D-SLR, Nikon Corporation, Tokyo, Japan), with the As this was an observational study of free ranging wild animals, camera trap beam set to maximum sensitivity and crossing the with no direct interaction between the observers and animals, pitcher mouth just above the peristome (Phototrap photographic ethics clearance was not required. The work was conducted in trigger system model 33, Phototrap, Amado, Arizona), Nikon SB- Sabah, Malaysia in accordance with an Economic Planning Unit 900 off-camera flash). Permit (0/200/19/2545) and a Sabah Parks Research Permit (TS/PTD/5/4 Jld/ 39 (37)) held by the authors. We thank Dr Measurement of scat inputs to pitchers Maklarin Lakim, Rimi Repin and Sabah Parks for assistance and Scat input to pitchers was monitored by mounting a thin plastic permission to conduct the research. barrier (hereafter referred to as a ‘cup’) across the orifice of the pitcher. The barrier was positioned below the level of the peristome Study site (a collar-like ridge of hardened tissue that lines the pitcher orifice All research was conducted at the ‘Mesilau Landslip’ on Mount [4]) a few millimeters above the surface of the fluid within the Kinabalu, Sabah, Malaysia (6.048uN, 116.599uE, 2050 m asl). pitcher and was held in place with small magnets. Scats deposited The study site is approximately 70650 m in size and is located on into the pitcher were trapped in the cups, and were counted and an east-facing slope on the land slip, over an ultramafic substrate, removed daily for 38 days between the 26 September and the 17 with patchy and stunted vegetation, surrounded by lower montane November, 2010. Initially, the origin of the scats was determined forest. The sparse over-story is coniferous and N. rajah plants grow using video recordings, but as we found that the scats of T. montana among sedges, ferns and small shrubs. and R. baluensis differed consistently in size, colour, consistency and odour subsequent determinations were made visually (n = 20).
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