Novel pitcher plant–spider mutualism is dependent upon environmental resource abundance
Positive species interactions are ubiquitous and crucial components of communities, but they are still not well incorporated into established ecological theories. The definitions of facilitation and mutualism overlap, and both are often context dependent. Many interactions that are facilitative under stressful conditions become competitive under more benign ones. This is known as the stress-gradient hypothesis, which is a specific case of context dependency. Stress can be further divided into resource and non-resource categories, but a better mechanistic understanding is necessary to improve the theory’s predictions. We examined if two pitcher-dwelling crab spiders (Thomisidae), Thomisus nepenthiphilus and Misumenops nepenthicola, can facilitate nitrogen sequestration in their pitcher plant host, Nepenthes gracilis, by ambushing pitcher-visiting flies and dropping their carcasses into pitchers after consumption. This relationship is, by definition, both mutualistic and facilitative. Laboratory experiments found that both crab spiders increased prey-capture rates of N. gracilis. Nutrient analyses showed that both crab spiders also decreased per unit nitrogen yield of prey. Using experiment duration as a proxy of prey-resource availability, we constructed a mechanistic conceptual model of nutritional benefit. The nutritional benefit received by N. gracilis from T. nepenthiphilus decreases with increasing levels of the limiting resource in the environment (i.e., decreasing levels of resource stress). Our findings suggest that any nutritional mutualism that increases the quantity of resource capture (e.g. number of prey individuals) but decreases the quality of the captured resource (e.g. nitrogen content of individual prey) will necessarily conform to the resource-based predictions of the stress gradient hypothesis.
KeywordsContext dependency Resource facilitation Stress-gradient hypothesis Nepenthes gracilis Crab spider (Thomisidae)
The authors are grateful towards Li Daiqin and Matthew L. M. Lim for constructive advice in study design, Tan Ming Kai for assistance with video recording, Goh Poi Moi for advice in starting and maintaining the fly culture and Liew Chye Fong, for assistance with spectrophotometry. We would also like to thank three anonymous reviewers, whose comments greatly improved the quality of the manuscript.
Author contribution statement
WNL and HTWT formulated the original study design, WNL and RJYL developed the methodology, and RJYL conducted experiments and analysis. WNL wrote the manuscript, and all other authors provided editorial advice.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Video S1 Thomisus nepenthiphilus ambushing a flesh fly on the pitcher lid, subsequently carrying its carcass into the pitcher interior (MPG 8938 kb)
Video S3 Misumenops nepenthicola ambushing a flesh fly under the peristome of a pitcher, dragging it down into the pitcher with it. (MPG 956 kb)
- Beaver RA (1979) Biological studies of the fauna of pitcher plants (Nepenthes) in west Malaysia. Ann Soc Entomol Fr 15:3–17Google Scholar
- Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
- Choo JPS, Koh TL, Ng PKL (1997) Pitcher fluid macrofauna: nematodes and arthropods. In: Tan HTW (ed) A guide to the carnivorous plants of Singapore. Singapore Science Centre, Singapore, pp 51–96Google Scholar
- Clarke CM (2001) Nepenthes of Sumatra and Peninsular Malaysia. Natural History Publications (Borneo), Kota KinabaluGoogle Scholar
- Mazerolle MJ (2016) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.0-4. http://CRAN.R-project.org/package=AICcmodavg. Accessed 24 Feb 2017
- Moran JA, Moran AJ (1998) Foliar reflectance and vector analysis reveal nutrient stress in prey-deprived pitcher plants (Nepenthes rafflesiana). Int J Plant Sci 159:996–1001Google Scholar
- Ruppert EE, Fox RS, Barnes RD (2004) Invertebrate zoology: a functional evolutionary approach, 7th edn. Thomson, BrooksGoogle Scholar
- Stachowicz JJ (2001) The structure of ecological communities. Bioscience 51:235–246. https://doi.org/10.1641/0006-3568(2001)051%5B0235:MFATSO%5D2.0.CO;2 CrossRefGoogle Scholar