Novel pitcher plant–spider mutualism is dependent upon environmental resource abundance

Abstract

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.

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Acknowledgements

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 information

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Authors

Contributions

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.

Corresponding author

Correspondence to Weng Ngai Lam.

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The authors declare that they have no conflict of interest.

Additional information

Communicated by Paulo Guimaraes.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Video S1 Thomisus nepenthiphilus ambushing a flesh fly on the pitcher lid, subsequently carrying its carcass into the pitcher interior (MPG 8938 kb)

442_2018_4246_MOESM3_ESM.mpg

Video S2 Thomisus nepenthiphilus ambushing a flesh fly under the peristome of a pitcher (MPG 262 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)

442_2018_4246_MOESM5_ESM.mpg

Video S4 Misumenops nepenthicola ambushing a flesh fly on the inner wall of a pitcher just as it lands; both fall into the pitcher together. (MPG 580 kb)

Supplementary material 1 (DOCX 20 kb)

Video S1 Thomisus nepenthiphilus ambushing a flesh fly on the pitcher lid, subsequently carrying its carcass into the pitcher interior (MPG 8938 kb)

Video S2 Thomisus nepenthiphilus ambushing a flesh fly under the peristome of a pitcher (MPG 262 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)

Video S4 Misumenops nepenthicola ambushing a flesh fly on the inner wall of a pitcher just as it lands; both fall into the pitcher together. (MPG 580 kb)

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Lim, R.J.Y., Lam, W.N. & Tan, H.T.W. Novel pitcher plant–spider mutualism is dependent upon environmental resource abundance. Oecologia 188, 791–800 (2018). https://doi.org/10.1007/s00442-018-4246-8

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Keywords

  • Context dependency
  • Resource facilitation
  • Stress-gradient hypothesis
  • Nepenthes gracilis
  • Crab spider (Thomisidae)