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.

Host Plant Specificity in Web-Building Spiders

“…Some Thomisidae crab spiders, which have been documented as obligate Nepenthes pitcher-plant dwellers ( Table 1 ), have likewise been reported to assist their host plant with nitrogen acquisition. The specialised leaves of pitcher-plants, which are used to attract, trap, and digest prey [ 33 , 34 ], also provide suitable microhabitats for the crab spiders Misumenops nepenthicola and Thomisus nepenthephilus [ 34 , 35 ]. These spiders feed on visiting insects drawn to the pitcher-plants [ 34 , 36 ], and in some circumstances, the spiders increase pitcher-plant prey consumption by dropping consumed prey remains into the pitchers.…”

“…The specialised leaves of pitcher-plants, which are used to attract, trap, and digest prey [ 33 , 34 ], also provide suitable microhabitats for the crab spiders Misumenops nepenthicola and Thomisus nepenthephilus [ 34 , 35 ]. These spiders feed on visiting insects drawn to the pitcher-plants [ 34 , 36 ], and in some circumstances, the spiders increase pitcher-plant prey consumption by dropping consumed prey remains into the pitchers. Interestingly, two studies by Lim et al [ 34 ], and Lam and Tan [ 37 ] concluded that the type of association between crab spiders and pitcher-plants is environmentally context-dependent.…”

Inside the trap: Biology and behavior of the pitcher‐dwelling crab spider,Misumenops nepenthicola

“…Chua and Lim (2012) suggested that spiders feed primarily on aquatic infauna organisms; however, we rarely observed spiders hunting for live prey such as mosquito larvae in the pitcher fluid. Recent studies point toward a neutral or even mutualistic relationship because they observed spiders ambushing pitcher visitors and dropping the carcasses into the pitcher after feeding, thereby potentially increasing the prey intake of the plant (Lam & Tan, 2019;Lim, Lam, & Tan, 2018 Bohn, H. F., & Federle, W. (2008). Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar.…”

Plant–animal interactions between carnivorous plants, sheet‐web spiders, and ground‐running spiders as guild predators in a wet meadow community

“…Carnivorous plants experience additional plant–animal interactions that other angiosperms do not. These include prey–pollinator conflict where capturing potential pollinators can reduce growth and reproduction (Ellison & Gotelli, 2009), digestive mutualism where animals help carnivorous plants acquire nutrients from prey (Anderson, 2005; Anderson & Midgley, 2003; Chin, Moran, & Clarke, 2011; Ellis & Midgley, 1996; Grafe, Schöner, Kerth, Junaidl, & Schöner, 2011; Lam, Lim, Wong, & Tan, 2018; Lim, Lam, & Tan, 2018; Scharmann, Thornham, Grafe, & Federle, 2013; Schöner et al, 2017), and antagonistic plant–animal interactions such as kleptoparasitism (Burbridge, 1880; Scharmann et al, 2013).…”