The crab spider–pitcher plant relationship is a nutritional mutualism that is dependent on prey‐resource quality

Abstract

Nutritional mutualisms are one of the three major categories of mutualisms and involve the provision of limiting nutrients (resources) to one species by another. It was recently shown in laboratory experiments that two species of pitcher‐dwelling crab spiders (Thomisidae), Thomisus nepenthiphilus and Misumenops nepenthicola, increased capture rates of flesh flies (Sarcophagidae) for their host, Nepenthes gracilis. The spiders ambushed pitcher‐visiting flesh flies and dropped their carcasses into pitchers after consuming them. The consumption of shared prey‐resources by crab spiders and pitcher plants presents the possibility of parasitism between them. However, ecologically generalizable mechanisms that predict the context‐dependent outcomes of such mutualisms are not known. The effectiveness framework (mutualism effectiveness = quality × quantity) is useful for examining the total effect of mutualisms, but its quality component can be difficult to define. We identify the crab spider–pitcher plant interaction as a type of resource conversion mutualism and propose that the quality component in such interactions is the amount of the underlying resource contained in each unit of resource processed. We then used the crab spider–pitcher plant interaction to test the hypothesis that resource conversion mutualisms are more beneficial to the nutrient recipient when operating through high‐quality resources (i.e., large prey, in this interaction). We sampled the prey and inquilines of 107 N. gracilis upper pitches in situ and analysed the differences between pitchers that were inhabited or uninhabited by crab spiders, and the differences between nutritional contents of prey that were consumed by crab spiders or not. Pitchers inhabited by T. nepenthiphilus contained higher numbers of several prey taxa, many of which were flying insects. Consumption by T. nepenthiphilus reduced the nutrient contents in all prey examined. Overall, T. nepenthiphilus‐assisted prey capture is likely to result in a net nutrient gain for N. gracilis that is proportional to the size of prey consumed by T. nepenthiphilus. Our results suggest that resource conversion mutualisms are more likely to operate through high‐quality resources, since the nutrient‐processing species necessarily reduces the quality of the resource it processes while increasing its availability to the nutrient recipient species.

Out of the trap: A new phytothelm‐breeding species ofPhilautusand an updated phylogeny of Bornean bush frogs (Anura: Rhacophoridae)

“…The observed strategy of P . nepenthophilus to breed in Nepenthes could represent a further case of mutualism (Lam & Tan, 2018, 2019), because frogs and tadpoles provide essential nutrients like nitrogen and phosphorus to the plant. The adult frogs leave their excrements, skin fragments, and egg capsules and the tadpoles produce feces and waste after consuming their yolk in the fluid of the pitchers.…”

Plant guttation provides nutrient-rich food for insects

“…In fact, the number of aphids was lower on traps near plants with guttation, possibly due to the increased abundance of natural enemies in plants with guttation. Interestingly, the numbers of mosquitoes were also approximately 40% lower on traps near plants with guttation, which could be due to the presence of Thomisidae spiders near the guttation drops, as these spiders are known to use mosquitoes as prey [54]. Finally, we would like to highlight that the manipulative assay was carried out at the end of the season, when guttation drops were almost completely absent in the field, to avoid the natural presence of guttation drops.…”

Host Plant Specificity in Web-Building Spiders

“…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. Lam and Tan [ 37 ] demonstrated that T. nepenthephilus increased the prey capture rates of Nepenthes gracilis , offsetting the nitrogen loss from consumption by T. nepenthephilus , resulting in an overall net gain.…”

“…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. Lam and Tan [ 37 ] demonstrated that T. nepenthephilus increased the prey capture rates of Nepenthes gracilis , offsetting the nitrogen loss from consumption by T. nepenthephilus , resulting in an overall net gain. However, this benefit only occurs under conditions where prey availability is low and is ultimately lost when prey availability increases, switching from a positively facilitative to a parasitic interaction [ 37 ].…”