A dipteran larva–pitcher plant digestive mutualism is dependent on prey resource digestibility

Abstract

Positive species interactions tend to be context dependent. However, it is difficult to predict how benefit in a mutualism changes in response to changing contexts. Nepenthes pitcher plants trap animal prey using leaf pitfall traps known as pitchers. Many specialized inquiline organisms inhibit these pitchers, and are known to facilitate the digestion of prey carcasses in them. Nepenthes gracilis traps diverse arthropod prey taxa, which are likely to differ greatly in the ease with which they may be digested, independently of inquilines, by plant enzymes. In this study, we used in vitro experiments to compare the nutritional benefit provided by phorid (scuttle fly) and culicid (mosquito) dipteran larvae to their host, N. gracilis, and to each other. The effects of phorids on N. gracilis nutrient sequestration were very variable, being positive for large prey which have low digestibility, but negative for small prey which are highly digestible. However, the effect of culicids on N. gracilis and the effects of culicids and phorids on each other were not significantly altered by prey type. These results show that a digestive mutualism is highly dependent on the digestibility of the resource-a context dependency that conforms well to the predictions of the stress-gradient hypothesis in facilitation research. Our findings have significant implications for many other digestive mutualisms, and also suggest that greater insights may be gained from the synthesis of concepts between the fields of mutualism and facilitation research.

Ecology and natural history of swimming pitcher mites (Creutzeria spp., Histiostomatidae) from the traps of Nepenthes pitcher plants

“…In vitro, model pitcher set-ups were established using 15-mL Cellstarâ centrifuge tubes with 3 mL of filtered pitcher fluids and 3.22 mg of D. thoracicus carcasses. In vitro experiments are a convenient yet realistic method for simulating conditions in Nepenthes pitchers and the methodology used in this study was the same as that used in other published Nepenthes inquiline community studies (Lam et al, 2017(Lam et al, , 2018aLeong et al, 2018). Ten randomly selected Creutzeria mite individuals were then introduced into each tube and allowed to feed and reproduce.…”

“…Fluids were filtered using 0.22 µm Amiconâ Ultra centrifugal filters (MilliporeSigma, Burlington, MA, USA) prior to chemical analyses. These methods were the same as those employed in Nepenthes nutrient studies (Lam et al, 2017(Lam et al, , 2018aLeong et al, 2018). Fluid microbe density was determined by measuring the optical density of unfiltered fluids at 600 nm (OD 600 ).…”

“…Separate analyses were conducted for experiments utilizing O. smaragdina and Philidris sp. ant prey, as interaction outcomes within the community were expected to be altered by differences in prey resource type (Leong et al, 2018). The total amount of nitrogen available to the Nepenthes pitcher host through pitcher fluids (which we hereafter term total pitcher-available nitrogen) was determined stoichiometrically from fluid soluble protein and ammonium concentrations as done in Leong et al (2018).…”

“…'phytotelma']) to specialized aquatic metazoan and microbial species known as inquilines (Clarke & Kitching, 1993;Chou, Clarke & Dykes, 2014;Chan et al, 2016;Adlassnig, Peroutka & Lendl, 2011;Gaume et al, 2019). Both aquatic metazoan and microbial inquilines have been shown to facilitate pitcher nutrient sequestration by assisting with the physical and biochemical breakdown of prey carcasses (Lam et al, 2017;Adlassnig et al, 2011), although the nature of this facilitation is still poorly understood and highly contextually variable (Leong, Lam & Tan, 2018).…”

“…Interspecific interactions clearly shape the inquiline communities within Nepenthes phytotelmata (Clarke & Kitching, 1993;Kitching, 2001). The diversity of such interactions, ranging from facilitation (Bradshaw & Creelman, 1984;Lam et al, 2017) to competition (Leong et al, 2018) and predation (Mogi & Chan, 1996;Chua & Lim, 2012;Lam et al, 2018a), make inquiline communities potentially valuable model systems for the study of community ecology and biodiversity phenomena (Srivastava et al, 2004). Nevertheless, knowledge gaps in the basic ecology and life history of some inquiline species greatly limit such a potential utility.…”