The fluid-containing traps of Nepenthes carnivorous pitcher plants (Nepenthaceae) are often inhabited by organisms known as inquilines. Dipteran larvae are key components of such communities and are thought to facilitate pitcher nitrogen sequestration by converting prey protein into inorganic nitrogen, although this has never been demonstrated in Nepenthes. Pitcher fluids are also inhabited by microbes, although the relationship(s) between these and the plant is still unclear. In this study, we examined the hypothesis of digestive mutualism between N. gracilis pitchers and both dipteran larvae and fluid microbes. Using dipteran larvae, prey and fluid volumes mimicking in situ pitcher conditions, we conducted in vitro experiments and measured changes in available fluid nitrogen in response to dipteran larvae and microbe presence. We showed that the presence of dipteran larvae resulted in significantly higher and faster releases of ammonium and soluble protein into fluids in artificial pitchers, and that the presence of fluid microbes did likewise for ammonium. We showed also that niche segregation occurs between phorid and culicid larvae, with the former fragmenting prey carcasses and the latter suppressing fluid microbe levels. These results clarify the relationships between several key pitcher-dwelling organisms, and show that pitcher communities facilitate nutrient sequestration in their host.
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.
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.
Positive species interactions are ubiquitous in natural communities, but the mechanisms through which they operate are poorly understood. One proposed mechanism is resource conversion – the conversion by a benefactor species of a resource from a resource state that is inaccessible to a potential beneficiary species into a resource state that is accessible. Such conversion often occurs as a byproduct of resource consumption, and sometimes in exchange for non‐resource benefits to the benefactor species. At least five known classes of interactions, including both facilitative and mutualistic ones, may be classified as resource conversion interactions. We formulated a generalizable mathematical model for resource conversion interactions and examined two model variants that represent processing chain and nurse plant interactions. We examined the conditions under which these conformed to the stress‐gradient hypothesis (SGH), which predicts increased interaction benefits in more stressful environments. These yielded four key insights: 1) resource conversion interactions can be positive (towards the resource recipient) only when facilitator‐mediated resource conversion is more efficient than the baseline, spontaneous, facilitator‐independent resource conversion; 2) the sign of resource conversion interaction outcomes never switches (e.g. from net positive to net negative) with changing levels of resource availability, when all other parameters are kept constant; 3) processing chain interactions at equilibrium can never be positive in a manner that conforms to the SGH; 4) nurse plant interactions can be positive and conform to the SGH, although the manner in which they do depends largely on how resource stress is defined, and the environmental supply rate of surface soil moisture. The first two insights are likely to be generalizable across all resource conversion interactions. The general agreement of the model with empirical studies suggest that resource conversion is the mechanism underlying the aforementioned interactions, and an ecologically meaningful way of classifying these previously unassociated positive species interactions.
Decomposition is a key ecosystem function, and the rate of decomposition in forests affects their carbon storage potentials. Processes and factors determining leaf litter decomposition rates in dry-land and temperate forests are well understood, but these are generally poorly studied in tropical wetland forests, especially freshwater swamp forests (FSF). The home-field advantage (HFA) hypothesis predicts that soil microbes specialize in decomposing leaf litter produced by the tree species in their immediate vicinity. However, empirical support for the HFA is equivocal, and the HFA has never been tested in the highly heterogeneous and biodiverse ecosystems of tropical FSFs.We collected leaf litter from swamp and non-swamp tree species in a tropical FSF in Singapore and monitored the decomposition rates of these in swamp and non-swamp plots for a period of eight months. Leaf litter decomposed 3.7 times more slowly in swamp plots. Leaf litter from swamp tree species were significantly poorer in quality (higher C:N ratio) than those of non-swamp FSF tree species, but this had only a weak effect on decomposition rates. There was also only weak evidence for the HFA and only in non-swamp conditions. Our results show that while the leaf litter of tropical FSF swamp and non-swamp tree species differ significantly in chemical traits, litter decomposition rate is ultimately determined by local abiotic conditions, such as hydrology. Additionally, the high FSF tree diversity may prevent decomposer communities from specializing on any group of leaf litter types and thus limit the extent of HFA observed in such heterogeneous forests.
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.
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