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Pollinator-prey conflicts in carnivorous plants: When flower and trap properties mean life or death.

ABSTRACT: Insect-pollinated carnivorous plants are expected to have higher fitness if they resolve pollinator-prey conflicts by sparing insects pollinating their flowers while trapping prey insects. We examined whether separation between flowers and traps of the carnivorous sundew species or pollinator preferences for colours of flowers enable these plants to spare pollinators. In addition, we collected odours from flowers and traps of each carnivorous species in order to identify volatile chemicals that are attractive or repellent to pollinators and prey insects. In Drosera spatulata and D. arcturi, no volatiles were detected from either their flowers or traps that could serve as kairomone attractants for insects. However, behavioural experiments indicated white colour and spatial separation between flowers and traps aid in reducing pollinator entrapment while capturing prey. In contrast, D. auriculata have flowers that are adjacent to their traps. In this species we identified chemical signals emanating from flowers that comprised an eight-component blend, while the plant's traps emitted a unique four-component blend. The floral odour attracted both pollinator and prey insects, while trap odour only attracted prey. This is the first scientific report to demonstrate that carnivorous plants utilize visual, spatial, and chemical signals to spare flower visitors while trapping prey insects.

SUBMITTER: El-Sayed AM

PROVIDER: S-EPMC4757879 | biostudies-other | 2016 Feb

REPOSITORIES: biostudies-other

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Pollinator-prey conflicts in carnivorous plants: When flower and trap properties mean life or death.

El-Sayed Ashraf M AM Byers John A JA Suckling David M DM

Scientific reports 20160218

Insect-pollinated carnivorous plants are expected to have higher fitness if they resolve pollinator-prey conflicts by sparing insects pollinating their flowers while trapping prey insects. We examined whether separation between flowers and traps of the carnivorous sundew species or pollinator preferences for colours of flowers enable these plants to spare pollinators. In addition, we collected odours from flowers and traps of each carnivorous species in order to identify volatile chemicals that ...[more]

PMID: 26888545

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Project description:Sarracenia pitcher plants display interspecific differences in prey, so far only explained by pitcher morphology. We hypothesized that pitcher odours play a role in prey composition. We first compared odour and prey compositions among Sarracenia taxa grown together, forming a kinship gradient from S. purpurea known to capture primarily ants towards S. leucophylla known to capture many flying insects: S. purpurea, S. X mitchelliana, and S. X Juthatip soper & S. X leucophylla horticultural hybrids. We then measured several pitcher traits to disentangle the contributions of morphology and odour to prey variation. The pitcher odours were as diverse as those of generalist-pollinated flowers but with notable differences among taxa, reflecting their relatedness. VOC similarity analyses revealed taxon specificities, that mirrored those revealed by prey similarity analyses. S. X leucophylla stood out by being more specialised in flying insects like bees and moths and by releasing more monoterpenes known to attract flower visitors. S. X Juthatip soper trapped as many bees but fewer moths, sesquiterpenes contributing less to its scent. Ants and Diptera were the main prey of the other two with fatty-acid-derivative-dominated scents. Quantities of the different prey groups can be inferred 98% from quantities of the odour classes and pitcher dimensions. Two syndromes were revealed: ants associated with fatty-acid-derivatives and short pitchers; flying insects associated with monoterpenes, benzenoids and tall pitchers. In S. X leucophylla, emission rate of fatty-acid-derivatives and pitcher length explained most variation in ant captures; monoterpenes and pitcher length explained most variation in bee and moth captures; monoterpenes alone explained most variation in Diptera and wasp captures. Our results suggest that odours are key factors of the diet composition of pitcher plants. They support the hypothesis of perceptual exploitation of insect biases in carnivorous plants and provide new insights into the olfactory preferences of insect groups.

Project description:Background and aimsCarnivorous plants of the genus Nepenthes possess modified leaves that form pitfall traps in order to capture prey, mainly arthropods, to make additional nutrients available for the plant. These pitchers contain a digestive fluid due to the presence of hydrolytic enzymes. In this study, the composition of the digestive fluid was further analysed with regard to mineral nutrients and low molecular-weight compounds. A potential contribution of microbes to the composition of pitcher fluid was investigated.MethodsFluids from closed pitchers were harvested and analysed for mineral nutrients using analytical techniques based on ion-chromatography and inductively coupled plasma-optical emission spectroscopy. Secondary metabolites were identified by a combination of LC-MS and NMR. The presence of bacteria in the pitcher fluid was investigated by PCR of 16S-rRNA genes. Growth analyses of bacteria and yeast were performed in vitro with harvested pitcher fluid and in vivo within pitchers with injected microbes.Key resultsThe pitcher fluid from closed pitchers was found to be primarily an approx. 25-mm KCl solution, which is free of bacteria and unsuitable for microbial growth probably due to the lack of essential mineral nutrients such as phosphate and inorganic nitrogen. The fluid also contained antimicrobial naphthoquinones, plumbagin and 7-methyl-juglone, and defensive proteins such as the thaumatin-like protein. Challenging with bacteria or yeast caused bactericide as well as fungistatic properties in the fluid. Our results reveal that Nepenthes pitcher fluids represent a dynamic system that is able to react to the presence of microbes.ConclusionsThe secreted liquid of closed and freshly opened Nepenthes pitchers is exclusively plant-derived. It is unsuitable to serve as an environment for microbial growth. Thus, Nepenthes plants can avoid and control, at least to some extent, the microbial colonization of their pitfall traps and, thereby, reduce the need to vie with microbes for the prey-derived nutrients.

Dataset Information

Pollinator-prey conflicts in carnivorous plants: When flower and trap properties mean life or death.

Publications

Pollinator-prey conflicts in carnivorous plants: When flower and trap properties mean life or death.

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