Time management and nectar flow: flower handling and suction feeding in long-proboscid flies (Nemestrinidae: Prosoeca)

Abstract

A well-developed suction pump in the head represents an important adaptation for nectar-feeding insects, such as Hymenoptera, Lepidoptera and Diptera. This pumping organ creates a pressure gradient along the proboscis, which is responsible for nectar uptake. The extremely elongated proboscis of the genus Prosoeca (Nemestrinidae) evolved as an adaptation to feeding from long, tubular flowers. According to the functional constraint hypothesis, nectar uptake through a disproportionately elongated, straw-like proboscis increases flower handling time and consequently lowers the energy intake rate. Due to the conspicuous length variation of the proboscis of Prosoeca, individuals with longer proboscides are hypothesised to have longer handling times. To test this hypothesis, we used field video analyses of flower-visiting behaviour, detailed examinations of the suction pump morphology and correlations of proboscis length with body length and suction pump dimensions. Using a biomechanical framework described for nectar-feeding Lepidoptera in relation to proboscis length and suction pump musculature, we describe and contrast the system in long-proboscid flies. Flies with longer proboscides spent significantly more time drinking from flowers. In addition, proboscis length and body length showed a positive allometric relationship. Furthermore, adaptations of the suction pump included an allometric relationship between proboscis length and suction pump muscle volume and a combination of two pumping organs. Overall, the study gives detailed insight into the adaptations required for long-proboscid nectar feeding, and comparisons with other nectar-sucking insects allow further considerations of the evolution of the suction pump in insects with sucking mouthparts.

Fig. 1

Linear regression between total flower handling time and proboscis length of Prosoeca sp. on flowers of L. oreogena

Fig. 2

Linear regression between flower handling time and proboscis length of Prosoeca sp. on flowers of Lapeirousia oreogena divided into three successive phases. In addition, for each phase, illustrating pictures are given above: a, d hovering fly with proboscis in feeding position; b, e drinking with proboscis fully inserted into the flower spur with the head in contact with the anthers; c, f proboscis is removed in a rapid movement. Of these, only drinking time shows a positive relationship to proboscis length

Fig. 3

MicroCT head scans of Prosoeca sp. displaying the cibarial pump (blue) and the pharyngeal pump with oesopharynx (both green). a, b Lateral and frontal view with cibarial valve, cibarial dilator and cibarial–pharyngeal valve. c, d Frontal and lateral view with pharyngeal dilator and compressor muscles together with oesopharyngeal dilators. e, f Cibarial protractor and retractor attached to a dorsolateral cuticular ledge on the cibarium. Cb cibarium, cpv cibarial–pharyngeal valve, mcc musculus clypeo-cibarialis, mcpd m. clypeo-pharyngealis dorsalis, mcpv m. clypeo-pharyngealis ventralis, mfc musculus fronto-cibarialis, mfp m. fronto-pharyngealis, mgc m. geno-cibarialis, mlc m. labro-cibarialis, mtod m. tentorio-oesopharyngealis dorsalis, mtol m. tentorio-oesopharyngealis lateralis, oe oesopharynx, ph pharynx

Fig. 4

Linear regression of suction pump muscles, proboscis and body lengths. a Positive correlation between proboscis and body length. b Cibarial pump. c Pharyngeal dilator (triangles) and compressor muscles (circles). Both cibarial and pharyngeal pump muscles are positively correlated to proboscis length

Fig. 5

Three-phase suction pump of Prosoeca sp. based on microCT scans. Contracting muscles are drawn in red with orange arrows; relaxing muscles are hollow with blue arrows. a Cibarial dilator muscles open the cibarial valve and suck nectar into the cibarium. b Pharyngeal dilators pump nectar through the cibarial–pharyngeal valve into the pharynx. In phase A and B, the cibarial protractor and retractor (light red) work as antagonists to the main dilator muscles to hold the pump stationary. c Pharyngeal compressor muscles push the nutrition into the oesopharynx, and the posterior dilator muscles open the oesopharyngeal valve. Cuticle elasticity of both pump chambers provides restoration force to reset the suction pump for the next food intake phase. Cb cibarium, cbd cibarial dilator, cbp cibarial protractor, cbr cibarial retractor, cpv cibarial–pharyngeal valve (true mouth), cv cibarial valve (functional mouth), oe oesophagus, ph pharynx, phc pharyngeal compressor, phd pharyngeal dilator