Mechanical determinants of nectar-feeding energetics in butterflies: muscle mechanics,feeding geometry,and functional equivalence

Summary We develop a mechanistic model for nectar feeding in butterflies that integrates the two basic components of the feeding process: the fluid dynamics of nectar flow through the food canal and the contractile mechanics of the muscular, cibarial pump. We use the model to predict the relation between rate of energy intake during feeding and nectar concentration. We then identify nectar concentations that maximize energy intake rates (the optimal concentrations). We illustrate the model using measurements of the food canal and cibarium of Pieris butterflies. The model predicts an overall optimal range of nectar concentration of 31–39% sucrose for butterflies, which is in agreement with previously reported laboratory values. The model also predicts an interaction among the geometries of the food canal, the cibarial cavity, and the cibarial muscles, that allows us to identify the combinations of food canal, cibarium, and muscle dimensions that yield the highest rates of energy intake. Nectar-feeding is functionally equivalent in butterflies and hummingbirds: two physically different feeding mechanisms can yield identical energy intake rates. This equivalence results from a mathematical and physical similarity between quasi-steady-state fluid flow in hummingbrid tongues and the force-velocity characteristics of contracting cibarial muscle in butterflies.     

Nectar uptake rates and optimal nectar concentrations of two butterfly species

Summary The relationship between sucrose concentration of nectar and volume uptake rate by the butterflies Agraulis vanillae (Nymphalidae) and Phoebis sennae (Pieridae) was examined. Recent theoretical models simulating feeding energetics of nectarivores have assumed that this volume uptake rate is produced by a constant but undetermined pressure drop (the difference between pressure at the proximal and distal ends of the feeding channel) at all nectar concentrations. These models predict that nectar of 20–25% sucrose maximizes the rate of energy intake and should thus be preferred by nectarivores. Data collected for Agraulis and Phoebis falsify this pressure drop assumption; both species produce greater pressure drops with increasing nectar concentration. In addition, males of both species produce greater suction pressure and uptake rates than females. This results in greater rates of energy intake for males of both species. The volume uptake rates produced by each species differ from those predicted by the models. This produces a maximal rate of energy intake at 35–40% sucrose rather than 20–25%. The empirically determined relationship between energy intake rate and nectar concentration esembles that predicted for discontinuous nectar feeders such as hummingbirds more closely than the relationship predicted for continuous suction feeders, suggesting that other basic assumptions about the feeding mechanism of butterflies should be critically examined.     

Experimental component analysis of blowfly feeding behaviour

The duration of feeding of starved Phormia regina on sucrose, in the range 0·1 to 2·0 M, is a constant. The increasing viscosity of sucrose concentrations greater than 0·5 M caused a reduction in the feeding rate over this feeding period, with a resulting decrease in the volume of sucrose ingested. For 2·0 M sucrose, viscosity effects reduce the potential quantity ingested by one-third. Using the Poiseuille equation, the relative pressures exerted by the cibarial pump were calculated, and from these data the efficiency of the cibarial pump in overcoming the impedance imposed by viscosity could be estimated. The efficiency was found to decrease with increasing viscosity. The application of experimental component analysis to the study yielded parameters which can be used for quantitative comparisons of sugars, and for evaluating the interactions between the various aspects of feeding behaviour.     

Effects of nectar volume and concentration on sugar intake rates of Australian honeyeaters (Meliphagidae)

Summary Sugar intake rates of captive Australian honeyeaters (Meliphagidae) feeding at artificial flowers varied across species, and as a function of nectar volume and concentration within each species. Red Wattlebirds (Anthochaera carunculata, 110 g), achieved higher intake rates than New Holland Honeyeaters (Phylidonyris novaehollandiae, 20 g), and both achieved higher rates than Eastern Spinebills (Acanthorhynchus tenuirostris, 10 g). These results reflect differences in bill and tongue dimensions as well as in body mass. Sugar intake rates for all three species increased with volume (5–50 l) at any given concentration (10–60% mass/mass sucrose). For a given volume, sugar intake rates peaked at intermediate concentrations: 40–50% for the two larger species, and 30–40% for the smallest species. Published studies for other nectarivores foraging at unlimited volume feeders also show optimal nectar concentrations of 30–50%. However, biophysical theory predicts optima at 20–26% for small volumes, and plants presumed to be adapted for bird-pollination often have dilute nectar (20–30%). To explore this discrepancy further, we presented New Holland Honeyeaters with a range of sucrose concentrations (10–50%) using two presentation schemes. In the first we varied concentration but kept volume constant, thus varying gross sugar reward available in each concentration. This gave maximum sugar intake rates at 50%. In the second we varied both volume and concentration so that gross sugar rewards were equal for all solutions, decoupling high concentrations and large sugar rewards. This gave optima at 20%. We argue that variation among plants in nature more closely resembles the latter, equal sugar presentation scheme, and therefore, that dilute nectars may indeed represent adaptations for bird pollination.     

The intake responses of three species of leaf-nosed Neotropical bats

Flower-visiting bats encounter nectars that vary in both sugar composition and concentration. Because in the new world, the nectars of bat-pollinated flowers tend to be dominated by hexoses, we predicted that at equicaloric concentrations, bats would ingest higher volumes of hexoses than sucrose-containing nectars. We investigated the intake response of three species of Neotropical bats, Leptonycteris curasoae, Glossophaga soricina and Artibeus jamaicensis, to sugar solutions of varying concentrations (292, 438, 584, 730, 876, and 1,022 mmol L⁻¹) consisting of either sucrose or 1:1 mixtures of glucose and fructose solutions. Bats did not show differences in their intake response to sucrose and 1:1 glucose–fructose solutions, indicating that digestion and absorption in bat intestines are designed under the principle of symmorphosis, in which no step is more limiting than the other. Our results also suggest that, on the basis of energy intake, bats should not prefer hexoses over sucrose. We used a mathematical model that uses the rate of sucrose hydrolysis measured in vitro and the small intestinal volume of bats to predict the rate of nectar intake as a function of sugar concentration. The model was a good predictor of the intake responses of L. curasoae and G. soricina, but not of A. jamaicensis.     

Behaviour of <Emphasis Type="Italic">Odontomachus chelifer</Emphasis> (Latreille) (Formicidae: Ponerinae) Feeding on Sugary Liquids

Sugary solution intake behavior by Odontomachus chelifer (Latreille), is studied. The feeding mechanism involved is described. Effects of sucrose concentration and solution viscosity on ingested load, feeding time and rate of liquid intake are assessed. Suction was always the feeding mechanism, regardless of concentration or viscosity of the solution. There were no differences in loads ingested for concentrations of up to 30% w/w, but feeding took longer at this concentration. Liquid intake rates were higher at the lowest concentrations. Above 40% w/w, values of all three variables were smaller. O. chelifer’s ability to ingest mildly viscous fluids could be related to its capacity to ingest other viscous fluids present in its diet.     

Sugar preferences, absorption efficiency and water influx in a Neotropical nectarivorous passerine, the Bananaquit (Coereba flaveola)

Nectarivory has evolved repeatedly in a number of unrelated bird taxa throughout the world and nectar feeding birds, regardless of their taxonomic affiliation, display convergent foraging and food processing adaptations that allow them to subsist on weak sugar solutions. However, phylogeny influences sugar type preferences of nectarivores. We investigated sugar preferences, assimilation efficiency and water flux in a Neotropical honeycreeper, the Bananaquit (Coereba flaveola; Coerebidae), a member of a radiation of tanagers and finches. Bananaquits showed no preference for nearly equicaloric (25% w/v) sucrose, glucose, fructose or glucose-fructose mixtures in pair-wise choice tests. In agreement with this lack of preference, they were equally efficient at absorbing sucrose and both hexoses. Apparent assimilation efficiency of these sugars was around 97.5%. In pair-wise tests, Bananaquits displayed a strong preference for the most concentrated sucrose solution when the lowest concentration ranged from 276 to 522 mM. Between 522 and 1120 mM sucrose solution concentrations, Bananaquits were able to adjust their volumetric food intake in order to maintain a constant energy intake. At solution concentration of 276 mM, birds could not maintain their rate of energy intake by increasing food consumption enough. We consider that at low sugar concentrations, Bananaquits faced a physiological constraint; they were unable to process food at a fast enough rate to meet their energy needs. We also explored the possibility that dilute nectars might be essential to sustain high water needs of Bananaquits by allowing them to control osmolarity of the food. Between 276 and 1120 mM sucrose solution concentrations, average amount of free water drunk by Bananaquits was independent of food concentration. They drank very little supplementary water and did not effectively dilute concentrated nectars. The evidence suggests that water bulk of dilute nectars is a burden to Bananaquits.     

Pollination by passerine birds: why are the nectars so dilute?

Bird-pollinated flowers are known to secrete relatively dilute nectars (with concentrations averaging 20–25% w/w). Many southern African plants that are pollinated by passerine birds produce nectars with little or no sucrose. Moreover, these hexose nectars are extremely dilute (10–15%). This suggests a link between sugar composition and nectar concentration. Nectar originates from sucrose-rich phloem sap, and the proportion of monosaccharides depends on the presence and activity of invertase in the nectary. Hydrolysis of sucrose increases nectar osmolality and the resulting water influx can potentially convert a 30% sucrose nectar into a 20% hexose nectar, with a 1.56 times increase in volume. Hydrolysis may also increase the gradient for sucrose transport and thus the rate of sugar secretion. When sucrose content and refractometer data were compared, some significant correlations were seen, but the occurrence of sucrose-rich or hexose-rich nectars can also be explained on phylogenetic grounds (e.g. Erythrina and Protea). Hexose nectars may be abundant enough to drip from open flowers, but evaporation leads to much variability in nectar concentration and increases the choices available to pollinators.     

Nectar intake rate is modulated by changes in sucking pump activity according to colony starvation in carpenter ants

Dynamics of fluid feeding has been deeply studied in insects. However, the ability to vary the nectar-intake rate depending only on the carbohydrate deprivation has been clearly demonstrated only in Camponotus mus ants. When insect morphometry and fluid properties remain constant, changes in intake rate could only be attributed to variations in sucking pump activity. Previous records of the electrical activity generated during feeding in C. mus have revealed two different signal patterns: the regular (RP, frequencies: 2–5 Hz) and the irregular (IP, frequencies: 7–12 Hz). This work studies the mechanism underlying food intake-rate modulation in ants by analysing whether these patterns are involved. Behaviour and electrical activity generated by ants at different starvation levels were analysed during feeding on sucrose solutions. Ants were able to modulate the intake rate for a variety of sucrose concentrations (10, 40 and 60%w/w). The IP only occurred for 60% of solutions and its presence did not affect the intake rate. However, during the RP generated under the starved state, we found frequencies up to 7.5 Hz. RP frequencies positively correlated with the intake-rate for all sucrose concentrations. Hence, intake-rate modulation according to sugar deprivation is mainly achieved by the ant’s ability to vary the pumping frequency.     

Foraging behavior adjustments related to changes in nectar sugar concentration in phyllostomid bats

Nectar-feeding bats regulate their food ingestion in response to changes in sugar concentration as a way to achieve a constant energy intake. However, their digestive capability to assimilate sugars can limit their total energy intake, particularly when sugar concentration in nectar is low. Our experimental study evaluated the effect that changes in sugar concentration of nectar have on the foraging behavior of the nectar-feeding bats Glossophaga soricina and Leptonycteris yerbabuenae in captivity. We measured foraging behavior and food intake when bats fed at different concentrations of sucrose (5, 15, 25 and 35%wt/vol.). To compensate for low-energy intake, both bat species reduced their flight time, and increased feeding time when sugar concentration decreased. Our results suggest that nectar-feeding bats in nature confront two scenarios with complementary ecological effects: 1) bats feeding on dilute nectars (i.e. ≤15%wt/vol.) should increase the number of flowers visited per night enhancing pollination, and 2) bats feeding on concentrated nectars could spend more time flying, including long- and short-distance-flights increasing food patch exploration for use during subsequent nights, and thus enhancing plant gene flow. Further studies on foraging behavior of nectarivorous bats under natural conditions are necessary to corroborate these hypotheses.     

Nectar feeding by the hovering hawk moth Macroglossum stellatarum: intake rate as a function of viscosity and concentration of sucrose solutions

Although nectar feeding in insects has long been studied, the knowledge of the effect of nectar energy content on the ingestion dynamics separately from the viscosity of the fluid is very limited. To determine the effects of both factors on the feeding behavior of the hovering hawk moth Macroglossum stellatarum, we developed a method to independently manipulate sucrose concentrations and viscosity. The intake rate was analyzed as a function of sucrose concentration, the concentration at constant viscosity (kept constant by adding tylose, an inert polysaccharide), and of the different viscosities of a 30% weight/weight (w/w) sucrose solution (by adding different amounts of tylose). By increasing the concentration, and thus its viscosity, the solution intake rate (in microl s (-1)) decreased beyond a 20% w/w sucrose solution. For a 30% sucrose solution, the intake rate decreased with increasing viscosity. At constant viscosity, the solution intake rate decreased beyond a 30% w/w sucrose solution. However, if we considered the quantity of sucrose ingested per unit time (sucrose intake rate), the same fitted maximum was attained for both series in which the sucrose concentration changed (33.6% w/w). Results suggest that the gustatory input affects the dynamics of fluid ingestion separately from the viscosity.     

Whitebellied sunbirds (<Emphasis Type="Italic">Nectarinia talatala</Emphasis>, Nectariniidae) do not prefer artificial nectar containing amino acids

Amino acids are the most abundant class of compounds in nectar after sugars. Like its sugar concentration, the amino acid concentration of nectar has been linked to pollinator type, and it has been suggested that amino acid concentrations are high in the floral nectars of plant species pollinated by passerine birds compared to those pollinated by hummingbirds. We investigated the feeding response of whitebellied sunbirds (Nectarinia talatala) to the inclusion of amino acids in artificial nectar (0.63 M sucrose solution). The response to asparagine, glutamine, phenylalanine, proline, serine and valine, amino acids commonly found in floral nectars, was tested individually and using a mixture of all six amino acids, at two different concentrations (2 and 15 mM). Sunbirds showed no significant preference for amino acids in nectar, or avoided them, especially at the higher concentration. We discuss these findings in the light of the nitrogen requirements of nectarivorous birds and data on amino acids in floral nectars.     

Nectar feeding by the ant Camponotus mus: intake rate and crop filling as a function of sucrose concentration

In independent assays, workers of the ant Camponotus mus were conditioned to visit an arena where they found a large drop of sucrose solution of different concentrations, from 5 to 70% weight on weight (w/w). Single ants were allowed to collect the sucrose solution ad libitum, and feeding time, feeding interruptions, crop load, and intake rates were recorded. Feeding time increased exponentially with sucrose concentration, and this relationship was quantitatively described by the increase in viscosity with concentration corresponding to pure sucrose solutions. Ants collecting dilute solutions (5 to 15% w/w) returned to the nest with partial crop loads. Crop filling increased with increasing sucrose concentration, and reached a maximum at 42.6% w/w. Workers collecting highly concentrated solutions (70% w/w) also returned to the nest with a partially-filled crop, as observed for dilute solutions. Nectar intake rate was observed to increase with increasing sucrose concentration in the range 5 to 30% sucrose. It reached a maximum at 30.8%, and declined with increasing sucrose concentration. Results suggest that both sucrose concentration and viscosity of the ingested solution modulate feeding mechanics as well as the worker's decision about the load size to be collected before leaving the source.     

Sucking pump activity in feeding behaviour regulation in carpenter ants

Modulation of liquid feeding-rate would allow insects to ingest more food in the same time when this was required. Ants can vary nectar intake rate by increasing sucking pump frequency according to colony requirements. We analysed electrical signals generated by sucking pump activity of ants during drinking solutions of different sucrose concentrations and under different carbohydrate-deprivation levels. Our aim was to define parameters that characterize the recordings and analyse their relationship with feeding behaviour.Signals showed that the initial and final frequencies of sucking pump activity, as well as the difference between them were higher in sugar-deprived ants. However, these parameters were not influenced by sucrose solution concentration, which affected the number of pump contractions and the volume per contraction. Unexpectedly, we found two different responses in feeding behaviour of starved and non-starved ants depending on concentration. Starved ants drank dilute solutions for the same length of time as non-starved ants but ingested higher volumes. While drinking the concentrated solutions, starved ants drank the same volume, but did so in a shorter time than the non-starved ones. Despite these differences, for each analysed concentration the total number of pump contractions remained constant independently of sugar-deprivation level. These results are discussed in the frame of feeding regulation and decision making in ant foraging behaviour.     

Effect of carbohydrate on age-related feeding behaviors and longevity in adult black cutworm,Agrotis ipsilon (Lepidoptera: Noctuidae)

Age-related consumption and longevity were monitored in the laboratory for adultA. ipsilon fed either a 1M sucrose solution or water. An additional group was completely starved. Adults consumed sucrose solution and water just after eclosion; the percentage feeding daily and the mean daily consumption for females and males fed sucrose solution declined with time, whereas the percentage feeding daily and the mean daily consumption of those fed water increased with time. Total consumption was significantly higher for those fed sucrose solution (P<0.01) because they lived longer, but consumption per day averaged over the entire adult stage was not significantly different between those fed sucrose solution and those fed water (P>0.05). Mean longevity was significantly extended for females and males fed sucrose solution over those fed water or starved (P<0.01). Moreover, consumption of either fluid was significantly correlated with extended longevity in all groups (P<0.05). These data on fluid consumption by adultA. ipsilon are discussed relative to posteclosion migratory activities.     

Bird pollinators differ in their tolerance of a nectar alkaloid

Although the function of nectar is to attract and reward pollinators, secondary metabolites produced by plants as anti‐herbivore defences are frequently present in floral nectars. Greater understanding is needed of the effects of secondary metabolites in nectar on the foraging behaviour and performance of pollinators, and on plant–pollinator interactions. We investigated how nectar‐feeding birds, both specialist (white‐bellied sunbirds Cinnyris talatala) and generalist (dark‐capped bulbuls Pycnonotus tricolor and Cape white‐eyes Zosterops virens), respond to artificial nectar containing the alkaloid nicotine, present in nectar of Nicotiana species. Preference tests were carried out with a range of nicotine concentrations (0.1–300 μM) in two sucrose concentrations (0.25 and 1 M), and for bulbuls also in two sugars (sucrose and hexose). In addition, we measured short‐term feeding patterns in white‐bellied sunbirds that were offered nicotine (0–50 μM) in 0.63 M sucrose. Both nicotine and sugar concentrations influenced the response of bird pollinators to nicotine. The birds showed dose‐dependent responses to nicotine; and their tolerance of high nicotine concentrations was reduced on the dilute 0.25 M sucrose diet, on which they increased consumption to maintain energy intake. White‐bellied sunbirds decreased both feeding frequency and feeding duration as the nicotine concentration in artificial nectar increased. Of the three species, bulbuls showed the highest tolerance for nicotine, and sugar type (sucrose or hexose) had no effect. The indifference of bulbuls to nicotine may be related to their primarily frugivorous diet. However, the response of white‐eyes to nicotine in the dilute sucrose solution was very similar to that of sunbirds, even though white‐eyes are generalist nectar‐feeders. Additional testing of other avian nectarivores and different secondary metabolites is required to further elucidate whether generalist bird pollinators, which utilise dilute nectars in which secondary metabolites have stronger deterrent effects, are more tolerant of ‘toxic’ nectar.     

Chirp rate variability in male song ofEphippigerida taeniata (Orthoptera: Ensifera)

Variability in the chirp rate of the male song of the ephippigerine speciesEphippigerida taeniata during intraspecific communication was investigated in the laboratory. Conspecific chirps were used as auditory stimuli. The stimulus rate was controlled by computer. Experiments were carried out at 19, 27, and 35°C. Acoustically isolated males ofE. taeniata sang with a relatively constant chirp rate, which depended on the ambient temperature. Chirp rate significantly increased with rising temperature from 19 to 27°C, whereas at 35°C the chirp rate did not differ significantly from that at 27°C. Male chirp rates were affected by stimulus rates. Males significantly increased their chirp rate in response to increasing stimulus rates at temperatures of 19 and 27°C. At 35°C the increase in the chirp rate was not significant. At 27 and 35°C males sang with a higher chirp rate than the stimulus rate within a certain range. Evaluating stimulus and response chirp pattern when the males increased their chirp rate in response to the stimulus rate showed that an alternation pattern was established. More than 50% of the male chirps occurred at a characteristic time range at around 40% of the interstimulus interval, which was slightly affected by temperature.     

Temperature and food quality influences feeding behavior,assimilation efficiency and growth rate of arctic woolly-bear caterpillars

Summary The energy budget for feeding activity and growth of larval Gynaephora groenlandica was investigated on the tundra and in the laboratory. Larvae fed only in June when the buds and young leaves of Salix arctica, its principal host plant, contained the highest concentrations of macro-nutrients and total nonstructural carbohydrates (TNC). The mid-summer hiatus in larval feeding was coincident with an abrupt decline in the TNC content of leaves and a buildup of plant secondary metabolites in the leaves of S. arctica. Following cessation of feeding, the larvae remained concealed from the sun within crevices and vegetation mats. Growth rates of larvae incubated at 15 and 30°C were similar (4.7–5.0 mg/larva/day), but the assimilation efficiency at 15°C was four times greater (40%) than at 30°C. Growth rates were lowest at 5°C (0.22mg/larva/day) as was the assimilation efficiency (6.6%), because of the extended residence time of food in the gut. The high rate of ingestion and excretion at 30°C was caused by elevated maintenance metabolism. Changes in metabolic state influenced oxygen consumption, which was highest for feeding larvae (0.29 ml/g/h) and significantly lower for each, digesting, moving, starved larvae, and lowest for inactive larvae (0.06 ml/g/h). An influence of temperature and leaf quality on digestion rate and maintenance metabolism is the most likely cause of the feeding behavior pattern in G. groenlandica. The larvae may undergo voluntary hypothermia in order to avoid an energy, deficit resulting from high maintenance metabolism during mid-season when the energy content and food quality declines. The restriction of growth and development to a very short period prior to mid-summer may have contributed, to the extended 14-year life cycle of this species.     

Scaling of nectar foraging in orchid bees

Morphology influences the rate at which foraging bees visit nectar flowers, the quantity of nectar they must consume to fuel their activities, and, consequently, the profitability of flower species. Because feeding time is a major determinant of visitation rate, I used a biomechanical model to examine how energy intake rate (E) varies with sucrose concentration, body mass (M), and proboscis length in orchid bees (Apidae: Euglossini). Under geometric scaling, the optimal sugar concentration (Smax) should be largely independent of body size, and E proportional to M1.0. In a comparative study of 30 orchid bee species ranging from 50 to 800 mg, Smax fell between 35% and 40% w/w, but E proportional to M0.54, significantly less than model predictions. Proboscis length and radius scale geometrically with body mass, but proboscis length exhibits substantial size-independent variation, particularly in small bees. One cost of a long proboscis is a reduction in both E and Smax in accordance with the scaling model. This finding highlights a difference between the lapping mechanism used by bumblebees and the suction mechanism used by orchid bees. A field study confirms that orchid bees harvest nectars with between 34% and 42% sucrose, independent of body size.