Secondary Nectar Research Articles

FIRST REPORT OF NECTAR ROBBING BY SWORD-BILLED HUMMINGBIRDS ENSIFERA ENSIFERA

A growing number of hummingbird species are known to practice nectar robbing. Hummingbirds that rob nectar tend to have short bills and to rob flowers with long, tubular corollas that prevent the birds from accessing nectar through its openings. We document that Sword-billed Hummingbirds Ensifera ensifera, which have the longest bills of any hummingbird species, are secondary nectar robbers on flowers of the red angel’s trumpet Brugmansia sanguinea, which have long tubular corollas and are regularly pollinated by Sword-billed Hummingbirds. When obtaining nectar through the floral opening of B. sanguinea, Sword-billed Hummingbirds' heads may be completely enveloped by the flower, severely limiting their vision. Sword-billed Hummingbirds might be at a lower risk of predation when they rob nectar than when they insert their heads into the floral opening. Thus, nectar robbing in this species might function to reduce predation risk, although we have no data to support this speculation.

Foraging Behavior of Two Pollen Wasp Species of the Genus Celonites Latreille, 1802 (Hymenoptera: Vespidae: Masarinae), from the Altai Mountains.

Celonites kozlovi Kostylev, 1935, and C. sibiricus Gusenleitner, 2007, coexist in semi-deserts of the Altai Mountains. The trophic relationships of these pollen wasp species to flowers are largely unknown. We observed the flower visits and behaviors of wasps on flowers; pollen-collecting structures of females were studied using SEM; the taxonomic position of these two species was ascertained with the barcoding sequence of the mitochondrial COI-5P gene. Celonites kozlovi and C. sibiricus form a clade together with C. hellenicus Gusenleitner, 1997, and C. iranus Gusenleitner, 2018, within the subgenus Eucelonites Richards, 1962. Celonites kozlovi is polylectic in the narrow sense, collecting pollen from flowers of plants belonging to five families (with the predomination of Asteraceae and Lamiaceae) using diverse methods for both pollen and nectar uptake. In addition, this species is a secondary nectar robber, which has not been observed in pollen wasps before. The generalistic foraging strategy of C. kozlovi is correlated with an unspecialized pollen-collecting apparatus on the fore-tarsi. In contrast, C. sibiricus is broadly oligolectic, predominantly collecting pollen from flowers of Lamiaceae. Its specialized foraging strategy is associated with apomorphic behavioral and morphological traits, particularly specialized pollen-collecting setae on the frons, which enable indirect pollen uptake using nototribic anthers. These adaptations in C. sibiricus evolved independently of similar specializations in the Celonites abbreviatus-complex. Celonites kozlovi is re-described, and males are described for the first time.

SECONDARY NECTAR ROBBING BY A VOLCANO HUMMINGBIRD (SELASPHORUS FLAMMULA)

Secondary nectar robbing is poorly studied in hummingbirds. Here, we provide an updated list of hummingbird species reported to be secondary nectar robbers and give the first detailed account of secondary nectar robbing by a Volcano Hummingbird (Selasphorus flammula) that obtained nectar through holes made by a Slaty Flowerpiercer (Diglossa plumbea) in two species of plants with long tubular flowers.

Secondary nectar robbing by Lycaenidae and Riodinidae: Opportunistic but not infrequent.

Secondary nectar robbing by Lycaenidae and Riodinidae: Opportunistic but not infrequent.

Are native nectar robbers against the alien? Effects of floral larceny on the reproductive success of the invasive yellow bells (Tecoma stans, Bignoniaceae)

Floral larceny is expected to impact negatively the female fitness of alien plant species; however, the effects of nectar robbers are context-dependent and sometimes neutral. In this study, the effect of nectar robbers on the female fitness of the ornamental and invasive yellow bells, Tecoma stans (L.) Juss. ex Kunth (Bignoniaceae), was tested in two typical exotic habitats in northeastern Brazil: urban area and rural land. In order to quantify the intensity of floral larceny and identify the flower-visiting insects on T. stans, we sampled robbery in pre-anthesis flowers, and the frequency of illegitimate and legitimate visits in both sites. We also described the nectar-secreting pattern, and conducted experiments to test the effect of nectar robbing on plant female fitness. Our results indicated that nectar robbers provided neutral rather than negative impact on fruit and number of seeds in T. stans, mediated by the continuous nectar secretion and low natural fruit set. The populations of both habitats differed in the intensity of nectar robbing and pollinator activity. The main nectar robbers were stingless bees (Meliponini, Apidae) and carpenter bees (Xylocopini, Apidae). We found a higher predominance of primary and secondary nectar robbers in the urban area than in the rural environment. In addition, urban T. stans faced up to higher resource theft (nectar and pollen) and lower fruit set. This pattern may not be controlled by nectar production since the secretion pattern was similar between habitats. Nevertheless, T. stans may spread throughout rural environments with more opportunity to interact with pollinators, instead of nectar robbers.

Nectar robbing in bellflower (Sesamum radiatum) benefited pollinators but unaffected maternal function of plant reproduction

Nectar robbing – foraging nectar illegitimately – has negative, neutral, or positive effects on maternal function of plant reproduction and/or on pollinators. It has been suggested that nectar robbing has a non-negative effect on maternal function of plant reproduction in autogamous and mixed breeding plants; however this hypothesis requires deeper understanding with more studies. We investigated the impact of natural nectar robbing on maternal function of plant reproduction and visitation characteristics of pollinators in Sesamum radiatum, an autogamous plant. Pollinators were observed on unrobbed open flowers and robbed open flowers. In robbed flowers, pollinators’ visit type and foraging time were examined. The seed sets of these flower types were examined. Xylocopa latipes was both a primary robber and a legitimate pollinator, X. bryorum was an exclusive primary robber, and Megachile disjuncta was a cosmopolitan pollinator. In robbed flowers, most of the pollinators foraged mostly as secondary nectar robbers. The foraging time shortened considerably when pollinators robbed nectar – a positive effect on pollinators’ foraging efficiency. Robbing did not negatively affect seed set – a neutral effect on the plant’s reproduction. Our study agrees that nectar robbing might have a non-negative effect on reproduction in autogamous and mixed breeding plants.

Structure of floral nectaries and comparison of reproductive and vestigial organs in the staminate and pistillate flowers of dioeciousSilene latifolia(Caryophyllaceae)

Silene latifolia Poiret of Eurasia has established in North America, prompting this structural study of its mature unisexual buds and flowers. Floral nectaries, anther and stigma changes, and vestigial reproductive structures were studied using light and scanning electron microscopy. In staminate flowers, anthers dehisced before anthesis and >90% of their pollen was liberated within 36 h. Accumulated in the tubular calyx, nectar descended an anthophore from the stomatal-bearing nectary at the stamen bases. Nectary tissue surrounded the pistillode, a central filamentous organ lacking ovules but tipped by hairs resembling stigmatic papillae. In pistillate flowers, nectar flowed into an inflated calyx. The annular nectary had 10 regularly spaced, stomatal-lined craters and was continuous with the adaxial surfaces of the infertile antisepalous and epipetalous staminodes. Key elements of entomophilous pollination leading to successful sexual reproduction of this invasive species include secondary nectar presentation from disparate floral nectaries that, for pistillate flowers, also incorporate the staminodes; rapid pollen release from anthers; and elongation of papillae by tip growth that enhances each stigma’s receptive surface. Context is also provided for future studies of floral nectary development in this model dioecious species.

Ant-Mediated Nectar Robbing from the Chilean Firetree Embothrium coccineum (Proteaceae): No Effect on Seed Production

Nectar robbing by the ant Camponotus distinguendus was observed in flowers of Embothrium coccineum (Proteaceae), a tree mainly pollinated by hummingbirds. We hypothesized that robbing would reduce the amount of nectar, affecting the foraging behaviour of floral visitors and reducing seed production. Nectar robbing affected one-third of mature tree blossoms and 93.3% of trees. This reduced the amount of nectar to about half. Foraging behaviour of floral visitors included pollinating visits to consume nectar and pollen, primary and secondary nectar robbing, and nectar theft. We found no effect of nectar robbing by C. distinguendus on seed production in E. coccineum, which was sparse and completely dependent on legitimate pollinator visits, mostly performed by the green-backed firecrown Sephanoides sephaniodes. Determining the effects of nectar robbing by ants on the reproduction of plants is important to understand the dynamics of plant-animal interactions in the temperate forests of Chile.

Legitimate visitors and nectar robbers of Aquilegia formosa have different effects on nectar bacterial communities

AbstractMetacommunity structure is strongly influenced by dispersal between habitat patches. Dispersal mode (e.g., active or passively via vector, wind, or water) is recognized to influence metacommunity dynamics, but it is not well understood how within‐mode heterogeneity impacts dispersal and community assembly, particularly for microbial communities. Microbes often rely on flower visitors for dispersal among short‐lived floral nectar habitats, but it is unclear whether flower visitor guilds (e.g., legitimate visitors vs. larcenists) differentially influence nectar microbial diversity and community structure. We surveyed the community of legitimate nectar foragers and nectar robbers, which damage flowers to obtain floral rewards, of Aquilegia formosa. Then, we evaluated how manipulating access by legitimate nectar foragers, primary nectar robbers, and/or secondary nectar robbers influenced the diversity, species composition, and beta diversity of nectar bacteria within individual flowers. A taxonomically diverse insect community visited A. formosa, and visitors differentially influenced nectar bacterial community structure at within‐flower (local) and among‐flower (regional) scales. When legitimate nectar foragers were allowed to access A. formosa, we observed an increase in bacterial diversity and changes in bacterial species composition such that common nectar bacteria had higher relative abundances. In contrast, effects of natural and simulated robbing had little effect on bacterial alpha diversity, but simulated robbing decreased the relative abundance of common nectar bacteria, and natural nectar robbing events reduced beta diversity of nectar bacteria. This work highlights the importance of visitor identity on microbial diversity and species composition in flowers, and, more broadly, suggests that vectors can differentially influence metacommunity structure.

Micromorphological and histochemical attributes of flowers and floral reward in Linaria vulgaris (Plantaginaceae)

The self-incompatible flowers of Linaria vulgaris have developed a range of mechanisms for attraction of insect visitors/pollinators and deterrence of ineffective pollinators and herbivores. These adaptive traits include the flower size and symmetry, the presence of a spur as a “secondary nectar presenter,” olfactory (secondary metabolites) and sensual (scent, flower color, nectar guide—contrasting palate) signals, and floral rewards, i.e. pollen and nectar. Histochemical tests revealed that the floral glandular trichomes produced essential oils and flavonoids, and pollen grains contained flavonoids, terpenoids, and steroids, which play a role of olfactory attractants/repellents. The nectary gland is disc-shaped and located at the base of the ovary. Nectar is secreted through numerous modified stomata. Nectar secretion began in the bud stage and lasted to the end of anthesis. The amount of produced nectar depended on the flower age and ranged from 0.21 to 3.95 mg/flower (mean = 1.51 mg). The concentration of sugars in the nectar reached up to 57.0%. Both the nectar amount and sugar concentration demonstrated a significant year and population effect. Pollen production was variable between the years of the study. On average, a single flower of L. vulgaris produced 0.31 mg of pollen. The spectrum of insect visitors in the flowers of L. vulgaris differed significantly between populations. In the urban site, Bombus terrestris and Apis mellifera were the most common visitors, while a considerable number of visits of wasps and syrphid flies were noted in the rural site.

Consequences of secondary nectar robbing for male components of plant reproduction.

Organisms engage in multiple species interactions simultaneously. While pollination studies generally focus on plants and pollinators exclusively, secondary robbing, a behavior that requires other species (primary robbers) to first create access holes in corollas, is common. It has been shown that secondary robbing can reduce plants' female fitness; however, we lack knowledge about its impact on male plant fitness. We experimentally simulated primary and secondary robbing in the monocarpic perennial Ipomopsis aggregata (Polemoniaceae), quantifying indirect effects on pollinator-mediated pollen (dye) donation. We also assessed whether continual nectar removal via the floral opening has similar effects on hummingbird-pollinator behavior as continual secondary robbing through robber holes. We found no significant indirect effects of secondary robbing on a component of Ipomopsis male fitness. Although robbing did reduce pollen (dye) donation due to avoidance of robbed plants by pollinating hummingbirds, pollen donation did not differ between the two robbing treatments. The effects of secondary robbing on hummingbird behavior resembled effects of chronic nectar removal by pollinators. Our results indicate that hummingbird pollinators may use a combination of cues, including cues given by the presence or absence of nectar, to make foraging decisions. Combined with prior research, this study suggests that secondary robbing is less costly to a component of male fitness than to female fitness in Ipomopsis, broadening our knowledge of the overall costs of mutualism exploitation to total plant fitness.

Foraging strategy predicts foraging economy in a facultative secondary nectar robber

In mutualistic interactions, the decision whether to cooperate or cheat depends on the relative costs and benefits of each strategy. In pollination mutualisms, secondary nectar robbing is a facultative behavior employed by a diverse array of nectar‐feeding organisms, and is thought to be a form of cheating. Primary robbers create holes in floral tissue through which they feed on nectar, whereas secondary robbers, which often lack chewing mouthparts, feed on nectar through existing holes. Because primary robbers make nectar more readily available to secondary robbers, primary robbers facilitate the behaviors of secondary robbers. However, the net effect of facilitation on secondary robber fitness has not been empirically tested: it is unknown whether the benefit secondary robbers receive is strong enough to overcome the cost of competing with primary robbers for a shared resource. We conducted foraging experiments using the bumble bee Bombus bifarius, which can alternatively forage ‘legitimately’ (from the floral opening) or secondary‐rob. We measured the relative foraging efficiencies (handling time per flower, flowers visited per minute, proportion of foraging bout spent consuming nectar) of these alternative behaviors, and tested whether the frequency of primary robbing and nectar standing crop in primary‐robbed flowers of Linaria vulgaris (Plantaginaceae) affected foraging efficiency. Surprisingly, there was no effect of primary robbing frequency on the foraging efficiency of secondary‐robbing B. bifarius. Instead, foraging strategy was a major predictor of foraging efficiency, with legitimate foraging being significantly more efficient than secondary robbing. Legitimate foraging was the more common strategy used by B. bifarius in our study; however, it is rarely used by B. bifarius foraging on L. vulgaris in nature, despite indications that it is more efficient. Our results suggest the need for deeper investigations into why bees adopt secondary robbing as a foraging strategy, specifically, the environmental contexts that promote the behavior.

Facilitated exploitation of pollination mutualisms: fitness consequences for plants

Summary Mutualisms are only rarely one‐to‐one interactions: each species generally interacts with multiple mutualists. Exploitation is ubiquitous in mutualisms, and we would therefore expect that each mutualist interacts with multiple exploiters as well. Exploiter species may also interact with one another. For example, the action of one exploiter species might open the opportunity for exploitation by a second species. Exploitation is common in many plant–pollinator mutualisms: ‘primary’ nectar robbers feed through holes they make in flowers, which can be subsequently used by ‘secondary’ nectar robbers unable to create holes themselves. The overall effect of nectar robbing on plant fitness is often (although not always) negative. No study has separated the effects of interacting with primary vs. secondary robbers. Here, we examine the effects of primary vs. secondary nectar robbing on pollinator visitation rate and female fitness in Ipomopsis aggregata. Manipulating the type of nectar robbing that flowers experienced, we found that secondary nectar robbing inflicted fitness costs to plants beyond that inflicted by primary robbing alone. Secondary nectar robbing significantly reduced pollen receipt to flowers, as well as fruit and seed production. Although the causes are elusive, the effect may be attributed to changes in pollinator behaviour at these plants. Synthesis. Our findings provide evidence that interacting with multiple exploiters can lead to increased negative effects for mutualists, and highlight the importance of incorporating multiple exploiters into the conceptual framework of mutualism.

Spatio-temporal variation of nectar robbing in Salvia gesneriflora and its effects on nectar production and legitimate visitors.

Nectar robbing occurs when floral visitors remove floral nectar through floral damage and usually without providing pollination in return. Even though nectar robbing may have negative, neutral or even positive effects on plant fitness, few studies have investigated temporal and spatial variation in robbing rate and their consequences, particularly in the tropics. In this study, robbing levels were estimated during 3 years in four populations of Salvia gesneriflora, a hummingbird-pollinated shrub endemic to central Mexico that is mainly robbed by birds, carpenter bees and bumblebees. The effect of robbing on nectar availability, flower longevity and on visitation rate by floral visitors was also evaluated. Our results indicate great variation in robbing levels across years and populations and a positive relationship between robbing level and flower abundance per population. Moreover, our results show that nectar availability is about eight times higher in unrobbed flowers than in robbed flowers, and that nectar robbers prefer younger flowers, although lifespan of robbed and unrobbed flowers did not differ statistically. Primary and secondary nectar robbers showed a higher visitation rate compared to legitimate visitors, and neither legitimate nor illegitimate floral visitors seem to discriminate between robbed and unrobbed flowers. These results suggest that robbers may respond to food availability and that no floral visitors apparently could differentiate between robbed and unrobbed flowers. Finally, results show that nectar robbers prefer the youngest flowers, which suggests that strong competition for access to nectar between pollinators and robbers might occur, mainly at the first stages of the flowers.

So many visitors and so few pollinators: variation in insect frequency and effectiveness governs the reproductive success of an endemic milkwort

Plant–pollinator interactions are one of the most important and variable mutualisms having major implications for plant fitness. The present study evaluates the interactions between an endemic milkwort, Polygala vayredae, and its floral visitors by studying the temporal variability, foraging behaviour and effectiveness of floral visitors in three populations during three consecutive years. The flowers were visited by a diverse array of insects, totalling 24 different species. However, only four species were effective pollinators, depositing pollen on stigmas after one visit, while the remaining species behaved as nectar robbers, secondary nectar robbers or nectar thieves and were completely ineffective for pollination. Among the effective pollinators, two groups with distinct foraging behaviours were observed: the nectar collecting long-tongued bees Bombus pascuorum and Anthophora sp. and the pollen collectors Eucera longicornis and Halictus sp. No significant differences were observed among pollinators in their efficiency in pollen deposition on stigmas, but significant differences were observed in the foraging behaviour between nectarivorous and pollen collectors. Variation in the abundance and assemblage of floral visitors was observed at the temporal scale and among populations, with the effective pollinators being generally scarce. Consequently, the reproductive outcome in this species was low and significantly variable among populations and years. The results highlight the importance of studying floral visitor effectiveness when determining pollinator assemblages.

Community‐dependent foraging habits of flower visitors: cascading indirect interactions among five bumble bee species

AbstractDespite the ubiquity and the importance of interspecific interactions among flower visitors, few studies have examined their effects on the realized feeding niches of visitor species in a community context. To evaluate the community‐wide effects of interactions among flower visitors, I have examined changes in the flower utilization patterns of each visitor species at several sites where the component of the visitor's community differed. Specifically, I compared the flower preferences and foraging habits (legitimate foraging vs. primary nectar robbing vs. secondary nectar robbing) of five bumble bee species in flower patches consisting of Trifolium pratense L. (red clover) and T. repens L. (white clover) on Hokkaido Island, Japan. I also examined the nectar production and standing crops of each flower species to evaluate the exploitation competition based on nectar. The bumble bee species exhibited different flower utilization patterns among sites. At sites where the long‐tongued Bombus diversus tersatus was common and the exotic short‐tongued B. terrestris was rare, B. diversus tersatus visited red clover (long‐tubed flowers) exclusively, whereas medium‐tongued B. pseudobaicalensis and short‐tongued B. hypocrita sapporoensis and B. hypnorum koropokkrus preferentially visited white clover (short‐tubed flowers). Conversely, at sites where the long‐tongued bee was rare, four other species frequently visited red clover in different modes: B. pseudobaicalensis visited legitimately, B. hypocrita sapporoensis and B. terrestris visited as primary nectar robbers, and B. hypnorum koropokkrus visited as a secondary nectar robber. The presence or absence of resource exploitation by the long‐tongued species and the interaction between primary and secondary nectar robbers via robbing holes was the major ecological sources of these differences. Diverse effects of interactions among flower visitors played important roles in shaping pattern of plant and flower visitor interactions.

Effects of nectar robbing on pollinator behavior and plant reproductive success of Pitcairnia angustifolia (Bromeliaceae)

AbstractNectar robbers may have direct and indirect effects on plant reproductive success but the presence of nectar robbing is not proof of negative fitness effects. We combined census data and field experiments to disentangle the complex effects of nectar robbing on nectar production rates, pollinator behavior, pollen export, and female reproductive success of Pitcairnia angustifolia. Under natural conditions flowers were visited by four different animal species including a robber‐like pollinator and a secondary robber. Natural levels of nectar robbing ranged from 40 to 100%. Natural variation in nectar robbing was not associated with fruit set in any year whereas seed set was weakly positively associated for 1 year only. Artificial nectar robbing did not increase nectar production or concentration, did not affect the behavior of long‐billed hummingbirds, and when faced with artificially robbed flowers, these visitors behaved as secondary nectar robbers. The number of stigmas within a patch that received pollen dye analogs and the average distance traveled by these analogs were not significantly different between robbing treatments (robbed flowers versus unrobbed flowers), but the maximum distance traveled by these pollen analogs was higher when nectar robbing was not prevented. Overall, the proportion of robbed flowers on an inflorescence had a neutral effect to a weak positive effect on the reproduction of individual plants (i.e. positive association between nectar robbing and fruit set in 2002) even when it clearly changed the behavior of its most efficient pollinator potentially increasing the frequency of nectar robbing within a plant.

The structure of septal nectaries and nectar presentation in the flowers of Allium aflatunense B. Fedtsch.

The location and structure of the septal nectaries in the flowers of <i>Allium aflatunense</i> B. Fedtsch. were studied. Light and scanning electron microscopy were used for examination. It has been shown that the septal nectaries are located in the lower part of the ovary and in the gynophore on which the ovary is borne. Nectar is secreted through the single-layered epidermis surrounding three nectary slits and nectar release occurs through three openings located at the base of the gynophore, which are the outlets of the ducts connected to the nectary slits. The expanded and fused bases of the stamen filaments and the tepals participate in secondary nectar presentation. In the flowers of <i>Allium aflatunense</i>, numerous purple elements: tepals, filaments, style and pedicle, perform the role of a colour attractant. On the intensely green ovary, there occur glistening conical outgrowths of epidermal cells, which may also function as signal attractants.

The position and structure of the nectary in spring heath (Erica carnea L.) flowers

Ecological traits of <i>Erica carnea</i> L. flowers and the morphology of floral nectaries were investigated using stereoscopic, light and scanning electron microscopy. The nectary in the flowers of <i>Erica carnea</i> is located in the basal part of the ovary. It represents the gynoecial nectary type. It has the form of a yellow, ribbed ring with eight outgrowths, pointed towards the base, which alternately adjoin the stamen filaments. The height of the nectary is 400 µm and its thickness 200 - 250 µm. The parenchyma of the nectary is composed of 6 - 8 layers. Nectar secretion occurs through anomocytic stomata with a diameter of 17 µm. Guard cells are only found on the outgrowths of the nectary and they are situated most frequently at the level of other epidermal cells. During nectar secretion, a small degree of pore opening was observed. In the flowers of <i>Erica carnea</i>, secondary nectar presentation was found, with the nectar accumulating at the base of the fused corolla.

Age-Related Changes in Characteristics and Prey Capture of Seasonal Cohorts of Sarracenia alata Pitchers

Abstract The characteristics associated with prey attraction and capture in pitcher plants are not well understood. Because of physiological constraints due to growth patterns and resource availability, pitcher characteristics should vary among seasonal cohorts and with pitcher age. We measured age-related changes in characteristics (funnel diameter, extrafloral nectar guides, extrafloral nectar concentration) and in prey capture of early- and mid-season cohorts of Sarracenia alata pitchers. Pitchers achieved their mature height before opening, and pitchers of the mid-season cohort were smaller than those produced early in the growing season. In both cohorts, extrafloral nectar concentration on the lip of the pitcher and the number of “secondary nectar guides” (an indication of hood coloration) were highest approximately 3 wk after pitchers opened. The rate of insect capture in both cohorts was highest approximately 3 wk after pitchers opened, corresponding with the peak in nectar concentration and the ma...