Nectar robbing

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Bombus terrestris stealing nectar Bumblebee October 2007-3a.jpg
Bombus terrestris stealing nectar

Nectar robbing is a foraging behavior used by some organisms that feed on floral nectar, carried out by feeding from holes bitten in flowers, rather than by entering through the flowers' natural openings. Nectar robbers usually feed in this way, avoiding contact with the floral reproductive structures, and therefore do not facilitate plant reproduction via pollination. Because many species that act as pollinators also act as nectar robbers, nectar robbing is considered to be a form of exploitation of plant-pollinator mutualism. While there is variation in the dependency on nectar for robber species, most species rob facultatively (that is, to supplement their diets, rather than as an absolute necessity).

Contents

Nectar robbers vary greatly in species diversity and include species of carpenter bees, bumblebees, stingless Trigona bees, solitary bees, wasps, ants, hummingbirds, and some passerine birds, including flowerpiercers. [1] Nectar-robbing mammals include the fruit bat [2] and Swinhoe's striped squirrel, which rob nectar from the ginger plant. [3]

History

Records of nectar robbing in nature date back at least to 1793, when German naturalist Christian Konrad Sprengel observed bumblebees perforating flowers. [4] This was recorded in his book, The Secret of Nature in the Form and Fertilization of Flowers Discovered, which was written in Berlin. Charles Darwin observed bumblebees stealing nectar from flowers in 1859. [4] These observations were published in his book The Origin of Species.

Forms of floral larceny

Nectar robbing is specifically the behavior of consuming nectar from a perforation (robbing hole) in the floral tissue rather than from the floral opening. There are two main types of nectar robbing: primary robbing, which requires that the nectar forager perforate the floral tissues itself, and secondary robbing, which is foraging from a robbing hole created by a primary robber. [5]

The former is performed most often on flowers whose nectar is concealed or hard to reach. For instance, long flowers with tubular corollas are prone to robbing. Secondary robbers often do not have suitable mouth parts to be able to create penetrations into the flowers themselves, nor to reach the nectar without robbing it. Thus they take advantage of the perforations already made by other organisms to be able to steal the nectar. For example, short-tongued bees such as the early bumblebee (Bombus pratorum) are unable to reach the nectar located at the base of long flowers such as comfreys. In order to access the nectar, the bee will enter the flower through a hole bitten at the base, stealing the nectar without aiding in pollination. Birds are mostly primary robbers and typically use their beaks to penetrate the corolla tissue of flower petals. The upper mandible is used to hold the flower while the lower mandible creates the hole and extracts the nectar. While this is the most common method employed by bird species, some steal nectar in a more aggressive manner. For example, bullfinches reach the nectar by completely tearing the corolla off from the calyx. Mammal robbers such as the striped squirrel chew holes at the base of the flower and then consume the nectar. [6]

The term "floral larceny" has been proposed to include the entire suite of foraging behaviors for floral rewards that can potentially disrupt pollination. [7] They include "nectar theft" (floral visits that remove nectar from the floral opening without pollinating the flower), and "base working" (removing nectar from in between petals, which generally bypasses floral reproductive structures). [5] Individual organisms may exhibit mixed behaviors, combining legitimate pollination and nectar robbing, or primary and secondary robbing. Nectar robbing rates can also greatly vary temporally and spatially. The abundance of nectar robbing can fluctuate based on the season or even within a season. This inconsistency displayed in nectar robbing makes it difficult to label certain species as "thieves" and complicates research on the ecological phenomenon of nectar robbing. [8]

Effects on plant fitness

Bumble bee biting.JPG
Biting open the base of a flower...
Bumble bee feeding.JPG
...and using its tongue to drink the nectar.
A bumblebee "nectar robbing" a flower

Pollination systems are mostly mutualistic, meaning that the plant benefits from the pollinator's transport of male gametes and the pollinator benefits from a reward, such as pollen or nectar. [1] As nectar robbers receive the rewards without direct contact with the reproductive parts of the flower, their behaviour is easily assumed to be cheating. However, the effect of robbery on the plant is sometimes neutral or even positive. [1] [9] [10] [11] For example, the proboscis of Eurybia elvina does not come in contact with the reproductive parts of the flower in Calathea ovandensis, but this does not lead to significant reduction in fruit-set of the plant. [12] In another example, when 80 percent of the flowers in a study site were robbed and the robbers did not pollinate, neither the seed nor fruit set were negatively affected. [13]

The effect of floral-nectar robbing on plant fitness depends on several issues. Firstly, nectar robbers, such as carpenter bees, bumble bees and some birds, can pollinate flowers. [1] Pollination may take place when the body of the robber contacts the reproductive parts of the plant while it robs, or during pollen collection which some bees practice in concert with nectar robbing. [1] [14] The impact of Trigona bees (e.g. Trigona ferricauda) on a plant is almost always negative, probably because their aggressive territorial behaviour effectively evicts legitimate pollinators. [15] Nectar robbers may change the behaviour of legitimate pollinators in other ways, such as by reducing the amount of nectar available. This may force pollinators to visit more flowers in their nectar foraging. The increased number of flowers visited and longer flight distances increase pollen flow and outcrossing, which is beneficial for the plant because it lessens inbreeding depression. [1] This requires a robber's not completely consuming all of a flower's nectar. When a robber consumes all of a flower's nectar, legitimate pollinators may avoid the flower, resulting in a negative effect on plant fitness. [1]

The response of different species of legitimate pollinators also varies. Some species, like the bumble bees Bombus appositus or B. occidentalis and many species of nectar-feeding birds can distinguish between robbed and unrobbed plants and minimize their energy cost of foraging by avoiding heavily robbed flowers. [14] [16] Pollinating birds may be better at this than insects, because of their higher sensory capability. [1] The ways that bees distinguish between robbed and unrobbed flowers have not been studied, but they have been thought to be related to the damage on petal tissue after robbery or changes in nectar quality. [14] Xylocopa sonorina steals nectar through a slit they make in the base of the petals. If nectar robbing severely reduces the success of legitimate pollinators they may be able to switch to other nectar sources. [1]

The functionality of flowers can be curtailed by nectar robbers that severely maim the flower by shortening their life span. Damaged flowers are less attractive and thus can lead to a decrease in visit frequency as pollinators practice avoidance of robbed flowers and favor intact flowers. Nectar robbers that diminish the volume of nectar in flowers may also leave behind their odor which causes a decrease in visitation frequency by legitimate pollinators. Nectar robbing can also cause plants to reallocate resources from reproduction and growth to replenishing the stolen nectar, which can be costly to produce for some plants. [17]

Nectar robbing, especially by birds, [18] can damage the reproductive parts of a flower and thus diminish the fitness of a plant. [10] In this case, the effect of robbery on a plant is direct. A good example of an indirect effect is the change in the behaviour of a legitimate pollinator, which either increases or decreases the fitness of a plant. There are both primary and secondary nectar robbers. [1] Secondary robbers are those that take advantage of the holes made by primary robbers. While most flies and bees are secondary robbers, some species, such as Bombylius major , act as primary robbers. [18]

The effect of robbing is positive if the robber also pollinates or increases the pollination by the legitimate pollinator, and negative if the robber damages the reproductive parts of a plant or reduces pollination success, either by competing with the legitimate pollinator or by lessening the attractiveness of the flower. [14] [19] Positive reproductive results may occur from nectar robbing if the robbers act as pollinators during the same or different visit. The holes created by primary robbers may attract more secondary robbers that commonly search for nectar and collect pollen from anthers during the same visit. Additionally, certain dense arrangements of flowers allow pollen to be transferred when robber birds pierce holes into flowers to access the nectar. Thus, plant reproduction can potentially be boosted from nectar robbing due to the increase in potential pollen vectors. [20] Distinguishing between a legitimate pollinator and a nectar robber can be difficult. [21]

Evolutionary implications

Vitorino 2016 fig1.png
Vitorino 2016 fig2.png
Female of a hummingbird, the horned sungem, robbing nectar from the plant Amphilophium elongatum (top), and hole used to obtain the nectar (bottom, red circle)

Pollination systems cause coevolution, as in the close relationships between figs and fig wasps as well as yuccas and yucca moths. [22] [23] If nectar robbers have an effect (direct or indirect) on a plant or pollinator fitness, they are part of the coevolution process. [1] Where nectar robbing is detrimental to the plant, a plant species might evolve to minimize the traits that attract the robbers or develop some type of protective mechanism to hinder them. [1] [7] Another option is to try to neutralize negative effects of nectar robbers. Nectar robbers are adapted for more efficient nectar robbing: for instance, hummingbirds and Diglossa flowerpiercers have serrated bills that are thought to aid them in incising flower tissue for nectar robbing. [24]

Nectar robbers may only get food in illegitimate ways because of the mismatch between the morphologies of their mouthparts and the floral structure; or they may rob nectar as a more energy-saving way to get nectar from flowers. [25]

It is not completely clear how pollination mutualisms persist in the presence of cheating nectar robbers. Nevertheless, as exploitation is not always harmful for the plant, the relationship may be able to endure some cheating. Mutualism may simply confer a higher payoff than nectar robbing. [21] Some studies have shown that nectar robbing does not have a significant negative effect on the reproductive success of both male and female plants. [20]

Defences in flowering plants

Even though there has not been much research on the defences evolved in plants against nectar robbers, the adaptations have been assumed not to rise from traits used in interactions between plants and herbivores (especially florivores). Some defences may have evolved through traits originally referred to pollination. Defences against nectar robbers have been thought to include toxins and secondary compounds, escape in time or space, physical barriers and indirect defences. [7]

Toxins and secondary compounds are likely to act as a defence against nectar robbing because they are often found in floral nectar or petal tissue. There is some evidence that secondary compounds in nectar only affect nectar robbers and not the pollinators. [7] One example is a plant called Catalpa speciosa which produces nectar containing iridoid glycosides that deter nectar-thieving ants but not legitimate bee pollinators. [26] Low sugar concentration in nectar may also deter nectar robbers without deterring pollinators because dilute nectar does not yield net energy profits for robbers. [7]

If robbers and pollinators forage at different times of day, plants may produce nectar according to the active period of a legitimate pollinator. [7] This is an example of a defence by escaping in time. Another way to use time in defence is to flower only for one day as a tropical shrub Pavonia dasypetala does to avoid the robbing Trigona bees. [15] Escaping in space refers to a situation in which plant avoids being robbed by growing in a certain location like next to a plant which is more attractive to the robbers. [7]

The last two methods of protection are physical barriers and indirect defence like symbionts. Tightly packed flowers and unfavourably sized corolla tubes, bract liquid moats and toughness of the corolla or sepal are barriers for some nectar robbers. A good example of an indirect defence is to attract symbiotic predators (like ants) by nectar or other rewards to scare away the robbers. [7]

The term 'resistance' refers to the plant's ability to live and reproduce in spite of nectar robbers. This may happen, for example, by compensating the lost nectar by producing more. With the help of defence and resistance, mutualisms can persist even in the presence of cheaters. [7]

Related Research Articles

<span class="mw-page-title-main">Pollinator</span> Animal that moves pollen from the male anther of a flower to the female stigma

A pollinator is an animal that moves pollen from the male anther of a flower to the female stigma of a flower. This helps to bring about fertilization of the ovules in the flower by the male gametes from the pollen grains.

<span class="mw-page-title-main">Coevolution</span> Two or more species influencing each others evolution

In biology, coevolution occurs when two or more species reciprocally affect each other's evolution through the process of natural selection. The term sometimes is used for two traits in the same species affecting each other's evolution, as well as gene-culture coevolution.

<span class="mw-page-title-main">Bumblebee</span> Genus of insect

A bumblebee is any of over 250 species in the genus Bombus, part of Apidae, one of the bee families. This genus is the only extant group in the tribe Bombini, though a few extinct related genera are known from fossils. They are found primarily in higher altitudes or latitudes in the Northern Hemisphere, although they are also found in South America, where a few lowland tropical species have been identified. European bumblebees have also been introduced to New Zealand and Tasmania. Female bumblebees can sting repeatedly, but generally ignore humans and other animals.

<span class="mw-page-title-main">Pollination</span> Biological process occurring in plants

Pollination is the transfer of pollen from an anther of a plant to the stigma of a plant, later enabling fertilisation and the production of seeds. Pollinating agents can be animals such as insects, for example beetles or butterflies; birds, and bats; water; wind; and even plants themselves. Pollinating animals travel from plant to plant carrying pollen on their bodies in a vital interaction that allows the transfer of genetic material critical to the reproductive system of most flowering plants. When self-pollination occurs within a closed flower. Pollination often occurs within a species. When pollination occurs between species, it can produce hybrid offspring in nature and in plant breeding work.

<span class="mw-page-title-main">Entomophily</span> Form of pollination by insects

Entomophily or insect pollination is a form of pollination whereby pollen of plants, especially but not only of flowering plants, is distributed by insects. Flowers pollinated by insects typically advertise themselves with bright colours, sometimes with conspicuous patterns leading to rewards of pollen and nectar; they may also have an attractive scent which in some cases mimics insect pheromones. Insect pollinators such as bees have adaptations for their role, such as lapping or sucking mouthparts to take in nectar, and in some species also pollen baskets on their hind legs. This required the coevolution of insects and flowering plants in the development of pollination behaviour by the insects and pollination mechanisms by the flowers, benefiting both groups. Both the size and the density of a population are known to affect pollination and subsequent reproductive performance.

<span class="mw-page-title-main">Zoophily</span> Pollination by animals

Zoophily, or zoogamy, is a form of pollination whereby pollen is transferred by animals, usually by invertebrates but in some cases vertebrates, particularly birds and bats, but also by other animals. Zoophilous species frequently have evolved mechanisms to make themselves more appealing to the particular type of pollinator, e.g. brightly colored or scented flowers, nectar, and appealing shapes and patterns. These plant-animal relationships are often mutually beneficial because of the food source provided in exchange for pollination.

<span class="mw-page-title-main">Nectar</span> Sugar-rich liquid produced by many flowering plants, that attracts pollinators and insects

Nectar is a viscous, sugar-rich liquid produced by plants in glands called nectaries, either within the flowers with which it attracts pollinating animals, or by extrafloral nectaries, which provide a nutrient source to animal mutualists, which in turn provide herbivore protection. Common nectar-consuming pollinators include mosquitoes, hoverflies, wasps, bees, butterflies and moths, hummingbirds, honeyeaters and bats. Nectar plays a crucial role in the foraging economics and evolution of nectar-eating species; for example, nectar foraging behavior is largely responsible for the divergent evolution of the African honey bee, A. m. scutellata and the western honey bee.

<span class="mw-page-title-main">Nectarivore</span> Animal in which nectar is a main source of nutrition in their diet

In zoology, a nectarivore is an animal which derives its energy and nutrient requirements from a diet consisting mainly or exclusively of the sugar-rich nectar produced by flowering plants.

<span class="mw-page-title-main">Ornithophily</span> Pollination by birds

Ornithophily or bird pollination is the pollination of flowering plants by birds. This sometimes coevolutionary association is derived from insect pollination (entomophily) and is particularly well developed in some parts of the world, especially in the tropics, Southern Africa, and on some island chains. The association involves several distinctive plant adaptations forming a "pollination syndrome". The plants typically have colourful, often red, flowers with long tubular structures holding ample nectar and orientations of the stamen and stigma that ensure contact with the pollinator. Birds involved in ornithophily tend to be specialist nectarivores with brushy tongues and long bills, that are either capable of hovering flight or light enough to perch on the flower structures.

<i>Habropoda laboriosa</i> Species of bee

Habropoda laboriosa, the southeastern blueberry bee, is a bee in the family Apidae. It is native to the eastern United States. It is regarded as the most efficient pollinator of southern rabbiteye blueberries, because the flowers require buzz pollination, and H. laboriosa is one of the few bees that exhibit this behavior. It is active for only a few weeks of the year, while the blueberries are in flower during early spring, when the temperature is warm and humid. H. laboriosa are solitary bees that live alone but nest in close proximity with other nests of their species. They have similar features to bumble bees, but they are smaller in size compared to them. H. laboriosa are arthropods so they have segmented bodies that are composed of the head, thorax, and abdomen.

<span class="mw-page-title-main">Palynivore</span> Group of herbivorous animals

In zoology, a palynivore /pəˈlɪnəvɔːɹ/, meaning "pollen eater" is an herbivorous animal which selectively eats the nutrient-rich pollen produced by angiosperms and gymnosperms. Most true palynivores are insects or mites. The category in its strictest application includes most bees, and a few kinds of wasps, as pollen is often the only solid food consumed by all life stages in these insects. However, the category can be extended to include more diverse species. For example, palynivorous mites and thrips typically feed on the liquid content of the pollen grains without actually consuming the exine, or the solid portion of the grain. Additionally, the list is expanded greatly if one takes into consideration species where either the larval or adult stage feeds on pollen, but not both. There are other wasps which are in this category, as well as many beetles, flies, butterflies, and moths. One such example of a bee species that only consumes pollen in its larval stage is the Apis mellifera carnica. There is a vast array of insects that will feed opportunistically on pollen, as will various birds, orb-weaving spiders and other nectarivores.

<span class="mw-page-title-main">Pollination syndrome</span> Flower traits that attract pollinators

Pollination syndromes are suites of flower traits that have evolved in response to natural selection imposed by different pollen vectors, which can be abiotic or biotic, such as birds, bees, flies, and so forth through a process called pollinator-mediated selection. These traits include flower shape, size, colour, odour, reward type and amount, nectar composition, timing of flowering, etc. For example, tubular red flowers with copious nectar often attract birds; foul smelling flowers attract carrion flies or beetles, etc.

<span class="mw-page-title-main">Trap-lining</span> Feeding strategy amongst certain families of birds

In ethology and behavioral ecology, trap-lining or traplining is a feeding strategy in which an individual visits food sources on a regular, repeatable sequence, much as trappers check their lines of traps. Traplining is usually seen in species foraging for floral resources. This involves a specified route in which the individual traverses in the same order repeatedly to check specific plants for flowers that hold nectar, even over long distances. Trap-lining has been described in several taxa, including bees, butterflies, tamarins, bats, rats, and hummingbirds and tropical fruit-eating mammals such as opossums, capuchins and kinkajous. Traplining is used to term the method in which bumblebees and hummingbirds go about collecting nectar, and consequently, pollinating each plant they visit. The term "traplining" was originally coined by Daniel Janzen, although the concept was discussed by Charles Darwin and Nikolaas Tinbergen.

<span class="mw-page-title-main">Flower constancy</span> Tendency to visit certain flower species

Flower constancy or pollinator constancy is the tendency of individual pollinators to exclusively visit certain flower species or morphs within a species, bypassing other available flower species that could potentially contain more nectar. This type of foraging behavior puts selective pressures on floral traits in a process called pollinator-mediated selection. Flower constancy is different from other types of insect specialization such as innate preferences for certain colors or flower types, or the tendency of pollinators to visit the most rewarding and abundant flowers.

Two-spotted bumble bee Species of bee

The two-spotted bumble bee is a species of social bumble bee found in the eastern half of the United States and the adjacent south-eastern part of Canada. In older literature this bee is often referred to as Bremus bimaculatus, Bremus being a synonym for Bombus. The bee's common name comes from the two yellow spots on its abdomen. Unlike many of the other species of bee in the genus Bombus,B. bimaculatus is not on the decline, but instead is very stable. They are abundant pollinators that forage at a variety of plants.

<i>Xylocopa pubescens</i> Species of carpenter bee

Xylocopa pubescens is a species of large carpenter bee. Females form nests by excavation with their mandibles, often in dead or soft wood. X. pubescens is commonly found in areas extending from India to Northeast and West Africa. It must reside in these warm climates because it requires a minimum ambient temperature of 18 °C (64 °F) in order to forage.

<i>Trigona fuscipennis</i> Species of bee

Trigona fuscipennis is a stingless bee species that originates in Mexico but is also found in Central and South America. They are an advanced eusocial group of bees and play a key role as pollinators in wet rainforests. The species has many common names, including mapaitero, sanharó, abelha-brava, xnuk, k'uris-kab, enreda, corta-cabelo, currunchos, zagaño, and enredapelos.

<span class="mw-page-title-main">Pollen theft</span> Net removal of pollen by an animal

Pollen theft, also known as pollen robbery or floral larceny, occurs when an animal actively eats or collects pollen from a plant species but provides little or no pollination in return. Pollen theft was named as a concept at least as early as the 1980, and examples have been documented well before that. For example, native honey bees were documented 'stealing' large amounts of pollen from the large, bat-pollinated flowers of Parkia clappertoniana in Ghana in the 1950s. Nevertheless, pollen theft has typically received far less research attention than nectar robbing, despite the more direct consequences on plant reproduction.

<span class="mw-page-title-main">UV coloration in flowers</span> Natural phenomenon

UV coloration is a natural phenomenon that leads to unique interactions between organisms that have evolved the ability to perceive these wavelengths of light. It serves as one method to attract pollinators to the flower along with scent, shape, and nectar quality. Flowers are known for their range of visible colors that humans can see with their eyes and observe an array of different shades and patterns. The naked eye cannot see the ultraviolet coloration many flowers employ to bring attention to themselves. By either reflecting or absorbing UV light waves, flowers are able to communicate with pollinators. This allows plants that may require an animal pollinator to stand out from other flowers or distinguish where their flowers are in a muddied background of other plant parts. For the plant, it is important to share and receive pollen so they can reproduce, maintain their ecological role, and guide the evolutionary history of the population.

<i>Chalepogenus</i> Genus of bees

The genus Chalepogenus, consisting of 21 species of solitary oil-collecting apid bees, demonstrates oligolecty by foraging on oil-producing flowers from the families Calceolariaceae, Iridaceae and Solanaceae. These oil-flowers are abundant in South America, where Chalepogenus is endemic. In contrast to honey bees, Chalepogenus species do not collect nectar; instead, they gather floral oil for various purposes, including provisioning their larvae, constructing nests, and sustaining foraging adult bees. Although oil collection has been reported to be performed by females only, both males and females have specialised oil-collecting structures.

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  22. ↑ Pellmyr O.; Thompson J.N.; Brown J.M.; Harrison R.G. (1996). "Evolution of pollination and mutualism in the yucca moth lineage". American Naturalist. 148 (5): 827–847. doi:10.1086/285958. S2CID   84816447.
  23. ↑ Anstett, M.C.; Hossaert, McKey M.; Kjellberg, F. (1997). "Figs and fig pollinators: Evolutionary conflicts in a coevolved mutualism". Trends in Ecology and Evolution. 12 (3): 94–99. doi:10.1016/s0169-5347(96)10064-1. PMID   21237991.
  24. ↑ Ornelas, J. F. (1994). "Serrate tomia: An adaptation for nectar robbing in hummingbirds?". The Auk. 111 (3): 703–713.
  25. ↑ Zhang Y.; Wang Y.; Guo Y. (2006). "The effects of nectar robbing on plant reproduction and evolution". Zhiwu Shengtai Xuebao. 30 (4): 695–702.
  26. ↑ Stephenson, A. G. (1981). "Toxic nectar deters nectar thieves of Catalpa speciosa". American Midland Naturalist. 105 (2): 381–383. doi:10.2307/2424757. JSTOR   2424757.
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