Nectar robbing refers to the act by an animal, typically an insect or a bird, of removing nectar from a flowering plant

Flowering plant

The flowering plants , also known as Angiospermae or Magnoliophyta, are the most diverse group of land plants. Angiosperms are seed-producing plants like the gymnosperms and can be distinguished from the gymnosperms by a series of synapomorphies...

, most often by drilling a hole in the corolla. In this way animals without morphological

Morphology (biology)

In biology, morphology is a branch of bioscience dealing with the study of the form and structure of organisms and their specific structural features....

 adaptation

Adaptation

An adaptation in biology is a trait with a current functional role in the life history of an organism that is maintained and evolved by means of natural selection. An adaptation refers to both the current state of being adapted and to the dynamic evolutionary process that leads to the adaptation....

s required by the structure of the flower may access nectar. Without entering the flower, the animal may avoid touching the reproductive parts, and circumvent the mutualistic requirement of the plant-pollinator relationship. It has been suggested that flower visitors which neither damage nor pollinate the plant be called nectar thieves to distinguish them from nectar robbers. The term floral larcenist has been proposed to include both nectar robbers and nectar thieves .

Nectar robbers include certain species of carpenter bee

Carpenter bee

Carpenter bees are large, hairy bees distributed worldwide. There are some 500 species of carpenter bee in 31 subgenera...

s, bumblebee

Bumblebee

A bumble bee is any member of the bee genus Bombus, in the family Apidae. There are over 250 known species, existing primarily in the Northern Hemisphere although they are common in New Zealand and in the Australian state of Tasmania.Bumble bees are social insects that are characterised by black...

s, Trigona

Trigona (genus)

Trigona is the largest genus of stingless bees, formerly including many more subgenera than the present assemblage; many of these former subgenera have been elevated to generic status. There are approximately 150 species presently included in the genus, in 11 subgenera...

bees, ant

Ant

Ants are social insects of the family Formicidae and, along with the related wasps and bees, belong to the order Hymenoptera. Ants evolved from wasp-like ancestors in the mid-Cretaceous period between 110 and 130 million years ago and diversified after the rise of flowering plants. More than...

s, hummingbird

Hummingbird

Hummingbirds are birds that comprise the family Trochilidae. They are among the smallest of birds, most species measuring in the 7.5–13 cm range. Indeed, the smallest extant bird species is a hummingbird, the 5-cm Bee Hummingbird. They can hover in mid-air by rapidly flapping their wings...

s, and birds of the genus Diglossa

Diglossa (bird)

Diglossa is a genus of flowerpiercers in the family Thraupidae. Sometimes classified in the bunting and American sparrow family Emberizidae, more recent studies have shown it to belong in the Thraupidae...

. Even though bats act as important pollinators in the tropics, their ability to practice nectar robbery has not been studied. Nevertheless, exploitation of nectar by a frugivorous

Frugivore

A frugivore is a fruit eater. It can be any type of herbivore or omnivore where fruit is a preferred food type. Because approximately 20% of all mammalian herbivores also eat fruit, frugivory is considered to be common among mammals. Since frugivores eat a lot of fruit they are highly dependent...

 bat has once been recorded in a study of better-known robbers of a tropical tree Mabea fistulifera

Mabea (genus)

Mabea is a plant genus of the family Euphorbiaceae. It is found in the Americas. It has about 40 species....

. One of the most peculiar examples of a nectar robbing species is the squirrel Tamiops swinhoei hainanus

Swinhoe's Striped Squirrel

Swinhoe's Striped Squirrel is a species of rodent in the Sciuridae family. It is found in China, Myanmar, and Vietnam....

which exploits ginger plant Alpinia kwangsiensis .

History

Charles Darwin

Charles Darwin

Charles Robert Darwin FRS was an English naturalist. He established that all species of life have descended over time from common ancestry, and proposed the scientific theory that this branching pattern of evolution resulted from a process that he called natural selection.He published his theory...

 believed that nectar robbing always had a negative impact on the plant and his assumption was unquestioned by the late twentieth century . Now it is fairly well known that the impact of nectar robbing on plants is not as straightforward as assumed. Only one third of the studies of nectar robbing have revealed a negative impact on the plant, while others have shown either neutral or positive effect .

Varying effects of nectar robbing on plant fitness

Pollination systems are mostly mutualistic, meaning that the plant benefits from the pollinator's transport of male gamete

Gamete

A gamete is a cell that fuses with another cell during fertilization in organisms that reproduce sexually...

s and the pollinator benefits from a reward, like pollen

Pollen

Pollen is a fine to coarse powder containing the microgametophytes of seed plants, which produce the male gametes . Pollen grains have a hard coat that protects the sperm cells during the process of their movement from the stamens to the pistil of flowering plants or from the male cone to the...

 or nectar . As nectar robbers utilize the rewards of the plant without being in direct contact with the reproductive parts of the flower, their behaviour is easily assumed to be cheating

Cheating (biology)

Cheating is a metaphor commonly used in behavioral ecology to describe organisms that receive a benefit at the cost of others. Cheating is common in many mutualistic and altruistic relationships. Natural selection favors cheating, but there are mechanisms to regulate cheating.- Theoretical Models...

. However, there are examples in which the effect of robbery on the plant is neutral or even positive . In one of the most extreme examples, even when 80 percent of the flowers in a study site were robbed and it was shown that the robbers were not pollinating, neither the seed nor fruit set was negatively affected .

The effect of robbery on plant fitness

Fitness (biology)

Fitness is a central idea in evolutionary theory. It can be defined either with respect to a genotype or to a phenotype in a given environment...

 depends on several issues. Firstly, it is not always clear that a nectar robber does not carry pollen. For example, nectar-robbing carpenter bees, bumble bees and some birds have been observed to take part in pollination

Pollination

Pollination is the process by which pollen is transferred in plants, thereby enabling fertilisation and sexual reproduction. Pollen grains transport the male gametes to where the female gamete are contained within the carpel; in gymnosperms the pollen is directly applied to the ovule itself...

 . 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 are known to practice in concert with nectar robbing . Different types of robbing organisms affect the plant in different ways. The impact of Trigona bees (e.g. Trigona ferricauda) on the plant is almost always negative. This is probably due to their aggressive territorial behaviour

Territory (animal)

In ethology the term territory refers to any sociographical area that an animal of a particular species consistently defends against conspecifics...

 which effectively evicts legitimate pollinators . In addition to evicting pollinators, nectar robbers may change the behaviour of legitimate pollinators in many other ways. As robbers reduce the amount of nectar available, pollinators may be forced to visit more flowers to fulfill their needs. The increased number of flowers visited and longer flight distances increase pollen flow and outcrossing

Outcrossing

Outcrossing is the practice of introducing unrelated genetic material into a breeding line. It increases genetic diversity, thus reducing the probability of all individuals being subject to disease or reducing genetic abnormalities...

, which is beneficial for the plant because it lessens inbreeding depression

Inbreeding depression

Inbreeding depression is the reduced fitness in a given population as a result of breeding of related individuals. It is often the result of a population bottleneck...

 . This is, of course, only possible if the robber does not empty the flower completely. In this case, pollinators usually avoid the flower and the effect on plant fitness is clearly negative .

The response of different species of legitimate pollinators also varies. Some species, like the bumble bee Bombus appositus and many species of nectar-feeding birds can distinguish between robbed and unrobbed plants and minimize the energy used for foraging

Foraging

- Definitions and significance of foraging behavior :Foraging is the act of searching for and exploiting food resources. It affects an animal's fitness because it plays an important role in an animal's ability to survive and reproduce...

 by avoiding the heavily robbed flowers . It is assumed that pollinating birds are better at this than insects, because of their higher sensory capability . The ways in which pollinators distinguish between robbed and unrobbed flowers have not been studied but they have been thought to be related to the damage on petal

Petal

Petals are modified leaves that surround the reproductive parts of flowers. They often are brightly colored or unusually shaped to attract pollinators. Together, all of the petals of a flower are called a corolla. Petals are usually accompanied by another set of special leaves called sepals lying...

 tissue after robbery or changes in nectar quality . If nectar robbing severely reduces the success of legitimate pollinators they may be able to switch their plant species .

Nectar robbing, especially by birds , can cause damage to the reproductive parts of a flower and thus diminish the fitness of a plant . 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 . The secondary robbers are those (e.g. flies and bees) that take advantage of the holes made by primary robbers .

In conclusion, the effect of robbing is positive if the robber also pollinates or increases the pollination by the legitimate pollinator. On the other hand, robbing is negative if the robber damages the reproductive parts of a plant or reduces the pollination success either by competing with the legitimate pollinator or by lessening the attractiveness of the flower . Distinguishing between a legitimate pollinator and a nectar robber can sometimes be extremely difficult .

Evolutionary implications

Pollination systems are known to cause coevolution. The close relationships between figs

Ficus

Ficus is a genus of about 850 species of woody trees, shrubs, vines, epiphytes, and hemiepiphyte in the family Moraceae. Collectively known as fig trees or figs, they are native throughout the tropics with a few species extending into the semi-warm temperate zone. The Common Fig Ficus is a genus of...

 and fig wasp

Fig wasp

Fig wasps are wasps of the family Agaonidae which pollinate figs or are otherwise associated with figs, a coevolutional relationship that has been developing for at least 80 million years...

s as well as yucca

Yucca

Yucca is a genus of perennial shrubs and trees in the family Asparagaceae, subfamily Agavoideae. Its 40-50 species are notable for their rosettes of evergreen, tough, sword-shaped leaves and large terminal panicles of white or whitish flowers. They are native to the hot and dry parts of North...

s and yucca moths

Prodoxidae

Prodoxidae is a family of primitive monotrysian Lepidoptera. Some of these small-to-medium sized moths are day flying, like Lampronia capitella, known to European gardeners as the "Currant Shoot Borer". Others occur in Africa and Asia.Tetragma gei feeds on Mountain Avens Geum triflorum in USA....

 are probably the most clear and well-known examples of this phenomenon . If nectar robbers have an effect (direct or indirect) on a plant or pollinator fitness, they are part of the coevolution process, as well . In the case where nectar robbing is detrimental to the plant, it is conceivable that a plant species might evolve to minimize the traits that attract the robbers or develop some type of protective mechanism to hinder them . Another option is to try to neutralize negative effects of nectar robbers. Nectar robbers also show adaptations for more efficient nectar robbing. Many hummingbirds and Diglossa bird species have serrated bills that are thought to aid them in incising flower tissue for nectar robbing .

Nectar robbing has been suggested to occur in two ways. The first is that the nectar robbing animal can only get food in illegitimate ways because of the mismatch between the morphologies of their mouthparts

Mouthparts

The mouthparts of arthropods have evolved into a number of forms, each adapted to a different style or mode of feeding. Most mouthparts represent modified, paired appendages, which in ancestral forms would have appeared more like legs than mouthparts. In general, arthropods have mouthparts for...

 and the floral structure. The second is that nectar robbing is a relatively more efficient and more energy-saving way for animals to get nectar from flowers .

It is not completely clear how pollination mutualisms are able to 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. Also, in many cases mutualism simply confers a higher payoff than exploitative behaviours would .

Do flowering plants protect themselves against nectar robbers?

Even though there has not been much research on the defences

Biological defense

In biology,*often biological defense mechanism, a form of adaptation that promotes the survivability of an organism by protecting it from its natural enemies. Also see chemical defense.In law,...

 evolved in plants against nectar robbers, the adaptations have been assumed to rise from traits used in interactions between plants and herbivore

Herbivore

Herbivores are organisms that are anatomically and physiologically adapted to eat plant-based foods. Herbivory is a form of consumption in which an organism principally eats autotrophs such as plants, algae and photosynthesizing bacteria. More generally, organisms that feed on autotrophs in...

s (especially florivores). Some defences may also have evolved through traits originally referred to pollination. Defences against nectar robbers have been thought to include 1) toxin

Toxin

A toxin is a poisonous substance produced within living cells or organisms; man-made substances created by artificial processes are thus excluded...

s and secondary compounds

Secondary metabolite

Secondary metabolites are organic compounds that are not directly involved in the normal growth, development, or reproduction of an organism. Unlike primary metabolites, absence of secondary metabolities does not result in immediate death, but rather in long-term impairment of the organism's...

, 2) escape in time or space, 3) physical barriers and 4) indirect defences .

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 . One example is a plant called Catalpa speciosa which produces nectar containing iridoid glycoside

Glycoside

In chemistry, a glycoside is a molecule in which a sugar is bound to a non-carbohydrate moiety, usually a small organic molecule. Glycosides play numerous important roles in living organisms. Many plants store chemicals in the form of inactive glycosides. These can be activated by enzyme...

s that deter nectar-thieving ants but not legitimate bee pollinators . Low sugar concentration in nectar may also deter nectar robbers without deterring pollinators because dilute nectar does not yield net energy profits for robbers .

If robbers and pollinators forage at different times of day, plants may produce nectar according to the active period of a legitimate pollinator . 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

Shrub

A shrub or bush is distinguished from a tree by its multiple stems and shorter height, usually under 5–6 m tall. A large number of plants may become either shrubs or trees, depending on the growing conditions they experience...

 Pavonia dasypetala

Pavonia (plant)

Pavonia is a genus of flowering plants in the mallow family, Malvaceae. The generic name honours Spanish botanist José Antonio Pavón Jiménez .-Selected species:* Pavonia arabica Hochst. & Steud. ex Boiss....

does to avoid the robbing Trigona bees . 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 .

The last two methods of protection are physical barriers and indirect defence like symbionts

Symbiosis

Symbiosis is close and often long-term interaction between different biological species. In 1877 Bennett used the word symbiosis to describe the mutualistic relationship in lichens...

. Tighly packed flowers and unfavourably sized corolla tubes, bract liquid moats and toughness of the corolla or sepal

Sepal

A sepal is a part of the flower of angiosperms . Collectively the sepals form the calyx, which is the outermost whorl of parts that form a flower. Usually green, sepals have the typical function of protecting the petals when the flower is in bud...

 are barriers for some nectar robbers. A good example of an indirect defence is to attract symbiotic predators

Predation

In ecology, predation describes a biological interaction where a predator feeds on its prey . Predators may or may not kill their prey prior to feeding on them, but the act of predation always results in the death of its prey and the eventual absorption of the prey's tissue through consumption...

(like ants) by nectar or other rewards to scare away the robbers .

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 .