Nectar robbing

Bombus terrestris stealing nectar.

Nectar robbing refers to the act by an animal, typically an insect or a bird, of removing nectar from a flowering plant, most often by drilling a hole in the corolla. In this way animals without morphological adaptations 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 ^[1].

Nectar robbers include certain species of carpenter bees, bumblebees, Trigona bees, ants, hummingbirds, and birds of the genus Diglossa ^[2]. 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 bat has once been recorded in a study of better-known robbers of a tropical tree Mabea fistulifera ^[3]. One of the most peculiar examples of a nectar robbing species is the squirrel Tamiops swinhoei hainanus which exploits ginger plant Alpinia kwangsiensis ^[4].

History

Charles Darwin believed that nectar robbing always had a negative impact on the plant ^{[5] [6]} and his assumption was unquestioned by the late twentieth century ^[2]. 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 ^[2].

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 gametes and the pollinator benefits from a reward, like pollen or nectar ^[2]. 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. However, there are examples in which the effect of robbery on the plant is neutral or even positive ^{[7] [2] [8] [9]}. 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 ^[10].

The effect of robbery on plant fitness 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 ^[2]. 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 ^{[2] [11]}. 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 which effectively evicts legitimate pollinators ^[12]. 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, which is beneficial for the plant because it lessens inbreeding depression ^[2]. 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 ^[2].

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 by avoiding the heavily robbed flowers ^[11]. It is assumed that pollinating birds are better at this than insects, because of their higher sensory capability ^[2]. 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 tissue after robbery or changes in nectar quality ^[11]. If nectar robbing severely reduces the success of legitimate pollinators they may be able to switch their plant species ^[2].

Nectar robbing, especially by birds ^[13], can cause damage to the reproductive parts of a flower and thus diminish the fitness of a plant ^[8]. 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 ^[2]. There are both primary and secondary nectar robbers ^[2]. The secondary robbers are those (e.g. flies and bees) that take advantage of the holes made by primary robbers ^[13].

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 ^{[11] [14]}. Distinguishing between a legitimate pollinator and a nectar robber can sometimes be extremely difficult ^[15].

Evolutionary implications

Pollination systems are known to cause coevolution. The close relationships between figs and fig wasps as well as yuccas and yucca moths are probably the most clear and well-known examples of this phenomenon ^{[16] [17]}. If nectar robbers have an effect (direct or indirect) on a plant or pollinator fitness, they are part of the coevolution process, as well ^[2]. 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 ^{[2] [1]}. 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 ^[18].

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 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 ^[19].

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 ^[15].

Do flowering plants protect themselves against nectar robbers?

Even though there has not been much research on the defences evolved in plants against nectar robbers, the adaptations have been assumed to rise from traits used in interactions between plants and herbivores (especially florivores). Some defences may also have evolved through traits originally referred to pollination. Defences against nectar robbers have been thought to include 1) toxins and secondary compounds, 2) escape in time or space, 3) physical barriers and 4) indirect defences ^[1].

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 ^[1]. One example is a plant called Catalpa speciosa which produces nectar containing iridoid glycosides that deter nectar-thieving ants but not legitimate bee pollinators ^[20]. Low sugar concentration in nectar may also deter nectar robbers without deterring pollinators because dilute nectar does not yield net energy profits for robbers ^[1].

If robbers and pollinators forage at different times of day, plants may produce nectar according to the active period of a legitimate pollinator ^[1]. 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 ^[12]. 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 ^[1].

The last two methods of protection are physical barriers and indirect defence like symbionts. Tighly 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 ^[1].

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 ^[1].

References

1. ^ ^{a b c d e f g h i} Irwin, R. E., Adler, L. S. & Brody, A. K. (2004). "The dual role of floral traits: pollinator attraction and plant defence.". Ecology 85 (6): 1503–1511. doi:10.1890/03-0390. 
2. ^ ^{a b c d e f g h i j k l m n o} Maloof, J. E. & Inouye, D. W. (2000). "Are nectar robbers cheaters or mutualists?". Ecology 81 (10): 2651–2661. doi:10.1890/0012-9658(2000)081[2651:ANRCOM]2.0.CO;2. 
3. ^ Olmos, F. & Boulhosa, R. (2000). A meeting of opportunists: birds and other visitiors to Mabea fistulifera (Euphorbiaceae) in florescences. Ararajuba 8(2):93 – 98.
4. ^ Deng, X., Ren, P., Gao, J. & Li, Q. (2004). The Striped Squirrel (Tamiops swinhoei hainanus) as a Nectar Robber of Ginger (Alpinia kwangsiensis). Biotropica. 36(4):633–636.
5. ^ Darwin, C. (1841). Humble-Bees. 142–145 in P. H. Barrett, editor. The collected papers of Charles Darwin, Volume 1. University of Chicago Press, Chicago, Illinois, USA.
6. ^ Darwin, C. (1872). The effects of cross and self fertilisation in the vegetable kingdom. Murray, London, UK.
7. ^ Morris, W. F. (1996). Mutualism denied? Nectar-robbing bumble bees do not reduce female or male success of bluebells. Ecology. 77 (5): 1451–1462.
8. ^ ^{a b} Irwin, R. E. (2003). "Impact of nectar robbing on estimates of pollen flow: conceptual predictions and empirical outcomes". Ecology 84 (2): 485–495. doi:10.1890/0012-9658(2003)084[0485:IONROE]2.0.CO;2. 
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10. ^ Maloof, J. E. (2001). The effects of a bumble bee nectar robber on plant reproductive success and pollinator behavior. American Journal of Botany. 88 (11): 1960–1965.
11. ^ ^{a b c d} Irwin, R. E. & Brody, A. K. (1998). "Nectar Robbing in Ipomopsis aggregata: effects on pollinator behaviour and plant fitness". Oecologia 116 (4): 519–527. doi:10.1007/s004420050617. 
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13. ^ ^{a b} Traveset, A., Willson, M. F. & Sabag, C. (1998). "Effect of nectar robbing birds on fruit set of Fuchsia magellanica in Tierra Del Fuego: a disrupted mutualism". Functional Ecology 12 (3): 459–464. doi:10.1046/j.1365-2435.1998.00212.x. 
14. ^ Irwin, R. E. & Brody, A. K. (1999). Nectar robbing bumble bees reduce the fitness of Ibomopsis aggregata (Polemoniaceae). Ecology. 80(5):1703–1712.
15. ^ ^{a b} Bronstein, J. L. (2001). "The exploitation of mutualisms". Ecology Letters 4 (3): 277–287. doi:10.1046/j.1461-0248.2001.00218.x. 
16. ^ 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.
17. ^ 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.
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19. ^ Zhang, Y., Wang, Y. & Guo, Y. (2006). The effects of nectar robbing on plant reproduction and evolution. Zhiwu Shengtai Xuebao. 30(4):695–702.
20. ^ Stephenson, A. G. 1981. Toxic nectar deters nectar thieves of Catalpa speciosa. American Midland Naturalist 105:381-383.