Conservation and Future Directions for Bats and Plants

Bats and plants clearly share a long history of mutual interactions and therefore exhibit specialized adaptations in extant species. These adaptations are evidence for coevolution between bats and plants and have been crucial to the establishment of pollination mutualisms. However, deforestation and human activities are threatening the persistence of bat-plant pollination mutualisms in recent times. In a land survey experiment, Garcia-Morales et al. (2013) found that all Neotropical bats responded negatively to human-use landscapes, including urban areas and monoculture crop fields. While Phyllostomid frugivores responded positively to agroforestry areas in this study, mainly due to increased fruit availability, overall bat diversity decreased (Garcia-Morales et al. 2013). The authors also found that human use areas were particularly detrimental to specialized nectarivorous bats. Since nectarivorous bats are among the most important bat pollinators of plants, human-induced land use change could threaten the persistence of specialized bat-plant pollination mutualisms. Deforestation is also displacing bat pollinators to edge habitat areas and thus pushing them farther from their foraging grounds (Kunz and Fenton 2003). By interfering with the feeding patterns of nectarivorous bats, deforestation may thus result in decreased pollination efficiencies of these specialists and threaten their plant hosts by extension. Similatly, Cosson et al. (1999) found that habitat fragmentation in French Guiana decreased the foraging range of nectarivorous bats, greatly reducing the chance that specialized nectarivores would visit their preferred plant host. This could translate into pollination frequency declines and thus threaten bat-plant pollination mutualisms in the area.

In addition to disrupting pollination activity, deforestation also threatens ecosystem services that bats provide including insect control, seed dispersal, and forest regeneration (Kunz and Fenton 2005). Frugivorous bats are important seed dispersers to many tropical plant species by increasing regional population size (Becker et al. 2010). By expanding plant species range, bats could potentially be important agents of promoting forest regeneration in deforested areas; Racey and Swift (1995) report that seed dispersal patterns vary between bats of different size categories, families, and feeding behaviors. Therefore, a heterogeneous pattern of seed dispersal occurs throughout forests with bat seed dispersers (Racey and Swift 1995).

Future studies should focus on the patterns of pollination efficiency of bat pollinators in disturbed habitats. Although the majority of the world’s plants rely on multiple pollinators for fertilization, there are still highly specialized relationships between bats and plants that need to be protected. If deforestation continues at current rates, the pollination mutualisms between bats and plants that have developed from millions of years of coevolution could vanish in the near future. In addition, other important ecosystem services provided by bats and their interactions with plants are at risk. The loss of even a single bat or plant species could have devastating consequences on an entire ecosystem, as specialized adaptations between bats and plants have required ideal circumstances over long periods of time in order to fully develop. These circumstances may never occur again in our Earth’s history, and therefore coevolved specialist species like bats and their hosts are important to conserve. 

Borrow (2008). Little red flying fox (Pteropus scapulatus). 

References

Becker, N.I., Rothenwöhrer, C. & Tschapka, M. 2010, "Dynamic feeding habits: efficiency of frugivory in a nectarivorous bat", Canadian journal of zoology, vol. 88, no. 8, pp. 764-773.

Cosson, J., Pons, J. & Masson, D. 1999, "Effects of Forest Fragmentation on Frugivorous and Nectarivorous Bats in French Guiana", Journal of Tropical Ecology, vol. 15, no. 4, pp. 515-534.

Garcia-Morales, R., Badano E.I. & Moreno, C.E. 2013, "Response of Neotropical Bat Assemblages to Human Land Use", Conservation Biology, vol. 27, no. 5, pp. 1096-1106.

Kunz, T.H. & Fenton, M.B. 2003, Bat ecology, Paperback edn, University of Chicago Press, Chicago.

Racey, P.A., Swift, S.M., Zoological Society of London & Mammal Society 1995, Ecology, evolution and behaviour of bats :the proceedings of a symposium held by the Zoological Society of London and the Mammal Society : London, 26th and 27th November 1993, Published for the Zoological Society of London by Clarendon Press, Oxford.

Flying Foxes: Natural Seed Dispersers

Whereas most of the coevolutionary relationships discussed in this blog have revolved around specialized microbats and their plant food sources, megabat flying foxes also have some important associations with plants. Flying foxes are nearly always frugivorous or nectarivorous, feeding on tropical fruits and flowers from Africa, Australia, and Asia (Figure 1; Kunz and Fenton 2003). There has been much speculation as to the extent of pollination actually achieved by flying foxes, but seed dispersal has been studied as a major ecosystem service provided by these bats. Like their microbat counterparts, flying foxes can travel enormous distances each night for forage (up to 200 km in some cases), and thus play an important role in dispersing seeds from the fruit they eat and in forest regeneration (Kunz and Fenton 2003). 

Fig 1. Flying fox eating an orange (species unknown). Accessed 23/5/2015; Available from http://www.batworlds.com/bat-feeding/. 

Nyhagen et al. (2005) found that Pteropus niger, an endemic species of flying fox on the island of Mauritius, has a profound role in forest regeneration of the island. They found that P. niger feeds on up to 22 different species of plants and disperses their seeds in their faeces, mature and undamaged. Many seeds were even found to be germinating within the bat droppings, possibly from an increased availability of fertilizing nutrients while passing through the bat's digestive system (Nyhagen et al. 2005). Because these bats feed on such a wide variety of fruits, they are important in maintaining genetic connectivity between forest fragments and can maintain plant diversity within these fragments (Nyhagen et al. 2005). In another study, Thomas (1982) found that up to 98% of the first woody plants to establish in forest fragments were from seeds dropped by flying foxes. 

These results suggest that plants have established important adaptations to improve seedling survival and germination following vertebrate dispersal. In order to survive the acidity and danger of a bat's digestive tract, plants dispersed by bats typically have very hardened embryos and even favor nutrients within a bat's faeces (Kunz and Fenton 2003). 

References

Kunz, T.H. & Fenton, M.B. 2003, Bat ecology, Paperback edn, University of Chicago Press, Chicago.

Nyhagen, D.F., Turnbull, S.D., Olesen, J.M. & Jones, C.G. 2005, "An investigation into the role of the Mauritian flying fox, Pteropus niger, in forest regeneration", Biological Conservation, vol. 122, no. 3, pp. 491-497.

Thomas, D.W. 1982, The ecology of an African savanna fruit bat community: resource partitioning and role in seed dispersal, .

Bats and Tequila

Bat-plant interactions not only provide a real-life example of coevolution, but they also provide some economic benefits for humans. Agave plants are succulent, cactus-like plants that are used in the production of tequila. They occupy semi-arid deserts of southern North America and northern Central America, and rely on nocturnal animal visitors for pollination (Figure 1; Kunz and Fenton 2003). Tequila production is a multi-billion dollar per year industry and occurs mainly in Mexico, where agave columnar cacti are extremely abundant (Arita and Wilson 1987). For many Mexican workers, agave cacti represent a way of life and contribute substantially to economic stability in Mexico (Arita and Wilson 1987). It has been shown in recent years that nectarivorous bats of Mexican deserts are important pollinators of agaves,  thus represent an important economic and ecological concern for the tequila industry. 

Fig 1. Tuttle, M.D. (2012). Choeronycteris mexicana pollinating an agave plant. Photo retrieved 22/5/2015: Available from http://www.wired.com/2014/06/tequila-booze-and-bats/.

In a field study in Mexico, Arizaga et al. (2000) found that bats were significantly better pollinators of the agave plant Agave macroacantha than were insects; agave plants had significantly more developed fruits following bat visitation. Of three different bat species studied, visitation by Leptonycteris curasoae caused the most fruitset in A. macroacantha (Arizaga et al. 2000). This bat is a highly specialized nectarivore with adaptations to favor nectar extraction from agaves. According to the study, Arizaga et al. (2000) propose that A. macroacantha has developed morphological adaptations, such as forming a "scape" or extended inflorescence, to attract nectarivorous bats and increase the probability of pollen transfer. Since these bats can travel up to 30 km to forage in one night, agaves greatly benefit from bats in that they can reproduce over long distances and maintain population stability (Arita and Wilson 1987). This is yet another example of the incredible coevolutionary adaptations developed by bats and plants to fuel ancient pollination mutualisms. 

References

Arita, H. & Wilson, D. 1987, "Long-nosed bats and agaves: the tequila connection", Bats, vol. 5, no. 4, pp. 3-5.

Arizaga, S., Ezcurra, E., Peters, E., de Arellano, F.R. & Vega, E. 2000, "Pollination ecology of Agave macroacantha (Agavaceae) in a Mexican tropical desert. II. The role of pollinators", American Journal of Botany, vol. 87, no. 7, pp. 1011-1017.

Kunz, T.H. & Fenton, M.B. 2003, Bat ecology, Paperback edn, University of Chicago Press, Chicago.

Nectar Bats vs. Fruit Bats: Which are the Better Pollinator?

Both nectarivorous and frugivorous bats most often come in physical contact with the flowers they visit. However, the extent of physical contact (and thus also the extent of pollen transfer) that these bats make with their food source depends on the morphological and behavioral adaptations they have developed. It is important to note that the mutualisms that have developed between flower visiting bats and flowers are not altruistic: they represent an evolutionary power struggle between plant and animal taxa in order for one to obtain ecological and energetic advantages over the other (Kunz and Fenton 2003). Therefore, many bats have established strategies to increase food extraction from plants and minimize pollen transfer (which is often a negative consequence for bats), and many plants have evolved adaptations to achieve the opposite (since nectar is an energetically costly reward).

Frugivorous bats and opportunistic nectarivores commonly land, perch, and crawl on plants in order to extract fruit and nectar. This increases the overall length and extent of physical contact between bats and their flower food sources, thus increasing the probability of pollen transfer (Tschapka 2003). In contrast, obligate nectarivores have highly specialized morphological (elongated tongue and rostrum, diminished dentition) and behavioral (hovering rather than perching) adaptations that reduce contact with flowers, reducing the probability that pollen will be deposited or picked up (Figure 1; Tschapka 2003). 

Fig 1. Tschapka (2003). (A) Artibeus spp., an opportunistic nectarivore, perching on inflorescence of Calyptrogyne ghiesbreghtiana to extract nectar from flowers. (B) Specialized nectarivore Glossophaga commisarisi hovering over the same inflorescence, but showing significantly reduced physical contact with flowers. Photo accessed 20/5/2015.

In a study by Tschapka (2003) in Costa Rican lowlands, bats were video recorded to observe perching and hovering behaviors on the understory palm Calyptrogyne ghiesbreghtiana, and bats were captured to measure pollen load of bats across families and dietary habits. In addition, plants of C. ghiesbreghtiana were analyzed for fruit set following visitation by bats. The study found that perching bats carried a significantly higher pollen load than did hovering bats (Tschapka 2003). In addition, plants that were visited by perching bats developed more fruits than did plants that were only visited by hovering bats (Fig 2; Tschapka 2003). These results suggest that increased contact caused by perching behaviors cause opportunistic nectarivores to be more effective pollinators than specialized nectarivorous bats. The high pollination efficiency of perching bats also suggests that the morphology of C. ghiesbreghtiana has evolved to favor a pollination system facilitated by opportunistic nectarivores rather than the specialized glossophagine bats. That is, perching bats have caused more successful pollination of the plant, which is reflected in the specific adaptations of that plant to perching bats (Tschapka 2003). In addition, the small, shallow flowers of C. ghiesbreghtiana attract perching bats because they do not require bats to have highly specialized rostrums or tongues to extract nectar. Therefore, perching bats are more likely to visit flowers of c. ghiesbreghtiana to obtain a nectar reward, and in turn, increase the probability of pollination and fruit set (Tschapka 2003). This study exemplifies the coevolutionary processes that occur between flower-visiting bats and plants. 

Fig 2. Tschapka (2003). Mean percent fruit set in C. ghiesbreghtiana visited by perching bats compared to those visited by only hovering bats. Figure accessed 20/5/2015.

References

Kunz, T.H. & Fenton, M.B. 2003, Bat ecology, Paperback edn, University of Chicago Press, Chicago.

Tschapka, M. 2003, "Pollination of the understorey palm Calyptrogyne ghiesbreghtiana by hovering and perching bats", Biological Journal of the Linnean Society, vol. 80, no. 2, pp. 281.

Mucuna holtonii: An Echolocation Plant

While many "bat plants" are pollinated by other animal species, some plants have evolved to be pollinated exclusively by bats and thus rely on them for survival. Such is the case of the Central American legume Mucuna holtonii. This plant is so highly specialized to attract bat pollinators, that it has evolved many structural and chemical adaptations truly unique to bat plants (Tschapka and Dressler 2002). Mucuna holtonii is an epiphytic vine found on rainforest edges and lining creeks throughout Central America. The plant has hanging inflorescences consisting of 3-8 flowers that bloom only at night. The flowers have 5 petals; two keel petals, two lateral petals, and a fifth, highly specialized petal that forms a concave, triangular vexillum that is only raised in mature flowers (Fig. 1; von Helversen and von Helversen 1999). 

Fig 1. von Helversen and von Helversen, 1999. Petal structures of mature M. holtonii with erect vexillum (left) and immature bud (right). Accessed 19/5/2015; available: http://www.nature.com/nature/journal/v398/n6730/pdf/398759a0.pdf.

When a flower of M. holtonii is mature and has completed nectar and pollen production, its fifth petal raises upwards at night and forms a concave vexillum. The vexillum serves as a reflective tunnel for bat echolocation waves, collecting them and directing them backwards toward the source. This signals to the bat that a mature flower with a virgin food source is within range. The bat continues to emit sonar and receive signals from the vexillum until the plant is located by the bat, at which point it lands and proceeds to extract nectar from the nectary (Fig 2; Simon et al. 2011). When the bat lands, it will cause the keel petals to burst and the staminal column of the plant will launch most of its pollen load onto the bat's back and rump. The bat will leave the flower once it has extracted approximately 100 microliters, carrying a large load of pollen to the next flower it will seek for nectar (Simon et al. 2011). Once the flower receives a bat visitor and has unloaded pollen, the vexillum petal will lower and thus will not attract bats to its nectary. This ensures that bats will not extract valuable, energy-intensive nectar without receiving a full pollen load, since the flower has already unloaded its pollen stores on the previous bat visitor (von Helversen and von Helversen 1999).

Fig 2. Tuttle, M.D. 2012. Glossophaga commisarisi visits a mature flower of Mucuna holtonii and extracts nectar. The staminal column of the flower will release a full load of pollen onto the bat once it bursts the keel petals. Accessed 19/5/2015; available: ngm.nationalgeographic.com.

These specialized adaptations of M. holtonii demonstrate the incredible specificity some organisms display as a result of coevolution. 

References

SIMON, R., HOLDERIED, M.W., KOCH, C.U. and VON HELVERSEN, O., 2011. Floral acoustics: conspicuous echoes of a dish-shaped leaf attract bat pollinators. Science (New York, N.Y.), 333(6042), pp. 631-633.

TSCHAPKA, M. and DRESSLER, S., 2002. Chiropterophily: On Bat–Flowers and Flower Bats. Curtis's Botanical Magazine, 19(2), pp. 114.

VON HELVERSEN, D. and VON HELVERSEN, O., 1999. Acoustic guide in bat-pollinated flower. Nature, 398(6730), pp. 759-760.

Plant Adaptations to Bats

As bats have evolved certain morphological and behavioral adaptations to favor flower visiting, so have plants developed similar specializations. The most common adaptation shared by all plants pollinated by bats is nocturnal flower blooming. By blooming at night, flowers become available only to nocturnal visitors and thus cause a very directional pollen transmission dynamic (Tschapka and Dressler 2002). Plants have also evolved a number of morphological adaptations to promote attraction and visitation by bats, as well as to maximize efficiency of conspecific pollen transfer. Since bats are long-distance pollinators, plant scent is a very important characteristic for bat flowers. Bat flowers are typically described as emitting scents considered to be unpleasant by humans, including scents resembling sour milk, chlorine, urine, and even cadavers or rotting meat (Tschapka et al. 2000). These scents likely attract bats due to their high potency, which can thus travel longer distances through the air and be detected more easily by swiftly flying bats (Tschapka and Dressler 2002). Many bat flowers have also evolved specialized structures that aid in reflecting bat echolocation signals so bats can easily identify them as a food source. An example of this is the highly specialized legume Mucuna holtonii, which will be discussed in further detail in the next blog post (Tschapka and Dressler 2002). 

Once bat flowers have attracted bats, they need to be able to withstand the large body size of bats in order to transfer pollen effectively. For this reason, many bat plants have developed large, robust platform-like structures for bats to land on while visiting the flower (Fig 1). This allows increased surface contact between the bat and plant, increasing the probability of successful pollen transfer (Tschapka and Dressler 2002). In addition, many bat plants have very conspicuous inflorescences that are highly accessible to hovering nectarivorous bats, and also increases the probability that bats will pick up and/or deposit pollen onto the flower stamen (Tschapka and Dressler 2002). In addition to morphology, most bat flowers have certain chemical adaptations to accommodate bat visitors. For example, bat plants often produce a very dilute nectar compared to that of other plants, which increases the frequency that bats visit other flowers of the same species and consequently increases the chance of conspecific fertilization (Tschapka and Dressler 2002).

Fig 1. Tschapka and Dressler, 2002. Large platform-like inflorescence of Macgravia nervosa to accommodate the large size of frequent nectarivorous visitor Hylonycteris underwoodii. Photo accessed 17/5/2015; Available: onlinelibrary.wiley.com. 

References

TSCHAPKA, M. and DRESSLER, S., 2002. Chiropterophily: On Bat–Flowers and Flower Bats. Curtis's Botanical Magazine, 19(2), pp. 114.

Facultative Nectarivory: The Pallid Bat

We have seen that many nectarivorous bats have evolved highly specialized morphological and behavioral adaptations to maximize their feeding efficiency. However, there are cases of facultative nectarivory and frugivory in some bat species that could be demonstrating a gradual evolution towards more obligate feeding patterns. Such is the case of the pallid bat (Antrozous pallidus), a primarily insectivorous microbat from Central and southern North America (Figure 1). A. pallidus has been observed visiting flowers and drinking the nectar of the cardon columnar cactus (Pachycereus pringlei) in northwestern Mexico, and represents the first case of facultative nectarivory in a bat outside of the New World microbat family Phyllostomidae (A. pallidus is in family Vespertilionidae) (Frick et al. 2012). Such behavior from an insectivorous bat may represent the evolutionary processes that took place nearly 40 million years ago, when obligate nectarivory first emerged in bat lineages (Kunz and Fenton 2003).


Figure 1. Tuttle, M. 2014. Pallid bat (Antrozous pallidus) sipping nectar from a flower of a columnar cactus. A. pallidus is most typically a gleaning insectivore, snatching arthropods and insects off the ground. https://www.thedodo.com/the-work-of-a-real-batman-843781039.html; retrieved 19/4/2015.


In a recent study in northwestern Mexico, experimental results show that A. pallidus actually deposits more pollen at cactus flowers per visit than the obligate nectarivore the lesser long-nosed bat (Leptonycteris yerbabuenae), suggesting the pallid bat may in fact be a more effective pollinator than a highly specialized nectarivore (Frick et al. 2012; Figure 2). This is mainly due to the feeding mechanisms of the pallid bat; since it is not specialized to hover and quickly extract nectar like the lesser long-nosed bat is, the pallid bat lands on the flowers and plunges its face and tongue into the flower to extract nectar. This increases physical contact between the bat and the flower, increasing the chance of pollen transfer at each flower visit (Frick et al. 2012).

Fig 2. Frick et al. 2012. Average pollen loads on cactus flower stigmas per visit by A. pallidus and L. yerbabuenae. A. pallidus, the facultative nectarivore, deposited significantly more pollen at cactus flowers per visit than did L. yerbabuenae. Reprinted from Frick et al. (2012); retrieved 19/4/2015.


This behavior of facultative nectarivory by a primarily insectivorous bat could exemplify the evolutionary processes that take place to develop obligate nectarivory. Whereas the highly specialized lesser long-nosed bat has adaptations to increase feeding efficiency and reduce metabolic costs, the pallid bat still expends a significant amount of energy while feeding on nectar due to a lack of traits specialized for nectarivory (Frick et al. 2014). It is possible that the pallid bat could eventually develop more adaptations specific to nectarivory given the proper selective pressures and mutations.