Bat Pollinated Flowers of a Mexican Columnar Cactus

Pollination syndromes – suites of floral traits used to determine potential pollinators and routes of pollination – have been informative in studying plant-pollinator interactions, but are generally too simplistic to tell the full story. Most flowering plants are generalists when it comes to pollinators, whereas pollination syndromes imply specialization. Not all pollinators are created equal though, and some may be more effective at pollinating particular plants than others. In fact, occasionally pollination syndromes ring true and a predicted plant-pollinator combination turns out to be the most effective and reliable interaction.

According to a study published in American Journal of Botany by Ibarra-Cerdeña, et al., Stenocereus queretaroensis, a species of columnar cactus endemic to western Mexico, adheres to this scenario. Stenocereus is a genus in a group of columnar and tree-like cacti called the Pachycereeae tribe. Cactus in this group are generally bat pollinated; however, their flowers are typically visited by various species of birds and insects as well, and in some cases, bats are not the primary pollinator. In their introduction, the authors note that specialization appears to be more common in tropical latitudes, and chiropterophilic (bat pollinated) columnar cacti that occur in temperate regions can be comparatively more generalized. This is because “extratropical chiropterophilic cacti appear to be faced with unpredictable seasonal year-to-year variation in pollinators,” while “cacti in tropical regions” experience “highly reliable seasonal availability of nectar-feeding bats, thereby leading to a temporally stable pollination system.”

Stenocereus queretaroensis is a massive cactus, reaching up to ten meters tall. Several vertical stems rise from a short, stocky, central trunk. Each stem has up to eight distinctive ribs and averages around 15 centimeters in diameter. Groupings of white to grey spines up to four centimeters long appear along the ribs. Flowers are light-colored, around 10 to 14 centimeters in length, and occur along the upper half of the stems, extended well beyond the spines. Flowers open at night – producing abundant nectar – and close by the afternoon the following day. Floral characteristics led the authors of this study to predict bats to be the main pollinator, and they set up a series of experiments to test this.

Stenocereus queretaroensis - photo credit: wikimedia commons

Stenocereus queretaroensis – photo credit: wikimedia commons

Part of their experiment consisted of five treatments involving 130 flowers on 75 plants. One group of flowers was bagged and allowed to self-pollinate naturally, while another group was bagged and self-pollinated manually. A third group was left exposed during the night but bagged in the morning, while a fourth group was bagged during the night and exposed during the daytime. The final group was left alone. For each of these five treatments, aborted flowers and mature fruits were counted and seed set was determined. Nectar samples were taken from a separate group of flowers at two hour intervals from 8:00 PM to 8:00 AM, after which no nectar was produced. A camera was also used to document floral visits. Visits were deemed “legitimate” when the “visitor’s body came in contact with anthers and/or stigma” and “illegitimate” when “no contact with anthers or stigma” was made.

The researchers found S. queretaroensis to be “incapable of self-pollination,” as no fruit set occurred for the first two treatments. The control group and the nocturnally exposed group had nearly identical results, producing significantly more fruits with greater seed set compared to the nocturnally bagged group. During the day, flowers were visited by four species of birds (two hummingbirds, a woodpecker, and an oriole) and several species of bees (mainly honey bees). During the night, apart from illegitimate visits from a nectar robbing hawkmoth, one species of bat was the dominant floral visitor, and the majority (93.8%) of the visits were legitimate. This bat species was Leptonycteris curasoae, the southern long-nosed bat.

Leptonycteris curasoae - photo credit: wikimedia commons

Leptonycteris curasoae – photo credit: wikimedia commons

The abundance of nectar-feeding bats was monitored in the study area over a four year period, and L. curasoae was by far the most abundant species throughout the study period. Nectar produced in the flowers of S. queretaroensis was at its maximum around midnight, which seemed to correlate with observations of bat visits. Even though daytime visitors appeared to contribute to fruit and seed set, the nocturnal treatment produced significantly more fruit with significantly higher seed set, suggesting that bats are the more efficient pollinator. Insects visiting during the daytime, when nectar was decreasingly available, were most likely robbing pollen.

The authors acknowledge that for most plant species, “a wide array of taxonomically diverse fauna such as insects, birds, and mammals usually serve as potential pollinators,” and that “generalized pollination systems are more frequent than specialized ones.” However, in this case, “a close association between L. curasoae and S. queretaroensis [suggests] that the chiropterophilic syndrome is still a useful model.”

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Year of Pollination: Most Effective Pollinator Principle and Beyond, part two

“The most effective pollinator principle implies that floral characteristics often reflect adaptation to the pollinator that transfers the most pollen, through a combination of high rate of visitation to flowers and effective deposition of pollen during each visit.” – Mayfield, et al., Annals of Botany (2001) 88 (4): 591-596

In part one, I reviewed a chapter by Jose M. Gomez and Regino Zamora in the book Plant-Pollinator Interactions: From Specialization to Generalization that argues that the most effective pollinator principle (MEPP) “represents just one of multiple evolutionary solutions.” In part two, I summarize a chapter by Paul A. Aigner in the same book that further explains how floral characteristics can evolve without strictly adhering to the MEPP.

maximilian sunflower
Aigner is interested in how specialization develops in different environments and whether or not flowering plants, having adapted to interact with a limited number of pollinators, experience trade-offs. A trade-off occurs when a species or population adapts to a specific environmental state and, in the process, loses adaptation to another state. Or in other words, a beneficial change in one trait results in the deterioration of another. Trade-offs and specialization are often seen as going hand in hand, but Aigner argues that trade-offs are not always necessary for an organism to evolve towards specialization. Plant-pollinator interactions provide an excellent opportunity to test this.

“Flowers demand study of specialization and diversification,” Aigner writes, not only due to their ubiquity, “but because much of the remarkable diversity seen in these organisms is thought to have evolved in response to a single and conspicuous element of the environment – pollination by animals.” If pollinators have such a strong influence on shaping the appearance of flowers, pollination studies should be rife with evidence for trade-offs, but they are not. Apart from not being well-studied, Aigner has other ideas about why trade-offs are not often observed in this scenario.

Aigner is particularly interested in specialization occuring in fine-grained environments. A course-grained environment is “one in which an organism experiences a single environmental state for all of its life.” Specialization is well understood in this type of environment. A fine-grained environment is “one in which an organism experiences all environmental states within its lifetime,” such as “a flowering plant [being] visited by a succession of animal pollinators.” For specialization to develop in a fine-grained environment, a flowering plant must “evolve adaptations to a particular type of pollinator while other types of pollinators are also present.”

It’s important to note that the specialization that Aigner mainly refers to is phenotypic specialization. That is, a flower’s phenotype [observable features derived from genes + environment] appears to be adapted for pollination by a specific type of pollinator, but in fact may be pollinated by various types of pollinators. In other words, it is phenotypically specialized but ecologically generalized. Aigner uses a theoretical model to show that specialization can develop in a fine-grained environment with and without trade-offs. He also uses his model to demonstrates that a flower’s phenotype does not necessarily result from its most effective pollinator acting as the most important selection agent. Instead, specialization can evolve in response to a less-effective pollinator “when performance gains from adapting to the less-effective pollinator can be had with little loss in the performance contribution of the more effective pollinator.”

Essentially, Aigner’s argument is that the agents that are the most influential in shaping a particular organism are not necessarily the same agents that offer the greatest contribution to that organism’s overall fitness. This statement flies in the face of the MEPP, and Aigner backs up his argument with (among other examples) his studies involving the genus Dudleya.

Dudleya saxosa (panamint liveforever) - photo credit: wikimedia commons

Dudleya saxosa (panamint liveforever) – photo credit: wikimedia commons

Dudleya is ecologically generalized. Pollinators include hummingbirds, bumblebees, solitary bees, bee flies, hover flies, and butterflies. “Some Dudleya species and populations are visited by all of these taxa, whereas others seem to be visited by only a subset.” Aigner was curious to see if certain species or populations were experiencing trade-offs by adapting to a particular category of pollinators. Aigner found variations in flower characteristics among species and populations as well as differences in pollinator assemblages that visited the various groups of flowers over time but could not conclude that there were trade-offs “in pollination performance.”

In one study, he looked at pollination services provided by hummingbirds vs. bumblebees as corolla flare changed in size. In male flowers, bumblebees were efficient at removing pollen regardless of corolla flare size, while hummingbirds removed pollen more effectively as corolla flare decreased. Both groups deposited pollen more effectively as corolla flare decreased, but hummingbirds more strongly so. Ultimately, Aigner concluded that “the interactions did not take the form of trade-offs,” or, as stated in the abstract of the study, ” phenotypic specialization [for pollination by hummingbirds] might evolve without trading-off the effectiveness of bumblebees.”

Aigner goes on to explain why floral adaptations may occur without obvious trade-offs. One reason is that different groups of pollinators are acting as selective agents for different floral traits, “so that few functional trade-offs exist with respect to individual traits.” Pollinators have different reasons for visiting flowers and flowers use the pollination services of visitors differently. Another reason involves the “genetic architecture” of the traits being selected for. Results can differ depending on whether or not the genes being influenced are linked to other genes, and genetically based fitness trade-offs may not be observable phenotypically. Further studies involving the genetic architecure of specialized phenotypes are necessary.

And finally, as indicated in part one, pollinators are not the only floral visitors. In the words of Aigner, “if floral larcenists and herbivores select for floral traits in different directions than do pollinators, plants may face direct trade-offs in improving pollination service versus defending against enemies.” These “floral enemies” can have an effect on the visitation rates and per-visit effectiveness of pollinators, which can drastically alter their influence as selective agents.

Like pollination syndromes, the most effective pollinator principle seems to have encouraged and directed a huge amount of research in the field of pollination biology, despite not holding entirely true in the real world. As research continues, a more complete picture will develop. It doesn’t appear that it will conform to an easily digestible principle, but there is no question that, even in its complexity, it will be fascinating.

I will end as I began, with an excerpt from Thor Hanson’s book, The Triumph of Seeds: “The notion of coevolution implies that change in one organism can lead to change in another – if antelope run faster, then cheetahs must run faster still to catch them. Traditional definitions describe the process as a tango between familiar partners, where each step is met by an equal and elegant counter-step. In reality, the dance floor of evolution is usually a lot more crowded. Relationships like those between rodents and seeds [or pollinators and flowers] develop in the midst of something more like a square dance, with couples constantly switching partners in a whir of spins, promenades, and do-si-dos. The end result may appear like quid pro quo, but chances are a lot of other dancers influenced the outcome – leading, following, and stepping on toes along the way.”