How to Become a Vulture and Not Die Trying: Following Tropical Bees and Their Gut Microbes
By Magda P. Argueta Guzmán
Here on Earth, multicellular life has its origins in single-celled bacteria. It took a billion years after the planet’s formation for single-celled organisms to arrive and, around 600 million years ago, multicellular animals to become established. And, fascinatingly, to this day we multicelled animals are still pretty much dependent on microbes to cover our metabolic functions.
Take termites, for example. Although unwelcome in the foundations of our houses, termites are essential in natural systems to decompose old wood and recycle energy. However, termites do not act alone. On their own, termites are not able to derive energy and nutrients from wood. But, some bacterial groups, such Enterobacteria, can degrade cellulose and live within the gut of termites. Thus, wood-degrading bacteria and termites co-exist in a type of symbiosis that represents mutual benefit for both, a relationship called mutualism.
Welcome to the Gut Microbiome
Harboring microbial allies in the digestive tract to obtain nutritional perks can be found across the animal kingdom, forming a fascinating but hidden world: The gut microbiome. We can think of the microbiome as a diverse but microscopic jungle in which different types of species interact with each other, actively modifying their surrounding environment. As with termites, every animal’s gut microbiome is finely tuned to its particular diet.
Bees are another fascinating example. Over millions of years, insect pollinators have played a major role in flower diversification, but bees stand out from the variety of pollinators because they present specialized structures in their body to carry floral rewards, thus enhancing pollination. Currently, there are about 17,000 bee species described, which is equivalent to three times the amount of mammal species on our planet. But where do bees come from? To answer this, we must acknowledge the power of dietary changes.
Evolutionarily speaking, bee species can be considered vegetarian wasps, because bees diverged from a carnivorous group of wasps scientifically referred to as the spheciform complex. Thus, the modification of feeding habits from a carnivorous style to a diet based on floral provisions provoked bees to exploit a new energy source not then used by other insects. As time passed and evolution selected in favor of these interactions, the radiation of bee species paralleled the evolution of flowering plants, a marvelous example of a co-evolutionary association. This separation between wasps and bees occurred about 140 million to 110 million years ago, when the dinosaurs were still inhabiting our planet in the mid-Cretaceous.
Although we can imagine that the bee gut microbiome changed when bees became vegetarian wasps, we cannot know the details of such an extreme change. But what if some living bee species reverted from a vegetarian lifestyle back to eating meat as a protein source? Research published in November 2021 in Microbial Ecology earned numerous headlines late last year after exploring this question, examining the gut microbiome of a group of bees in the American tropics. As crazy as it sounds, these bees are perhaps the most surprising living example of how changes in diet influence the gut microbiome in animals.
Meet the ‘Vulture’ Bees
If I ask you to think of a bee, you will undoubtedly picture a field of flowers where bees are collecting pollen, nectar, and floral oils. This is the case for most bee species living on our planet. However, hidden in dense tropical rainforests from Costa Rica to Brazil, a group of specialized bees collects meat from carcasses instead of pollen from flowers. The so-called “vulture” bees are intriguing species given their partial or total reversion to a carnivorous diet.
Vulture bees are part of a group known as the stingless bees, in the tribe Meliponini. All stingless bees are eusocial, which means that they live in perennial colonies, exhibit social organization, and divide the tasks among the colony members. In 1982, David Roubik, Ph.D., an entomologist at the Smithsonian Tropical Research Institute, was the first scientist to document a bee exhibiting obligate necrophagy—feeding only on carrion, i.e., dead animals—which was found in the tropical rainforest in Panama, a species called Trigona hypogea. Two other such species were later discovered, and today Trigona hypogea, Trigona necrophaga, and Trigona crassipes are the only three known bee species in the world that feed exclusively on carrion.
Other stingless bee species can eat both pollen and carrion to obtain nutrients, an equivalent of an omnivorous diet regimen. But how do vulture bees use carrion exclusively? After slicing flesh from dead animals such as lizards, snakes, birds, or even fish, vulture bees transport the carrion to their colonies, though it is unclear how they store the carrion therein. Experts have proposed two competing scenarios: In the first, vulture bees directly deposit and mix the carrion in wax pots. After 14 days, the mixture matures in a nutritional paste used to feed the colony members. In the second hypothesis, young vulture bee workers eat the collected carrion to produce a secretion with a specialized gland. Later, the workers store the produced secretion in wax pots to form the nutritional paste. Regardless of the mechanism that vulture bees follow to use the collected flesh, one thing is clear: Vulture bees recovered the taste for rotting flesh that vegetarian bees lost!
Change in Diet, Change in Gut Microbiota
But what about the vulture bee microbiome? Such a dramatic change in the dietary regimen may have also impacted the bacterial groups living in their gut.
All stingless bees, including vulture bees, are closely related to bumble bees, honey bees, and orchid bees, forming a group known as the corbiculate bees. The gut microbiota of corbiculate bees is composed of five major core bacterial groups that are shared and conserved among most bee species within the corbiculate group. However, the response of the vulture bee gut microbiota to the extreme shift in diet regimen remained a mystery for bee experts.
So, in 2019 a team of scientists from Cornell University and the University of California, Riverside, traveled to the jungle in Costa Rica to collect vegetarian, omnivorous, and carnivorous bees. Entomologists Laura Figueroa, Ph.D., Quinn McFrederick, Ph.D., and Erin Krichilsky explored the Costa Rican tropical rainforest searching for 17 species of stingless bees. Eight of these stingless bees collect pollen as an exclusive source of protein, eight more can feed on pollen and carrion, and one feeds completely on animal cadavers. To collect the pollen-eating bees, the scientists observed flowers, as per usual in bee research. However, to collect the vulture bees, the scientists had to change the collection method, setting up 16 chicken-meat baits hanging from tree branches.
After collecting the focused bee species, the researchers brought the specimens to the laboratory at UC Riverside. Doug Yanega, Ph.D., senior museum scientist, identified the collected bee species, while graduate student Jessica Maccaro used DNA techniques to identify and compare the bacteria present in the bee gut microbiota of vulture, omnivorous, and pollen-eating bees. The research team found that “vulture bees lost some ancestral core microbes, retained others, and entered into novel associations with acidophilic microbes.”
But why acidophilic bacteria? If you were to feed on rotten meat, you would be more exposed to pathogens, increasing the chances of contracting a severe infection. In such a case, acidophilic bacteria would be your best allies! For example, Carnobacterium and Apilactobacillus may make your gut more acidic, preventing pathogens from making you sick while you chew chunks of rotten meat. Thus, to feed on carrion, the vulture bee microbiome contains lactic acid bacteria and acetic acid bacteria in its repertoire, unlike the microbiome of pollen-eating bees.
Since the evolution of life on Earth, bacteria have played a major role in the origin, structure, and function of our ecosystems. Beyond that, bacteria are fundamental to the survival of all vertebrate and invertebrate animals that inhabit our planet nowadays. Microscopic but powerful, the gut microbiota can adjust to dramatic diet shifts like the one taken on by vulture bees. DNA technologies today allow the massive sequencing of all the genetic material in a biological sample, something unthinkable when David Roubik described necrophagy for the first time in tropical bees. So, next time you see some bees visiting flowers, stop to think of their vulture relatives and acknowledge how marvelous the gut microbiome is.
Magda P. Argueta Guzmán, is Ph.D. candidate in the Department of Entomology at the University of California, Riverside. Email: firstname.lastname@example.org.