Stop grousing about your toxic relationship with food
You’ve got nothing on the Greater Sage Grouse, the only bird species known to thrive on poisonous sagebrush leaves. A new study shows that the real heroes are microorganisms.
During bitter cold winter days on the plains of the northwestern United States, the greater sage-grouse (Centrocercus urophasianus) spends much of its time concealed under low brush and deep snow to conserve body heat. In early morning and late evening it stuffs its crop (a storage pouch in its esophagus) with tiny pieces of sagebrush leaves, snipped off with its sharp beak, then finds a place to hide from predators as it digests its meagre meal.
Yet, just as carnivores such as eagles, coyotes and bobcats are ever ready to kill the timid sage grouse, other living organisms are hard at work helping it thrive in its hostile environment. A complex assembly of microbial allies are forever busy in the bird’s digestive tract converting sagebrush cellulose into digestible fatty acids and neutralizing the toxins the plant produces as a natural defense. No other bird is known to be able to survive on a diet of toxic sagebrush leaves.
Sagebrush pops up through a snowy winter landscape.
Now, for the first time, a team of Smithsonian scientists using marker gene sequencing have taken a closer look at the communities of microbes living in these bird’s intestines. Their findings, recently published in the journal Animal Microbiome, show two distinct suites of bacterial communities in the bird’s cecum (digestive pouches attached to its large intestine) that rise and fall as the bird’s dependence on toxic sagebrush increases in the winter and falls in summer when insects and other plants make up more of its diet. The study also revealed significant variation among the communities of microbiota living in different regions of the sage grouse gut.
“If you look at the 10,400-plus species of birds in the world, the greater sage grouse is one that immediately comes to mind as a bird with a really extreme diet,” says Gary Graves, an ornithologist at the Smithsonian’s Natural Museum of Natural History in Washington, D.C., and one of the study’s authors. For ornithologists studying avian gut microbes, this fact put the sage grouse front and center as a study subject.
A male greater sage grouse in magnificent display. (Photo by Tom Wick, Bureau of Land Management)
Using sage grouse specimens collected in Wyoming during both winter and summer, the researchers extracted fluid samples with syringes from five specific areas of their digestive tract: the crop, ventriculus (stomach), duodenum (small intestine), cecum (an appendix) and colon (large intestine). After extraction the fluids were placed in vials, labeled and shipped in liquid nitrogen to the Natural History Museum, where the material was sequenced and its genetic bacterial lineages identified.
The study revealed that the bird’s cecum contains more of a specific microbe community in winter—bacteria responsible for the detoxification and digestion of tough plant matter—when the bird is subsisting on a diet strictly of sagebrush. In summer, when the sage grouse is eating a mix of less toxic material—insects and the leaves of non-toxic plants—a different microbe community dominates the cecum.
Female greater sage grouse, Centrocercus urophasianus, in Bighorn National Forest
“These birds have figured out how to harness bacteria that not only can ferment sagebrush leaves and convert them into short-chain-fatty-acids from which the birds get energy, but which also neutralizes toxins in the leaves…the tars, saps and phenols,” Smithsonian ornithologist Sergei Drovetski, lead author of the study, points out. “The bacteria breaks down those chemicals into non-toxic products.”
“In winter, because of lower temperatures, wind and snow, the demand for energy by the bird’s body is a lot higher,” Drovetski adds. “The bird needs more energy to stay warm at a time when sagebrush leaves are the only food available. As a result they consume a lot of sagebrush in winter.”
Acid in the sage grouse’s stomach begins the first stage of the breakdown of the sagebrush cellulose. Afterward, the leaf particles are packed into the cecum under pressure. Filled with fluid mixture of plant material and bacteria, the cecum acts as a fermentation chamber where the sagebrush is broken down and digested.
Greater sage grouse in Seedskadee National Wildlife Refuge, Wyoming.
“What we found is that seasonal differences in bacteria are the largest in the crop and the cecum,” Drovetski says. “In summer, when there are more sugar and proteins in the plants the bird eats, more bacteria that consume sugars and proteins are present. In winter, when only sagebrush leaves are available, the abundance of bacteria that deal with toxins increases. Both bacterial communities are always inside the bird, but their composition in the gut depends upon what kind of food is entering it.”
Most previous studies of bird-gut microbiotas have focused on captive birds that were fed a zoo diet. “What differentiates this study is we focused on wild birds. Much of the gut microbes in wild birds originate from external sources in the environment.”
For the sage grouse one of these bacterial sources are open pools and streams of water, from which they drink twice a day—morning and late afternoon—in summer, Drovetski says. In winter water is frozen and not accessible to grouse.
Greater sage grouse drink from ponds and streams twice a day. It is thought this helps maintain their unique gut biome.
A second source are food plants. “Lupines, for example, come with a whole suite of nitrogen-fixing bacteria that is tightly associated with legumes,” Drovetski says. “You find this bacteria in the sage grouse gut in summer, not in winter, and it changes the microbiome of the bird.”
The study of gut microbiomes is a relatively new world in ornithology and vertebrate zoology, Graves adds. “It’s kind of like exploring a new planet. What do you know about life on Mars? Not much, but you are not going to know anything until you start looking.
“It’s not the bird itself that is converting the sagebrush, it is the billions of bacteria that are in every sage grouse that are helping it along. The sage grouse wouldn’t be able to do it by itself.”
“Distinct microbiotas of anatomical gut regions display idiosyncratic seasonal variation in an avian folivore,” Animal Microbiome, (2019) 1:2, Sergei V. Drovetski, National Museum of Natural History; Michael J. V. O’Mahoney, Kenan O. Matterson, Brian K. Schmidt and Gary R. Graves
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Posted: 17 May 2019
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