The Western corn rootworm is called that because its larvae ravage America's corn crops to the economic tune of $1 billion a year.
Enter a team of nine researchers, including UC Davis biologist Scott Carroll. They analyzed data over a six-year period and concluded that crop rotation works well in battling the notorious pest that annually causes $800 million in yield loss and $200 million in treatment costs.
“Answering this question was important not only to grower success but the agricultural economy, said Carroll, an associate of the UC Davis Department of Entomology and Nematology and owner of the Davis-based Institute for Contemporary Evolution. “Bt crops are far-and-away the single most important factor reducing soil and crop insecticide applications in the United States at present.”
When Bacillus thuringiensis (Bt) corn was introduced in 2003, the pest seemed under control. The genetically engineered corn is a transgenic, insecticidal crop that kills rootworm larvae but is harmless to humans.
However, when the pest began developing resistance to the Bt corn toxins, the U.S. Department of Agriculture recommended crop rotation as a method of control. Crop rotation, an age-old agricultural tactic, is a consistent and economical means of controlling rootworms the season following an outbreak. It reduces rootworm densities, and is considered more effective than insecticides.
With crop rotation, “the frequency of problem fields declined by 92 percent in 2014 to 2016 relative to 2011 to 2013,” the nine-member team wrote in the research article, “Crop Rotation Mitigates Impacts of Corn Rootworm Resistance to Transgenic BT Corn,” in the current edition of the Proceedings of the National Academy of Sciences.
“Corn rootworm is one of the nation's most devastating pests, giving a sense of urgency to protecting the efficacy of industrial pest control approaches with reduced non-target effects,” said Carroll, who studies basic and applied aspects of evolutionary biology. “Transgenic insecticidal Bt crops in the United States are cultivated under a very interesting socio-evolutionary model of resistance management that is mandated by the U.S. Environmental Protection Agency. Individual growers must implement resistance management--usually by devoting a small acreage to planting a 'refuge' of non-Bt crops in order to nurture a local reservoir population of Bt-susceptible pest insects.”
Carroll pointed out that the “outstanding productivity of Bt corn has led a portion of growers to reduce or eliminate their required refuge planting. Moreover, many time-tested practices for integrated pest management have fallen by the wayside as growers have found they could rely solely on the genetics of the seemingly invulnerable Bt varieties.”
“As predicted, Bt resistance evolution in corn rootworm has accelerated. In response to this dire risk, in 2016 EPA began mandating crop rotation as a complementary means of reducing the damage to Bt corn fields caused by resistant corn rootworms. Our working group analyzed the success of this traditional agricultural tactic to help sustain the efficacy of the high-tech Bt tactic.”
Carroll said that under the leadership of his colleague Yves Carrière at the University of Arizona, “our team analyzed six years of field data from 25 crop reporting districts in Illinois, Iowa and Minnesota—three states facing some of the most severe rootworm damage to Bt cornfields.
“The answer we found is that traditional crop rotation is working to protect the Bt corn fields from rootworm damage, including in areas that have seen the evolution of behavioral resistance to crop-rotation by rootworms.”
The bottom line, said Carrière, is this: "Farmers have to diversify their Bt crops and rotate. Diversify the landscape and the use of pest control methods. No one technology is the silver bullet.”
The project also included scientists from North Carolina State and McGill University, along with Carroll's colleague, Peter Jørgensen of the Stockholm Resistance Center.
While Jorgensen was pursuing his master's degree program at the University of Copenhagen and studying at UC Davis, he worked with Carroll and Sharon Strauss of the Department of Evolution and Ecology.
“This PNAS paper,” Carroll said, “is one of several that have developed from a pursuit Peter and I organized on 'Living with Resistance' at the National Socio-Environmental Synthesis Center in Annapolis, with the aim to explore more sustainable approaches to managing evolutionary challenges to health and food security.”
"Transgenic crops that produce insecticidal proteins from Bacillus thuringiensis (Bt) can suppress pests and reduce insecticide sprays, but their efficacy is reduced when pests evolve resistance. Although farmers plant refuges of non-Bt host plants to delay pest resistance, this tactic has not been sufficient against the western corn rootworm, Diabrotica virgifera virgifera. In the United States, some populations of this devastating pest have rapidly evolved practical resistance to Cry3 toxins and Cry34/35Ab, the only Bt toxins in commercially available corn that kill rootworms. Here, we analyzed data from 2011 to 2016 on Bt corn fields producing Cry3Bb alone that were severely damaged by this pest in 25 crop reporting districts of Illinois, Iowa, and Minnesota. The annual mean frequency of these problem fields was 29 fields (range 7 to 70) per million acres of Cry3Bb corn in 2011 to 2013, with a cost of $163 to $227 per damaged acre. The frequency of problem fields declined by 92% in 2014 to 2016 relative to 2011 to 2013 and was negatively associated with rotation of corn with soybean. The effectiveness of corn rotation for mitigating Bt resistance problems did not differ significantly between crop-reporting districts with versus without prevalent rotation-resistant rootworm populations. In some analyses, the frequency of problem fields was positively associated with planting of Cry3 corn and negatively associated with planting of Bt corn producing both a Cry3 toxin and Cry34/35Ab. The results highlight the central role of crop rotation for mitigating impacts of D. v. virgifera resistance to Bt corn."
And about the newly published research paper, “Introduced Herbivores Restore Late Pleistocene Ecological Functions” in the Proceedings of the National Academy of Sciences (PNAS).
It's the work of an 11-member international team led by Australian ecologist Erick Lundgren of the University of Technology, Sydney. The co-authors include evolutionary biologist Scott Carroll of the UC Davis Department of Entomology and Nematology.
Out-of-place and troublesome species, such as hippos, feral hogs, wild horses and burros, may actually be restoring the ecological services of extinct animals, the ecologists said.
The authors pored over scientific literature; created a list of living and extinct herbivores over the last 126,000 years; and categorized them by their body size, anatomy, habitat, diet, and how their bodies digested the vegetation. Then they compared their lifestyles in overlapping regions.
One of the studies dealt with the abandoned hippos of Colombian drug lord Pablo Escobar (1949-1993), who purchased a male and three females in the 1980s from a California zoo and kept them in fields along the Magdalena River, northwestern Colombia. Without humans and other predators decimating them, the population today is 80 to 100 and is expected to reach 800 to 5000 by 2050.
The out-of-place hippos may be filling the exotic roles of extinct massive animals, such as giant llamas and rhinoceros-sized relatives, the ecologists related.
Said Carroll: “That paleontological analysis found that, amazingly, introduced herbivores– including Pablo Escobar's escaped Colombian hippos– often match the functional traits of extinct natives better than do those missing species' closest living native relatives. In this way, the ‘out-of-place' make the world more similar to the pre-extinction past. The ‘shoot-first- and-ask-questions later' approach as a maxim is as reckless as it sounds, and it's not going to sustain our life-saving drugs, nor the species we revere or ecosystems we rely on, into the future.”
“Many introduced herbivores restore trait combinations that have the capacity to influence ecosystem processes, such as wildfire and shrub expansion in drylands,” the team wrote.
As for feral hogs in North America, Carroll said their rooting increases tree growth and attracts bird flocks, like the ecological work of their extinct ancestors. Likewise, the feral horses and burros, known for their well-digging behavior, are replacing the original American horses, which went extinct 12,000 years ago.
In their abstract, the authors pointed out that humans “have caused extinctions of large-bodied mammalian herbivores over the past 100,000 years, leading to cascading changes in ecosystems. Conversely, introductions of herbivores have, in part, numerically compensated for extinction losses. However, the net outcome of the twin anthropogenic forces of extinction and introduction on herbivore assemblages has remained unknown. We found that a primary outcome of introductions has been the reintroduction of key ecological functions, making herbivore assemblages with nonnative species more similar to preextinction ones than native-only assemblages are. Our findings support calls for renewed research on introduced herbivore ecologies in light of paleoecological change and suggest that shifting focus from eradication to landscape and predator protection may have broader biodiversity benefits.”
Carroll, who also co-led an author group of the newly published “Coevolutionary Governance of Antibiotic and Pesticide Resistance” in the journal Trends in Ecology, said that the publications together “address both sides of the human-environment co-existence issue.”
“Reading the titles, you might not expect these two studies are two sides of the same coin,” Carroll said, “but for me they address both sides of the human-environment issue that most compels me: How can we create more workable, productive and respectful long-term relationships with other species? To help think about this as an evolutionary biologist, I divide the key challenges of human interactions with Nature into those that arise from competitor and parasite species that adapt too quickly for us to control, and those that arise in in our efforts to protect more valued species– like endangered large mammals– that adapt too slowly to survive human impacts.”
“Pesticide and drug resistance are nature's predictable resilience to our reliance on an escalating war of toxic eradication,” Carroll commented. “A broader understanding shows how we can develop our own behavior to instead cultivate susceptibility to control in species we fight, using both new and known practices for improved sanitation, locally diversified agriculture, and eating lower on the food chain to inflect their evolution in a positive direction. Similarly, after millennia of driving much of the Earth's giant mammal community to extinction, we need to step back from our reflex to extinguish the errant survivors to preserve a modern sense of what's natural, without stopping to consider how these new neighbors (commonly fading from their native lands) may restore ancient ecological functions our own ancestors extinguished not so long ago.”
Carroll emphasized that “neither of these studies dismisses the serious problems irruptive populations can cause for meeting our food, health and environmental needs, nor seeks to oversimplify complex challenges. But it's actually important to work against being limited by prejudicial generalizations that lead us to sort other species into ‘good' versus ‘bad' bins. This is a sensibility that ecologists in particular should strive to cultivate. To continue to feed and shelter ourselves and remain healthy while sharing the Earth with other species, we need to develop methods that respect the tremendous information and know-how inherent in each species. I want us to do a much better job of working with that intrinsic functional diversity and adaptive potential as our best resource for advancing resilient and biodiverse ecological systems into the future.”
Carroll and his wife, UC Davis ecologist Jenella Loye, own Carroll-Loye Biological Research, Davis. They engage in public health and environmental entomology and natural product development.
(Editor's Note: The lead author of Coevolutionary Governance of Antibiotic and Pesticide Resistance is Peter Søgaard Jørgensen, who during his University of Copenhagen graduate work, spent a year at Davis studying soapberry bug host adaptation in California with Scott Carroll. The duo led the multi-year international "Living with Resistance" pursuit at the National Science Foundation's National Socio-Environmental Synthesis Center. Carroll served as the senior author.)/span>/span>
When the United Nations meets Sept. 21 in New York, they want the UN to reframe its action on the global antimicrobial drug resistance (AMR) crisis.
It's crucial. How crucial is it?
Antimicrobial drug resistance threatens both personal and planetary health and the issue is as crucial as the global threat of climate change, Carroll says.
In a paper titled “Use Antimicrobials Wisely,” published in the current edition of Nature, a nine-member international research team, including Carroll, explained their advocacy.
“We're concerned about what will happen if the proposed UN solutions focus mainly on incentives for new drug development, at a time when the drug industry itself is abandoning those efforts against infectious disease due to AMR,” said Carroll, who co-leads the international group on resistance to pesticides and antimicrobial drugs. He founded and directs the Institute for Contemporary Evolution, Davis, and is affiliated with the Sharon Lawler lab, UC Davis Department of Entomology and Nematology.
The paper, published in the Comment section, is the first product from a two-year working group sponsored by the National Socio-Environmental Synthesis Center in Annapolis, Md. “We are taking a similar socio-environmental approach in our concurrent work on pesticide stewardship,” Carroll said.
“While new drugs have a role, we think it's more important for society to learn how to steward pathogen susceptibility, so we develop that theme in the paper,” Carroll said. “And because we also depend on microbes for digestion, immunity, and general health, and microbes support ecosystem functioning through nutrient cycles and the maintenance of soil and water quality, we further argue that our AM drug habits and waste streams threaten both personal and planetary health. “
Lead authors of the paper are Peter Jorgensen of Stockholm, Sweden, and Didier Wernli of Geneva Switzerland. Jørgensen, who spent part of his Danish graduate program working with Carroll in Davis, is now a postdoctoral researcher at the Royal Swedish Academy of Science, Stockholm.
Carroll described AMR as more than a medical dilemma—it's a socio-ecological problem. “The vulnerability of pathogens to antimicrobial drugs is a communal resource, readily threatened by overuse, to be lost as a classic 'tragedy of the commons.' There is a lot of contemporary theory for social resilience in the face of socio-ecological challenges, and– linking to entomology– the early success of the pioneering management of Bt crop pest resistance evolution is an encouraging precedent.”
In its planetary health approach, the group seeks to be “more cognizant not only of preserving drug susceptibility in pathogenic microbes, but also protecting from wholesale destruction the community of microbes on which we depend for life,” Carroll said.
In the paper, the scientists pointed out that “Resistance affects animal and environmental health as well as human health, and so requires coordinated action across economic sectors. No single concern exemplifies this better than the high rate of antibiotic use in agriculture (largely as growth promoters or disease prevention).” They wrote that in the United States, 70 to 80 percent of all anti-microbials consumed are given to livestock.
An example of antimicrobial resistance involves the malaria mosquito, Anopheles gambiae. The World Health Organization (WHO) in a document, "Global Action Plan on Anti-Microbial Resistance," wrote:
"Antimicrobial resistance can affect all patients and families. Some of the commonest childhood diseases in developing countries – malaria, pneumonia, other respiratory infections, and dysentery – can no longer be cured with many older antibiotics or medicines. In lower- income countries, effective and accessible antibiotics are crucial for saving the lives of children who have those diseases, as well as other conditions such as bacterial blood infections. In all countries, some routine surgical operations and cancer chemotherapy will become less safe without effective antibiotics to protect against infections."
Expect to hear more about this alarming crisis--the global antimicrobial drug resistance crisis. Meanwhile, read the WHO Global Action Plan.
Forget the soaps; let's talk about soapberry bugs and an entomologist at the University of California, Davis, who studies them.
And why and how she decided to pursue entomology as a career. That we'll save until the end of this blog.
Doctoral candidate Meredith Cenzer of the Louie Yang lab, UC Davis just published her research on soapberry bugs, which are a classic evolutionary example of how rapidly insects can switch hosts, adapting from a native to an invasive plant.
Her research shows that soapberry bugs have not only lost adaptations to their native host plant but are regionally specializing on an invasive host.
The work, "Adaptation to an Invasive Host Is Driving the Loss of a Native Ecotype," published in the current edition of the journal Evolution, “collapses a classic and well-documented example of local adaptation,” said doctoral candidate Meredith Cenzer of the Louie Yang lab, UC Davis Department of Entomology and Nematology. The plant-host switch can lead to disruption of native plant communities and a breakdown of the ecosystem.
The players involved are the soapberry bug (Jadera haematoloma), also known as “the red-shouldered bug”; its native host plant, the balloon vine (Cardiospermum corindum), and the invasive host, the golden rain tree or Taiwanese rain tree (Koelreuteria elegans).
The study, which took place in Florida, expands on the 1989 groundbreaking research of UC Davis evolutionary ecologist and soapberry expert Scott Carroll, who documented local adaptation in beak length, survival, and development time and other traits between soapberry bugs, balloon vine and the golden rain tree in Florida.
Said Carroll: "Meredith Cenzer's findings carry an important message for those concerned with biodiversity conservation, because she shows that even highly distinct adaptive specializations can disappear rapidly due to human influence on the environment– even in cases where the key native habitat has not been lost."
The soapberry bug, which lives throughout the United States and much of the world, feeds on seeds within the soapberry plant family, Sapindaceae, which includes soapberries, boxelders and maples. Mostly black, it has red eyes, red lateral stripes on the sides of its head and red on its “shoulders” (pronotum). It is often mistaken for the boxelder bug.
“As part of my doctoral dissertation, I documented that this pattern of local adaptation has been lost in the last 27 years,” Cenzer said, “and that all populations of soapberry bugs in Florida-- even those still found on the native --are now adapted only to the invasive host.“
“Locally adapted populations are often used as model systems for the early stages of rccological speciation, but most of these young divergent populations will never become complete species,” Cenzer noted in her abstract. “The maintenance of locally adapted populations relies on the strength of natural selection overwhelming the homogenizing effects of gene flow; however, this balance may be readily upset in changing environments.”
“All populations that were adapted to the native host--including those still found on that host today--are now better adapted to the invasive host in multiple phenotypes,” she wrote in her abstract.” Weak differentiation remains in two traits, suggesting that homogenization across the region is incomplete. This study highlights the potential for adaptation to invasive species to disrupt native communities by swamping adaptation to native conditions through maladaptive gene flow.”
Cenzer characterized local adaptation as “high performance in one habitat coming at the cost of performance in other habitat types, such that populations specialized on each habitat will have higher fitness in that environment than immigrants from other habitats.”
“This results directly in two types of ecological reproductive isolation between locally adapted populations: 1) selection against migrants, who will be outcompeted by residents, and 2) selection against hybridization (if hybrids show intermediate phenotypes), as hybrid offspring will be outcompeted in each habitat by one parental type,” she wrote in her research paper. “However, such reproductive isolation relies on ongoing differential selection balanced with low rates of gene flow between habitats. In most well studied systems demonstrating local adaptation, we do not know how perturbation – either to selection pressures or gene flow – will influence the long-term stability of differentiation.”
Carroll, who maintains a website, “Soapberries of the World,” says the soapberry bugs are “very approachable native guides to how evolution is taking place on earth day.” His website shows “how evolution happens every day and why it matters.”
How did Meredith Cenzer, a native of Gainesville, Fla., become interested in entomology? We love her answer.
"I first became interested in entomology as a kid," she recalled. "The defining moment in my memory is when my gifted science teacher, Ms. Linda Osborne, told me in third grade that there are people who study insects for a living and that they're called entomologists. She was going to put me in timeout for being too loud (a lifelong problem), but told me she'd let it slide this time if I promised to become an entomologist."
"Two years later, she let me come in and teach her first graders about insects. For my first science fair project, in sixth grade, I tracked the progress of tent caterpillar aggregations; we weren't allowed to manipulate animals, so I photographed them every day and made notes on their behavior - my parents still have the poster from that one."
So, she promised her teacher she'd become an entomologist. And she kept her promise. She received her bachelor of science degree in entomology at the University of Florida in 2009.
Future plans, after receiving her doctorate in entomology from UC Davis?
“I am broadly interested in evolutionary ecology, particularly in plant-insect interactions, and the balancing roles of selection, gene flow, and plasticity on determining the phenotypes we see in nature,” she said. After receiving her doctorate in entomology from UC Davis in the fall, she will start a postdoctoral position at Florida State University with biology professor Leithen M'Gonigle, developing theory on the evolution of dispersal in patchy landscapes.
A tip of the insect net to Meredith Cenzer!
(Editor's Note: Meredith Cenzer participated in the Entomological Society of America's Linnaean Games competition in 2011. See Bug Squad blog of Nov. 22, 2011.)
And unleash the secret of soapberry bugs?
Students in the Entomology 1 class, offered by the UC Davis Department of Entomology and Nematology, studied soapberry bugs under the tutelage of evolutionary ecologists/soapberry scientists Scott Carroll and Jenella Loye. The students then created screen-printed tile mosaics (like the photo at right).
The popular class, headed by Diane Ullman, professor of entomology, UC Davis Department of Entomology and Nematology, fuses art with science. Ullman, not only a noted entomologist but an accomplished artist, co-founded and co-directed the UC Davis Art/Science Fusion Program.
Where can you see the students' art? It will be among the work featured at "The Secret World of Insects" exhibition and reception, set from 5 to 8 p.m., Wednesday, June 3 in the Third Space Art Collective, 946 Olive Drive. It's free and open to the public.
"Soapberry bugs are beautiful insects that are found in many parts of the world. Their most defining ecological characteristic is their specialized diet," Carroll says on his website, Soapberry Bugs of the World. "They feed on the seeds of the soapberry family, which includes well known plants like boxelders, maples, soapberries (or soapnuts), jacket plums, rambutans, and litchis. These plants have evolved many ways to protect their seeds from soapberry bugs: flying seeds, seeds protected in inflated spheres, seeds with cyanide, and seeds that are held unfilled on the plant for months while the bugs slowly starve. Yet these insects work around the plants' co-evolved defenses and use the seeds to fuel their own development and reproduction."
Carroll directs the UC Davis Institute for Contemporary Evolution. Both he and Loye, husband and wife, are members of the Sharon Lawler lab, UC Davis Department of Entomology and Nematology.
Ullman said that 70 students participated in the Entomology 1 class last quarter. "We had four sections," she added. They were:
- Ceramics. The students created a screen-printed tile mosaic about evolution of the soapberry bug with the support and scientific advice of Jenella Loye and Scott Carroll. Also, this quarter, self-described rock artist Donna Billick, co-founder and former co-director of the UC Davis Art/Science Fusion Program, assisted the students.
- Sculpture with reuse materials. The students made sculptural story boards about insects.
- Painting and multimedia.The students did trip tic-like canvases about a diversity of insects.
- Bioart. The students created insect drawings with fungi on agar.