Preprints (not peer-reviewed)
Hammer, T.J., Janzen, D.H., Hallwachs, W., and N. Fierer. 2017. Caterpillars lack a resident gut microbiome. bioRxiv doi:https://doi.org/10.1101/132522 (Link)
Press: Nature News, Interview on Nature Podcasts, Interview on Slightly Evolved Podcast
Peer-reviewed articles
Hammer, T.J., Fierer, N., Hardwick, B., Simojoki, A., Slade, E., Taponen, J., Viljanen, H., and T. Roslin. 2016. Treating cattle with antibiotics affects greenhouse gas emissions, and microbiota in dung and dung beetles. Proceedings of the Royal Society B 283, 20160150. (Link)
Press: New Scientist, Science Magazine, BBC News, NBC News, Huffington Post, ABC News
Antibiotics are frequently used to increase livestock growth and treat disease, especially in the US. If we think of the farm as an open ecosystem, what are the broader ecological consequences of this practice? The evolution of antibiotic resistance is a major and well-recognized problem, but in this paper, we found two additional types of effects. First, by altering the microbial milieu within the gut and dung of cows, antibiotics can increase methane emissions from manure left on pasture. This could be a major problem, as methane is a potent greenhouse gas that contributes to climate change. Second, antibiotics delivered to cattle can affect the microbiome of nontarget organisms--in this case, dung beetles. If, in turn, the microbiome is important to the well-being of these organisms, antibiotics could indirectly affect the services (such as dung burial and recycling) they provide to agroecosystems. Check out Tomas Roslin's group for future work on these interactions!
Barberán, A., Hammer, T.J., Madden, A., and N. Fierer. 2016. Microbes should be central to ecological education and outreach. Journal of Microbiology & Biology Education 17, 23-28. (Link)
In this article, we highlight that microbes have been neglected in ecological education and outreach. We also argue that there are particular benefits to including microbes in secondary school curricula, higher education, and citizen science projects, and provide some examples of how. Microbes are increasingly prominent in public discussions of antibiotic use, hygiene, climate change, vaccination, and the microbiome (not to mention disease!), so microbial education needs to keep pace!
Hammer, T.J., and M.D. Bowers. 2015. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179, 1-14. (Link)
Insect herbivores include some of the most spectacular examples of intimate and integrated host-microbe symbioses. In many cases, microbial symbionts help digest plant material, supply nutrients, or protect their host from disease. Here, Deane Bowers and I call attention to a relatively neglected additional microbial service in herbivory--the detoxification of harmful chemical compounds plants use to defend their tissues from attack. We also discuss additional types of interactions between plant chemistry, insects, and microbial symbionts. For example, why do many plant chemicals have antimicrobial effects? Is it only for protection from plant pathogens? Consider an insect herbivore that itself is immune to plant toxins, but hosts toxin-sensitive microbes that it needs for nutrition. (Although a caterpillar graces the cover of this issue of Oecologia, my subsequent work indicates that caterpillars may not have been the best choice of an insect reliant on microbes for detoxification!) However, there is gradually mounting evidence from other herbivores that these insect-microbe-plant-chemical interactions are pervasive, and important.
Hammer, T.J., Dickerson, J., and N. Fierer. 2015. Evidence-based recommendations on storing and handling specimens for analyses of insect microbiota. PeerJ 3:e1190. (Link)
Research on insect-associated microbes is booming. For practically any such study where molecular methods (such as DNA sequencing) will be used, a critical step is preservation of the insect specimens, and the microbes they may contain. If the preservation step doesn't work as it should, then all the data and analyses could be erroneous. Hence, there has been much concern over the best way to process and store insects for microbiome analyses. In collaboration with an excellent undergraduate student (J. Dickerson), I found that five different storage methods all worked well in terms of preserving insect-associated microbes, with minimal bias. Some preservatives, such as CTAB and DMSO, may be good choices for fieldwork as they are nonflammable, relatively inexpensive, and work at room temperature. This paper also suggests that insects stored for nonmicrobial purposes (e.g., museum specimens in ethanol) could still be useful for microbiome work, and that meta-analyses may be robust to cross-study differences in how insects were preserved.
Hammer, T.J., and S.A. Van Bael. 2015. An endophyte-rich diet increases ant predation on a specialist herbivorous insect. Ecological Entomology 40, 316-321. (Link)
Pick up any leaf (say, in your salad), and chances are that its tissues are teeming with fungi. What do these endophytic fungi do? Are they good, bad, or neutral for the host? Quite a bit of research has focused on the pairwise interaction between plant and fungus, and many studies have brought in other players such as herbivores or pathogens. Sunshine Van Bael and I were interested in the dynamics of this relationship considering an additional trophic level--in this case, predators of the herbivore of the plant. In a classic trophic cascade, by eating herbivores, predators indirectly benefit plants ("the enemy of my enemy is my friend")--so plants have evolved ways to increase predation. Here we found that fungal endophytes increased ant predation on a beetle herbivore, potentially providing their host plant with an indirect anti-herbivore defense. These beetles (Acromis sparsa) form literal shields made out of their feces, and there are all sorts of interesting mechanisms involving plant chemicals, fungi, and gut bacterial interactions that underlie this effect--and about which we don't have a clue!
Hammer, T.J., McMillan, W.O., and N. Fierer. 2014. Metamorphosis of a butterfly-associated bacterial community. PLOS ONE doi: 10.1371/journal.pone.0086995. (Link)
When I first became interested in microbes associated with lepidopterans (butterflies and moths), many nonscientists I talked to, including taxi drivers and canvassers at the door, would ask me whether their microbes changed during metamorphosis. This confirmed that the question was broadly interesting. I was therefore surprised to find that it had not been scientifically addressed at all, with the exception of an almost completely ignored paper from 1971. In this paper, in collaboration with Owen McMillan of the Smithsonian Tropical Research Institute, I compared the internal bacterial communities of different life stages of one species, Heliconius erato. We found that the changes in the microbiome across metamorphosis loosely parallel changes in the structure of the butterfly itself. Specifically, the microbiome simplifies in terms of diversity, and reorganizes in terms of composition, much as the caterpillar simplifies morphologically as it becomes a pupa, and reorganizes to become the adult butterfly. This result did not make it into the final publication, but I also found that caterpillars' microbiomes were much more similar to those of beetles eating the same plant, than to those of their own siblings as adult butterflies. So from a microbial perspective, caterpillars and butterflies might as well be completely different animals! Another discovery of this paper was the novel microbes we found associated with Heliconius butterflies; previously, the microbiome of any adult moth or butterfly was all but unknown. Although my recent work indicates that the caterpillar microbiome is mostly transient and unimportant to larval biology, the adult butterfly microbiome is almost certainly a different story.
Hammer, T.J., Hata, C., and J.C. Nieh. 2009. Thermal learning in the honey bee, Apis mellifera. Journal of Experimental Biology 212, 3928-3934. (Link)
My first foray into scientific research was under the mentorship of James Nieh, a biologist at UCSD. We were interested in honeybee behavior, which is highly sophisticated. The cognitive abilities of bees are especially impressive considering their small size and invertebrate status, which we do not typically associate with intelligence. It had long been known that bees can learn to associate novel stimuli (the scent of vanilla) with a reward (a drop of sugar water). These stimuli can be olfactory (such as vanilla), visual, or mechanical. We wanted to see how well bees could learn using a different sensory modality, temperature. I spent many hours strapping bees into tiny duct-tape harnesses, poking them with what is essentially a temperature-controlled stick, and recording whether they extended their tongue. Working with another undergraduate in the Nieh lab, we found that bees are really good at learning to associate both hot and cold stimuli with rewards. Bees are extremely sensitive too: they could respond to a stimulus only 0.4 degrees C above ambient temperature. This thermal learning could be an important part of honeybee communication and of foraging, and is yet another facet of the surprising intelligence of social insects.
Hammer, T.J., Janzen, D.H., Hallwachs, W., and N. Fierer. 2017. Caterpillars lack a resident gut microbiome. bioRxiv doi:https://doi.org/10.1101/132522 (Link)
Press: Nature News, Interview on Nature Podcasts, Interview on Slightly Evolved Podcast
Peer-reviewed articles
Hammer, T.J., Fierer, N., Hardwick, B., Simojoki, A., Slade, E., Taponen, J., Viljanen, H., and T. Roslin. 2016. Treating cattle with antibiotics affects greenhouse gas emissions, and microbiota in dung and dung beetles. Proceedings of the Royal Society B 283, 20160150. (Link)
Press: New Scientist, Science Magazine, BBC News, NBC News, Huffington Post, ABC News
Antibiotics are frequently used to increase livestock growth and treat disease, especially in the US. If we think of the farm as an open ecosystem, what are the broader ecological consequences of this practice? The evolution of antibiotic resistance is a major and well-recognized problem, but in this paper, we found two additional types of effects. First, by altering the microbial milieu within the gut and dung of cows, antibiotics can increase methane emissions from manure left on pasture. This could be a major problem, as methane is a potent greenhouse gas that contributes to climate change. Second, antibiotics delivered to cattle can affect the microbiome of nontarget organisms--in this case, dung beetles. If, in turn, the microbiome is important to the well-being of these organisms, antibiotics could indirectly affect the services (such as dung burial and recycling) they provide to agroecosystems. Check out Tomas Roslin's group for future work on these interactions!
Barberán, A., Hammer, T.J., Madden, A., and N. Fierer. 2016. Microbes should be central to ecological education and outreach. Journal of Microbiology & Biology Education 17, 23-28. (Link)
In this article, we highlight that microbes have been neglected in ecological education and outreach. We also argue that there are particular benefits to including microbes in secondary school curricula, higher education, and citizen science projects, and provide some examples of how. Microbes are increasingly prominent in public discussions of antibiotic use, hygiene, climate change, vaccination, and the microbiome (not to mention disease!), so microbial education needs to keep pace!
Hammer, T.J., and M.D. Bowers. 2015. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179, 1-14. (Link)
Insect herbivores include some of the most spectacular examples of intimate and integrated host-microbe symbioses. In many cases, microbial symbionts help digest plant material, supply nutrients, or protect their host from disease. Here, Deane Bowers and I call attention to a relatively neglected additional microbial service in herbivory--the detoxification of harmful chemical compounds plants use to defend their tissues from attack. We also discuss additional types of interactions between plant chemistry, insects, and microbial symbionts. For example, why do many plant chemicals have antimicrobial effects? Is it only for protection from plant pathogens? Consider an insect herbivore that itself is immune to plant toxins, but hosts toxin-sensitive microbes that it needs for nutrition. (Although a caterpillar graces the cover of this issue of Oecologia, my subsequent work indicates that caterpillars may not have been the best choice of an insect reliant on microbes for detoxification!) However, there is gradually mounting evidence from other herbivores that these insect-microbe-plant-chemical interactions are pervasive, and important.
Hammer, T.J., Dickerson, J., and N. Fierer. 2015. Evidence-based recommendations on storing and handling specimens for analyses of insect microbiota. PeerJ 3:e1190. (Link)
Research on insect-associated microbes is booming. For practically any such study where molecular methods (such as DNA sequencing) will be used, a critical step is preservation of the insect specimens, and the microbes they may contain. If the preservation step doesn't work as it should, then all the data and analyses could be erroneous. Hence, there has been much concern over the best way to process and store insects for microbiome analyses. In collaboration with an excellent undergraduate student (J. Dickerson), I found that five different storage methods all worked well in terms of preserving insect-associated microbes, with minimal bias. Some preservatives, such as CTAB and DMSO, may be good choices for fieldwork as they are nonflammable, relatively inexpensive, and work at room temperature. This paper also suggests that insects stored for nonmicrobial purposes (e.g., museum specimens in ethanol) could still be useful for microbiome work, and that meta-analyses may be robust to cross-study differences in how insects were preserved.
Hammer, T.J., and S.A. Van Bael. 2015. An endophyte-rich diet increases ant predation on a specialist herbivorous insect. Ecological Entomology 40, 316-321. (Link)
Pick up any leaf (say, in your salad), and chances are that its tissues are teeming with fungi. What do these endophytic fungi do? Are they good, bad, or neutral for the host? Quite a bit of research has focused on the pairwise interaction between plant and fungus, and many studies have brought in other players such as herbivores or pathogens. Sunshine Van Bael and I were interested in the dynamics of this relationship considering an additional trophic level--in this case, predators of the herbivore of the plant. In a classic trophic cascade, by eating herbivores, predators indirectly benefit plants ("the enemy of my enemy is my friend")--so plants have evolved ways to increase predation. Here we found that fungal endophytes increased ant predation on a beetle herbivore, potentially providing their host plant with an indirect anti-herbivore defense. These beetles (Acromis sparsa) form literal shields made out of their feces, and there are all sorts of interesting mechanisms involving plant chemicals, fungi, and gut bacterial interactions that underlie this effect--and about which we don't have a clue!
Hammer, T.J., McMillan, W.O., and N. Fierer. 2014. Metamorphosis of a butterfly-associated bacterial community. PLOS ONE doi: 10.1371/journal.pone.0086995. (Link)
When I first became interested in microbes associated with lepidopterans (butterflies and moths), many nonscientists I talked to, including taxi drivers and canvassers at the door, would ask me whether their microbes changed during metamorphosis. This confirmed that the question was broadly interesting. I was therefore surprised to find that it had not been scientifically addressed at all, with the exception of an almost completely ignored paper from 1971. In this paper, in collaboration with Owen McMillan of the Smithsonian Tropical Research Institute, I compared the internal bacterial communities of different life stages of one species, Heliconius erato. We found that the changes in the microbiome across metamorphosis loosely parallel changes in the structure of the butterfly itself. Specifically, the microbiome simplifies in terms of diversity, and reorganizes in terms of composition, much as the caterpillar simplifies morphologically as it becomes a pupa, and reorganizes to become the adult butterfly. This result did not make it into the final publication, but I also found that caterpillars' microbiomes were much more similar to those of beetles eating the same plant, than to those of their own siblings as adult butterflies. So from a microbial perspective, caterpillars and butterflies might as well be completely different animals! Another discovery of this paper was the novel microbes we found associated with Heliconius butterflies; previously, the microbiome of any adult moth or butterfly was all but unknown. Although my recent work indicates that the caterpillar microbiome is mostly transient and unimportant to larval biology, the adult butterfly microbiome is almost certainly a different story.
Hammer, T.J., Hata, C., and J.C. Nieh. 2009. Thermal learning in the honey bee, Apis mellifera. Journal of Experimental Biology 212, 3928-3934. (Link)
My first foray into scientific research was under the mentorship of James Nieh, a biologist at UCSD. We were interested in honeybee behavior, which is highly sophisticated. The cognitive abilities of bees are especially impressive considering their small size and invertebrate status, which we do not typically associate with intelligence. It had long been known that bees can learn to associate novel stimuli (the scent of vanilla) with a reward (a drop of sugar water). These stimuli can be olfactory (such as vanilla), visual, or mechanical. We wanted to see how well bees could learn using a different sensory modality, temperature. I spent many hours strapping bees into tiny duct-tape harnesses, poking them with what is essentially a temperature-controlled stick, and recording whether they extended their tongue. Working with another undergraduate in the Nieh lab, we found that bees are really good at learning to associate both hot and cold stimuli with rewards. Bees are extremely sensitive too: they could respond to a stimulus only 0.4 degrees C above ambient temperature. This thermal learning could be an important part of honeybee communication and of foraging, and is yet another facet of the surprising intelligence of social insects.
