Lee Dyer, Professor, ; Lee Dyer Professor and Director PhD program Ecology, Evolution and Conservation Biology

Transcription

1 TROPHIC INTERACTIONS, BIODIVERSITY, AND CLIMATE CHANGE LEE DYER, ANGELA SMILANICH, CHRIS JEFFREY, LORA RICHARDS, JANE DELL, ANDREA GLASSMIRE, NICK PARDIKES, DANIELLE SALCIDO, TOM WALLA ECOLOGY, EVOLUTION, AND CONSERVATION BIOLOGY, UNIVERSITY OF NEVADA, RENO EARTHWATCH EXPEDITIONS, 1-JUNE TO 31-DECEMBER, 2016 PAGE 1

2 Lee Dyer Professor and Director PhD program Ecology, Evolution and Conservation Biology 28-May, 2017 Dear Volunteers, Thanks to your unique contributions, the 2016 field season was successful and fun. It included multiple trips to 4 of our research sites and 7 excellent research teams in California, Nevada, Arizona, Florida, Alabama, Costa Rica, and Ecuador. As a group, our teams in 2016 quantified herbivory and parasitism, discovered new species, and documented complex relationships between climate, plants, plant chemistry, caterpillars, parasitoids, interaction diversity, and ecosystem services. The sites where we worked offered great experiences in deserts, forests, and grasslands, and our exciting discoveries were balanced by insect bites, extreme heat, rainy days, and long hours. It was all worth it. I can t say enough how grateful I am for your help on our small project, and I hope that the positive consequences of our data continue to grow. One great accomplishment for 2016 was that two PhD students in my laboratory, who have helped lead a combined 18 Earthwatch teams, finished their doctoral work and were just awarded their PhDs this month (May 2017). If you were at the Ecuador or Great Basin sites, you met these (former) students: Dr. Nick Pardikes and Dr. Andrea Glassmire. Those students each published important papers with Earthwatch data, including one very nice paper by Glassmire in the high-impact journal New Phytologist, entitled, Intraspecific phytochemical variation shapes community and population structure for specialist caterpillars. This paper is fairly complex and includes state-of-the-art genetic and chemistry data (genomics and metabolomics), along with our special labor-of-love caterpillar rearing data. We found that special genes and special chemical compounds predict unique caterpillar communities at higher elevations in Ecuador, which is consistent with our predictions about how climatic conditions have very strong effects on biotic communities. Information like this will help us understand how biodiversity is responding to climate change and how we can manage natural and agricultural ecosystems to buffer against warming and increases in extreme weather events. I ve included a lot more information in this report and results from all of the sites. I hope that you are all able to find something interesting in our results. Hopefully the report will provide you with a sense of how successful the Climate Change and Caterpillars project has been because of your hard work. I will always be impressed with the amount of high quality data that Earthwatch volunteers have collected with us over the past decades. In the face of continual bad news about increases in extreme weather events, rising sea levels, massive extinctions, and loss of our favorite habitats, it is important to continue the hard work of documenting and protecting the amazing diversity that will persist, despite substantive human impacts. My collaborators and I have enjoyed working with all of you! Please feel free to keep in touch and we will do our best to respond. Hopefully we'll see you again in the field. Sincerely, Lee Dyer, Professor, ; ldyer@unr.edu Ecology, Evolution, Conservation Biology University of Nevada, Reno/0314 Reno, Nevada PAGE 2

3 SUMMARY As a collaborative group of 7 Earthwatch teams, we collected over 1,400 caterpillars at 7 sites (Sierra Nevada, Great Basin, Arizona, Alabama, Florida, Costa Rica, Ecuador), reared out over 350 parasitic flies and wasps, discovered new phytochemicals, discovered dozens of novel interactions, and published a dozen papers with 2016/2017 publication dates. Our papers demonstrate the complex mechanisms by which climate change can cause damaging decreases in biodiversity and again provide an impetus to document the vast unknown biodiversity on earth in this case plant chemical diversity and insect diversity. We made progress towards documenting this biodiversity and continued to discover new interactions, new phytochemicals, and new species of insects at all of our sites. GOALS, OBJECTIVES, AND RESULTS Objective 1: Determine how climate change and other global change parameters affect biodiversity. We continue to make progress towards our long-term goals of determining effects of hurricanes, climatic variation, and other large scale disturbances on interaction diversity through our modeling approach and through empirical data (Scherrer et al. 2016). Our models, including analytical, simulation, and statistical approaches are being parameterized using all of the Earthwatch data from all of our sites (e.g., see Dyer and Forister 2016). One particularly exciting result that is important for enhancing these models addresses questions that are seemingly unrelated to the climate-change-biodiversity crisis: What are the consequences of changes in plant chemistry across climatic (elevation and precipitation) gradients? How do caterpillars and parasitoids respond? How does tritrophic network structure change? What are the consequences for biodiversity and ecosystem management? In 2016, we used 18 years of Earthwatch data in Costa Rica and Ecuador to address these questions and published 8 papers (2016/2017) in top journals about these topics (Rodríguez-Castañeda et al. 2016, Stireman et al. 2017, Dell et al. 2017, Massad et al. 2017, Glassmire et al. 2016, Hansen et al. 2016, Smilanich et al. 2016, Scherrer et al. 2016). For example, for a special group of rainforest plants at our Costa Rica and Ecuador sites, the wild peppers (Piper spp., Piperaceae), we found that the concentration and types of different toxins vary predictably with climate across an elevational gradient (Figure 1). We determined that there were genetic changes across this elevation/climate gradient and that the changes in chemistry as you move downslope (i.e. more like future climate scenarios) result in lower caterpillar and parasitoid diversity and lower levels of caterpillar and parasitoid specialization. Previously we had published results showing that more potent toxins increase in response to higher temperatures and increasing CO 2 concentrations or lower phytochemical diversity (Dyer et al. 2013). Thus, it is likely that the high correlation between plant chemical diversity and insect diversity is being strongly disrupted by climate change parameters. Taken together, these published results are another example demonstrating the complex mechanisms by which climate change can cause damaging decreases in biodiversity and again provide an impetus to document the vast unknown biodiversity on earth in this case plant chemical diversity and insect diversity (see also Smilanich et al and Glassmire et al. 2016). We also made progress towards documenting PAGE 3

4 this biodiversity and continued to discover new interactions, new phytochemicals, and new species of insects at all of our sites. Finally, we contributed an important paper, inspired and parameterized by our Earthwatch data, to help clarify a debate about whether or not summer populations of monarch butterflies are in decline in response to climate change. It is still not clear what those populations are doing, but we do know that we have almost no data on the effects of changing plant chemistry, parasitoid diversity, and other natural enemies on these special butterflies (Dyer and Forister 2016) and these are the exact data that Earthwatch teams are collecting. We continue to model the importance of interaction diversity as buffers to climate change and disruptive effects of losing biodiversity and we plan to continue the research over the coming decades. Figure 1. Using genomics methods (upper left panel) and principal components analysis (upper right panel), we found that geometrid caterpillars (here, Eois encina) were genetically distinct based on different climatic conditions (different elevations a genetically distinct group of caterpillars at higher elevations is circled in the lower left panel). This genetic differentiation was associated with distinct chemistry (prenylated benzoic acid concentrations increased at the highest elevations, lower right panel). This change of chemistry under different climatic conditions was also associated with less rich caterpillar communities, and considerably lower parasitism rates at the warmer, drier (lower elevation) sites. Our Earthwatch teams in Costa Rica and Ecuador collected data and specimens for this project, the Earthwatch teams in Nevada helped with the chemistry. PAGE 4

5 Objective 2: Determine how hurricanes and variation in climate affect levels of parasitism and caterpillar densities. Models of climate change have predicted greater frequency and duration of droughts and floods and a widespread increase in the frequency of extreme weather events (e.g., Rahmstorf and Coumou 2011). Such increased unpredictability and variability in regional climates will likely impact all aspects of biodiversity, including interactions between plants, caterpillars, and their natural enemies. As we reported in previous Earthwatch reports, our hurricane damaged sites have experienced outbreaks by a dozen different caterpillar species that reached outbreak proportions in response to storm damage. This is part of a general pattern for which outbreaks are more likely at sites which experience more variance in precipitation (Stireman et al. 2005). One clear consequence of climate change and increased drought is that fires are increasing in intensity and frequency in arid regions and decreasing in other regions that are more fire adapted (Moritz et al. 2012). At our Florida, Great Basin, and Sierra Nevada sites, Earthwatch volunteers helped us examine the relationship between fire and plant and insect diversity. For Eglin Air Force Base, which is the last extensive area of protected longleaf pine forest, we used Earthwatch plot data and previous diversity data to examine fire and spatial patterns of diversity. As with all ecological relationships, our results are complex, but they provide insight into how plant diversity can be maintained by healthy fire intervals (Figure 2). We are still attempting to do the same type of analysis for caterpillars and their enemies for the North American sites, but we still have plenty of work to do to predict how insects and interactions are associated with different levels of fire. More generally, and relevant to all of our sites, we are modeling how disturbance in general (not just fire) affects trophic interactions. In addition to the modeling approaches mentioned in Objective 1, we continue to document the details of phenological asynchrony between parasitoids and their hosts when weather events such as floods and droughts create temporal shifts in caterpillar populations such that they are unavailable to specialized wasp parasitoids during their host-searching phase (Stireman et al. 2005). To this end, we hope to accumulate at least 3 more years of data to provide informationrich time series to allow us to determine which subfamilies and genera of parasitoids are most affected by specific extremes in weather. PAGE 5

6 Figure 2. Summary of a structural equation model that shows relationships between fire, our measures of forest attributes, and understory plant diversity at our Florida Earthwatch site. Overstory, midstory, understory, and surface densities were quantified using satellite data (LIDAR). Positive effects are shown with blue headed arrows and negative correlations in red lines. Line thickness corresponds to strength of the relationship. Black dashed line represents total indirect effects of fire on diversity. Although the relationships are complex, the effects of fire on plant diversity are very clear and are likely to be affected by increases in drought. Earthwatch teams in Florida, Arizona, and the Sierra Nevada will continue to examine how plant chemistry, arthropods, and interactions are affected by fire frequency. PAGE 6

7 Objective 3: Specialization, trophic interactions, and biodiversity The diet breadth (number of food plants) of insects has been a focal point for understanding current levels of biodiversity, which are increasingly threatened by global change. Estimates of species richness (counts of the numbers of species in an area) that are published for the most diverse forests on earth are only crude approximations, and the methods for estimating biodiversity rely on poor natural history data and untested assumptions about herbivore specialization (Basset et al. 2012). For years our Earthwatch data have facilitated investigation of specialization and co-diversification across multiple trophic levels, a long-standing challenge in biodiversity research and evolutionary theory. In 2015 we made excellent progress towards documenting specialization across climatic and latitudinal gradients, and we published a half dozen papers about this topic in 2016/2017 (Rodríguez-Castañeda et al. 2016, Stireman et al. 2017, Massad et al. 2017, Hansen et al. 2016, Smilanich et al. 2016, Scherrer et al. 2016). In these papers we report strong pattern of relationships between climate, plant chemistry, and specialization. Along with these published results, we completed numerous quantitative food webs for all of our Earthwatch sites (e.g., Figure 3 for Juniper feeders in Arizona). These networks provide a quantitative summary of interaction diversity and provide a baseline for examining how interactions will change with future disturbances and changes in climate. Figure 3. First ever Juniper tritrophic network! Each bottom bar is a juniper species, each middle bar is a caterpillar species, and each of the top bars is a parasitoid species. The thickness of the lines indicates the abundance of that particular interaction. PAGE 7

8 As we have reported in past years, another significant accomplishment for 2016 came in the form of new species and new chemistry discoveries. For example, we reported on how three new chemical compounds (discovered by our team) at our Ecuador site are responsible for structuring populations of caterpillars and their associated parasitoids (Glassmire et al. 2016), which is a significant discovery. We have reported in many other papers that plant chemistry changes with increases in temperature and CO 2 (Dyer et al. 2012), and this paper shows similar changes across an elevational gradient. Chemical compounds produced by plants are not only responsible for the plants unique flavors, aromas, and colors, but also possible deterrent or toxic properties and resistance to herbivores (e.g., Hansen et al. 2016). Also similar to previous years, in 2016, we attempted to improve our sister sites to caterpillars.org most notably the site created in collaboration with the Encyclopedia of Life (EOL). The URL for the site is: Both of these websites are in serious need of updates, and we plan to completely revamp them in the next two years, with the help of volunteers. In addition to updates to the life history data and images newly available on the web, we published several new life history descriptions for our focal taxa, many of which are the first biological information known for particular genera. We continue to rear out new species from the project at a rapid rate and we continue to publish species descriptions for as many of these as possible (Figures 4, 5, 6). At the Arizona site volunteers contributed to the Western North America caterpillar guide, the sequel to Dave Wagner s Eastern Caterpillars book. Finally, we were awarded a grant from the National Science Foundation (NSF) to integrate images of all our adult specimens (e.g., Figure 5) with all other museums in North America this effort is called "LepNet" and is summarized in Seltmann et al. (2017). And a final fun result! We found that insects can hear fire (Figure 7) and avoid it by walking up the boles of trees. We hope to find out more about this adaptation to fire in the near future as we continue to address questions about climate-induced changes in fire frequency across terrestrial ecosystems. PAGE 8

9 Figure 4. A representative sample of the caterpillar communities and new network associations uncovered at the Great Basin and Arizona Earthwatch sites. The juniper caterpillar and parasitoid communities were completely unknown before we started this project. This type of discovery of new life histories and interactions is common at all of our sites. PAGE 9

10 Figure 5. Adults of some Earthwatch-reared caterpillars from Juniperus species in Arizona and the Great Basin. In 2016 we sequenced genes from these caterpillars to help identify the species that we have reared. Most species have been described previously based on adult specimens, but there was no existing information on the immature stages (Figure 4), the host plant affiliations, and the parasitoids (Figure 6). PAGE 10

11 Figure 6. Parasitoids from caterpillars of some Earthwatch-reared caterpillars from Juniperus species in Arizona and the Great Basin. All of the parasitoids that we have reared at all of our sites represent new host information and some are new species to science. PAGE 11

12 Figure 7. Experiment to determine arthropod movement during fires. Upper left shows sticky trap installed on longleaf pine tree pre-ignition. Traps were located both within burn units and in paired unburned control sites. Photo on right shows sticky trap contents collected during a fire from within a burn unit. Arthropods were engaged in vertical dispersal as indicated by their orientation which is preserved upon contact with the trap. Figure: Traps within burn units captured 615% more arthropods than control traps in unburned units showing a clear pattern of an adaptive arthropod behavior to fire by way of upward movement. In forests with lowintensity surface fires and short residence times, such as those found in longleaf pine systems, severity is lower in the canopy with cooler temperatures and reduced combustion compared with the understory. Thus, it is likely that arthropods may move upwards towards the canopy and cooler temperatures. This may allow them to survive the burn, and subsequently recolonize the burned area below via a downward migration. PAGE 12

13 PROJECT IMPACTS 1. Increasing Scientific Knowledge a) Total citizen science research hours Provide an estimate for the number of hours per day that volunteers spent collecting data, being trained to collect data in the field, and performing data entry. b) Peer-reviewed publications 380 hours spread over 7 teams. Dyer, L.A., C.S. Philbin, K.M. Ochsenrider, L.A. Richards, T.J. Massad, A.M. Smilanich, M.L. Forister, T.L. Parchman, L. Galland, P.J. Hurtado, A.E. Espeset, A.E. Glassmire, J.G. Harrison, C. Mo, S. Yoon, N.A. Pardikes, N.D. Muchoney, J.P. Jahner, H.L. Slinn, O. Shelef, and C.S. Jeffrey. Modern Chemical Ecology Theory for Plant Insect Interactions. Nature Chemistry Reviews. In press. Stireman III, J.O., Dyer, L.A., and Greeney, H.F Specialized generalists? Food web structure of a tropical tachinid-caterpillar community? Insect Conservation and Diversity doi: /icad Dell, J.E., O Brien, J.J., Doan, L., Richards, L.A., and Dyer, L.A An arthropod survival strategy in a frequently burned forest. Ecology. In press. Massad, T. J., Martins de Moraes, M., Philbin, C., Oliveira, C., Cebrian Torrejon, G., Fumiko Yamaguchi, L., Jeffrey, C. S., Dyer, L. A., Richards, L. A. and Kato, M. J Similarity in volatile communities leads to increased herbivory and greater tropical forest diversity. Ecology doi: /ecy Seltmann, K.C., Cobb, N.S., Gall, L.F., Bartlett, C.R., Basham, M.A., Betancourt, I., Bills, C., Brandt, B., Brown, R.L., Bundy, C., Dyer, L.A., Pardikes, N., et al., LepNet: The Lepidoptera of North America Network. Zootaxa 4247: Richards, L.A., Glassmire, A.E., Ochsenrider, K.M., Smilanich, A.M., Dodson, C.D., Jeffrey, C.S. and Dyer, L.A Phytochemical diversity and synergistic effects on herbivores. Phytochemistry Reviews 15: Glassmire, A. E., Jeffrey, C. S., Forister, M. L., Parchman, T. L., Nice, C. C., Jahner, J. P., Wilson, J. S., Walla, T. R., Richards, L. A., Smilanich, A. M., Leonard, M. D., Morrison, C. R., Simbaña, W., Salagaje, L. A., Dodson, C. D., Miller, J. S., Tepe, E. J., Villamarin- Cortez, S. and Dyer, L. A Intraspecific phytochemical variation shapes community and population structure for specialist caterpillars. New Phytologist 212: PAGE 13

14 Rodríguez-Castañeda, G., Brehm, G., Fiedler, K. and Dyer, L.A., Ant predation on herbivores through a multitrophic lens: how effects of ants on plant herbivore defense and natural enemies vary along temperature gradients. Current Opinion in Insect Science 14: Hansen, A.C., A.E. Glassmire, L.A. Dyer, and A.M. Smilanich Cascading effects of diet induced variation in the immune response of two specialist herbivores. Ecography. Smilanich, A.M., R.M. Fincher, and L.A. Dyer Does plant-apparency matter? Insights from 30 years of data reveal clear patterns of the effects of plant chemistry on herbivores. New Phytologist 210: Scherrer, S., C. Lepesqueur, M.C. Vieira, M. Almeida-Neto, L.A. Dyer, M.L. Forister, I. Rezende Diniz Seasonal variation in host plant specialization by folivorous lepidopterans: contrasting patterns at the species and community levels. Biotropica 48: Dyer, L.A. and M.L. Forister Wherefore and whither the modeler: understanding the population dynamics of monarchs will require integrative and quantitative techniques. Annals of the Entomological Society of America 109: c) Presentations: "Biological control of the diamondback moth, Plutella xylostella, using various natural predators.", S. Pema, A. Smilanich, L. Dyer, L. A. Robinson, International Congress of Entomology, ICE. (September 30, 2016). "Phytochemistry and immunity influence local and regional networks of host-parasite-pathogen interactions.", L. Dyer, A. Smilanich, et. al., International Congress of Entomology, ICE. (September 30, 2016). "Modern natural history versus "networks": A view of chemically mediated trophic interactions at local, regional, and global scales.", L. Dyer, et. al., Annual meeting, Ecological Society of America, ESA. (August 12, 2016). "Phytochemical diversity and synergistic effects", L. A. Robinson, L. Dyer, et. al., Annual meeting, Ecological Society of America, ESA. (August 12, 2016). "Despite decreased immune function caterpillars continue to feed on the heavily defended tropical plant Piper.", H. Slinn, L. Dyer, et. al., Annual meeting, Ecological Society of America, ESA. (August 8, 2016). "Adventures across the Americas discovering associations between climate and biodiversity.", L. Dyer, Tyson Summer Seminar Series in Ecology and Evolution, Tyson Research Center. (July 28, 2016). "Interacciones Multritróficas asociadas a Piper lepidópteros hospederos- parasitoides en un contexto de Cambio Climático.", L. Dyer, Public Seminar, Estación Biológica La Selva, Costa Rica. (January 11, 2016). "Redes locais e globais em ecologia e evolução.", L. Dyer, invited departmental seminar, University of Brasilia. (January, 2016). PAGE 14

15 2. Mentoring a) Graduate students List graduate students doing thesis work on the project Student Name Graduate Degree Project Title Anticipated Year of Completion Andrea Glassmire PhD Causes and consequences of intraspecific phytochemical variation on the physiology, abundance, and diversity of specialist consumers Nick Pardikes PhD Determinants of interaction diversity in Juniper woodlands Jane Dell PhD Untangling patterns of diversity in a fire forest: Spatiotemporal influence and interactions Danielle Salcido PhD Global change, citizen science, and effective outreach for all ages Heather Slinn PhD Tritrophic interactions mediated by chemistry and fungal endophytes. Tara Langus MS Roles of pathogens, beneficial microbiota, and plant chemistry in the immune response of caterpillars b) Community outreach Provide details on how you have supported the development of environmental leaders in the community in which you work. Name of school, organization, or group Education level Participants local or non-local Details on contributions/ activities Nevada Bugs and Butterflies All levels local Worked with Earthwatch volunteers and uses Earthwatch data as part of general outreach. Daugherty Summer Science Exploration K-9 local Worked with Earthwatch volunteers in the field. UNR Museum All levels local Earthwatch volunteers assisted with National Pollinator Week activities. PAGE 15

16 3. Partnerships list your current active professional partnerships that contribute to your project and indicate the type of support these partners provide Partner Support Type(s) 1 Years of Association (e.g present) Serra Bonita Reserve, Bahia, Brazil Fundo Genova, Chanchamayo, Peru Organization for Tropical Studies Smithsonian National Museum of Natural History (UNMSM) American Museum of Natural History Museo de Historia Natural, Lima, Peru Museo Ecuatoriano de Ciencias Naturales (MECN) University of Nevada Natural History Museum partners in research, access to specimens, accepts voucher specimens in museum, contributes to conservation goals partners in research, access to specimens, contributes to conservation goals partners in research, access to specimens, contributes to conservation goals partners in research, provides space and access to specimens, accepts voucher specimens in museum partners in research, provides space and access to specimens, accepts voucher specimens in museum partners in research, provides space and access to specimens, accepts voucher specimens in museum partners in research, provides space and access to specimens, accepts voucher specimens in museum partners in research, provides space and access to specimens, accepts voucher specimens in museum 2014-present 2013-present 1991-present 2004-present 2004-present 2012-present 2002-present 2015-present University of Brasilia partners in research, access to specimens 2008-present FAPESP Sao Paulo Research Foundation Conselho Nacional de Desenvolvimento Científico e Tecnológico Yanayacu Biological Station Southern Research Station, USFS provides additional funding and contributes to outreach goals provides additional funding and contributes to outreach and training goals (Science without Borders) partners in research, contributes to conservation and outreach goals provide funding for the Florida site, collaborate, contribute to management plans for Eglin 2014-present 2013-present 2001-present 2012-present PAGE 16

17 4. Conserving natural and sociocultural capital a) Conservation of ecosystems In the past year, has your project helped conserve or restore habitats? If so, please describe below. Habitat type Habitat significance 7 Description of contribution Resulting effect 8 Cloud forest b) Ecosystem services Extremely high levels of diversity and endemism. Providing an economic incentive for managing lands for biodiversity by supporting the only research station in the area and providing long-term employment to local citizens. Yanayacu Biological Station and surrounding lands are still protected from logging, grazing, and development. Indicate which ecosystem service categories you are directly studying in your Earthwatch research and provide further details in the box below. Food and water Flood and disease control Spiritual, recreational, and cultural benefits Nutrient cycling Details: We continued to utilize a methodology that combined data using completely standardized methods in Costa Rica, Ecuador, Brazil, Argentina, Peru, and the United States to create plant-caterpillar-parasitoid diversity databases that can be used by land managers to search for natural enemies of agricultural pests and to examine relationships between enemy diversity and outbreak potential. Parasitoids provide an important, yet mostly unquantified ecosystem service that needs to be documented globally before it is enhanced, restored, or maintained. ACKNOWLEDGEMENTS We first thank all of the amazing volunteers for hard work, patience, sharing their skills, and producing high quality ecological data and natural history observations. The support of the quality staff at Earthwatch Institute is also greatly appreciated. This study was co-funded by NSF grants DEB , DEB , DEB , DEB , DEB , DEB , DEB , the Department of Defense, and the University of Nevada. Our projects would not have functioned without expert assistance from many field technicians and colleagues who helped in the field and laboratory, gave lectures to volunteers, and discussed ideas with us; these include: M. Forister, T. Parchman, P. Poopat, C. Morrison, A. Palmer, M. Robinson, G. Blaustein, W. Lumpkin, J. Miller, S. Rab-Green, J. Jahner, R. Lindgren, A. Dietrick, R. Hazen, H. Greeney, D. Wagner, M. Singer, L. Salazar Vega, W. Simbaña, J. Simbaña, T. Walla, K. Fredrickson, T. Barber, H. Garcia Lopez, W. Simbaña, M. Ryan, M. Fox, T. Massad, And C. Pearson. PAGE 17

18 LITERATURE CITED Dell, J.E., O Brien, J.J., Doan, L., Richards, L.A., and Dyer, L.A An arthropod survival strategy in a frequently burned forest. Ecology. In press. Dyer, L.A. and M.L. Forister Wherefore and whither the modeler: understanding the population dynamics of monarchs will require integrative and quantitative techniques. Annals of the Entomological Society of America 109: Dyer, L.A., C.S. Philbin, K.M. Ochsenrider, L.A. Richards, T.J. Massad, A.M. Smilanich, M.L. Forister, T.L. Parchman, L. Galland, P.J. Hurtado, A.E. Espeset, A.E. Glassmire, J.G. Harrison, C. Mo, S. Yoon, N.A. Pardikes, N.D. Muchoney, J.P. Jahner, H.L. Slinn, O. Shelef, and C.S. Jeffrey. Modern Chemical Ecology Theory for Plant Insect Interactions. Nature Chemistry Reviews. In press. Dyer, L.A., Richards, L.A., Short, S. A., Dodson, C.D Effects of CO 2 and temperature on tritrophic interactions. PLOS ONE 8(4): e Dyer, L.A., T.J. Massad, and M.L. Forister The question of scale in trophic ecology. Pages in: Hanley, T. and K. La Pierre (eds.). Trophic Ecology: Bottom-Up and Top-Down Interactions across Aquatic and Terrestrial Systems. Cambridge University Press, Cambridge, MA. Forister, M. L., Novotny, V., Panorska, A. K., Baje, L., Basset, Y., Butterill, P. T., Cizek, L., Coley, P. D., Dem, F., Diniz, I. R., Drozd, P., Fox, M., Glassmire, A., Hazen, R., Hrcek, J., Jahner, J. P., Kama, O., Kozubowski, T. J., Kursar, T. A., Lewis, O. T., Lill, J., Marquis, R. J., Miller, S. E., Morais, H. C., Murakami, M., Nickel, H., Pardikes, N., Ricklefs, R. E., Singer, M. S., Smilanich, A. M., Stireman, J. O., Villamarín-Cortez, S., Vodka, S., Volf, M., Wagner, D. L., Walla, T., Weiblen, G. D., and L. A. Dyer Global distribution of diet breadth in insect herbivores. Proceedings of the National Academy of Sciences 112: Glassmire, A. E., Jeffrey, C. S., Forister, M. L., Parchman, T. L., Nice, C. C., Jahner, J. P., Wilson, J. S., Walla, T. R., Richards, L. A., Smilanich, A. M., Leonard, M. D., Morrison, C. R., Simbaña, W., Salagaje, L. A., Dodson, C. D., Miller, J. S., Tepe, E. J., Villamarin-Cortez, S. and Dyer, L. A Intraspecific phytochemical variation shapes community and population structure for specialist caterpillars. New Phytologist 212: Greeney, H.F., R. Meneses, C.E. Hamilton, E.R. Hough, E.K. Austudillo, E. Lichter-Marck, R.W. Mannan, N. Snyder, H. Snyder, C.M. Ripplinger, S.M. Wethington, and L.A. Dyer Traitmediated trophic cascade creates enemy-free space for nesting hummingbirds. Science Advances - 1, e Hansen, A.C., A.E. Glassmire, L.A. Dyer, and A.M. Smilanich Cascading effects of diet induced variation in the immune response of two specialist herbivores. Ecography. Lewinsohn E, Gijzen M Phytochemical diversity: The sounds of silent metabolism. Plant Sci. 176: PAGE 18

19 Massad, T. J., Martins de Moraes, M., Philbin, C., Oliveira, C., Cebrian Torrejon, G., Fumiko Yamaguchi, L., Jeffrey, C. S., Dyer, L. A., Richards, L. A. and Kato, M. J Similarity in volatile communities leads to increased herbivory and greater tropical forest diversity. Ecology doi: /ecy Moritz, M.A., Parisien, M.A., Batllori, E., Krawchuk, M.A., Van Dorn, J., Ganz, D.J. and Hayhoe, K., Climate change and disruptions to global fire activity. Ecosphere, 3:1-22. Pardikes, N.A., A.M. Shapiro, L.A. Dyer, and M.L. Forister Global weather and local butterflies: variable responses to a large-scale climate pattern along an elevational gradient. Ecology 96: Rahmstorf, S. and Coumou, D., Increase of extreme events in a warming world. Proceedings of the National Academy of Sciences, 108(44), pp Richards, L.A., Glassmire, A.E., Ochsenrider, K.M., Smilanich, A.M., Dodson, C.D., Jeffrey, C.S. and Dyer, L.A Phytochemical diversity and synergistic effects on herbivores. Phytochemistry Reviews 15: Richards, L.A., L. A. Dyer, M.L. Forister, A.M. Smilanich, C.D. Dodson, M.D. Leonard and C. S. Jeffrey Phytochemical diversity drives tropical plant-insect community diversity. Proceedings of the National Academy of Sciences 112: Rodríguez-Castañeda, G., Brehm, G., Fiedler, K. and Dyer, L.A., Ant predation on herbivores through a multitrophic lens: how effects of ants on plant herbivore defense and natural enemies vary along temperature gradients. Current Opinion in Insect Science, 14: Scherrer, S., C. Lepesqueur, M.C. Vieira, M. Almeida-Neto, L.A. Dyer, M.L. Forister, I. Rezende Diniz Seasonal variation in host plant specialization by folivorous lepidopterans: contrasting patterns at the species and community levels. Biotropica. Seltmann, K.C., Cobb, N.S., Gall, L.F., Bartlett, C.R., Basham, M.A., Betancourt, I., Bills, C., Brandt, B., Brown, R.L., Bundy, C., Dyer, L.A., Pardikes, N., et al., LepNet: The Lepidoptera of North America Network. Zootaxa 4247: Smilanich, A.M., R.M. Fincher, and L.A. Dyer Does plant-apparency matter? Insights from 30 years of data reveal clear patterns of the effects of plant chemistry on herbivores. New Phytologist 210: Stireman III, J.O., Dyer, L.A., and Greeney, H.F Specialized generalists? Food web structure of a tropical tachinid-caterpillar community? Insect Conservation and Diversity doi: /icad Stireman III, J.O., L.A. Dyer, D.H. Janzen, M.S. Singer, J.T. Lill, R.J. Marquis, R.E. Ricklefs, G.L. Gentry, W. Hallwachs, P.D. Coley, J.A. Barone, H.F. Greeney, H. Connahs, P. Barbosa, H.C. Morais, and I.R. Diniz Climatic unpredictability and caterpillar parasitism: implications of global warming. Proceedings of the National Academy of Sciences 102: PAGE 19