Water availability drives urban tree growth responses to herbivory and warming

Journal of Applied Ecology

Volumn 55, Issue 4, 2018, Pages 1701-1713

  Meineke, Emily K ^a   Frank, Steven D ^b  

^a HARVARD UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

climate change; herbivory; trees; urban heat island effect; warming; water relations

Indexed keywords

ABUNDANCE; CARBON SEQUESTRATION; CLIMATE CHANGE; DECIDUOUS TREE; ENVIRONMENTAL MANAGEMENT; GLOBAL CHANGE; GLOBAL WARMING; GROWTH; GROWTH RESPONSE; HEAT ISLAND; HERBIVORY; SURVIVAL; URBAN AREA; URBAN FORESTRY; URBAN POPULATION; URBANIZATION; WATER AVAILABILITY; WATER STRESS;

UNITED STATES;

HEMIPTERA; HEXAPODA; QUERCUS; QUERCUS PHELLOS;

EID: 85043579443     PISSN: 00218901     EISSN: 13652664     Source Type: Journal    
DOI: 10.1111/1365-2664.13130     Document Type: Article

References (62)

1. Abrams, M. D. (1990). Adaptations and responses to drought in Quercus species of North-America. Tree Physiology, 7, 227–238. https://doi.org/10.1093/treephys/7.1-2-3-4.227
2. Akbari, H., Pomerantz, M., & Taha, H. (2001). Cool surfaces and shade trees to reduce energy use and improve air quality in urban areas. Solar Energy, 70, 295–310. https://doi.org/10.1016/S0038-092X(00)00089-X
3. Angilletta, M. J. (2009). Thermal adaptation: A theoretical and empirical synthesis. Oxford: Oxford University Press. https://doi.org/10.1093/acprof:oso/9780198570875.001.1
4. Banfield-Zanin, J. A., & Leather, S. R. (2015). Drought intensity and frequency have contrasting effects on development time and survival of the green spruce aphid. Agricultural and Forest Entomology, 17, 309–316. https://doi.org/10.1111/afe.12109
5. Bennett, J. M., Cunningham, S. C., Connelly, C. A., Clarke, R. H., Thomson, J. R., & Mac Nally, R. (2013). The interaction between a drying climate and land use affects forest structure and above-ground carbon storage. Global Ecology and Biogeography, 22, 1238–1247. https://doi.org/10.1111/geb.12083
6. Brzostek, E. R., Dragoni, D., Schmid, H. P., Rahman, A. F., Sims, D., Wayson, C. A., & Phillips, R. P. (2014). Chronic water stress reduces tree growth and the carbon sink of deciduous hardwood forests. Global Change Biology, 20, 2531–2539. https://doi.org/10.1111/gcb.12528
7. Camacho, E. R., Chong, J.-H., Braman, S. K., Frank, S. D., & Schultz, P. B. (2017). Life history of Parthenolecanium spp. (Hemiptera: Coccidae) in urban landscapes of the southeastern United States. Journal of Economic Entomology, 110, 1668–1675. https://doi.org/10.1093/jee/tox170
8. Cavender-Bares, J., & Bazzaz, F. (2000). Changes in drought response strategies with ontogeny in Quercus rubra: Implications for scaling from seedlings to mature trees. Oecologia, 124, 8–18. https://doi.org/10.1007/PL00008865
9. Choat, B., Jansen, S., Brodribb, T. J., Cochard, H., Delzon, S., Bhaskar, R., & Zanne, A. E. (2012). Global convergence in the vulnerability of forests to drought. Nature, 491, 752–755.
10. Chung, H., Muraoka, H., Nakamura, M., Han, S., Muller, O., & Son, Y. (2013). Experimental warming studies on tree species and forest ecosystems: A literature review. Journal of Plant Research, 126, 447–460. https://doi.org/10.1007/s10265-013-0565-3
11. Coffelt, M. A., Schultz, P. B., & Wolf, D. D. (1993). Impact of late-season orange-striped oakworm (Lepidoptera, Saturniidae) defoliation on oak growth and vigor. Environmental Entomology, 22, 1318–1324. https://doi.org/10.1093/ee/22.6.1318
12. Coutts, A. M., Tapper, N. J., Beringer, J., Loughnan, M., & Demuzere, M. (2013). Watering our cities: The capacity for water sensitive urban design to support urban cooling and improve human thermal comfort in the Australian context. Progress in Physical Geography, 37, 2–28. https://doi.org/10.1177/0309133312461032
13. Creeden, E. P., Hicke, J. A., & Buotte, P. C. (2014). Climate, weather, and recent mountain pine beetle outbreaks in the western United States. Forest Ecology and Management, 312, 239–251. https://doi.org/10.1016/j.foreco.2013.09.051
14. da Silva, R. P., dos Santos, J., Tribuzy, E. S., Chambers, J. Q., Nakamura, S., & Higuchi, N. (2002). Diameter increment and growth patterns for individual tree growing in Central Amazon, Brazil. Forest Ecology and Management, 166, 295–301. https://doi.org/10.1016/S0378-1127(01)00678-8
15. Dai, A. (2013). Increasing drought under global warming in observations and models. Nature Climate Change, 3, 52–58. https://doi.org/10.1038/nclimate1633
16. Dale, A. G., & Frank, S. D. (2014a). The effects of urban warming on herbivore abundance and street tree condition. PLoS ONE, 9, e102996–e102996. https://doi.org/10.1371/journal.pone.0102996
17. Dale, A. G., & Frank, S. D. (2014b). Urban warming trumps natural enemy regulation of herbivorous pests. Ecological Applications, 24, 1596–1607. https://doi.org/10.1890/13-1961.1
18. Dale, A. G., & Frank, S. D. (2017). Warming and drought combine to increase pest insect fitness on urban trees. PLoS ONE, 12, e0173844. https://doi.org/10.1371/journal.pone.0173844
19. Gaylord, M. L., Kolb, T. E., Pockman, W. T., Plaut, J. A., Yepez, E. A., Macalady, A. K., & McDowell, N. G. (2013). Drought predisposes pinon-juniper woodlands to insect attacks and mortality. New Phytologist, 198, 567–578. https://doi.org/10.1111/nph.12174
20. Grinnan, R., Carter, T. E., & Johnson, M. T. J. (2013). Effects of drought, temperature, herbivory, and genotype on plant-insect interactions in soybean (Glycine max). Arthropod-Plant Interactions, 7, 201–215. https://doi.org/10.1007/s11829-012-9234-z
21. Hawkes, C. V., & Sullivan, J. J. (2001). The impact of herbivory on plants in different resource conditions: A meta-analysis. Ecology, 82, 2045–2058. https://doi.org/10.1890/0012-9658(2001)082[2045:TIOHOP]2.0.CO;2
22. Hubbart, J., Link, T., Campbell, C., & Cobos, D. (2005). Evaluation of a low-cost temperature measurement system for environmental applications. Hydrological Processes, 19, 1517–1523. https://doi.org/10.1002/(ISSN)1099-1085
23. Huberty, A. F., & Denno, R. F. (2004). Plant water stress and its consequences for herbivorous insects: A new synthesis. Ecology, 85, 1383–1398. https://doi.org/10.1890/03-0352
24. Jactel, H., Petit, J., Desprez-Loustau, M.-L., Delzon, S., Piou, D., Battisti, A., & Koricheva, J. (2012). Drought effects on damage by forest insects and pathogens: A meta-analysis. Global Change Biology, 18, 267–276. https://doi.org/10.1111/j.1365-2486.2011.02512.x
25. Kargar, M., Suresh, R., Legrand, M., Jutras, P., Clark, O. G., & Prasher, S. O. (2017). Reduction in water stress for tree saplings using hydrogels in soil. Journal of Geoscience and Environment Protection, 5, 27. https://doi.org/10.4236/gep.2017.51002
26. Kurz, W. A., Dymond, C. C., Stinson, G., Rampley, G. J., Neilson, E. T., Carroll, A. L., & Safranyik, L. (2008). Mountain pine beetle and forest carbon feedback to climate change. Nature, 452, 987–990. https://doi.org/10.1038/nature06777
27. Kuster, T. M., Dobbertin, M., Guenthardt-Goerg, M. S., Schaub, M., & Arend, M. (2014). A phenological timetable of oak growth under experimental drought and air warming. PLoS ONE, 9, e89724–e89724. https://doi.org/10.1371/journal.pone.0089724
28. Maherali, H., Moura, C. F., Caldeira, M. C., Willson, C. J., & Jackson, R. B. (2006). Functional coordination between leaf gas exchange and vulnerability to xylem cavitation in temperate forest trees. Plant, Cell & Environment, 29, 571–583. https://doi.org/10.1111/j.1365-3040.2005.01433.x
29. Maherali, H., Pockman, W. T., & Jackson, R. B. (2004). Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology, 85, 2184–2199. https://doi.org/10.1890/02-0538
30. McCluney, K. E., Burdine, J. D., & Frank, S. D. (2017). Variation in arthropod hydration across US cities with distinct climate. Journal of Urban Ecology, 3, jux003.
31. Meineke, E. K., Dunn, R. R., & Frank, S. D. (2014). Early pest development and loss of biological control are associated with urban warming. Biology Letters, 10, 20140586–20140586. https://doi.org/10.1098/rsbl.2014.0586
32. Meineke, E. K., Dunn, R. R., Sexton, J. O., & Frank, S. D. (2013). Urban warming drives insect pest abundance on street trees. PLoS ONE, 8, e59687–e59687. https://doi.org/10.1371/journal.pone.0059687
33. Meineke, E. K., & Frank, S. D. (2018). Data from: Water availability drives urban tree growth responses to herbivory and warming. Dryad Digital Repository, https://doi.org/10.5061/dryad.pb50v53/1
34. Meineke, E. K., Holmquist, A. J., Wimp, G. M., & Frank, S. D. (2017). Changes in spider community composition are associated with urban temperature, not herbivore abundance. Journal of Urban Ecology, 3, juw010. https://doi.org/10.1093/jue/juw010
35. Meineke, E., Youngsteadt, E., Dunn, R. R., & Frank, S. D. (2016). Urban warming reduces aboveground carbon storage. Proceedings of the Royal Society B-Biological Sciences, 283, 20161574–20161574. https://doi.org/10.1098/rspb.2016.1574
36. Mody, K., Eichenberger, D., & Dorn, S. (2009). Stress magnitude matters: Different intensities of pulsed water stress produce non-monotonic resistance responses of host plants to insect herbivores. Ecological Entomology, 34, 133–143. https://doi.org/10.1111/j.1365-2311.2008.01053.x
37. Mullaney, J., Lucke, T., & Trueman, S. J. (2015). A review of benefits and challenges in growing street trees in paved urban environments. Landscape and Urban Planning, 134, 157–166. https://doi.org/10.1016/j.landurbplan.2014.10.013
38. 2 enrichment (FACE) experiments. New Phytologist, 209, 17–28. https://doi.org/10.1111/nph.13593
39. Nowak, D. J. (1994). Atmospheric carbon dioxide reduction by Chicago's urban forest. In E. G. McPherson, D. J. Nowak & R. A. Rowntree (Eds.), Chicago's urban forest ecosystem: Results of the Chicago Urban Forest Climate Project. Gen. Tech. Rep. NE-186 (pp. 83–94). Radnor, PA: US Department of Agriculture, Forest Service, Northeastern Forest Experiment Station.
40. Oke, T. R. (1973). City size and urban heat island. Atmospheric Environment, 7, 769–779. https://doi.org/10.1016/0004-6981(73)90140-6
41. Omkar, A. (2004). Temperature-dependent development and immature survival of an aphidophagous ladybeetle, Propylea dissecta (Mulsant). Journal of Applied Entomology, 128, 510–514. https://doi.org/10.1111/j.1439-0418.2004.00881.x
42. Pan, Y., Birdsey, R. A., Fang, J., Houghton, R., Kauppi, P. E., Kurz, W. A., & Hayes, D. (2011). A large and persistent carbon sink in the world's forests. Science, 333, 988–993. https://doi.org/10.1126/science.1201609
43. Penuelas, J., Gordon, C., Llorens, L., Nielsen, T., Tietema, A., Beier, C., & Gorissen, A. (2004). Nonintrusive field experiments show different plant responses to warming and drought among sites, seasons, and species in a north-south European gradient. Ecosystems, 7, 598–612.
44. Percival, G. C., Keary, I. P., & Sulaiman, A.-H. (2006). An assessment of the drought tolerance of Fraxinus genotypes for urban landscape plantings. Urban Forestry & Urban Greening, 5, 17–27. https://doi.org/10.1016/j.ufug.2006.03.002
45. Pinheiro, J., Bates, D., DebRoy, S., & Sarkar, D.; R Core Team. (2016). nlme: Linear and nonlinear mixed effects models. R package version 3.1-124.
46. Ponsonby, D., & Copland, M. (2000). Environmental effects on the development and survival of the scale insect Abgrallaspis cyanophylli (Signoret) (Homoptera: Diaspididae) with reference to its suitability for use as a host for rearing biological control agents. Biocontrol Science and Technology, 10, 583–594. https://doi.org/10.1080/095831500750016389
47. R Core Team. (2015). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
48. Roman, L. A, McPherson, E. G., Scharenbroch, B. C., & Bartens, J. (2013). Identifying common practices and challenges for local urban tree monitoring programs across the United States. Arboriculture & Urban Forestry, 39, 292–299.
49. Schaffer, B., & Mason, L. J. (1990). Effects of scale insect herbivory and shading on net gas-exchange and growth of a subtropical tree species (Guaiacum sanctum L.). Oecologia, 84, 468–473. https://doi.org/10.1007/BF00328162
50. Walling, L. L. (2008). Avoiding effective defenses: Strategies employed by phloem-feeding insects. Plant Physiology, 146, 859–866. https://doi.org/10.1104/pp.107.113142
51. Wang, J.-J., & Tsai, J. H. (2000). Effect of temperature on the biology of Aphis spiraecola (Homoptera: Aphididae). Annals of the Entomological Society of America, 93, 874–883. https://doi.org/10.1603/0013-8746(2000)093[0874:EOTOTB]2.0.CO;2
52. Wang, J. J., Tsai, J. H., & Broschat, T. K. (2006). Effect of nitrogen fertilization of corn on the development, survivorship, fecundity and body weight of Peregrinus maidis (Hom., Delphacidae). Journal of Applied Entomology, 130, 20–25. https://doi.org/10.1111/j.1439-0418.2005.01030.x
53. Way, D. A., & Oren, R. (2010). Differential responses to changes in growth temperature between trees from different functional groups and biomes: A review and synthesis of data. Tree Physiology, 30, 669–688. https://doi.org/10.1093/treephys/tpq015
54. Wickham, H. (2011). The split-apply-combine strategy for data analysis. Journal of Statistical Software, 40, 1–29.
55. Willis, K. J., & Petrokofsky, G. (2017). The natural capital of city trees. Science, 356, 374–376. https://doi.org/10.1126/science.aam9724
56. Wood, B. W., Tedders, W. L., & Reilly, C. C. (1988). Sooty mold fungus on pecan foliage suppresses light penetration and net photosynthesis. HortScience, 23, 851–853.
57. Youngsteadt, E., Dale, A. G., Terando, A. J., Dunn, R. R., & Frank, S. D. (2015). Do cities simulate climate change? A comparison of herbivore response to urban and global warming. Global Change Biology, 21, 97–105. https://doi.org/10.1111/gcb.12692
58. Youngsteadt, E., Ernst, A. F., Dunn, R. R., & Frank, S. D. (2017). Responses of arthropod populations to warming depend on latitude: Evidence from urban heat islands. Global Change Biology, 23, 1436–1447. https://doi.org/10.1111/gcb.13550
59. Zarnetske, P. L., Skelly, D. K., & Urban, M. C. (2012). Biotic multipliers of climate change. Science, 336, 1516–1518. https://doi.org/10.1126/science.1222732
60. Ziska, L. H., Gebhard, D. E., Frenz, D. A., Faulkner, S., Singer, B. D., & Straka, J. G. (2003). Cities as harbingers of climate change: Common ragweed, urbanization, and public health. Journal of Allergy and Clinical Immunology, 111, 290–295. https://doi.org/10.1067/mai.2003.53
61. Zvereva, E. L., Lanta, V., & Kozlov, M. V. (2010). Effects of sap-feeding insect herbivores on growth and reproduction of woody plants: A meta-analysis of experimental studies. Oecologia, 163, 949–960. https://doi.org/10.1007/s00442-010-1633-1
62. Zwack, J. A., Graves, W. R., & Townsend, A. M. (1998). Leaf water relations and plant development of three freeman maple cultivars subjected to drought. Journal of the American Society for Horticultural Science, 123, 371–375.