The effects of biotic interactions on Ambrosia artemisiifolia L. by Arthur Andrew Meahan MacDonald A Thesis submitted in conformity with the requirements for the degree of Master of Science, Graduate Department of Ecology and Evolutionary Biology, in the University of Toronto © Copyright by Andrew MacDonald 2009 The effects of biotic interactions on Ambrosia artemisiifolia L. Arthur Andrew Meahan MacDonald Master’s of Science Ecology and Evolutionary Biology University of Toronto 2009 Abstract Plant invasions can ensue when plants are introduced to regions without their specialist enemies (the Enemy Release Hypothesis). This assumes natural enemies limit survival and fecundity in an invader's native range. I tested this assumption for a native invasive species, Common Ragweed (Ambrosia artemisiifolia), by excluding natural enemies from seeds, seedlings and adults. At the adult stage, I added disturbance and conspecific density treatments. Protection from herbivores slightly improved performance at the seedling stage only, while disturbance greatly increased survival and fecundity. Increasing conspecific density reduced performance only in disturbed plots. I also tested herbivore tolerance using simulated damage. Heavy (75%) damage did not reduce fecundity; light damage even increased seed production. These results suggest enemies do not limit Ambrosia in its native range, especially compared to the effects of habitat disturbance. While enemy release may have occurred during Ambrosia’s invasions, it is not likely to be their principal cause. ii Acknowledgements “What admirable training is science for the more active warfare of life. Indeed, the unchallenged bravery, which these studies imply, is far more impressive than the trumpeted valor of the warrior. Science is always brave, for to know, is to know good; doubt and danger quail before her eye. But cowardice is unscientific; for there cannot be a science of ignorance.” --- Henry David Thoreau This project has in one sense been about testing the limits of ragweed’s performance in various ecological contexts. Besides testing the limits of this plant, I have also explored my own limits, and perhaps sometimes the limits of the patience of those in my environment! The following people have my gratitude, as I have learned a great deal from each of them. First of all I must thank my supervisor Dr. Peter Kotanen. I was terrifically fortunate to end up in his lab (for that, thanks also go to Sean Blaney and Dave McCorquodale). Peter has been precisely the mentor I needed to transition from a naturalist trained at a small university to an empirical ecologist. Also, I am very grateful to my supervisory committee, Dr. John Stinchcombe and Dr. Spencer Barrett for their frank and candid advice. Among the wider faculty, I am indebted to Ivana Stehlik, Helene Wagner and especially Monika Havelka, an inspiration. I had great luck with labmates as well– James MacKay and Steve Hill are good friends and good teachers. Steve in particular has been a statistics mentor of the first rank. Every error bar on the following thesis would have been larger were it not for the efficient and competent help of Kateryna Kostyukova. Our (hon.) labmate Megan Saunders helped keep the ecology culture alive in our lab. Outside our lab there have been too many grad students to list easily. In particular I’d like to thank the Gwynne Lab: Laura Robson, Kyla Ercit, Murray McConnell, Edyta Piascik and especially Kevin Judge. These intelligent and friendly people kept up my morale and tolerated my frequent presence in their Lab. Kevin in particular is a better friend and housemate than I could wish for; no opinion of mine as been uninfluenced by his thoughtful lifestyle. I would also like to thank the on campus grad community: Yessica Rico, Shekar Biswas, George Lamont, I-San Chan, April Wong, Mike Adorjan and most especially Megan S., Steve Carradona (and Lumi and Chelcea). These wonderful folks have fed me and kept me company throughout the cold winter months. Off-campus, Marion Andrew has warmed my opinion of Toronto dramatically with her hospitality. iii Probably the best part of my education here were the summers spent at KSR. I am forever grateful to the Kofflers for the opportunity. The staff (Ann Zimmerman, John Jensen, Paul, and (in 2008) Art Weis) were always helpful and made working there a pleasure. Everyone who lived at Willow Ridge can attest to the sense of community there and the fun and learning that is guaranteed when smart people spend time in Nature. In particular: Anna Simonsen, Russel Dinnage, Brechann McGoy, Rob Colautti, Emily Austen, Viet Pham and most of all Zuzana Burivalova and Ron McKenzie. I want to briefly acknowledge some literary sources of support: Steven Covey, David Allen, Yamuna Devi, H.D. Thoreau, E.O. Wilson, G. M. Hopkins. I would not even be a scientist if it were not for a very supportive and loving family back in Cape Breton. Thanks Mom, Dad, Brian and Marybeth for being there, all the way from giving me science books in elementary school to helping with field work in 2009! Thanks to my entire extended family, in particular Sr. Rita Clare. Also, thanks for all the friendship and love from all of Angela Petersen’s extended family. Finally, to Angela Petersen herself, my constant source of love, encouragement and support – its been twice as great and half as difficult. Thanks so much. iv Table of Contents Abstract...................................................................................................................................ii Acknowledgements...............................................................................................................iii List of Figures.......................................................................................................................vii List of Tables........................................................................................................................viii List of Tables........................................................................................................................viii 1 General Introduction.......................................................................................................1 1.1 Invasions.....................................................................................................................................................................1 1.1.1 Type of herbivore damage......................................................................................................................................3 1.1.2 Life history stage....................................................................................................................................................4 1.1.3 Plant habitat............................................................................................................................................................7 1.2 Native range studies are important..........................................................................................................................8 1.3 Study species..............................................................................................................................................................8 1.4 Questions..................................................................................................................................................................11 2 The effects of disturbance and enemy exclusion on performance of Ragweed (Ambrosia artemisiifolia L.) at three life-history stages....................................................23 2.1 Introduction.............................................................................................................................................................23 2.2 Methods....................................................................................................................................................................26 2.2.1 Site........................................................................................................................................................................26 2.2.2 Species..................................................................................................................................................................27 2.2.3 Experimental Design............................................................................................................................................27 2.2.4 Statistical Analyses...............................................................................................................................................31 2.3 Results......................................................................................................................................................................32 2.3.1 Seed survival........................................................................................................................................................32 2.3.2 Seedling survival..................................................................................................................................................32 2.3.3 Adult: 2007...........................................................................................................................................................33 2.3.4 Adult: 2008...........................................................................................................................................................34 2.4 Discussion.................................................................................................................................................................35 2.4.1 Seed survival........................................................................................................................................................35 2.4.2 Seedling survival..................................................................................................................................................37 2.4.3 Adult survival and reproduction...........................................................................................................................38 2.5 Figures......................................................................................................................................................................42 v 2.6 Tables........................................................................................................................................................................50 3 Leaf damage has weak effects on fecundity in Ambrosia artemisiifolia L...............59 3.1 Introduction.............................................................................................................................................................59 3.2 Methods....................................................................................................................................................................61 3.2.1 Site........................................................................................................................................................................61 3.2.2 Species..................................................................................................................................................................62 3.2.3 Experimental design.............................................................................................................................................62 3.2.4 Data collection......................................................................................................................................................63 3.2.5 Analyses...............................................................................................................................................................64 3.3 Results......................................................................................................................................................................66 3.3.1 i) Direct effects of damage...................................................................................................................................66 3.3.2 ii) Size-dependent effects.....................................................................................................................................66 3.4 Discussion.................................................................................................................................................................67 3.4.1 Weak effects of damage on plant performance.....................................................................................................68 3.4.2 Leaf clipping changes the pattern of allocation to biomass..................................................................................70 3.4.3 Tolerance effects on invasions..............................................................................................................................71 3.4.4 Tolerance and the ERH.........................................................................................................................................72 3.5 Conclusions..............................................................................................................................................................72 3.6 Acknowledgments....................................................................................................................................................73 3.7 Figures......................................................................................................................................................................74 3.8 Tables........................................................................................................................................................................82 4 General Discussion.......................................................................................................91 4.1 Summary of results.................................................................................................................................................91 4.2 Ambrosia and invasions..........................................................................................................................................92 4.2.1 Ragweed in North America..................................................................................................................................92 4.2.2 Ragweed’s Invasions............................................................................................................................................93 4.2.3 Invasions in general..............................................................................................................................................93 4.3 Suggestions for future work....................................................................................................................................94 4.3.1 Seeds.....................................................................................................................................................................94 4.3.2 Seedlings..............................................................................................................................................................95 4.3.3 Mechanisms of tolerance and allocation...............................................................................................................95 4.3.4 Indirect effects of tolerance..................................................................................................................................98 vi List of Figures Figure 2-1) Relationship between seed biomass and fecundity..............................................................42 Figure 2-2) Germinating seeds from samples of 10 seeds......................................................................43 Figure 2-3) Seedling survivorship in response to herbivore exclusion treatments.................................44 Figure 2-4) Damage to adult plants during the summer of 2007...........................................................45 Figure 2-5) Damage to individual adult plants during the summer of 2008..........................................46 Figure 2-6) The incidence of stem-galling insects in 2008.....................................................................47 Figure 2-7) Measures of plant performance in response to factorial field experiment in 2007.............48 Figure 2-8) Measures of plant performance in response to factorial field experiment in 2008.............49 Figure 3-1) Stem biomass in response to removal of leaves...................................................................74 Figure 3-2) Seed production in response to leaf removal.......................................................................75 Figure 3-3) The relationship between seed and plant biomass decreases with clipping damage.........76 Figure 3-4) Back-transformed elevations of the lines in Fig. 3-3..........................................................77 Figure 3-5) The comparison of allometric reproduction between control and 75% damage.................78 Figure 3-6) Seed mass in response to apical meristem clipping.............................................................79 Figure 3-7) The relationship between seed and plant biomass not affected by apical removal............80 Figure 3-8) 95% confidence intervals for the regressions described in Fig 3-7....................................81 Figure 4-1) A rough estimate of male flower mass................................................................................99 vii List of Tables Table 2-1) A Table of the common enemies which occur on Ambrosia at our field site.........................50 Table 2-2) ANOVA of enemy exclusion on seed germination..................................................................50 Table 2-3) ANOVA of enemy exclusion on seedling survival..................................................................51 Table 2-4) Factorial ANOVA on the adult experiment in 2007..............................................................51 Table 2-5) Factorial ANOVA on the adult experiment in 2008...............................................................52 Table 2-6) Proportion of plants surviving to reproduction in summer 2007..........................................52 Table 2-7) Proportion of plants attacked by stem-galling insects in 2008.............................................52 Table 3-1) Comparison of natural and simulated damage types............................................................82 Table 3-2) ANOVA table for the linear model including plant size (stem biomass) as a continuous variable and clipping as an ordered factor.............................................................................................83 Table 3-3)Parameter estimates (SE) for slopes and intercepts from the linear model of log(seed mass) on log(stem mass)...................................................................................................................................83 viii 1 General Introduction 1.1 Invasions Human activities, particularly habitat alteration and the intentional and unintentional transport of organisms, have caused rapid, unprecedented mixing of the Earth’s biota in a breakdown of what Charles Elton (1958) called “Wallace’s Realms”: great biogeographic regions of distinctive, coadapted organisms. While invasions do occur in nature, humans have accelerated that rate tremendously (Vitousek et al. 1997) and are creating management crises that cost billions to control in the United States (Pimentel et al. 2000, Mack et al. 2000) and in Canada (Colautti 2006). In particular, the introduction of alien plant species has caused profound change in many now-threatened ecosystems around the world with a concomitant loss of conservation, economic and aesthetic value. For example, Bromus tectorum has altered the fire regime in North American grasslands and shrublands (Mack 1981), while Melaleuca quinquenervia has replaced entire areas of the Florida Everglades (Serbesoff- King 2003). Invaded landscapes can be less economically productive: Leafy Spurge (Euphorbia esula) prevents cow grazing in pastures (Leistritz et al. 1992) and Water Hyacinth (Eichhornia crassipes) clogs fish habitat in the African Great Lakes making fishing difficult (Ogutu-Ohwayo et al. 1997). Wind-pollinated introduced plants can cause allergies and pose a public health concern, as Common Ragweed (Ambrosia artemisiifolia) has done in Europe (Igrc 1995). Despite decades of active research (Callaway and Maron 2006), these invasions are likely to increase still more as the developing world becomes more industrialized; for example, in China, biological invasions are rapidly increasing in frequency (Ding et al. 2008, Weber and Li 2008). Despite their negative consequences for the biosphere – indeed, often because of them – invasions can be tools in our exploration of ecology and evolution (Kolar and Lodge 2001, Lodge 1993, reviewed in Callaway and Maron 2006). To this end they have been studied for a century and a 1 half (Darwin 1859, Elton 2000, Callaway and Maron 2006) and have furthered our understanding of rapid evolution, community assembly and top-down control of plant populations. Invasion biology has increased our understanding of population biology (Sakai et al. 2001), the phenomena of rapid evolution (Blossey and Notzold 1995, Sakai et al. 2001) and the importance of biotic interactions in determining plant distribution and abundance (Klironomos 2002, Mitchell et al. 2006). Theoretical approaches to understanding invasions and the communities they invade has progressed from verbal ideas (Elton 1958) to sophisticated modeling (e.g. Eppstein and Molofsky 2007) taking into account the multiple interacting factors which together influence invasion. Much research in Invasion biology is organized around the Enemy Release Hypothesis. The Enemy Release Hypothesis (ERH) suggests that invaders benefit from a reduced consumer and/or pathogen load in their new range; it is often invoked to explain the success of non-natives (Elton 1958, Mitchell et al. 2006, Agrawal and Kotanen 2003, Keane and Crawley 2002, Mitchell and Power 2003, Maron and Vila 2001, Wolfe 2002). This popular theory has generated a tremendous amount of discussion and research since it was suggested by Charles Elton 50 years ago and continues to be refined and explored by modern invasion ecologists (Richardson and Pysek 2008). Liu and Stiling (2006) identify several assumptions of the ERH, most importantly that top-down control is important for many plant species and that plants are likely to be introduced without their oligophagous consumers. Because generalists are present in most habitats and are likely to be able to feed on invaders (Liu and Stiling 2006, but see Jogesh et al. 2008), invaders continue to experience some damage in their new habitat. However, because oligophagous consumers in the introduced range are unlikely to recognize the invader as food, individual plants incur less tissue damage and so enjoy enhanced probabilities of survival and reproduction. Additionally, invasive plants may be those able to repel generalist attack as well: for example, in several recent studies (e.g. Jogesh et al. 2008, 2