Source: OHIO STATE UNIVERSITY submitted to
ECOLOGY OF AMBROSIA TRIFIDA (GIANT RAGWEED): INTERACTION WITH LUMBRICUS TERRESTRIS AND ITS IMPACT ON WEED POPULATION DYNAMICS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
0202357
Grant No.
(N/A)
Project No.
OHO01122
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Sep 30, 2010
Project End Date
Sep 30, 2015
Grant Year
(N/A)
Project Director
Harrison, S.
Recipient Organization
OHIO STATE UNIVERSITY
1680 MADISON AVENUE
WOOSTER,OH 44691
Performing Department
Horticulture and Crop Science
Non Technical Summary
Ambrosia trifida (giant ragweed) is a major annual weed of crop fields throughout the eastern two-thirds of North America, and its pollen is a principal cause of seasonal allergies in humans and domestic animals in the U.S., Europe, and Asia. A. trifida is unusual for a persistent weed in that its reproductive output and seed survival rates are relatively low, yet it successfully colonizes and persists in agricultural fields and successional environments under varying levels of soil disturbance. Seeds of A. trifida and other weedy species are collected and cached by Lumbricus terrestris L., a naturalized, anecic earthworm. Burial of seeds in earthworm burrows or middens reduces seed exposure to surface predators and influences depth-dependent seed germination and seedling recruitment. We hypothesize that earthworms play a major role in the weedy behavior of A. trifida, and that the relationship between L. terrestris and A. trifida is a conditional mutualism wherein the outcome for A. trifida seeds can be negative or positive depending on habitat type, vegetative cover, seed availability, and how they influence the activity-density of seed predators. The goal of this research is to understand A. trifidas mechanisms of environmental adaptation and how they contribute to its behavior as an invasive weed, but also to utilize A. trifida as a model species by which to obtain a better understanding of the ecological relationships among seed characteristics, seed predation, and seed dispersal. By understanding how habitats, soil-dwelling organisms, and seeds interact to influence weed survival, we hope to gain knowledge necessary for developing ecosystem-based strategies for managing A. trifida and preventing its spread.
Animal Health Component
(N/A)
Research Effort Categories
Basic
(N/A)
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
21323001140100%
Knowledge Area
213 - Weeds Affecting Plants;

Subject Of Investigation
2300 - Weeds;

Field Of Science
1140 - Weed science;
Goals / Objectives
We hypothesize that the relationship between the earthworm L. terrestris and A. trifida seeds is a conditional mutualism wherein L. terrestris benefits from the relationship and the outcome for A. trifida can be negative or positive depending on habitat type, vegetative cover and seed availability and their influence the activity-density of seed predators. The overall goal of the proposed research is to better understand the ecological relationships among L. terrestris, A. trifida, and seed predators, and how they impact giant ragweed population dynamics in agroecosystems. The specific objectives of the project are: 1. To determine how habitat characteristics and environmental factors impact the L. terrestris-A. trifida association. 2. To determine the net effects of L. terrestris on A. trifida seedling establishment in the presence and absence of seed predators. 3. To determine how L. terrestris foraging behavior is affected by seed factors. The outputs from the project will include presentations at annual meetings of the North Central Weed Science Society and Weed Science Society of America, presentations at biennial meetings on Earthworm Ecology and Seed Ecology, and publication of experimental results in appropriate peer-reviewed scientific journals. Additional activities associated with the project will include undergraduate and graduate teaching, and extension education via electronic media and related outreach activities.
Project Methods
Field experiments will be conducted to determine the combined effect of L. terrestris and seed predators on A. trifida seedling recruitment. The experiment will be in a split-plot arrangement, with habitat type (bare or vegetated) as the main plot factor, and a factorial combination of seed predators (present or absent), L. terrestris (present or absent) and A. trifida seed density (0, 320, or 960 seeds m-2) as subplot factors. Main plots will be in a randomized complete block design with six blocks. The vegetated main plots are expected to provide favorable foraging sites for small rodents and the bare habitat to discourage foraging. Subplots will be separated by at least 1 m. For subplots where vertebrate seed predators were not desired, exclosures will be installed consisting of aluminum flashing topped with metal mesh screen. To prepare subplots without L. terrestris, 10 L of dilute formaldehyde solution will be applied to cause L. terrestris to surface from burrows, and the earthworms will be removed by hand. Carbaryl will applied to the earthworm-absent plots to kill any remaining L. terrestris that were not flushed from their burrows with the formaldehyde solution. For subplots where L. terrestris is desired, resident L. terrestris populations will be left undisturbed. Seed population density treatments will be established at levels equivalent to 0, 6, and 20% of a typical seed rain from a dense stand of A. trifida. To explore the relationships between habitat type, L. terrestris presence, predator presence, seed burial by L. terrestris, seed predation, and seedling emergence, we will construct a hierarchical Bayesian model to combine data of both stringed seeds and seedling emergence. The model will be based on equations describing A. trifida seedling emergence under four different conditions of presence or absence of earthworms and seed predators: 1) earthworms and seed predators both absent; 2) seed predators present, earthworms absent; 3) earthworms present, seed predators absent; and 4) both earthworms and seed predators present. We propose to investigate how seed physical and chemical factors influence the seed foraging behavior of L. terrestris. Preliminary experiments will consist of foraging preference trials and will be conducted under laboratory conditions using individual microcosms as experimental units. Nocturnal foraging behavior will be monitored by digital timelapse photography. Treatments will consist of different types of seeds and/or objects placed on the soil surface. In the first experiment, plaster-cast A. trifida seed surrogates will be used to determine if L. terrestris exhibits equal preference for actual seeds and seed surrogates based on similarities in physical/tactile properties. The rate and extent of seed foraging for each seed type will be monitored daily by reviewing the timelapse movies. Rates of seed/object removal and final number of seeds removed from the soil surface by L. terrestris will be compared to determine foraging preference, and data will also be collected on foraging frequency, duration, and method (subterranean vs. surface foraging).

Progress 09/30/10 to 09/30/15

Outputs
Target Audience: Agricultural professionals, academicians, industry scientists, farmers, land managers, and health care providers. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? The results have been presented at scientific meetings and published in a peer-reviewed journal. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? The current project report addresses Objective 1: To determine how habitat characteristics and environmental factors impact the L. terrestris-A. trifida association. 1) Major activities completed/experiments conducted: We published the results of a web-based survey of over 1000 Certified Crop Advisors across the U.S. Corn Belt to determine the distribution of giant ragweed and gain insights into possible factors associated with its spread. In addition, we completed a database incorporating 1,795 giant ragweed specimens from 157 herbaria. Based on the database, maps illustrating the historical distribution of giant ragweed were constructed from 1852 to the present. 2) Data collected: The survey instrument consisted of an online questionnaire with Likert-scale responses. Questions concentrated on giant ragweed history, prevalence, and management issues within each respondent's' geographic area of responsibility. 3) Summary statistics and discussion of results: Respondents rated giant ragweed as the most or one of the most difficult weeds to manage in 45% of 421 U.S. counties responding, and 57% of responding counties reported giant ragweed populations with herbicide resistance to ALS-inhibitors, glyphosate, and/or to both herbicides. Results suggest that giant ragweed is increasing in crop fields outward from the east-central U.S. Corn Belt in all directions. Crop production practices associated with giant ragweed populations included minimum tillage, continuous soybean, and multiple-application herbicide programs; ecological factors included giant ragweed presence in non-crop edge habitats, early and prolonged emergence period, and presence of the seed-burying common earthworm in crop fields. Managing giant ragweed in non-crop areas could reduce giant ragweed migration from non-crop habitats into crop fields and slow its spread. Where giant ragweed is already established in crop fields, including a more diverse combination of crop species, tillage practices, and herbicide sites of action will be critical to reduce populations and select against late-emerging and herbicide-resistant giant ragweed genotypes. Incorporation of a cereal grain into the crop rotation may help suppress early giant ragweed emergence and provide chemical or mechanical control options for late-emerging giant ragweed. 4) Key outcomes or other accomplishments realized: Results suggest that giant ragweed is increasing in crop fields outward from the east-central Corn Belt, facilitated by the pre-existence of populations in non-crop habitats and a favorable habitat provided by similar crop rotation, tillage and herbicide practices across much of the Corn Belt. Managing giant ragweed in non-crop areas could reduce giant ragweed migration from non-crop habitats into crop fields and slow its spread. Where giant ragweed is already established in crop fields, incorporating diversity in crop rotations (e.g., use of a winter small grain or cover crop), tillage practices, and herbicide sites of action will be critical to reduce populations and select against late-emerging and herbicide-resistant giant ragweed genotypes. Results from this project produced a change in knowledge by providing new insight into agricultural management practices that have led to the rapid spread of giant ragweed in agricultural fields. The participants affected by this new applied knowledge include agricultural professionals, academicians, industry scientists, farmers, and health care professionals.

Publications

  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Regnier, E. E., S. Kent Harrison, Mark M. Loux, Christopher Holloman, Ramarao Venkatesh, Florian Diekmann, Robin Taylor, Robert A. Ford, David E. Stoltenberg, Robert G. Hartzler, Adam S. Davis, Brian J. Schutte, John Cardina, Kris J. Mahoney, and William G. Johnson. 2016. Certified crop advisors' perceptions of giant ragweed (Ambrosia trifida) distribution, herbicide resistance, and management in the Corn Belt. Weed Sci. 64: (In press).
  • Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Regnier, E. E., S. Kent Harrison, Mark M. Loux, Christopher Holloman, Ramarao Venkatesh, Florian Diekmann, Robin Taylor, Robert A. Ford, David E. Stoltenberg, Robert G. Hartzler, Adam S. Davis, Brian J. Schutte, John Cardina, Kris J. Mahoney, and William G. Johnson. 2016. Certified crop advisors' perceptions of giant ragweed (Ambrosia trifida) distribution, herbicide resistance, and management in the Corn Belt. Agronomy Abstr. 254-8 http://tps://scisoc.confex.com/scisoc/2015am/webprogram/Paper94442.html


Progress 10/01/13 to 09/30/14

Outputs
Target Audience: Agriculture professionals in the public and private sector, Certified Crop Advisers, Weed Scientists Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? This project has generated new knowledge on historical, landscape, and agricultural factors that have contributed to the spread of giant ragweed in the United States. Professional development opportunities were provided to academic and industry weed scientists, Certified Crop Advisers, agriculture professionals, and crop producers via publication of conference proceedings/presentations and online newsletters. How have the results been disseminated to communities of interest? Publication of study results in conference presentations/proceedings (NCWSS proceedings) and online newsletter (C.O.R.N.) geared toward ag professionals and crop producers. What do you plan to do during the next reporting period to accomplish the goals? We will conduct more detailed statistical analyses of survey results and publish the findings in a peer-reviewed scientific journal.

Impacts
What was accomplished under these goals? Giant ragweed is one of a relatively few native plant species that has become a major weed of grain crops in North America. It is also a major source of allergenic pollen that has adverse health effects on approximately 25% of the U.S. population. We conducted a web-based survey of Certified Crop Advisors in the Corn Belt to determine the distribution of giant ragweed and gain insights into possible factors associated with its spread. The questionnaire asked participants to provide their perceptions and county-level estimates of giant ragweed related to its first occurrence as a problematic weed in crop fields, the proportion of crop acres infested, and habitats where found. Based on the survey responses, giant ragweed was reported to appear in crop fields 20 years ago or longer in western Ohio, most of Indiana, northern Illinois, southern Wisconsin, southeastern Minnesota, and eastern Iowa. In most counties outside this area of the Corn Belt, giant ragweed was reported to appear in crop fields more recently, and in some counties, only in the last 5 years (e.g., northern Wisconsin). Nearly all respondents indicated that giant ragweed was already present in non-crop edge habitats such as riverbanks and fencerows before it appeared in crop fields. Although giant ragweed is considered a riparian species, the survey results indicated that it is well established throughout the Corn Belt in both riparian and upland edge habitats. The timing of giant ragweed emergence varied across the region with giant ragweed emerging earlier and for a longer period of time in the east-central region of the Corn Belt (i.e., Ohio and Indiana) than in other areas. Difficulty of managing giant ragweed was associated with its presence in waterways, and with an earlier and longer emergence period. Reduced use of conventional tillage in corn and soybean fields was associated with increased difficulty of managing giant ragweed. Based on these results, it appears that giant ragweed first became a problem weed in the east-central region of the Corn Belt and is now becoming established in crop fields in areas outside of that region, especially toward the North and West. It is likely that giant ragweed spreads initially through a variety of non-crop edge habitats and then becomes established in areas adjacent to crop fields such as waterways and fencerows, and from there it can quickly get established in crop fields. Overall survey results indicate that proper management and containment of giant ragweed within its natural riparian habitats must be implemented to prevent its subsequent spread into edge habitats and crop fields. The current project report addresses Objective 1: To determine how habitat characteristics and environmental factors impact the L. terrestris-A. trifida association. 1) Major activities completed/experiments conducted: We conducted a web-based survey of over 1000 Certified Crop Advisors across the U.S. Corn Belt to determine the distribution of giant ragweed and gain insights into possible factors associated with its spread. 2) Data collected: The survey instrument consisted of an online questionnaire with Likert-scale responses. Questions concentrated on giant ragweed history, prevalence, and management issues within each respondent's' geographic area of responsibility. 3) Summary statistics and discussion of results: Giant ragweed was listed as the most difficult weed to manage in counties located in Indiana, Wisconsin, Minnesota, Iowa and Nebraska. Most of these counties were located near the upper Mississippi River where Wisconsin, Minnesota, Iowa, and Illinois meet, and counties reporting giant ragweed present in 60% or more of crop fields were located in this same region. East of the Mississippi, counties with giant ragweed present in 60% or more of crop acres were located in northwest Illinois, most of Indiana, and west-central Ohio. It is likely that giant ragweed spreads initially through a variety of non-crop edge habitats and then becomes established in areas adjacent to crop fields such as waterways and fencerows, and from there it can quickly get established in crop fields. Overall survey results indicate that proper management and containment of giant ragweed within its natural riparian habitats must be implemented to prevent its subsequent spread into edge habitats and crop fields. 4) Key outcomes or other accomplishments realized: Giant ragweed appears to spread initially from its native riparian habitats to various non-crop edge habitats (e.g., forest borders), then becomes associated with cropland via invasion of fencerows, where it subsequently invades adjacent crop fields. Information on the co-occurrence of giant ragweed and the earthworm (Lumbricus terrestris) remains unclear based on survey responses. Results produced a change in knowledge by providing new insight into agricultural management practices that have led to the rapid spread of giant ragweed in agricultural fields. The participants affected by this new applied knowledge include scientists, crop producers, and agricultural professionals in the public and private sector.

Publications

  • Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Regnier Emilie E., Christopher Holloman, Steven K. Harrison, Mark M. Loux, Ramarao Venkatesh, Robert A. Ford, Robin Taylor, Florian Diekmann. Survey of giant ragweed distribution and spread in the North Central Region. Proc. North Cent. Weed Sci. Soc. 68:181. Venkatesh, R., Robert A. Ford, Emilie E. Regnier, Steven K. Harrison, Christopher Holloman, Robin Taylor, and Florian Diekmann. Historical distribution of giant ragweed and common cocklebur in the North Central Region. Proc. North Central Weed Sci. Soc. 68:74. Ford, R.A., Ramarao Venkatesh, Emilie E. Regnier, Steven K. Harrison, Christopher Holloman, Robin Taylor, and Florian Diekmann. GIS analysis of glyphosate resistance in giant ragweed. Proc. North Cent. Weed Sci. Soc. 68:75.


Progress 01/01/13 to 09/30/13

Outputs
Target Audience: Professional colleagues, industry personnel, public stakeholders Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? Results of the bibliometric analysis have been published in peer-reviewed journal. Survey participants will be informed of the results upon request. What do you plan to do during the next reporting period to accomplish the goals? Present the survey findings at the North Central Weed Science Society meeting in December 2013, and publish survey results in a peer-reviewed journal.

Impacts
What was accomplished under these goals? A bibliometric analysis of the scientific literature and a survey of >1000 Certified Crop Advisors across the U.S. North Central region was completed to gather data on the historical factors, agricultural practices, and co-occurrence of giant ragweed and L. terrestris (earthworms) that have contributed to the spread of giant ragweed in the region. Survey results are currently being analyzed. The overall goal of the bibliometric analysis was to help construct a theoretical framework by which to identify the causal factors of giant ragweed’s increased abundance in order to facilitate development of an ecosystem-wide weed management strategy. The bibliometric analysis identified publication outputs, major subject categories and journals, author productivity and collaborations, main research themes, and most frequently cited publications on a worldwide basis. Literature searches revealed 1209 unique entries spanning the period from 1903 to 2012. Results showed that research articles on giant ragweed were scant prior to 1922, and then increased to an average of five per year until the 1970s. In the1970s, research articles on giant ragweed began to show a steady annual increase and reached an average of 48 papers per year from 2003 to 2012. Over most of the study period, an average of <10 countries were represented in research articles, but that number has expanded to 49 countries since 1990. To date, a total of 391 different journals have published articles on giant ragweed, with the articles representing 45 countries, 775 institutions, and 2759 authors. Article title word and author keyword usage analyses showed that the word “allergy” ranked 285th from 1903 to1982 and increased to 38th from 2003-2012. Reference to “weed” in the title or keywords ranked 12th from 1903 to 1982 but increased to 2nd from 2003-2012. Reference to “resistance” ranked 175th prior to 1982 but ranked 3rd from 2003 to 2012, likely reflecting the sharp increase in development of herbicide-resistant giant ragweed populations over the past decade. Nine of the top ten most influential giant ragweed publications in agriculture-related journals, assessed as citations per publication, have been published since 2000. Similarly, seven of the top ten publications in the allergy and immunology subject area have been published since 2000. Overall results of the bibliometric analysis indicated that publication of scientific articles on giant ragweed, number of cited references, and number of citations received have increased substantially over the past three decades relative to those prior to 1980. The number of authors, collaborations, and international involvement associated with giant ragweed publications has also increased dramatically over the past three decades. Since 2000 there has been a marked increase in the output of research articles investigating giant ragweed biology, management, and allergenicity, reflecting the relatively recent and rapid expansion of giant ragweed as a major weed problem worldwide. Further content analysis of the literature published since 1980 should help shed light on possible factors and/or mechanisms that have contributed to the invasive behavior of this native species.

Publications

  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Diekmann, F., R.A. Ford, S.K. Harrison, E.E. Regnier, and R. Venkatesh. 2013. Bibliometric analysis of the literature on giant ragweed (Ambrosia trifida L.). J. Agric. and Food Info. 14:290-320. DOI: 10.1080/10496505.2013.823865.


Progress 01/01/12 to 12/31/12

Outputs
OUTPUTS: Seeds of giant ragweed exhibit a complex system of dormancy that includes physiological embryo dormancy and a restriction of embryo enlargement by fruit and seed covering structures (referred to hereafter as covering structure-enforced [CSE] dormancy). To clarify the roles of embryo and CSE dormancy in giant ragweed seedling emergence timing, we conducted two experiments to address the following objectives: (1) determine changes in germinability for giant ragweed dispersal units (hereafter "involucres") and their components under natural burial conditions, and (2) compare embryo and CSE dormancy alleviation and emergence periodicity between successional and agricultural populations. In Experiment 1, involucres were buried in crop fields at Columbus, OH, periodically excavated, and brought to the laboratory for dissection. Involucres, achenes, and embryos were then subjected to germination assays at 20 C. In Experiment 2, temporal patterns of seedling emergence were determined at a common burial site. Reductions in embryo and CSE dormancy were compared with controlled-environment stratification followed by germination assays at 12 and 20 C, temperatures representative of soil conditions in spring and summer. Results indicated that overwinter dormancy loss involved sequential reductions in embryo and CSE dormancy. CSE dormancy, which may limit potential for fatal germination during fall, was caused by the pericarp and/or embryo-covering structures within the pericarp. In Experiment 2, successional populations emerged synchronously in early spring, whereas agricultural populations emerged throughout the growing season. Levels of embryo dormancy were greater in the agricultural populations than the successional populations, but CSE dormancy levels were similar among populations. In 12 C germination assays, embryo dormancy levels were positively correlated with time required to reach 95% cumulative emergence (run 1: r  =  0.81, P  =  0.03; run 2: r  =  0.76, P  =  0.05). These results suggest that late-season emergence in giant ragweed involves high levels of embryo dormancy that prevent germination at low temperatures in spring. PARTICIPANTS: E. Regnier and K. Harrison were Co-PIs for this project. B. Schutte was a Ph.D. student who completed the work. TARGET AUDIENCES: Crop producers and educators, ragweed researchers. Publication in Weed Science delivers science-based knowledge to people with access to the journal. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
The findings from these studies elucidate the physical and physiological mechanisms regulating the prolonged seedling emergence period that contributes to the weedy and invasive nature of giant ragweed in agroecosystems. The covering structures of giant ragweed appear to be responsible for maintaining giant ragweed seed dormancy in the fall when the seeds are first dispersed. Following a cold stratification period, physiological embryo dormancy was greater in agricultural giant ragweed populations that in successional populations, extending the period of seedling emergence throughout the growing season. These results suggest that the invasivity of giant ragweed in agricultural fields is due in part to the weed's adaptation to agricultural weed control practices that are concentrated early in the growing season. By evolving an extended emergence period via the aforementioned dormancy mechanisms, giant ragweed is able to bypass early weed control measures and complete its life cycle later in the season. These findings represent a change in our knowledge of ragweed persistence and spread, and also increase our understanding of invasion biology. The results provide practical information on the importance of adopting preventive weed management methods in areas where wild giant ragweed populations are growing in close proximity to crop fields.

Publications

  • Schutte, B.J., E. E. Regnier, and S. K. Harrison. 2012. Seed dormancy and adaptive seedling emergence timing in giant ragweed (Ambrosia trifida). Weed Sci. 60:19-26.


Progress 01/01/11 to 12/31/11

Outputs
OUTPUTS: Giant ragweed germination is delayed by both a physiological dormancy of the embryo (embryo dormancy) and an inhibitory influence of embryo-covering structures (covering structure- enforced [CSE] dormancy). To clarify the roles of embryo and CSE dormancy in giant ragweed seedling emergence timing, we conducted two experiments to address the following objectives: 1) determine changes in germinability for giant ragweed dispersal units (hereafter "involucres") and their components under natural burial conditions, and 2) compare embryo and CSE dormancy alleviation and emergence periodicity between successional and agricultural populations. In Experiment 1, involucres were buried in crop fields at Columbus, OH, periodically excavated, and brought to the laboratory for dissection. Involucres, achenes, and embryos were then subjected to germination assays at 20 C. In Experiment 2, temporal patterns of seedling emergence were determined at a common burial site. Reductions in embryo and CSE dormancy were compared with controlled-environment stratification followed by germination assays at 12 and 20 C; temperatures representative of soil conditions in spring and summer. Results indicated that overwinter dormancy loss involved sequential reductions in embryo and CSE dormancy. CSE dormancy, which may limit potential for fatal germination during fall, was caused by the pericarp and/or embryo-covering structures within the pericarp. In Experiment 2, successional populations emerged synchronously in early spring, whereas agricultural populations emerged throughout the growing season. Levels of embryo dormancy were greater in the agricultural populations than the successional populations, but CSE dormancy levels were similar among populations. In 12 C germination assays, embryo dormancy levels were positively correlated with time required to reach 95% cumulative emergence (run 1: r = 0.81, p = 0.03; run 2: r = 0.76, p = 0.05). These results suggest that late-season emergence in giant ragweed involves high levels of embryo dormancy that prevent germination at low temperatures in spring. PARTICIPANTS: K. Harrison and Emilie Regnier (co-PIs), and Brian Schutte (graduate student) conducted research and reported results. TARGET AUDIENCES: Scientists, consultants, growers, educators, non-governmental organizations and students. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
The findings from these studies elucidate the physical and physiological mechanisms regulating the prolonged seedling emergence period that contributes to the weedy and invasive nature of giant ragweed in agroecosystems. The covering structures of giant ragweed appear to be responsible for maintaining giant ragweed seed dormancy in the fall when the seeds are first dispersed. Following a cold stratification period, physiological embryo dormancy was greater in agricultural giant ragweed populations that in successional populations, extending the period of seedling emergence throughout the growing season. These results suggest that the invasivity of giant ragweed in agricultural fields is due in part to the weed's adaptation to agricultural weed control practices that are concentrated early in the growing season. By evolving an extended emergence period via the aforementioned dormancy mechanisms, giant ragweed is able to bypass early weed control measures and complete its life cycle later in the season. These findings represent a change in our knowledge of ragweed persistence and spread, and also increase our understanding of invasion biology. The results provide practical information on the importance of adopting preventive weed management methods in areas where wild giant ragweed populations are growing in close proximity to crop fields.

Publications

  • Schutte, B.J., E. E. Regnier, and S. K. Harrison. 2011. Seed dormancy and adaptive seedling emergence timing in giant ragweed (Ambrosia trifida). Weed Sci. (Early online release, doi: http://dx.doi.org/10.1614/WS-D-11-00049.1).
  • Venkatesh, Ramarao, R. A. Ford, E. E. Regnier, S. K. Harrison, R. A. Taylor, C. H. Holloman, M. Tadesse, J. Witkop, J. R. Moser, and N. A. Read. 2011. Historical distribution of giant ragweed in the Midwest based on herbaria records. Proc. North Cent. Weed Sci. Soc. 66:46.
  • Harrison, S.K. and E.E. Regnier. 2011. Trophic interactions and their potential impacts on giant ragweed. Proc. North Cent. Weed Sci. Soc. 66:158.
  • Diekmann, F., Emilie E. Regnier, Ramarao Venkatesh, Steven K. Harrison. 2011. Management of giant ragweed (Ambrosia trifida): a systematic review. Proc. North Cent. Weed Sci. Soc. 66:48.
  • Regnier, E.E., R. Venkatesh, S. K. Harrison, F. Diekmann, C. H. Holloman, R. A. Taylor, M. M. Loux, J. Cardina, J. E. Heimlich, A. S. Davis, B. J. Schutte, D. E. Stoltenberg, K. J. Mahoney R. Hartzler, William G. Johnson. 2011. Ecosystem Based Weed Management: Giant Ragweed in the Corn Belt. Proc. North Cent. Weed Sci. Soc. 66:47.


Progress 01/01/10 to 12/31/10

Outputs
OUTPUTS: Lumbricus terrestris L. (common nightcrawler) is a naturalized earthworm in North America that actively collects and caches seeds of Ambrosia trifida (giant ragweed) in its burrow. As a native annual plant of North America, A. trifida has become an important agricultural and allergenic weed of the U.S. within the past 30 years. Burial of A. trifida seeds in L. terrestris burrows reduces seed exposure to predators and influences depth- dependent seed germination and seedling recruitment. We conducted field experiments to determine the interaction of L. terrestris and vertebrate seed predators on A. trifida seed fate and seedling recruitment in different habitats. A Bayesian model was fit to the data to assess the effects of L. terrestris on A. trifida in the presence and absence of seed predators. Burial of A. trifida seeds by L. terrestris increased the probability of seedling recruitment in areas where seed predation intensity was high, but decreased the probability of recruitment when predators were excluded or when predation intensity was low. In areas with high vegetative cover, seed predators consumed more seeds than were cached by L. terrestris. Conversely, L. terrestris cached more seeds than were consumed by seed predators in areas with low vegetative cover. Results from field studies provide evidence that the relationship between L. terrestris and A. trifida is a context dependent, conditional mutualism wherein L. terrestris benefits A. trifida survival by increasing seedling recruitment in habitats where seed predation intensity is high. Furthermore, seed caching by L. terrestris may also increase A. trifida survivorship by burying some seeds below the germination depth limit, thereby maintaining seed dormancy and increasing seed bank longevity. A survey of 30 fields across the eastern U.S. Corn Belt showed that the spatial association of L. terrestris and A. trifida occurred across states and soil types, but the strength of the association varied with climate differences during the previous September through March. The strongest environmental driver of association was frequency of "moderate rain day" (MRD; day that received 12.8-25.3 mm of precipitation), with a 1-day increase in MRD frequency increasing the odds of LtAt association by a factor of 1.42. Thus, the potential for L. terrestris to cache seeds and facilitate seedling recruitment is increased by precipitation frequency and amount during September through March. Laboratory experiments designed to investigate L. terrestris nocturnal foraging behavior revealed that the earthworms preferentially collected real seeds over plaster-cast seed duplicates and debris, and that they were able to detect and forage the seeds from below as well as above the soil surface. This feeding behavior suggests that the earthworm utilizes olfactory sensing to forage seeds surreptitiously, thus limiting its exposure to predators while promoting the mutualism with A. trifida. PARTICIPANTS: K. Harrison and Emilie Regnier (co-PIs) conducted research and reported results. Clive Edwards (OSU), Norman Arancon (Univ. of Hawaii), Jianyang Liu (Univ. Illinois), Adam Davis (ARS), Brian Schutte (ARS), and Christopher Holloman (OSU) were research collaborators. TARGET AUDIENCES: Scientists, consultants, growers, educators, non-governmental organizations and students. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
The findings from these studies (1) verify and quantify the association between L. terrestris and A. trifida at the field scale across the eastern U.S. Corn Belt, and (2) shed light on a mechanism by a which weedy and invasive behavior of a native plant (giant ragweed) has likely evolved as a result of its mutualistic relationship with a non-native species (the earthworm L. terrestris). These findings also increase our understanding of invasion biology, and they provide practical information on the importance of adopting preventive weed management methods in areas where L. terrestris and giant ragweed can potentially co-occur.

Publications

  • Schutte, Brian J., Jianyang Liu, Adam S. Davis, S. Kent Harrison, Emilie E. Regnier. 2010. Environmental factors that influence the association of an earthworm (Lumbricus terrestris L.) and an annual weed (Ambrosia trifida L.) in no-till agricultural fields across the eastern U.S. Corn Belt. Agriculture, Ecosystems, and Environment 138:197-205.
  • Harrison, K., Emilie Regnier, Jianyang Liu, Norman Arancon, and Clive Edwards. 2010. Secondary seed dispersal of Ambrosia trifida by Lumbricus terrestris: Implications for Earthworm and Weed Interactions. Abstracts of The Ninth International Symposium on Earthworm Ecology, Xalapa, Mexico, p. 167.
  • Regnier, E. E., S. K. Harrison, C. Holloman, N. Arancon, and C. A. Edwards. 2010. Why do earthworms (Lumbricus terrestris) collect and bury seeds Abstr. Weed Sci. Soc. Am. 49:PC102.


Progress 01/01/09 to 12/31/09

Outputs
OUTPUTS: A central goal of this project is to elucidate the apparent symbiotic relationship between giant ragweed (Ambrosia trifida) and the naturalized nightcrawler earthworm (Lumbricus terrestris). The earthworm collects giant ragweed seeds from the soil surface and stores them in its burrow, thereby protecting the seeds from various seed predators. L. terrestris also collects and stores other plant material and some inorganic material (i.e., small pebbles)inside its burrow. It derives nourishment from the decomposing organic matter, but its reasons for collecting the pebbles are unknown; however, they may possibly serve as a structural material. Given the physical resemblance between hardened seeds and rock fragments, it is unclear whether L. terrestris buries seeds as a possible food source or as structural elements, or haphazardly in an instinctive behavior. As a first step to understand why earthworms bury seeds, we conducted a laboratory experiment to test the hypothesis that L. terrestris discriminates between seeds and inert objects. The experiment was conducted in a controlled environment with earthworms that established burrows in PVC pipes. Giant ragweed seeds, plaster duplicates of seeds, and plaster sticks ("debris") were laid on the soil surface. Nocturnal earthworm foraging was observed nightly for 12 days by means of time-lapse photography. The earthworms buried all of the types of items but showed a strong preference for actual seeds over the plaster-cast seed surrogates and plaster debris. There was no evidence that earthworms collected items haphazardly. Earthworms removed real seeds from below the soil surface, exhibiting a subterranean foraging behavior that suggests they were able to detect seeds on the soil surface from below; a behavior not reported previously in the literature. These results provide evidence that earthworms collect seeds specifically for food and suggest that a mutualism has developed that benefits the survival of both A. trifida and L. terrestris. PARTICIPANTS: Not relevant to this project. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
The findings presented above represent a change in knowledge about L. terrestris behavior and about a mutualism that has evolved between an exotic species (L. terrestris) and a native annual plant (A. trifida). The apparent facilitation of A. trifida colonization by L. terrestris has the potential to change actions of crop producers and land managers in new efforts to manage and control A. trifida, a highly competitive weed of crops and a plant that directly impacts human health through the release of allergenic pollen. It may also impact these actions in other parts of the world where the north American native annual A. trifida has become a serious exotic invasive weed species and where its threat to human health is even higher due to a higher level of susceptibility to the ragweed allergen exhibited by those populations. Successful implementation of ragweed management strategies that utilize the basic knowledge gained in this project would result in a change in conditions manifested by reduced weed competition in crops and other plant communities, and a significant reduction in the most widely abundant aeroallergen in several parts of the world.

Publications

  • No publications reported this period


Progress 01/01/08 to 12/31/08

Outputs
OUTPUTS: Multi-year field and laboratory studies were conducted to investigate the species interactions and other ecological factors that contribute to the establishment and survival of giant ragweed (Ambrosia trifida), a severe weed problem of agricultural fields in the U.S. Corn Belt. Collectively, results showed that: (1) Earthworms (Lumbricus terrestris) collected and buried over 90% of A. trifida seeds placed on the soil surface at a rate eightfold faster than abiotic seed burial. There was a sixfold higher concentration of seeds in earthworm burrows than in surrounding soil and a mean of 127 A. trifida seeds per burrow after a single season. Earthworms foraged selectively among seeds of 11 plant species and collect more seeds of A. trifida than seeds of other species. The novel interaction of L. terrestris and A. trifida increases A. trifida seed bank formation, and L. terrestris burrows provide safe sites for A. trifida seeds that may increase seedling establishment in environments with a high risk of seed predation by other organisms. (2) Cumulative percent emergence of A. trifida in central OH increased rapidly in early spring and reached 60% of maximum by late April, leveled off for a period in May, and increased again at a lower rate before concluding in late July. The biphasic pattern of emergence was fit to a predicitive hydrothermal time model, and the model was validated in a tilled and a no-tillage environment the following year. Root-mean-square values for comparing actual and model-predicted cumulative emergence values ranged from 8.0 to 9.5%, indicating a high degree of accuracy. This experiment demonstrated an approach to emergence modeling that can be used to forecast ragweed emergence on a local basis using easily obtainable soil and weather data. (3) Despite fluctuating environmental conditions during seed development, seed weight within maternal families of A. trifida remained constant for different maturation times. Differences among families constituted 69% of total variation in seed weight, whereas differences within maternal families composed 31% of the variation in seed weight. Percentage late emergence and percentage seed-bank persistence varied among maternal families. In four maternal families, either 0% or 100% of seedlings emerged after 1 May, but a majority of other maternal families produced seedlings both before and after 1 May. Seed-bank persistence rates ranged from 1 to 51% among maternal families. Percentage late emergence and percentage seed-bank persistence were inversely related to maternal-family mean seed weight in 2006, but not in 2005. These results suggest that the inverse relationship between seed size and seed longevity occurs among individuals of a population, but is affected by the environment. PARTICIPANTS: S. K. Harrison and E. Regnier worked equally on this project in 2008, supported by a grant from USDA-NRI. Part of the work was completed in partial fulfillment of the Ph.D. requirements for Brian Schutte at Ohio State University. TARGET AUDIENCES: Target audiences for this effort include the scientific community, particularly students and scientists involved in the general field of agroecology and weed science. The audience also includes agricultural industry clientele, crop producers, and allied professionals. Efforts to disperse this new information include undergraduate and graduate teaching efforts at Ohio State University, outreach via electronic newsletter and popular press releases, radio interviews, and presentation of results at scientific meetings. PROJECT MODIFICATIONS: Not relevant to this project.

Impacts
Research outcomes from this project have resulted in changes in our fundamental knowledge of the ecology of giant ragweed, a severe weed problem in the U.S. Corn Belt and a major source of allergenic pollen in the U.S. and Europe. In the field of invasion biology, it revealed for the first time how an invasive exotic species (L. terrestris), via mutualism, can promote the weedy and invasive behavior of a native annual plant (giant ragweed). Our findings have shed new light on how giant ragweed spreads and becomes established in agricultural and non-agricultural sites with regard to its disperal mechanisms (burial by earthworms), pattern of seedling emergence (continuous and biphasic), and adaptation to agricultural fields (plasticity in seed size and its relationship to seed longevity). These new findings will contribute to more effective weed management by making land managers and crop producers aware of the weed's life history and mechanisms of adaptation, thereby allowing them to develop management strategies that will prevent or minimize its introduction, reproduction, and adaptation in sensitive areas.

Publications

  • Schutte, B., Regnier, E. E., Harrison, S. K., Spokas, K., and Forcella, F. 2008. A hydrothermal seedling emergence model for giant ragweed (Ambrosia trifida). Weed Science 56:555-560.
  • Regnier, E. E., Harrison, S. K., Liu, J., Schmoll, J. T., Edwards, C. A., Arancon, N., and Holloman, C. 2008. Impact of an exotic earthworm on seed dispersal of an indigenous U.S. weed. Journal of Applied Ecology 45:1621-1629.
  • Schutte, B., Regnier, E. E., and Harrison, S. K. 2008. The association between seed size and seed longevity among maternal families in Ambrosia trifida L. populations. Seed Science Research 18:201-211.
  • Davis, A.S., Regnier, E., Harrison, K., Liu, J., Schutte, B., Luschei, E. 2008. Mutualism between common earthworm (Lumbricus terrestris) and giant ragweed (Ambrosia trifida) varies between Ohio and Illinois. Weed Science Society of America Meeting Proceedings. 47:62.
  • Liu, J., Regnier, E. Harrison, K., Holloman, C., Schmoll, J., Diekman, F., and D. Barker. 2008. Net influence of earthworms (Lumbricus terrestris) on giant ragweed (Ambrosia trifida) seedling recruitment. Abstr. Weed Sci. Soc. Am. 47:268.


Progress 01/01/07 to 12/31/07

Outputs
Ambrosia trifida L., an aggressive weed of U.S. grain crops and indigenous to North America, colonizes no-tillage crop fields and undisturbed soils despite its low fecundity, large seed size, and susceptibility to seed predation. Secondary seed dispersal is critical to seed survival and seedling establishment yet mechanisms of secondary dispersal are unknown for A. trifida. Large seeds often require assistance from animals to achieve burial. Field experiments were conducted to determine how foraging for seeds by the European exotic burrowing earthworm, Lumbricus terrestris L., affected A. trifida seed burial, seed bank formation, and seedling recruitment. Experiments were also conducted to determine seed selectivity by L. terrestris. Earthworms buried 94% of A. trifida seeds placed on the soil surface through a deliberate behaviour at a rate up to14-fold greater than abiotic seed burial. There was a six-fold higher concentration of seeds in burrows than in surrounding soil and a mean of 127 A. trifida seeds per burrow after a single season of seed dispersal. Earthworms buried A. trifida seeds from 0.5 to 22 cm deep. Compared to seeds buried abiotically, recruitment from seeds buried by L. terrestris was reduced by 35% due to burial of seeds below emergence depth limits, but biomass of emerged seedlings was increased by 30%. Lumbricus terrestris foraged selectively among eleven large-seeded species tested and collected up to 3.7-fold more seeds of A. trifida than of other species. The earthworms buried small (8.5 mm) A. trifida seeds more deeply than large (11.5 mm) A. trifida seeds.

Impacts
The novel interaction of L. terrestris and A. trifida likely contributes to A. trifida's weedy behavior. Burrows of L. terrestris provide safe sites for A. trifida seeds that can increase seedling establishment in environments with a high risk of seed predation and low probability of seed burial. Efforts to manage A. trifida by increasing seed predation may be ineffective in soils with L. terrestris. The potential for L. terrestris to cache large seeds in its burrows and middens may contribute to the changing dynamics of native versus exotic invasive plant species in ecosystems by increasing recruitment of large-seeded herb, shrub, or tree species. Selective seed collection by L. terrestris and seed size-burial depth interactions may also exert a strong influence on plant community structure and the evolution of seed traits.

Publications

  • Harrison, S. K., E. E. Regnier, J. T. Schmoll, and J. M. Harrison. 2007. Seed size and burial effects on giant ragweed (Ambrosia trifida) emergence and seed demise. Weed Sci. 55:16-22.
  • Liu, J., Regnier, E. E., and Harrison, S. K. 2007. Influence of seed burial by earthworms and seed predation by vertebrates on seedling recruitment in giant ragweed. Proc. North Cent. Weed Sci. Soc. 62:108.


Progress 01/01/06 to 12/31/06

Outputs
Giant ragweed is a competitive, allergenic weed that persists in agricultural fields and early successional sites. Field experiments were conducted to determine the effects of seed size and seed burial depth on giant ragweed emergence and seed demise. In a seedling emergence experiment, small (<4.8-mm-diam) and large (>6.6-mm-diam) seeds were buried 0, 5, 10 and 20-cm in fall 1997 and weed emergence was monitored over the next seven growing seasons. A generalized linear mixed model fit to the cumulative emergence data showed that maximum emergence for both seed sizes occurred at the 5-cm burial depth, where probability of emergence was 19% for small seeds and 49% for large seeds. Emergence probability at the 10-cm burial depth was 9% for small seeds and 30% for large seeds, and no seedlings emerged from the 20-cm burial depth. The model predicted that &#8805; 98% of total cumulative emergence was completed after four growing seasons for large seeds buried 5-cm, five growing seasons for small seeds buried 5-cm and large seeds buried 10-cm, and seven growing seasons for small seeds buried 10-cm. Seed size and burial treatment effects on seed demise were tested in a second experiment using seed packets. Rates of seed demise were inversely proportional to burial depth, and the percentage of viable seeds remaining after four years ranged from 0% on the soil surface to 19% at the 20-cm burial depth. Some seeds recovered from the 20-cm burial depth were viable after nine years of burial. These results coupled with previous research suggest that seed size polymorphism facilitates giant ragweed adaptation across habitats, and that a combination of no-tillage cropping practices, habitat modification, and timely weed control measures can reduce its active seed bank in agricultural fields by 90% or more after four years.

Impacts
Prolonged seedling emergence is a key component of giant ragweed interference in grain crops, yet the factors that contribute to this behavior are not understood. These results showed that emergence behavior depended greatly on the plant from which seeds were produced. Late emergence within the population at large was due to the presence of particular plants within the population which produced seeds that germinated over a prolonged period. High plant-to-plant variation in seed dormancy characteristics in giant ragweed may be one of the causes of weedy behavior in this species. This research may help in developing guidelines for predicting weedy and/or invasive behavior in native and introduced plant species.

Publications

  • Harrison, S. K., E. E. Regnier, J. T. Schmoll, and J. M. Harrison. 2007. Seed size and burial effects on giant ragweed (Ambrosia trifida) emergence and seed demise. Weed Sci. 55: (In press).
  • Regnier, E., K. Harrison, and J. Schmoll. 2006. Impact of seed caching by the earthworm, Lumbricus terrestris, on giant ragweed (Ambrosia trifida) establishment. Abstr. Weed Sci. Soc. Am. 46:247.
  • Schutte, B., E. Regnier, and K. Harrison. 2006. Dissection of divergent emergence patterns in agricultural and successional populations of giant ragweed (Ambrosia trifida). Abstr. Weed Sci. Soc. Am. 46:249.
  • Schutte, B., E. Regnier, and K. Harrison. 2006. Maternal plants as sources of emergence variation within giant ragweed (Ambrosia trifida) populations. Abstr. Weed Sci. Soc. Am. 46:118.


Progress 01/01/05 to 12/31/05

Outputs
Giant ragweed is an annual broadleaf weed in summer annual crop production. Its weediness is attributed in part to prolonged seedling emergence since late-season seedlings evade early-season control measures and are competitive. Giant ragweed dispersal units exhibit plant-to-plant variation in size, color and shape. Variation in seed dormancy within a species is often associated with variation in seed morphology. Field studies were conducted to determine the influence of interplant variation on emergence behavior of two central Ohio giant ragweed populations sampled two consecutive years. Dispersal units from 25 giant ragweed individuals (i.e. 25 half-sib families) were planted each autumn at a uniform depth. The following spring, emergence was monitored and first and final emergence date were compared among individuals with nonparametric Friedman tests based on rank scores. Dispersal unit dimensions were measured and their relationships with emergence parameters were evaluated with Wilcoxon rank sum tests. Dates of first and final emergence were each significantly different among half-sib families, resulting in unique emergence phenologies among the progeny of different maternal plants. Among half-sib families, two distinct emergence patterns were identified: 1) synchronous early emergence and 2) asynchronous prolonged emergence. Day of final emergence was negatively correlated with dispersal unit size. Therefore, half-sib families of smaller dispersal units concluded emergence later in the season than half-sib families of larger dispersal units. These results are consistent with seed size and seed dormancy as parts of a coadaptive syndrome for seedling establishment. Furthermore, results indicate that variation in seed dormancy and/or germination characteristics within particular maternal genotypes is the primary cause of late-season emergence in giant ragweed populations. Knowledge of the causes of variable seed dormancy in giant ragweed individuals will enable a better understanding of late-season emergence in this species.

Impacts
Prolonged seedling emergence is a key component of giant ragweed interference in grain crops, yet the factors that contribute to this behavior are not understood. These results showed that emergence behavior depended greatly on the plant from which seeds were produced. Late emergence within the population at large was due to the presence of particular plants within the population which produced seeds that germinated over a prolonged period. High plant-to-plant variation in seed dormancy characteristics in giant ragweed may be one of the causes of weedy behavior in this species. This research may help in developing guidelines for predicting weedy and/or invasive behavior in native and introduced plant species.

Publications

  • Schutte, B., E. Regnier, and S. K. Harrison. 2005. The effect of interplant variation on Ambrosia trifida L. emergence patterns. Proc. Ohio Invasive Weed Conf., Columbus, OH. Ohio Agric. Res. Devt. Ctr. Special Circular 196:105-108.
  • Schutte, B., E. Regnier, and S. K. Harrison. 2005. Maternal plants as sources of emergence variation within Ambrosia trifida populations. Ecol. Soc. Am. Abstract 222.


Progress 01/01/04 to 12/31/04

Outputs
Giant ragweed is a severe annual broadleaf weed in summer annual crop production. The severity of giant ragweed interference in Ohio crop production is partially attributed to prolonged, continuous seedling emergence. Within a population, nonsynchronous emergence can result from interplant and intraplant variation. Giant ragweed populations exhibit a high degree of variation in sizes of diaspores (dispersal units) among individual plants and diaspore size is known to affect emergence phenology of other species. Therefore, we hypothesized that within giant ragweed populations, there is interplant variation in emergence phenology, and diaspore size influences emergence phenology. Diaspores from 25 giant ragweed individuals (i.e. 25 half-sib families) were planted at a uniform depth in the autumn of 2002. In spring of 2003, emergence was monitored on a regular basis. Diaspore dimensions were determined with image analysis software and relationships between diaspore dimensions and emergence were examined. Emergence phenology differed significantly among half-sib families, and two forms of emergence phenology were identified: 1) synchronous and 2) continuous. A negative relationship between dispersal unit dimensions and days to 95% emergence was detected in one population. Definitive conclusions concerning diaspore size and emergence phenology require additional experiments. Results of this experiment show unique emergence behaviors among half-sib families, which could contribute to the overall continuous emergence pattern commonly observed in giant ragweed populations of Ohio crop fields. Results of this experiment show unique emergence behaviors among half-sib families, which helps explain the prolonged emergence of giant ragweed in Ohio crop fields.

Impacts
Results of this study show that seed dormancy varies among individual mother plants within a giant ragweed population. Results of this study shed light on the prolonged emergence of giant ragweed in Ohio that often requires additional weed control measures by crop producers during the corn and soybean growing season. A greater understanding of the factors controlling weed emergence will allow crop producers to time control practices more efficiently and thus reduce production costs and yield losses.

Publications

  • Schutte, B. J., E. E. Regnier, and S. K. Harrison. 2004. The effects of interplant variation on Ambrosia trifida L. emergence patterns. Proc. North. Cent. Weed Sci. Soc. 59:55.
  • Schutte, B. J., E. E. Regnier, and S. K. Harrison. 2004. Primary seed dormancy in Ambrosia trifida L. (giant ragweed). Proc. North. Cent. Weed Sci. Soc. 59:119.