Progress 08/15/05 to 08/14/10
Outputs
OUTPUTS: Field and laboratory studies showed that the common nightcrawler, a non-indigenous earthworm species in North America, collects large numbers of seeds of giant ragweed, an indigenous weed of grain crop fields, and buries them in its burrow, presumably as a source of food. The seeds are too large for the earthworm to ingest directly, however, the earthworm could conceivably feed on the woody seed hull, which decays in soil within a few years. The enclosed seed can remain intact, if buried sufficiently deep, seeds can remain dormant in the soil for up to nine years. In field and laboratory experiments, the earthworm preferred the seeds of giant ragweed to those of other large-seeded weedy species, but collected and buried at least some seeds from all the species tested, suggesting that foraging for seeds is a common behavior in this earthworm. Seed burial by the earthworm in various crop habitats protected seeds from being consumed by mice, the primary post-dispersal predator of giant ragweed seeds. Earthworm burrows and giant ragweed seedlings were associated to varying degrees in no-tillage corn and soybean fields across Ohio, Indiana, and Illinois. The degree of association between the two species increased with precipitation and temperature during fall and winter months, when the earthworm is most active. This indicates that the potential for the earthworm to influence seed burial and thereby seed survival, varies with climatic conditions. The earthworm is well known to bury small bits of inorganic materials such as pebbles in its burrow, perhaps as structural elements. In laboratory experiments, the earthworm preferentially collected giant ragweed seeds over plaster-cast duplicates of the seeds, and foraged the seeds from below in addition to from above the soil surface. This subterranean foraging suggests that the earthworm utilized olfactory sensing to detect the seeds and supports the hypothesis that the earthworms collect seeds as a source of food rather than structure. Collectively, these studies suggest that in the association of the earthworm and giant ragweed, the earthworm gains nutrition from the expendable seed hulls and the seeds gain protection from predators. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Scientists, consultants, growers, educators, non-governmental organizations, and students PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
As a result of the research, crop producers and land managers can better predict and prevent the spread of giant ragweed into crop fields and non-crop habitats. Presence of the earthworm in crop fields is desirable due to its positive effects on crop growth, thus the findings of this research suggest that a major emphasis be placed on management systems that prevent ragweed introduction, establishment, and seed dispersal in fields colonized by the earthworm. Better ragweed management systems will improve crop production efficiency and reduce allergenic pollen levels. The research findings also represent a change in knowledge about earthworm foraging behavior and evolution of a mutualism between a non-indigenous invasive species and a native annual plant. Discovery of this phenomenon sheds new light on the potential impacts of biological invasions on native flora and fauna by other non-indigenous organisms.
Publications
- Schutte, B., J. Liu, A. S. Davis, S. K. Harrison, and 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
- Regnier, E., Harrison, K., Liu, Schmoll, J., Edwards, A., Arancon, N. & C. Holloman. 2008. Impact of an exotic earthworm on seed dispersal of an indigenous U.S. weed. Journal of Applied Ecology 45:1621-1629
- 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
- Regnier, E., K. Harrison, C. Holloman, C. Edwards, J. Liu, B. Shutte, A. Davis, and N. Arancon. 2010. Active dispersal of Ambrosia trifida seeds by the earthworm Lumbricus terrestris: Impact on seed survival and plant establishment. Proceedings of Seed Ecology III, the Third International Seed Science Society Meeting for Seeds and the Environment, Vol 3:146-147
- Harrison, K., E. Regnier, J. Liu, N. Arancon, and C. Edwards. 2010. Secondary seed dispersal of Ambrosia trifida by Lumbricus terrestris: Implications for Earthworm Weed Interactions. Proceedings of the 9th International Symposium on Earthworm Ecology. Vol. 9: 167
- Regnier, E., K. Harrison, C. Holloman, N. Arancon, and C. Edwards. 2010. Why do earthworms (Lumbricus terrestris) collect and bury seeds Abstr. Weed Sci. Soc. Am. 49:P C-102
- Schutte, B., J. Liu, A. Davis, K. Harrison, and E. Regnier. 2009. The association between the earthworm Lumbricus terrestris and giant ragweed (Ambrosia trifida) in agricultural fields across the eastern U.S. Corn Belt. Abstr. Weed Sci. Soc. Am. 48:255
- Davis, A. S., Regnier. E., Harrison, K. Liu, J., Schutte, B. and E. Luschei. 2008. Mutualism between common earthworm (Lumbricus terrestris) and giant ragweed (Ambrosia trifida) varies between Ohio and Illinois. Abstr. Weed Sci. Soc. Am. 48
- 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. 48
- Regnier, E. E., Harrison, S. K., and Schmoll, J. T. 2006. Impact of seed caching by the earthworm, Lumbricus terrestris, on giant ragweed (Ambrosia trifida) establishment. Abstr. Weed Sci. Soc. Am. 46:247
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Progress 08/15/08 to 08/14/09
Outputs
OUTPUTS: The primary goal of this project is to elucidate the relationship between the naturalized earthworm, Lumbricus terrestris, and the native annual noxious weed, Ambrosia trifida (giant ragweed). This earthworm is abundant across much of the eastern U.S. and collects organic and inorganic debris from the soil surface, and then stores the materials in its burrow. It derives nourishment from the decomposing plant matter, but its reasons for collecting the inorganic debris (pebbles, glass, etc.) are unknown; however, these materials may possibly serve as a structural burrow components. It also collects seeds of various weed species, including giant ragweed, thereby protecting the seeds from predation and increasing the probability of weed emergence in some environments. Given the physical resemblance between hardened seeds and rock fragments, it is unclear whether L. terrestris buries large 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. In duplicate experiments, 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. This behavior has not been reported previously in the literature. These results provide evidence that earthworms collect seeds specifically for food and suggest that a conditional mutualism has evolved that benefits the survival of both A. trifida and L. terrestris. PARTICIPANTS: Not relevant to this project. TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
The findings presented above represent a change in knowledge about L. terrestris behavior and about a mutualism that has evolved between an exotic invasive species (L. terrestris) and a native annual plant (A. trifida). The apparent facilitation of A. trifida weedy behavior by L. terrestris has the potential to change actions of crop producers and land managers as new efforts are developed 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 A. trifida, a native of North America, has become a serious exotic invasive weed species. A. trifida's threat to human health is even higher abroad than in North America due to a higher level of susceptibility to the ragweed allergen exhibited by human populations of those regions, including several countries in Europe and Asia. Successful implementation of ragweed management strategies that utilize the basic knowledge gained in this project could result in a change in conditions manifested by reduced weed competition in crops and other plant communities, and by a significant reduction in the most widely abundant aeroallergen in several parts of the world.
Publications
- No publications reported this period
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Progress 08/15/07 to 08/14/08
Outputs
OUTPUTS: We established a field study to determine the depth distribution of giant ragweed seeds in earthworm (Lumbricus terrestris) burrows, which will influence their ability to emerge, and to determine the effect of the burrow environment on giant ragweed seed germination and viability. Burrows are enriched in nutrients, microorganisms, moisture and oxygen, which could accelerate seed demise and earthworms may feed on seed or seedling tissues. Giant ragweed seeds were placed near individual earthworm burrows and earthworms buried all or nearly all the seeds. "Artificial control" burrows were created by extracting a soil core (3 cm in diameter by 20 cm deep) with a soil corer, seeding the core lengthwise with giant ragweed seeds, wrapping the core in plastic window screen, and replacing it in the soil. The aim was to compare seed integrity in earthworm and artificial burrows at comparable depths. Burrows were retrieved for seed analysis in the fall and spring. Extraction of the earthworm burrows was difficult due to their irregular orientation (mostly vertical but with some horizontal segments). Coring methods were unsatisfactory. Ultimately, we extracted the burrows in short depth sections with a cup cutter so we could track the burrow. The artificial burrows were easily removed, however, the narrow diameter caused crowding of giant ragweed seedlings, which may have affected total emergence. Also, the surrounding screen may have limited lateral diffusion of water into the soil core, which could also affect seed germination. Procedures will be modified to address these problems in fall 2008. Field studies were conducted to determine the intensity of seed predation by rodents and seed burial by earthworms in 10 different fields at the Ohio State University Waterman Farm in Columbus, OH. At each site, two treatments were established: low (mowed) and high vegetative cover (unmanaged edge vegetation). The study was conducted to gain insight into the magnitude of variation in seed predation and seed burial by earthworms as influenced by habitat, since the interaction of these two organisms is expected to influence seed fate and seedling recruitment. At each site, giant ragweed seeds were attached to 30-cm threads and the ends of the threads pinned to the soil by flags distributed along transects. The seeds were monitored for predation and burial during fall and winter. Data are being used to refine a Bayesian model (developed from a previous study) that estimates the probabilities of seed predation and seed burial by earthworms and the net effects of earthworms on seedling recruitment. A survey was conducted in collaboration with Adam Davis (USDA, University of Illinois) in Ohio, Indiana, and Illinois (total of 11 sites) to determine whether giant ragweed is associated with earthworm burrows across the broader Corn Belt. The proportion of giant ragweed emerging from burrows, total number of burrows, surface area covered by middens (mounds of debris and castings overlying the burrows), spatial distribution of middens and seedlings, soil resistance in middens vs areas outside of middens, and soil analysis data were taken. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Results of the various experiments are undergoing analysis. However, some conclusions can be drawn. Earthworms bury the vast majority of giant ragweed seeds in the upper 5 cm of the soil, from where they can easily germinate. A large proportion of giant ragweed seeds buried below emergence depth limits germinate but fail to emerge and it appears that fatal germination is a major source of seed loss from giant ragweed seed banks. We have not found any evidence to date that seed burial by earthworms has any effect on seed viability, dormancy, or germination in comparison to seed burial at comparable depths outside of burrows. However, experimental procedures need to be refined before drawing definitive conclusions. In areas with established populations of Lumbricus terrestris, the probability of seed burial by earthworms is affected only slightly little by habitat (mowed vs unmanaged edge vegetation). However, habitat had a large impact on seed predation by rodents, with much greater predation in unmanaged vegetation, probably due to provision of greater protective cover. In these areas, seed burial by earthworms was slightly lower, possibly due to competition for seeds with rodents. Giant ragweed was significantly associated with earthworm burrows at all sites sampled in Ohio, Indiana, and Illinois, indicating that earthworms exhibit the same seed collecting behavior over a broad geographic area and may influence giant ragweed seedling recruitment wherever the two species occur together. The degree of aggregation of seedlings in burrows appeared to be lower in Illinois than in Indiana or Ohio, but this remains to be verified statistically.
Publications
- Regnier, E., Harrison, K., Liu, J., Schmoll, J., Edwards, C., Arancon, N., and Holloman, C. 2008. Impact of an exotic earthworm on seed dispersal of an indigenous US weed. J. Appl. Ecol. (In Press).
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Progress 08/15/06 to 08/14/07
Outputs
Field and laboratory experiments were conducted to explore the bases for seed selection in the seed foraging behavior of the anecic earthworm, Lumbricus terrestris. Previous research showed that L. terrestris collects and buries large numbers of Ambrosia trifida seeds (i.e., 127 seeds per burrow). Ambrosia trifida is a prominent weed in crop fields in the U. S. Corn Belt. There is increasing interest in managing weed populations by reducing tillage and providing refugia to increase weed seed predation. Lumbricus terrestris may influence weed seed survival by burying seeds selectively. Field and laboratory experiments were conducted to test the selectivity of the earthworms between seeds and other plant litter, among seeds of various species and different seed sizes, and between seeds with and without an intact embryo. Lumbricus terrestris showed no preference between A. trifida seeds and fragments of A. trifida leaf or stem litter of similar sizes as seeds, and
collected a similar number of A. trifida seeds in the presence or absence of soybean (Glycine max) leaf litter, which is commonly collected by the earthworms. Lumbricus terrestris foraged selectively among seeds of eleven weed and crop species that ranged in size from 3.4 to 18.6 mm long. In field studies, L. terrestris collected similar numbers of A. trifida, Helianthus annuus, and Sicyos angulatus seeds, and collected more seeds of these species than of Glycine max, Zea mays, or Xanthium strumarium seeds (n = 16, P < 0.001). The percent seed collection ranged from 23% for X. strumarium to 86% for A. trifida. In laboratory studies, L. terrestris collected similar numbers of A. trifida, Convolvulus avensis, and Pastinaca sativa seeds, and collected more A. trifida seeds than Arctium minus, Bidens frondosa or Ipomoea purpurea seeds (n = 24, P < 0.05). Seeds collected ranged from 64% for I. purpurea to 90% for A. trifida. Differences in the percentages collected were less pronounced
among smaller seeds (laboratory study) than larger seeds (field study), suggesting that seed size was an important factor in selectivity by L. terrestris. Very smooth seeds lacking protuberances (i.e., I. purpurea), or bearing long or dense spines (i.e., X. strumarium), or highly spheroid (i.e., G. max) were collected in fewer numbers than other seeds. In other experiments, the earthworms buried small (8.5 mm) A. trifida seeds more rapidly and deeply than large (11.5 mm) A. trifida seeds. Earthworms collected equal numbers of A. trifida seeds that contained or lacked an intact embryo. We conclude that L. terrestris deliberately forages for seeds too large to ingest (> 3 mm). Selection by L. terrestris among large seeds may depend on morphological traits that influence gripping and pulling seeds across the soil surface and into their burrows. We hypothesize that L. terrestris perceives seeds as bits of organic material rather than as seeds per se. Seeds may be a desirable source of
organic material due to easy storage inside burrows, where they may be protected from pilfering by neighboring earthworms. Further research is needed to determine if the earthworms feed on the collected seeds or their germinants.
Impacts
Selective seed collection by L. terrestris and seed responses to burial depth inside its burrows may result in differential seedling establishment among species, or among different seed morphologies within a single species, thereby influencing plant community composition in agroecosystems and contributing to plant biotype selection and evolution. Burrows of L. terrestris may provide safe sites for A. trifida seeds that increase seedling establishment. Efforts to manage A. trifida by reducing tillage and increasing seed predation may be ineffective in soils with L. terrestris, and other tactics such as preventing seed production should be employed. Seed burial by L. terrestris should be considered as a factor that may influence weed community composition in crop fields.
Publications
- No publications reported this period
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Progress 08/15/05 to 08/15/06
Outputs
Field experiments and surveys were conducted to determine the interaction of the common earthworm, Lumbricus terrestris, and giant ragweed. Giant ragweed is native to the U.S. and a major annual crop weed in the midwest. Lumbricus terrestris is a burrow-dwelling earthworm introduced from Europe and widely distributed in agricultural fields and grasslands. Lumbricus terrestris caches giant ragweed seeds while foraging at the soil surface by gripping the large seeds with its mouthparts and pulling them inside its burrow. The function of caching seeds remains unknown but the outer covering of giant ragweed seeds decays rapidly and may provide nourishment to the earthworms. The majority of cached seeds are buried within the top 5 cm of the soil profile but seeds can be buried over 20 cm deep. Lumbricus terrestris has both a positive and negative effect on seedling emergence. A positive impact results from rapid burial, decreasing seed vulnerability to seed predators. A
negative impact results from burial of seeds below the emergence depth limit. An experiment was conducted for a two-year period to determine the net effects of L. terrestris on giant ragweed seedling establishment in the presence and absence of seed predators in unvegetated and early successional habitats. When fit in a Bayesian model, the data showed that the influence of seed predators on the probability of a seed surviving to seedling stage was reduced by the presence of L. terrestris (20% in the bare site and 50% in the successional site). This change in seed predator effects caused by L. terrestris suggests that L. terrestris are somewhat protective of seeds in the presence of predators. The results are consistent with conditional mutualism, in which the outcome of the interaction of two species ranges from antagonistic to mutualistic depending on ecological and life-history factors. We expect that L. terrestris has a positive impact on giant ragweed establishment where
opportunities for seed burial are low, predation intensity is high, and soil conditions for L. terrestris are favorable. This earthworm species may play an important role in the establishment and persistence of giant ragweed.
Impacts
This research reveals a new dispersal mechanism for giant ragweed seeds involving one of the most common agricultural earthworm species, Lumbricus terrestris, adding to our fundamental understanding of weed establishment.
Publications
- No publications reported this period
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