Source: SOUTH DAKOTA STATE UNIVERSITY submitted to
PLANT-ANIMAL INTERACTIONS IN A CHANGING WORLD
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
1021629
Grant No.
(N/A)
Project No.
SD00H708-20
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Jan 17, 2020
Project End Date
Dec 21, 2020
Grant Year
(N/A)
Project Director
Razafindratsima, ON, .
Recipient Organization
SOUTH DAKOTA STATE UNIVERSITY
PO BOX 2275A
BROOKINGS,SD 57007
Performing Department
Natural Resource Management
Non Technical Summary
Anthropogenic pressures on natural systems (such as land use, overexploitation, and biological invasions) have resulted in alarming environmental changes that pose critical concerns for the maintenance and persistence of biological diversity and the ability of ecosystems to provide society with vital goods and services to prosper. For example, the invasion of various non-native plant species in North America's northern Great Plains (such as weeds in rangeland, introduced grasses and forbs in South Dakota prairies) has resulted in substantial reductions of the diversity of native plant communities and loss of important ecological function, as well as impacted the economy related to livestock and crop production. Limiting the long-term impacts of these environmental changes requires an understanding of species responses and ecosystem resilience.The functioning of an ecosystem often relies on crucial ecological processes, such as seed dispersal services provided by fruit-eating animals. Seed dispersal is an important process in plant life cycles, ensuring their continued existence, as it provides advantages for the survival and establishment of seedlings, genetic diversity within populations, and their spread across landscapes. It can also indirectly benefit humans by supporting vital ecosystem services. For example, by supporting wild plant populations, it provides key resources (e.g., food and habitat) that sustain pollinators for agricultural crops and facilitates the natural restoration of degraded landscapes. Consequently, establishing strategies for the conservation and management of seed dispersers can benefit society. For instance, knowledge of the impacts of anthropogenic activities on seed dispersal processes can be applied to slow biodiversity decline, increase the extent of activities aimed at restoring ecological functions and increasing wildlife populations, manage biological invasions, and facilitate the adaptations of interacting species to environmental changes.The disruption of such vital biotic interactions can have cascading impacts within the ecosystem, imperiling its functioning, because if one species disappears the roles it played can be lost as well, especially if no other species can perform similar roles. In addition, if one of the partners is absent or vulnerable to an environmental change, the other partner may also become vulnerable indirectly. For example, over-harvest of large animal seed-dispersers through hunting has been shown to negatively influence regeneration processes within plant communities, reducing plant diversity and eventually affecting other associated taxa and impacting ecosystem health.The goal of this project is to investigate species responses to the drivers of environmental changes with respect to the mutualistic seed-dispersal interactions in which they are involved, with a focus on woody plant communities (trees and shrubs) and their dispersers in the heterogeneous landscapes of South Dakota. The project will employ an integrative approach combining field-based sampling, experiments, and modeling to address the following specific objectives: (1) Assess whether seed-dispersing animals provide adaptive advantages for plants to cope with local environmental changes, (2) Examine how plant species that rely on specific/restricted seed disperser community persist in the face of seed disperser loss, and (3) Investigate the impacts of losing animal seed dispersers on ecosystem health.Field sampling will include the use of camera-traps to identify animal seed-dispersers, observations of fruiting trees and shrubs, and surveys of tree/shrub species composition. Experiments will be either field-based or in a controlled environment in the lab to assess seed fate, including seed germination and seedling survival. Mechanistic models and simulations will be developed to examine the persistence of plants in the face of seed disperser loss, using empirical data from field and lab work. This project will also take advantage of existing geospatial and climatic databases for some of the analyses. In addition to the potential of this project to advance our understanding of seed dispersal ecology in a changing world, it will also fill knowledge gap on the important roles and impacts of mammals and birds as seed dispersers in South Dakota. Such information can be used as a baseline for other research and for educational purposes at any level.
Animal Health Component
0%
Research Effort Categories
Basic
75%
Applied
25%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
1360830107040%
1360850107030%
1360860107030%
Goals / Objectives
Anthropogenic pressures on natural systems (e.g., fragmentation due to conversion of land for agriculture, over-exploitation, and biological invasions) have resulted in environmental changes that pose critical concerns, threatening the maintenance and persistence of biodiversity, and affecting the ability of ecosystems to provide vital goods and services to society. For example, the invasion of various non-native plant species in North America's northern Great Plains (such as weeds in grasslands and introduced grasses and forbs in prairies) has resulted in substantial reduction of the diversity of native plant communities and loss of important ecological functions, as well as impacted the economy related to livestock and crop production (DiTomaso 2000, Grant et al. 2009, Pejchar and Mooney 2009). Finding solutions to limit the long-term impacts of these environmental changes requires a deeper understanding of the magnitude of the impacts and how species and ecosystems respond.These anthropogenic environmental changes can lead to a collapse of the ecological equilibrium within an ecosystem, especially when vital biotic interactions, such as mutualism, are affected. Given that every single species on Earth participates in at least one mutualistic interaction, and many key aspects of ecosystem health closely depend on biotic interactions, the disruption of such interactions can have pervasive cascading impacts on the ecosystem. In fact, if one of the interacting species is vulnerable to an environmental change, its partner may also indirectly become vulnerable. The disruption of mutualistic interactions may be especially challenging for certain species because mutualisms are suggested to have evolved as a response to stressful environmental conditions and limiting factors. Characterizing how an ecosystem might respond to environmental changes should, therefore, consider the multi-faceted aspects of the importance of biotic interactions and the responses of the interacting species.Mutualistic interactions are fundamental to reproduction and survival of many organisms, and therefore to the healthy functioning of an ecosystem. Essential ecosystem services provided by mutualists include pollination and seed dispersal (i.e, movement of seeds away from the parent plant). Seed dispersal by animals (such as birds and mammals), has been demonstrated to play a fundamental role in shaping the diversity, structure, composition, and spatial arrangement of plant communities, and in influencing a plant population's ability to escape local environmental changes. These impacts of animal-mediated seed dispersal on plants can have important implications on ecosystem integrity, and support the ecosystem's ability to provide important goods and services for human society. For example, by supporting wild plant populations, seed dispersal can provide habitat and food to sustain the availability of pollinators for agricultural crops and wildlife harvested as game. It can also facilitate the natural regeneration of plants that are commonly harvested from the wild - e.g. wild raspberries, wild grapes and medicinal plants such as Ligusticum porteri that are commonly harvested in South Dakota.The disruption of seed dispersal interactions as a result of anthropogenic environmental changes could result in cascading negative impacts in an ecosystem. For instance, the loss of an animal species that provides crucial seed dispersal services may negatively reduce the recruitment of the plant population that relies on it for its dispersal, increasing its probability of extinction. If no other animal species can fill this functional gap of seed dispersal, this plant species may essentially be "living dead" with the long-term outlook being local, or even global, extinction. The significant decrease and/or loss of biodiversity can result in the reduction of ecosystem productivity (including biomass production and nutrient recycling) and change the dynamics of ecosystem functions over time.Therefore, maintaining seed dispersal interactions can have important implications for conservation and management. In addition to its importance in maintaining a healthy ecosystem, seed dispersal also favors the natural restoration of degraded landscapes, consequently reducing management costs and helping with climate change mitigation. In addition, seed dispersal can facilitate the spread of plant populations and the maintenance of genetic movement within and among populations between isolated habitats across a fragmented landscape. This is of particular concern in South Dakota and the Midwest, as the conversion of land for agriculture and urban/suburban development has resulted in fragmentation in much of the landscape into isolated habitats.The overarching goal of this project is to investigate species responses to the drivers of environmental changes with respect to mutualistic seed-dispersal interactions in which the species are involved. With a focus on seed dispersal interactions within terrestrial communities, it will address the following specific objectives:1)Assess whether seed-dispersing animals provide adaptive advantages for plants to cope with local environmental changes2)Examine how plant species that rely on specific/restricted seed disperser communities persist in the face of seed disperser loss3)Investigate the impacts of losing animal seed dispersers on ecosystem healthThis project will focus on seed dispersal of woody plant communities (trees and shrubs) by animals in the heterogeneous landscape of South Dakota. Globally, up to 90% of flowering plants rely on fruit-eating animals for the dispersal of their seeds, and mammals and birds are considered the most important seed dispersers in many ecosystems. While many studies have greatly contributed to our understanding of animal-mediated seed dispersal, knowledge of the relative importance of seed dispersal by animals is sparse in North-temperate regions compared to the tropics. However, many species in North America, even those considered as carnivores, include fleshy fruits as a significant part of their diet and can contribute to the seed dispersal of many plant species. Therefore, in addition to the potential of this project to advance our understanding of seed dispersal ecology in changing environments, it will also fill our knowledge gap on the important roles and impacts of animals on seed dispersal in the ecosystems in North America, specifically South Dakota.Known and potential seed dispersers (i.e., with fruits and/or seeds in their diet) in the heterogeneous landscapes of South Dakota include the following: Mammals - Virginia opossum (Didelphis virginiana), eastern cottontail (Sylvilagus floridanus), white-tailed jackrabbit (Lepus townsendii), coyotes (Canis lantrans), swift fox (Vuples velox), and white-tailed deer (Odocoileus virgianus); Birds - rock dove (Columba livia), blue jay (Cyanocitta cristata), American robin (Turdus migratorius), yellow-rumped warbler (Dendroica coronata), Northern cardinal (Cardinalis cardinalis), rose-breasted grosbeak (Pheucticus ludovicianus), and dickcissel (Spiza americana).The potential of plants to be primarily dispersed by animals is often characterized by the presence of a rewarding structure, such as fleshy edible pulp, to attract consumers. This project will thus focus on such plants which include: hackberry (Celtis occidentalis), crabapple (Mallus), hawthorn (Crataegus spp.), American linden (Tilia americana), bur oak (Quercus macrocarpa), red mulberry (Morus rubra), red-osier dogwood (Cornus sericea), black walnut (Juglans nigra), wild plum (Prunus americana), nannyberry (Viburnum lentago), Kinnikinnik (Arctostaphylos uvaursi), and juniper (Juniperus spp.).
Project Methods
This project will employ an integrative approach, combining field-based sampling, experiments, and modeling to address each specific objective. It will focus mostly on the East River portion of South Dakota, in sites that are mostly dominated by tree/shrub plant communities (such as upland forests and woodlands).To develop baseline information for this project, the composition of seed disperser assemblages will first be examined by monitoring plants bearing fruits using camera traps to record their animal visitors consuming fruits, both arboreal and on the ground. The focal plants will be selected based on their fruit traits - i.e. whether they are exhibiting traits related to seed dispersal by animals. The use of camera traps in studies of frugivory interactions has recently gained much attention given the inherent difficulty in tracking multiple frugivores that may be responsible for the dispersal of a single plant species. For each focal plant, one camera trap will be set-up to overlook its branches bearing fruit and another trap put at the base. These cameras will be checked every two weeks until no more fruit is present on the focal plant. The pictures/videos will be used to identify the animal species and examine their seed-handling behavior to classify it as seed disperser, fruit-pulp consumer, or seed predator.Direct observations of some fruiting focal plants will also be conducted (on plants with no camera traps) to record the identity and behavior of seed dispersers that may not have been caught on camera. Each focal plant will be watched for at least a total of 24 non-continuous hours that will encompass day and night hours. During each watch, each animal visitor feeding on fruits and their seed-handling behavior will be recorded.Finally, tree/shrub species composition within a site will be determined by sampling all stems ≥ 2.5 cm in diameter in 10 transects of 2 x 50 m. These trees/shrubs will be also mapped and tagged. Each tree/shrub species will be categorized as animal-dispersed and non-animal dispersed (i.e. dispersed by other means such as gravity, wind, or explosion) based on fruit/seed traits. This will establish a database of the tree/shrub species with their characteristics at different stages, supported with photographic images.Objective 1: Assess whether seed-dispersing animals provide adaptive advantages for plants to cope with local environmental changesI will conduct an environment-controlled experiment to determine seed germination and seedling survival of animal-defecated seeds under different scenarios of local environmental change: 1) no change in environmental conditions, 2) increased temperature, 3) nitrogen enrichment, 4) increased dryness, and 5) moisture saturation.Fecal samples containing seeds will be collected at least every other week for a year by searching on the ground in the field sites and by using seed traps to collect fecal samples from arboreal animals. Each trap will be made of durable window screening stapled on a rind of polyvinyl tubing (total trap area ~0.5 m2) and hung on tree branches to minimize seed predation/removal. The experiment will be initiated as soon as we have samples. Each seed will be subject to a treatment that reflects either one of the five scenarios listed above, following a gradient of change (from zero to higher value). Individual seeds will be placed on the surface of soil-less pottery mix in individual pots and kept moist; then put in a growth chamber with daily light/dark cycle. To allow for accurate identification of the species dispersed, the seedlings will be kept until identification to species, based on leaf traits, could be confirmed. I will also explore the cost effectiveness of using DNA analysis to determine plant identity. In addition, during each sample collection period, the fruiting phenology of the plant communities in the area will also be recorded. This will provide additional information on what species the seed might be. For any plant fruiting during that period, fruit samples will also be collected to extract seeds to be used as a control in the experiment.Objective 2: Examine how plant species that rely on specific/restricted seed disperser community persist in the face of seed disperser lossSeveral hypotheses have been put forth as an alternative mechanism of seed dispersal in "orphan" plant species (i.e. lacking extant seed dispersers), ensuring their persistence despite the absence of their primary seed dispersers. These include (i) dispersal by strong winds and runoff/flooding associated with heavy precipitation events, and (ii) secondary dispersal by ground-dwelling animals such as scatter-hoarding rodents. Secondary seed dispersal refers to the dispersal of a seed after it has reached a surface. My lab group will test these hypotheses on large-seeded plant species that may have already lost their dispersers - e.g. Osage-orange, Maclura pomifera, once dispersed by Pleistocene megafauna in North America (such as mammoths).This objective will be approached via the following:·establishment of a weather-sensitive mechanistic wind-dispersal model based on plant functional traits and weather parameters;·lab experiments on the movement of large seeds subject to moving water;·field- and lab-based seed germination and survival experiments to investigate whether seeds dispersed through abiotic means would germinate even without the removal of the pulp by a seed consumer, and to determine the consequences of partial consumption of seeds (if any) on their germination success;·field surveys with camera traps, similar to what was described earlier, to determine the animal assemblages that disperse large seeds (in fruits) that fall on the ground of the parent plant;·field monitoring of seeds marked with telemetric thread tags, which will consist of nylon-coated stainless steel leader wire with a cylindrical very high frequency (VHF) transmitter and a pink flagging tape with unique code;·development of simulation models parameterized using these empirical data.Objective 3: Investigate the impacts of losing animal seed dispersers on ecosystem healthThe disruption of seed-dispersal interactions, in the event of extinction of one of the interacting species, can have far-reaching cascading consequences leading to a collapse in the ecosystem equilibrium. To investigate the multi-faceted aspects of the consequences of seed dispersal loss on the ecosystem health, this project will integrate the aforementioned empirical data with modeling under two scenarios: (1) no dispersers (in which seeds simply fall under the parent plant and thus have high mortality), and (2) with dispersers. Both scenarios will consider within-landscape microhabitat variations to account for differences in the suitability of the habitats for germination and establishment. Plant recruitment probability and the potential of the ecosystem to provide vital services (such as carbon sequestration) will be measured for each scenario.EffortsEfforts to cause a change in knowledge will include dissemination of the findings to the scientific community through publications in scientific journals and presentations at scientific conferences, formal training and mentoring of undergraduate, graduate students, and research technicians, and experiential learning for students. I will also use the findings of this research in my teaching as case study examples. Efforts to cause a change in action will also include dissemination of the findings through outreach geared toward conservation practitioners.

Progress 01/17/20 to 12/21/20

Outputs
Target Audience: Nothing Reported Changes/Problems:There was a delay in the start of the field data collection because 1) the MS student hired to work on this project changed their mind at the last minute and I couldn't find a replacement on time, and 2) issues related to Covid-19 made it a little bit difficult to plan the field research for summer 2020. The main challenge to fully achieving goal #1 was the inefficiency of the methods used to collect fecal samples. Only a handful of samples were collected, but hopefully, this would still provide a preliminary understanding of the impacts of the seed-dispersing animals. The main change to the project was the integration of microbial ecology into the study of seed dispersal. This does not affect the goals, but adds an important layer to understand the potential influence of microbial community on the germination of seeds, making the project transcends disciplines. The PI has accepted a position at another university and will be leaving SDSU at the end of 2020. Therefore this project will be terminated. What opportunities for training and professional development has the project provided?This project provided an opportunity for an undergraduate student in Ecology and Environmental Sciences (Sadie R. Tornberg) to receive formal training in conducting field research and lab work. It has also fostered a collaboration to integrate microbial ecology into the project. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Goal 1: Assess whether seed-dispersing animals provide adaptive advantages for plants to cope with local environmental changes (50% Accomplished) We have been conducting fieldwork at Oak Lake Field Station since June 2020 to develop the baseline information for this goal. Specifically, we have accomplished the following: 1) Identified and mapped the tree/shrubs species that are potentially dispersed by animals at OLFS: hackberry (Celtis occidentalis), hawthorn (Crataegus spp.), bur oak (Quercus macrocarpa), red-osier dogwood (Cornus sericea), wild plum (Prunus americana), nannyberry (Viburnum lentago), juniper (Juniperus spp.), Missouri gooseberry (Ribes missouriense), serviceberry (Amelanchier sp) and honeysuckles (Lonicera spp.), for a total of 212 trees/shrubs tagged; 2) Monitored the fruiting phenology of these species; 3) Measured the functional traits of the fruits/seeds of these species; 4) Identified potential seed dispersers of these plant species by monitoring the animal visitors consuming fruits on plants bearing fruits, using camera traps and conducting direct observations. We found the following animals consuming the fruits of some of these species: white-tailed deer (Odocoileus virgianus), blue jay (Cyanocitta cristata), American robin (Turdus migratorius), gray catbird (Dumetella carolinensis), brown thrasher (Toxostoma rufum), Cedar waxing (Bombycilia cedrorum); 5). Conducted an environment-controlled experiment to determine seed germination and seedling survival of animal-defecated seeds. Goal Two: Examine how plant species that rely on specific/restricted seed disperser communities persist in the face of seed disperser loss (0% Accomplished) Not started yet Goal Three: Investigate the impacts of losing animal seed dispersers on ecosystem health (0% Accomplished) Not started yet

Publications