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Herbivores influence nutrient cycling and plant nutrient uptake: insights from tundra ecosystems
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. (Arcum)
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Reindeer appear to have strong positive effects on plant productivity and nutrient cycling in strongly nutrient-limited ecosystems. While the direct effects of grazing on vegetation composition have been intensively studied, much less is known about the indirect effect of grazing on plant-soil interactions. This thesis investigated the indirect effects of ungulate grazing on arctic plant communities via soil nutrient availability and plant nutrient uptake.

At high density, the deposition of dung alone increased plant productivity both in nutrient rich and nutrient poor tundra habitats without causing major changes in soil possesses. Plant community responses to dung addition was slow, with a delay of at least some years. By contrast, a 15N-urea tracer study revealed that nutrients from reindeer urine could be rapidly incorporated into arctic plant tissues. Soil and microbial N pools only sequestered small proportions of the tracer. This thesis therefore suggests a strong effect of dung and urine on plant productivity by directly providing nutrient-rich resources, rather than by stimulating soil microbial activities, N mineralization and ultimately increasing soil nutrient availability. Further, defoliation alone did not induce compensatory growth, but resulted in plants with higher nutrient contents. This grazing-induced increase in plant quality could drive the high N cycling in arctic secondary grasslands by providing litter of a better quality to the belowground system and thus increase organic matter decomposition and enhance soil nutrient availability. Finally, a 15N natural abundance study revealed that intense reindeer grazing influences how plants are taking up their nutrients and thus decreased plant N partitioning among coexisting plant species.

Taken together these results demonstrate the central role of dung and urine and grazing-induced changes in plant quality for plant productivity. Soil nutrient concentrations alone do not reveal nutrient availability for plants since reindeer have a strong influence on how plants are taking up their nutrients. This thesis highlights that both direct and indirect effects of reindeer grazing are strong determinants of tundra ecosystem functioning. Therefore, their complex influence on the aboveground and belowground linkages should be integrated in future work on tundra ecosystem N dynamic.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2016. , 36 p.
Keyword [en]
Reindeer grazing, large herbivores, nutrient cycling, plant nutrient uptake, soil nutrient availability, arctic plant ecology, soil microbial communities, 15N stable isotopes, plant-soil interactions, plant quality, dung and urine.
National Category
Ecology
Research subject
biology, Environmental Science; biology
Identifiers
URN: urn:nbn:se:umu:diva-120191ISBN: 978-91-7601-456-1 (print)OAI: oai:DiVA.org:umu-120191DiVA: diva2:927068
Public defence
2016-06-03, Lilla Hörsalen, KBC (KB3A9), Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2016-05-12 Created: 2016-05-10 Last updated: 2016-06-30Bibliographically approved
List of papers
1. Strong Responses of Subarctic Plant Communities to Long-Term Reindeer Feces Manipulation
Open this publication in new window or tab >>Strong Responses of Subarctic Plant Communities to Long-Term Reindeer Feces Manipulation
2015 (English)In: Ecosystems (New York. Print), ISSN 1432-9840, E-ISSN 1435-0629, Vol. 18, no 5, 740-751 p.Article in journal (Refereed) Published
Abstract [en]

Deposition of feces is a key mechanism by which herbivores influence soil nutrient cycling and plant production, but the knowledge about its importance for plant production and community structure is still rudimental since experimental evidence is scarce. We thus performed a 7-year long reindeer feces manipulation experiment in two tundra vegetation types with contrasting nutrient availability and analyzed effects on plant community composition and soil nutrient availability. Despite feces being fairly nutrient poor, feces manipulation had strong effect on both the nutrient-poor heath and the nutrient-rich meadow. The strongest effect was detected when feces were added at high density, with a substantial increase in total vascular plant productivity and graminoids in the two communities. Doubling natural deposition of reindeer feces enhanced primary production and the growth of deciduous shrubs in the heath. By contrast, removal of feces decreased only the production of graminoids and deciduous shrubs in the heath. Although the response to feces addition was faster in the nutrient-rich meadow, after 7 years it was more pronounced in the nutrient-poor heath. The effect of feces manipulation on soil nutrient availability was low and temporarily variable. Our study provides experimental evidence for a central role of herbivore feces in regulating primary production when herbivores are abundant enough. Deposition of feces alone does, however, not cause dramatic vegetation shifts; to drive unproductive heath to a productive grass dominated state, herbivore trampling, and grazing are probably also needed.

Place, publisher, year, edition, pages
Springer, 2015
Keyword
alpine meadow, feces fertilization, forage quality, plant-herbivore interactions, microbial mobilization, plant productivity, reindeer grazing, soil nutrient availability, tundra heath
National Category
Ecology Earth and Related Environmental Sciences
Identifiers
urn:nbn:se:umu:diva-106774 (URN)10.1007/s10021-015-9856-y (DOI)000358089100002 ()
Available from: 2015-08-14 Created: 2015-08-07 Last updated: 2017-12-04Bibliographically approved
2. Effect of herbivory on the fate of added 15N-urea in a grazed Arctic tundra
Open this publication in new window or tab >>Effect of herbivory on the fate of added 15N-urea in a grazed Arctic tundra
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Mammalian herbivores can strongly influence nitrogen cycling and herbivore urine could be an important component of the nutrient cycle in grazed ecosystems. Despite its potential role for ecosystem productivity and soil processes, the distribution of N from urine in the different ecosystem compartments is poorly understood. This study investigates the fate of 15N enriched urea applied above the plant canopy in two tundra sites either heavily or lightly grazed by reindeer for the last 50 years. We explored the fate of the 15N in the different ecosystem N pools at 2 weeks and 1 years following tracer addition. We hypothesized that cryptogams would take up most N under light grazing, but graminoids most N under heavy grazing. The 15N-urea was rapidly incorporated in cryptogams and aboveground parts of vascular plants, while the soil microbial pool and plant roots sequestered only a marginal proportion of the labelled N applied. Hence, urine addition supports a higher primary production in tundra since most of the nutrients released from urine could be assimilated by the aboveground components with little N reaching the belowground compartments. Mosses and lichens still constituted the largest sink of the 15N-urea 1 year after tracer addition at both levels of grazing intensity demonstrating their large ability to capture and retain N  from urine. Deciduous and evergreen shrubs were just as efficient as graminoids in taking up the 15N-urea. The total recovery of the labelled urea was lower in the heavily grazed sites, suggesting that reindeer reduce the N retention in the system. Rapid incorporation of the applied 15N-urea indicates that arctic plants can take advantage of a pulse of incoming N in the form of urea, which supports a higher primary production. However, whether urine also maintains a high production of forage plants depend on plant community composition, since most urea was recovered in non-forage plants for reindeer.

Keyword
Above-belowground linkages, Arctic tundra, Cryptogams, Microbial N biomass, Nutrient cycling, Plant-herbivore interactions, nutrient uptake, Grazing intensity, urine, 15N labelling
National Category
Ecology
Research subject
biology
Identifiers
urn:nbn:se:umu:diva-120177 (URN)
Available from: 2016-05-10 Created: 2016-05-10 Last updated: 2016-06-30
3. Defoliation, soil grazing legacy, dung and moss cover influence growth and nutrient uptake of the common grass species, Festuca ovina
Open this publication in new window or tab >>Defoliation, soil grazing legacy, dung and moss cover influence growth and nutrient uptake of the common grass species, Festuca ovina
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Herbivores can strongly influence plant growth directly through defoliation and the return of nutrients in the form of dung and urine but also indirectly by reducing the abundance of neighbouring plants and inducing changes in soil processes. The relative importance of these driving mechanisms of plant response to herbivory are still poorly understood. In a common garden experiment, we studied the aboveground and belowground responses of Festuca ovina, a grazing tolerant grass common in arctic secondary grassland, to defoliation, reindeer dung addition, changes in soil microclimate induced by the presence or the absence of a moss cover, and soil grazing legacy. Defoliation strongly reduced shoot and root growth and plant nutrient uptake. Plants did thus not compensate for the tissue lost due to defoliation, even at a higher nutrient availability. By contrast, defoliation enhanced plant N concentration and decreased plant C to N ratio. Soil from heavily grazed sites and dung addition increased plant production, plant N concentrations and nutrient uptake, although the effects of dung addition were only small. Mosses had a strong negative effect of root biomass and reduced plant compensatory growth after defoliation. Interestingly mosses also had facilitative effects on aboveground plant growth in absence of defoliation and on plant nutrient uptake and N concentrations. Although plants suffered severely from defoliation, they were also strongly favoured by the increased nutrient availability associated with herbivory. After two years, plants produced as much biomass when all positive and negative effects of herbivores were considered (defoliation, soil communities and nutrient availability under heavily grazing, dung addition and no moss cover) as in the ungrazed conditions (no defoliation, soil communities and nutrient availability under lightly grazing, no dung addition, a thick moss cover). This study indicates that graminoids can tolerate high densities of herbivores, although it suffer from defoliation directly, and suggests that changes in plant quality following defoliation and grazing-induced changes in soil processes are two key mechanisms through which herbivores can control plant productivity in arctic secondary grasslands. Plant tolerance to herbivory will depends on how herbivores utilise a pasture area and on the balance between the positive and the negative effects of grazing on plant growth.

Keyword
Arctic tundra, Compensatory growth, Defoliation, Mosses, Plant nutrient uptake, Plant performance, Plant tolerance to herbivory, Reindeer grazing, Soil nutrient availability
National Category
Ecology
Research subject
biology
Identifiers
urn:nbn:se:umu:diva-120189 (URN)
Available from: 2016-05-10 Created: 2016-05-10 Last updated: 2016-06-30
4. Grazing decreases N partitioning among coexisting plant species
Open this publication in new window or tab >>Grazing decreases N partitioning among coexisting plant species
2017 (English)In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 31, no 11, 2051-2060 p.Article in journal (Refereed) Published
Abstract [en]

1. Herbivores play a key role in shaping ecosystem structure and functions by influencing plant and microbial community composition and nutrient cycling.

2. This study investigated the long-term effects of herbivores on plant resource acquisition. We explored differences in the natural delta N-15 signatures in plant, microbial and soil N pools, and examined mycorrhizal colonization in two tundra sites that have been either lightly or heavily grazed by reindeer for more than 50 years. The study examined changes in nutrient acquisition in five common tundra plants with contrasting traits and mycorrhiza status; the mycorrhizal dwarf shrubs, Betula nana, Vaccinium myrtillus and Empetrum hermaphroditum; a mycorrhizal grass, Deschampsia flexuosa, and a non-mycorrhizal sedge, Carex bigelowii.

3. There were large variations in delta N-15 among coexisting plant species in the lightly grazed sites. This variation was dramatically reduced in the heavily grazed sites. At an individual species level, delta N-15 was higher in E. hermaphroditum and lower in C. bigelowii in the heavily grazed sites. Mycorrhizal colonization in B. nana and E. hermaphroditum roots were also lower in the heavily grazed sites. The delta N-15 signatures of the total soil N pool and of the microbial N pools were higher in the heavily grazed sites.

4. Since the strong delta N-15 differentiation among plant species has been interpreted as a result of plants with different mycorrhizal types using different sources of soil nitrogen, we suggest that the lower variation in delta N-15 in heavily grazed sites indicates a lower niche differentiation in nitrogen uptake among plants. Reduced mycorrhizamediated nitrogen uptake by some of the species, a shift towards a more mineral nutrition due to higher nutrient turnover, and uptake of labile nitrogen from dung and urine in the heavily grazed sites could all contribute to the changes in plant delta N-15.

5. We conclude that herbivores have the potential to influence plant nutrient uptake and provide the first data suggesting that herbivores decrease nutrient partitioning on the basis of chemical N forms among plant species. Reduced niche complementarity among species is potentially important for estimates of the effects of -herbivory on plant nutrient availability and species coexistence.

Keyword
above-below-ground linkages, Arctic tundra, microbial N biomass, mycorrhizal colonization, nutrient cycling, plant-herbivore interactions, plant nutrient uptake, ungulate grazing
National Category
Ecology
Research subject
biology
Identifiers
urn:nbn:se:umu:diva-120190 (URN)10.1111/1365-2435.12917 (DOI)000414248100003 ()
Note

Originally included in thesis in manuscript form.

Available from: 2016-05-10 Created: 2016-05-10 Last updated: 2017-12-06Bibliographically approved

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Barthelemy, Hélène

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