The role of diet in vole population cycles

To upubliserte artikler har blitt fjernet fra den digitale versjonen, og kan leses i den trykte avhandlingen./Two unpublished articles have been removed from this digital version, and can be read in the printed thesis.Smågnagerpopulasjoner med store bestandssvingninger finner vi over hele verden. I denne avhandlingen har jeg inkludert en litteraturstudie om både regelmessige sykluser og mer uregelmessige utbrudd i smågnagerpopulasjoner og som peker på de viktigste problemstillingene å svare på for videre forståelse (Paper I). Smågnagere i boreale, alpine og arktiske økosystem er særlig kjent for sine sykliske populasjonsendringer, hvor både sesongvariasjon og/eller endringer i mattilgang er viktige faktorer. I et observasjonsstudium i de boreale skogene på Evenstad, fant vi en klar sammenheng mellom høyde over havet og hvor mye smågnagere det var i museårene. Smågnagerpopulasjonen hadde et syklisk forløp over hele høydegradienten, men syklusen var tydeligst høyt oppe i liene der det var mer mus i toppåret enn det var nede i dalene og bekreftet slik den viktige rollen vintersesongen spiller (Paper II). En tydelig tetthetsavhengighet om vinteren er forventet ved begrensede ressurser. En systematisk gjennomgang av litteraturen om forholdet mellom smågnagere og planter (Paper III) viste at begrenset mattilgang kan påvirke smågnagernes populasjonstetthet, og at det var best støtte for dette om vinteren. Det var derimot ikke mulig å hverken bekrefte eller avkrefte noen «plantehypothese» på grunn av for få studier med like respons- og forklaringsvariabler. Begge litteraturstudiene (Paper I og Paper III) poengterer viktigheten av at fremtidige studier utforsker videre om det forekommer systematiske endringer i dietten til smågnagerne som kan påvirke deres populasjonsdynamikk. Jeg har forsøkt å belyse nettopp dette ved å ta i bruk DNA-strekkoding (metabarcoding) for å analysere om diettens komposisjon eller diversitet endrer seg systematisk i forhold til sesong og syklusens faser (Paper V). DNA-strekkoding kan dog ikke forventes å reflektere relative proporsjoner av matinntaket nøyaktig (Paper IV). Diettstudien fant stor fleksibilitet i dietten, noe som støtter opp under at det forekommer moderate endringer mellom sesong og faser hos både klatremus Myodes glareolus og fjellmarkmus Microtus oeconomus. Men diettvariasjonen som kan tilskrives syklusenes faser var relativt marginal i forhold til den generelle fleksibiliteten i dietten. Det virker derfor ikke sannsynlig at fasenes diettvariasjon er tilstrekkelig for å drive smågnagerpopulasjonenes særegne dynamikk.Abstract: Small rodent populations throughout the world show massive density fluctuations. In this thesis, I have included a review highlighting the most critical issues essential for understanding the generality of small rodent population cycles and outbreaks (Paper I). Herbivorous voles in boreal, alpine, and arctic ecosystems are especially renowned for their multi-annual population cycles in which both seasonality and plant-herbivore interaction may play an important role. Using observational data from a boreal ecosystem, the importance of seasonality was confirmed in Paper II where winter length was positively associated with the amplitude of vole population cycles. Strong density dependence during winter is expected if resources are limited. Indeed, a systematic literature review focusing on plant-rodent interactions (Paper III) found the most robust evidence for food resource dependency during winter. However, the evidence was scattered across study systems to such a degree that only a few specific topics were addressed in a replicated manner. Thus, the hypothesis that interactions with plants cause rodent cycles could not be discarded. Because all hypotheses predicting that plants cause rodent cycles have explicit, yet largely untested, assumptions of diet shifts across population cycles, both review papers (Paper I, Paper III) conclude that one of the essential issues to explore further is whether a diet shift occurs that change population dynamics. I pursued this research question with DNA metabarcoding to quantify diets of two functionally important boreal vole species (Paper V). However, care should be taken when inferring the diet composition obtained by DNA metabarcoding of vole faeces as a direct mirror of the consumed food’s composition (Paper IV). Paper V is the first metabarcoding study to assess whether vole diet composition and diversity change systematically according to season and critical phases of a population cycle. We observed large diet flexibility and tendencies for moderate shifts in the proportions of plant taxa in the diets of bank voles Myodes glareolus and tundra voles Microtus oeconomus both between phases and seasons. Thus, changes do occur through time in vole diet composition, although the temporal change at population level appeared to be minor compared to other sources of diet variation. Overall, this study indicates that the variation in diet that could be attributed to cyclic phases is marginal relative to the overall diet flexibility. Hence, it seems unlikely that temporal variation in diets is driving the transition between increase/peak and crash/low phase of the population cycle.publishedVersio

Comparison of methods for revegetation of vehicle tracks in High Arctic tundra on Svalbard.

Natural regeneration after anthropogenic disturbance is slow in the tundra biome, but assisted regeneration can help speed up the process. A tracked off-road vehicle damaged a High Arctic dwarf shrub heath in Svalbard in May 2009, drastically reducing vegetation cover, soil seed bank and incoming seed rain. We assisted regeneration the following year using six different revegetation treatments, and monitored their effects one month-, and one- and eight years after their application. By 2018, all treatments still had a lower vegetation cover and limited species composition than the undamaged reference vegetation. The fertiliser treatment was the most effective in restoring vegetation cover (71 % vegetation cover, of which 62 % were bryophytes and 38 % vascular plant species). Compared to the reference plots (98 % vegetation cover, of which 32 % were bryophytes and 66 % were vascular plant species), the composition of the disturbed vegetation was still far from regenerated to its original state nine years after the tracks were made. The slow regrowth demonstrated in this study underlines the importance of avoiding disturbance of fragile tundra, and of implementing and upholding regulations restricting or banning such disturbance.publishedVersio

Seasonality shapes the amplitude of vole population dynamics rather than generalist predators

publishedVersio

Issues of under-representation in quantitative DNA metabarcoding weaken the inference about diet of the tundra vole Microtus oeconomus

During the last decade, methods based on high-throughput sequencing such as DNA metabarcoding have opened up for a range of new questions in animal dietary studies. One of the major advantages of dietary metabarcoding resides in the potential to infer a quantitative relationship between sequence read proportions and biomass of ingested food. However, this relationship’s robustness is highly dependent on the system under study, calling for case-specific assessments. Herbivorous small rodents often play important roles in the ecosystem, and the use of DNA metabarcoding for analyses of rodent diets is increasing. However, there has been no direct validation of the quantitative reliability of DNA metabarcoding for small rodents. Therefore, we used an experimental approach to assess the relationship between input plant biomass and sequence reads proportions from DNA metabarcoding in the tundra vole Microtus oeconomus. We found a weakly positive relationship between the number of high-throughput DNA sequences and the expected biomass proportions of food plants. The weak relationship was possibly caused by a systematic under-amplification of one of the three plant taxa fed. Generally, our results add to the growing evidence that case-specific validation studies are required to reliably make use of sequence read abundance as a proxy of relative food proportions in the diet

Climate variability indices for ecological and crop models in R: the climatrends package.

Abiotic factors play an important role in most ecological and crop systems that depend on certain levels of temperature, light and precipitation to initiate important physiological events (Schulze et al., 2019). Understanding how these factors drive the physiological processes is a key approach to provide recommendations for adaptation and biodiversity conservation in applied ecology studies. The package climatrends aims to provide the methods in R (R Core Team, 2020) to compute precipitation and temperature indices that serve as input for climate and crop models (Kehel et al., 2016; van Etten et al., 2019), trends in climate change (Aguilar et al., 2005; de Sousa et al., 2018) and applied ecology (Liu & El-Kassaby, 2018; Prentice et al., 1992

Small rodent monitoring at Birkebeiner road, Norway

Background. Northern small mammal populations are renowned for their multi-annual population cycles. Population cycles are multi-faceted and have extensive impacts on the rest of the ecosystem. In 2011, we started a student-based research activity to monitor the variation of small rodent density along an elevation gradient following the Birkebeiner Road, in southeast Norway. Fieldwork was conducted by staff and students at the University campus Evenstad, Inland Norway University of Applied Sciences, which has a long history of researching cyclic population dynamics. The faculty has a strong focus on engaging students in all parts of the research activities, including data collection. Small rodents were monitored using a set of snap trap stations. Trapped animals were measured (e.g. body mass, body length, sex) and dissected to assess their reproductive status. We also characterised the vegetation at trapping sites. New information. We provide a dataset of small rodent observations that show fluctuating population dynamics across an elevation gradient (300 m to 1,100 m a.s.l) and in contrasting habitats. This dataset encompasses three peaks of the typical 3-4-year vole population cycles; the number of small rodents and shrews captured show synchrony and peaked in years 2014, 2017 and 2021. The bank vole Myodes glareolus was by far (87%) the most common species trapped, but also other species were observed (including shrews). We provide digital data collection forms and highlight the importance of long-term data collection.publishedVersio

Population cycles and outbreaks of small rodents : ten essential questions we still need to solve

Correction: 10.1007/s00442-021-04856-4, Oecologia (2021)Most small rodent populations in the world have fascinating population dynamics. In the northern hemisphere, voles and lemmings tend to show population cycles with regular fluctuations in numbers. In the southern hemisphere, small rodents tend to have large amplitude outbreaks with less regular intervals. In the light of vast research and debate over almost a century, we here discuss the driving forces of these different rodent population dynamics. We highlight ten questions directly related to the various characteristics of relevant populations and ecosystems that still need to be answered. This overview is not intended as a complete list of questions but rather focuses on the most important issues that are essential for understanding the generality of small rodent population dynamics.Peer reviewe

The role of diet in vole population cycles

Smågnagerpopulasjoner med store bestandssvingninger finner vi over hele verden. I denne avhandlingen har jeg inkludert en litteraturstudie om både regelmessige sykluser og mer uregelmessige utbrudd i smågnagerpopulasjoner og som peker på de viktigste problemstillingene å svare på for videre forståelse (Paper I). Smågnagere i boreale, alpine og arktiske økosystem er særlig kjent for sine sykliske populasjonsendringer, hvor både sesongvariasjon og/eller endringer i mattilgang er viktige faktorer. I et observasjonsstudium i de boreale skogene på Evenstad, fant vi en klar sammenheng mellom høyde over havet og hvor mye smågnagere det var i museårene. Smågnagerpopulasjonen hadde et syklisk forløp over hele høydegradienten, men syklusen var tydeligst høyt oppe i liene der det var mer mus i toppåret enn det var nede i dalene og bekreftet slik den viktige rollen vintersesongen spiller (Paper II). En tydelig tetthetsavhengighet om vinteren er forventet ved begrensede ressurser. En systematisk gjennomgang av litteraturen om forholdet mellom smågnagere og planter (Paper III) viste at begrenset mattilgang kan påvirke smågnagernes populasjonstetthet, og at det var best støtte for dette om vinteren. Det var derimot ikke mulig å hverken bekrefte eller avkrefte noen «plantehypothese» på grunn av for få studier med like respons- og forklaringsvariabler. Begge litteraturstudiene (Paper I og Paper III) poengterer viktigheten av at fremtidige studier utforsker videre om det forekommer systematiske endringer i dietten til smågnagerne som kan påvirke deres populasjonsdynamikk. Jeg har forsøkt å belyse nettopp dette ved å ta i bruk DNA-strekkoding (metabarcoding) for å analysere om diettens komposisjon eller diversitet endrer seg systematisk i forhold til sesong og syklusens faser (Paper V). DNA-strekkoding kan dog ikke forventes å reflektere relative proporsjoner av matinntaket nøyaktig (Paper IV). Diettstudien fant stor fleksibilitet i dietten, noe som støtter opp under at det forekommer moderate endringer mellom sesong og faser hos både klatremus Myodes glareolus og fjellmarkmus Microtus oeconomus. Men diettvariasjonen som kan tilskrives syklusenes faser var relativt marginal i forhold til den generelle fleksibiliteten i dietten. Det virker derfor ikke sannsynlig at fasenes diettvariasjon er tilstrekkelig for å drive smågnagerpopulasjonenes særegne dynamikk

Comparison of methods for revegetation of vehicle tracks in High Arctic tundra on Svalbard.

Natural regeneration after anthropogenic disturbance is slow in the tundra biome, but assisted regeneration can help speed up the process. A tracked off-road vehicle damaged a High Arctic dwarf shrub heath in Svalbard in May 2009, drastically reducing vegetation cover, soil seed bank and incoming seed rain. We assisted regeneration the following year using six different revegetation treatments, and monitored their effects one month-, and one- and eight years after their application. By 2018, all treatments still had a lower vegetation cover and limited species composition than the undamaged reference vegetation. The fertiliser treatment was the most effective in restoring vegetation cover (71 % vegetation cover, of which 62 % were bryophytes and 38 % vascular plant species). Compared to the reference plots (98 % vegetation cover, of which 32 % were bryophytes and 66 % were vascular plant species), the composition of the disturbed vegetation was still far from regenerated to its original state nine years after the tracks were made. The slow regrowth demonstrated in this study underlines the importance of avoiding disturbance of fragile tundra, and of implementing and upholding regulations restricting or banning such disturbance

Small rodent population cycles and plants – after 70 years, where do we go?

Small rodent population cycles characterise northern ecosystems, and the cause of these cycles has been a long-lasting central topic in ecology, with trophic interactions currently considered the most plausible cause. While some researchers have rejected plant–herbivore interactions as a cause of rodent cycles, others have continued to research their potential roles. Here, we present an overview of whether plants can cause rodent population cycles, dividing this idea into four different hypotheses with different pathways of plant impacts and related assumptions. Our systematic review of the existing literature identified 238 studies from 150 publications. This evidence base covered studies from the temperate biome to the tundra, but the studies were scattered across study systems and only a few specific topics were addressed in a replicated manner. Quantitative effects of rodents on vegetation was the best studied topic, and our evidence base suggests such that such effects may be most pronounced in winter. However, the regrowth of vegetation appears to take place too rapidly to maintain low rodent population densities over several years. The lack of studies prevented assessment of time lags in the qualitative responses of vegetation to rodent herbivory. We conclude that the literature is currently insufficient to discard with confidence any of the four potential hypotheses for plant–rodent cycles discussed herein. While new methods allow analyses of plant quality across more herbivore-relevant spatial scales than previously possible, we argue that the best way forward to rejecting any of the rodent–plant hypotheses is testing specific predictions of dietary variation. Indeed, all identified hypotheses make explicit assumptions on how rodent diet taxonomic composition and quality will change across the cycle. Passing this bottleneck could help pinpoint where, when, and how plant–herbivore interactions have – or do not have – plausible effects on rodent population dynamics