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Effect of climate and land use on niche utilization and distribution of nettle-feeding  butterflies
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0003-0312-4343
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Anthropogenic changes in climate and land use are causing a dramatic erosion of biodiversity. To understand this erosion, and predict future transformations of biodiversity, we need to understand better species’ response to these changes at different spatial and temporal scales. Modeling studies have identified correlations between physical parameters of the environment and species’ distribution at large spatial scales. However, this does not accurately characterize the response of a specific species, since this does not account for the constraints arising from the biology of the species. This thesis shall combine knowledge on the biology of species obtained from laboratory experiments with modeling studies. This will allow us (i) to identify life history traits and biotic interactions that influence species’ adaptive potential, and hence, explain possible differences in species’ distribution, and (ii) to consider, not only the ecological but also the evolutionary aspects of species’ response to changes. This integrative approach is likely to improve our predictions on species’ population dynamic in a changing environment.

I focus on a community of butterflies in Sweden (Vanessa cardui, Polygonia c-album, Aglais urticae, Aglais io, Araschnia levana) that feeds on the stinging nettle (Urtica dioica). The available knowledge on the biology of these species and their short life cycles, which allow investigations of their response to changes on a short-time scale, make them a good system to study. Among three of these species, I showed great differences in organisms’ response to variation in food nutrient content. This is a potentially important finding considering the increased use of chemical fertilizers. These differences are to a large extent explained by differences among species in their degree of host plant specialization and voltinism (paper II). Thus, life history traits determine the response of species to environmental changes, but are themselves likely to evolve in response to such changes. Climate change, for instance, may alter the phenological synchrony between plant-feeding insects and their host plants, making it necessary for the insects to evolve their host plant range in order to ensure the availability of resources during larval development (paper I & III). The biology of a species, including biotic interactions, helps to explain the observed shift in a species’ distribution and environmental niche that result from climate change. I have shown that the recent establishment of A. levana in southern Sweden has modified the niche of the resident species, A. urticae and A. io (Paper IV). Niche partitioning in this community is likely mediated by parasite-driven apparent competition.

Abstract [sv]

Mänsklig påverkan på klimat och markanvändning har orsakat en dramatisk förlust av biologisk mångfald. Effekten av dessa förändringar på lokal och regional nivå är dock komplex, och kräver integrativa strategier för att kunna förstå och förutsäga förändringar, på individ-, art- och samhällsnivå. Experimentella studier har utforskat arters plastiska och evolutionära respons till främst abiotiska förändringar, och observationsdata har använts för att modellera skiften i fenologi och utbredning som en konsekvens av klimatförändringar. Trots detta är det fortfarande mycket kvar att förstå för att kunna förutsäga hur miljöförändringar ska påverka arters respons på olika rumsliga och tidsliga skalor. Denna avhandling undersöker i vilken utsträckning arters specifika livshistoria och artinteraktioner kan förklara deras ekologiska och evolutionära respons på miljöförändringar.

För att angripa detta har jag fokuserat på ett samhälle av fjärilar i Sverige (Vanessa cardui, Polygonia c-album, Aglais urticae, Aglais io, Araschnia levana) som alla lever på brännässla (Urtica dioica). Den tillgängliga kunskapen om dessa arters biologi samt deras korta livscykler gör det möjligt att undersöka deras svar på förändringar över korta tidsskalor, vilket gör dem till ett lämpligt studiesystem. Huvudslutsatsen från denna avhandling är att för att beskriva hur en art svarar på en förändring måste man ta hänsyn till variation i livshistorieegenskaper och artinteraktioner. Till exempel har den ökade användningen av kemiska gödningsmedel förändrat näringstillgången även i naturliga ekosystem, vilket gynnar växtarter som är kapabla att växa under höga näringsnivåer, som brännässla. Variation i växternas näringsinnehåll kommer i sin tur att påverka herbivorerna som äter av dem, och artikel II visar att skillnader mellan fjärilsarter i hur de svarar på variation i näringstillgång till stor del beror på specialiseringsgrad och voltinism (antal generationer per år). Livshistorieegenskaper avgör således hur arter kommer att svara på förändringar i klimat och markanvändning, men sådana miljöförändringar påverkar i sin tur också evolution av livshistorieegenskaperna (artikel I & III). Slutligen, förändringar i utbredning som ett resultat av klimatförändring kommer även att påverka den lokala sammansättningen av interagerande arter (resurser, predatorer, konkurrenter). Ett exempel på detta är hur den relativt nyliga koloniseringen av södra Sverige av A. levana har förändrat nischerna hos de inhemska arterna A. urticae och A. io (artikel IV).

Abstract [fr]

Le réchauffement climatique et les changements d’occupation des terres d'origine anthropique provoquent une forte érosion de la biodiversité. Pour comprendre cette érosion, et prédire les transformations futures de la biodiversité, il nous faut mieux connaitre la réponse des espèces à ces changements, aux différentes échelles spatiales et temporelles. Grâce à des outils de modélisation statistique, des corrélations entre les paramètres physiques de l’environnement et la distribution des espèces à grande échelle spatiale ont été observées. Mais ceci ne suffit pas à caractériser finement la réponse d’une espèce donnée, car celle-ci dépend des caractéristiques biologiques propres de l’espèce. Cette thèse se propose donc d’associer les connaissances sur la biologie des espèces obtenues par des expériences en laboratoire à des études de modélisation. Ceci permettra (i) d’identifier des traits d’histoire de vie et les relations biotiques qui influencent le potentiel adaptatif des espèces, et donc expliquent d’éventuelles différences de répartition, et (ii) d’envisager, au-delà des aspects écologiques, la composante évolutive de cette réponse. Une telle approche intégrative est susceptible d’améliorer nos prédictions sur la dynamique des espèces dans un environnement changeant.

Le système d’étude de cette thèse est une communauté de papillons en Suède (Vanessa cardui, Polygonia c-album, Aglais urticae, Aglais io, Araschnia levana), se nourrissant de l'ortie (Urtica dioica). La biologie de ces espèces est bien connue et leur cycle de vie rapide permet d’étudier leur réponse aux changements à une échelle de temps court. Chez trois de ces espèces, j’ai mis en évidence des réponses très différentes à une augmentation de la teneur en nutriments de leur nourriture, conséquence attendue de l’utilisation accrue d’engrais chimiques. Ces différences sont dans une large mesure expliquée par la gamme de plantes hôtes utilisées et le voltinisme (article II). Ces traits d'histoire de vie déterminent donc la réponse des espèces aux changements, mais sont eux-mêmes susceptibles d’évoluer. Par exemple, le réchauffement climatique modifie la synchronie entre les insectes herbivores et leurs plantes hôtes et pousse à l’évolution du régime alimentaire des papillons afin que la présence de ressources soit assurée durant le développement des larves (articles I & III). Les connaissances sur la biologie des espèces, y compris leurs interactions biotiques, permettent de comprendre les variations de leur distribution spatiale et de leur niche environnementale. Ainsi, l’établissement récent d’A. levana dans le sud de la Suède, suite au réchauffement, a modifié les niches des espèces résidentes, A. urticae et A. io (article IV).

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2015. , 39 p.
National Category
Zoology
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-119719ISBN: 978-91-7649-202-4 (print)OAI: oai:DiVA.org:su-119719DiVA: diva2:848156
Public defence
2015-10-02, De Geersalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 10:00 (English)
Opponent
Supervisors
Projects
Ekoklim
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: Manuscript. Paper 4: Manuscript.

Available from: 2015-09-10 Created: 2015-08-23 Last updated: 2017-03-16Bibliographically approved
List of papers
1. Why stay in a bad relationship? The effect of local host phenology on a generalist butterfly feeding on a low-ranked host
Open this publication in new window or tab >>Why stay in a bad relationship? The effect of local host phenology on a generalist butterfly feeding on a low-ranked host
2016 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 16, 144Article in journal (Refereed) Published
Abstract [en]

Background: In plant-feeding insects, the evolutionary retention of polyphagy remains puzzling. A better understanding of the relationship between these organisms and changes in the metabolome of their host plants is likely to suggest functional links between them, and may provide insights into how polyphagy is maintained. Results: We investigated the phenological change of Cynoglossum officinale, and how a generalist butterfly species, Vanessa cardui, responded to this change. We used untargeted metabolite profiling to map plant seasonal changes in both primary and secondary metabolites. We compared these data to differences in larval performance on vegetative plants early and late in the season. We also performed two oviposition preference experiments to test females' ability to choose between plant developmental stages (vegetative and reproductive) early and late in the season. We found clear seasonal changes in plant primary and secondary metabolites that correlated with larval performance. The seasonal change in plant metabolome reflected changes in both nutrition and toxicity and resulted in zero survival in the late period. However, large differences among families in larval ability to feed on C. officinale suggest that there is genetic variation for performance on this host. Moreover, females accepted all plants for oviposition, and were not able to discriminate between plant developmental stages, in spite of the observed overall differences in metabolite profile potentially associated with differences in suitability as larval food. Conclusions: In V. cardui, migratory behavior, and thus larval feeding times, are not synchronized with plant phenology at the reproductive site. This lack of synchronization, coupled with the observed lack of discriminatory oviposition, obviously has potential fitness costs. However, this opportunistic behavior may as well function as a source of potential host plant evolution, promoting for example the acceptance of new plants.

Keyword
Adaptation, GC-MS, Host plant range, Larval performance, LC-MS, Metabolomics, Oviposition preference, Plasticity, Primary and secondary metabolites, Vanessa cardui
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-132390 (URN)10.1186/s12862-016-0709-x (DOI)000378675500004 ()27356867 (PubMedID)
Available from: 2016-08-15 Created: 2016-08-11 Last updated: 2017-11-28Bibliographically approved
2. Plant Fertilization Interacts with Life History: Variation in Stoichiometry and Performance in Nettle-Feeding Butterflies
Open this publication in new window or tab >>Plant Fertilization Interacts with Life History: Variation in Stoichiometry and Performance in Nettle-Feeding Butterflies
2015 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 5, e0124616Article in journal (Refereed) Published
Abstract [en]

Variation in food stoichiometry affects individual performance and population dynamics, but it is also likely that species with different life histories should differ in their sensitivity to food stoichiometry. To address this question, we investigated the ability of the three nettle-feeding butterflies (Aglais urticae, Polygonia c-album, and Aglais io) to respond adaptively to induced variation in plant stoichiometry in terms of larval performance. We hypothesized that variation in larval performance between plant fertilization treatments should be functionally linked to species differences in host plant specificity. We found species-specific differences in larval performance between plant fertilization treatments that could not be explained by nutrient limitation. We showed a clear evidence of a positive correlation between food stoichiometry and development time to pupal stage and pupal mass in Aglais urticae. The other two species showed a more complex response. Our results partly supported our prediction that host plant specificity affects larval sensitivity to food stoichiometry. However, we suggest that most of the differences observed may instead be explained by differences in voltinism (number of generations per year). We believe that the potential of some species to respond adaptively to variation in plant nutrient content needs further attention in the face of increased eutrophication due to nutrient leakage from human activities.

National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-118276 (URN)10.1371/journal.pone.0124616 (DOI)000353887100050 ()
Available from: 2015-06-22 Created: 2015-06-15 Last updated: 2017-12-04Bibliographically approved
3. Implications of a temperature increase for host plant range: predictions for a butterfly
Open this publication in new window or tab >>Implications of a temperature increase for host plant range: predictions for a butterfly
2013 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 3, no 9, 3021-3029 p.Article in journal (Refereed) Published
Abstract [en]

Although changes in phenology and species associations are relatively well-documented responses to global warming, the potential interactions between these phenomena are less well understood. In this study, we investigate the interactions between temperature, phenology (in terms of seasonal timing of larval growth) and host plant use in the polyphagous butterfly Polygonia c-album. We found that the hierarchy of larval performance on three natural host plants was not modified by a temperature increase as such. However, larval performance on each host plant and temperature treatment was affected by rearing season. Even though larvae performed better at the higher temperature regardless of the time of the rearing, relative differences between host plants changed with the season. For larvae reared late in the season, performance was always better on the herbaceous plant than on the woody plants. In this species, it is likely that a prolonged warming will lead to a shift from univoltinism to bivoltinism. The demonstrated interaction between host plant suitability and season means that such a shift is likely to lead to a shift in selective regime, favoring specialization on the herbaceous host. Based on our result, we suggest that host range evolution in response to temperature increase would in this species be highly contingent on whether the population undergoes a predicted shift from one to two generations. We discuss the effect of global warming on species associations and the outcome of asynchrony in rates of phenological change.

Keyword
host plant range, insect-plant interactions, seasonality, specialization, voltinism shift
National Category
Ecology Environmental Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-94737 (URN)10.1002/ece3.696 (DOI)000324046400020 ()
Note

AuthorCount:3;

Available from: 2013-10-09 Created: 2013-10-09 Last updated: 2017-12-06Bibliographically approved
4. Species range expansion constrains the ecological niches of resident butterflies
Open this publication in new window or tab >>Species range expansion constrains the ecological niches of resident butterflies
Show others...
2017 (English)In: Journal of Biogeography, ISSN 0305-0270, E-ISSN 1365-2699, Vol. 44, no 1, 28-38 p.Article in journal (Refereed) Published
Abstract [en]

Aim: Changes in community composition resulting from environmental changes modify biotic interactions and affect the distribution and density of local populations. Such changes are currently occurring in nettle-feeding butterflies in Sweden where Araschnia levana has recently expanded its range northward and is now likely to interact with resident species (Aglais urticae and Aglais io). Butterfly occurrence data collected over years and across regions enabled us to investigate how a recent range expansion of A. levana may have affected the environmental niche of resident species.

Location: We focused on two regions of Sweden (Skane and Norrstrom) where A. levana has and has not established and two time periods (2001-2006 and 2009-2012) during its establishment in Skane.

Methods: We performed two distinct analyses in each region using the PCA-env and the framework described in Broennimann etal. (2012). First, we described the main sources of variation in the environment. Second, in each time period and region, we characterized the realized niches of our focal species across topographic and land use gradients. Third, we quantified overlaps and differences in realized niches between and within species over time.

Results: In Skane, A. levana has stabilized its distribution over time, while the distribution of the native species has shifted. These shifts depicted a consistent pattern of avoiding overlap between the native species and the environmental space occupied by A. levana, and it was stronger for A. urticae than for A. io. In both regions, we also found evidence of niche partitioning between native species.

Main conclusions: Interspecific interactions are likely to affect local species distributions. It appears that the ongoing establishment of A. levana has modified local biotic interactions and induced shifts in resident species distributions. Among the mechanisms that can explain such patterns of niche partitioning, parasitoid-driven apparent competition may play an important role in this community.

Keyword
biotic interactions, citizen science, community composition, environmental niche model, indirect competition, nettle-feeding butterflies, ordination technique, parasitoid, realized niche
National Category
Biological Sciences Earth and Related Environmental Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-140397 (URN)10.1111/jbi.12787 (DOI)000391956900004 ()
Available from: 2017-03-16 Created: 2017-03-16 Last updated: 2017-11-29Bibliographically approved

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