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Effects of climate on phenological synchrony between butterflies and their host plants
Stockholm University, Faculty of Science, Department of Zoology. (Ecology)ORCID iD: 0000-0002-7262-6091
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Shifts in species’ phenologies and phenological asynchronies between the interacting organisms have received a lot of attention in the context of climate change. Changes in temporal overlap between species, caused by phenological asynchrony, make species depending on one another become so separated in time that they can no longer interact. This may have important consequences both for single species, like fluctuations in abundances, and for the functioning of whole communities by creating mismatches between trophic levels and rearrangements of community structure. This thesis focuses on the impact of temperatures on spring timing and phenological synchrony in a herbivorous insect – host plant system, consisting of the orange tipbutterfly Anthocharis cardamines and five of its Brassicaceae host plant species. Paper I demonstrates that diapause duration and winter thermal conditions can determine the timing of spring emergence in the herbivore, and these traits may differ between species with different feeding strategies. In paper II we show that thermal reaction norms of post-winterdevelopment of A. cardamines display cogradient latitudinal variation.Paper III shows that temperature-mediated phenological plasticity of A. cardamines butterflies and a majority of the most used host plant species is similar within populations originating from different latitudes. Thus, the species’ timing appeared well conserved in response to thermal variation. In paper IV we explored the importance of the butterfly’s adult emergence and thermal conditions on the succeeding part of the butterfly’s life-cycle – larval development. The outcome from the interaction was examined for both the insect and the plant side. The degree in phenological overlap between the female butterflies and host plants as well as temperatures during larval development were found to influence larval development but had no effect on plant reproductive fitness. The four papers of the presented thesis demonstrate that developmental preadaptations, evolvedin a herbivore to maintain phenological synchrony with host plants across yearly variation of spring conditions, can prevent disruption of the interaction under a wide range of temperatures. This indicates that temporary constrained interactions are not always vulnerable to decoupling, particularly if they involve generalist strategy.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2015. , 16 p.
Keyword [en]
Phenology, phenological synchrony, Anthocharis cardamines, Pieris napi, latitudinal variation
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-116664ISBN: 978-91-7649-162-1 (print)OAI: oai:DiVA.org:su-116664DiVA: diva2:807135
Public defence
2015-06-04, Magnélisalen, Kemiska övningslaboratoriet, Svante Arrhenius väg 16 B, Stockholm, 09:30 (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 3: Manuscript. Paper 4: Submitted.

Available from: 2015-05-12 Created: 2015-04-22 Last updated: 2015-06-23Bibliographically approved
List of papers
1. Latitudinal variation in diapause duration and post-winter development in two pierid butterflies in relation to phenological specialization
Open this publication in new window or tab >>Latitudinal variation in diapause duration and post-winter development in two pierid butterflies in relation to phenological specialization
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2015 (English)In: Oecologia, ISSN 0029-8549, E-ISSN 1432-1939, Vol. 177, no 1, 181-190 p.Article in journal (Refereed) Published
Abstract [en]

Diapause plays a central role in insect life cycles by allowing survival during adverse seasonal conditions as well as synchronizing life cycles with the period of mate and food availability. Seasonal timing is expected to be particularly important for species that are dependent on resources available during a short time window-so-called phenological specialists-and latitudinal clines in seasonality are expected to favor local adaptation in phenological timing. However, to what degree latitudinal variation in diapause dynamics and post-winter development due to such local adaptation is influenced by the degree of phenological specialization is not well known. We experimentally studied two pierid butterfly species and found that the phenological specialist Anthocharis cardamines had shorter diapause duration than the phenological generalist Pieris napi along a latitudinal gradient in Sweden. Moreover, diapause duration increased with latitude in P. napi but not in A. cardamines. Sensitivity of the two species to winter thermal conditions also differed; additional cold temperature during the winter period shortened diapause duration for P. napi pupae but not for A. cardamines pupae. In both species, post-winter pupal development was faster after longer periods of cold conditions, and more southern populations developed faster than northern populations. Post-winter development was also invariably faster at higher temperatures in both species. We argue that the observed differences in diapause dynamics between the two species might be explained by the difference in phenological specialization that influences the costs of breaking diapause too early in the season.

Keyword
Anthocharis cardamines, Pieris napi, Local adaptation, Voltinism, Development
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-113960 (URN)10.1007/s00442-014-3125-1 (DOI)000347406500017 ()
Note

AuthorCount:5;

Available from: 2015-02-20 Created: 2015-02-16 Last updated: 2017-12-04Bibliographically approved
2. Latitudinal variation in thermal reaction norms of post-winter pupal development in two butterflies differing in phenological specialization
Open this publication in new window or tab >>Latitudinal variation in thermal reaction norms of post-winter pupal development in two butterflies differing in phenological specialization
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2014 (English)In: Biological Journal of the Linnean Society, ISSN 0024-4066, E-ISSN 1095-8312, Vol. 113, no 4, 981-991 p.Article in journal (Refereed) Published
Abstract [en]

Latitudinal clines in thermal reaction norms of development are a common phenomenon in temperate insects. Populations from higher latitudes often develop faster throughout the range of relevant temperatures (i.e countergradient variation) because they must be able to complete their life cycle within a shorter seasonal time window compared to populations at lower latitudes. In the present study, we experimentally demonstrate that two species of butterflies Anthocharis cardamines (L.) and Pieris napi (L.) instead show a cogradient variation in thermal reaction norms of post-winter pupal development so that lower latitude populations develop faster than higher latitude populations. The two species share host plants but differ in the degree of phenological specialization, as well as in the patterns of voltinism. We suggest that the pattern in A. cardamines, a univoltine phenological specialist feeding exclusively on flowers and seedpods, is the result of selection for matching to the phenological pattern of its local host plants. The other species, P. napi, is a phenological generalist feeding on the leaves of the hosts and it shows a latitudinal cline in voltinism. Because the latitudinal pattern in P. napi was an effect of slow development in a fraction of the pupae from the most northern population, we hypothesize that this population may include both bivoltine and univoltine genotypes. Consequently, although the two species both showed cogradient patterns in thermal reaction norms, it appears likely that this was for different reasons.

Keyword
:Anthocharis cardamines, cogradient, degree days, local adaptation, Pieris napi
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-116657 (URN)10.1111/bij.12371 (DOI)000345319000007 ()
Available from: 2015-04-22 Created: 2015-04-22 Last updated: 2017-12-04Bibliographically approved
3. Weak effect of spring temperatures on phenological synchrony between herbivore emergence and host plant suitability
Open this publication in new window or tab >>Weak effect of spring temperatures on phenological synchrony between herbivore emergence and host plant suitability
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Many species interactions are maintained by precise timing of life-cycle events across seasonal variation. Ecological implications of changes in phenologies, associated with climate change, with respect to species interactions are to a large extent unexplored. Changes in phenological distance between herbivores and their host plant species under new environmental conditions may potentially lead to shifts in host use patterns, with some plant species becoming more or less available at the time of a herbivore’s emergence. In addition, latitudinal variation in the timing of phenological events can lead to different patterns in host use shifts among populations of a given herbivore. Here we explored latitudinal variation in the effects of temperature on the degree of phenological synchrony between emergence of a butterfly, A. cardamines, and five of its herbaceous host plant species in a set of laboratory experiments to investigate the possibility that there will be shifts in the butterfly’ host utilization due to changes in thermal environment. The results suggest a similar temperature-mediated phenological plasticity between the butterflies and their host plants in three latitudinally divergent populations. In general, butterflies appeared to be well-synchronized with the majority of their host plant species across temperatures. In the most northern region, however, phenological distance between the butterfly and two out of four plant species was affected by temperature and decreased in warmer treatments. We relate this to a lower diversity of plant species and shorter period of host availability in the northern region. This creates a stronger selection pressure on the northern butterflies for a closer matching of their emergence to the plant flowering period. As the butterflies discriminated against non-flowering hosts with respect to oviposition, we conclude that a shift in host use in A. cardamines appears to be a possible scenario under spring warming, especially in the northern region.

Keyword
Anthocharis cardamines, climate change, herbivore – host plant, orange tip butterfly, oviposition preference, phenological synchrony
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-116660 (URN)
Available from: 2015-04-22 Created: 2015-04-22 Last updated: 2016-01-29Bibliographically approved
4. The developmental race between maturing host plants and their butterfly herbivore – the influence of phenological matching and temperature
Open this publication in new window or tab >>The developmental race between maturing host plants and their butterfly herbivore – the influence of phenological matching and temperature
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2015 (English)In: Journal of Animal Ecology, ISSN 0021-8790, E-ISSN 1365-2656, Vol. 84, no 6, 1690-1699 p.Article in journal (Refereed) Published
Abstract [en]

Interactions between herbivorous insects and their host plants that are limited in time are widespread. Therefore, many insect-plant interactions result in a developmental race, where herbivores need to complete their development before plants become unsuitable, while plants strive to minimize damage from herbivores by outgrowing them. When spring phenologies of interacting species change asymmetrically in response to climate warming, there will be a change in the developmental state of host plants at the time of insect herbivore emergence. In combination with altered temperatures during the subsequent developmental period, this is likely to affect interaction strength as well as fitness of interacting species. Here, we experimentally explore whether the combined effect of phenological matching and thermal conditions influence the outcome of an insect-host interaction. We manipulated both developmental stages of the host plants at the start of the interaction and temperature during the subsequent developmental period in a model system of a herbivorous butterfly, Anthocharis cardamines, and five of its Brassicaceae host plant species. Larval performance characteristics were favoured by earlier stages of host plants at oviposition as well as by higher developmental temperatures on most of the host species. The probability of a larva needing a second host plant covered the full range from no influence of either phenological matching or temperature to strong effects of both factors, and complex interactions between them. The probability of a plant outgrowing a larva was dependent only on the species identity. This study demonstrates that climatic variation can influence the outcome of consumer-resource interactions in multiple ways and that its effects differ among host plant species. Therefore, climate warming is likely to change the temporal match between larval and plant development in some plant species, but not in the others. This is likely to have important implications for host plant use and possibly influence competitive relationships.

Keyword
climate change, insect – plant interaction, orange tip butterfly, phenological matching, synchronization
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-116662 (URN)10.1111/1365-2656.12417 (DOI)000362741000024 ()
Available from: 2015-04-22 Created: 2015-04-22 Last updated: 2017-12-04Bibliographically approved

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