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Spatiotemporal Pattern of Phenology Across Geographic Gradients in Insects

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Spatiotemporal Pattern of Phenology Across Geographic Gradients in Insects Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2017 Spatiotemporal pattern of phenology across geographic gradients in insects Khelifa, Rassim Abstract: Phenology – the timing of recurrent biological events – influences nearly all aspects of ecology and evolution. Phenological shifts have been recorded in a wide range of animals and plants worldwide during the past few decades. Although the phenological responses differ between taxa, they may also vary geographically, especially along gradients such as latitude or elevation. Since changes in phenology have been shown to affect ecology, evolution, human health and the economy, understanding pheno- logical shifts has become a priority. Although phenological shifts have been associated with changes in temperature, there is still little comprehension of the phenology-temperature relationship, particularly the mechanisms influencing its strength and the extent to which it varies geographically. Such ques- tions would ideally be addressed by combining controlled laboratory experiments on thermal response with long-term observational datasets and historical temperature records. Here, I used odonates (drag- onflies and damselflies) and Sepsid scavenger flies to unravel how temperature affects development and phenology at different latitudes and elevations. The main purpose of this thesis is to provide essential knowledge on the factors driving the spatiotemporal phenological dynamics by (1) investigating how phenology changed in time and space across latitude and elevation in northcentral Europe during the past three decades, (2) assessing potential temporal changes in thermal sensitivity of phenology and (3) describing the geographic pattern and usefulness of thermal performance curves in predicting natural responses. Additionally, this thesis presents (4) a new behavior in odonates and (5) a commemoration of the 100th anniversary of a noteworthy book in odonatology. In Chapter I, the phenological shift of adult odonates across latitude and elevation was examined with long-term observation data of 54 species in six European countries, historical temperature records and experimental studies on species-specific thermal performance curves. Geographic variation in phenological shifts is expected since the magnitude of recent climate warming varies across both space (latitude and elevation) and time (seasons). However, little information exists on whether the average temperature, fluctuation of temperature or physiologi- cal response to such temperature fluctuations is the best predictor of phenology. First, phenology has shifted across both latitude and elevation, but to a different extent (magnitude), increasing with latitude and decreasing with elevation. Although average temperature explained some of the variation in spa- tiotemporal pattern of phenology, the physiological response (development) to temperature fluctuations provided better predictions. These results indicate that while researchers rely mostly on temperature data to explain phenological shifts, understanding the non-linear relationship between temperature and development would permit more robust predictions. Chapter II investigates the temporal changes in sensitivity of phenology to temperature (ST) using the same data as chapter one. Here, I tested the hypothesis that the phenology of species has become less sensitive to temperature over time, and that this pattern may vary geographically. There was an overall decline in ST between 1980 and 2013, but geographically this decline was observed along latitudinal but not elevational gradients. To explain this geographic pattern of ST, I tested three non-mutually exclusive hypotheses: (1) the position of the envi- ronmental temperature within the thermal performance curve determines the strength of the response of species to warming, (2) photoperiod has declined after phenological advancements and caused the decline in the thermal response of species, and (3) reduced chilling by winter warming has affected the response of species to spring temperature. I found the strongest support for hypotheses 2 (photoperiod limitation) and 3 (winter warming). These findings reveal that interactions between environmental cues may change the response of species to warming, thereby rendering long-term predictions very challenging. Chapter III focuses on the use of the thermal performance curve (TPC) for predicting larval development under laboratory and field conditions. Although the average temperature has been used extensively to assess the effect of warming, recent studies have highlighted the relevance of temperature fluctuations inshaping thermal responses. More importantly, there is missing knowledge on the usefulness of TPC in predicting development under natural conditions. I therefore combined laboratory and field experiments in five species of Sepsis flies (Diptera: Sepsidae), using distant populations from the temperate region (Europe, Africa and North America), to compare observed development data with theoretical estimates derived from TPC. The predictability of development under fluctuating temperature was better in the laboratory than in the field. Interestingly, accounting for temperatures that fall below a critical minimum improves the predictability of development such that flies not encountering cold conditions show predictable de- velopment times whereas flies encountering cold conditions tend to emerge earlier than expected. This study reveals the importance of cold temperatures in shaping thermal reaction norms, thus providing new insights to improve predictions of the responses of ectotherms to future climate change. Chapter IV provides the first description of sexual death feigning in a dragonfly species. Death feigning (playing dead) is a widespread behavior in animals, being recorded in mammals, birds, fish, reptiles, amphibians and insects. However, sexual death feigning, with one sex playing dead to avoid the opposite sex, is particularly rare. To date, the only four cases recorded include a species of spider, two species of robber flies and a species of mantis. Although death feigning has been documented in odonates, thisthesisis the first record of sexual death feigning in the moorland hawker (Aeshna juncea). I suggest that sexual conflict has been the primary driver of the evolution of this behavior due to high levels of maleharass- ment in this species. Since the moorland hawker is widespread in Europe where dragonflies have been studied extensively, it is likely that other cases of sexual death feigning remain undiscovered. Chapter V presents a commemoration of an important book in odonatology – The Biology of Dragonflies by Tillyard (1917) – and discusses the influence of this book on the field of odonatology, the contributions ofthe author to the understanding of dragonfly biology and systematics and the scientific advances overthe last century. Tillyard has set the foundation for the study of the biology of dragonflies by providing the basic knowledge on their morphology, anatomy and embryology that is still in use today. I divide the history of odonatology into four major periods: Selys era, Tillyard era, Corbet era and the blossoming era (contemporary odonatology). This thesis, as well as many other studies on dragonflies, would not have seen the light of day without Tillyard’s (1917) ‘The Biology of Dragonflies’; I therefore dedicate a chapter of my thesis to its 100th anniversary. The results shown in this thesis are particularly important because, unlike plants, ectotherms (cold-blooded animals) have received very little attention in the study of geographic and temporal patterns of phenology. Even though this group of animals encompasses most of the global biodiversity, its members share similar thermal adaptations (thermal performance curve). Consequently, understanding the mechanisms affecting their spatiotemporal pattern of phenology would help us predict their future response and adjust management plans accordingly. Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-139320 Dissertation Published Version Originally published at: Khelifa, Rassim. Spatiotemporal pattern of phenology across geographic gradients in insects. 2017, University of Zurich, Faculty of Science. 2 Spatiotemporal Pattern of Phenology across Geographic Gradients in Insects Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch-naturwissenschaftlichen Fakultät der Universität Zürich von Rassim Khelifa aus Algerien Promotionskommission PD Dr. Josh Van Buskirk (Vorsitz, Leiter der Dissertation) Prof. Dr. Wolf U. Blanckenhorn Prof. Dr. Lukas Keller Dr. Marc Kéry Zürich, 2017 Aeshna juncea (Flumserberg 2016, Rassim Khelifa) CONTENTS Summary i-iii iv-vii Zusammenfassung 1-6 General Introduction Geographic gradients in climate change response explained 7-37 Chapter I by non-linear thermal-performance curves Impact of climate change on insect phenology declines with 38-57 Chapter II latitude but not with elevation The use of thermal performance curves to predict 58-85 Chapter III development under variable lab and field conditions Faking death to avoid male coercion : extreme sexual conflict Chapter IV 86-95 resolution in a dragonfly A century on from The Biology of Dragonflies by Tillyard 96-117 Chapter V 1917: what have we learned since then? Conclusions & future directions 118-122 Acknowledgements
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