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Spatial and Temporal Flower Presentation in Apiaceae-Apioideae

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Spatial and Temporal Flower Presentation in Apiaceae-Apioideae SPATIAL AND TEMPORAL FLOWER PRESENTATION IN APIACEAE-APIOIDEAE DISSERTATION zur Erlangung des Grades „Doktor der Naturwissenschaften“ am Fachbereich Biologie der Johannes Gutenberg-Universität Mainz eingereicht von Kerstin Ulrike Reuther geb. am 15.03.1977 in Alzenau-Wasserlos Mainz, März 2013 Dekan: Prof. Dr. Hans Zischler 1. Berichterstatterin: Prof. Dr. R. Claßen-Bockhoff 2. Berichterstatter: Prof. J. W. Kadereit Ph. D. Tag der mündlichen Prüfung: 30.4.2013 "The day is coming when a single carrot freshly observed will set off a revolution." Paul Cezanne (1839-1906) Kapitel 2 dieser Arbeit wurde veröffentlicht als: Reuther, K. & Claßen- Bockhoff, R. (2010) Diversity behind uniformity – inflorescence architecture and flowering sequence in Apioideae - Plant Div. Evol. 128/1-2: 181-220. Kapitel 3 dieser Arbeit wurde veröffentlicht als: Reuther, K. & Claßen- Bockhoff, R. (2013) Andromonoecy and developmental plasticity in Chaerophyllum bulbosum (Apiaceae-Apioideae) - Annals of Botany [PART OF A SPECIAL ISSUE ON INFLORESCENCES; doi: 10.1093/aob/mct073; online verfügbar & im Druck]. Diese Arbeit ist allen gewidmet, die sehnsüchtig darauf gewartet haben, dass sie endlich fertig wird, insbesondere Christian und meinen Eltern. .............................................................................................................................................. I Contents CONTENTS SUMMARY OF THE THESIS……………………………….…………………….……..1 ZUSAMMENFASSUNG…………………………………………………………………..3 1 GENERAL INTRODUCTION…………………………….…….…………………….5 2 DIVERSITY BEHIND UNIFORMITY – INFLORESCENCE ARCHITECTURE AND FLOWERING SEQUENCE IN APIACEAE-APIOIDEAE……………………...9 2.1 ABSTRACT…………………………………………..……………………………..9 2.2 INTRODUCTION………………………………………..…………………………9 2.3 MATERIAL & METHODS………………………………………………………..14 2.3.1 Species investigated………………………………..………………………..14 2.3.2 Plant architecture……………………………………………………………14 2.3.3 Umbel organisation………………………………………………………….17 2.3.4 Dichogamy…………………………………………………………………..19 2.3.5 Flower types and sex distribution……………...……………………………20 2.3.6 Sex ratio……………………………………………………………………..20 2.3.7 Flowering sequence…………………………………………………………21 2.3.8 Photographical documentation………………………………………...……21 2.3.9 Symbols……………………………………………………………………..21 2.4 RESULTS………………………………………………………………………….22 2.4.1 Xanthoselinum alsaticum……………………………………………………23 2.4.2 Anthriscus caucalis………………………………………………………….26 2.4.3 Anthriscus sylvestris………………………………………………...………29 2.4.4 Myrrhis odorata………………………………………………………..........32 2.4.5 Daucus carota……………………………………………………….............34 2.4.6 Oenanthe pimpinelloides…………………………………………………....37 2.4.7 Echinophora spinosa………………………………………………………..39 2.4.8 Trinia glauca………………………………………………………..............42 2.4.9 Zizia aurea…………………………………………………………………..44 2.5 DISCUSSION……………………………………………………………………...47 2.5.1 The flower level……………………………………………………………..47 2.5.2 The umbellet and umbel level………………………………………………48 2.5.3 The plant level………………………………………………………………50 2.6 CONCLUSIONS…………………………………………………………………..52 Contents II 3 ANDROMONOECY AND DEVELOPMENTAL PLASTICITY IN CHAEROPHYLLUM BULBOSUM (APIACEAE-APIOIDEAE)……………...……...53 3.1 ABSTRACT…………………………………………..……………………………53 3.2 INTRODUCTION………………………………………..………………..………54 3.3 MATERIAL & METHODS………………………………………………………..56 3.3.1 Study species and site ………………………………………………………56 3.3.2 Experimental design………………………………………………………...57 3.3.3 Data collection………………………………………………………………59 3.3.4 Statistical analysis…………………………………………………………...61 3.4 RESULTS………………………………………………………………………….61 3.4.1 Percentages of male flowers………………………………………………...61 3.4.2 Fruit production……………………………………………………………..62 3.5 DISCUSSION………………………………………………………...……………65 3.5.1 Andromonoecy as an inherited character………………………...…………66 3.5.2 Fruit set and self-pollination capacity ……………………………………...66 3.5.3 Developmental plasticity ...…………………………………………………67 3.6 CONCLUSIONS…………………………………………………………………..68 4 ‘AND YET THEY VARY’ - SPATIAL-TEMPORAL DIVERSIFICATION IN FLOWERING APIACEAE-APIOIDEAE & THEIR UNIFORMOUS FUNCTIONAL SYNDROME...69 4.1 ABSTRACT…………………………………………..……………………………69 4.2 INTRODUCTION………………………………………..………..………………70 4.3 MATERIAL & METHODS………………………………………………………..74 4.3.1 Sampling and taxon origins…………………………………………………74 4.3.2 Taxonomy and geography of the selected species……………...…………...75 4.3.3 Data collection………………………………………………………………77 4.3.4 Data analysis and illustration…………………………………...…………...84 4.4 RESULTS………………………………………………………………………….85 4.4.1 The model apioid – frequent character states in the Apioideae...…………...85 4.4.2 Diversification..……………………………………………………………..93 4.4.3 Summary……...……………………………………………………………139 4.5 DISCUSSION…………………………………………………………………….141 4.6 CONCLUSIONS………………………………………………..………………..148 5 GENERAL CONCLUSIONS…………………………….…….……………………149 6 REFERENCES…………………………….…….…………………………………...150 7 APPENDICES……………..…………………………….…….……………………..174 1 Summary SUMMARY OF THE THESIS All members of the carrot family (Apiaceae), among them cosmopolitain subfamily Apioideae, resemble in inflorescence characters. The ‘compound’ umbels are formed by small, white or yellow flowers and visited by many unspecialized insects. The uniformous impression, that is created, may be a reason that the underlying morphology has been barely analyzed to date. The purpose of the present dissertation is therefore, to demonstrate ‘cryptic diversity’ in the flowering shoots of the Apiaceae-Apioideae with the aim to identify the influence of the plants’ architecture on flower presentation in space and time and thereby on the reproductive system. In the first chapter, a comparative analysis of nine selected species shows that in the self-fertile and unspecifically pollinated plants outcrossing is promoted by synchronized and rhythmic presentation of flowers. Thereby, the dichogamous plants either pass only one male and female flowering phase (Xanthoselinum alsaticum), or the modular construction of the plants entails a sequence of male and female phases (multicycle dichogamy). Dioecy in Trinia glauca may be regarded as a split of the flowering phases into separate individual. It is demonstrated that in the andromonoecious taxa the proportion of (functionally) male flowers increases inconsistently with umbel order. Thus, the plants, at different times and to different degrees, function rather as pollen acceptors or donors. It becomes clear that the uniformous inflorescence pattern of the Apioideae including umbels of different order, dichogamous flowers and diverse sex forms represents a complex space-time-unit to optimize the breeding system. The second chapter illustrates the results of manipulation experiments (hand-pollination, bagging, umbel removal) in Chaerophyllum bulbosum showing that, as a space-time-unit in flower presentation, the species is able to respond flexibly to environmental stress. Mechanical damage emerges to merely influence the degree of andromonoecy and percentage fruit set of the individuals. The basis requirement of the ability to respond to environmental influences is again the modular construction. This allows the plants, together with the andromonoecy-induced reservoir of – sexually flexible – male flowers, to compensate in the later-developing flowers for the lack of fruits in the early-flowering umbels. Summary 2 In the third chapter, I provide data of a character analysis in 255 apioid taxa representing all major clades, life forms and distribution areas of the group. The aim of the study was the identification of character syndromes that were supposed to clarify the relationship of plant architecture and breedings system. Interestingly, the only traits that consistently accompany each other are protogyny and the gradual decrease in the number of male flowers with increasing umbel order. All other plant characters vary independently from each other and in many ways create a similar functional model that can be interpreted as the apioid ‘breeding syndrome’. This dissertation contributes towards the functional comprehension of Apiaceae inflorescences and to morphological variation in ‘unspecialized’ breeding systems. Obviously, in the Apiodeae selective pressure upholds the generalist pollination system and superimposes onto all morphological-phylogenetic character variations. 3 Zusammenfassung ZUSAMMENFASSUNG Alle Doldengewächse (Apiaceae), darunter die größte, weltweit verbreitete Unterfamilie der Apioideen, weisen in ihren Blütenständen sehr einheitliche Merkmale auf. Die `Doppeldolden´ werden aus kleinen, weißen oder gelben Blüten gebildet und von vielen unspezialisierten Insekten besucht. Der uniforme Eindruck, der damit erweckt wird, ist unter Umständen ein Grund, dass die zugrundeliegende Morphologie bislang wenig untersucht wurde. Gegenstand der vorliegenden Dissertation ist es daher, die `verborgene Diversität´ im Blütenstandsbereich der Apiaceae -Apioideen mit dem Ziel darzustellen, den Einfluss der Architektur der Pflanzen auf die Art der Blütenpräsentation in Raum und Zeit und damit auf das Reproduktionssystem der Art zu ermitteln. Im ersten Kapitel zeigt der Vergleich von neun ausgewählten Arten, dass in den selbstfertilen und unspezifisch bestäubten Pflanzen durch Synchronisation und Rhythmik in der Präsentation von Blüten Fremdbefruchtung gefördert wird. Entweder durchlaufen die Pflanzen dabei nur eine getrennte männliche und weibliche Blühphase (Xanthoselinum alsaticum) oder der moduläre Bau der Pflanzen führt zu einer Folge männlicher und weiblicher Blühphasen (multizyklische Dichogamie). Die Diözie in Trinia glauca kann in diesem Zusammenhang als eine Trennung der Blühphasen
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