The Evolution and Ecology of Hygrochastic Capsule Dehiscence
Authors:   , Pufal Gesine 
Published: November 2021

<p>This dissertation aims to explore hygrochasy in different genera of various habitats by investigating biomechanics, challenging accepted hypotheses and broadening the knowledge of the ecology and evolution of this dispersal mechanism. Hygrochasy, the dehiscence of capsules in response to moisture, is a specialized plant movement that facilitates primary dispersal by raindrops. This research enhances the understanding of this intriguing plant behaviour with a multidisciplinary approach outlined in the following paragraphs. Hygrochastic New Zealand Veronica (Plantaginaceae) have been identified and investigated in regards to the anatomy and biomechanics of their opening mechanism and comparisons to related ripening dehiscent species have been drawn. Light microscopy has been used to analyse the capsule anatomy and function, while multivariate methods have been used to explore the data and associations with other characters. A swelling tissue in the septum, which absorbs water quickly and expands and a lignified resistance tissue have been found to cause the opening of hygrochastic capsules. This imbibition mechanism can be found in a number of hygrochastic genera in different habitats but the position of involved tissues due to capsule anatomy is unique for New Zealand Veronica. Morphological analysis revealed that hygrochasy in Veronica is most likely associated with solitary, erect, narrowly angustiseptate capsules on short peduncles of creeping subshrubs or cushions. The hypothesis that hygrochasy in alpine Veronica is an adaptation to ensure short distance dispersal to safe sites is explored. Dispersal distances were measured in the field and in laboratory experiments and habitat patch size was measured for hygrochastic and related non-hygrochastic species. Habitat patches for alpine hygrochastic Veronica are small and distinctly different from surrounding habitat. They provide safe sites due to their microtopography and the presence of adult cushion plants. Hygrochastic capsules facilitate ombrohydrochory by raindrops, which is an antitelechoric strategy previously reported from desert plant species. For the first time directed short distance dispersal to safe sites could be demonstrated in alpine hygrochastic species. Additionally, environmental attributes for known locations of hygrochastic and related non-hygrochastic Veronica were obtained from LENZ IV in arcGIS. These have been used to identify the environmental amplitude for each species as well as variations in habitat. Non-hygrochastic species show a higher environmental amplitude and grow in a wider range and variety of habitats than hygrochastic species. Hygrochastic Veronica are specialists with a narrow ecological niche and are usually confined to small habitat patches in specific alpine habitats. By combining both approaches I show that hygrochasy in alpine Veronica not only supports safe site strategies in seed dispersal but that hygrochastic Veronica are limited to special habitats requiring specific edaphic conditions. Short-distance dispersal also ensures the persistence of existing populations in these rare habitats. Opening of some sessile New Zealand Colobanthus capsules during rain has been observed in the field and I carried out investigations regarding hygrochastic movements in this genus. Various staining and sectioning techniques for light microscopy have been carried out and scanning electron microscopy has been used to further analyse capsule anatomy. Statistical analysis similar to the investigation of Veronica capsules was employed. In contrast to other species with hygrochastic capsules, Colobanthus capsules are not lignified. Here, opening under wet conditions is a result of a combination of imbibition and cohesion mechanisms. Outer cells of the capsule have a thickened outer cell wall, which absorbs moisture, whereas the inner cells have thin cell walls and the cell lumen swells when water is absorbed. Interestingly, all Colobanthus species have the same capsule anatomy and are therefore capable of hygrochastic opening. Earlier it was assumed that only Colobanthus species with sessile capsules might potentially be hygrochastic. In order to understand the relations between those species and other Colobanthus and to investigate whether this genus is monophyletic, I attempted to solve the phylogeny of this genus. I used the nuclear marker ITS and the chloroplast markers rps16 and trnT-trnE to investigate the phylogeny with parsimony and Bayesian analyses. A number of outgroups in the family of Caryophyllaceae were used to test for monophyly of Colobanthus. Analyses of combined datasets show that the genus Colobanthus is monophyletic with Sagina as sister clade. Colobanthus forms a crown clade with no distinct differences between species. Results suggest a very recent speciation but further study with different markers or AFLPs is warranted, since the markers used in this study showed very little variation. Hygrochasy has previously been reported and described to some extent in some North American Oenothera (Onagraceae) of subclade B, characterized by winged fruits. Here, I use the same methods employed by Poppendieck to extend the list of known hygrochastic Oenothera and I also describe xerochasy in one additional species. The position of the swelling tissue and resistance tissue is the same in all hygrochastic Oenothera, whereas the positions of these tissues are reversed in the xerochastic species. Hygrochastic movement was also observed in a ripening dehiscent species of subclade B, which is characterized by lanceoloid fruits. Here, hygrochasy occurs when the exocarp disintegrates and the endocarp expands after water absorption, similar to hygrochastic species of subclade B. However, due to the morphology of the capsule, the opening of the fruit does not resolve in a wide splash cup. Hypotheses for hygrochastic capsules have mostly been developed for plants in arid regions. The most prevalent theories are that hygrochasy restricts dispersal in time by limiting dispersal events to rainfall events and therefore favourable germination conditions. Also, hygrochasy restricts seed dispersal to short distances, which increases the survival chance of seeds in the very local parental habitat, rather than surrounding harsh environments. However, hygrochasy occurs in a wide range of unrelated genera in a variety of habitats. Here, I investigate whether the widely accepted hypotheses for arid species also apply to hygrochastic Oenothera in North America. Dispersal experiments, cluster analysis of morphological traits and the analysis of environmental and distribution data were used in this study and compared with similar data for hygrochastic Veronica in New Zealand and hygrochastic Aizoaceae in Southern Africa. Character evolution was also investigated using the latest published phylogenies of Oenothera and Veronica. Results indicate that none of the hypotheses for hygrochasy applies to current day Oenothera. However, it appears that hygrochasy evolved only once in this genus and previous research implies that Oenothera have evolved as part of the Madro-Tertiary flora in the mid- to late Miocene. The Madro-Tertiary flora evolved in a dry, highly seasonal climate. Possessing hygrochastic capsules would be advantageous to restrict dispersal to rare rainfall events in the wet seasons. It therefore appears that at least the temporal restriction hypothesis applies to Oenothera at the time of their evolution. Other, unknown factors might play a role in the persistence of this character.</p>