Seed dispersal by a generalist duck Ingestion, digestion and transportation by mallards (Anas platyrhynchos) Thesis committee: Prof. dr. J. Elmberg Prof. dr. T. Piersma Prof. dr. M. Rietkerk Prof. dr. M.E. Visser Dr. L. Santamaría Cover design: Jetty den Daas Printed by: GVO drukkers & vormgevers B.V. | Ponsen & Looijen, Ede, The Netherlands Photo courtesy of: Erik Kleyheeg & Mary Ann Morison This thesis should be cited as: Kleyheeg E. (2015) Seed dispersal by a generalist duck: ingestion, digestion and transportation by mallards (Anas platyrhynchos). PhD thesis. Utrecht University, Utrecht, The Netherlands ISBN: 978-90-6464-897-7 Seed dispersal by a generalist duck Ingestion, digestion and transportation by mallards (Anas platyrhynchos) Zaadverspreiding door een generalistische eend Consumptie, vertering en transport door Wilde Eenden (Anas platyrhynchos) (met een samenvatting in het Nederlands) Proefschrift ter verkrijging van de graad van doctor aan de Universiteit Utrecht ingevolge het besluit van het college voor promoties in het openbaar te verdedigen op gezag van de rector magnificus, prof. dr. G.J. van der Zwaan, op woensdag 23 septemberdoor 2015 des ochtends te 10.30 uur Erik Kleyheeg geboren op 5 oktober 1987 te Voorburg Promotor: Prof. dr. J.T.A. Verhoeven Copromotor: Dr. M.B. Soons (NWO;This thesis VIDI was grant accomplished 864.10.006 withto M.B. financial Soons). support from the Research Council for Earth and Life Sciences (ALW) of the Netherlands Organization for Scientific Research Contents Chapter 1 General introduction 7 Part I. Ingestion Chapter 2 19 mallards (Anas platyrhynchos) promotes seed dispersal. High variability in diet composition and gut morphology in wild Part II. Digestion traits and digestive processes determine seed viability. Chapter 3 Passing through waterbird guts, part I: Interactions between seed 39 Chapter 4 55 and seed size affect seed dispersal by mallards (Anas Passing through waterbird guts, part II: How do diet composition platyrhynchos)? Chapter 5 71 active birds modulates dispersal capacity of plant seeds. Bird-mediated seed dispersal: reduced digestive efficiency in Chapter 6 89 Regurgitation by waterfowl: an overlooked mechanism for long- distance dispersal of wetland plant seeds? Part III. Transportation Chapter 7 Daily movement distances and home range sizes of mallards 101 (Anas platyrhynchos) are strongly affected by landscape configuration. Chapter 8 Daily movements of mallards (Anas platyrhynchos) result in 125 frequent directional long-distance dispersal of plant seeds. Chapter 9 Synthesis References 157143 Summary 175 Nederlandse samenvatting 181 187 190 Dankwoord Publication list 191 Author’s affiliations Curriculum Vitae 192 Chapter 1 General Introduction Erik Kleyheeg CHAPTER 1 Movement and dispersal Movement is a key aspect of the ecology of all living organisms, whether animal, plant or micro-organism, at least during part of their life cycle (Nathan 2008). The impor- sessiletance of and movement unable tois particularlyrelocate themselves, obvious inmovement animals, mostis crucial of which for their walk, survival fly, swim and or adaptation,crawl to find and food, occurs shelter during or a mate.a mobile However, life-history even forstage organisms (e.g. as thatseed, are spore, apparently egg or larva). In a changing, human-dominated world, where natural habitats are increasingly fragmented and degraded by land use change and climate change, this movement is Olivieri et al. et al. et al. ever more important to escape unfavourable conditions (Howe & Smallwood 1982, genetic information between isolated populations to avoid inbreeding (Greenwood et 1995, McKinnon 2010, Altizer 2011), maintain exchange of al. et al. et al. 2002). For ‘sessile’ organisms, the movement as dispersal unit thus 1978, Waser 1986) and colonize newly available patches (Howe & Smallwood strategy1982, Bullock and the mechanisms determining its success are crucial factors in population largely determines future survival and fitness. Hence, on a broader scale, their dispersal- - dynamics (Jordano & Herrera 1995, Nathan & Muller-Landau 2000), community struc ture (Levine & Murrell 2003, Howe & Miriti, 2004) and eventually, ecosystem biodiver sity (Bascompte & Jordano 2007). et al. Dispersal is defined as the unidirectional movement of an organism away from its et al. et parent or place of birth (Nathan 2001, Levin 2003). By dispersal, organisms avoid al. kin competition (Levin 2003), density-dependent predation risk (Hammond 1998) and inbreeding (‘escape hypothesis’, Howe & Smallwood 1982), and colonize et al. et al. 2002), suggesting and persist in ephemeral habitats (‘colonization hypothesis, Howe & Smallwood 1982). poorDispersal adaptation occurs of in endangered nearly all taxa species (Clobert to environmental 2001, Bullock change is often associated with that it is of significant importance for individual fitness and species persistence. Indeed, et al. while the rapid spread of invasive species is often facilitated by high dispersal capacity dispersal limitation (Kokko & Lopez-Sepulcre 2006, Pearson 2006, Ozinga 2009), et al. et al. knowledge about its underlying mechanisms is essential for biodiversity conservation and(Sakai the management 2001, Phillips of invasive 2006,). species. Given More the fundamentally, important consequences studying dispersal of dispersal, pro- vides basic insights in spatial population dynamics and ecosystem functioning. From a life-history perspective, dispersal is successful when it results in estab- lishment and reproduction at any distance from the location where the organism was produced. The success of dispersal depends largely on the ‘disperser effectiveness’, a et al. designedconceptual as frameworka framework introduced for seed dispersal for plants by byanimals, Schupp the (1993) basic principlesand later arerevised valid and for reformulated as ‘dispersal effectiveness’ (Schupp 2010). Although originally 8 GENERAL INTRODUCTION any dispersal vector and any immobile (sedentary) organism: The success of dispersal, - ities of a disperser’, depends on the number of individuals dispersed by a vector and the probabilitydefined by Schupp that the (1993) individuals as the ‘numbersurvive dispersal of new adults and producedestablish atby the dispersaldeposition activ site et al. mechanisms(Schupp involved 2010). Thisin vector-based framework dispersalemphasizes and the evaluating crucial role their of effectsdispersal on thevectors dis- in the dispersal process of immobile organisms and its consequences. Unravelling the persed organism has been a central theme in the study of dispersal (Howe & Smallwood et al. et al. 1982), but many interactions between organisms and their dispersers have yet to be understood (Clobert 2001, Nathan 2005). Figure 1.1 A conceptual overview of the three potential natural dispersal mechanisms for (mainly) aquatic and riparian plants. Hydrochory is limited to the water body where the seeds around the source location in more or less random direction, irrespective of habitat type (shaded are produced, but seeds remain within suitable habitat. Anemochory results in seed deposition area). Zoochory (e.g. by waterbirds) potentially results in long-distance dispersal directed towards suitable habitat (arrows). How do plants disperse? the dispersal of seeds and other detachable reproductive structures (‘propagules’) to Once rooted in the soil, plants are fixed to a location in the landscape. They depend on on dispersal have resulted in adaptations for a wide range of dispersal mechanisms escape from unfavourable conditions or move to other suitable habitats. Selective forces (Howe & Smallwood 1982), which all interact with propagules in different ways. Many plants invest in structures that facilitate a specific dispersal mechanism which may be 9 CHAPTER 1 particularly effective for the species (e.g. sticky viscin on mistletoe seeds dispersed by - birds; Wenny 2001). Two fundamental modes of dispersal can be distinguished: auto- tations.chory (self-dispersal) In some species, and theallochory parent (dispersal plant produces by a vector; structures Van der that Pijl build-up 1982). Autochory pressure includes the release of seeds by gravity, which usually does not require specific adap onand the forcefully other hand, launch can the potentially seeds. However, result autochory in dispersal does over usually hundreds not result to thousands in dispersal of kilometres,over more than and acan few be meters roughly from divided the parent into three plant modes: (Vittoz dispersal & Engler by2007). wind Allochory, (anemo- Dispersal by humans (anthropochory) is sometimes considered as a fourth mechanism chory), water (hydrochory), or animals (zoochory) (Fig. 1.1; Howe & Smallwood 1982). et al. (Wichmann 2009). “As lakes and river-systems are separated from each other by barriers of land, it might have been thought that fresh-water productions would not have ranged widely within the same country, and as the sea is apparently a still more impassable barrier, that they never would have extended to distant countries. But the case is exactly the reverse.” Charles Darwin (1859) On the Origin of Species, chapter XII, p 343. - Seeds dispersed by wind or water usually have adaptations to reduce their ter hydrochoryminal velocity strongly or their depend density, on so the they direction can stay and afloat speed in ofair wind or on and the water water currents. surface (e.g. For a pappus for anemochory and low-density tissues for hydrochory).