PDF hosted at the Radboud Repository of the Radboud University Nijmegen The following full text is a publisher's version. For additional information about this publication click this link. http://hdl.handle.net/2066/93702 Please be advised that this information was generated on 2021-10-07 and may be subject to change. SPEEDING UP THE SNAIL’S PACE Bird-mediated dispersal of aquatic organisms Casper H.A. van Leeuwen Speeding up the snail’s pace Bird-mediated dispersal of aquatic organisms The work in this thesis was conducted at the Netherlands Institute of Ecology (NIOO-KNAW) and Radboud University Nijmegen, cooperating within the Centre for Wetland Ecology. This thesis should be cited as: Van Leeuwen, C.H.A. (2012) Speeding up the snail’s pace: bird-mediated dispersal of aquatic organisms. PhD thesis, Radboud University Nijmegen, Nijmegen, The Netherlands ISBN: 978-90-6464-566-2 Printed by Ponsen & Looijen, Ede, The Netherlands Speeding up the snail’s pace Bird-mediated dispersal of aquatic organisms PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Radboud Universiteit Nijmegen op het gezag van de rector magnificus prof. mr. S.C.J.J. Kortmann, volgens besluit van het College van Decanen in het openbaar te verdedigen op woensdag 27 juni 2012 om 13.00 uur precies door Casper Hendrik Abram van Leeuwen geboren op 18 september 1983 te Odijk Promotoren: Prof. dr. Jan van Groenendael Prof. dr. Marcel Klaassen (Universiteit Utrecht) Copromotor: Dr. Gerard van der Velde Manuscriptcommissie: Prof. dr. Hans de Kroon Dr. Gerhard Cadée (Koninklijk NIOZ) Prof. dr. Edmund Gittenberger (Universiteit Leiden) Prof. dr. Andy Green (Estación Biológica de Doñana, CSIC, Spain) Prof. dr. Luc de Meester (KU Leuven, Belgium) Contents 1. General introduction 7 2. Gut travellers: internal dispersal of aquatic organisms by waterfowl 17 3. Experimental quantification of long distance dispersal potential of 49 aquatic snails in the gut of migratory birds 4. Vector activity and propagule size affect dispersal potential by vertebrates 67 5. Prerequisites for flying snails: external transport potential of aquatic 85 snails by waterbirds 6. How did this snail get here? Multiple dispersal vectors revealed for an 101 aquatic invasive species 7. A snail on four continents: bird-mediated dispersal of a parasite vector? 121 8. Synthesis 141 Summary 161 Nederlandse samenvatting 165 Dankwoord 169 Affiliations of co-authors 173 Publication list 174 Curriculum vitae 175 Chapter 1 General introduction Casper H.A. van Leeuwen 7 Chapter 1 Dispersal Movement of species in the landscape is essential for the long term survival of their populations. It enables species to colonize new suitable habitat and escape potential deteriorating conditions in their present habitat, which is crucial for their prolonged existence in a continuously dynamic environment (Cain et al., 2000; Holt, 2003; Lest- er et al., 2007). Biological dispersal, defined as the directional movement away from a source location to establish or reproduce, occurs in nearly all species and has im- portant consequences at the individual, population and community level (Clobert et al., 2001; Bullock et al., 2002; Nathan, 2006). It occurs at all spatial scales, ranging from vertical movements of larvae in the water column (Sundelöf & Jonsson, 2011) to pollen drifting in wind over many kilometres in rainforests (Ndiade-Bourobou et al., 2010). Dispersal thereby influences most ecological and evolutionary processes (Dieckmann et al., 1999). However, for many species it is still unknown how and in which directions they disperse (Clobert et al., 2001). Dispersal allows individuals to find other locations where there may be more nutrients and less diseases and predators (McKinnon et al., 2010; Altizer et al., 2011), and can dilute negative effects of inbreeding or loss of genetic variation in popula- tions (Hamilton & May, 1977; Fayard et al., 2009). Nowadays, in an attempt to cope with global change processes, a species’ ability to escape from rapidly deteriorat- ing environmental conditions or exploit new suitable areas may be of even greater relevance. Dispersal can thereby positively affect biodiversity if it allows species to e.g. follow changing climatic boundaries, maintain populations in increasingly fragmented landscapes or avoid genetic drift in small populations (Kokko & Lopez- Sepulcre, 2006; Pearson, 2006). On the other hand, biodiversity can be negatively affected by increased dispersal rates if species with very good dispersal abilities ex- pand their home ranges drastically and thereby outcompete other species after inva- sion (Phillips et al., 2006; Van der Velde et al., 2010). Vector-mediated dispersal Despite the ecological significance of dispersal for many species, the heterogene- ity of the earth’s landscape may restrict their movement. Whereas it is often rela- tively easy to travel within a certain habitat type (e.g. a forest, ocean or lake), it becomes more challenging when this involves crossing a different type of terrain over a longer distance, i.e. an ecological barrier (Cain et al., 2000). Nevertheless, even remote islands in the ocean and isolated ponds in the desert often harbour a high biodiversity (Schabetsberger et al., 2009; Jocque et al., 2010). Many species are able to cross ecological barriers to suitable patches using their own propulsion, i.e. active dispersers (Jenkins et al., 2007, see also Fig. 1.1). Others, so-called passive dispers- ers, require transport by vectors (Zickovich & Bohonak, 2007). Organisms may be blown across land or sea by the wind (anemochory, e.g. Soons & Ozinga, 2005), can be carried by water (hydrochory, e.g. Van de Meutter et al., 2006), or may be trans- ported by more mobile animals (zoochory, e.g. Enders & Vander Wall, 2011; Pollux, 2011) including humans (e.g. Wichmann et al., 2009). Although passive dispersal can involve transport of whole organisms, it frequently involves transport of dispersal units called “propagules”. These are here considered all (parts of) organisms that 8 General introduction can disperse and regenerate, regardless of their dispersal mode or metabolic state (e.g. plant seeds, fruits, algae spores, cladoceran ephippia, bryozoan statoblasts, pieces of plants that can regenerate). Islands provide ideal model systems to investigate vector-mediated dispersal of propagules (MacArthur & Wilson, 1967), because island biodiversity is largely de- termined by which species are able to disperse across another habitat type from (dis- tant) source populations (Gillespie et al., 2008). Freshwater habitats, often referred to as “islands in a sea of land” (essay of 1844 of C. Darwin, in F. Darwin 1909), are particularly suitable to study dispersal of aquatic organisms over land. The fact that many wetlands harbour a high biodiversity (Green et al., 2002b; Junk et al., 2006) seems contrasting to their often high degree of isolation, and can usually not entirely be explained by wind- and water-mediated dispersal. This paradox already fasci- nated Darwin over 150 years ago (Darwin, 1859). It made him propose waterbirds as potential dispersal vectors for aquatic organisms. Waterbirds travel fast, directed and in large numbers between ecologically simi- lar habitats (Figuerola & Green, 2002; Green et al., 2002a; Nathan et al., 2008). Terres- trial birds are already known to be effective dispersers of plant seeds and fruits that survive digestion after ingestion (internal transport or endozoochory, reviewed by Traveset, 1998). Seeds and fruits may also be transported on feet or between feath- ers of birds (external transport or ectozoochory, reviewed by Sorensen, 1986). How- ever, in comparison to what is known in terrestrial ecosystems, knowledge on the potential of waterbirds to disperse aquatic organisms is still limited (reviewed by Figuerola & Green, 2002; Green & Figuerola, 2005). Species distributions Capacity to Capacity to disperse survive in environment Active dispersal Passive dispersal by vectors (own propulsion) Animals Wind Water Birds Other animals, e.g. Chapter 6 mammals, fish, insects at small scale Internal External Chapter 7 dispersal dispersal at large scale Chapter 2,3,4 Chapter 5 Molecular genetic Mechanistic approach approach Figure 1.1: Conceptual diagram of the topics addressed in this thesis. Species distributions are determined by their capacity to disperse through as well as survive in their environment. Dispersal can be either passive by vectors such as animals, wind or water, or active by own propulsion. In this thesis the mechanistic approach is used to investigate internal and external dispersal by birds, whereas the molecular genetic approach addresses dispersal on small scales by multiple vectors and dispersal on a large scale by birds. 9 Chapter 1 This is surprising, given the presumably even higher relevance of dispersal between discrete, isolated aquatic systems than within more continuous terrestrial habitats. The aim of this thesis was therefore to assess the importance of waterbirds for the dispersal of aquatic organisms (Fig. 1.1). Waterbirds as vectors for small aquatic species The idea of waterbirds as dispersal vectors originates from Darwin (1859), followed by Kew (1893) and Ridley (1930). After the idea was mentioned, scientists started to report observations of small species adhering to waterbirds that were caught in the field for other purposes (Adams, 1905; McAtee, 1914). These field observations were extended by a series of experiments on waterbird-mediated dispersal by Proctor and