Endozoochory of aquatic ferns and angiosperms by mallards in Central Europe

Abstract

Modern literature on plant dispersal by birds focuses mainly on the importance of frugivory and scatter‐hoarding, yet recent studies show that endozoochory by migratory waterbirds is an important mechanism of long‐distance dispersal for a broad range of plants. Nevertheless, there is a lack of empirical field studies that identify the plants dispersed by waterbirds in a comprehensive manner. In particular, so far there are no detailed studies of the level of spatial variation in the plant taxa dispersed by a waterbird vector, and no clear demonstration that aquatic ferns can be dispersed by endozoochory. Consequently, we remain ignorant of the networks of dispersal interactions between granivorous waterbirds and plants. Five sets of faecal samples (total n = 215) were collected from mallards Anas platyrhynchos on autumn migration in the Hevesi‐holm and Balaton regions in Hungary, central Europe. Intact diaspores were extracted, identified and their germinability assessed under standard conditions. The plant communities recorded at different sites were compared with PERMANOVA and other multivariate methods. Macrospores of the floating watermoss Salvinia natans were recorded in 32 samples, and a total of 16 macrospores germinated, providing the first field demonstration of endozoochory of ferns by birds. Of 21 angiosperm taxa recorded (of which eight germinated), 13 were terrestrial species, although the most abundant taxa were aquatic species such as the alkali bulrush Bolboschoenus maritimus and the sago pondweed Potamogeton pectinatus. Two naturalized alien species, the common fig Ficus carica and the hackberry Celtis occidentalis were also recorded. Only four of the taxa had an endozoochory syndrome. The plant taxa dispersed varied at two different spatial scales, with minor but significant differences between samples from sites separated by less than 1 km, and major differences between the two regions separated by c. 220 km. Synthesis. This is a unique study of the spatial variation in plants dispersed by endozoochory by a migratory waterfowl species, with a high taxonomic resolution and the first demonstration of avian endozoochory of ferns. We recorded eight taxa not previously reported as dispersed by mallards, showing how more empirical studies are essential, so we can understand which plants are dispersed by migratory birds. We found evidence that networks of interactions between granivorous waterbird vectors and dispersed plants vary spatially.

Seed mass, hardness, and phylogeny explain the potential for endozoochory by granivorous waterbirds

“…Although to our knowledge, only three of them ( Echinochloa crus‐galli , Elatine hydropiper , Sparganium erectum ) have been recorded in the alimentary tract of dabbling ducks, congeners of the other species have been recorded in ducks or geese (Costea et al, ; Hattermann et al, ; Soons et al, ). Dispersal of our study species by mallards is likely, since the list of plant species ingested by ducks is far from complete, and there is a lack of diet data from central Europe (Lovas‐Kiss, Vizi, et al, ; Soons et al, ). We found here that not only do widespread, common plant species have strong potential for endozoochory, but also rare species with limited distributions, such as Astragalus contortuplicatus , the glacial relict Angelica palustris , or the Pannon‐basin endemic Cirsium brachycephalum .…”

“…This is a form of “nonclassical endozoochory,” as it does not coincide with the “endozoochory syndrome” (Green, Elmberg, & Lovas‐Kiss, ). Diet studies for dabbling ducks suggest they disperse over 500 plant species in Europe alone (Lovas‐Kiss, Vizi, et al, ; Soons, Brochet, Kleyheeg, & Green, ). The maximum plant dispersal distances provided by migratory waterbirds greatly exceed those expected from abiotic vectors, and therefore, have an important influence on changes in plant distribution in response to climate change, or biological invasions (Bullock et al, ; Viana, ).…”

“…Migratory waterbirds such as ducks, shorebirds, and gulls disperse a broad range of angiosperms and other plants with propagules capable of surviving passage through the avian gut (i.e., through "endozoochory", Green et al 2016;Lovas-Kiss, Sanchez, et al, 2018b;Lovas-Kiss, Vizi, Vincze, Molnár, & Green, 2018a;Lovas-Kiss et al, 2019;Reynolds & Cumming 2016a). Recent models confirm that these birds are major vectors for long-distance dispersal (LDD), and angiosperm seeds are often moved over hundreds of km within the digestive tract of waterbirds such as granivorous dabbling ducks Anas spp.…”

A mechanistic assessment of the relationship between gut morphology and endozoochorous seed dispersal by waterfowl

“…Together, they determine the potential dispersal distance, although this also depends heavily on the spatial behavior of the disperser animal (Figuerola & Green, ; Kleyheeg, ; Kleyheeg, Treep, Jager, Nolet, & Soons, ; Will & Tackenberg, ). Endozoochorous dispersal is crucial to the population dynamics of numerous plant species in a wide range of ecosystems (e.g., Pakeman, ; Jordano, García, Godoy, & García‐Castaño, ; Sasal & Morales, ; Lovas‐Kiss, Vizi, Vincze, Molnár, & Green, ) and has the advantage over other dispersal mechanisms that it is often directed toward habitat patches that are suitable for establishment and not necessarily physically connected (Howe & Murray, ; Kleyheeg et al, ; Wenny, ). A broad range of aquatic and terrestrial plant species benefit from this by dispersing via the guts of waterfowl (Figuerola and Green, (); Leeuwen, Velde, et al, ; Lovas‐Kiss et al, ; Soons, Brochet, Kleyheeg, & Green, ; Kleyheeg, Klaassen, & Soons, ; Farmer, Webb, Pierce, & Bradley, ).…”

“…Endozoochorous dispersal is crucial to the population dynamics of numerous plant species in a wide range of ecosystems (e.g., Pakeman, ; Jordano, García, Godoy, & García‐Castaño, ; Sasal & Morales, ; Lovas‐Kiss, Vizi, Vincze, Molnár, & Green, ) and has the advantage over other dispersal mechanisms that it is often directed toward habitat patches that are suitable for establishment and not necessarily physically connected (Howe & Murray, ; Kleyheeg et al, ; Wenny, ). A broad range of aquatic and terrestrial plant species benefit from this by dispersing via the guts of waterfowl (Figuerola and Green, (); Leeuwen, Velde, et al, ; Lovas‐Kiss et al, ; Soons, Brochet, Kleyheeg, & Green, ; Kleyheeg, Klaassen, & Soons, ; Farmer, Webb, Pierce, & Bradley, ). Recent mechanistic models predicting dispersal patterns shaped by migrating waterfowl (Soons, Vlugt, Lith, Heil, & Klaassen, ; Viana et al, ; Viana, Santamaría, Michot, & Figuerola, ) and resident waterfowl (Kleyheeg et al, ) have highlighted the importance of variation in seed gut passage survival and retention time for the outcome of dispersal events.…”