A predatory waterbird as a vector of plant seeds and aquatic invertebrates

Abstract

Omnivorous waterbirds play an important role in aquatic ecosystems as dispersal vectors via direct ingestion, transportation, and egestion of plant and invertebrate propagules (i.e. endozoochory). Predatory birds also have the potential to disperse plants and invertebrates that were first carried internally or externally by their prey animals. However, the potential contribution of predatory waterbird species to propagule dispersal in aquatic ecosystems remains understudied. We chose the grey heron Ardea cinerea (Ardeidae) to study the potential of predatory waterbirds to disperse propagules within and among aquatic ecosystems. We hypothesised that: (1) herons disperse a wide variety of plant and invertebrate propagules, from different habitats, with different morphologies (i.e. dispersal syndromes), and including both native and alien species; (2) propagules are ingested with prey species that are primary dispersal vectors (i.e., herons are secondary dispersers); (3) heron pellets show a similar abundance and richness of propagules across their widespread range. We collected 73 regurgitated heron pellets containing undigestible remains from 12 locations across the U.K. and The Netherlands, and examined the taxonomic diversity of plant seeds, invertebrates and prey remains. Pellets were dominated by mammal hairs (99% by volume), and bones confirmed the ingestion of small mammals (prevalence of 38%, e.g. water voles Arvicola amphibius), fish (14%), and birds or amphibians (6%). A total of 266 intact plant seeds were recovered from 71% of the pellets, representing 50 taxa from 17 plant families, including the alien Cotula coronopifolia. The cumulative number of plant species dispersed was lower at higher latitudes. Eight plant species recorded had not previously been recorded as dispersed via waterbirds, and only three species have an endozoochorous dispersal syndrome. Plant taxa were dominated by Caryophyllaceae, Cyperaceae, Juncaceae, and Poaceae, with 24 species from the littoral zone (Ellenberg moisture values of 7–12) and 21 terrestrial species (Ellenberg moisture values of 4–6). Intact invertebrate propagules were found in 30% of the pellets, dominated by Cladocera (Daphniidae) and Bryozoa (including the alien Plumatella casmiana). Our results demonstrate that grey herons disperse plant seeds and aquatic invertebrates widely in north‐western Europe. Herons regurgitate pellets that contain plant and invertebrate propagules from both aquatic or terrestrial habitats, for which secondary dispersal via ingestion along with prey is the likely underlying mechanism (i.e. propagules either attached to or in the digestive systems of the various prey). Our findings showcase the potential of predatory waterbirds as vectors of plants and invertebrates, and how they may facilitate connectivity between freshwater and terrestrial habitats.

Dispersal of aquatic and terrestrial organisms by waterbirds: A review of current knowledge and future priorities

“…Predatory waterbirds are similar to predatory seabirds (Maggio et al, 2022) and raptors (Pérez‐Méndez & Rodríguez, 2018), in that they disperse propagules inside or attached to their own prey (i.e., secondary dispersal), which can include granivores, herbivores or frugivores. Many plants and invertebrates have now been recorded in excreta of fish‐eating cormorants (van Leeuwen et al, 2017) and pelicans (Green et al, 2008), storks and gulls feeding on crayfish (Lovas‐Kiss, Sánchez, et al, 2018; Martín‐Vélez, Lovas‐Kiss, et al, 2021; Martín‐Vélez et al,2022), and also herons that feed on small mammals around wetland edges (Navarro‐Ramos et al, 2021). Recent research suggests that such secondary processes are widespread, largely cryptic and unpredictable in nature, and can be strongly influenced by biological invasions involving waterbird prey (Lovas‐Kiss, Sánchez, et al, 2018; Navarro‐Ramos et al, 2021).…”

“…Many plants and invertebrates have now been recorded in excreta of fish‐eating cormorants (van Leeuwen et al, 2017) and pelicans (Green et al, 2008), storks and gulls feeding on crayfish (Lovas‐Kiss, Sánchez, et al, 2018; Martín‐Vélez, Lovas‐Kiss, et al, 2021; Martín‐Vélez et al,2022), and also herons that feed on small mammals around wetland edges (Navarro‐Ramos et al, 2021). Recent research suggests that such secondary processes are widespread, largely cryptic and unpredictable in nature, and can be strongly influenced by biological invasions involving waterbird prey (Lovas‐Kiss, Sánchez, et al, 2018; Navarro‐Ramos et al, 2021). All birds also can disperse seeds and other plant diaspores by epizoochory (Hernández‐Brito et al, 2021; Johansson et al, 2021), or when constructing nests (Parnikoza et al, 2012).…”

“…For example, predatory waterbirds will secondarily disperse propagules from their prey (Lovas‐Kiss, Sánchez, et al, 2018). Furthermore, predators that dive in the pelagic zone (e.g., cormorants; van Leeuwen et al, 2017) ingest and disperse a different set of propagules to the long‐legged predators that stand in the littoral zone or onshore (e.g., herons; Navarro‐Ramos et al, 2021). Among ducks, the density of lamellae in the bill influences the feeding process, and species with higher lamellar densities tend to ingest a relatively higher abundance of small propagules (Green et al, 2016; Green & Figuerola, 2005).…”

“…Specific traits of waterbird species that are known to influence the fate of propagules after ingestion include diet and gut morphology (Green et al, 2016; van Leeuwen, van der Velde, van Groenendael, et al, 2012). Some species can regurgitate propagules in pellets (Lovas‐Kiss, Sánchez, et al, 2018; Navarro‐Ramos et al, 2021) or otherwise (Kleyheeg & van Leeuwen, 2015), allowing larger propagules to disperse even if they cannot survive complete gut passage into faeces. There are complex interactions of propagules with other food ingested simultaneously.…”

“…Recent research suggests that such secondary processes are widespread, largely cryptic and unpredictable in nature, and can be strongly influenced by biological invasions involving waterbird prey (Lovas-Kiss, Sánchez, et al, 2018;Navarro-Ramos et al, 2021). All birds also can disperse seeds and other plant diaspores by epizoochory (Hernández-Brito et al, 2021;Johansson et al, 2021), or when constructing nests (Parnikoza et al, 2012).…”