Dispersal of aquatic invertebrates by lesser black-backed gulls and white storks within and between inland habitats

Abstract

Waterbirds can transport aquatic invertebrates internally, contributing to metapopulation dynamics between aquatic habitats in a terrestrial matrix. However, research into this dispersal process to date has focused on individual field sites or laboratory studies. We investigated the invertebrates dispersed by endozoochory by the lesser black-backed gull Larus fuscus wintering in Andalusia, south-west Spain in 2016–2017, comparing seven sites interconnected by their movements, with different degrees of anthropogenization [three landfills, two saltpan complexes, a natural lake, and a large (370 km2) ricefield area]. In the ricefields, we also compared invertebrates dispersed by gulls with those dispersed by the larger white stork Ciconia ciconia. A total of 642 intact invertebrates and their propagules (mainly plumatellid bryozoans, cladocerans, and other branchiopods) were recorded in excreta (faeces and pellets) from gulls and storks. A greater diversity and abundance of invertebrates were recorded in ricefields, notably 43 individuals of the alien snail Physella acuta. One snail was still alive in a gull pellet 3 weeks after being stored in a fridge. This represents the first record of snail dispersal within waterbird pellets. Viability was also confirmed for the cladoceran Macrothrix rosea recorded in ricefields, and the alien brine shrimp Artemia franciscana recorded mainly in saltpans. In ricefields, gulls and pellets had significantly fewer propagules and fewer taxa per gram of excreta than storks and faeces, respectively. Through their high mobility, gulls and storks can disperse invertebrates between different natural and artificial habitats, and even to landfills. They can promote metapopulation dynamics for native bryozoans and branchiopods, but also the spread of invasive snails and brine shrimp.

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

“…Insect eggs and aquatic snails also may be dispersed by epizoochory, as when corixids lay eggs on bird legs or snails crawl on birds (Carbonell et al, 2021; van Leeuwen & van der Velde, 2012). Alien aquatic snails are now known to be dispersed via endozoochory in regurgitated pellets as well as faeces (Martín‐Vélez et al, 2022). Tardigrades are another group with a widespread distribution that may partly be explained by dispersal through bird migration.…”

“…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).…”

“…In many genetic studies of aquatic plants and invertebrates, high levels of gene flow are detected which support an influence of bird movements. For example, van Leeuwen et al (2013) demonstrated high rates of genetic interchange for Spanish populations of the alien aquatic snail Physella acuta , for which waterbird endozoochory has since been confirmed (Martín‐Vélez et al, 2022). Martin et al (2020) found that the population structure of the gastropod Planorbella trivolvis suggested LDD along a migratory flyway.…”

“…Insect eggs and aquatic snails also may be dispersed by epizoochory, as when corixids lay eggs on bird legs or snails crawl on birds (Carbonell et al, 2021;. Alien aquatic snails are now known to be dispersed via endozoochory in regurgitated pellets as well as faeces (Martín-Vélez et al, 2022).…”

Even short‐distance dispersal over a barrier can affect genetic differentiation in Gyraulus, an island freshwater snail

“…LDD often requires vectors, such as other animals, wind, and ocean currents (Gillespie et al, 2012). In particular, other animals seem to be important vectors for LDD in freshwater molluscs, and there is experimental and observational evidence that many animals can be the vector for LDD by internal and external transport (e.g., Bespalaya et al, 2020; Green & Figuerola, 2005; Martín‐Vélez et al, 2022; Rees, 1965; van Leeuwen et al, 2012; van Leeuwen & van der Velde, 2012; Walther et al, 2008). However, because Chichijima Island is an oceanic island, the development of its fauna should have required time.…”