Evaluating the potential for weed seed dispersal based on waterfowl consumption and seed viability

Farmer, Jaime Austin; Webb, Elisabeth B.; Pierce, Robert A.

doi:10.1002/ps.4710

Cited by 56 publications

(65 citation statements)

References 42 publications

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“…All seven of the agricultural weeds we recorded (Table ) are already known to have herbicide‐resistant populations (Heap, ). Herbicide‐resistant weeds reduce crop production and increase herbicide costs (Powles & Yu, ), and LDD of herbicide‐resistant genotypes via waterbirds is likely to exacerbate these problems (Farmer et al., ). Furthermore, two of the plants recorded are alien to Europe (Table ), and others are important aliens in other continents (Benedí & Orell, ; Pyšek et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…We compared propagules dispersed by gulls in pellets and faeces, because the latter are likely to be retained in the gut for longer, with more chance of undergoing LDD (Nogales, Medina, Quilis, & González‐Rodríguez, ). We also investigated whether taxa dispersed included alien species or agricultural weeds, whose dispersal by migratory birds may constitute an ecosystem disservice (Farmer, Webb, Pierce, & Bradley, ; Green et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Crayfish invasion facilitates dispersal of plants and invertebrates by gulls

et al. 2018

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The red swamp crayfish (Procambarus clarkii), originally from North America, is one of the world's worst aquatic invaders. It is a favoured prey item for waterbirds, but the influence of this novel predator–prey relationship on dispersal of other organisms has not previously been considered. We investigated the potential for dispersal of plants and invertebrates by migratory waterbirds feeding on alien P. clarkii in European ricefields at harvest time. In November–December of 2014–2015, we collected propagules from the outside of 13 crayfish captured as they moved out of ricefields during harvest in Doñana, south‐west Spain. We also collected excreta (N = 76 faeces, 14 pellets) of lesser‐black backed gull (Larus fuscus). We recorded diaspores from at least 11 plant species (161 seeds from 10 angiosperm taxa, and 14 charophyte oogonia) on the outside of crayfish, together with 54 eggs from eight aquatic invertebrate taxa. Adults and juveniles of at least nine microcrustaceans, including the alien ostracods Hemicypris reticulata and Ankylocythere sinuosa, were also recovered from crayfish. No intact propagules were present in the digestive system of the crayfish. Contents of regurgitated pellets confirmed P. clarkii as the main food item for gulls. Diaspores from at least 12 plant species (154 seeds from 11 angiosperm taxa, and 17 charophyte oogonia) were recovered from gull excreta, together with 129 eggs of 12 aquatic invertebrate taxa. A statoblast of the alien bryozoan Plumatella vaihiriae was found in gull faeces. Seven of the plant species are important agricultural weeds, and two are alien to Spain. Diaspores from six plant taxa were germinated, confirming viability. These propagules were from a similar set of plants and invertebrates to those found on the outside of crayfish, suggesting that propagules in gull excreta were ingested inadvertently with their crayfish prey. Ricefields constitute a major artificial aquatic habitat covering an increasing proportion of the world's land surface and typically support native or alien crayfish. Crayfish invasion can lead to novel secondary dispersal pathways for plants and invertebrates through interactions with their predators, promoting the expansion of alien and native species (including weeds) through long‐distance dispersal via migratory waterbirds and increasing connectivity of organisms between artificial and natural ecosystems. This represents a previously overlooked impact of crayfish invasion on ecosystem services.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Crayfish invasion facilitates dispersal of plants and invertebrates by gulls

et al. 2018

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“…In this study, we assess the role of seed traits on their survival and retention time during passage through the mallard digestive tract. Mallards are one of the most numerous and widely distributed waterbird species of the Holarctic region and are good vectors for LDD (Farmer et al, ; Kleyheeg et al, ; Soons et al, ). We aimed to tease apart the relative importance of seed size, hardness, water permeability, and shape, while controlling for the effect of phylogenetic relatedness.…”

Section: Introductionmentioning

confidence: 99%

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

Lovas‐Kiss

Vincze

Kleyheeg

et al. 2020

Ecology and Evolution

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Field studies have shown that waterbirds, especially members of the Anatidae family, are major vectors of dispersal by endozoochory for a broad range of plants lacking a fleshy fruit, yet whose propagules can survive gut passage. Widely adopted dispersal syndromes ignore this dispersal mechanism, and we currently have little understanding of what traits determine the potential of angiosperms for endozoochory by waterbirds. Results from previous experimental studies have been inconsistent as to how seed traits affect seed survival and retention time in the gut and have failed to control for the influence of plant phylogeny. Using 13 angiosperm species from aquatic and terrestrial habitats representing nine families, we examined the effects of seed size, shape, and hardness on the proportion of seeds surviving gut passage through mallards (Anas platyrhynchos) and their retention time within the gut. We compiled a molecular phylogeny for these species and controlled for the nonindependence of taxa due to common descent in our analyses. Intact seeds from all 13 species were egested, but seed survival was strongly determined by phylogeny and by partial effects of seed mass and hardness (wet load): species with seeds harder than expected from their size, and smaller than expected from their loading, had greater survival. Once phylogeny was controlled for, a positive partial effect of seed roundness on seed survival was also revealed. Species with seeds harder than expected from their size had a longer mean retention time, a result retained after controlling for phylogeny. Our study is the first to demonstrate that seed shape and phylogeny are important predictors of seed survival in the avian gut. Our results demonstrate that the importance of controlling simultaneously for multiple traits and relating single traits (e.g., seed size) alone to seed survival or retention time is not a reliable way to detect important patterns, especially when phylogenetic effects are ignored.

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“…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.…”

Section: Introductionmentioning

confidence: 99%

“…A broad range of aquatic and terrestrial plant species benefit from this by dispersing via the guts of waterfowl (Figuerola and Green, (2002); Leeuwen, Velde, et al, 2012;Lovas-Kiss et al, 2018;Soons, Brochet, Kleyheeg, & Green, 2016;Kleyheeg, Klaassen, & Soons, 2016;Farmer, Webb, Pierce, & Bradley, 2017). Recent mechanistic models predicting dispersal patterns shaped by migrating waterfowl (Soons, Vlugt, Lith, Heil, & Klaassen, 2008; and resident waterfowl (Kleyheeg et al, 2017) have highlighted the importance of variation in seed gut passage survival and retention time for the outcome of dispersal events.…”

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confidence: 99%

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

Kleyheeg

Nolet

Otero-Ojea

et al. 2018

Ecology and Evolution

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Many plants and invertebrates rely on internal transport by animals for long‐distance dispersal. Their dispersal capacity is greatly influenced by interactions with the animal's digestive tract. Omnivorous birds adjust their digestive tract morphology to seasonally variable diets. We performed feeding trials in waterfowl to unravel how changing organ size, in combination with seed size, affects dispersal potential. We subjected captive mallards to mimics of summer (animal‐based), winter (plant‐based), and intermediate diets, and analyzed gut passage of seeds before and after the treatment (trials 1 and 2). To test the effect of gut morphology on seed digestion, we measured digestive organ size after euthanasia. Three hours before euthanasia, differently sized seeds were fed to test how seed size affects gut passage by determining their relative position in the digestive tract (trial 3). Trials 1 and 2 showed that intact seed passage was lower in the plant‐based than in the animal‐based diet group. Retention time changed only within groups, decreasing in the animal‐based, and increasing in the plant‐based diet group. No post‐diet differences in organ size were detected, probably due to large between‐individual variation within groups. Digestive tract measures did not explain variation in seed survival or retention time. Trial 3 revealed that small seeds pass the digestive tract rapidly, while large seeds are retained longer, particularly in the gizzard. Differential retention in the gizzard, the section where seeds can be destroyed, is likely why larger seeds have a lower probability to pass the digestive tract intact. Our results confirm that rapid, flexible adaptation to diet shifts affects seed digestion in waterfowl, although we could not conclusively relate this to organ size. Large interindividual variation in digestive efficiency between mallards feeding on the same diet may provide opportunities for seed dispersal in the field throughout the annual cycle.

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Evaluating the potential for weed seed dispersal based on waterfowl consumption and seed viability

Cited by 56 publications

References 42 publications

Crayfish invasion facilitates dispersal of plants and invertebrates by gulls

Crayfish invasion facilitates dispersal of plants and invertebrates by gulls

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

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

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