The Importance of Waterbirds As an Overlooked Pathway of Invasion for Alien Species

The importance of waterbirds as an overlooked pathway of invasion for alien species

Andy J. Green

Department of Wetland Ecology, Estación Biológica de Doñana-CSIC, Sevilla, Spain

Correspondence: Andy J. Green, Department of Wetland Ecology, Estación Biológica de Doñana-CSIC, Americo Vespucio s/n, 41092 Sevilla, Spain. E-mail: [email protected]

RUNNING TITLE Waterbirds as vectors of alien species

ARTICLE TYPE Biodiversity Viewpoint

ABSTRACT

The importance of waterbirds as vectors of aliens has been recognized since Darwin's time, yet research by pioneers has been forgotten during the development of modern invasion biology, which tends to overlook this means of dispersal. Waterbirds are ignored in databases of alien species and invasion pathways, making management and prevention of invasions more difficult. I summarize 22 studies that provide empirical evidence for the dispersal of alien plants and invertebrates by waterbirds in aquatic and terrestrial ecosystems, complementing 14 studies recently identified by Reynolds et al.

(2015). Together, these studies provide empirical evidence for the dispersal of 79 alien plant species and eight alien invertebrates by waterbirds, including some of the worst aquatic invaders and the most widely distributed alien terrestrial plant species.

Waterbirds known to be vectors include ducks, geese, swans, shorebirds, gulls, herons and rails. Aliens are usually dispersed after being ingested or becoming attached to plumage, bills or feet, but waterbirds also disperse alien species when making nests, when preying on other vectors such as fish, or even attached to leg rings. While waterbirds may have a trivial role in explaining the arrival of alien species to new continents, they have a vital role in spreading aliens around once they get there. Greater focus on the role of waterbird vectors is essential if management of invasions is to be effective, and I make proposals for future research.

Key words

Angiosperms, biological invasions, geese, gulls, invasion pathways, long-distance dispersal, non-indigenous species, seed dispersal, waterfowl, zoochory.

INTRODUCTION

Reynolds et al. (2015) provide a useful review of evidence that migratory waterbirds play an important and overlooked role in the dispersal of aquatic alien species, and show that they can transport plant and invertebrate propagules between locations at a variety of spatial scales. Based on a literature search, they identify 14 quantitative studies providing strong evidence that waterbirds disperse alien plants (both aquatic and terrestrial) and invertebrates both via their guts (endozoochory) and by carrying them on the outside on feathers, feet or beaks (ectozoochory or epizoochory). Reynolds et al.

(2015) argue convincingly that the role of migratory waterbirds as vectors in the spread of aliens has been underestimated in recent times, and needs to be taken more into account for us to understand what makes some species particularly invasive, and to enable us to manage alien species successfully. They make a plea for basic research to identify which alien organisms are dispersed by waterbirds, but at the same time they overlook existing historical and contemporary research which should be taken into account when planning future work and action.

In this paper I summarize additional studies not included in their review, and discuss the significance of this collective body of evidence for invasion biology. I consider important historical literature, and identify an additional 22 quantitative studies (Table

1), including 10 field studies and 12 laboratory experiments. I adopted a conservative approach when compiling this list (Table 1), which does not include numerous field studies where seeds of alien plants were found in waterbird guts or their faeces without assessing their viability. Nor did I include studies where zoochory was demonstrated in the native range of taxa that are alien elsewhere. For example, the Olive Olea europaea

3 is highly invasive in Oceania and its seeds are dispersed by gulls in its native range

(Calvino-Cancela 2011). Smooth cordgrass Spartina alterniflora is a widespread alien in the Pacific region and Europe, and its seeds were abundant on the outside of waterfowl in its native range (Vivian-Smith & Stiles 1994). Plants shown experimentally to survive gut passage in their native range include the water mint

Mentha aquatica (widespread alien in North America, Soons et al. 2008) and the water primrose Ludwigia peploides (widespread alien in Europe, de Vlaming & Proctor 1968).

Furthermore, I have not included experimental studies that lend indirect support to ectozoochory by waterbirds. Many recent studies of desiccation resistance of alien aquatic plants and invertebrates focus on their implications for dispersal by humans on boats or fishing gear (e.g. Havel et al. 2014, Bruckerhoff et al. 2015), but have obvious implications for the potential to disperse on the outside of birds, as recognized by

Ridley (1930, see below), Alonso & Castro-Díez (2012) and Águas et al. (2014).

Neither have I covered the ability of waterbirds to disperse alien microbes such as phytoplankton (Stoyneva 2015) or parasites of other organisms (e.g. by dispersing infected crustaceans that are intermediate hosts for alien fish parasites, Gagne et al.

2015).

HISTORICAL EVIDENCE FOR THE ROLE OF WATERBIRDS

The current perception is that empirical evidence for waterbird-mediated dispersal of aliens is rare (Reynolds et al. 2015), but this is partly because important historical

4 research has been largely forgotten, and ignored during the development of the modern field of invasion biology. Darwin (1859) recognized the importance of waterbirds as vectors in explaining the broad distributions of native aquatic plants and invertebrates.

Their role as vectors in the rapid spread of the Canadian pondweed Elodea canadensis in Europe was recognized by the 19th century American botanist Asa Gray who wrote

(in Ridley 1930): "As it occurred not only in streams, but isolated ponds and lakes, and succeeded in crossing the Channel, it seems almost certain that much of its migration was due to small pieces of it being carried by ducks, coots, moorhens or grebes". Elodea canadensis was first recorded in Europe in 1836 (in Ireland) and by 1861 had already spread to the United Kingdom, France, the Netherlands and elsewhere, despite its lack of seeds in the introduced range.

Ridley (1930) considered the role of birds in the spread of aliens at length. He considered that E. canadensis was dispersed as small fragments by ectozoochory, and found fragments to remain viable when left in open air for 23 h. Woodruffe-Peacock (in

Ridley) reported shooting ducks that had fragments on their backs or around their necks.

Ridley argued that ducks had a role in the worldwide distribution of common purslane

Portulaca oleracea and the balloon vine Cardiospermum halicacabum, through endozoochory. He also identified several locations in England where the alien waterfern

Azolla filiculoides probably arrived as fronds, spores or winter buds on the feet or feathers of moorhens or wildfowl.

Gillham (1956) identified gulls as major vectors of cereal grains and annual weeds to coastal islands, establishing oats Avena sativa and barley Hordeum vulgare at sites up to

12 miles away from the nearest source of these seeds. He identified seeds of 14 native

5 weeds in the regurgitated pellets of gulls, but cited five alien species he considered to be established in gull feeding grounds via pellets. He also demonstrated how the guano of gulls creates suitable habitats for alien and native weeds by increasing soil nutrient content (see also Rajakaruna et al. 2009). Gillham (1970) considered colonial waterbirds such as gulls and cormorants to be responsible for spreading alien annual plants of European origin such as nettles Urtica spp. and grasses Hordeum spp. around

Australia, New Zealand and South Africa.

In the 1960s, Vernon W. Proctor and coworkers carried out extensive experimental investigations of endozoochory by waterbirds, and included many alien taxa. De

Vlaming & Proctor (1968) showed that alien seeds could be retained in a viable state within guts of ducks and Charadriiformes (shorebirds) for up to 29 h. Proctor (1968) showed how viable seeds of alien plants can also be regurgitated from the gizzard of shorebirds after being retained for up to 152 h (Table 1), facilitating long-distance dispersal. Proctor (1964) also demonstrated that many crustaceans are readily dispersed by endozoochory, without focusing specifically on alien species.

Elton's (1958) pioneering work on biological invasions was largely forgotten by the time modern invasion biology took off in the 1990s (Simberloff 2011). In a similar manner, Ridley, Gillham and Proctor were pioneers whose classic works were carried out too early to influence the growth of modern research into invasion pathways and vectors.

ALL KINDS OF WATERBIRDS ARE VECTORS, FOR A WIDE VARIETY OF

ALIENS

It is likely that all kinds of waterbirds (sensu Wetlands International 2012) have an important role in the dispersal of alien as well as native species. When added to the contemporary studies providing evidence for dispersal of aliens by waterbirds reviewed by Reynolds et al. (2015), the additional 22 studies listed in Table 1 increase the diversity of alien plants and invertebrates for which a major role for waterbird vectors is supported, but also increase the diversity of their vectors.

Reynolds et al. found empirical support that 12 Anatidae species (11 ducks and one swan), four shorebird species and one coot act as vectors of 27 alien plant species

(including both terrestrial and aquatic species) and three aquatic invertebrate species. I have added five species of geese, two ducks, one rail, two herons, five gulls, three shorebirds and four seabirds to this list (Table 1). A combination of the present paper and Reynolds et al. (2015) provides direct evidence that 39 species of waterbirds are involved in dispersing 79 species of alien plants and eight species of alien invertebrates.

These figures are still likely to greatly underestimate the importance of waterbirds in dispersing aliens. The growing body of evidence for the importance of waterbirds as vectors for a diversity of native taxa (Green et al. 2013, 2016) strongly suggests they disperse alien species from similar taxonomic groups. For example, dispersal of native ostracods by waterbirds has been repeatedly demonstrated (Green et al. 2013), and they are considered highly likely to be involved in the spread of alien ostracod species (Valls et al. 2014).

WATERBIRDS DISPERSE ALIENS BY MULTIPLE MEANS

Reynolds et al. (2015) identified studies supporting endozoochory of alien plant seeds

(n = 6 studies), ectozoochory of alien plants (n = 2), endozoochory of alien crustaceans

(n = 2) and ectozoochory of alien invertebrates (n = 2). They also listed three studies of population genetics of alien invertebrates that support a major role for waterbirds as vectors. After adding 22 studies I have identified (Table 1), endozoochory of seeds has been supported for a total of 63 alien plant species, and ectozoochory for 15 plants (14 as seeds, plus duckweed fronds Lemna minuta) and eight aquatic invertebrates (three molluscs and five crustaceans). The additional studies of ectozoochory are of considerable significance, and include experimental evidence that waterbirds can spread the highly invasive crayfish Procambarus clarkii and zebra mussel Dreissena polymorpha (Table 1). Aliens can be dispersed not only on the feet, bills or feathers of birds, but even on the structures scientists use to study their movements, as shown for alien barnacles attached to the leg rings of gulls (Tøttrup et al. 2010). In yet another kind of external transport, alien plants are also dispersed when used as nest material by waterbirds (Morton & Hogg 1989).

This additional literature also diversifies the forms of endozoochory. Recent research on the New Zealand pigmyweed Crassula helmsii suggests that vegetative fragments of aquatic plants may disperse by endozoochory (Denys et al. 2014) as well as by ectozoochory. Indirect or secondary endozoochory also occurs, when predatory waterbirds disperse alien propagules that have been ingested by fish or other vertebrates, as shown for herons feeding on lizards that contain alien seeds (Rodriguez et al. 2007).

Waterbirds can only play a key role in biological invasions if some of the alien propagules they disperse become successfully established in the field. In some cases, waterbirds have been shown to actively contribute to the successful establishment of the alien plants they disperse, at the expense of native plants. Canada Geese Branta canadensis in British Columbia disperse alien grasses and forbs by endozoochory, and exclosure experiments showed that the geese are directly responsible for increasing cover of alien grasses through grazing (Best & Arcese 2009). Gulls change soil chemistry in a manner that facilitates the colonization of annual weeds that they themselves disperse by endozoochory (Gillham 1956).

IMPORTANCE OF THE AVIAN PATHWAY IN MANAGEMENT AND ALIEN

DATABASES

The recent boom in invasion biology research has focused on the consequences of human activity, whilst zoochory has been neglected. Spread of alien species by birds is one of the so-called “unaided” pathways by which aliens can undergo natural spread into new, neighbouring biogeographical or political regions. “Unaided” pathways have been underestimated in most analyses of invasion pathways (Hulme et al. 2008). The pathway of spread of alien plants and invertebrates into different countries is often listed as “unknown” (Hulme et al. 2008), and waterbirds may be responsible for many of these, including terrestrial plants (Table 1). An analysis for species on the NOBANIS database (http://www.nobanis.org/) shows that the mode of entry to Denmark is

9 unknown for the majority of alien angiosperm species (Madsen et al. 2014), and birds are likely to be involved in many of these cases.

Birds are typically overlooked as vectors for spread in the many databases of alien species, which tend to recycle information from one to another. The extent to which waterbird vectors are ignored is illustrated by the following examples. There is no mention of birds as vectors in the European Alien Species Information Network

(EASIN http://easin.jrc.ec.europa.eu) database for E. canadensis, A. filiculoides,

Crassula helmsii, Ludwigia spp. or Heteranthera spp., these all being taxa for which a role of waterbirds has been demonstrated. Nor is there any mention of birds for E. canadensis in the DAISIE database (http://www.europe- aliens.org/pdf/Elodea_canadensis.pdf). In the Global Invasive Species Database

(http://www.issg.org/database/welcome/), there is no mention of waterbirds in the introduction pathways or dispersal means listed for aquatic plants such as Potamogeton crispus, Myriophyllum spicatum or Ceratophyllum demersum, all of which were considered by Ridley (1930) to be waterbird-dispersed.

Parties to the Convention on Biological Diversity have agreed that, by 2020, invasion pathways will be identified, prioritized and managed to prevent the introduction of invasive alien species (CBD 2014a). However, this objective will be hindered by ignoring the role of waterbirds as vectors. Avian vectors are completely ignored in CBD’s own analysis of invasion pathways (CBD 2014b). The Invasive Alien

Species Pathway Management Resource (http://acronym.co.nz:8086/about.aspx) was developed to provide information on the identity of pathways and dispersal vectors, so

10 as to help to contain their further spread of invasive species. However, their database does not include "unaided" pathways such as avian vectors.

Waterbirds are being systematically overlooked as a pathway for further spread of alien species, and this is likely to seriously compromise management decisions. I suggest a change in approach is required, in which all available information on zoochory in the native or introduced range is integrated into alien databases. Managers should adopt the precautionary principle, assuming a role for birds for aliens from taxonomic groups with a general capacity for zoochory (particularly aquatic plants, crustaceans and mollusks), until empirical studies prove otherwise.

FUTURE RESEARCH PRIORITIES

Improving our understanding of the role of waterbirds in the spread of aliens and in determining invasiveness is a high priority and should be added to future challenges for invasion ecology that have recently been identified (Caffrey et al. 2014, Havel et al.

2015). There is a need for much more baseline identification of the alien organisms being dispersed by waterbirds in different parts of the globe (Reynolds et al. 2015), taking advantage of modern techniques such as metabarcoding of gut contents (Coghlan et al. 2013). This information should be integrated into studies of the movement ecology of waterbirds, and how this is being modified by global change (see Reynolds et al. for full discussion).

The ability of alien propagules to disperse by endozoochory should be tested with laboratory simulations of the effects of gut passage (Vazacova & Munzbergova 2013), just as the ability of seeds to stick to fur can be used as a predictor of invasion success

(Moravcová et al. 2015). Such laboratory tests of dispersal potential should be incorporated into risk assessments of potential invasiveness, and routinely added to alien databases. Comparative studies are a valuable approach to increase our understanding of the role of avian vectors, and the ability of alien taxa in a given area to disperse by waterbirds should be compared with the ability of native taxa from the same area. Among island floras in the Great Lakes, 85% of alien plants were adapted for dispersal by birds such as gulls, compared to only 54% of native species, suggesting that birds are a major invasion pathway (Morton & Hogg 1989). Similarly, among the flora of coral islands in the Great Barrier Reef frequented by gulls, 33% of alien plants were adapted for zoochory compared to 21% of native species (Heatwole & Walker

1989).

The ability of individual alien taxa to disperse by waterbirds should also be compared between the introduced and native range. Plants that are particularly invasive in the introduced range may be better adapted to zoochory than conspecific populations in the native range. Ridley (1930) reported that small stem fragments of E. canadensis grow much faster in the introduced than the native range. Germination performance can differ between native and alien populations of plants (Hirsch et al. 2012), and the response to gut passage might be more positive in the introduced range.

The spread of alien plants through time can be traced via herbarium records (e.g. Piya et al. 2013) or through citizen science (e.g. as monitored by the Early Detection and

Distribution Mapping System (https://www.eddmaps.org/), or can be retraced using genetic markers. These data should be related to waterbird movements to assess their role as vectors. Network models of vector movement as applied to human vectors or transport corridors (Hulme 2009) should be used to predict the spread of aliens along waterbird flyways.

The role of fish-eating birds as secondary vectors has hardly been addressed since

Darwin (1859) demonstrated that this is an important mode of plant dispersal, and warrants more study. The Cyprinidae and tilapia are major seed vectors (Boedeltje et al.

2015), as well as being widely introduced alien fish. The dispersal of alien plants by birds feeding on them is worthy of attention. For example, water hyacinth Eichhornia crassipes seeds are consumed and probably dispersed by carp in North America where both taxa are invasive (VonBank et al. 2014), and the seeds may be dispersed between catchments by piscivorous birds feeding on carp.

It is also it a research priority to determine to what extent multiple bird species are spreading the same alien taxon (Reynolds et al. 2015). In general, multiple vectors are to be expected (Table 1), and for terrestrial plants there can be considerable overlap between the roles of waterbirds and other birds. Terrestrial seeds often end up in water where they can be ingested by waterbirds and returned to terrestrial habitats (e.g. when defecated during flight). Waterbirds often forage, rest or nest in terrestrial habitats.

Many avian vectors may have contributed to making the sow-thistle Sonchus oleraceus the most widespread invasive plant on Earth (Essl et al. 2014). S. oleraceus is readily dispersed via endozoochory by ducks and shorebirds (Reynolds et al. 2015), is an important food item in its introduced range for herbivorous geese (Baldwin 1947) and is

13 probably also dispersed by ectozoochory like S. asper (Table 1). However, it is also dispersed by endozoochory by songbirds such as the bullfinch Pyrrhula vulgaris (W.E.

Collinge in Ridley 1930). Studying the combined effect of multiple avian vectors on the spread of alien species is probably essential to understand many past invasions and predict many future ones.

CONCLUSION

A broad range of waterbird taxa have a major role in the spread of alien species in aquatic, terrestrial, coastal and island ecosystems. There is an important body of historical and contemporary evidence that demonstrates this, and a diversity of dispersal mechanisms have been identified. Aliens that can be dispersed by waterbirds include some of the worst invasive species in Europe such as E. canadensis, C. helsmii, P. clarkii and D. polymorpha (http://www.europe-aliens.org/speciesTheWorst.do).

However, much more work is required to increase our understanding of how waterbirds contribute to biological invasions. Waterbirds are frequently ignored during the compilation of databases, risk assessments and horizon scanning initiatives. This must be corrected because, if management of alien species is to be effective, dispersal processes involving waterbirds must be fully taken into account. Several priorities for future research activities have been identified.

ACKNOWLEDGEMENTS

A previous version of this article was improved after helpful comments from Franz

Essl, Ádám Lovas-Kiss and anonymous referees.

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BIOSKETCH

Andy J. Green D.Phil. (Oxon) is Professor of Research at Doñana Biological Station

(https://www.researchgate.net/profile/Andy_Green2). He is interested in aquatic ecology and the functional role of waterbirds, as well as the ecosystem services they provide. He studies aliens such as Artemia francisana, Trichocorixa verticalis and

Palaemon macrodactylus. He investigates the co-dispersal of other organisms with birds in Europe, Australasia and North America.