Darwin’s Digestion Myth: Historical and Modern Perspectives on Our Understanding of Seed Dispersal by Waterbirds

Abstract

Internal transport (endozoochory) and external transport (epizoochory) by migratory waterbirds are key mechanisms of long-distance dispersal for seeds and other diaspores of plants lacking a fleshy fruit. Beginning with Darwin in 1859, we review how opinions about the relative importance of epizoochory and endozoochory have changed repeatedly over time and how this allows us to reassess our modern understanding of plant dispersal. Darwin was mistaken in asserting that diaspores cannot survive passage through the gut of waterbirds or other granivorous birds. This “digestion myth” led him to underestimate endozoochory and overstate the importance of epizoochory, an approach which is echoed throughout the literature until the present day. Darwin also focused on aquatic plants, yet it is now clear that waterbirds are also major vectors of terrestrial plants. Based on their empirical observations and experiments, other less influential scientists (notably Hesselman in 1897, Guppy in 1906 and Proctor in the 1960s) argued that endozoochory is the more important mechanism for waterbirds. Modern field and experimental studies demonstrate the dominant role for endozoochory. Unfortunately, avian endozoochory of dry-fruited plants continues to be ignored as a dispersal mechanism by many plant ecologists, which we attribute to Darwin’s continuing influence. However, this endozoochory has major implications for plant biogeography and requires wider recognition and research.

1. Introduction

Dispersal can be seen as one of the fundamental processes in ecology [1]. Seed dispersal underlies a range of vital ecological and evolutionary processes in plant populations and communities [2]. As Schaefer and Ruxton [3] pointed out, ‘dispersal is a fundamental life-history process… seeds are not self-powered and almost exclusively rely on some external agent to provide transport’. The dispersal of plant diaspores (seeds, spores and other propagules) and invertebrates by birds occurs both when they are transported internally, if they are ingested and they survive gut passage (known as “endozoochory”), and/or when they are transported externally when attached to feathers, feet or bills (variously known as “ectozoochory”, “exozoochory” or “epizoochory”). Both types of dispersal interaction can occur simultaneously in the same bird and plant populations [4,5,6]. There has been growing interest in recent years in the role of migratory waterbirds (i.e., birds ecologically dependent on wetlands sensu [7]) as dispersal vectors of plants and aquatic invertebrates [8,9]. The most intensively studied groups of waterbirds are the waterfowl (Anatidae, i.e., ducks, geese and swans) and shorebirds (Charadriiformes), but other waterbirds such as Ciconiiformes (storks, ibis and spoonbills) or Laridae (gulls and terns) are also important dispersal vectors [8].

In 1859, Darwin [10] saw migratory waterbirds and their ability to disperse plants and invertebrates as a vital explanation for the extensive distributions of many aquatic species and incorrectly thought that endozoochory only applied to a few specialized types of seeds (termed ‘Darwin’s digestion myth’ in this paper). While Darwin’s contributions to evolutionary biology are monumental, his views on seed dispersal by waterbirds have led to persistent myths. This paper seeks to unravel these myths by examining historical and contemporary evidence. A correct understanding of the role of waterbirds in long-distance dispersal (LDD) is now even more important under rapid global change and the spread of alien species. Recent work has underlined the extensive capacity of angiosperm seeds to survive gut passage, and identified a wide range of plant taxa undergoing endozoochory by migratory waterbirds [11,12]. Modelling based on experimental data and ringing recoveries as well as GPS tracking has emphasized the long distances over which ducks and geese can disperse angiosperm seeds by endozoochory [13,14]. In contrast, recent studies of waterbird epizoochory have usually focused on diaspores of other organisms such as diatoms or bryophytes [15,16].

Importantly, there has been no consideration in the recent literature of the history of research into plant dispersal by waterbirds and how and why our understanding of this process has itself developed over time and, to some extent, gone in circles. Biologists sometimes effectively “reinvent the wheel” by reaching conclusions while in ignorance of earlier work that has already covered the same ground. For these reasons, the history of the subject is important, and it also gives us perspective and allows us to see how current research fits into the wider ‘scheme of things’ [17]. As we demonstrate below, there has been a long-standing and rather polarized debate between advocates of epizoochory on the one hand and advocates of endozoochory on the other, which to some extent continues to the present day. This review provides a good example of how our views as biologists can be strongly conditioned by opinions expressed by famous pioneers (particularly Darwin), even when later research (often overlooked) has shown these opinions to be mistaken.

In this review we concentrate on dispersal of plants, as far more attention has been paid historically to them, but the “inside or outside” debate (i.e., “endo- or epizoochory”) applies equally to invertebrates or free-living microorganisms [9]. Herein, we are not dealing with the dispersal of plants with fleshy fruits by terrestrial vertebrates, which strongly dominates the modern literature on endozoochory [2], even to the extent where it is sometimes wrongly assumed that only such plants undergo endozoochory [18,19]. On the other hand, we are concerned with the dispersal of terrestrial as well as aquatic plants, since both are dispersed by waterbirds [11,12]. This paper aims to reassess the role of endozoochory in seed dispersal by waterbirds, challenging the long-standing misconceptions rooted in Darwin’s early assertions. We ask how did a misconception from Darwin’s era shape over a century of ecological research on seed dispersal?

2. Methodology

Below, we review the history of ideas about plant dispersal from the early work by Darwin up to the present day. As scientists writing about history for publication in a scientific journal that is primarily to be read by other scientists, we naturally tend to emphasize those studies more relevant to current understanding—an approach that differs from that of many historians writing about science [20]. Table 1 provides an overview of our major findings by summarizing key publications in chronological order.

Not all important early work was published in English. This was particularly the case before the rise of English as a global scientific language, starting around the 1930s [21]. In this paper, we have made every effort to identify and include historical publications not written in the English language, but it remains possible that we may have overlooked some important literature, especially away from the main European languages. We did not conduct a systematic electronic literature search, as this would not be reliable for historical literature of previous centuries. Rather, we base our review on many years of reading classical works and retracing earlier citations whenever possible. In some cases, we were unable to locate primary sources of historical literature and quote secondary sources where necessary.

Table 1. Chronological summary of some key research on plant dispersal by waterbirds discussed in this paper, with an emphasis on influential books and key papers. From Darwin onwards, dispersal is discussed in an evolutionary context (although prior to the First World War not necessarily in the context of natural selection). Many other studies are discussed in the text.

Date	Scientist	Description	Reference
1859	Charles Darwin	Darwin favoured epi- rather than endozoochory because he assumed seeds were destroyed during gut passage (called ‘Darwin’s digestion myth’ in this paper). He described early experiments into zoochory.	[10]
1898	William Beal	Reinforced Darwin’s digestion myth in an influential book on plant dispersal.	[22]
1906	Henry Guppy	Favoured endozoochory and showed gut passage can increase germination of pondweeds.	[23]
1914–1918		First World War forms a dividing line between the early work of the long 19th Century and later 20th century studies.
1930	Henry Ridley	Major book on plant dispersal recognized both epi- and endozoochory.	[24]
1959–1968	Vernon Proctor	Series of papers, first on algae and liverworts, later on flowering plants, demonstrated experimentally the importance of endozoochory and its potential for long-distance dispersal (LDD).	Two key papers in Science. [25]—on algae. [26]—on flowering plants.
1966	Robert Cruden	Argued that only epizoochory of seeds can provide LDD for plants	[27]
1967	Sherwin Carlquist	Suggested both epi- and endozoochory are important for colonization of oceanic islands.	[28]

Table 1. Chronological summary of some key research on plant dispersal by waterbirds discussed in this paper, with an emphasis on influential books and key papers. From Darwin onwards, dispersal is discussed in an evolutionary context (although prior to the First World War not necessarily in the context of natural selection). Many other studies are discussed in the text.

Date	Scientist	Description	Reference
1859	Charles Darwin	Darwin favoured epi- rather than endozoochory because he assumed seeds were destroyed during gut passage (called ‘Darwin’s digestion myth’ in this paper). He described early experiments into zoochory.	[10]
1898	William Beal	Reinforced Darwin’s digestion myth in an influential book on plant dispersal.	[22]
1906	Henry Guppy	Favoured endozoochory and showed gut passage can increase germination of pondweeds.	[23]
1914–1918		First World War forms a dividing line between the early work of the long 19th Century and later 20th century studies.
1930	Henry Ridley	Major book on plant dispersal recognized both epi- and endozoochory.	[24]
1959–1968	Vernon Proctor	Series of papers, first on algae and liverworts, later on flowering plants, demonstrated experimentally the importance of endozoochory and its potential for long-distance dispersal (LDD).	Two key papers in Science. [25]—on algae. [26]—on flowering plants.
1966	Robert Cruden	Argued that only epizoochory of seeds can provide LDD for plants	[27]
1967	Sherwin Carlquist	Suggested both epi- and endozoochory are important for colonization of oceanic islands.	[28]

3. Early Perspectives on Dispersal: The Pre-Darwinian Context

Explaining how organisms disperse between different locations has been a significant problem for understanding the natural world for centuries. In the cultural context of early modern Europe, if a literal reading of the biblical account was accepted (many scholars often had a more nuanced view of the bible), then all organisms must have dispersed to their current locations from Mount Ararat in Turkey. The late 15th century ‘discovery’ of the Americas with their unrecognizable flora and fauna by Europeans, made these dispersal events much more problematic—as did the ever-increasing knowledge of the world’s geography and biota during the following three centuries [29,30]. This is a period that is often considered to mark the invention of modern looking science, especially in the 17th century, a period often referred to as ‘The scientific revolution’ [31,32]. In the aftermath of this revolution, more naturalistic explanations became increasingly common. For example, Georges Leclerc, the comte de Buffon, was a major figure in enlightenment natural philosophy. Rudwick ([33], p. 141) nicely summarized his approach: ‘Without being openly atheistic, Buffon had simply redefined the scope of the natural sciences in such a way that divine action was marginalized’. However, even without the link to biblical literalism and Mount Ararat, Buffon’s ideas still envisaged organisms migrating around the world over geological time [29]. This problem of dispersal did not feature as prominently in all pre-Darwinian theories. For example, in the 1830s, the geologist Charles Lyell envisaged species coming into existence wherever the climate was right for them—although there was also some dispersal suggested in Lyell’s writings too. However, his views about species coming into existence wherever the climate was correct were viewed as rather odd by most of his contemporaries because they were linked to the idea that there was a lack of any directional change in conditions on Earth over geological time [34,35].

Two other important 19th-century ideas made understanding the dispersal of apparently immobile organisms such as plants particularly important. During the late 1830s, ideas of widespread ice ages in the geologically recent past started to achieve prominence [36]. This obviously implied that some flora, such as that of northern Europe or Canada, must have colonized following the retreat of the ice. In addition, the ideas on evolution by natural selection that were published mid-century, associated particularly with Darwin and Wallace, implied species evolved at a particular location from which they would have to disperse to other parts of the globe if they were to expand their ranges.

The Special Case of Aquatic Habitats as Ecological Islands

There are two obvious situations in which dispersal becomes a particularly prominent problem, namely the colonization of real islands and of habitat islands such as water bodies surrounded by land that provide a habitat hostile to aquatic species. This is particularly obvious in the colonization of newly created ponds [37,38,39]. Aquatic plants provide an obvious problem because of their inability to move unaided, and because submerged and floating plants have no obvious capacity for wind dispersal. There is a long history of discussions about the potential role of waterbirds in the dispersal of aquatic and terrestrial plants—along with the passive dispersal of microorganisms such as diatoms and small aquatic invertebrates without a flying stage in their life history (see [9] for a review of recent research).

4. Darwin and His Powerful Influence

4.1. What Darwin Said

Charles Darwin was especially prominent in developing ideas on dispersal in an evolutionary context during the second half of the 19th century. Darwin’s ideas on evolution envisaged species having an origin at a particular point in both time and space and so created similar problems for dispersal to those raised by the biblical dispersal from Mount Ararat. This is illustrated by a letter from Darwin to the American geologist and zoologist J. D. Dana (29 September 1856), where he wrote that his developing ideas on a ‘single points of creation’ of species gave him real problems when it came to their dispersal, writing ‘No facts seem to me so difficult as those connected with the dispersal of Land Mollusca. If you ever think of, or hear of, any odd means of dispersal of any organisms I should be infinitely obliged’ [40]. Clearly dispersal was of great importance to Darwin’s key theoretical ideas and he was particularly interested in the role of migratory waterbirds in passive dispersal because of their long-distance movements and capacity to disperse propagules between land masses. In his chapters on geographical distribution in “On the origin of species”, Darwin [10] repeatedly referred to the contrast in range size between aquatic and terrestrial genera and attributed this principally to the capacity of aquatic plants and invertebrates to disperse passively using migratory waterbirds as vectors—see [41] for alternative explanations. Darwin’s use of plant distributions to infer dispersal by birds has been very influential in the literature ever since, a particularly good example being offered by Cruden [28], in which five shorebird species are identified as likely vectors for terrestrial and marsh plants with disjunct distributions between North and South America based on their migration routes, but in the complete absence of direct evidence of diaspore transport.

Furthermore, Darwin [10] effectively initiated a debate on the relative importance of endo- and epizoochory that has attracted strong opinions on both sides to this day (note, these terms for internal and external transport were not in widespread use prior to van der Pijl [42]). Darwin wrongly assumed that ducks and other granivorous birds destroy most of the diaspores they ingest during the digestive process: “I have never seen an instance of nutritious seeds passing through the intestines of a bird” ([10] Darwin, 1859, p. 361). In other words, he considered non-frugivorous birds such as waterbirds to be exclusively “seed predators” and not “seed dispersers” [43]. Nevertheless, Darwin did not dismiss endozoochory as an important process and recognized that hard seeds from fleshy fruits (e.g., berries) could survive the intestinal tract of frugivorous birds.

We can speculate that Darwin wrongly assumed that nutritious diaspores would not survive gut passage through an animal that intentionally ingested them, because he would not see an adaptive explanation for how such diaspores would be egested before completing digestion. The explanation for why a large proportion of diaspores survive gut passage lies in the diminishing returns of retaining food in the gut for longer periods and the greater energetic intake rate of birds constrained by gut volume and ingesta mass when they ingest continuously and digest inefficiently [8,44,45].

Because Darwin believed conventional endozoochory to be impossible due to complete digestion of seeds, he proposed indirect or secondary dispersal involving predation of granivorous birds (he seems to particularly have had in mind ducks and pigeons) by birds of prey. These raptors would scatter seeds from the crop of their prey as they fed on them [46] or ingest them and then retain them in their own upper gut, later expelling them in regurgitated pellets, thus completing dispersal [47]. Darwin reported experiments showing that seven types of cultivated seeds germinated after spending 12–21 h in the stomachs of birds of prey. His views on this topic appear to have remained unchanged for the rest of his life, as the text describing endozoochory remains unchanged from the first edition of “The Origin” [10] to the 6th edition published in 1872 [48], which was the last edition personally revised by Darwin. However, in nature, such secondary endozoochory by predatory birds is likely to be much rarer than endozoochory by the granivorous bird itself, and repeated studies have since shown that a high proportion of diaspores can survive passage through the entire waterbird gut ([49,50,51,52], see Figure 1).

Darwin also proposed that piscivorous birds had a major role in diaspore dispersal via secondary endozoochory, by ingesting fish after they have consumed diaspores and expelling the diaspores elsewhere. He reported on further experiments: “I forced many kinds of seeds into the stomachs of dead fish, and then gave their bodies to fishing-eagles, storks and pelicans; these birds after an interval of many hours, either rejected the seeds in pellets or passed them in their excrement: and several of these seeds retained their power of germination. Certain seeds, however, were always killed by this process”. Darwin mentioned that the seeds of a water lily (probably Nelumbo lutea) were found in the stomach of a heron, and that these seeds within a fish’s stomach may be dispersed indirectly by herons, either in their pellets or spilling them when feeding young at the nest. The role of secondary dispersal by piscivorous birds has received little further attention from researchers until recently [53,54,55].

In the ‘Origin’, Darwin [10] considered that these endozoochory events had a range limited by the finite retention time in the gut, writing “These means would suffice for occasional transport across tracts of sea some hundred miles in breadth, or from island to island, or from a continent to a neighbouring island, but not from one distant continent to another”. For LDD such as that required to reach oceanic islands, he favoured epizoochory and specifically the transport of diaspores within mud stuck on feet and beaks (see Figure 2). He particularly had in mind shorebirds, which are frequent visitors to oceanic islands. In a later edition of the ‘Origin’ [48], he reported germinating a seed of toad rush Juncus bufonius removed from mud attached to the leg of a woodcock, Scolopax rusticola. Darwin [10] also cited ducks and herons as likely to transport snails on their feet and noted how such epizoochory in mud is more likely for smaller propagules. As will be apparent from this summary of his work, a key feature of Darwin’s approach to the question of dispersal was the use of simple experiments. Indeed, Mayr ([30], p. 447) wrote that Darwin ‘was the first to approach these problems by ingenious experiments that showed that the dispersal power of organisms, particularly of plant seeds, is much greater than previously believed’. We are now so familiar with such an experimental approach in whole organism biology (for example, both authors of this paper were influenced as young scientists by the experimental tradition in behaviour developed by Niko Tinbergen and his students) that it is easy to forget how novel it was at the time Darwin was performing this work. Indeed, Richards [56] has argued that experiments played an important and underappreciated role in Darwin’s thinking.

4.2. Other Pioneers from the Nineteenth Century

Not surprisingly, given his prominence, the emphasis that Darwin [10] placed on epizoochory appears to have had a strong influence on biologists interested in diaspore dispersal later on and to the present day. When referring to the importance of waterbirds as vectors in aquatic systems, this has been summarized as “the proverbial duck’s foot” [57]. What could be termed the “digestion myth” (i.e. that ducks and other waterbirds destroy all diaspores ingested as food items) was also reiterated 40 years after publication of the “Origin” by the influential American botanist William. J. Beal [22] in his 1898 book on plant dispersal. Beal emphasized the importance of epizoochory, stating that ducks disperse buds of bladderwort Utricularia vulgaris on their legs and feathers, and that ducks and herons disperse “seeds of water plantain, sedges, grasses, rushes, docks, arrowhead, pondweeds, duckweed, cat-tail flag, bur reed, bladderwort, water crowfoot, and many others on their feet, beaks or feathers from one pond, lake, or stream, to another”. In contrast, he foresaw no role for endozoochory on the basis of his mistaken view that seeds lose their viability during gut passage and claimed that “Kerner von Marilaun fed seeds of 250 species of plants to duck” (as well as various terrestrial birds and mammals), finding that “no seed was found to germinate after passing through the duck”.

In fact, Kerner von Marilaun’s 1894 book [58] is miscited by Beal, who did not summarize his results in their entirety. According to Kerner von Marilaun, he found that ‘ducks’ (presumably domestic mallards Anas platyrhynchos) destroyed seeds in the gizzard under undefined “ordinary conditions”, but in contrast, “when food was forcibly administered to the hen and to ducks, so that their crops must have been overloaded, a few seeds still possessed the power of development”. Those seeds included thyme-leaved sandwort Arenaria serpyllifolia, field poppy Papaver rhoeas, flixweed Sisymbrium Sophia, redcurrant Ribes rubrum, privet Ligustrum vulgare and wild strawberry Fragaria indica. Contrary to Beal’s interpretation, modern research ([50,53,59], Figure 1) shows that these latter results are more indicative of what happens in natural conditions than the results from the so-called “ordinary conditions”. The proportion of seeds that survive gut passage varies between species, but also within species according to diet and individual and seasonal variation [9,51,60].

Nevertheless, Kerner von Marilaun [58] placed much more emphasis on epizoochory, reporting that Hydrocharis and Utricularia buds stick to waterbird feathers, whereas entire plants of Lemna or Riccia attach to ducks and coots and are so moved between lakes (see Figure 3). He reported diaspores of many aquatic genera to have the capacity to stick to feathers when floating at the water surface without the assistance of sticky mud, whereas other genera were reported as sticking in mud to herons, snipe and terrestrial birds visiting the shoreline. Whereas Darwin [10] germinated 537 plants from 190 g (dry mass) of mud collected from a pond, mud removed by Kerner von Marilaun from “swallows, snipe, wagtails and jackdaws resulted in about half as productive a yield of fertile seeds”. Kerner von Marilaun listed 21 species “found most frequently in the mud taken from birds”, including two Cyperus, three Juncus and three Nasturtium species, plus floating sweet-grass Glyceria fluitans, hair grass Eleocharis acicularis and sea clubrush Bolboschoenus (Scirpus) maritimus.

It remains unclear what methods were used in these early studies of epizoochory and whether there may have been contamination from soil containing seeds if birds were shot for collections. Modern studies have usually failed to find high concentrations of seeds on external parts of birds ([4,5,61], but see [6]).

Alfred R. Wallace wrote extensively about the biogeography and dispersal of different organisms. Although he did not himself pay detailed attention to diaspore dispersal by waterbirds, in several publications he suggested that diaspores are often dispersed to oceanic islands in mud on the feet of shorebirds (citing Darwin, [62,63]). In 1895 Wallace [63] also suggested that albatrosses, petrels and puffins disperse diaspores that become attached to their feathers when nesting in vegetation or in burrows.

In contrast to the previous authors, Henrick Hesselman [64] proposed that endozoochory by waterfowl is more important than epizoochory, based on the scarcity of diaspores he observed on the outside of birds and his observation of diaspores in an intact state in the gizzards of birds collected near Stockholm. He observed seeds of 12 genera in the guts of teal Anas crecca and mallard, with large numbers of Carex and Eleocharis. Likewise, in 1900 Holmboe [65] recognized the potential for endozoochory and identified numerous seeds in the gizzards of individuals of the water rail Rallus aquaticus, the Anatidae Anas crecca, Aythya fuligula and Cygnus bewickii and the great-crested grebe Podiceps cristatus.

At the close of the century, the geologist Clement Reid [66] reviewed what was known about the origin of the British flora following the retreat of ‘Ice Age’ ice. He was very interested in plant dispersal—devoting a whole chapter to the topic. In the context of aquatic plants, he suggested that shorebirds were probably particularly important for the dispersal of both seeds and fragments of living vegetation. In this context, he was clearly considering mainly epizoochory. However, like Kerner von Marilaun [58] and Wallace [62], Clement Reid recognized the importance of endozoochory by terrestrial frugivorous birds such as pigeons for plants with fleshy-fruits.

Plant ecology started to develop as a distinct discipline in the late 19th century [67]. The two most influential books from these early years were Schimper in 1898 [68] and Warming ([69]—The first edition was published in 1895 but in Dutch and so little read. Its influence was mainly through German translations followed by the 1909 English second edition). Neither of these books say much about seed dispersal, apart from passing comments about the role of wind, water and birds. The exception to this generalization is a short section on water dispersal in [68]. So, unlike the case with biogeographers, it appears that dispersal, in general, was of limited interest in early plant ecology, which at the time had a strong emphasis on community ecology, as shown by Warming’s and Schimper’s books.

5. Pioneers of the Twentieth Century

5.1. Henry Guppy

Like Hesselman [64], in 1906 Henry Guppy [23] also assigned a major and dominant role to endozoochory. He reported an experiment in which he fed a domestic duck with broad-leaved pondweed Potamogeton natans diaspores and recovered many from feces, of which 60% germinated the following spring, compared to only 1% of control seeds that had not been fed to the duck. He noted that some seeds took at least 7–8 h to pass through the gut. Furthermore, he removed numerous diaspores of Sparganium, Potamogeton and Cyperaceae from the gizzard and intestines of 13 wild ducks and found them to germinate quickly. He attributed the broad distribution of aquatic and semi-aquatic genera such as Najas, Potamogeton, Sparganium, Polygonum, Ranunculus, Ceratophylum and Ruppia to endozoochory by ducks and coots. He stated that “ducks, coots, and other water birds might often be characterized as “travelling germinators”. He cited an earlier experiment by Caspary (originally reported by Schenck [70]) in which seeds of water-lilies were fed to domestic ducks and were totally destroyed during gut passage. However, he argued that the seeds of Nuphar and Nymphaea are atypical (presumably owing to their large size) and not comparable to the smaller diaspores of other aquatic plants more suitable for endozoochory. This view is supported by recent literature [71].

Guppy [23] paid little attention to the role of mud and dismissed Kerner von Marilaun’s [58] suggestion that water alone would be sufficient to bind aquatic diaspores to plumage on the basis that water would dry out quickly during flight. After finding experimentally that Lemna minor, L. gibba and Spirodela polyrhiza do not survive exposure to dry air for 24 h, he concluded that, bearing in mind the much faster desiccation due to airflow during flight, waterbirds would not disperse duckweeds as whole plants over long distances, e.g., to islands. Although he was primarily concerned with the arrival of plants to Pacific islands (and was cited in this context for water dispersal of seeds by Schimper [68]), he was much less supportive of a role for epizoochory than more recent authors such as Carlquist [27].

In contrast, Guppy made the interesting point that waterbirds are particularly likely to disperse the diaspores of those plants they use to make their nest (a form of synzoochory), citing the example of how geese, ducks, gulls, and other birds use Leptinella (Cotula) plumosa (Asteraceae) in the Kerguelen Islands for making their nests. As pointed out by Hesselman [64] in the case of gulls, the transport of nest material to the nest itself can achieve dispersal when diaspores are included. In an 1915 English-language botany textbook with a pronounced ecological emphasis, Woodhead [72] discusses endozoochory in the context of herbivorous mammals dispersing seeds and birds feeding on edible fruit but also points out that ‘birds sometimes carry seeds great distances in mud adhering to their feet’.

Dividing a historical account into centuries is somewhat arbitrary. Indeed, some science historians suggest that the First World War makes a more natural break point (marking the start of the so-called ‘short twentieth century’) for considering recent history [73]. At the start of this period, Arber [74] emphasized the lack of direct evidence up to that date for dispersal of aquatic plants by waterbirds but advocated the role of epizoochory, especially of vegetative fragments. She reported that Duval-Jouve [75] observed fragments of 12 species, including Alisma, Glyceria and Juncus on the feet and feathers of waterbirds. She repeated the “digestion myth” when claiming incorrectly that for floating plants “their seeds and fruits would be digested and destroyed if eaten by birds” (see, e.g., [53] for endozoochory of Lemna seeds). She reported how Weddell [76] (pre-dating Darwin) observed a tiny and then unknown floating plant on the feathers of a waterbird in Brazil (“Camichi”, which is the Horned Screamer Palamedea cornuta according to Maximilian [77]). Weddell described this new species as Wolffia brasiliensis, and these tiny duckweeds (the smallest of all angiosperms, less than 1 mm across) can also be dispersed by endozoochory [78].

5.2. Henry Ridley

Henry Ridley [24] paid unprecedented detail to the role of different birds as diaspore vectors in his classic 744 page book on plant dispersal published in 1930. He was aware of the great capacity of Anatidae for both epizoochory and endozoochory and the capacity of diaspores to survive gut passage in these birds. He provided extensive lists of diaspores recorded in the guts of Anatidae and implied that he expected many of them to have the capacity to survive digestion. He noted their potential for the spread by endozoochory of alien terrestrial plants such as common purslane Portulaca oleracea. Ridley [24] also considered other waterbirds, such as rails, to be plant vectors by endozoochory. For example, he proposed that the fleshy red disc in which the stony black achenes of Scleria sumatrensis (Cyperaceae) are supported is an adaptation to visually attract birds such as rails. Nevertheless, different sections in his book are somewhat contradictory, and elsewhere he apparently accepted Darwin’s predation prerequisite for endozoochory: “They [ducks] are often attacked and torn to pieces by large falcons, eagles and foxes, so that the seeds they have swallowed may be scattered far from where they picked them up”. Confirming his ambiguity regarding the capacity for diaspores to survive gut passage, he stated, “all the species [Anatidae] feed largely on herbage, fruits, and seeds, and convey a large quantity of seeds in the viscera, though perhaps, to a larger extent, on their bodies and feet”.

Despite the fact that many of the same diaspores were listed in his review of duck diet, when considering the most likely dispersal means of particular plants, Ridley stated that epizoochory is the most likely means of transport for diaspores of “small-seeded marsh plants”, including Ceratophyllum demersum, Polygonum hydropiper, Scirpus maritimus, S. lacustris, Juncus, Zannichellia palustris, Ranunculus aquatilus, Sagittaria latifolia, Montia fontana and Ruppia maritima. He was particularly interested in the means of arrival of plants to oceanic islands and listed the genera he thought likely to have arrived via birds, probably in mud stuck on their feet. Ridley considered epizoochory of small diaspores in mud via shorebirds to be a particularly important process, given their frequent visits to islands and long-distance movements. He considered that Cyperaceae, Poaceae, Chara, Polygonum and Eriocaulon were all dispersed in mud on their feet or feathers, from one muddy shoreline to another.

Ridley realized that wetland connectivity greatly aids such epizoochory by reducing the overland distance across which propagules must remain viable. He attached much importance to the epizoochory of vegetative fragments on the feet and feathers of waterbirds—especially when birds are disturbed on the water and take flight quickly, usually moving over a short distance to nearby waterbodies. He considered that this process explained the rapid expansion of the alien Canadian pondweed Elodea canadensis in the UK and northern Europe after its appearance in Ireland in 1836, as this species does not usually set fruit in Europe. He performed an experiment and found that Elodea fragments could survive exposure to the open air for 23 h. In the same way, he showed that Chara fragments could survive such exposure for 1 h but not for 23 h, whereas Lemna minor could survive for 22 h (somewhat contrary to the conclusions of Guppy [23]; see also [79]). He also reported a duck shot while carrying a fragment of E. canadensis. He suggested that this epizoochory of fragments is also a key dispersal process for Hydrilla, Lagarosiphon, Ceratophyllum, Potamogeton, Zannichellia and Ranunculus and reported observations of ducks carrying fragments of P. perfoliatus and P. crispus. Similarly, he considered this epizoochory as key to the expansion of floating plants such as Lemnaceae and Azolla. However, he also supported epizoochory of seeds in the absence of mud and suggested that this occurs with floating P. lucens seeds. He also considered that Phragmites australis seeds are especially likely to be dispersed on feathers when this plant is used by waterbirds to line their nests.

Ridley reported how Ostenfeldt carried out an experiment strikingly similar to that of Guppy [23] at about the same time, feeding Potamogeton natans seeds to a mute swan and finding that seeds recovered from feces were more likely to germinate than control seeds and germinated at a faster rate. He suggested that endozoochory must be the key dispersal mechanism for P. natans, as “the plant is too bulky to be conveyed by attachment to a bird’s leg, and the seed perhaps too large to be conveyed in mud on its foot, and it has no hooked adhesive stigma to allow of its attachment to the plumage”.

Ridley’s book became one of the standard mid-twentieth-century sources for information on plant dispersal. For example, Matthews ([80], p. 48) in his 1955 book on the “Origin and distribution of the British flora” writes that he only needs to describe plant dispersal briefly, as the methods of dispersal are dealt with by Ridley [24].

5.3. Cruden and Carlquist

Cruden [28] considered that epizoochory was “the only plausible mechanism for long-distance dispersal” of diaspores by shorebirds, in this case because he both overestimated the time it can take shorebirds to migrate long distances and underestimated the length of the maximum retention times for which diaspores can be retained in the avian gut (according to Proctor and recent literature, see below).

In the late 1960s, Sherwin Carlquist [27] recognized a major role for endozoochory by shorebirds and other waterbirds as a means by which many plants reach oceanic islands, but was also a strong advocate of the role of epizoochory and argued that the dispersal mechanism used to colonize islands could be predicted by diaspore morphology. Later on, this idea led to the formal definition of “dispersal syndromes” based on morphological criteria [81]. Carlquist considered that shorebirds played a key role in allowing plants to reach Hawaii and emphasized that species such as the Pacific Golden Plover Pluvialis fulva use inland habitats on oceanic islands and not just aquatic habitats, thus facilitating their dispersal of terrestrial plants. Carlquist and Pauly [82] later provided experimental support for a link between diaspore morphology and adhesive capacity for epizoochory. Carlquist [27] observed sticky Boerhavia diffusa fruits on the feathers of the sooty tern Onychoprion fuscatus (Figure 4) and suggested that this plant and Pisonia umbellifera are widespread across Pacific islands owing to this kind of epizoochory.

Carlquist [27] went on to predict dispersal mechanisms for individual genera and identified many genera as dispersed by epizoochory, which are now known to be frequently dispersed by endozoochory. For example, he identified Ruppia, Najas, Eleocharis and Ranunculus as genera embedded in mud on feet, Plantago as a genus attached by viscid substances or viscid fruit, and Paspalum as a genus attached to feathers mechanically via barbs, bristles, etc. However, these are all genera frequently recorded in the feces or guts of ducks and geese [11]. Based on diaspore morphology, he estimated the relative importance of different dispersal mechanisms in the establishment of the flora of different Pacific islands, calculating up to 21% for mud on birds’ feet on a given island and up to 29% for attachment to feathers mechanically (endozoochory up to 57%, mainly plants with fleshy-fruits).

Amongst his conclusions, Carlquist [27] specifically identified migratory ducks as likely vectors and as generalist diaspore consumers that may disperse diaspores “thought to have no obvious adaptation for long-distance dispersal” by endozoochory. He emphasized the need for further research into endozoochory which “has received little effective investigation since Guppy’s time and is very much in need of renewed examination”. He was apparently unaware of Vernon Proctor’s work, which was underway at the same time.

6. Vernon W. Proctor

In a series of seminal papers from 1959 to 1968, Proctor and his coworkers at Texas Technological College revolutionized the understanding of endozoochory by waterbirds. In the context of the debates about endo- and epizoochory, in 1966 Proctor [83] argued that mud on the feet of migratory birds would quickly become dislodged during flight. He considered that most waterbirds will carry far more propagules internally rather than on their feet and feathers, as recently argued by [8,9]. Schlichting [84] reported in 1960 how the muddy feet of ducks exposed to air for half an hour became clean, suggesting that there is indeed a limited ability for diaspores to be dispersed a long distance by being stuck in mud on birds’ feet.

Proctor’s were the first modern systematic experimental investigations of endozoochory by waterfowl. He worked initially on a diversity of freshwater algae and liverworts [25,83,85,86,87,88] before later taking an interest in angiosperm seeds [26,89]. His work on algae, liverworts and various crustaceans has been advanced relatively little in the subsequent six decades. He showed conclusively that vegetative cells of algae and other propagules that are not resistant to desiccation can remain viable for much longer inside a waterbird than on the outside. Similar work was carried out a few years later by Kathleen Atkinson at the Freshwater Biological Association in Cumbria, UK [90,91,92], and she cited Proctor’s algal work.

In the case of Charophytes, Proctor [86] found that oospores of Chara hornemannii germinated more readily after passage through the duck gut but that vegetative fragments and bulbils did not survive passage. He predicted greater dispersal of oospores by autumn migrants when they are still on the plants, rather than by birds feeding later when oospores are present in sediments or along the shoreline. This represents a seasonal coupling hypothesis that was not tested for any aquatic diaspores until recently (and has received only limited support [4,59,93]). He showed that shorebirds such as the killdeer Charadrius vociferus can be better vectors than Anas dabbling ducks, probably because their smaller, less muscular gizzard does less damage to diaspores. Proctor et al. [88] were the first to attempt to quantify the maximum retention time of propagules (24 h for Chara zeylanica oospores in Killdeer) and the first to document a negative correlation between retention time in the gut and viability of propagules after excretion (a finding since repeated for various wetland angiosperms [50,94,95]).

De Vlaming and Proctor [89] cited an unpublished thesis (dated 1937) as having experimentally shown the viability of Scirpus paludosus seeds after passage through the mallard gut. De Vlaming and Proctor were the first to demonstrate emphatically the value of Charadriidae shorebirds as angiosperm vectors by endozoochory, showing that killdeer ingest many seeds of aquatic and semi-aquatic plants in the field and that the maximum retention times of seeds in captive killdeer were consistently longer than that in captive mallard. Of 23 plant species tested, all but one (Samolus parviflorus) survived gut passage by killdeer and/or mallard. They recorded extraordinarily long maximum retention times for plants such as P. pectinatus (76 h for killdeer, 73 h for mallard), Eleocharis spp. (120 h for killdeer, 93 h for mallard) and Scirpus paludosus (58 h for killdeer, 30 h for mallard), which exceed the times for which most recent experimental studies of endozoochory have been run (e.g., [50,51,71]) and suggest great capacity for LDD even to remote oceanic islands. However, De Vlaming and Proctor [89] suggested that maximum retention times were longer for plant taxa with small, hard seeds, those with soft seeds being destroyed by long retention times.

Contrary to van der Pijl’s [42] assumption that plants lacking a fleshy fruit have “non-adapted diaspores”, De Vlaming and Proctor [89] considered that aquatic plants are adapted for endozoochory as a result of selection for small, hard seeds, which are more readily transported internally. They suggested there is a phylogenetic component to the extent of such adaptation, for example with Cyperaceae being more adapted than Poaceae and Compositae, which were rarely retained in the gut for more than 10 h by mallard and killdeer. They criticized Ridley [24] for suggesting that epizoochory was the main dispersal mechanism for Juncus, Jussiaea and Sagittaria genera, which they showed to be likely to disperse by endozoochory, having retention times of up to 29 h.

Proctor [26] also studied how viable seeds can be regurgitated from the gizzard of shorebirds after being retained for even longer periods of up to 340 h for killdeer and 216 h for least sandpiper Calidris minutilla, this being a process in which seeds avoid passage through the entire gut without the predation of the vector as envisaged by Darwin. These maxima were shown for the berry Rhus glabra (Anacardiaceae), but three other terrestrial taxa (the small-flowered mallow Malva parviflora, the invasive field bindweed Convolvulvus arvensis and the sugarberry Celtis laevigata) were regurgitated after more than 120 h. The species retaining seeds for the longest before regurgitation were the shorebirds that did not regurgitate compacted fibrous pellets from the gizzard, but rather unconsolidated particles at irregular intervals (which also included western sandpiper C. mauri and Wilson’s phalarope Phalaropus tricolor).

Proctor [26] also observed how shorebirds reingest seeds cast up by other individuals by regurgitation and suggested how the same seed could thus be transferred between species and be dispersed to and from microhabitats used by different bird species (e.g., terrestrial habitats). In this way effective LDD of non-aquatic diaspores can be facilitated: “Transfer of resistant seeds from one bird to another, that is, from a “commuter species” to a “transoceanic express” might reasonably be assumed to occur anywhere shorebirds mingle in mixed flocks during spring and autumn migration”. The same point could be made about Anatidae, since, e.g., a diaspore in the feces of a migratory swan can be ingested by coprophagous migratory ducks [96]. Although the passage of seeds through the guts of two different birds is likely to reduce viability, the germination of seeds recovered from predatory birds provides support for such “diploendozoochory” [47,55].

De Vlaming and Proctor [89] emphasized how most aquatic plants are monoecious, such that one viable diaspore that is dispersed to a new habitat is potentially enough to establish a new population. Similarly, Cruden [28] pointed out that most plants with a distribution suggesting LDD by shorebirds are self-compatible. Proctor [97] went on to show for the Characeae that only bisexual self-compatible or parthenogenetic taxa are present on isolated oceanic islands, for which dispersal events are likely to be particularly rare. In contrast, dioecious taxa are restricted to continental land masses and islands within a maximum range of 200–300 km, such that repeated dispersal events allow establishment of both sexes. Proctor [97] cited an example of how isolated individuals of one sex of a dioecious taxa are occasionally recorded in remote islands (a female Nitella cernua in the Galapagos).

7. State of the Art: Modern Understanding of Epizoochory and Endozoochory

From Darwin [10] onwards, most scientists writing on this topic in the 19th or 20th centuries were ardent supporters of either an external mechanism of transport (epizoochory, e.g., Darwin, Beal, Amber and Cruden) or an internal mechanism (endozoochory, e.g., Hesselman, Guppy and Proctor) for the dispersal of plants by migratory waterbirds. Other workers were clearly ambivalent (notably Ridley and Carlquist), although they sided more towards epizoochory. So, who was right?

We can expect both epizoochory and endozoochory to have a role, as even for a single plant taxon, it is highly unlikely that all seeds will be transported by just one mechanism [98,99]. As Lawton [100] eloquently pointed out, in ecology there are often multiple mechanisms contributing to any phenomena and the ‘question is not so much about which mechanism is correct, but about the relative contributions of a plurality of mechanisms’. However, amongst recent papers focusing specifically on plant dispersal by migratory waterbirds, endozoochory is considered to be the dominant mechanism [9], as previously argued by Proctor. This has been strongly supported by comparisons of the rates of internal and external transport of viable seeds in the same waterbird populations. Brochet et al. [4] found much greater rates of endozoochory than epizoochory in teal wintering in France. Similar results were found in a study of various ducks and coot in Spain [61,93], and in a duck study in Australia [101]. A South African study of six waterfowl species recorded seeds in a particularly high proportion (27%) of epizoochory samples, but more seeds were dispersed by endozoochory [6].

In the case of the numerous plant genera cited by Ridley [24] as most likely to disperse by epizoochory, the combination of Proctor’s work with more recent work [9,11] provides strong evidence that endozoochory is the dominant process for dispersal by waterbirds over both short and long distances, even for plants assigned to an “epizoochory syndrome” based on their fruit morphology [19]. Even whole duckweed plants and the spores of aquatic ferns, which we might have assumed to be dependent on epizoochory, have recently been shown to disperse by endozoochory [78,102,103]. Although epizoochory of plants on mammal fur is clearly a major process [19,104], like pollen [105], seeds seem to stick more easily to fur than to feathers. Nevertheless, there are clearly some plants with adhesive seeds that are readily dispersed by seabirds (see Figure 4 and [106]). Furthermore, the use of plant material for nesting can lead to the dispersal of numerous terrestrial and aquatic plant taxa [8,107].

Various experimental endozoochory studies have focussed on survival, gut retention times, and germination response for diaspores of different plants [45,50,51,108]. Both animal experiments and use of laboratory protocols simulating gut passage (both through scarification and acidification) have shown that many plants increase their germinability and/or reduce their time to germination after endozoochory [109,110]. When conditions for germination are not suitable, seeds can follow endozoochory by entering seed banks where they may retain high germinability for at least a year [111]. Spatially explicit models have confirmed how waterbirds readily disperse seeds by endozoochory over tens of km (with maxima of >100 km) outside migratory periods [13,112,113]. Mechanistic models show how migration provides LDD over extreme distances of thousands of km [14,114].

Not surprisingly, given the influence of Darwin’s “digestion myth”, in contrast to the extensive literature about coevolution between frugivores and fleshy-fruited plants, few authors have considered the potential for coevolutionary relationships between waterbirds and dry-fruited plants. Without question, the study of interactions between plants with fleshy fruits and frugivores has been more fashionable in recent decades than those between other plants and granivores or herbivores (a point also made by Janzen [115]). Fleshy fruits have been perceived as more obviously “designed to be ingested” than other diaspores such as dry fruits, seeds and oospores, yet these perceptions are not necessarily correct. Microscopic studies have found no evidence to suggest that seeds from fleshy-fruited plants are somehow “better adapted” to resist gut passage than those from dry-fruited plants [116]. At least for waterfowl, seeds from aquatic plant species tend to be dispersed in greater numbers and by more bird species than those from terrestrial species [11], and they are also more likely to show a positive germination response to gut passage [109]. This suggests that aquatic plants are more likely to be adapted for waterbird endozoochory than terrestrial plants, although some waterbirds (e.g., geese) are particularly important vectors of terrestrial plants [11].

The importance of endozoochory of plants lacking a fleshy fruit (including Juncaceae and Cyperaceae) by other granivorous birds such as songbirds, corvids, parrots and galliformes was recognized by Ridley [24] and has also been confirmed in recent decades [5,117,118,119,120]. In contrast to endozoochory, despite a recent mini-boom in experimental studies addressing the potential of epizoochory by waterbirds for aquatic invertebrates (e.g., [121,122,123]), there have been relatively few recent experimental avian epizoochory studies for plants [124,125]. This likely reflects the recognition amongst specialists of the greater significance of endozoochory.

8. Continuing Influence of Darwin’s Digestion Myth in the 21st Century

Overall, there is now near-consensus amongst specialists in the field of waterbird zoochory that endozoochory is the dominant process [9] and that Darwin’s “digestion myth” has been repeatedly disproven. In general, Darwin’s work rightly remains hugely influential amongst all ecologists and evolutionary biologists (although it could be argued that Wallace deserves more credit [126]). An undesirable consequence of this is that the “digestion myth” remains influential in the broader plant ecology literature, in which endozoochory of dry-fruited plants is often completely overlooked. This habit is reinforced by a dominant paradigm in which all angiosperms can be assigned to a set of widely accepted “dispersal syndromes”, which are applied by inspecting diaspore morphology according to established criteria [127], an approach that has been popular since the 1980s [81,128]. This set of classical syndromes follows the “digestion myth”, and only plants with a fleshy-fruit can be assigned to an “endozoochory syndrome” [19]. For that reason, the endozoochory of other plants may be called “non-classical endozoochory” to highlight how this does not correspond to these popular syndromes [19,118]. Among the other established syndromes, diaspores with hooks would be assigned an “epizoochory syndrome”, and those that lack a fleshy fruit, hooks, wings or similar diagnostic traits are assigned to an “unassisted syndrome” (otherwise known as the “barochory” [i.e., gravity], “unspecialized” or “non-adapted” syndrome). Most of the European flora, most of the world’s agricultural weeds, and many of the plants dispersed by waterbird endozoochory have been assigned to this latter category [19].

Perhaps not surprisingly, the legacy of Darwin’s digestion myth and his preference for epizoochory is still very apparent in the literature, and here we only mention a handful of many examples (see also [19,129]). Schenk and Saunders [130] reviewed species with disjunct distributions in the Americas, classified their diaspores into classical dispersal syndromes, then took these as “empirical evidence” for the LDD mechanisms while dismissing the evidence for endozoochory of non-fleshy fruited plants. Like Cruden [28], they assumed that epizoochory by migratory birds is the main explanation for such distributions (followed by wind dispersal). Earlier, Renner [131] evaluated phylogenetic evidence for historical dispersal in various plant lineages across the Atlantic and attributed them partly to waterbird epizoochory, while denying the possibility of endozoochory. Ozinga et al. [132] related plant dispersal mechanisms to changes over time in range size for the northwestern European flora but did not include zoochory by non-frugivorous birds as a potential dispersal mechanism. Hintze et al. [133] summarized contemporary dispersal data in a database for over 5,000 plant species, mainly from central Europe. Their analysis shows that endozoochory by waterbirds of plants lacking a fleshy-fruit is hardly recognized as a dispersal mechanism by the general botanist community and is hence almost absent as a dispersal mechanism in their database. For example, their database suggests that, unlike epizoochory, endozoochory is of trivial importance for the Cyperaceae, when this family is one of those that has been most recognized by De Vlaming and Proctor [89] and contemporary authors [4,11,14,53,59,134] as subject to waterbird endozoochory. A similar emphasis on epizoochory is seen in the book by Schaefer and Ruxton [3], where they suggest that this mechanism of dispersal is particularly suited to LDD events, citing waterfowl and aquatic plants as an example.

It seems that botanists and ecologists have yet to take on board the broader consequences of historical work reviewed above and recent work that shows that endozoochory by waterbirds is not simply a dispersal mechanism for strictly aquatic plants, but is also likely to be an important dispersal mechanism for countless terrestrial plants whose diaspore morphology may give no obvious clue about this interaction with avian vectors [11,19,59,135]. To a lesser extent, this blindness also applies to the major role that herbivorous mammals play as dispersal vectors for these plants [19]. An analogous argument was made several decades ago by one of us [98] who suggested that many ‘wind dispersed’ seeds may in fact often be animal dispersed, especially for LDD events. A careful read of Ridley [24], Cruden [28] and Proctor’s work also suggests dispersal by avian endozoochory for many terrestrial plants with no obvious signal for this dispersal mechanism in the seed morphology.

That terrestrial plants are dispersed by “waterbirds” should come as no surprise. It is increasingly being recognized that aquatic and terrestrial ecosystems are highly interdependent, with continuous mutual exchange of subsidies of resources and nutrients. Waterbirds have an important role in this exchange [136], as they often spend much of their time resting or feeding on land, nesting on or over land, and flying over land. Ducks, geese, shorebirds and other waterbirds often ingest and disperse “terrestrial” seeds, either taking them on land, off the mother plant, or after they are blown or washed into waterbodies, and also move aquatic seeds into terrestrial habitats [13,113]. Any plant for which hydrochory is an important dispersal mechanism (including a wide variety of terrestrial taxa [135,137,138]) is also likely to have its seeds dispersed by endozoochory by birds living in aquatic environments [139].

The general failure to recognize and catalogue the role of endozoochory by migratory waterbirds as a major dispersal mechanism for terrestrial and semi-aquatic plants has important implications for plant biogeography and conservation (see also [19,129]), especially considering the great capacity for LDD by this means [12,13,14,114]. It may also help to explain contemporary paradoxes, such as how plants assigned to an “unassisted syndrome” turn out (a) to be excellent colonizers of oceanic islands [140], (b) to be particularly common in grasslands and swamps [141], which are waterbird habitats, and (c) to have lower rates of population decline than those considered to disperse by mammal fur or water [132]. In all three cases, waterbird endozoochory is a potential explanation.

9. Conclusions and Recommendations

Darwin [10] correctly highlighted the importance of migratory waterbirds as vectors for plant dispersal but wrongly assumed that none of the seeds they ingest can survive gut passage. This “digestion myth” has been influential through history until the present day, and when lesser-known authors disproved this assumption, their work failed to prevent the resurgence of this myth. Darwin overstated the importance of epizoochory by waterbirds, and a considerable body of modern research shows that they disperse more plants by endozoochory. Although Darwin associated the wide distribution of aquatic plants with waterbird migration, waterbird endozoochory is a major mechanism for LDD of both terrestrial and aquatic dry-fruited plants. Our review exemplifies the importance of being aware of older literature and of correcting historical misconceptions for the advancement of scientific knowledge.

Plant ecologists, in general, need to pay much more attention to zoochory by migratory birds as a dispersal mechanism for both aquatic and terrestrial plants that lack a fleshy fruit, and should not repeat assumptions that classical dispersal syndromes (i.e., hypotheses based on subjective interpretations of diaspore traits) are reliable predictors of dispersal mechanisms. The so-called “endozoochory syndrome” should be renamed the “frugivory syndrome” to avoid reinforcing these misconceptions. Existing information from the literature on zoochory by waterbirds (e.g., the European plant taxa listed by [11] should be incorporated into plant dispersal and trait databases.

Here, we highlight future research priorities regarding the role of waterbirds in plant dispersal (see also those identified in recent reviews by [9,19,124]). There is a need to quantify more plant traits that may determine the potential of different plant taxa lacking a fleshy fruit to disperse by endozoochory. This should include systematic experimental assessments of the resistance to gut passage by seeds of different taxa (as conducted for 48 species by [109]), in a similar manner to earlier systematic assessment of their capacity to disperse via wind (by quantifying terminal velocity) or water (through quantifying flotation, e.g., [133,135]). The physiological traits of seeds that determine their response to gut passage should be explored and related to existing knowledge about seed dormancy strategies. Such experimental ‘integrated plant screening programmes’ of traits have proved highly effective in other areas of plant ecology—especially in work led by the Late J. Philip Grime [142,143].

Future research should quantify the relative contributions of endo- and epizoochory in different ecosystems and among various bird species. More empirical research is needed into plant dispersal (especially endozoochory) by lesser studied waterbird groups (e.g., swans, screamers, jacanas), poorly studied regions (e.g., Asia), and other granivorous birds (e.g., galliformes). Given the influence of Darwin [10], it is surprising that relatively little attention has been paid to secondary endozoochory by fish-eating birds of diaspores ingested by fish. Recent studies confirm that this dispersal mechanism may have considerable importance [54,55], and it deserves more attention. Research is also needed to compare the importance of zoochory with other dispersal mechanisms for a given plant population [19,43]. For example, comparing the relative importance of waterbird zoochory, hydrochory and anemochory for given aquatic plants in a particular ecosystem. The relative roles of birds, fish and other animal vectors for a particular aquatic plant may also be compared [144].

Such research will further our understanding of the role of zoochory by waterbirds in the origins, population ecology and conservation of plant communities. It is vital to recognize the importance of avian endozoochory of dry-fruited plants so as to enhance policy for ecological restoration, spread of invasive species, and management of plant migration in response to global heating. At the same time, these policies must consider ongoing changes in the migration routes and sizes of waterbird populations [145].