Sven August Heintze was born in Skurup in southern Sweden in 1881 and earned a doctorate in botany at Lund University in 1913. His thesis was on zonation in alpine plants in Swedish Lapland, but he soon changed focus to study seed dispersal by birds. In 1912, Heintze already had the ambition to study the general role of corvids as dispersers of seeds in “Holarctic and Neoboreal” regions. His main contributions to this field were made in 1910–1917, when he collected feces, pellets and gut samples from European corvids (Heintze, 1917a,b, 1918). He also carried out extensive literature compilations, using sources in at least eight languages.

A description of his objectives and methods is found (in Swedish) on page 210 in Heintze (1917a). He traveled extensively in Sweden to collect corvid feces and pellets and examined the gastrointestinal tract of shot corvids. In his exhaustive review of terms for different plant dispersal processes, Heintze (1932) even proposed separate terms for seeds dispersed by egestion in pellets (“hemiendozoochory”) and feces (“euendozoochory”). Heintze was well aware of the role of corvids as scatter-hoarders, which was already widely acknowledged in the literature in the early 1900's, and this is why he focused on endozoochory instead. He emphasized the importance of carrying out these studies “in all seasons,” as he recorded the occurrence of germinated plants in nature (in excreta, at corvid nests, roosts, and at feeding sites) which had been dispersed by corvids. In addition, Heintze made ambitious germination experiments to study the implications of endozoochory; “fresh regurgitates and excrements were subjected to a rinsing/washing process [in the lab] similar to that accomplished by rain- and snowmelt water in nature” (Heintze, 1917a, p. 210). He carried out germination experiments of the contents of regurgitated pellets and excrements from Magpie and Hooded Crow. Most germination trials were carried out in early spring, of seeds that had been collected the preceding autumn or winter. Although many seeds germinated within a few weeks, trials were run throughout summer and autumn if necessary to detect later germinations (e.g., in 1916 the germination experiments were run until October 16th, Heintze, 1917a, p. 240). Further details of these experiments (e.g., substrate, indoor/outdoor, water supply, etc.) are unknown.

We extracted empirical data from the Swedish texts of Heintze explicitly focussing on seed dispersal by corvids (Heintze, 1917a,b, 1918). These sources list observations about regurgitated pellets, sampling of feces (mainly at roost and nest sites), and on contents of the upper (gizzard) and lower (intestines) gut. These data were originally reported in a rather unsystematic way, with variation in the level of detail and the extent to which different sample types were described. Interfoliated among Heintze's own data are references to research by colleagues, mainly in Central Europe, which are included in his summaries of the general role of corvids as seed dispersers. Many of his original sources are obscure and difficult to trace.

From Heintze's texts, we extracted details of those plant species with strong evidence of endozoochory, in particular cases where details of the bird species were provided, together with good evidence for endozoochory either because seeds were found in an intact state in pellets, feces or the alimentary canal, or they were germinated after removal from pellets or feces. Heintze stated that his list of species he considered to be dispersed by endozoochory “contains plant species that with full certainty or with high degree of certainty are spread endozooically by European corvids” (Heintze, 1918, p. 35). He also specified which plants were dispersed by synzoochory (i.e., scatter hoarding or for direct consumption at roosts without caching), especially by European Jays and Northern Nutcrackers, and we summarize these data for comparison.

We present detailed results for two different sets of Heintze's data. Firstly, a complete list of the plant taxa dispersed by endozoochory in Northern and Central Europe by any of the 11 species of corvids which he reviewed (Heintze, 1918). Secondly, his own detailed empirical dataset on pellets and fecal samples of Magpies and Hooded Crows in Sweden, for which he provided the number of intact seeds extracted for each plant species. The first dataset allows us to analyse what kinds of plant taxa were dispersed by endozoochory. The second dataset allows us to do a quantitative analysis of the relative abundance of seeds from each plant category (i.e., of seed size, fruit morphology, dispersal syndrome or habitat requirements) in pellets and feces for both species. The vast majority of this second dataset was collected from a restricted area on the west coast of southern Sweden.

The categories of fruit type and dispersal syndrome were assigned for each plant species from the Baseflor database (Julve, 1998). Seed length data were from the LEDA traitbase (Kleyer et al., 2008). When multiple measurements were available, we used their mean. Ellenberg moisture values were obtained from Hill et al. (1999).

For Heintze's detailed dataset for Magpies and Hooded Crows, we compared the frequency of occurrence of intact seeds of different plant species between pellets and feces using Fisher exact tests using online software (http://vassarstats.net/tab2x2.html). We then compared the frequency of occurrence of different plants in pellets of the two corvid species. We did not repeat this for feces because of small sample sizes. We also compared the paired frequencies of occurrence of each plant species between pellets (fp) and feces (fe) for each corvid species using a matched paired t-test (i.e., testing fp-fe), to see if there was a consistent difference between sample types (e.g., higher frequency of seeds in pellets). We then tested if the difference between the frequencies in pellets and feces (i.e., fp-fe) for individual plant taxa was related to seed size, using a non-parametric correlation (between fp-fe and seed length). T-tests and correlations were carried out in R (R Core Team, 2017).

Unfortunately, it was not possible for us to realize all the statistical tests of interest, as many of the details of which seeds were present in each individual sample were lacking, even for Magpies and Hooded Crows. Heintze did not always report which plant species were found together, or the combined total number of seeds, in each sample.

When combining Heintze's reviews of the literature with his own data, a total of 157 plant species from 42 angiosperm families were recorded as dispersed by endozoochory by at least one corvid species (Table S1). In contrast, Heintze cited nine taxa as dispersed exclusively by synzoochory (including scatter-hoarding): Aesculus hippocastanum, Carpinus betulus, Castanea sativa, Corylus avellana, Fagus silvatica, Juglans regia, Pinus cembra, Quercus robur, and Q. sessiliflora.

Of those species dispersed by endozoochory, 91 (56%) do not have a fleshy fruit and hence do not belong to the “endozoochory syndrome,” and were dispersed by non-classical endozoochory (Table S1; Figure 2). Many taxa with epizoochory, barochory and anemochory syndromes were recorded (Figure 2). Hence, many plants generally assumed to disperse via other mechanisms, such as wind, attached to fur, or self-dispersal, were dispersed by non-classical endozoochory. Those plant species dispersed by the most corvid species were fleshy-fruited, with up to nine different vectors per plant (Table S1). Nevertheless, some species with dry achenes and associated with barochory or epizoochory syndromes were dispersed by as many as six different corvid species (e.g., Polygonum aviculare, Rumex acetosella, Urtica urens, Table S1). Amongst the corvid species, the Magpie (114 plant species) and Hooded Crow (105) were recorded as vectors for the most plant species, reflecting Heintze's extensive work with those corvid species. They were followed by the Raven (71), Carrion Crow (33) and Jackdaw (29), whereas the Red-billed Chough (4) dispersed the fewest plant species (Table S1). The relative importance of classical and non-classical endozoochory varied between species. For example, of 29 species dispersed by Jackdaws, 18 (62%) were via non-classical endozoochory, compared to 36 (51%) of 71 species dispersed by Ravens.

Five species alien to the European continent were included amongst the plants dispersed by corvid endozoochory (Table S1). Aliens to Europe included the Dwarf Serviceberry Amelanchier spicata which is native to North America, the other four being cultivated species, such as the Cucumber Cucumis sativus, White Mulberry Morus alba, and Buckwheat Fagopyrum esculentum. Amongst the species recorded in Heintze's samples from Sweden, there were also an additional 10 species alien to Sweden but native to other parts of Europe, such as the grass Bromus arvensis (Table S1).

For the quantitative dataset on pellets and feces of Magpie and Hooded Crow produced from intensive study by Heintze, intact seeds from a total of 65 plant species (plus 5 plants identified to genus and one to family) were recorded, of which 37 (56%) do not have a fleshy fruit and so do not belong to an “endozoochory syndrome” (Table 1). Many taxa assigned to epizoochory (24% of taxa), barochory (20%) and anemochory (10%) syndromes were dispersed by non-classical endozoochory (Table 1). Nevertheless, when considering the total abundance of seeds from each syndrome, and not merely the number of taxa, the pattern changed markedly, and 97% of seeds were from an endozoochory syndrome (Table 1).

Germination tests confirmed the viability of seeds from 25 plant species (from a total of 35 species tested, i.e., 71%) plus two taxa identified to genus whose seeds were recovered from pellets and feces of Magpies and Hooded Crows (Table 1). Viability was confirmed for taxa from four dispersal syndromes, including all of 6 species with an endozoochory syndrome, 6 of 12 with barochory, 3 of 4 with anemochory and 10 of 13 with epizoochory (note, the number of seeds tested per species varied, Table 1). Overall, two taxa were only germinated from feces, 16 were only germinated from pellets, and 5 species (20% of the total) were germinated from both pellets and feces (Table 1). In addition, Heintze germinated Polygonum aviculare from the rectum of a European Jay, and Vaccinium cf vitis-idea from the feces of a Raven.

In addition, Heintze (1917a, 1918) recorded seedlings of at least 32 plant species in the process of becoming established in nature after germinating within the remnants of excreta (27 plant species in Magpie pellets and at least 10 in Hooded Crow pellets). These species included at least 11 that lack fleshy fruits and have been assigned to epizoochory, anemochory and barochory syndromes (Table 1; Table S2), confirming the importance of non-classical endozoochory.

Plant taxa dispersed by corvid endozoochory were from a broad range of fruit types, of which berries, drupes and achenes were the most frequent (Figure 3). Only seven of 45 taxa with achenes had a fleshy achene, corresponding to the “endozoochory syndrome.” When considering fruit types for plant taxa recovered from pellets and feces of Magpies and Hooded Crows (Figure 4), berries and drupes were more dominant, together with smaller numbers of achenes (only 11% of achenes recovered were fleshy). This is consistent with the dominance of seeds with an endozoochory syndrome in these samples (Table 1). For Hooded Crows, drupes appeared more likely to be recorded in feces and berries more likely to be recorded in pellets (Figure 4), although we were unable to test the statistical significance of this difference.

European corvids dispersed seeds with a broad size range by endozoochory, from a minimum seed length of 0.75 mm (Cerastium fontanum) to a maximum length of 11.5 mm (Prunus domestica), although most taxa had a length of <4 mm (Figure 5). In the detailed dataset for Magpies and Hooded Crows, the size distribution was more skewed toward smaller seeds (Figure 6). Comparing the size distribution for all taxa dispersed by corvids (Figure 5) with the data on relative abundance (Figure 6) suggests that taxa with relatively small seeds (<4 mm in length) were dispersed more often.

Seeds dispersed by Magpies tended to be larger than those dispersed by Hooded Crows, with a higher proportion of seeds of 2–4 mm for Magpies. Surprisingly, seeds tended to be larger overall in the fecal samples of Hooded Crows than in their pellets, although the largest seeds of >4 mm were more frequent in pellets (Figure 6).

Plant taxa dispersed by corvid endozoochory were from a broad range of terrestrial habitats, as indicated by Ellenberg moisture values (Figure 7). When considering the numbers of seeds from pellets and feces of Magpies and Hooded Crows assigned to each Ellenberg value, there was a tendency for higher soil moisture, and values 6 and 8 were better represented (Figure 8). No aquatic plants were recorded.

Overall, on average there were more intact seeds in Magpie pellets (9.9 seeds per sample) than their feces (6.6 seeds). Similarly, there were more seeds in Hooded Crow pellets (16.3 seeds per sample) than in their feces (2.8 seeds). However, since Heintze did not provide the combined total number of seeds in individual samples, we could not test these differences statistically.

For Magpies there were relatively few fecal samples, but Rubus idaeus was significantly more prevalent in feces than in pellets (Fisher exact, P = 0.0004). For Hooded Crows, Triticum aestivum was more prevalent in feces (P = 0.001), whereas Prunus avium was more prevalent in pellets (P = 0.0003). Eight plant species were significantly more frequent in Magpie pellets than in Hooded Crow pellets, and two species were more frequent in Hooded Crow pellets (Table 2).

In Hooded Crows, there was a higher overall frequency of seeds in pellets than in feces (comparing the frequencies of occurrence for each plant taxon with a matched paired t-test: t = 2.73, df = 64, p = 0.0082). In Magpies, there were few fecal samples and no significant difference in frequencies with pellets (t = 0.373, df = 63, p = 0.71). There was no relationship between the seed size of a particular plant species and the difference in its frequency of occurrence between pellets and feces, whether for Magpies (ρ = 0.106, p = 0.48) or Hooded Crows (ρ = 0.074, p = 0.72).

Based on presence/absence of plant taxa dispersed by endozoochory, classical and non-classical endozoochory by corvids appear to be equally important. However, the quantitative dataset for Magpies and Hooded Crows suggest that classical endozoochory events are considerably more frequent. Heintze found a similar diversity of plant taxa with and without a fleshy-fruit to be dispersed by these two species, but seeds from the latter were much less abundant. Heintze's extensive dataset suggests important differences among different corvid species as plant vectors by endozoochory, although this dataset is influenced by differences in sampling effort and relative abundance of each corvid in the habitats where he and his colleagues worked. His data do not allow us to fully assess the relative importance of classical vs. non-classical endozoochory in the other nine species, but more recent research demonstrates that classical endozoochory is not always dominant. Czarnecka and Kitowski (2013) found for Rooks in Poland that seeds were present in 18% of pellets, and half of all seeds belonged to dry-fruited species.

Differences among corvid species in their roles as plant vectors are inevitable, given their differences in habitat use. Heintze argued that in landscapes transformed by agriculture in southern Sweden, the role of Magpie and Hooded Crow as plant vectors by endozoochory was equivalent to that played by the Raven and European Jay in forest landscapes. He also observed that some corvids disperse plants by secondary endozoochory, a form of diplochory (Vander Wall and Longland, 2004). Magpies, Hooded Crows, Rooks, and Jackdaws frequently extracted seeds from the dung of horses, cows, sheep, goats, and wild ungulates, and Ravens consumed seeds from dung of reindeer, cows, and horses (Heintze, 1917a,b, 1918). Similarly, seeds in the feces of herbivores, such as ungulates or elephants are often secondarily dispersed by rodents that extract them from the dung (Jaganathan et al., 2016).

Heintze recognized that differences between corvid species in the amounts of grit in the gizzard are likely to influence seed survival (as shown for Anatidae, Figuerola et al., 2002), and suggested that Magpie, Raven, Siberian Jay, and Northern Nutcracker all have little or no grit. In contrast, he found Eurasian Jays to contain the most grit, and combined with their habit of rarely producing pellets he concluded “the Jay surely has a much lesser importance as an endozoochoric species than do other corvids” (Heintze, 1917a, pp. 209, 225; Heintze, 1918, pp.7, 11, 15), although this species is a major plant vector by synzoochory (Pesendorfer et al., 2016).

For dispersal to be effective, seeds must be dispersed into a suitable habitat allowing germination and subsequent growth. Heintze frequently reported field observations on established plants growing near Magpie nests, which he concluded had been dispersed there by the birds (Heintze, 1917a). His extensive observations of seedlings growing among the remnants of Magpie and Hooded Crow pellets are particularly important (Table 1; Table S2), confirming that not only are viable seeds dispersed by classical and non-classical endozoochory, but that they are moved into suitable microhabitats. Heintze also considered Raven pellets to be important in the establishment of plants in nature, and cited Holmboe as recording many germinated plants under Raven nests, e.g., Actea spicata in Norway and Ficus caria and Olea europea at nests in Cyprus (Heintze, 1918, p. 7–8).

Central to the role of corvids as endozoochoric seed dispersers are their movements between ingestion and egestion of a viable seed. Heintze knew that the Magpies and Hooded Crows he studied mainly undertook daily, local movements rather than long-distance migrations. He wrote that Magpies “regularly transport seeds ca 2 km, rarely more than 5 km” (Heintze, 1917a, p. 229–230). He found seeds from seashore plants in Magpie pellets retrieved 5 km from the closest seashore (Heintze, 1917a, pp. 217 and 230). For Hooded Crow, he stated “they frequently fly 10–20 km, or even longer, to reach their regular night roost” (Heintze, 1918, p. 2). He also provided known dispersal distances for Raven; “often 20–30 km” (Heintze, 1918, p. 9) and Rook [50–60 km, citing Altum (Heintze, 1918, p. 6)]. Moreover, Heintze was interested in endozoochory over longer distances during seasonal migrations by the Hooded Crow. He suggested that this species has the capacity for overseas seed dispersal between land masses, particularly since his dissections showed that seeds may remain in the gizzard for up to 24 h (Heintze, 1918, pp. 34–35). Some northern populations of Hooded Crow still undertake seasonal migrations.

The likely dispersal distances identified by Heintze a century ago are remarkably similar to known movement distances in present-day corvids in northern Europe (see also Cramp and Perrins, 1994; e.g., Wernham et al., 2002; Fransson and Hall-Karlsson, 2008; Czarnecka and Kitowski, 2010; Pesendorfer et al., 2016; Marchand et al., 2018). This confirms that corvids are important vectors for long-distance dispersal of plants, and offer a maximum dispersal distance far greater than is generally recorded for other mechanisms including epizoochory, anemochory, and obviously barochory (Bullock et al., 2017).

Corvids can be important vectors for alien species (Nogales et al., 1999), especially in urban environments (Czarnecka et al., 2013). Interestingly, Heintze showed they were already dispersing numerous alien plants a century ago. Heintze also stated that Magpies were responsible for spreading “our cultivated garden trees, bushes and herbs with berries into the wild” (1917a, p. 230). Furthermore, many of the native species dispersed by corvids in Europe by non-classical endozoochory are alien species in other continents, where they may be spread by corvids in a manner not predicted by diaspore morphology. For example, the Hemp-nettle Galeopsis tetrahit has a dry achene that was recorded from six corvid species by Heintze (Table S1), was particularly frequent in Magpie pellets (Table 2), and is a widespread and problematic alien in North America (USDA and NRCS, 2019).

Plants with the largest seeds can be expected to be dispersed less often by corvid endozoochory since they are more likely to be destroyed in the foregut, and also because of the general negative relationship between seed size of a given species and the numbers of seeds produced by individual plants (Bruun and Poschlod, 2006; Green et al., 2016). Comparing the seed size distribution for all plants dispersed by corvid endozoochory (Figure 5) with the relative abundance of seeds dispersed by Magpies and Hooded Crows (Figure 6) does provide indirect support for a greater dispersal frequency of smaller seeds. Heintze (1917a, 1918) suggested that larger seeds were more likely to be egested and dispersed via pellets and smaller ones in the feces. Heintze stated that “all larger, most middle-sized, and more than half of the small-sized seeds are spread hemiendozoically [i.e., in pellets], whilst the rest comes out in the excrements” (1918, p. 30). This would be consistent with expectations based on gut morphology, since the sphincter passage between the gizzard and intestines should make it harder for larger seeds to pass intact. It is also consistent with literature for other birds, such as gulls and shorebirds, in which larger seeds were egested in pellets (Lovas-Kiss et al., 2018b, 2019). However, such a clear pattern is not supported from our analyses of Heintze's dataset for Magpies and Hooded Crows (Figure 6).

Heintze suggested (at least for Magpie and Hooded Crow) that seed dispersal via regurgitated pellets was more important than seed dispersal via feces (Heintze, 1917a, p. 228). We found evidence that seeds are more frequent in pellets than in feces, especially for Hooded Crows. However, rates of endozoochory events depend on the rate of egestion, and it is likely that each pellet sample contains a higher proportion of the daily regurgitated output than each feces sample contains of daily fecal output. Some birds produce <1 pellet a day (e.g., White Storks, Rosin and Kwiecinski, 2011). Based on dissections, Heintze concluded that seeds may remain in the gizzard of a Hooded Crow for up to 24 h (Heintze, 1918, pp. 34–35), suggesting they produce at least one pellet a day.

Owing to the focus on classical endozoochory in the literature, little information is available about the importance of non-classical endozoochory by other granivorous birds so as to enable a comparison with corvids. The best known vectors of non-classical endozoochory are the waterfowl Anatidae (Green et al., 2016). In particular, the dabbling ducks Anas spp. are likely to disperse over 500 plant species in Europe, and only a small fraction of seeds they disperse have an endozoochory syndrome (Soons et al., 2016; Lovas-Kiss et al., 2018a). Interestingly, there is a considerable overlap in plant species dispersed by corvids and waterfowl, mainly being cases of non-classical endozoochory (see Table S1 for full details). Of the 157 plant species listed by Heintze as dispersed by corvid endozoochory, 56 are also thought to be dispersed by dabbling ducks (Soons et al., 2016), and 20 were listed as dispersed by Greylag Geese Anser anser in the Stockholm archipelago in Sweden (Jerling et al., 2001). We found corvids to disperse more seeds from large size categories (most of which are of fleshy-fruited plants) than dabbling ducks (see Figure 2 in Soons et al., 2016). Plant species common to corvid and waterfowl endozoochory are terrestrial species. Not surprisingly, the distributions of Ellenberg moisture values differ among the plant taxa and seeds dispersed by corvids and dabbling ducks, because ducks disperse many moist soil and aquatic taxa with an Ellenberg value of 9–12 (see Figure 3 in Soons et al., 2016).

Based on the work of others and his own extensive research Heintze concluded (1917a, p. 210) that “It appears that within these zoogeographic areas [the Holarctic and the Neoboreal] corvids are the most important seed dispersers among all landbirds.” This article lends support to this statement, given the demonstrated importance of corvids as vectors for an extensive diversity of plants dispersed by both classical and non-classical endozoochory. Much has changed in European habitats over the past century, and it would be interesting to conduct similar research again in the same parts of Sweden where Heintze collected his own data.

It is unfortunate that the work of Heintze and co-workers a century ago or before has been overlooked for so long. The scientific community has effectively lost their understanding about the role of corvids as seed dispersers for a very wide range of terrestrial plants, and we hope our paper helps to restore this knowledge. The effort and knowledge required by Heintze to retrieve and study thousands of pellets and fecal samples is awe-inspiring, and should humble us all to pay more attention to the work of such pioneers. Increasing access to digitalized older literature is making this easier. His work also illustrates the immense value that natural history plays in ecology, and the serious consequences of its current decline (Tewksbury et al., 2014).

Many corvid species are likely to be vectors for a broad range of plants through both frugivory and granivory because they are opportunistic, generalist foragers able to exploit a range of habitats in both natural and human-created landscapes. In urban environments, Magpies, Jackdaws and other species can be amongst the most abundant birds. Corvids worldwide may be one of the most important bird groups in providing a vital seed dispersal service that maintains and restores a wide range of plants with a variety of growth forms and other traits, and in forested and open landscapes, as well as urban habitats. Corvids are heavily hunted in many countries, and this may negatively impact their important role as native plant vectors. On the other hand, corvids also have a role in unwanted spread of alien plants.

As shown previously for waterfowl, shorebirds and gulls (Jerling et al., 2001; Lovas-Kiss et al., 2018a,b, 2019), non-classical endozoochory by corvids is a major dispersal process that requires more attention if we are to fully understand plant dispersal processes and plant-animal interactions. We hope this paper will inspire others to look beyond frugivory and synzoochory and pay more attention to the importance of non-classical endozoochory by corvids, as well by other little-studied granivorous birds, such as galliformes and small passerines (Swank, 1944; Orlowski et al., 2016).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.