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- Discussion and conclusions
- Supporting Information
In plants, dispersal of diaspores is crucial for gene flow and colonization. Dispersal is especially important in plants of dynamic and ephemeral habitats such as shorelines, river and ditch banks, and terrestrialization phases of open water. Accordingly, plants from such dynamic wetland habitats may be expected to have evolved a high capacity for dispersal. Plants from these habitats have several dispersal vectors at their disposal to achieve dispersal on a landscape or even larger scale (long-distance dispersal (LDD)): dispersal by water, by wind and by animals moving over long distances. Dispersal by water transports diaspores to other wet sites, thus dispersing them ‘directionally’ (sensu Howe & Smallwood 1982) to sites with a high probability of being suitable habitat. However, water dispersal is limited to areas connected by surface water to the seed source, and, in moving waters, areas downstream of the seed source (Boedeltje et al. 2003, 2004). Wind dispersal does not have these spatial limitations, as wind transports diaspores to a wide variety of sites in all directions, but dispersal by wind is not directed specifically to suitable habitat (Soons et al. 2005; Soons 2006). Dispersal by waterfowl is intermediate between water and wind, as waterfowl are likely to deposit diaspores in or near water, but may also drop diaspores during flight or other activities in non-wetland areas.
In their reviews, Charalambidou and Santamaria (2002) and Figuerola and Green (2002) conclude that a relatively low number of experimental studies have been carried out on internal (endozoochorous) dispersal of seeds by waterfowl. They call for more research, focussing on comparisons of groups of dispersed plant species, especially to assess if they possess characteristics that favour endozoochorous transport, and on research analysing the different steps of the dispersal process (among others, the distinction between gut survival and subsequent germination). Recently, quantitative studies on the survival of plant seeds ingested by ducks have been carried out for Potamogeton pectinatus (Santamaria 2002; Charalambidou et al. 2005), Ruppia maritima (Figuerola et al. 2002; Charalambidou et al. 2003b) and Sparganium emersum and Sagittaria sagittifolia (Pollux et al. 2005), but each study has been carried out under different conditions so that it is difficult to generalize results. A larger and more comparative study on a wide range of plant species is therefore needed to quantify seed characteristics determining the potential for LDD by waterfowl.
To study the potential contribution of waterfowl to LDD of wetland plants we selected 23 common plants from dynamic wetland habitats, fed their seeds to mallards (Anas platyrhynchos), a common and highly omnivorous duck species (Cramp & Simmons 1977), and quantified their gut survival and subsequent germination. We used this large number of species, representing a wide range of seed traits, to study the mechanisms underlying successful endozoochorous dispersal and identify adaptations to dispersal by waterfowl. Specifically, we tested the following hypotheses:
Mallards have the potential to disperse wetland plant seeds: seeds survive passage through the digestive tract intact and germinate afterwards when deposited in wetland conditions.
Intact survival through the digestive tract and subsequent germination are dependent on the retention time in the digestive system of the duck: seeds that are retained shorter have higher survival and germination.
Intact survival through the digestive tract and subsequent germination are dependent on seed traits of the wetland species:
Wetland species with small seeds and thick seed coats are specifically adapted to endozoochorous dispersal and in these species passage through the digestive tract enhances seed germination, while in other species germination remains unaltered or decreases.
- Top of page
- Discussion and conclusions
- Supporting Information
Seeds of all species except N. lutea and Rumex hydrolapathum were retrieved from the mallard faeces, with retrieval percentages ranging from 0% to 54% (Table 1). Retrieved seeds of J. effusus, L. salicaria and T. latifolia that could not be sieved and counted due to their small size were also present in the faeces as demonstrated by their germination from the faeces samples in the germination experiment. In all species most seeds were retrieved within the first 10 h after feeding, with no or very few seeds after 10 h (Table 1).
Germination percentages of retrieved seeds ranged from 0% to 78%, with almost always a decrease in germination percentage with increasing retention time in the mallard. In most species these germination percentages did not differ from the germination percentages of the control seeds (Table 1). In the cases of Berula erecta, Epilobium palustre, I. pseudacorus, Lysimachia vulgaris and Phragmites australis, the germination rates of the retrieved seeds were significantly lower than the germination rates of the control seeds, while retrieved seeds of S. erectum had significantly higher germination percentages than control seeds (Table 1). The difference in germination between the retrieved seeds and the control seeds was mostly very small, particularly in the first time interval (0–5 h).
In general, 0–32% of the ingested seeds were retrieved and germinated (Table 1). This proportion decreased with increasing retention time, from 0–27% after 0–5 h to 0–1% after 10–48 h (Table 1). These percentages are relatively modest, which is mainly caused by low retrieval percentages. Still, internal seed transport and subsequent germination were observed for 19 of the 23 plant species.
Nonparametric correlation analyses revealed that retrieval percentage, germination percentage and retrieval speed were highly positively correlated (Table 2). This shows that the seeds that were retrieved in greater numbers also germinated better and proceeded more rapidly through the mallards’ digestive system. Retrieval percentage, germination percentage and retrieval speed were all best explained by seed volume in stepwise multiple regression analyses (Table 4), even while there were strong correlations among seed traits (Table 3). This result shows that smaller seeds are retrieved in greater numbers, germinate better and pass faster through the digestive tract (Fig. 1). Unexpectedly, seed coat thickness had almost no effect on retrieval or germination (Table 4). Seed coat thickness did explain effects of gut passage on the germination of seeds compared to control seeds: in species with thick seed coats, gut passage enhanced germination, while in species with thin seed coats germination was reduced. Seed volume and coat thickness data are given in Appendix S1 in Supplementary material. Overall, these findings identify the mechanism of successful internal dispersal by ducks: the species with the smallest seed volume pass the fastest and in the greatest numbers through the digestive tract and are most viable afterwards.
Table 2. Spearman's correlations for the seed dispersal characteristics show that seed retrieval, germination and retrieval speed are highly correlated to each other
|Spearman's ρ||Retrieval (% of ingested)||Germination (ratio of retrieved to control seeds)||Germination (% of ingested seeds)||Retrieval speed (% seeds in first time interval)|
|Retrieval (% of ingested)|| ||NS||0.90**||0.56*|
|Germination (ratio of retrieved to control seeds)|| || ||NS||NS|
|Germination (% of ingested seeds)|| || || ||0.71**|
|Retrieval speed (% seeds in first time interval)|| || || || |
Table 4. Stepwise multiple regression analyses of the seed dispersal characteristics on the seed traits (seed mass, volume, density and coat thickness) show that seed volume is the main determinant of seed retrieval, germination and retrieval speed, while seed coat thickness determines the ratio of germination and plays a minor role in seed retrieval
|Regression analyses||Significant independent variables (seed traits) in the regression model|
|Retrieval (% of ingested)||1. Seed volume (2. Seed coat)||Negative relationship (Positive relationship)||R2 change = 0.25 (R2 change = 0.15)||P = 0.024 (P = 0.057)|
|Germination (ratio of retrieved to control seeds)||1. Seed coat||Positive relationship||R2 change = 0.43||P = 0.003|
|Germination (% of ingested seeds)||1. Seed volume||Negative relationship||R2 change = 0.22||P = 0.025|
|Retrieval speed (% seeds in first time interval)||1. Seed volume||Negative relationship||R2 change = 0.37||P = 0.008|
Table 3. Spearman's correlations for the seed traits show that seed mass, volume, density and coat thickness are highly correlated to each other
|Spearman's ρ||Seed mass||Seed volume||Seed density||Seed coat thickness|
|Seed mass|| ||0.98**||–0.55**|| 0.78**|
|Seed volume|| || ||–0.66**|| 0.80**|
|Seed density|| || || ||–0.47*|
|Seed coat thickness|| || || || |
The next step is to use our simple dispersal model to estimate effects on dispersal distributions. As usual in seed shadows, the resulting dispersal distributions are strongly skewed, with a decreasing probability of dispersal over longer distances (Fig. 2). Most (19 out of 23) species show relatively high probabilities of dispersal of ingested seeds over short to landscape scale distances, with 10 species showing a probability of > 0.01 of dispersal up to c. 350 km. Also LDD is highly possible for most of the species. Most species have a probability of > 0.0001 to be dispersed up to c. 780 km, and about half of the species (12 out of 23) have a probability of > 0.001 to be dispersed over such distances. In addition, five of the species can be dispersed in low probabilities over distances > 780 km, up to a maximum of 3000 km. The species that are dispersed with the highest probabilities and over the longest distances are the species with the smaller seeds.
Figure 2. Estimated seed shadows for the 23 wetland species if dispersed endozoochorously by mallards during migratory flight. For species in grey, seed germination is significantly reduced by endozoochorous dispersal; for the species in bold seed germination is significantly increased after endozoochorous dispersal (in comparison to control seeds). Potamogeton pectinatus and Sagittaria sagittifolia are excluded (see text).
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Discussion and conclusions
- Top of page
- Discussion and conclusions
- Supporting Information
We assessed the potential for endozoochorous seed dispersal by mallards of 23 common wetland plant species with a wide range of seed characteristics. At least 19 of the 23 plant species can be dispersed endozoochorously by mallards. One species (S. erectum) seems to be especially adapted to endozoochorous dispersal, as it exhibited enhanced germination following transport through the mallard digestive tract. Thirteen species, the majority, had unaltered germination following endozoochorous dispersal by mallards when compared to control seeds, while five species can be dispersed endozoochorously but show reduced germination afterwards. The species that have the highest potential to be dispersed, based on their high (> 25%) germination percentages of ingested seeds, are H. tetrapterum, Lycopus europaeus, Mentha aquatica and Silene flos-cuculi. Only two species (N. lutea and R. hydrolapathum) cannot be dispersed endozoochorously by mallards, as also found for N. lutea by Smits et al. (1989). The percentages of successful germination after internal dispersal found in this study (0–32%) are comparable to, but covering a wider range than, viability percentages found in eight other wetland species (1–16%) by Mueller and van der Valk (2002).
On the dispersal of the remaining two species, P. pectinatus and S. sagittifolia, we are unable to draw firm conclusions. These species were retrieved intact from mallard faeces, as in previous studies (Santamaria et al. 2002; Charalambidou et al. 2005; Pollux et al. 2005), but in contrast to these studies no germination was found. This was probably due to the germination conditions, because the control seeds of these species also did not germinate. Germination conditions were equal for all species and selected to be optimal for the majority of species (see Methods), most of which occur under more variable or somewhat drier conditions than the submerged P. pectinatus and S. sagittifolia. Consequently, the conditions used in the germination experiment may have been too dry for them. Given the germination of these species following internal transport by mallards in previous studies (Santamaria et al. 2002; Charalambidou et al. 2005; Pollux et al. 2005), there is evidence that these species can be successfully dispersed endozoochorously by mallards.
Our study shows that the plant species with the smallest seed sizes have the highest potential to be dispersed by mallards, a result also found for seed lengths (instead of seed volumes) by Mueller and van der Valk (2002). We show that the species with the smallest seeds have the highest and fastest seed retrieval and the highest germination after gut passage, indicating that the mechanism for successful seed dispersal by mallards is that smaller seeds travel through the digestive tract faster, are deposited in larger numbers and are more viable. Seed coat thickness plays only a minor role, and is of importance mostly in one species that appears to be adapted specifically to endozoochorous dispersal, S. erectum. This species has large seeds and slow and relatively low retrieval and germination, but seeds germinate much better after passage through the mallards’ digestive tract than in a control situation, probably due to breaking or removal of the thick seed coat, as also found in Sparganium emersum (Pollux et al. 2005).
Our model calculations estimate how far seeds of the wetland species might be dispersed by mallards in migratory flight. These estimates represent maximum dispersal distances that seeds may reach via endozoochorous transport by mallards, as they assume that the mallards depart directly after seed ingestion and fly continuously in one direction at average flight speed until the seeds are dropped. Such conditions occur only during long migratory flights, the mechanism for reaching maximum dispersal distances via transport by ducks (Figuerola & Green 2002; Green et al. 2002; but see Clausen et al. 2002). These maximum dispersal distances are long. Our calculations show that most species have relatively high probabilities of dispersal of ingested seeds over short to landscape scale distances, while about half of the species have a relatively high probability to be dispersed over distances up to 780 km, and five species have the potential to be dispersed in low probabilities over distances > 780 km, up to a maximum of 3000 km. Our estimate of 3000 km as the upper limit of dispersal distances is likely to be an overestimation, as seeds may not remain in the mallard for the full time interval required to cover such a distance (38 h). Nevertheless, our findings show that mallards have the potential to contribute to the LDD of wetland plants, and have the potential to disperse wetland seeds over longer distances than wind (up to 6 km during very heavy storms, Soons et al. 2004b, or 4 km under more frequently occurring conditions, Soons 2006), fish (up to 27 km, Pollux et al. 2007) and water (e.g. the EU's longest river, the Danube, is 2860 km).
Although ducks are known to be able to cover long distances during flight (56 ringed ducks in Spain travelled a mean distance of 384 km, range of 59–1801 km, within 1 week, Green & Figuerola 2005; one individual ringed teal travelled 1285 km in < 24 h, Clausen et al. 2002), their movement pattern will normally consist of shorter flights. Ducks often fly tens of kilometres between feeding and roosting sites and show high regional mobility, especially during winter, which is also the seed dispersal season (Green et al. 2002). This behaviour will result in significantly shorter dispersal distances than the maximum estimates from our model. These distances may be in any direction, as the movement pattern of ducks is often nomadic rather than directional (Figuerola & Green 2002). The majority of seeds are thus likely to be dispersed over landscape scale distances, and be much more in line with the distances reached by wind and fish. More elaborate and more realistic models including the daily movement patterns of birds, such as the models recently developed by Spiegel and Nathan (2007) and Levey et al. (2008), will allow the calculation of complete dispersal kernels for wetland species. The collection of detailed spatial movement data for mallards will be an important next step towards this goal.
We conclude that, in line with our first hypothesis, mallards have the potential to disperse wetland plant seeds endozoochorously. For 21 out of the 23 common wetland plant species used in this study, seeds survived passage through the digestive tract and germinated afterwards when deposited in wetland conditions. This indicates that a wide variety of wetland plants can be dispersed by mallards. As expected from our second hypothesis, survival through the digestive tract and subsequent germination are dependent on the retention time in the digestive system of the duck: seeds that are retained shorter have higher survival and germination. Ingestion by mallards does not hamper seed germination in most (14 out of 23) species, especially after short retention times. In line with our third hypothesis, survival through the digestive tract and subsequent germination are dependent on seed traits of the wetland species. Species with smaller seeds are dispersed in the largest numbers and germinate most successfully afterwards. Seed volume is the trait that matters most, while seed coat thickness plays only a minor role in gut survival. As stated in our final hypothesis, passage through the mallard digestive tract enhances seed germination compared to control seeds in species with a thick seed coat (but not small seed size). However, our findings show that the ability to be successfully endozoochorously dispersed by mallards is widespread among wetland plants, and not limited to species with thick seed coats.
Overall, endozoochorous transport by mallards appears to be a widespread, successful dispersal mechanism among wetland plants. Mallards can disperse wetland seeds over a wide range of distances, including LDD, with the potential to disperse relatively high numbers of seeds between 0 and 350 km during flight, and the potential to disperse small-seeded species over more than 780 km, up to 3000 km. Mallards are thus potentially (very) long-distance dispersers of wetland plant seeds. This shows how an individual seed trait, seed volume, can have a large effect on the landscape scale and larger scale species dynamics of wetland plants.