Freshwater Biology (2011) 56, 1390–1402

doi:10.1111/j.1365-2427.2011.02576.x

Do birds of a feather disperse plants together?
ELISA RAULINGS, KAY MORRIS, ROSS THOMPSON AND RALPH MAC NALLY Australian Centre for Biodiversity, School of Biological Sciences, Monash University, Clayton, Vic., Australia

SU M M A R Y 1. Dispersal of propagules by waterbirds is thought to be important for wetland plants because of the abundance of birds and their frequent movements among aquatic habitats. Differences in bird characteristics (size, movement, feeding ecology) were expected to lead to different outcomes for plant dispersal. 2. We investigated heterogeneity in plant dispersal by ducks (Anas superciliosa, Anas gracilis, Anas castanea). We calculated the probability of transport of viable seeds by germinating propagules retrieved from feathers and feet (epizoochory) and the contents of the oesophagus, gizzard and lower gut (endozoochory). 3. The abundance and richness of seeds carried internally and externally did not differ among sympatric bird species. We used estimates from the literature of movements of Anas species to approximate dispersal kernels for the transport of plant propagules. 4. Heterogeneity in the abundance and movement ecology of disperser species will result in differing patterns and degrees of connectivity for wetland plant metacommunities. Sedentary waterfowl are likely to have an important role in replenishing propagules and connecting aquatic metacommunities over small distances. Nomadic waterfowl may facilitate long-distance dispersal. We discuss the implications of differences between duck species in movement patterns for connectivity of aquatic plant metacommunities across landscapes.
Keywords: aquatic macrophytes, biotic connectivity, metacommunities, waterbird dispersal

Introduction
Aquatic habitats such as rivers, floodplains and wetlands are connected biotically across landscapes by dispersal of aquatic plants (Amezaga, Santamaria & Green, 2002). Dispersal via waterbirds may be crucial for the exchange of seeds and vegetative fragments (collectively, ‘plant propagules’) because of the abundance, widespread distribution and high frequency of movement of waterbirds within and among habitats (Amezaga et al., 2002). Waterbirds disperse plant propagules in three ways: first, by attachment to feathers, feet and bill (epizoochory or external dispersal), second, in the crop or oesophagus
Correspondence: Elisa Raulings, Australian Centre for Biodiversity, School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia. E-mail: elisa.raulings@monash.edu

coupled with regurgitation (endozoochory or internal dispersal) and third, through gut passage and subsequent faecal deposition (also endozoochory). Differences in foraging mode and movement patterns among waterbirds may influence the plant species dispersed and the frequency, distance and direction of their dispersal (Green, Figuerola & Sanchez, 2002). As such, different bird species may produce different patterns of biotic connectivity across landscapes. Several factors suggest that waterbird species may disperse different plant taxa or disperse similar taxa but with different frequencies. Co-occurring waterbird species may forage in different vegetation communities and consume different food sources (Marchant & Higgins, 1990; Green et al., 2002). Duck species with heavier gizzards may destroy a higher proportion of ingested seeds (Figuerola, Green & Santamaria, 2002), and differences in mechanical or chemical digestion among waterbird species may
Ó 2011 Blackwell Publishing Ltd

1390

43¢S. 2002). 1930. We anticipated that there would be differences among dispersers in the types of plants dispersed. Vallisneria australis S. Australian Salt Grass (Distichlis distichophylla Labill. 2002a.94¢E: Fig.) and Common Reed [Phragmites australis (Cav. 1980). Mehlman & Oring.-Sternb. in wetlands of the Gippsland Lakes Ramsar site. 2008). stripping the . Tackenberg. Figuerola et al. Santamarı Information on external transport is relatively scarce (but see Vivian-Smith & Stiles.g. We attempted to germinate propagules in the gut contents and propagules borne externally on ducks. Seeds transported by these species are likely to be deposited in different locations.W.L. 2010a.. J. Brochet et al. and the relative importance of internal and external dispersal. creeks and brackish or saline wetlands (Frith. Figuerola & Green. They rarely feed far from water. 1) contains a diversity of wetland types from deep freshwater marshes to semi-permanent saline wetlands (Corrick & Norman. We also obtained estimates of the Ó 2011 Blackwell Publishing Ltd. Scott]. 1390–1402 movements of waterbird species to construct approximate dispersal kernels for propagules transported by these ducks. while more sedentary species move frequently between feeding and resting areas. Figuerola & Green. Frith. which often involves complex foraging patterns (Roshier. Fassett) and Beaded Glasswort [Sarcocornia quinqueflora (Ung. Deep. 2003. and these species have different foraging behaviour in the same habitat (Frith. 56. effective viability (Brochet et al. the probability of transport and movement behaviour. herbs and submerged species (e. Grey Teal Anas gracilis Buller and Chestnut Teal Anas castanea Eyton) and considered implications for patterns of connectivity of aquatic plant populations across landscapes. Norman. 147°13¢41. hence. Norris et al. Here. which describe the probability of seed deposition as a function of distance from a source (Nathan & Muller-Landau. 1994. 1978) as males of Grey Teal (670 g) and Chestnut Teal (708 g). Nomadic waterbirds make rapid and long-distance movements in response to spatial fluctuations in wetland availability. 2003). 1968. up-ending to feed from the bottom.). Methods Study site The Gippsland Lakes Ramsar site (38°08¢02.. Dispersal kernels. 1968. we investigated heterogeneity in the dispersal of plant propagules by three duck species (Pacific Black Duck Anas superciliosa Gmelin. ´a & Langevoord. 2010b) but the frequency and type of plant propagules carried also may differ with bird size and foraging mode (Ridley. 1990). 1998. The area surrounding the Gippsland Lakes is predominantly cleared agricultural land dominated by introduced grasses and herbs.. Foraging behaviour and dispersal of waterbirds Waterfowl in eastern Australia display a regular breeding peak in the late Austral winter and spring (August–November. 1983. Assessing patterns of connectivity for aquatic plant populations requires knowledge of the movement and behaviour of birds (Haig. Flocks of the Pacific Black Duck co-occur with the small dabbling ducks. because of differences in the plant species carried..b). Many studies have attempted to predict the maximum distances over which plant populations are connected by waterbird dispersal. Saline wetlands have diverse saltmarsh vegetation including Sea Rush (Juncus kraussii Hochst. Asmus & Klaassen. 2002b.. 1968). with rushes. Charalamabidou. the frequency with which they are transported. 1968. differ among disperser species because of different movement patterns (Sun et al. Brochet et al. Freshwater Biology. Pacific Black Duck males weigh almost twice as much (up to 1300 g. 1983). permanent. Johnsgard.) A. Posschlod & Bonn.) Steud. We tested whether waterbirdmediated dispersal of aquatic plant propagules differs among dispersers.. Holt Mueller & Van Der Valk. 1959.Plant dispersal by ducks 1391 affect seed viability (Proctor. Grey Teal and Chestnut Teal. Pacific Black Duck are among the most abundant ducks in Australia and occur in a range of habitats from deep. 1997) and also because of differences in retention time and. 2010). Jacobs & Les) scattered throughout.]. sedges. dredging mud in shallow water. 2000. Marchant & Higgins. 2010a). We hypothesized that interspecific differences in dispersal ecology of waterbird species would result in differences in the dispersal kernels for aquatic plants. freshwater wetlands are dominated by the woody Swamp Paperbark (Melaleuca ericifolia Sm. reed-dominated freshwater wetlands to rivers. although shorter events are also important in determining metacommunity dynamics of aquatic plants.

saltwater estuaries and the lower reaches of creeks around coastal areas. 1968) and can move hundreds of kilometres overnight (Slater. The feet were placed in water to the ankle and scrubbed with a toothbrush. between New Zealand and Australia). 1979). Slater & Slater. 1). 1982). Roshier et al. 2008). although they are typically more local and sedentary than Grey Teal and can remain in the same waterbody for long periods (Frith. 1979). 1968. seeds from plants growing in or overhanging the water and filtering seeds from the surface (Frith. 1983. 56. they were excluded from external propagule sampling. Sampling We sampled Pacific Black Duck. with occasional samples from Lake Wellington and Clydebank Morass (Fig. Norris et al. 1968. Lake Wellington and Lake Victoria) and the collection site for external transport (Dowd Morass). Waterbirds were shot during flight over Dowd Morass and Heart Morass State Game reserves. Grey Teal consume fallen seeds. 1968. 2002. Fig. Chestnut Teal are most common in brackish coastal lagoons. 1990). Birds were shot in-flight. In contrast to the highly nomadic Grey Teal. To assess external transport. 1390–1402 . Clydebank Morass. Tracey et al. Waterbirds were retrieved immediately and placed by hunters into clean plastic bags. Ducks were collected in early morning as they returned from feeding areas. Heart Morass. Freshwater Biology. They are common and widely distributed across Australia in a range of habitats from mangrove estuaries on the coast to deep cold lakes in the highlands and inland Australia. They are common in south-eastern and south-western Australia. 22 Chestnut Teal and one Grey Teal harvested at Dowd Morass. Grey Teal rarely stay in the same wetland for extended periods of time (Frith. but vagrants may occur elsewhere. Marchant & Higgins.. Chestnut Teal and Grey Teal harvested by licensed Field and Game Australia hunters on the opening morning of the legal duck-hunting season (21 March 2009). If ducks had been placed on the ground or on other surfaces. 1 Map of the study area showing the collection sites for gut samples (Dowd Morass. Raulings et al.1392 E.. move in response to local conditions and occasionally move from Australia to neighbouring parts of Asia (Frith.. although some animal material is often also taken (Goodrick. 1983).. so propagules recovered from these birds were in the process of dispersal. seeds were removed from the feathers and feet of three Black Duck. Further sampling throughout duck hunting season was not feasible because sample sizes would have been too small to compare among waterbird species. Chestnut Teal are more or less sedentary with some summer movement (Norris et al. 2004). The bird then was held Ó 2011 Blackwell Publishing Ltd. Grey Teal are highly nomadic.g. Goodrick. They occasionally make long journeys (e. They feed in and around the margins of wetlands and tend to be non-selective and opportunistic in their feeding preferences (Norman & Mumford.

Data were pooled across localities because birds were harvested in-flight and had not necessarily been feeding at the location from which the samples were obtained. Eleocharis pusilla R. To distinguish whether waterbirds differed in diets or in the digestion of plant propagules. Kruskal–Wallis tests were used to compare differences in the abundance and richness of seedlings emerging from different gut regions and among all three bird species. and the remaining tissue was thoroughly rinsed with water to ensure propagules had been removed. 2002). The crop is located near the throat and remained in the head cavity when gut contents were removed by hunters. clonally produced plants were identified from connecting rhizomes and counted as one individual. Where present. Mann Whitney U-tests were used to compare differences among Black Duck and Chestnut Teal in the abundance and richness of seedlings emerging from feather and feet samples. 56. we sampled the gizzard and the lower intestine. This method facilitates germination of most wetland plant species and species associated with moist habitats (Boedeltje. and are most representative of faecal mate´a. Plants were formally identified by staff at the Royal Botanic Gardens (Melbourne) and taxonomic nomenclature follows Ross & Walsh (2003).5 mm (Cottrell. have seeds <200 lm and visual estimates are biased towards seeds with a maximum axial dimension of ‡0. Freshwater Biology. presence ⁄ absence) internally (in its lower gut) or externally (on its feet and feathers). such as Juncus sp. Seedlings were checked daily and removed from trays when they could be identified and prior to flowering. Therefore.Br. the gut contents of 21 Black Duck. 1390–1402 used to control for any seeds blown into the glasshouse.Plant dispersal by ducks 1393 over a tray. gizzard and lower gut were obtained by squeezing. we report the minimum probability as the larger value of P(i) or P(e) and the maximum probability as P(i) + P(e).08 · 0. Twenty additional soil-only trays were Ó 2011 Blackwell Publishing Ltd. we were interested not only in dispersal per se but also in which plant species could germinate in a wetland habitat after dispersal. Therefore. To test whether there were interspecific differences in the composition and abundance of plant taxa . The conrial (Charalambidou & Santamarı tents of the oesophagus. We separated samples into oesophagus. common aquatic plants. We used a seedling-emergence trial to estimate the number of viable seeds transported by waterbirds. First. Where possible. 2004). Germination was followed for 4 months. spread across the soil and placed in a temperature-controlled glasshouse. We assumed internal and external carriage of viable propagules were not mutually exclusive. External and internal duck samples were washed through 125 lm mesh.11 m diameter) that maintained the water level just below the soil surface. Data were analysed in S Y S T A T version 10 (SPSS. 2000). 2005).08 m) were filled with potting compost and placed in water-filled trays (0. and the feathers on the head and body of the bird were brushed continuously for 3 min using a brush. Ter Heerdt & Bakker. and it was difficult to distinguish whether new emergents were a consequence of seed germination or subsequent clonal growth. the dispersal unit) would transport ‡1 viable propagule (Pt) internally (i) or externally (e) or both as Pði [ eÞ ¼ Pi þ Pe À Pði \ eÞ We did not collect externally and internally carried propagules from the same waterbirds.e. gizzard and lower gut. We preferred this approach to visual estimates for two reasons. Second. To assess internal dispersal of aquatic plant propagules by ducks. Containers (0.. We sampled the lower two-thirds of the gut because viable propagules in this part of the digestive system are considered to have survived the harsh digestive juices and mechanical forces of the gizzard and upper intestine. rapidly produces clonal growth after germinating. the oesophageal sample included the region below the crop and above the proventriculus and is likely to underestimate the number of seeds present in this part of the tract. 24 Chestnut Teal and 21 Grey Teal were removed by hunters in the field and placed in sealed bags on ice. so we do not have an estimate of P(i \ e). We used logistic regression with a binomial error distribution to determine the probability that a species of bird could disperse at least one viable seed (i. we calculated the probability that a single bird (i. Statistical analyses Grey Teal were eliminated from the analysis of external transport because there was just one individual.e. Seedlings that failed to grow or showed signs of senescence under the waterlogged conditions were transferred to irrigated pots and the water level altered.

f..f.e. Gut retention time also has important effects on the percentage of seeds that germinate and the germination rate. and the median ranks of abundance (Mann–Whitney U-test = 360. 2008). and varies depending on both the seed species and bird vectors involved (Figuerola et al. or fall off easily (e. but germination rates may decline as a consequence of desiccation over long periods. He tallied band returns with distance from the banding site for species recaptured from 1953 to 1963. Reliable flight speeds were not available for Chestnut Teal or Pacific Black Duck. on the head. The median ranks of seedling abundance (Kruskal–Wallis Ó 2011 Blackwell Publishing Ltd. we combined data from studies of faecal matter retention with flight speeds for Grey Teal. a one-way A N O S I M analysis was undertaken using P R I M E R version 5 (Clarke & Gorley. Santamaria & Ouborg. Northern Territory and South Australia. it is not yet possible to modify the dispersal curve as a function of gut retention time. P = 0. 1986). 22 taxa germinated from gut samples.. dispersal kernel) also depends on propagule retention time and the flight speed of birds. 56.g. P = 0. Propagules may be carried long distances on feathers and feet if they are carried in positions where they cannot be removed by the bird. P = 0. one individual moved 502 km in 6. approximately one in five birds carried one or more seed on their feathers or feet).. 2010a). as measured by the emergence of ‡1 seedling from feathers or feet. 2010a. the small sample of Black Duck reduced the statistical power for these tests. but up to 94% of seeds are evacuated within 12 h (Brochet et al. There was little evidence that feet and feather samples of Chestnut Teal and Black Duck differed in having ‡1 seedling (v2 = 1. Figuerola et al.e. 2010) to 60 h (Pollux.125) of plant taxa were greater in feathers than on feet.1394 E. To determine the distances over which internally carried propagules are likely to be egested. Freshwater Biology. 2010)..162) and richness (Mann– Whitney U-test = 354.. New South Wales.22 (i. Sorensen. 1 d. To calculate the range of distances Grey Teal may travel before propagules may be egested. three species of introduced pasture weeds and one native herb germinated from feathers and feet of Black Duck and Chestnut Teal (Table 1).f. Waterbird dispersal and construction of dispersal kernels To determine the range of distances over which propagules may be carried by Black Duck and Grey Teal. Feeding studies of other Anas species suggest the retention time of seeds in the gut varies from 1 h (Brochet et al. 1 d. 1 d... 1 d. Quantitative information on the mobility of Chestnut Teal is not available. Raulings et al. in the gizzards of waterbirds. Roshier et al.6 h and was travelling at 99 km h)1 for the first half of this period (Roshier et al. we used the average flight speed (76 km h)1) rather than the maximum flight speed (99 km h)1... 2005). The probability that a bird would carry one or more seeds externally. 2008) because individual birds may not be able to sustain this speed over longer distances.e. The native grass Lachnagrostis filiformis Trin.f. 1 d. Thus. 2001).099) and richness (Mann–Whitney U-test = 171. Frith (1959) banded 5535 Black Duck at 10 locations and 10 333 Grey Teal at 12 locations in Tasmania. Between 31 December 1957 and 31 March 1958.. Distances travelled by recovered or recaptured birds from the original banding locality were provided. but not significantly so. the joint probability of internal or external transport) with movement data from two studies.30). we combined data on the probability that a bird (the ‘dispersal unit’) carried ‡1 viable propagule(s) (i. Results External transport of plants by waterbirds Few seedlings emerged from feather and feet samples (Table 1). Norman (1971) banded 2041 Black Duck and 1915 Grey Teal at five locations in South Australia over a 10 year period (1953–63). The median ranks of abundance (Mann–Whitney U-test = 172.f. the dispersal curves presented here assume 100% retention of externally carried seed.11) of plant taxa emerging from external samples did not differ between Black Duck and Chestnut Teal.. Internal transport of plants by waterbirds Overall. P = 0. Thus. was 0. P = 0. However. 1390–1402 .1. The distance that a propagule will be deposited from its source (i.. Satellite tracking of Grey Teal showed that they regularly make longdistance movements.

rushes and herbs (Table 2). 2 d. six of the 22 species were unique to different disperser species. in each of these cases. Eleocharis pusilla was the most abundant taxon. and did not differ among bird species (v2 = 3. The number of seedlings emerging from the lower gut contents was typically one per bird. only one individual carried seed.f. Chestnut Teal (n = 22) Feet Pacific Black Duck (n = 3) Feathers Feet 1 (3) 4 (12) 1 (1) 5 1 1 (1) 1 (1) 2 (2) 1 (1) 1 1 1 2 4 2 (2) 15 2 1 3 H test = 38. Some 396 seedlings emerged from gizzard samples from 19 plant taxa (Table 2).* Plantago coronopus L. but was not found in Chestnut Teal gizzards. Most of the seedlings (40) were E. and seven gizzard samples had the maximum of three plant species germinate. 2 d.9. sedges. the ducks consumed similar plants. Overall. Values given are the number of birds with viable seeds (total number of viable seeds) Total number of birds carrying germinants Chestnut Teal (n = 22) Feathers Pacific Black Duck (n = 3) Grasses Lachnagrostis filiformis (G.001) differed significantly among oesophagus. P < 0. pusilla rapidly produced clonal growth and it was difficult to distinguish vegetative spread from seedlings. Herbs Trifolium cf.. Forst. After germination. germinated from the lower gut contents (Table 2).16) and diversity (A N O S I M global R = 0. was empty (i. and were a mixture of aquatic and terrestrial species.. Unidentified taxa Species 1 Total number of germinants *An introduced species. pusilla. Freshwater Biology. which were from a single Grey Teal (Table 2).20). This species was present in 19% of Black Duck gizzards and 24% of Grey Teal gizzards.e. One Grey Teal had two species (E. The species composition of the seedlings germinating from the contents of duck gizzards was similar among bird species based on abundance (A N O S I M global R = 0. 1390–1402 from a gizzard sample was 0.) Trin. 56. The probability of ‡1 seedling emerging Ó 2011 Blackwell Publishing Ltd. At least 60% of plant taxa were carried by two or more duck species. These taxa were native sedges and introduced herbs. P = 0.f.) emerge from the oesophagus sample. Thirteen plants. where present. representing 70% of all seedlings. Only a few individuals of .Plant dispersal by ducks 1395 Table 1 List of plant taxa that germinated from the feathers and feet of Pacific Black Duck and Chestnut Teal. P < 0.. pusilla and Isolepis sp. E. Four birds carried one or more seeds and the probability of carrying ‡1 seed in the oesophagus also was 0. n = 23). with several other introduced species (Table 2). However. digestive contents were absent and presumably lost during gut removal from the body cavity. pusilla. Seedling emergence from gizzards showed that waterbirds consumed a varied diet of grasses. but one Black Duck carried four seeds of E.175. P = 0. Seeds did not germinate from the Grey Teal sample (n = 1).019. That is. The introduced plant Water Buttons (Cotula coronopifolia) was abundant in the gizzards of all bird species.* Conyza bonariensis (L. 45 seedlings from five plant species emerged from 18 oesophageal samples.08). from seven plant taxa.) Cronquist* Senecio glomeratus Desf. glomeratum L.001) and seedling richness (Kruskal–Wallis H test = 37. but at least 125 seeds germinated from the gizzard of one Black Duck. 2 d.f.22.011. The oesophagus was often missing from gut samples (n = 25) or.1. ex Poir. P = 0.61. gizzard and lower gut samples.

1 1 (4) 1 (1) 1 (1) 1 1 (1) 1 1 1 4 Juncaginaceae Unidentified taxa Species 1 Species 2 Species 3 Total number of germinants 1 167+ 7 0 1 (1) 54 3 44 175+ 3 Ó 2011 Blackwell Publishing Ltd. Eleocharis pusilla species were extensively and rapidly clonal. Bolboschoenus medianus Sojak Eleocharis acuta R. Plant taxa O (n = 7) G (n = 21) LG (n = 21) O (n = 6) G (n = 24) LG (n = 22) O (n = 5) G (n = 21) LG (n = 20) O G LG Grasses Poaceae 1 (4) 1 (1) 4 (129 + ) 3 (5) 1 (1) 1 (1) 1 (2) 1 (14) 1 (1) 1 (4) 1 (2) 1 (40) 1 (1) Lachnagrostis filiformis (G. 1390–1402 *An introduced species. Freshwater Biology. Br.) Trin. Br. but where they could not be distinguished they are indicated with a +.* Persicaria prostrata (R. Forst.Br. Conyza sp. Trifolium glomeratum* L. individual seedlings were counted.Table 2 List of plant taxa that germinated from the oesophagus (O). Isolepis sp. . Johnson Juncus pallidus R. Some birds carried one or more plant species Total number of birds carrying germinants 1396 Pacific Black Duck Chestnut Teal Grey Teal E.) Sojak Atriplex prostrata DC. Lactuca serriola* L. gizzard (G) and lower gut (LG) samples of Pacific Black Duck. Schoenoplectus tabernaemontani Palla 1 (1) 1 (2) 6 (8) 1(5) 1(1) 1 (1) 2 (3) 1 (1) 1 (1) 1 (1) 1 (1) 1 (1) 2 (4) 6 (24) 1 (1) 1 (1) 1 Rushes Juncaceae Juncus gregiflorus L. Triglochin striata Ruiz & Pav. 56. Cotula coronopifolia* L.S.A. Raulings et al. 1 1 1 (1) 1 (1) 1 (2) 4 (14) 1 (1) 1 (1) 1 1 2 1 2 2 1 (1) 1 (1) 12 1 1 1 4 Herbs Asteraceae Asteraceae Asteraceae Asteraceae Asteraceae Polygonaceae Chenopodiaceae Fabaceae 2 (7) 1 (1) Aster subulatus Michx. Unidentified grass 2 1 5 (148 + ) 4 (6) 1 (1) 1 1 9 8 3 2 7 1 1 Sedges Cyperaceae Eleocharis pusilla R.Br. Grey Teal and Chestnut Teal. Sonchus sp. Values given are the number of birds with germinants (total number of germinants). Trifolium cernuum* Brot.

Dispersal kernels assume 100% retention of externally and internally transported seed. For these three closely related duck species.Plant dispersal by ducks 1397 several plant species survived gut passage. 1% chance that Grey Teal will carry viable propagules ‡1000 km. 56. P = 0. different patterns of connectivity of aquatic plant metacommunities arise from differences in the abundance and movement patterns of dispersers. Similarly. This value assumes that internal carriage and external carriage of seeds are not mutually exclusive events and does not include oesophageal data nor detachment from feathers and feet.14. while the equivalent figure for Black Duck is 501–1000 km. 2). and hence the shape of the dispersal kernel differed among ducks because of different mobility (Fig.8 0.6 1h 60 h 0. 1390–1402 Fig. before declining with increasing distance (Fig. 0.2 0.g.413. the distances that propagules are carried.13). seeds remained viable in both means of transport. Internally transported seeds will be egested at a given distance along this curve depending on gut retention time and flight speeds. P = 0.36. Distances travelled by recovered Pacific Black Duck and Grey Teal individuals that were banded by Frith (1959) and Norman (1971) at locations across Australia are presented as a mean ± SE. P = 0. The large number of birds moving between habitats means that the total number of propagules moved among metacommunities is likely to be high. there was no evidence of interspecific differences in median ranks of abundance (Kruskal–Wallis H test = 2. 0. and there was no difference among waterbird species (v2 = 0. but disperser species did not differ in their capacity to transport seed.f.23) than those carried by the nomadic Grey Teal (c. 10% chance that propagules attached to. The range of distances potentially travelled by Grey Teal between the minimum (c. Although these waterbird species have a similar maximum probability (c. sedges (Cyperaceae). The probability of gut samples having ‡1 seedling that germinate from the lower gut was 0. although the rates of transport both internally and externally were low. 2).380. 2). There is a c. or ingested. 2 Dispersal kernels for seed carriage by Pacific Black Duck and Grey Teal. and there is a c. propagules carried by Black Duck are almost twice as likely to arrive at locations within 100 km of the source plant (c. 2).98).36) of carrying ‡1 viable propagule(s). 1 h) and maximum (60 h) retention times is illustrated here. 1.035.4 0. 2 d. we estimate that during migratory flights propagules carried internally and egested after 1 h would be deposited <100 km from the source and up to 1800 km from the source Ó 2011 Blackwell Publishing Ltd. Seeds did not germinate in control trays. and vegetative propagules were not observed in external or internal samples. We calculated the maximum probability that a waterbird would carry ‡1 viable propagule(s) internally or externally was 0. the plant taxa germinating from lower gut samples differed among waterbirds (Table 2).50) of seeds germinating from the lower gut. wetland after 24 h if the bird is able to fly continuously during this period (Fig. Externally transported seed may be detached anywhere along the dispersal kernel. Freshwater Biology.0 Pacific black duck Grey teal Probability of seed carriage 0.0 0 1–100 101–300 301–500 501–1000 1000+ Distance from source (km) Dispersal of waterbirds and dispersal kernels for plant propagules The dispersal kernels for propagules carried by Black Duck and Grey Teal suggest propagules have a comparatively high probability of dispersal within 100 km of the source..30) or richness (Kruskal–Wallis H test = 1. Relatively few individuals of each plant species germinated from external (feather and feet) . Discussion The duck species considered have the potential to spread large numbers of viable seeds. With the exception of Sonchus. 0. If gut retention as a function of flight time is overlaid on the dispersal kernel for Grey Teal. Assuming 100% retention. grasses (Poaceae) and amphibious herbs (particularly Asteraceae)]. Plant taxa dispersed by waterfowl were aquatic and terrestrial plants [e. by Grey Teal will be transported more than 100 km (Fig.

(Powers. the effects of ducks on seed viability. visual identification versus germination). Raulings et al. 2005. 2010). 2002a). despite differences in waterbird size. the abundance of plant propagules in faecal samples differed between Black Swan. it is difficult to interpret whether this reflects real differences among waterbird diets. for example. 32% of diaspores ingested by teal were recovered intact (Brochet et al.. 2009). or incidental ingestion of propagules. to 33% Europe (Charalambidou & Santamarı of hunted ducks in Louisiana..g. ingestion rate may be the best predictor of seed viability in the lower gut. these closely related disperser species may also have more overlap in habitat use and feeding ecology than previously reported. 2002b) have found no differences among waterbirds in numbers of seed attached externally. closely related duck species consumed.. dispersal of plants species. Occasionally. The probability of a waterbird carrying ‡1 viable seed(s) in the gizzard was higher (0. conditions. for these taxa. Ducks were hunted after early morning feeding and a large proportion of the previous day’s food would have been egested when they were hunted. seed viability and waterbirds sampled (Figuerola & Green. 2002). 2008. Freshwater Biology.. but differences in substratum Ó 2011 Blackwell Publishing Ltd. who reported seeds adhering to feathers and feet of 78% of Brant Geese Branta bernicla (L.. The probability of a waterbird carrying ‡1 viable seed(s) in the lower gut at any time was low (0. 2003. these disperser species probably transport similar types of plant taxa between wetland metacommunities. Dispersers consumed similar numbers and species of seeds in this study. We may have underestimated the probability of internally mediated dispersal if the large numbers of seeds in the gizzard pass through the lower gut intact and remain viable. despite differences in body size and reportedly feeding in different habitats within a swamp. Green & Santamaria. 2002).. The percentage of birds carrying ‡1 seeds on feathers or feet was 22% for Black Duck and Chestnut Teal.A. Aquatic plant propagules were abundant in our study region at the time of sampling and reduced competition for dietary resources may partly explain dietary overlap among Anas species in this study.. In captive experiments. although the likelihood of internally mediated dispersal is likely to have been underestimated.. divergent feeding preferences of other types of waterfowl are likely to be maintained under these . Therefore. 2005).. Pollux et al. Brochet et al. Grey Teal and Pelican (Green et al. Seasonal differences in propagule availability may partly explain dietary overlap of duck species in our study (Green et al. Figuerola. 56. 2010a). Noble & Chabreck. However. The latter estimates are likely to be inflated because viability was not measured. similar quantities of seed on a per capita basis. diets diverged (Guillemain et al. However. 1978). This is much lower than that found by Vivian-Smith & Stiles (1994). Brochet et al. When propagules are abundant. 2008). which restricted our capacity to determine whether different ducks disperse a similar suite of plant species externally. Many of these propagules were likely to have remained viable and subsequently egested had they not been hunted.S. Figuerola et al. plant taxa were represented by a single germinant. The ducks consumed similar numbers and species of seeds.. 1390–1402 samples. Quantity of waterbird-mediated dispersal In our study.14). estimates vary from 28% of faecal samples containing propagules collected from five waterbird species in ´a. and all plant species present in the gizzard have dispersal potential (Brochet et al.) and ducks. 2002.61) and many seedlings emerged from some gizzard samples (up to 125 seedlings per gizzard). Others have reported interspecific differences in the abundance of internally dispersed plant propagules (Guillemain et al. Green et al. 2010a). Eurasian Coot. 2002).1398 E. 2010a. Our study and others (Figuerola & Green. Mallard and Teal had considerable food overlap in early winter. 2003. U. In arid Australia.. to 66% of faecal samples collected from six duck species in the prairie potholes of North America (Holt Mueller & Van Der Valk. and potentially dispersed.. despite having different foraging behaviour in the same habitat and variation in body size. In western France. when food was abundant. It is difficult to compare the proportion of samples in which one or more seeds survived digestion in our study with other studies because of small sample sizes and differences in sampling approaches (e. but as food availability declined. or within 12 h of consumption (Charalamabidou et al. However. It is plausible that differences in digestion or physiology among the duck species may result in different germination and subsequently. but only a few individuals of each species survived gut passage.

Plant dispersal by ducks 1399 (e.. Pollux et al. or in suitable condition.. Figuerola et al. Presuming these ducks are equally likely to be harvested. or deposited when they come into contact with vegetation or water (Sorensen. Black Duck would have transported nearly half of these propagules over the 7-week period. dispersal ‘‘quality’’) than on the quantity of seeds that any individual waterbird disperses.g. Wongsriphuek. Using gut retention times of 1–60 h (Holt Mueller & Van Der Valk. This is particularly so if such movements occur without any particular directionality (as opposed to directed migration. Frequent movements from foraging to resting areas for all duck species suggest aquatic plant metacommunities in the study region are relatively well connected over short distances (<100 km) and are likely to occur in any direction. The time between seed consumption or attachment and departure from the seed source will affect rates of deposition and thus distances over which plant populations are effectively connected (Green et al. 2010a. There are few data on how long plant propagules remain attached externally to birds. 16 000 total) were shot in the study catchment during the 7-week duck-hunting season (Gormley & Turnbull. Assuming equal retention times across species. but seeds may be removed immediately by the ducks once detected. 2008). or lost from. 2005. 1983). Freshwater Biology. 2002a) or between different habitat types. 2010) and an average flight speed of 76 km h)1 (Roshier et al. The lag phase associated with internal transport (1 h minimum. There remains an unavoidable bias in field studies such as this that seeds may have been added to. Dugger & Bartuszevige. Propagules transported on feet are likely to be washed off relatively quickly. 2009). 3600 Grey Teal and 10 000 Black Duck (c. 2010) suggests that seeds are unlikely to be deposited adjacent to the parent plant. 1390–1402 .. 1981.g. Aquatic plants may be more reliant on nomadic waterbird species for long-distance dispersal. is poorly known. 2008. for germination and establishment. but propagules may be carried indefinitely in plumage. The quantity of seed dispersed by each duck species is likely to be positively related to the abundance of that species at any given time. sedentary ducks may be more influential in facilitating arrival of propagules to suitable sites and influencing the genetic structuring of plant populations over 10–100s of km.. wetland and arrive in a greater variety of locations and habitats. Norman. 5760. Estimating the abundance of waterfowl is difficult. feathers and feet between being shot and picked up. the rate and frequency with which seeds are regurgitated by waterbirds. 2400 Chestnut Teal. We estimate conservatively that the minimum number of viable plant propagules being actively dispersed across the catchment by birds at any time during the 7-week duck hunting period was c.e. Most aquatic plant propagules are likely to be deposited at short distances (<100 km) from the propagule source. migrating more frequently and possibly at greater speeds than Black Duck and Chestnut Teal. Figuerola et al. Such dispersal events will be of great importance in replenishing propagule banks in the first instance and facilitating genetic exchange if plants subsequently establish. 56. 2002b). 2002). Sedentary species such as Chestnut Teal may be more likely to deposit seeds over short distances than more nomadic species. such as Black Duck and Grey Teal. movement and the connectivity of aquatic metacommunities The probability of success or failure of dispersal for aquatic plant propagules depends more on the abundance and movement of the dispersers (i... Nomadic Grey Teal have a higher probability of dispersing seeds furthest from the source wetland. Local interactions (e. Brochet et al. Brochet et al. seeds transported by Grey Teal may be deposited 76–1800 km from the source during migratory flights. 1986). The tail of the dispersal kernel was characterized by low(er) probability. but may be less likely to arrive in a suitable site. competition and habitat mismatch) may constrain species diversity in metacommunities over these scales more than the supply of propagules dispersed by waterbirds. but conservative estimates suggest that c. 2010a. if at all. The lower limit Waterbird density. because of longer residence times of the birds within wetlands and shorter flying distances (Norman & Powell. 2002. long-distance dispersal events that occur when birds undertake long periods of flight at relatively high speeds. Seeds retained for longer will be deposited further from the source Ó 2011 Blackwell Publishing Ltd. mud versus sand) also may contribute towards variation in attachment capacity (Figuerola & Green. Similarly.. but most seeds will be deposited within 12–24 h. as a greater proportion of the population fly longer distances. Figuerola & Green.

Fritz H. seed by mallard (300–1400 km. Gippsland Lakes Taskforce.J. 747–753. (2010a) Endozoochory of Mediterranean aquatic plant seeds by teal after a period of desiccation: determinants of seed survival and influence of retention time on germinability and viability. Figuerola J. Ecography. Brochet A. 17. 483– 494. BC Journal of Ecosystems and Management.J. 2005). Our research provides the first step in understanding how landscape scale connectivity of wetland plant communities may be mediated by animals.. Department of Sustainability and Victoria. 2008).. Proceedings of the Royal Society of Victoria. Functional Ecology. 213–222.J. concurs with estimated internal dispersal distances of Ruppia maritima L. LPO776494 with contributions from Parks Victoria. dispersal limitation may constrain the geographical ranges of aquatic plants and influence the structure of aquatic plant metacommunities. ´a L. Ter Heerdt G. For the first time. 919–928. Further research is required to reduce uncertainties associated with propagule retention and frequency of duck movements between habitats. Fritz H. 23.P. 1–15. (2005) Field evidence Charalambidou I. Guillemain M.. (2004) Seed rain traps for forest lands: considerations for trap construction and study design. At these broader spatial scales (100–1000 km). but whether species subsequently persist and reproduce in such environments depends on a suitable water regime and water quality over long periods. 252–258. manuscript and Alan Lill. we have been able to provide an integrated assessment of the effects of waterbirds on propagule transport at landscape scales. Santamaria L.J. Green & Figuerola. Fritz H. The realized impact of dispersal by waterfowl on aquatic plant population dynamics is also difficult to evaluate without information on how dispersal subsequently translates into plant fitness (Figuerola & Green. Australian Ecosystems and Field and Game Victoria. East Gippsland Catchment Management Authority. Royal Botanic Gardens (Victoria).8 days in the Lake Eyre Basin (Roshier et al. 2002) and invertebrate propagules by waterfowl (60–1800 km. & Green A. & Green A. (2002) Biotic wetland connectivity – supporting a new approach for wetland policy. Gauthier-Clerc M.. & Bakker J. Primer-E Ltd. 72. This paper is contribution number 223 from the Australian Centre for Biodiversity. & Green A.I. (2010b) Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. (2002b) How frequent is external transport of seeds and invertebrates by Ó 2011 Blackwell Publishing Ltd. & Langevoord O.. Charalamabidou I.H. Freshwater Biology. Aquatic Botany. The maximum recorded distance flown by a Grey Teal within the range of retention times was 978 km in 1. (2009) The role of migratory ducks in the long-distance dispersal of native plants and the spread of exotic plants in Europe. Gauthier-Clerc M. (2002) Applying the seedling-emergence method under waterlogged conditions to detect the seed bank of aquatic plants in submerged sediments. (1980) Wetlands of Victoria I.. & Gorley R. ´a L. Gary Howard and Field and Game Australia members for their assistance. 121–128. 1390–1402 Acknowledgments This work was funded by ARC grant no.L.K. and seeds are likely to fall in unsuitable places for germination and survival if deposited en route. Monash University. Freshwater Biology. 56.M. 5.. Boedeltje G. Research was conducted under the specifications of the Department of Sustainability and Environment Wildlife Act Research Permit 10004314 and Monash University School of Biological Sciences Animal Ethics Committee application BSCI ⁄ 2008 ⁄ 19.J. Wetlands. Freshwater Biology. Birgita Hansen. & Green A.N.J. & Norman F. Figuerola J. Whether Grey Teal can actually fly 1800 km without a stopover or in-flight egestion is unknown. Guillemain M. References Amezaga J.L. 1–6. Guillemain M. 99–106. Holt Mueller & Van Der Valk. Brochet A.. & Santamarı for the potential of waterbirds as dispersers of aquatic organisms. Wetlands and waterbirds of the Snowy River and Gippsland Lakes catchment. & Green A.. 91. 32.1400 E. Gauthier-Clerc M. (2001) Primer v5. 47. 55. Cottrell T. 2002a). (2002a) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. West Gippsland Catchment Management Authority. 1262–1273. Plymouth. & Green A. Clarke K. Santamarı (2003) Effect of ingestion by five avian dispersers on the retention time.. U. retrieval and germination of Ruppia maritima seeds. We mimicked water regime conditions that simulate requirements for germination in moist or aquatic habitats. Corrick A. 93..R. Brochet A.. Acta Oecologia. We thank Andy Green and an anonymous reviewer for their comments on the . 25. Zachary Powell. Raulings et al.L.. Aquatic Botany.

. Angus and Robertson. (2008) The potential role of waterbirds in dispersing invertebrates and plants in arid Australia. 321– 322. & Chabreck R. 12. (2010) Internal dispersal of seeds by waterfowl: effect of seed size on gut passage time and germination patterns. (2003) A Census of the Vascular Plants of Victoria.I. 97. Norman F. University of Nebraska Press. Charalambidou I. SPSS Inc. Naturwissenschaften. 443–463. Archiv fur Hydrobiologie. New Zealand and Antarctic Birds. Geese and Swans of the World.. Norman F. 555–565.. with reference to plant population persistence in rivers.. (1981) Rates of recovery of bands. 177–189. (1990) Handbook of Australian.J. Figuerola J. (2005) Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. (1983) Grey Teal. Emu. Chicago. (2002) Ecomorphology and coexistence in dabbling ducks: the role of lamellar density and body length in winter.W..T. Norris K. Norman F. Santamaria L. (2002) The Slater Field Guide to Australian Birds. Singapore.A.A. 17. Sorensen A. (2003) Passive internal transport of aquatic organisms by waterfowl in Donana..I. Goodrick G. Ahern K. Figuerola J. 8.Plant dispersal by ducks 1401 waterbirds? A study in Donana. Anas castanea. Acta Oecologia. 262– 270. Green A. Food habits. 83. Asmus M. Science.. Australia. & Walsh N.I. 149– 156. (1968) Long-distance dispersal of seeds by retention in digestive tract of birds. 659–664. Haig S. National Herbarium of Victoria. 598–605. 90. & Slater R. Belcher C. Green A. Pollux B. 50. SPSS (2000) SYSTAT version 10. 557–565. & Powell D. 6. 4. Lincoln. Australian Wildlife Research. Grey Teal and Mountain Duck shot during Victorian open seasons.E. (1982) Food of the Chestnut Teal. Mehlman D.G.. Noble R. & Van Der Valk A.G. Ltd. 474–484. (2000) Spatial patterns of seed dispersal.D.G. 196.H. 319–324.H.. Figuerola J. Holt Mueller M.. in the Gippsland Lakes Region of Victoria. Sun C. 23. Ashford. 1390–1402 Nathan R. (2005) Differences in endozoochorous dispersal between aquatic plant species.. Ó 2011 Blackwell Publishing Ltd. Green A. Fisheries and Wildlife Division. Proctor V. Australian Wildlife Research.. Green A. (1968) Waterfowl in Australia. (2002) The potential role of ducks in wetland seed dispersal. South Yarra. (1959) The ecology of wild ducks in Inland New South Wales. Johnsgard P. Reeve and co. Sydney. Ministry for Conservation. Temby I. Slater P. 42. Fritz H. Figuerola J.C.C. Kent. 53. Guillon N. (1983) Vertebrate fauna of the Gippsland Lakes Catchment Victoria.M. Gormley A. Kraeuter H. & Oring L.. Journal of Ecology..N. Oikos.E. Freshwater Biology. (1978) Ducks. IL. 427–436.. (1930) The Dispersal of Plants Throughout the World. (2002) Implications of waterbird ecology for the dispersal of aquatic organisms. 22. & Green A. Oecologia. Green A. Global Ecology and Biogeography.M. Ridley H. 95. their determinants and consequences for recruitment.M. Wetlands. (2002) Comparative dispersal effectiveness of wigeongrass seeds by waterfowl wintering in south-west Spain: quantitative and qualitative aspects. Conservation Biology. Oxford University Press. (1979) Food of the Black Duck and Grey Teal in Coastal Northern New South Wales. 232– 242. 170–178.H.J. & Turnbull J.J. (1986) Seed dispersal by adhesion. 278– 284.. Annual Review of Ecology and Systematics.D. Freshwater Biology. & Walsh N. & Simon G. 989–1001. Melbourne. 150. Morris P. (1971) Movement and mortality of Black duck. Victorian Government.A.. Diversity and Distributions. 9.J. & Figuerola J.J. Transactions of the Royal Society of South Australia. East Melbourne. (1997) Effectiveness of three turacos as seed dispersers in a tropical montane forest. Csiro Wildlife Research.D. 547–551.J.J. 94–103..M. & Santamaria L. Slater P. Journal of Wildlife Management. duck and quail in Victoria: results from surveys of Victorian game license holders in 2009. 112.J. & Kingsford R. Marchant S. 15.I.A. & Higgins P.G..W. Ltd. 1953-77. Norman F. 155. III. Chestnut Teal.I.. south-west Spain..N. & Muller-Landau H. Victoria. 12. Jenkins K...J. Chestnut Teal and Pacific Black Duck at a saline habitat in Victoria. & Santamaria L. 1–7.J. (2008) What drives long-distance movements in the nomadic Grey Teal Anas gracilis in Australia? Ibis. Mountain duck and Grey Teal banded in South Australia.. Freshwater Biology. Mansergh I. New Holland Publishers (Australia) Pty. Roshier D. 11.R.. & Ouborg N. (1998) Avian movements and wetland connectivity in landscape conservation. (2009) Estimates of harvest for deer. Frith H.M. In: Occasional Paper Series Number 1. Powers K. (1978) Seed distribution by waterfowl in southwestern Louisiana. Santamaria L. harvest patterns and estimates for Black Duck. Ives A. 160.J.J. 380–392. Frith H.D. Australian Wildlife Research. Guillemain M. Trends in Ecology & Evolution. & Sanchez M. 151–155. 1953–1963. & Klaassen M. & Mumford L. 98. Arthur Rylah Institute for Environmental Research Technical series No.J. Ross J. & Moermond T. 749–758.. Bell D. SW Spain. 131–155. 56.

& Bonn S. 1390–1402 . Wetlands. 28. (Manuscript accepted 5 January 2011) Tackenberg O.. Wongsriphuek C. Roshier D. & Saunders G.D.P.. 290–299. (2004) The role of wild birds in the transmission of avian influenza for Australia: an ecological perspective. retention and germination.. (2003) Assessment of wind dispersal potential in plant species. 191–205. Dugger B. 316–319. 14. & Bartuszevige A. West P. 109–124. 104. Ó 2011 Blackwell Publishing Ltd. Tracey J.W.R.1402 E. Vivian-Smith G. (1994) Dispersal of salt marsh seeds on the feet and feathers of waterfowl. Wetlands. & Stiles E.. Raulings et al. Woods R. 56. Posschlod P. Freshwater Biology. 73. Emu. (2008) Dispersal of wetland plant seeds by Mallards: influence of gut passage on recovery. Ecological Monographs.M.A..