Germination ecology and seed dispersal of a critically endangered plant: a case study of Pomaderris vacciniifolia (Round-leaf Pomaderris)

Change in ecosystem disturbance regimes from human land-use poses a worldwide problem for management of rare species. Two important types of disturbance influencing the persistence of species in Australian ecosystems are habitat fragmentation and fire. In this study, seed dispersal and the germination ecology of Pomaderris vacciniifolia-a critically endangered, rare endemic Australian shrub-were examined to identify likely influences of fire and fragmentation on the decline of populations. The response of seed germination to simulated effects of wildfire and canopy openings was investigated, as was the unaided dispersal capability of seeds from parent plants. A significant increase in germination rate was observed following 100°C heat treatment to seeds, while smoke and light exposure had little influence. Seed imbibition was strongly influenced by heat treatment. The findings indicate a likely positive post-fire germination response, with implications for recruitment success determined by moisture availability following fire. Unaided seed dispersal was limited, which partly explains the apparent decline of populations. Understanding disturbance requirements for threatened species, and subsequent management of landscapes for disturbance, will aid conservation of rare species throughout the world.

Seed dispersal potential by wild mallard duck as estimated from digestive tract analysis

Dispersal of plant seeds by ducks and other waterbirds is of great importance to the ecology of freshwater habitats. To unravel the mechanisms of waterbird-mediated seed dispersal, numerous laboratory experiments have been conducted, but effects of seed and waterbird traits on dispersal potential have rarely been investigated under field conditions. Through analysis of the digestive tracts of 100 wild mallards (Anas platyrhynchos) across a winter season in the Netherlands, we assessed (i) the inter-individual and seasonal variability of seeds in the digestive tract, (ii) the variability of digestive tract organ size and gizzard grit mass, and (iii) the potential effects of seed species traits and gut traits on the survival potential of ingested seeds. We found 4548 ingested seeds of at least 66 plant species from a wide range of habitats, most of which were retained in the gizzard. Nineteen species had not previously been reported from mallard diets. Individual tracts contained anywhere between 0 and 1048 seeds, of up to 14 species (median of three species). Diet composition and digestive tract size varied substantially between individuals and over the course of the winter season. As predicted from controlled feeding studies, we found that also in wild mallards, size-dependent gut passage survival favours the dispersal of small-seeded species. Despite the large variation in gizzard and small intestine size in this study, their effect on the dispersal potential of ingested seeds in the field remains unclear. We found no difference in dispersal potential between plants species growing in wet or dry habitats. This study demonstrates that wild mallards are opportunistic seed consumers with a very diverse diet as reflected by seed species composition in both the foregut and hindgut. However, we also show that serious limitations of field-based analyses compared to controlled experiments can impede drawing conclusions about gut passage survival of seeds. The large variability in diet composition among individuals and over time indicates high endozoochorous dispersal potential for a wide range of plant species by wild mallard in aquatic and wetland, as well as surrounding terrestrial habitats.

Small seed size increases the potential for dispersal of wetland plants by ducks

1. Long-distance dispersal (LDD) is important in plants of dynamic and ephemeral habitats. For plants of dynamic wetland habitats, waterfowl are generally considered to be important LDD vectors. However, in comparison to the internal (endozoochorous) dispersal of terrestrial plants by birds, endozoochorous dispersal of wetland plants by waterfowl has received little attention. We quantified the capacity for endozoochorous dispersal of wetland plants by waterfowl and identified the mechanisms underlying successful dispersal, by comparing the dispersal capacities of a large number of wetland plant species.

2. We selected 23 common plant species from dynamic wetland habitats and measured their seed characteristics. We fed seeds of all species to mallards (Anas platyrhynchos), a common and highly omnivorous duck species, and quantified seed gut survival, gut passage speed and subsequent germination. We then used a simple model to calculate seed dispersal distances.

3. In total 21 of the 23 species can be dispersed by mallards, with intact seed retrieval and subsequent successful germination of up to 32% of the ingested seeds. The species that pass fastest through the digestive tract of the mallards are retrieved in the greatest numbers (up to 54%) and germinate best (up to 87%). These are the species with the smallest seeds. Seed coat thickness plays only a minor role in determining intact passage through the mallard gut, but determines if ingestion enhances or reduces germination in comparison to control seeds.

4. Model calculations estimate that whereas the largest seeds can hardly be dispersed by mallards, most seeds can be dispersed up to 780 km, and the smallest seeds up to 3000 km, by mallards during migration.

5. Synthesis. This study demonstrates the mechanism underlying successful endozoochorous dispersal of wetland plant seeds by mallards: small seed size promotes rapid, and hence intact and viable, passage through the mallard gut. Mallards can disperse wetland plant seeds of all but the largest-seeded species successfully in relatively large numbers (up to 32% of ingested seeds) over long distances (up to thousands of kilometres) and are therefore important dispersal vectors.

Consequences of intraspecific seed-size variation in Sparganium emersum for dispersal by fish

1. The potential for seed dispersal by fish (ichthyochory) is likely to vary within aquatic plant species, depending on intraspecific variation in phenotypic seed traits.

2. We studied the effect of seed size variation within the unbranched burreed (Sparganium emersum) on the potential for internal dispersal by the common carp (Cyprinus carpio), by feeding them light (< 10 mg), medium (10–20 mg) and heavy ( > 20 mg) seeds, seed mass being positively related to seed size.

3. We hypothesized: (i) that ingestion, retention time, survival during gut passage and viability after gut passage of S. emersum seeds would be affected by seed size; and (ii) that this would translate into intraspecific variation in dispersal probability and dispersal distance among seed size categories.

4. Ingestion was negatively related to seed size, while survival during gut passage was positively related to seed size. Seed viability after gut passage was not affected by seed size. Since the negative effect of ingestion was counterbalanced by an equally strong but positive effect on seed survival, the probability of dispersal did not differ between the tested seed-size categories.

5. The time that seeds remained in the digestive tract of carp did not differ between seed sizes, suggesting equal potential dispersal distances for all seeds. Based on optimum swimming speeds of carp, ranging from 0·9 to 1·8 km h−1, maximum dispersal distances will most likely range from 13·5 to 27 km.

6. This study highlights the importance of studying all stages of the endozoochorous dispersal process in order to estimate the effect of a phenotypic seed trait on plant dispersal.

The effect of seed morphology on the potential dispersal of aquatic macrophytes by the common carp (Cyprinus carpio)

1. The potential for seed dispersal by fish (ichthyochory) will vary among aquatic plants because of differences in seed size and morphology.

2. To examine how seed morphology influences the probability of dispersal by the common carp (Cyprinus carpio), we studied seed ingestion, retention time and subsequent egestion and germination of seeds of Sparganium emersum and Sagittaria sagittifolia, two aquatic plant species with similar sized but morphologically different seeds.

3. We compared dispersal probabilities between the two plant species, in which the probability of dispersal is assumed to be a function of the probabilities of seed ingestion, egestion and germination, and the dispersal distance is assumed to be a function of seed egestion rate over time.

4. We found that, although the soft seeds of S. sagittifolia had an approximately 1.5 times higher probability of being ingested by the carp than the hard seeds of S. emersum (83.15% ± 1.8% versus 56.16% ± 2.7%, respectively), the latter had an almost twofold higher probability of surviving the passage through the digestive tract (38.58% ± 2.7% versus 20.97% ± 1.5%, respectively). Patterns of seed egestion over time did not differ between the two plant species, despite the difference in seed morphology. Gut passage had a different effect on seed germination between plant species. Compared with non-ingested controls, seeds of S. emersum showed a 12.6% increase in germination and a 2.1 day acceleration in germination rate, whereas seeds of S. sagittifolia displayed a 47.3% decrease and 5.1 day delay, respectively.

5. Our results suggest that seed morphology affects the dispersal probability and postdispersal establishment, but not the dispersal distance, of aquatic plants that are dispersed by fish.

Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds

Many plant seeds and invertebrates can survive passage through the digestive system of birds, which may lead to long distance dispersal (endozoochory) in case of prolonged retention by moving vectors. Endozoochorous dispersal by waterbirds has nowadays been documented for many aquatic plant seeds, algae and dormant life stages of aquatic invertebrates. Anecdotal information indicates that endozoochory is also possible for fully functional, active aquatic organisms, a phenomenon that we here address experimentally using aquatic snails. We fed four species of aquatic snails to mallards (Anas platyrhynchos), and monitored snail retrieval and survival over time. One of the snail species tested was found to survive passage through the digestive tract of mallards as fully functional adults. Hydrobia (Peringia) ulvae survived up to five hours in the digestive tract. This suggests a maximum potential transport distance of up to 300 km may be possible if these snails are taken by flying birds, although the actual dispersal distance greatly depends on additional factors such as the behavior of the vectors. We put forward that more organisms that acquired traits for survival in stochastic environments such as wetlands, but not specifically adapted for endozoochory, may be sufficiently equipped to successfully pass a bird's digestive system. This may be explained by a digestive trade-off in birds, which maximize their net energy intake rate rather than digestive efficiency, since higher efficiency comes with the cost of prolonged retention times and hence reduces food intake. The resulting lower digestive efficiency allows species like aquatic snails, and potentially other fully functional organisms without obvious dispersal adaptations, to be transported internally. Adopting this view, endozoochorous dispersal may be more common than up to now thought.

A simple parametric method for reducing sample sizes in gut passage time trials

Seed dispersal is now regularly analyzed using spatially explicit models, relying in part on frugivore gut passage times to produce model outputs. In determining species-specific gut passage times, there is a trade-off in sample size between minimizing collection effort and maintaining statistical reliability. Here we demonstrate that a two-parameter lognormal parametric distribution reliably fits empirical gut passage time distributions and is easily parameterized using relatively small data sets of approximately 30 defecations. We suggest this approach as a statistically reliable substitute for larger empirical gut passage data sets in seed dispersal modeling, and also as a way of using published gut passage data sets to parameterize new models.

Attitudes and knowledge of shade-coffee farmers towards vertebrates and their ecological functions.

The purpose of this study was to assess farmers’ attitudes, as well as perceptions and knowledge that shape those attitudes, toward the ecological role of vertebrates inhabiting shaded-coffee farms. We also aimed to determine whether differences existed among two groups of farmers: one that had attended environmental education workshops, and one that had not. We conducted 36 oral interviews of farmers in the region of Cuetzalan, Mexico. All farmers were members of an important regional cooperative, Tosepan Titataniske. In general, farmers’ attitudes towards birds were positive. Snakes were perceived as useful but dangerous animals. Attitudes towards nonflying mammals were mostly indifferent. Bats were poorly understood and badly perceived. Seed dispersal was perceived as an important ecological function performed by animals. Pollination was also perceived as important, but to a lesser degree. Knowledge about ecological functions was high for seed dispersal, and low for pollination. We found a positive correlation between attendance of educational workshops and the presence of “environmentally-friendly” attitudes, perceptions, and knowledge. However, a cause-effect relationship could not be clearly established. We suggest that environmental education programs include the objective of increasing the knowledge of people about the ecological functions played by different groups of animals that live in agroecosystems. Particular efforts should be directed toward improving the way in which certain non-charismatic groups of animals, such as bats, are perceived.

Non-linear effects of landscape properties on mistletoe parasitism in fragmented agricultural landscapes

Ecological processes such as plant–animal interactions have a critical role in shaping the structure and function of ecosystems, but little is known of how such processes are modified by changes in landscape structure. We investigated the effect of landscape change on mistletoe parasitism in fragmented agricultural environments by surveying mistletoes on eucalypt host trees in 24 landscapes, each 100 km² in size, in south-eastern Australia. Landscapes were selected to represent a gradient in extent (from 60% to 2% cover) and spatial pattern of remnant wooded vegetation. Mistletoes were surveyed at 15 sites in each landscape, stratified to sample five types of wooded elements in proportion to their relative cover. The incidence per landscape of box mistletoe (Amyema miquelii), the most common species, was best explained by the extent of wooded cover (non-linear relationship) and mean annual rainfall. Higher incidence occurred in landscapes with intermediate levels of cover (15–30%) and higher rainfall (>500 mm). Importantly, a marked non-linear decline in the incidence of A. miquelii in low-cover landscapes implies a disproportionate loss of this species in remaining wooded vegetation, greater than that attributable to decreasing forest cover. The most likely mechanism is the effect of landscape change on the mistletoebird (Dicaeum hirundinaceum), the primary seed-dispersal vector for A. miquelii. Our results are consistent with observations that habitat fragmentation initially enhances mistletoe occurrence in agricultural environments; but in this region, when wooded vegetation fell below a threshold of ~15% landscape cover, the incidence of A. miquelii declined precipitously. Conservation management will benefit from greater understanding of the components of landscape structure that most influence ecological processes, such as mistletoe parasitism and other plant–animal mutualisms, and the critical stages in such relationships. This will facilitate action before critical thresholds are crossed and cascading effects extend to other aspects of ecosystem function.

Simplification of arboreal marsupial assemblages in response to increasing urbanization

Arboreal marsupials play an essential role in ecosystem function including regulating insect and plant populations, facilitating pollen and seed dispersal and acting as a prey source for higher-order carnivores in Australian environments. Primarily, research has focused on their biology, ecology and response to disturbance in forested and urban environments. We used presence-only species distribution modelling to understand the relationship between occurrences of arboreal marsupials and eco-geographical variables, and to infer habitat suitability across an urban gradient. We used post-proportional analysis to determine whether increasing urbanization affected potential habitat for arboreal marsupials. The key eco-geographical variables that influenced disturbance intolerant species and those with moderate tolerance to disturbance were natural features such as tree cover and proximity to rivers and to riparian vegetation, whereas variables for disturbance tolerant species were anthropogenic-based (e.g., road density) but also included some natural characteristics such as proximity to riparian vegetation, elevation and tree cover. Arboreal marsupial diversity was subject to substantial change along the gradient, with potential habitat for disturbance-tolerant marsupials distributed across the complete gradient and potential habitat for less tolerant species being restricted to the natural portion of the gradient. This resulted in highly-urbanized environments being inhabited by a few generalist arboreal marsupial species. Increasing urbanization therefore leads to functional simplification of arboreal marsupial assemblages, thus impacting on the ecosystem services they provide.

A review of the conservation ecology of round-leaf Pomaderris Pomaderris vacciniifolia F. Muell. ex Reissek (Rhamnaceae)

Round-leaf Pomaderris Pomaderris vacciniifolia F. Muell. ex Reissek (Rhamnaceae) is a Victorian endemic shrub listed as threatened under the Flora and Fauna Guarantee Act 1988 and critically endangeredunder the Environment Protection and Biodiversity Conservation Act 1999. A review of the available literature for P. vacciniifolia indicated most information is anecdotal or found in unpublished works. Better understanding of the ecology of P. vacciniifolia may help explain why it is vulnerable, and enhance future management. Future research should focus towards better understanding of P. vacciniifolia habitat, reproductive ecology, seed dispersal mechanisms and competitive ability and how these compare with more common sympatric congeners, to determine whether any differences could explain the relative success of these species. Targeted searches for this species on public and private land are warranted to reveal additional populations and fully appreciate the distribution of this species. (The Victorian Naturalist 131 (2) 2014, 44-51).

The restricted seed rain of a mistletoe specialist

Specialist frugivores are the dominant consumers of mistletoe fruit in many regions and have been shown to intensify infections of host plants as a result of their rapid gut passage rates and dependence on existing infections. The role of specialist frugivores in long distance dispersal of mistletoe and establishment of new infections is unclear, and has not been explicitly evaluated previously. Here we critically examine the premise that specialists are the dominant dispersers by examining the role of an Australian mistletoe specialist (mistletoebird Dicaeum hirundinaceum Dicaeidae) in dispersing mistletoe (Amyema preissii Santalales: Loranthaceae) seeds beyond infected host stands. We use two primary lines of evidence - presence of birds using remote call recorders, and presence of dispersed seeds via surveys for defecated seeds on host branches. The observed and inferred movements of the mistletoebird were wholly restricted to habitat patches containing mistletoe, and this bird was not observed to transport seeds to nearby uninfected host stands within the study system. While mistletoe specialists may provide much of the within-stand dispersal service for mistletoes, this serves only to aggregate and intensify existing infections. We suggest that long distance dispersal of mistletoe seeds beyond existing hosts and infection centres is not performed by these dietary specialists, these services more likely to be provided by generalist frugivores and other occasional mistletoe fruit consumers.

Seagrass viviparous propagules as a potential long-distance dispersal mechanism

Resilience of seagrass meadows relies on the ability of seagrass to successfully recolonise denuded areas or disperse to new areas. While seed germination and rhizome extension have been explored as modes of recovery and expansion, the contribution of seagrass viviparous propagules to meadow population dynamics has received little attention. Here, we investigated the potential of seagrass viviparous propagules to act as dispersal vectors. We performed a series of density surveys, and in situ and mesocosm-based experiments in Port Phillip Bay, VIC, Australia, using Zostera nigricaulis, a species known to produce viviparous propagules. Production of viviparous propagules was higher at sites with high wind and current exposure, compared to more sheltered environments. A number of propagules remained buoyant and healthy for more than 85 days, suggesting the capacity for relatively long-distance dispersal. Transplanted propagules were found to have improved survivorship within seagrass habitats compared to bare sediment over the short term (4 weeks); however, all propagules suffered longer-term (<100 days) mortality in field experiments. Conditions outside of meadows, including sediment scouring, reduced the likelihood of successful colonisation in bare sediment. Furthermore, sediment characteristics within meadows, such as a smaller grain size and high organic content, positively influenced propagule establishment. This research provides preliminary evidence that propagules have the potential to act as an important long-distance dispersal vector, a process that has previously gone unrecognised. Even though successful establishment of propagules may be rare, viviparous propagules show great potential for seagrass populations given they are facing global decline. © 2014 Coastal and Estuarine Research Federation.

Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe - a critical review of possibilities and limitations

We review whether migratory Anatidae, i.e., swans, geese and ducks, could be acting as vectors for dispersal of Zostera, Ruppia and Potamogeton propagules by endozoochory (carrying seeds in their guts). We list six prerequisites that must all be fulfilled, if successful dispersal should occur. Several Anatidae species feed on these macrophytes, and undertake rapid long-distance movements, making dispersal possible. We identify four problems, which in combination leads us to conclude that long-distance dispersal events are likely to be rare. (i) Most long-distance movements are out of phase with the reproductive efforts of the plants, and if birds arrive at sites when plants still bear seeds, they are likely to depart well after seed stocks have been depleted. (ii) Seed transport by birds will usually be uni-directional, from north to south on autumn migrations. (iii) Most of the gut contents of migratory birds are likely to have been discarded within 300 km of departure. (iv) In many cases, birds will arrive in habitats seriously different from those they departed, i.e., any seeds carried along will have low chances of surviving in their new site. We suggest that northbound dispersal by endozoochory can only occur during spring if waterbirds feed on seeds that have not been depleted and remained frozen down or buried in sediments, or during moult- or post-moult migrations. Moult migration takes place in summer in phase with the reproductive efforts of the plants. Also epizoochorous dispersal (external attachment) is subject to restrictions i, ii and iv.