Data from: seed dispersal by frugivores without seed swallowing: evaluating the contributions of stomatochoric seed dispersers
- 1. University of Nottingham Malaysia Campus
- 2. Sálim Ali Centre for Ornithology and Natural History*
- 3. Ashoka Trust for Research in Ecology and the Environment
Description
The process of seed dispersal that underpins ecosystem maintenance is performed by diverse arrays of fruit-eating animals. However, seed dispersal studies are primarily focused on a subset of these animal communities that disperse seeds by endozoochory. Stomatochory (seed dispersal in which seeds are carried externally and are not swallowed) is rarely considered to be effective, despite an increasing number of taxa-focused studies that indicate otherwise.
We collated the available information on stomatochory to provide a quantitative overview of the dispersal mechanism, including plant-types and fruit-traits dispersed, dispersal distances and germination potential for all available taxa. We compared seed sizes dispersed, dispersal distances, and germination potential with corresponding data on endozoochory for bats and primates. We also identified the main taxa dispersing seeds by stomatochory and assessed what factors influenced the distances that they carried seeds to.
Stomatochoric dispersers can displace large quantities of seeds, including large seeds and those of large fruits, and over short to long distances (> 1 km). Compared to similar-sized endozoochoric dispersers, they can disperse larger seeds, but over shorter distances, on average. Similar to endozoochory, seed handling by stomatochory also improves the germination potential of dispersed seeds. Dispersal distances achieved by stomatochory were influenced by body mass, daily path length, seed width, fruit type and seed handling techniques.
Five main taxonomic groups of stomatochoric dispersers were identified: bats, parrots, squirrels, corvids and Old World monkeys (cercopithecines). Parrots perform dispersal services for the largest fruits and over the longest distances. However, given the lack of research on stomatochory, it is likely other taxa are also important stomatochoric dispersers but have not been identified yet.
More research attention must be directed towards seed dispersal services that are not provided by endozoochory. Many stomatochoric dispersers are common animals within communities and could be playing dominant seed dispersal roles, even without swallowing seeds. Community-wide studies should incorporate all seed dispersal interactions, rather than focusing solely on endozoochory. This will ensure a more robust understanding of community-wide patterns.
Methods
We searched for published articles reporting stomatochory observations using Google Scholar, Web of Science and Scopus. Searches included the words "seed carrying" or "pulp predators" or "pulp consumers" or "pulp feeders" or "stomatochory". We scanned the titles and abstracts of the papers to determine if they were likely to include information on stomatochory and extracted the appropriate information from the full paper. We also used these papers to identify taxa that regularly consumed pulp-only or often carried seeds away from parent crowns and conducted more intensive searches on these taxa (mainly primates, rodents, bats, parrots, corvids). We excluded papers on synzoochory and only included papers documenting carrying of fruits for the immediate consumption of pulp (e.g., by squirrels), or seeds (e.g., husking stations of rats). Ruminants are also identified as "seed spitters", but in these cases seeds are transported in the rumen and are a form of endozoochory so are not considered here (Delibes et al. 2019).
For each stomatochory interaction between animal species and plant species we recorded details on the type of stomatochory behaviour: (i) spat (seed stored within the mouth or cheek pouches, and then spat out once pulp is removed. The seed/s might be spat with mouthfuls of fruit fibre) (Aziz et al., 2021; Lambert, 1999), (ii) dropped (fruit is carried in the mouth, beak or by the feet (Tella et al. 2020) and pulp is removed externally, before the seed is dropped, or the seed might be dropped incidentally while traveling (Aziz et al. 2021, Blanco et al. 2015). We only recorded an interaction when the animal had been recorded to remove a seed from the vicinity of the parent plant on at least one occasion. The searches generated many papers of pulp feeding of birds, but only rarely was seed removal confirmed to occur; hence, these interactions were not included in the database.
When available, we also recorded details on intact rate (how many handled seeds were deposited undamaged), proportion of seeds removed beyond the canopy area, seed dispersal distances, seed germination, fruit and seed size, plant life-form and fruit-type; the trait data for plants was supplemented by searching for information from other sources. When a choice of data summary was available (e.g., for dispersal distance) we preferentially used medians, but some values represent mean since this was the only value available. We also collected data on germination tests for endozoochoric interactions involving cercopithecine primates and bats, as a comparison to the stomatochory data.
Literature cited
Aziz, S.A., McConkey, K.R., Tanalgo, K., Sritongchuay, T., Low, M.-R., Yong, J.Y., Mildenstein, T.L., Nuevo-Diego, C.E., Lim, V.-C., Racey, P.A., 2021. The Critical Importance of Old World Fruit Bats for Healthy Ecosystems and Economies. Frontiers in Ecology and Evolution 9. https://doi.org/10.3389/fevo.2021.641411
Blanco, G., Hiraldo, F., Rojas, A., Denes, F. V., Tella, J. L. 2015. Parrots as key multilinkers in ecosystem structure and functioning. Ecology and Evolution 5: 4141-4160. https://doi.org/10.1002/ece3.1663
Delibes M., Castaneda I, Fedriani J. M. 2019. Spitting seeds from the cud: a review of an endozoochory exclusive to ruminants. Frontiers in Ecology and Evolution 7 https://doi.org/10.3389/fevo.2019.00265
Lambert, J.E., 1999. Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit‐processing strategies and seed dispersal. American Journal of Physical Anthropology 109, 365–386. https://doi.org/10.1002/(SICI)1096-8644(199907)109:365
Tella, J.L., Hiraldo, F., Pacífico, E., Díaz-Luque, J.A., Dénes, F.V., Fontoura, F.M., Guedes, N., Blanco, G., 2020. Conserving the diversity of ecological interactions: The role of two threatened macaw species as legitimate dispersers of "megafaunal" fruits. Diversity 12, 45. https://doi.org/10.3390/d12020045
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