DOI: 10.5061/dryad.2rbnzs7x6
title: Plant and frugivore species characteristics drive frugivore contributions to seed dispersal effectiveness in a hyper-diverse community

description: Seed dispersal by frugivores is a crucial step of the life cycle of most
 plants, influencing plant population and community dynamics. Although very
 important for most ecosystems, we are just beginning to understand which
 are the mechanisms driving frugivore-mediated seed dispersal. Most studies
 identifying the drivers of seed dispersal use interaction frequency as a
 proxy for estimating seed dispersal success, rather than looking at the
 functional outcomes of those interactions (e.g., contributions to
 successful seed germination). A valuable tool to link plant-frugivore
 interactions to seed dispersal success is the seed dispersal effectiveness
 (SDE) framework, which accounts for the quantity and quality components of
 seed dispersal. We evaluated which mechanisms, including
 morphological traits, trait matching, and phenological overlap of
 interacting species, as well as the degree of frugivory and feeding
 behavior of frugivores, influenced the quantity (interaction frequency and
 number of seeds dispersed per visit) and quality (seed germination after
 gut passage) components of SDE. To this end, we combined three methods
 (focal observations, mist-netting, and camera traps) to sample
 interactions between plants, birds, and mammals in a species-rich
 community of Cerrado in southeastern Brazil. We recorded 590
 pairwise interactions between 34 plants and 49 frugivores. We found that
 phenological overlap among interacting species explained most of the
 variation in interaction frequencies. Trait matching affected the number
 of seeds dispersed per visit more for gulpers than mashers and peckers,
 and frugivore body mass and seed sizes positively affected seed
 germination. Finally, interaction frequencies had a stronger contribution
 to SDE, compared to the number of seeds dispersed per visit and seed
 germination, indicating an indirect effect of phenological overlap on
 SDE. We found that highly abundant plant-frugivore species with
 the most overlap in their phenologies also yield the highest values of
 SDE, suggesting that phenological overlap was the most important driver of
 SDE in our community. However, the number of seeds dispersed per visit
 also influenced SDE and seed germination was species-specific, suggesting
 that estimating SDE at the community level is necessary to understand how
 communities work, and the current and future challenges they face.
description: # Plant and frugivore species characteristics drive frugivore
 contributions to seed dispersal effectiveness in a hyper-diverse community
 Access this dataset on Dryad in DOI:10.5061/dryad.2rbnzs7x6 This dataset
 gathers plant-frugivore interactions, with their respective interaction
 frequencies and number of seeds dispersed per visit by frugivores for 171
 unique interactions between 34 plant and 49 frugivore species. It also
 contains seed germination probabilities and seed dispersal effectiveness
 (SDE) values for 38 unique interactions between 16 plants and 16 frugivore
 species. The data shown here was recorded in 6 sites within a species-rich
 neotropical savanna, the Cerrado, located in Southeast Brazil. Because we
 wanted to assess whether different plant and frugivore species
 characteristics influenced frugivore contributions to seed dispersal
 effectiveness in our community, the dataset also has a number of different
 plant-frugivore characteristics likely to affect each of the subcomponents
 of SDE and ultimately SDE. Specifically, we evaluated the effects of plant
 and frugivore morphological traits (body mass and seed sizes),
 phenological overlap and trait matching of interacting species, as well as
 animal degree of frugivory and feeding behavior, on interaction
 frequencies, the number of seeds dispersed per visit (SDE quantity
 component) and seed germination (SDE quality component), identifying which
 drivers explained most variation in frugivore contributions to SDE. ###
 Description #### 1.Dataset and 2.Partial\_dataset The
 **"1.Dataset**" contains the complete set of data with all 171
 plant-frugivore interactions, while **"2.Partial_dataset"**
 contains the 38 interactions for which we had values of seed germination
 and SDE. Also, both datasets have all plant-frugivore characteristics used
 in the models described in the data analysis section of the research
 paper. Please note that interaction frequencies and trait-matching values
 may differ between the complete and the partial dataset since the
 calculation of those variables depends on the set of interactions used.
 Each row represents an interaction, and columns show: *plantSp*: the
 scientific names of plant species recorded in the study. *animalSp*: the
 scientific names of frugivore species recorded in the study.
 *temp_overlap*: the number of months both plant and frugivore species were
 simultaneously present in the sites. *phe_overlap*: degree of temporal
 overlap between plant and frugivore species based on the abundance of
 interacting species co-occurring in the same month. For each pair of
 plant-frugivore species, we selected the minimum relative abundance of the
 interacting pair each month. Then, we added all minimum relative
 abundances across all months for each pair of species (Pleasants, 1990).
 *trait_matching*: a measure of how much plant and frugivore traits match.
 We used morphological plant and frugivore traits known to affect animal
 frugivory (gape/gullet size × fruit diameter, and fruit length × beak
 length; Dehling et al., 2014), and quantified trait matching of
 interacting partners using a multivariate trait congruence approach
 (Peralta, et al., 2020). To this end, we built a similarity matrix of
 morphological traits for plants and a similarity matrix of morphological
 traits for frugivore species using the Gower similarity coefficient
 (Gower, 1971) and the “vegdist” function from the vegan R package (Oksanen
 et al., 2022). Then, using the plant and frugivore trait similarity
 matrices and a binary species interaction matrix, we ran a Parafit test
 (Legendre et al., 2002) with the “parafit” function from the ape R package
 (Paradis et al., 2004). The Parafit test allowed us to assess whether
 frugivore species interact more frequently with plant species with similar
 traits, compared to a scenario where species interact randomly.
 *body_mass* (kg): the body mass of frugivores in kilograms (kg). The data
 on body masses were obtained from bird captures with mist nets, and for
 the frugivore species that failed to be captured, we used databases
 (Wilman et al., 2014; Bello et al., 2017; Souza et al., 2019; Tobias et
 al., 2022). When bird and mammal body masses were available from more than
 one source, we calculated average values considering all sources.
 *gape_width* (mm): the width of birds' beaks, and the width of
 mammals' mouths (i.e., gullet sizes; Fuzessy et al., 2022) in
 millimeters (mm). Gape widths and gullet sizes were obtained from bird
 captures with mist nets, databases (Wilman et al., 2014; Bello et al.,
 2017; Souza et al., 2019; Tobias et al., 2022), and measurements taken
 from museum specimens (3-10 individuals per species) at the USP Zoological
 Museum (MZUSP). When bird and mammal traits were available from more than
 one source, we calculated average values considering all sources.
 *beak_length* (mm): the length of birds' beaks in millimeters (mm).
 Beak lengths were obtained from bird captures with mist nets, databases
 (Wilman et al., 2014; Bello et al., 2017; Souza et al., 2019; Tobias et
 al., 2022), and measurements taken from museum specimens (3-10 individuals
 per species) at the USP Zoological Museum (MZUSP). When beak lengths were
 available from more than one source, we calculated average values
 considering all sources. Beak length is unavailable for mammals and marked
 with NA, as we could not find a good substitute for this specific trait
 that applied to mammals. *behavior*: frugivore feeding behavior,
 determined based on the most common behavior observed during interaction
 sampling. Specifically, for each plant-frugivore interaction, the
 frugivore was classified as a gulper when most of its feeding behavior
 toward the plant species consisted of swallowing entire fruits, as a
 masher when most fruits were crushed and mandibulated before ingestion,
 and as a pecker when the frugivore only pecked the fruit pulp without
 removing the seed (Levey, 1987; Moermond & Denslow, 1985).
 *degree_frugivory*: percentages of fruits in frugivore diets. We extracted
 the percentages of fruits in frugivore diets from Wilman et al. (2014) for
 birds and, when available, from diet reports for mammals (Bueno &
 Motta-Junior, 2004; Gayot et al., 2004; Pedrosa et al., 2019; Rodrigues da
 Silva et al., 2014). As we could not find values of frugivory degree for
 all frugivore species, a few rows have NAs. *nseeds*: the number of seeds
 contained inside fruits of each plant species. The number of seeds inside
 fruits was obtained from fruits collected in the study sites and are the
 rounded average values of 1-20 ripe fruits of 1-5 plant individuals of
 each species, according to their availability. *fruit_length* (mm): the
 length of fruits in millimeters (mm). Fruit length was measured as the
 maximum distance between the base of the fruit (where it was attached to
 the plant) to the apex, using a caliper (Pérez-Harguindeguy et al., 2013).
 *fruit_diameter* (mm): the diameter of fruits in millimeters (mm). Fruit
 diameter was measured as the maximum distance perpendicular to fruit
 length (considering how fruits were attached to the plant;
 Pérez-Harguindeguy et al., 2013). *seed_size* (mm): the largest dimension
 of seeds, considering seed length, diameter, and height
 (Pérez-Harguindeguy et al., 2013), in millimeters (mm). The dimensions of
 seeds were obtained from fruits collected in the study sites and are the
 average values from 1-20 ripe fruits of 1-5 plant individuals of each
 species, according to their availability. *int_frequency*: interaction
 frequency estimates for each pair of interacting species. Because we
 recorded plant-frugivore interactions using three different sampling
 methods (focal observations, captures with mist nets, and camera traps),
 we had to merge interaction frequencies using the grand total
 standardization method (Quintero et al., 2022). The grand total
 standardization approach transforms the interaction frequencies of each
 sampling method into the probability that a certain pairwise interaction
 will occur among all interactions sampled. To calculate it, we first
 weighted the number of interactions (i.e., visits) by dividing them by the
 corresponding effort in hours used to sample interactions for each method.
 Second, the values of each interaction frequency matrix were weighted by
 the total sum of interactions per hour recorded under each specific
 sampling method. Third, each interaction matrix was weighted by the
 sampling completeness corresponding to the specific sampling method. Once
 all matrices were weighted, we combined them to obtain a matrix
 representing species-interaction frequencies by calculating the average
 value for each pairwise interaction. *n_seeds_dispersed*: the number of
 seeds dispersed per visit by frugivores for each pair of interacting
 species. When we recorded more than one interaction between the same pair
 of species, we calculated the average values of seeds being dispersed per
 visit. When we recorded only one interaction between a pair of species, we
 used the unique value of seeds dispersed in that specific visit.
 *seed_germination* (only available in the partial dataset): the
 probability of seeds germinating after interactions. Those values were
 obtained from droppings collected from captured birds, droppings collected
 after fruit offering to captive birds of *Turdus leucomelas*, or droppings
 collected from easily identifiable frugivore species’ droppings in the
 field, i.e., when we saw the frugivore defecating or when feces were very
 characteristic of a certain animal species. Unfortunately, we were not
 able to estimate seed germination values for all of the recorded
 interactions, so this variable was only available in the partial dataset
 for unique 38 interactions. *SDE* (only available in the partial dataset):
 seed dispersal effectiveness values, i.e., the product of interaction
 frequencies, number of seeds dispersed per visit, and seed germination
 values. Because seed germination was only available for a subset of
 interactions, SDE is also only available in the partial dataset for 38
 unique interactions. #### 3.Data\_seed\_germ This dataset contains the raw
 seed germination data for seeds immersed in pulp (i.e., whole fruits),
 manually de-pulped (i.e., de-pulped), and passing through the guts of
 frugivores (i.e., gut passed). “AnimalSp” column is specific for
 gut-passed seeds and specifies the animal species interacting with the
 seed. Seeds and fruits were sowed in Petri dishes (9 cm diameter each)
 according to treatment (gut-passed, manually-depulped, and whole fruits).
 The number of seeds and fruits in each Petri dish depended on their sizes.
 For small seeds (&lt; 2 mm long), we included up to 300 seeds in each
 Petri dish, whereas for large seeds (&gt; 2 mm long), we included 10 to 30
 seeds per Petri dish. For fruits, we followed the same logic, including
 from 5 to 20 fruits per Petri dish, depending on fruit size. Petri dishes
 were stored in germination chambers set at 27 ° C and 12-12 dark-light
 hours and watered every 2–3 days. We considered a germination event when a
 seed showed the protrusion of the radicle. Seeds and fruits remained in
 germination chambers until seeds germinated or for a maximum of 6 months.
 Each row of this table represents an event when seeds were sowed into a
 petri dish, or in the case of gut-passed seeds, seeds contained in a
 single fecal sample from a single individual. *PlantSp*: the scientific
 names of the plant species from which seeds were sowed. *Treatment*: the
 treatment received by seeds. They could be seeds immersed in pulp (i.e.,
 whole_fruit), seeds manually de-pulped (i.e., de-pulped), and seeds
 passing through the guts of frugivores (i.e., gut_passed). *AnimalSp*: for
 seeds passing through the guts of frugivores, this column specifies
 frugivore species by their scientific names. NA rows here refer to
 treatments different from "gut_passed". *Seeded*: the number of
 seeds sowed for each specific treatment into Petri dishes. *Germinated*:
 the number of seeds that germinated after being sowed into Petri dishes.
 *Proportion*: the proportion of seeds that germinated from the total of
 seeds sowed. ### References Bello, C., Galetti, M., Montan, D., Pizo, M.
 A., Mariguela, T. C., Culot, L., Bufalo, F., Labecca, F., Pedrosa, F.,
 Constantini, R., Emer, C., Silva, W. R., Da Silva, F. R., Ovaskainen, O.,
 & Jordano, P. (2017). Atlantic frugivory: a plant–frugivore
 interaction data set for the Atlantic Forest. Ecology, 98(6), 1729.
 [https://doi.org/10.1002/ecy.1818](https://doi.org/10.1002/ecy.1818)
 Bueno, A. D. A., & Motta-Junior, J. C. (2004). Food habits of two
 syntopic canids, the maned wolf (*Chrysocyon brachyurus*) and the
 crab-eating fox (*Cerdocyon thous*), in southeastern Brazil. Revista
 Chilena de Historia Natural, 77(1), 5–14.
 [https://doi.org/10.4067/s0716-078x2004000100002](https://doi.org/10.4067/s0716-078x2004000100002) Dehling, D. M., Töpfer, T., Schaefer, H. M., Jordano, P., Böhning-Gaese, K., & Schleuning, M. (2014). Functional relationships beyond species richness patterns: Trait matching in plant-bird mutualisms across scales. Global Ecology and Biogeography, 23(10), 1085–1093. [https://doi.org/10.1111/geb.12193](https://doi.org/10.1111/geb.12193) Fuzessy, L., Sobral, G., Carreira, D., Rother, D., Barbosa, G., Landis, M., Galetti, M., Dallas, T., Cláudio, V. C., Culot, L., & Jodano, P. (2022). Functional roles of frugivores and plants shape hyper-diverse mutualistic interactions under two antagonistic conservation scenarios. Biotropica, 00, 1–11. [https://doi.org/10.1111/btp.13065](https://doi.org/10.1111/btp.13065) Gayot, M., Henry, O., Dubost, G., & Sabatier, D. (2004). Comparative diet of the two forest cervids of the genus *Mazama *in French Guiana. Journal of Tropical Ecology, 20, 31–43. [https://doi.org/10.1017/S0266467404006157](https://doi.org/10.1017/S0266467404006157) Gower, J. C. (1971). A general coefficient of similarity and some of its properties. Biometrics, 27(4), 857–871. [https://doi.org/10.2307/2528823](https://doi.org/10.2307/2528823) Legendre, P., Desdevises, Y., & Bazin, E. (2002). A Statistical test for host-parasite coevolution. Systematic Biology, 51(2), 217–234. [https://doi.org/10.1080/10635150252899734](https://doi.org/10.1080/10635150252899734) Levey, D. J. (1987). Seed size and fruit-handling techniques of avian frugivores. The American Naturalist, 129(4), 471–485. [https://doi.org/10.1086/284652](https://doi.org/10.1086/284652) Moermond, T. C., & Denslow, J. S. (1985). Neotropical avian frugivores: patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Ornithological Monographs, 36, 865–897. [http://www.jstor.org/stable/40168322%0Ahttp://www.jstor.org/page/info/about/policies/terms.jsp](http://www.jstor.org/stable/40168322%0Ahttp://www.jstor.org/page/info/about/policies/terms.jsp) Oksanen, J., Simpson, G. L., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Solymos, P., Stevens, M. H. H., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., Caceres, M., Durand, S., … Weedon, J. (2022). Package “vegan” (p. 297). Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20(2), 289–290. [https://doi.org/10.1093/bioinformatics/btg412](https://doi.org/10.1093/bioinformatics/btg412) Pedrosa, F., Bercê, W., Levi, T., Pires, M., & Galetti, M. (2019). Seed dispersal effectiveness by a large-bodied invasive species in defaunated landscapes. Biotropica, 00, 1–12. [https://doi.org/10.1111/btp.12706](https://doi.org/10.1111/btp.12706) Peralta, G., Vázquez, D. P., Chacoff, N. P., Lomáscolo, S. B., Perry, G. L. W., & Tylianakis, J. M. (2020). Trait matching and phenological overlap increase the spatio-temporal stability and functionality of plant–pollinator interactions. Ecology Letters, 23(7), 1107–1116. [https://doi.org/10.1111/ele.13510](https://doi.org/10.1111/ele.13510) Pérez-Harguindeguy, N., Díaz, S., Garnier, E., Lavorel, S., Poorter, H., Jaureguiberry, P., Bret-Harte, M. S., Cornwell, W. K., Craine, J. M., Gurvich, D. E., Urcelay, C., Veneklaas, E. J., Reich, P. B., Poorter, L., Wright, I. J., Ray, P., Enrico, L., Pausas, J. G., De Vos, A. C., … Cornelissen, J. H. C. (2013). New handbook for standardized measurement of plant functional traits worldwide. Australian Journal of Botany, 61(3), 167–234. [https://doi.org/10.1071/BT12225](https://doi.org/10.1071/BT12225) Pleasants, J. M. (1990). Null-model tests for competitive displacement: the fallacy of not focusing on the whole community. Ecology, 71(3), 1078–1084. [https://doi.org/10.2307/1937376](https://doi.org/10.2307/1937376) Quintero, E., Isla, J., & Jordano, P. (2022). Methodological overview and data-merging approaches in the study of plant–frugivore interactions. *Oikos*, 2022(e08379), 1–18. [https://doi.org/10.1111/oik.08379](https://doi.org/10.1111/oik.08379) Rodrigues da Silva, A., Forneck, E. D., Bordignon, S. A. de L., & Cademartori, C. V. (2014). Diet of *Didelphis albiventris* Lund, 1840 (Didelphimorphia, Didelphidae) in two periurban areas in southern Brazil. Acta Scientiarum - Biological Sciences, 36(2), 241–247. [https://doi.org/10.4025/actascibiolsci.v36i2.20444](https://doi.org/10.4025/actascibiolsci.v36i2.20444) Souza, Y., Gonçalves, F., Lautenschlager, L., Akkawi, P., Mendes, C., Carvalho, M. M., Bovendorp, R. S., Fernandes-Ferreira, H., Rosa, C., Graipel, M. E., Peroni, N., Cherem, J. J., Bogoni, J. A., Brocardo, C. R., Miranda, J., Zago da Silva, L., Melo, G., Cáceres, N., Sponchiado, J., … Galetti, M. (2019). ATLANTIC MAMMALS: a data set of assemblages of medium- and large-sized mammals of the Atlantic Forest of South America. Ecology, 100(10), e02785. [https://doi.org/10.1002/ecy.2785](https://doi.org/10.1002/ecy.2785) Tobias, J. A., Sheard, C., Pigot, A. L., Devenish, A. J. M., Yang, J., Sayol, F., Neate-Clegg, M. H. C., Alioravainen, N., Weeks, T. L., Barber, R. A., Walkden, P. A., MacGregor, H. E. A., Jones, S. E. I., Vincent, C., Phillips, A. G., Marples, N. M., Montaño-Centellas, F. A., Leandro-Silva, V., Claramunt, S., … Schleuning, M. (2022). AVONET: morphological, ecological and geographical data for all birds. Ecology Letters, 25(3), 581–597. [https://doi.org/10.1111/ele.13898](https://doi.org/10.1111/ele.13898) Wilman, H., Belmaker, J., Simpson, J., de la Rosa, C., Rivadeneira, M. M., & Jetz, W. (2014). EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology, 95(7), 2027–2027. [https://doi.org/10.1890/13-1917.1](https://doi.org/10.1890/13-1917.1)