Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 1 Animal-Plant Interaction: A Review On Terrestrial Vertebrate Seed Disperser Diversity And The Daniel R. NDIZIHIWE Assistant lecturer, Department of Agriculture and Selectivity Pattern Based On The Size Of Fruits And Seeds Agribusiness, Bishop Stuart University P.O BOX 9, Mbarara Uganda Achille E. ASSOGBADJO Professor, Laboratory of Applied Ecology, Faculty of Agronomic Sciences, University of Abomey Calavi, Benin Sylvestre C. A. M. DJAGOUN Lecturer, Laboratory of Applied Ecology, Faculty of Agronomic Sciences, University of Abomey Calavi, Benin Barthélémy KASSA Laboratory of Applied Ecology, Faculty of Agronomic Sciences, University of Abomey Calavi, Benin www.researchjournali.com Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 ABSTRACT The study was based on 107 studies and data concerning disperser species, plant species and family, fruit type and size, seed size plant life form and the habitat, were presented in matrix form. Data from this matrix were used in determining the disperser species diversity considering large taxonomic groups (mammals, birds and reptiles) and selection pattern based on the fruit and seed size. The diversity of mammals was high followed by birds and then reptiles with 65%, 30% and 5% respectively. Mammal taxonomic group dominated and was sub divided into primates, ungulates, carnivores, rodents and bat sub-groups which accounted for 45%, 22%, 17%, 9% and 7% respectively confirming the dominance of primates. Simple correspondence analysis showed that ungulates dispersed very small fruits while carnivores, primates, bats and reptiles were categorized together for both small and medium sized fruits. Ungulates, birds and bats dispersed the smallest seeds while others dispersed both small and large sized seeds. The study revealed high diversity of mammals particularly primates therefore playing a huge role in structuring and restructuring terrestrial ecosystems, with a warning that the loss of ungulates may have catastrophic impacts on the structure and composition of small fruited and seeded plants. Key words: Terrestrial vertebrates, seed dispersal, seed and fruit size 1. INTRODUCTION Animal and plant traits were the products of coevolution according to the preliminary conceptual treatments of fruits and frugivores coevolution (Bongers et al. 2013), thus, Zoochory accounts for the highest percentage (57%) of terrestrial seed dispersal (Diogo et al. 2016) but less is known about how some characteristics mediate this relationship (McConkey et al. 2012, Trolliet et al. 2013, Kuhlmann and Ribeiro 2016). The composition of seed banks in terms of species is strongly influenced by vertebrate seed dispersers (Jordano 2013, Wandrag et al. 2015) but there is a lack in understanding the diversity of these dispersers in terms of species. Loss of big and medium-sized frugivores reduces dispersal distance (Pérez-Méndez et al. 2016) as well as massive loss of trees (Estrada and Fleming 2012, Caughlin et al. 2015), hence affecting plant species distribution across ecosystems and landscapes. Functional complementarity between species (Tilman and Snell-Rood 2014) facilitates seed dispersal implying the importance of species richness (García and Martínez 2012, Poisot et al. 2013) where high disperser species diversity maintains stable ecosystem (Baur 2014, Reid et al. 2015). Fruit and seed characteristics also play an important role in determining the preferences of frugivorous animals (Aslan and Rejmanek 2012, Valenta et al. 2013) and the differences in these fruit and seed characteristics explains why some plants are more adapted to dispersal by some groups of animals but not others (Estrada and Fleming 2012). Seed size is one of the factors that influence seed dispersal patterns in animal-dispersed plants (Lai et al. 2014). Likewise, the size of the fruit may determine the animal groups adapted for its dispersal (Flörchinger et al. 2010, Burns 2013) but the relationship between the seed and fruit size and the disperser group www.researchjournali.com 2 Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 associated has not yet been elaborated. This study focused on collection, extracting and supplementing data from various published articles. In this case, the data looked almost primary (Alsheikh-Ali et al. 2011) and aimed at elaborating on the diversity of terrestrial vertebrate seed dispersers, relationship between fruit and seed size characteristic and the type of animal dispersal agent involved. 2. METHODS Only published studies were electronically searched and sorted to get the appropriate ones and a total of 441 articles was obtained and re-screened to get the more appropriate ones. 107 studies were retained and data was extracted based on the set parameters which included terrestrial vertebrate disperser taxonomic groups, sub taxonomic groups in case of mammals, plant species and families, plant life forms, fruit type and size (mm), the seed size (mm) and habitat type. All these parameters were extracted from all the articles and presented in matrix as well as indicating the authors and the year of publication. The final set up took a form of primary data (Alsheikh-Ali et al. 2011) The missing information such as seed size, fruit size, plant life form and plant families were searched electronically. Blank spaces were left in case of failure to find the required data. (APPENDIX 1). The number of species for each vertebrate taxonomic group (birds, mammals and reptiles), the number of plant families and plant species associated with each vertebrate taxonomic group was determined and presented in Microsoft excel spreadsheet. Mammals were thereafter sub-divided into different groups (primates, ungulates, bats, rodents, and carnivores) because they showed high dominance in the first instance. Likewise, the number of species for each mammalian group, the number of plant families and species associated with each mammalian group was determined and presented in Microsoft excel spread sheet. The size of the fruits and seeds were rarely presented in the studies reviewed. It therefore required direct internet search for this data to fulfil the set objective. To proceed with this, the frequency of interactions was used (Vázquez et al. 2015) where the size (mm) of both fruits and seeds was organized in ranges/classes and the frequency of vertebrate groups that fell in each range/class was considered to determine the most frequent taxonomic group in each size range. For fruits, the size ranges considered were; <5, 5-10, 10.1-20, 20.1-30, 30.1-40, 40.1-50 and 50.1-100. For the case of seeds, the size ranges considered were; <1, 1-5, 5.1-10, 10.1-20, 20.1-30, >30. At this level, terrestrial vertebrate disperser categories considered were; birds, primates, rodents, bats, ungulates and reptiles. Data was arranged in Microsoft excel spreadsheet as size ranges (mm) with the frequency of each of the disperser group considered. 3. RESULTS 3.1 TAXONOMIC GROUP DIVERSITY www.researchjournali.com 3 Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 4 A total of 104 terrestrial vertebrate species was recorded, of which birds accounted for 30%, mammals 65% and lastly reptiles with only 5% (figure1 part A). This showed a high species diversity in the group of mammals (68 species) followed by birds (31 species) and then reptiles (5 species). Figure 1: Large terrestrial vertebrate taxonomic groups and the associated plant species and families A 5% Birds 30% Mammals Reptiles 65% No of plant species and families B 200 100 0 Birds Mammals Reptiles Taxonomic groups Number of plant families Number of plant species 3.2 MAMMALIAN DIVERSITY The species diversity in this case was high in primate subgroup which accounted for 45% (34) of the total number of species within the group. However, the dominance was not very high in comparison to the first instance where mammals over dominated birds and reptiles. Here, ungulates accounted for 22% and also carnivores with 17%, the least being rodents and bats with 9% and 7% respectively. Figure 2: Mammalian sub groups and the associated plant species and families A Primates 7% 9% 17% 22% Angulates 45% Carnivores Rodents Bats www.researchjournali.com Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 No of plant species and families 5 B 100 50 0 Primates Angulates Carnivores Rodents Bats Mammalian subgroups Number of plant families Number of plant species 3.3 FRUIT SIZE AND ASSOCIATED DISPERSERS Carnivores, primates, bats reptiles and to the small extent birds were associated with the fruit size ranges of 510, 10.1-20 and 20.1-30 while ungulates were classed in the <5 size range. Rodents dispersed fruits ranging from 40.1-50 and >100 but data was not sufficient enough to be relied on as opposed to ungulates that were accompanied by enough and reliable set of data. The size range of 50.1-100 was not associated to a specific vertebrate group. It can be noted that there was no clear difference in fruit sizes predated by different terrestrial vertebrate groups except a clear distinction in ungulates that predated small fruits of <5mm. Figure 3: The fruit size ranges and the terrestrial vertebrate dispersers 3.4 SEED SIZE AND ASSOCIATED DISPERSERS The ungulates, birds and to smaller extent bats dispersed small sized seeds (<5 and 1.0-5.0mm). Rodents, reptiles and carnivores dispersed seed sizes of 10.1-20.0 and >30mm, but rodents dispersed seeds of >30mm contrary to reptiles and carnivores that are much close to the dispersion of 10.1-20.0 mm sized seeds. Finally, the isolated vertebrate group of primates was found to be dispersing seeds of 5.1-10.0 and 20.1-30.0mm and this was the only vertebrate group to dispersed both small and large seeds in significant numbers. Briefly, ungulates and birds are observed as the dispersers of small seeded plants while the big seeded plants may be dispersed by rodents, primates and to the smaller extent by carnivores, other groups being intermediates www.researchjournali.com Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 6 Figure 4: The seed size ranges and the terrestrial vertebrate dispersers 4. DISCUSSION 4.1 TAXONOMIC GROUP DIVERSITY Vertebrate dispersal exerts a strong role in the identity of seeds and seed banks (Wandrag et al. 2015). Species richness is the only factor for the frugivore assemblage that affects the probability of seed dispersal in degraded landscapes (García and Martínez 2012). Findings showed that the vertebrate disperser species diversity is proportional to the plant species dispersed due to functional complementarity between these species (García and Martínez 2012). Mammals play a great role in seed dispersal compared to others due to their high diversity (Matias et al. 2010, McConkey et al. 2014). Most plants produce fleshy fruits (Greenberg and Walter 2010) that are preferred by mammals (Koike et al. 2008) and this partly explains why mammalian species diversity was higher than birds and reptiles. Therefore extinction of mammals is disastrous to the structure and composition of plant communities in various ecosystems (Wang et al. 2007). Birds are also greatly involved in seed dispersal (Garcia et al. 2010, Heleno et al. 2011). Ecosystem fluxes and mechanisms separated by times and distances are effectively linked by birds because of their ability to fly (Whelan et al. 2008). The species diversity in reptile group was less possibly due to diet selectivity and less information available on the species that makes it up (Godinez-Alvarez 2004), thus less number (13) of plant species. Galàpagos tortoises are important in ecosystem structuring due their ability to regularly move large quantities of seeds over reasonably long distances to places favorable for new plant establishment (Blake et al. 2012). 4.2 MAMMALIAN DIVERSITY The dominance of primates was because fruits are their favourite food (Chapman and Russo 2007). Recent research has shown that primates provide unique seed dispersal services that cannot be compensated for by any other taxa (Clark et al. 2001). Despite this indispensable role, half of the world’s primates is threatened (Aslan 2013) and this implies the need for adaptive conservation measures (Lambert 2011). Ungulates can play a crucial role in dynamics of plant community (Albert et al. 2015) and they do not primarily target fruits unlike most of the primates, they instead search for fleshy leaves and stem parts and end up dispersing seeds www.researchjournali.com Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 accidentally by either endo-zoochory or epi-zoochory (Albert et al. 2015). Carnivores not only disperse seeds (Koike et al. 2008) from their parent plants but also enhance germinability (Aronne and Russo 1997). The findings shows that carnivores accounted for 17% (13 species) of all mammal species recorded and effectively dispersed 34 plant species from 23 families, most of which were large seeded plants, thus they have a remarkable effect on forest dynamics (Nakashima et al. 2010). Carnivorous low species diversity in comparison with primates and ungulates could be explained by their preferred diet which is dominated by meat (Pereira et al. 2014). Rodents and bats were represented by the small number of species, 7 and 5 that dispersed 6 and 5 plant species respectively. This number looked low but it did not mean less participation in an ecosystem functionality (Mello et al. 2011, Sunyer et al. 2013). It may also be attributed to less attention given to these groups of animals in the domain of seed dispersal since data was obtained from published studies. 4.3 FRUIT SIZE AND ASSOCIATED DISPERSERS The size of the fruit determines the animal groups adapted for its dispersal (Flörchinger et al. 2010, Burns 2013). Results obtained from this review showed that different seed categories were associated with different terrestrial vertebrate dispersers which is consistent with the results found by (Flörchinger et al. 2010). However some vertebrate groups were found in the same size classes which meant no significant difference between them. According to the results obtained from simple correspondence analysis (SCA), carnivores and primates predated fruits of 20.1-30 and 10.1-20mm (medium sized to large fruits). Considering carnivores, the findings are consistent with the study by (Takahashi et al. 2008) on the foraging behavior of the Japaneese Black Bear (Ursus thibetanus japonicus). A study conducted by (Flörchinger et al. 2010) confirmed that primates selected large fruits over the small ones that were preferred by birds, but in this review, the output from analysis was general in favor of medium sized class that dominated the large class, otherwise primates and carnivores dispersed more large seeds of 50.1-100mm than any other group. Birds and bats were associated with size class of 5-10. Most of the bird species have small gapes that limit them from swallowing large fruits (Flörchinger et al. 2010). The consumption of small fruits by birds may also be attributed to the reduction in number of large species due to different threats (Galetti and Pizo 2013). Bats were found dispersing seeds that were too large to be dispersed by some bird species (Jordaan et al. 2012) but the size of course remained small which can as well be explained by their size. Sometimes, bats and birds attack large fruits by spatting them and getting out seeds hence dispersal possibilities. Reptiles were as well associated to this medium sized fruit class because lizards and tortoises that dominate hence predating medium sized fruits (Jerozolimski 2003). Rodents were associated to the size classes of large fruits but data retrieved were not sufficient enough to be globally generalized. Fruit size was considered among the minor factors that influence the removal of fruits and their seeds in rodents (Perea et al. 2011). Ungulates were associated with the smallest fruit size class which is connected to domination of herbivores that prefer grazing on herbaceous species particularly of Poaceae family (Treydte et al. 2013) which are characterised by small fruits. Due to their large www.researchjournali.com 7 Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 surface area, some small hooked fruits can adhere to their skin and be transported to distant places. Small seeds have a likelihood also to adhere to the hooves of large ungulates (hoof epizoochory) and be transported away from parent plants (Albert et al. 2015). 4.4 SEED SIZE AND ASSOCIATED DISPERSERS Fruit size factor may be different from seed size factor. This is primarily based on the type of the fruit such as a drupe or a berry. The size of the fruit is not directly proportional to seed size hence suitability differences to different dispersal agents. Small sized seeds were dispersed by ungulates, birds and bats. As discussed in the previous part, various species of birds possess small gape that limits them to swallowing large seeds (Flörchinger et al. 2010, Gosper and Vivian-Smith 2010), the same applies to bats (Seltzer et al. 2013) while ungulates prefer small seeded species of Poaceae family (Treydte et al. 2013) and the lightness (small size) characteristic of seeds to be attached to their hooves and fur (Albert et al. 2015). Rodents, reptiles and carnivores were grouped together in the seed size classes of >30, and 10.1-20.0 mm. From figure 4, rodents dispersed large seeds though it was not reliable due to less data. Carnivores suit the category because of the large sized seeds they disperse of which some may be drupes and capsules with large seeds. In the previous section, reptiles dispersed medium sized fruits (Jerozolimski 2003), which could be characterized by medium to large seeds. Primates are known for ingesting and dispersing smaller seeds more than larger seeds (Oliveira and Ferrari 2000). The effect of seed and fruit attributes on the probability of being ingested is associated with seed shadow consequences because primate ingested seeds are usually dispersed to distant places than those dispersed by spitting (McConkey 2000). Based on findings of this study, they fell in the seed size classes of 5.1-10.0 and 20.1-30.0 that evidently showed their clear participation in dispersal of both small and large seeds. This together with herbivory maintains the demography of plant communities hence regarded as ecosystem engineers (Chapman et al. 2013). 5. CONCLUSION AND PERSPECTIVES Ecosystem architecture is specially engineered by animals particularly vertebrates that are capable of clearly exhibiting a certain level of intelligence in fruit predation and consequently displacing seeds from their parents to more favorable conditions for establishment. The difference in the diversity of terrestrial vertebrates involved in seed dispersal signifies the most indispensable animal groups, on which their extinction may lead to eminent traumatic effect on the ecosystem structure. Therefore in first place, knowing these groups such as mammals and birds and moving further to distinguish the most active sub-groups within these major groups is important to appreciate the priority status and appropriate measures for adaptive conservation. The findings of the study clearly shows that some animals are completely outweighed in as far as plant seed dispersal is concerned as exemplified by reptiles, bats and amphibians that were not reported in this study which necessitates deep www.researchjournali.com 8 Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 research in these less frequent groups to find out the truth about their role in structuring the plant communities in terrestrial ecosystems. Animal adaptation to seed dispersal is driven by different plant traits, one of which is seed and fruit size. Different terrestrial vertebrate groups can disperse different seed and fruit sizes, but still others disperse the same sized fruits and seeds despite being morphologically different. The uniqueness of some plant seed dispersal agents for example ungulates that disperse very small fruits and seeds, should be the field of great concern as loss in the diversity or even abundance may be followed by loss of the plant species that solely rely on this animal group. The findings thus, showed the expected seed dispersal agent given a seed and/or fruit size though it was not evident in some animal categories such as rodents and bats that were accompanied by less data. 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APPENDICES APPENDIX I: Data Extracted From The Published Primary Studies On The Plant Seed Dispersal By Terrestrial Vertebrates Animal species Vertebrate taxonomic group Mammal Mammal groups Primate Nasalis larvatus (proboscis monkeys) Mammal Primate Dusicyon culpaeus (Fox) Tapirus Indicus (Tapirs) Mammal Carnivore Mammal Ungulate Turdinae Catharus guttatus Turdus migratorius Mimus polyglottos Sturnus vulgaris Bombycilla cedrorum Iguana iguana (Green iguanas) Ateles spp. (spider monkeys) Plant family Plant species Moraceae Cecropiaceae Myristicaceae Moraceae Phyllanthaceae Rubiaceae Lauraceae Brosimum sp. Cecropia sp. Virola sp. Ficus sp. Antidesma thwaitesianum Nauclea subdita Cryptocarya alba Dilleniaceae Fabaceae Moraceae Dillenia indica Tamarindus indica Artocarpus integer Bird Caprifoliaceae Lonicera maackii Reptile Anacardiaceae Araliaceae Tapirira guianensis Didymopanax morototoni Smilax sp Cynoglossum officinale L Olea capensis Syzygium guineense Celtis spinosa Cordia sellowiana Eugenia pyriformis Celtis spinosa Eugenia ligustrina Jacaratia spinosa Cattle Mammal Ungulate Pan troglodytes (chimpanzees) Alouatta. guariba (brown howler monkey) Brachyteles arachnoides (muriquis) Mammal Primate Mammal Primate Mammal Primate www.researchjournali.com Smilacaceae Boraginaceae Oleaceae Myrtaceae. Cannabaceae Boraginaceae Myrtaceae Cannabaceae Myrtaceae Caricaceae Fruit fruit type/life form Fruit size (mm) Seed size (mm) Habitat type Reference Forest Campbell et al. 2005 Tropical forest Matsuda et al. 2013 Savannah Bustamante et al. 1992 Campos-Arceiz et al. 2012 Drupe/Shrub 8 5 Berry/Shrub Drupe/Tree 18 20 1.5 13 Berry/Shrub Pod/Tree 100 150 13 20 Syncarp/Tree Berry/Shrub 150 5 30 1 Shrub land Bartuszevige and Gorchov 2006 Drupe/Tree 20 10 Forest Moura et al.2014 Berry/Tree 12 4 Nut/Herb 5 2 Woodland Drupe/Shrub Drupe/Tree Drupe/Shrub Drupe/Shrub Drupe/Tree Drupe/Shrub Berry/Tree Drupe/Tree 20 30 7 15 28 7 12 13 23 3 9 13 3 3 Afromontane forest Clerck-Floate, 2007 Gross‐Camp and Kaplin 2005 Martins 2006 Forest Forest Martins 2006 Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 12 Ramphastos sulfuratus R. swainsinii Cercopithecus lhoesti, (l’Hoest’s monkeys) Bird Mammal Primate Pan troglodytes (chimpanzees) Mammal Primate Rubiaceae Rudgea sp. Flacourtiaceae Casearia nitida Capsule/Tree 10 15 6.3 6 Sapotaceae Chrysophyllum rwandense Sericanthe leonardii Syzygium guineense Ekebergia capensis D Grewia mildibraedii Myrianthus holstii D Olea capensis D Olinia rochetiana D Prunus africana D Syzygium guineense Berry/Tree 50 10 Drupe/Tree Drupe/Tree Berry/Tree Berry/Tree Nut/Shrub Drupe/Tree Berry/Shrub Berry/Tree Drupe/Tree 50 30 20 15 40 20 10 13 30 18 23 2 1.2 3 13 1.1 1.3 23 Rubiaceae Myrtaceae Meliaceae Malvaceae Urticaceae Tamias senex (Shadow Chipmunk) Nucifera Columbiana (Clark’s nutcrackers) Mammal Lagothrix cana (woolly monkeys) Bellbirds Bilvereyes. Mammal Howler monkeys Mammal Primate Callithrix jacchus (Marmosets) Pan paniscus (bonobo) Mammal Primate Mammal Primate Rodent Bird Primate Bird Oleaceae Penaeaceae Rosaceae Myrtaceae Pinaceae Cone/tree 130 19 Thick forest Fiehler, 2007 Cone/Tree 60 9 Open plantation Tomback, 1982 Sapotaceae Manilkara bidentata Berry/Tree 40 10 Thick forest Levi and Peres Loranthaceae Loranthaceae Loranthaceae Loranthaceae Loranthaceae Melastomataceae Arecaceae Myrtaceae Fabaceae Alepis flavida, Peraxilla colensoi, P. tetrapetala, Ileostylus micranthus Tupeia antarctica M. cinnamomifolia Syagrus oleraceae Myrcianthes pungens C. langsdorffii Berry/Shrub 14 1 Clear forest LADLEY and DAVE KELLY, 1996 Berry/Tree Drupe/Tree Drupe/Tree Capsule/Tree 5 40 15 14 <1 32 9 6 Semi-decidous forest FIGUEIREDO &LONGATII, 1997 Melastomataceae Moraceae Ebenaceae Meliaceae Clusiaceae Sapotaceae M. cinnamomifolia Ficus sp. Diospyros sp. Guarea aurentii Garcinia sp. Manilkara yangambiensis Urtica dioica Juncus spp. Cistus albidus L. Rhamnus lycioides L. Quercus ilex Berry/Tree Syconium/Tree 5 14 <1 1 Capsule/Tree 20 14 Semi-decidous forest Lowland tropical rain forest Berry/Tree 55 10 Achene/Herb 1.5 1 Grassland Capsules/Shrub Berry/Shrub Arcon/Tree 10 6 10 3 1 <1 Shrub land Berry/Tree 20 5 Pod/Herb 8 4 4 80 2.5 10 1 3.5 1.7 1 Goats Mammal Ungulate Apodemus sylvaticus Mammal Rodent Urticaceae Caryophyllaceae Cistaceae Rhamnaceae Fagaceae Aceros cassidis (Sulawesi red-knobbed hornbill) Sheep Bird Ungulate Myristiceae Annonaceae Myrtaceae Fabaceae Bat Apiaceae Poaceae Plantaginaceae Moraceae Bird Mammal Carnivore Mammal Ungulate Ungulate Mammal Primate Lowland tropical rain forest Shrub land Cosyns et al. 2005 Grande et al 2013 Gómez et al. 2007 Kinnaird 1998 Manzano and Malo, 2006 Ficus trigonata Moraceae Ficus continifolia Syconium//Tree 10 1 Tropical rain forest Jordano, 1983 Zygophylaceae Anacardiaceae Arecaceae Arecaceae Porlieria chilensis Schinus molle Euterpe edulis Syagrus romanzoffiana S. oleracea Copaifera langsdorffii Enterolobium contortisiliquum Inga sp. Ficus sp. Psidium guajava Mangifera indica Nut/Shrub Berry/Tree Drupe/Tree Drupe/Tree 7.8 5 13 30 2 <1 7 21 Thornscrub Silver et al. 2005 Forest Galetti et al, 2001 Drupe/Tree Capsule/Tree 50 14 32 6 Pod/Tree 35 8 Berry/Tree Drupe/Tree Berry/Shrub 40 60 10 3 26 1 Shrub land Nogales et al. 1995 Cardoso et al. 2011 Fabaceae Mammal Horsfelida brachiate Cananga odorata Syzygium sp. Trifolium angustifolium Daucus carota Hordeum murinum Plantago lagopus Beaune et al.2013 Umbel/Herb Caryopsis/Herb Capsule/Herb Syconium//Tree Arecaceae Fabaceae Oryctolagus cuniculus (Rabbit) Leontopithecus chrysomelas (goldenheaded lion tamarins) Sem-iidecidous forest Pinus albicaulis Ungulate Mammal Howe and Primack, 1975 Gross-Camp and Kaplin, 2011 Pinus ponderosa Mammal Artibeus jamaicensis (Jamaican fruit bat) Orioles, Tanagers, Trogons and Flycatchers Pseudalopex culpaeus, (Native fox) Tapirus terrestris (Lowland Tapir) Sem-iidecidous forest Pinaceae Cattle and horse Mammal Open plantation Fabaceae Moraceae Myrtaceae Anacardiaceae Rubiaceae Melastomataceae Celastraceae Plocama pendula Henriettea succosa Cheiloclinium cognatum Pourouma acutiflora Passifloraceae sp. Myrcia fallax Inga subnuda Brosimum alicastrum August, 1981 Tropical forest Berry/Shrub 40 15 Nut/Tree 15 9 Ever green rain forest Berry/Tree 35 2 Riverine forest Berry/Herb 20 1 Smi-decidous fores Forest gragment Aouatta palliate (Howling monkeys) Mammal Primate Urticaceae Passifloraceae Myrtaceae Fabaceae Moraceae Rhinoceros unicornis Mammal Ungulate Euphorbiaceae Trewia nudiflora Platyrrhinus lineatus Geoffroy Didelphis Virginiana (Opossums) Mammal Bat Moraceae Ficus sp. Mammal Ungulate Rosaceae Rubus rosifolius Paradoxurus hermaphroditus (common palm civets) Felis catus Mammal Carnivore Sapindaceae Nepheliym lappaceum Mammal Carnivore Cupressaceae Rutaceae Cone/Tree 14 5 Open forest Nogales, 1996 Eulemur fulvus rufus (Brown lemur) Alouatta spp (Howler monkeys ) Tapirus terrestris (Lowland Tapir) Anas crecca (teal/duck) Mammal Primate Solanaceae Malvaceae Juniperus phoenicea Neochamaelea pulverulenta Withania aristana Grewia grandulosa Drupe/shrub 28 19 Dry deciduous forest Mammal Primate Moraceae Ficus enormis Syconium/Tree 13 3 Mammal Ungulate Arecaceae Maximiliana maripa. Nut/Tree 60 40 Characeae Cyperaceae Chara oogonia Spehn and Ganzhorn de Figueiredo 1993 Fragoso et al. 2003 Brochet et al. 2010 www.researchjournali.com Bird Rain forest Riverine forest Estrada and Coates-Estrada 1984 Coates-Estrada and Estrada 1986 Figueiredo and Perin, 1995 Cáceres and Monteiro-Filho, 2007 Nakashima and Sukor 2010 Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 13 Ungulate Annonaceae Burseraceae Cannabaceae Fabaceae Sapindaceae Rubiaceae Urticaceae Eleocharis palustris Juncus spp. Potamogeton pusillus Isolona pleurocarpa Santiria trimera Celtis gomophylla Parkia filiciodea Deinbollia pinnata Rytigynia umbellulata Cecropia hololeuca Mammal Ungulate Urticaceae Urtica dioica Didelphis albiventris (White-eared opossum) Mammal Ungulate Cacajao melanocephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus Mammal Piperaceae Urticaceae Solanaceae Cannabaceae Urticaceae Rubiaceae Lecythidaceae Fabaceae Fabaceae Piper L. Cecropia Loefl. Solanum L., Trema Lour. Urera Gaudich Duroia velutina Eschweilera tenuifolia Inga rhynchocalyx Macrolobium acaciifolium Vulpes vulpes L (Red fox.) Mammal Carnivore Cannabaceae Celtis australis L. Berry/Tree 10 Gorilla gorilla gorilla (Low land gorilla) Mammal Primate Sapindaceae Ganophyllum giganteum Uapaca guineensis Astrocaryum aculeatissimum Securinega virosa Azadirachta indica Nauclea latifolia Protium sp Celtis pubescens Mendoncia sp. Cordia sp Vaccinium spp. Ribes spp. Oplopanax spp. Rubus spp. Streptopus spp. Sambucus spp. Myriallfhus holstii PycnanthusAngolensis Pseudospondias microcarpa Lycium intricatum Opuntia ficus-indica Rubia fruticosa Plocama pendula Juniperus sp Phoenix canariensis Asparagus pastorianus Myrica faya Drupe/Tree Euphorbiaceae Arecaceae Berrylike/Tree Drupe/Tree Juncaceae Potamogetonaceae Cercopithecus nictitans (putty-nosed monkey) Mammal Primate Didelphis aurita (the common opossum) Sheep Mammal Primate Dasyprocta ssp. (common agouti) Papio Anubis (Baboon) Mammal Rodent Mammal Primate Leontopithecus chrysopygus (black lion tamarin) Mammal Primate Ursus arctos (Brown Bears) Mammal Carnivore Pan troglodytes (chimpanzees) Mammal Primate Corvus corax Bird Domestic goats Macaca fuscata (Japanese macaques) Hemiphaga novaeseelandiae (Kereru) Trachemys scripta elegans (red-eared sliders) Macaca mulatta (rhesus macaques) Chlorocebus tantalus tantalus (tantalus monkeys) Ungulate Mammal Primate Myristicaceae Cactaceae 45 25 10 8 17 6 Berry/Shrub Berry/Shrub Achene/Tree 15 9 160 1.1 <1 3 Achene/Herb 1.5 1 Achene/Tree 150 2.3 Drupe/Tree Achene/Liana 5 3.5 3.8 3 Montane Forest Chapman et al. 2009 Tropical semideciduous forest Grassland de Viveiros and Garcia 1999 Kuiters & Huiskes, 2010 Cantor et al. 2010 Seasonal semideciduous forest. Dense forest Barnett, 2012 1 Shrub land Juan et al. 2006 20 15 Tropical forest Petre et al. 2013 25 50 7 33 Rainforest Berrylike/Shrub Drupe/Tree Drupe/Shrub 5 25 80 <1 10 30 Donatti et al. 2009 Lieberman & Swaine, 1979 Berrylike/Tree 5 <1 Drupe/Tree 35 10 Berry/Tree Berry/Shrub Tuna/Herb Berry/Shrub Berry/Shrub 25 14 50 5 5 6 1 2 <1 <1 Drupe/Tree Berry/Shrub 11 5 5 <1 Drupe/Shrub 5 <1 Cactus spp. Savannah woodland Semideciduous mesophytic forest Passos, 1997 Rainforest Willson1 and gende, 2004 Woodland Takasaki, 1983 Shrub land Nogales et al. 1999 Thornscrub Actinidiaceace Aquifoliaceae Actinidia arguta Ilex macropoda Akebia sp. Berry/Liana Berry/Tree 40 6.5 2.5 1 Coniferous fores Baraza and Valiente-Banuet, 2008 Tsuji, 2011 Bird Lauraceae Beilschmiedia tawa Berry/Tree 33 1.5 Forest Bell, 1995 Reptile Moraceae Poaceae Morus spp. Echinochloa crus-galli Rumex crispus Mammal Primate Mammal Primate Polygonaceae Moraceae Phyllanthaceae Zingiberaceae Guttiferaceae Reptile Odocoileus virginianus Zimm (white-tailed deer) Mammal Lagothrix lagothricha (Woolly Monkeys) Mammal www.researchjournali.com Anacardiaceae Solanaceae Cactaceae Rubiaceae Rubiaceae Cupressaceae Arecaceae Liliaceae Mammal Terrapene carolina bauri (Florida box turtle) Melursus ursinus (Sloth Bear) Helarctos malayanus (sun bear) Odocoileus virginianus (White-tailed deer) Caracara plancus (Crested caracaras) Macaca fuscata (Japanese macaques) Euphorbiaceae Meliaceae Rubiaceae Burseraceae Cannabaceae Acanthaceae Boraginaceae Ericaceae Grossulariaceae Araliaceae Rosaceae Liliaceae Adoxaceae Moraceae Myristicaceae Pod/Tree Drupe//Tree Drupe/Tree Apocynaceae Vitaceae Euphorbiaceae Fabaceae Arecaceae Mammal Carnivore Mammal Carnivore Mammal Ungulate Primate Ungulate Bird Mammal Primate Myrtaceae Anacardiaceae Convolvulaceae Moraceae Burseraceae Amaranthaceae Lythraceae Rosaceae Amaranthaceae Caprifoliaceae Urticaceae Moraceae Melastomataceae Urticaceae Urticaceae Fabaceae Lecythidaceae Caprifloriaceae Ficus sp. Baccaurea sp Aframomum angustifolium. Harungana madagascariensis Landolphia sp. Leea guineensis Bridelia speciosa Albizia gummifera Serenoa repens Syzigium cumini Mangiifera indica Erycibe maingayi Ficus consociata Canarium pilosum Chenopodium glaucum Lythrum salicaria Potentilla norvegica C. album Lonicera sp. Cecropia spp, Ficus spp. Henriettella spp. Coussapoa spp. Pourouma bicolor Inga bonplandiana Gustavia hexapetala Lonicera maackii Kimmons and Moll Achene 5 1 Berry/Herb 60 5 Berrylike/Shrub 4 <1 Berry/Shrub Drupe/Shrub Pod/Tree Drupe/Tree 6 5 25 20 <1 4 6 12 Berry/Tree Drupr/Tree 50 60 40 26 Syconium/Tree Drupe/Tree Achene/Herb 11 45 3 1 27 <1 Capsule/Herb Achene/Herb Achene/Herb 4 2 2 <1 <1 <1 Drupe/Tree 20 15 Berry/Tree Berry/Shrub 50 5 10 1 Arecaceae Attalea phalerata Berry/Tree 52 10 Actinidiaceace Rosaceae Actinidia arguta Rabus phoenicolasius Berry/Liana Berrylike/Shrub 40 10 2.5 1 Secondary forest Tsuji et al. 2013 Montane forest Agme et al. 2009 Pine rockland forest Liu et al. 2004 Rain forest Tobler, 2002 Ever green rain forest McCONKEY and Galetti 1999 Deciduous forest Myers et al. 2004 Tropical rain forest Stevenson, 2000 Agriculturalforest matrix Guiden et al 2015 Galetti and Guimarães, 2004 Otani, 2003 Warm temperate forest Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 14 O’Connor* and Dave Kelly, 2012 Haugaasen et al. 2010 Buen and Ornelas 2001 Sus scrofa (feral pigs) Mammal Ungulate Prumnopityaceae Prumnopitys taxifolia Berrylike/Tree 13 1 Scatter-hoarding rodents Ptilogonys cinereus (Gray Silkyflycatchers) Myiozetetes similis (Social Flycatchers); Civets (Viverridae) Mammal Rodent Lecythidaceae Bertholletia excelsa Capsule/Tree 150 50 Flooded forest Loranthaceae Psittacanthus schiedeanus Berry/Shrub 20 1.3 Cloud forest remnant Lamiaceae Rosaceae Vitex glabrata Prunus ceylanica Berry/Tree Drupe/Tree 15 30 1 10 Tropical forest Geochelone denticulata (Amazonian tortoise) Reptile Apocynaceae, Fabaceae Annonaceae Moraceae Rauvolfia micrantha Lecointea amazonica Rollinia sp. Helicostylis tomentosa, Ficus spp. Brosimum lactescens Capsule/Shrub Capsule/Tree 7 50 3 35 Rainforest Drupe/Tree 30 24 Drupe/Tree 20 15 Berry/Tree 60 10 Montane rain forest Overdorff and Strait 1998 Pod/Tree 150 20 Gallery forests Mertl-Millhollen et al. 2011 Bird Mammal Carnivore Propithecus diaderna edwardsi, Eulemur fuluus rufus, Eulemur rubriventer) Lemur catta (Ringtailed Lemurs) Nucifera Columbiana (Clark’s nutcrackers) Cerdocyon thous (Crab-eating Fox) Saguinus mystax Saguinus fuscicollis Papio cynocephalus Cercopithecus albogularis Heliosciurus rufobrachium Paraxerus palliatus Alouatta caraya (black and gold howlers) Mammal Podarcis lilfordi (lizard) Cerradomys subflavus Reptile Mammal Rodent Pan paniscus (bonobo) Mammal Macaca fuscata (Japanese macaques) Sus scrofa (Wild boar) Mammal Primate Primate Moraceae Moraceae Anacardiaceae Sapotaceae Myrtaceae Fabaceae Protorhrrs sp. Chrysophyllum madagascariensis Eugenia sp. Tamarindus indica Chakravarthy and Ratnam 2015 Guzmán and Stevenson Pinaceae Pinus albicaulis Cone/Tree 60 9 Open plantation Mammal Carnivore Myrtaceae Eugenia umbelliflora Berry/Tree 13 2 Rainforest Mammal Primate Vitaceae Dupe/Tree 30 23 Rainforest Mammal Primate Fabaceae Leonia glycycarpa Pourouma sp., Afzelia quanzensis Hutchins and Lanner 1982 Cazetta and Galetti 2009 Garber 1986 Pod/Tree 100 10 Rainforest Gathua, 2000 Mammal Rodent Mammal Primate Drupe/Shrub Drupe/Tree Drupe/Tree 26 15 6 14 8 4 Flooded forest Bravo 2011 Berry/Liana 60 1.2 Arecaceae Eugenia punicifolia Ocotea diospyrifolia Nectandra megapotamica Lycopersicon esculentum Allagoptera arenaria Drupe/Tree 25 18 Primate Fabaceae Dialium spp. Semi deciduous forest Rain forest Mammal Primate 20 22 25 25 4 18 18 18 Rain forest Ungulate Myrica rubra Persea thunbergii Neolitsea sericea Litsea acuminata Morus sp. Amaranthus blitum Ficus religiosa Rubus ulmifolius Berry/Tree Drupe/Tree Drupe/Tree Drupe/Tree Mammal Myricaceae Lauraceae Lauraceae Lauraceae Moraceae Amaranthaceae Moraceae Rosaceae Achene/Herb Syconium/Tree Berry/Herb 2 15 19 <1 1 1 Bird Sylivia atricapilla Erithacus rebecula S. borin S. melanocephala Turdus merula Chiroderma doriae C. villosum Lepus Capensis L (Hares) Bird Myrtaceae Lauraceae Lauraceae Solanaceae Castilla, 2009 Shrub land Grenha et al. 2010 Beaune et al. 2013 Tsujino and Yumoto, 2009 Dovrat et al. 2012 Jordano 1982 Mammal Bat Moraceae Ficus sp. Mammal Ungulate Mammal Ungulate Tragus berteronianus Achyranthes aspera Pupalia lappacea Boerhavia repense Harpachne schimperi Themeda triandra Sagina apetala Senecio jacobaea Urtica dioica Veronica arvensis Caryopsis/Herb Achene/Herb Achene/Herb Berrylike/Shrub Caryopsis/Herb Caryopsis/Herb Capsule/Herb Achene/Herb Achene/Herb Capsule/Herb 2 3 3 4 1.3 2 5 4 1.5 5 <1 <1 <1 <1 <1 <1 <1 <1 1 <1 Grassland Rabbit Poaceae Amaranthaceae Amaranthaceae Nyctaginaceae Poaceae Poaceae Caryophyllaceae Asteraceae Urticaceae Plantaginaceae Grassland Pakeman et al. 1999 Sheep Mammal Ungulate Trifolium stellatum L. T. tomentosum L. T. campestre Schreb Viscum album Pod/Herb Pod/Herb Pod/Herb Berry/Tree 5 5 5 25 1 1 1 10 Grassland Russi et al. 1992 Temperate forest Amico and Aizen 2000 Aronne and Russo 1997 Auger et al. 2002 Humid forest Nogueira and Peracchi Agnew and Flux 1970 Dromiciops australis Mammal Marsupial Fabaceae Fabaceae Fabaceae Santalaceae Vulpes vulpes L. (red fox) Ursus americanus (black bears) Mammal Carnivore Myrtaceae Myrtus communi Berry/Shrub 8 1 Mammal Carnivore Rosaceae Rosaceae Berberidaceae Anacardiaceae Caprifoliaceae Berry/Shrub Drupe/Shrub Berry/Shrub Berry/Shrub Drupe/Shrub 13 10 12 7 25 1 7 1 1 16 Loxodonta africana africana Tapirus indicus (Tapirs) Cyanocitta cristata (blue jays) Nucifera Columbiana (Clark’s nutcrackers) Mammal Ungulate Fabaceae Amelanchier alnifolia Prunus virginiana Mahonia repens Rhus trilobata Symphoricarpos oreophilus Acacia erioloba Pod/Tree 28 5 Forest Dudley 1999 Mammal Ungulate Arecaceae Drupe/Tree 30 21 Atlantic forest Nut/Tree 15 4 Woodlot Open plantation Cattle Mammal Cervus elaphus (Red deer) Pteropus dasymallus (Orii’s flying fox) Macaca fuscata yakui (Yakushima macaque) Mammal Mammal Primate Warm temperate forest Giombini et al. 2009 Johnson and Adkisson 1985 Lanner and Vander Wall 1980 Malo and Suarez 1995 Malo and Suárez 1998 Nakamoto et al. 2009 Otani and Shibata 2000 Civettictis civetta (African civet) Mammal Carnivore Rain forest Pendje 1994 Bird Fagaceae Syagrus romanzoffiana Fagus grandifolia Bird Pinaceae Pinus flexilis Cone/Tree 40 10 Ungulate Fabaceae Biserrula pelecinus Pod/Shrub 20 2 Ungulate Cistaceae Cistus ladanifer Capsules/Shrub 10 <1 Combretaceae Moraceae Moraceae Pentaphylacaceae Ericaceae Burseraceae Myristicaceae Terminaria catapa Ficus sp. Ficus thunbergii Eurya japonica Euphorbiaceae Dacryodes edulis Pycnanthus angolensis Elaeis guineensis Staudtia stipitata Trilepisium sp. Drupe/Tree 60 30 Syconium/Tree Berrylike/Shrub Berry/Shrub Drupe/Tree Drupe/Tree 20 5 6 90 30 1 <1 <1 70 20 Drupe/Tree Drupe/Tree 70 60 32 40 Bat Arecaceae Myristicaceae www.researchjournali.com Mediteranean ecosystem Researchjournali’s Journal of Ecology Vol. 4 | No. 1 February | 2017 15 Canis latrans (Coyote) Mammal Carnivore Moraceae Ebenaceae Diospyros virginiana Alouatta palliata mexicana (Mexican howler monkeys) Eulemur fulvus fulvus (common brown lemur) Martes foina (Pine martens) Cebus apella Ateles aniscus Macaca fuscata yakui (Japanese monkeys) Mitu salvini (Salvin’s curassows) Dicaeurn hirundinaceurn Acanthagenys rufogularis Mammal Primate Moraceae Ficus spp Mammal Primate Lamiaceae Malvaceae Vitex sp. Grewia triflora Berry/Tree 60 10 Tropical rain forest 10 7 Tropical dry forest Sato 2012 Drupe/Shrub Schaumann and Heinken 2002 Zhang and Wang 1995 Yumoto et al. 1998 Yumoto 1999 Mammal Carnivore Vaccinium myrtillus Rubus idaeus Ziziphus sp. 7 15 1 1 Temperate woodland Primate Ericaceae Rosaceae Rhamnaceae Berry/Shrub Berry/Herb Mammal Mammal Primate Lauraceae Persea thunbergii Drupe/Tree 22 18 Rubiaceae Moraceae Loranthaceae Geophila repens Ficus sphenophylla Lysiana exocarpi Drupe/Herb Syconium/Tree Berry/Shrub 5 10 10 3 1 1 warm temperate evergreen forest Lowland tropical forest Bird Bird Yan 1993 APPENDIX II: The Frequency Of Different Vertebrate Groups Per Fruit Size Range Fruit size (mm) <5 5.0-10 10.1-20.0 20.1-30.0 30.1-40 40.1-50 50.1-100 >100 Animal group Birds Primates 0 1 9 19 7 21 0 16 2 7 0 4 4 6 0 1 Ungulates 18 13 6 3 2 2 3 4 Carnivores 0 7 8 3 0 2 5 0 Reptiles 0 2 4 1 0 1 1 0 Bats 0 1 0 0 1 0 0 0 Rodents 0 1 0 1 0 1 1 2 APPENDIX III: The frequency of different vertebrate groups per seed size range www.researchjournali.com Roehm and Moran 2013 Serio-Silva and Rico-Gray 2003 Seed size (mm) <1 Animal group Birds Primates 4 9 Ungulates 15 Carnivores 1 Reptiles 0 Bats 0 Rodents 1 1.0-5.0 5.1-10.0 13 4 23 15 26 3 12 3 4 1 1 0 0 1 10.1-20.0 20.1-30.0 >30 0 0 0 13 6 2 2 4 1 3 2 4 2 1 1 0 1 0 2 0 2