Seed predation and dispersal of Ardisia solanacea in habitats with different degree of disturbance

doi:10.3724/SP.J.1003.2008.07231

Abstract

Abstract:

Effective dispersal is one essential course for invasive species on their process of invasion, while study on the effectiveness of seed dispersal was often neglected when predicting species’ invasion. Native to Tropical Asia,Ardisia elliptica is an invasive species in North America. A. solanacea is a tree naturally distributed in southern Yunnan with biological characteristics similar to A. elliptica. In this study, we conducted observation on seed dispersal and seed predation of A. solanacea in two habitats with different degree of disturbance: the Wild Elephant Valley (WEV) with few disturbances and the Xishuangbanna Tropical Botanical Garden (XTBG) with high disturbances. The aim of the study was to understand how disturbances affect seed dispersal and seed predation of A. solanacea.In both habitats, three frugivorous birds were the main seed dispersers, i.e., Alophoixus pallidus, Pycnonotus melanicterus and Iole propinqua. However, the visiting frequency and feeding behaviour differed in the two habitats. In WEV, the visiting frequency of the three birds was 25%, 32% and 26%, respectively; while in XTBG, it was 67%, 8% and 5%, respectively. Only 4% of the birds got first stop far than 10 m away from the fruiting tree after feeding in WEV, but 26% in XTBG. Seed placement experiment indicated that rodents were the major predators to the seeds on ground. The predation rate in both habitats were rather low (2-6%) while seed predation rate in WEV was significantly higher than that in XTBG. In WEV, larvae of Curculionidae were another seed predator, which caused 17.9±3.5% (n = 512) of seeds parasitized. In contrast, no seeds was found to be parasitized by the larvae (n = 489) in XTBG. Disturbance significantly affect the composition and behaviour of animals inhabited. Consequently, those changes may influence seed dispersal and seed predation of related plants, and indirectly, affect the population recruitment of plants.

Key words: Ardisia solanacea, different disturbed habitats, frugivorous birds, seed dispersal, seed predation

Jin Zhao, Jin Chen, Shaobin Ma. Seed predation and dispersal of Ardisia solanacea in habitats with different degree of disturbance[J]. Biodiv Sci, 2008, 16(1): 34-43.

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URL: https://www.biodiversity-science.net/EN/10.3724/SP.J.1003.2008.07231

https://www.biodiversity-science.net/EN/Y2008/V16/I1/34

Figures/Tables 5

Fig. 1 Comparison of visiting frequency of three frugivorous birds to the fruiting trees of Ardisia solanacea in Xishuangbanna Tropical Botanical Garden (XTBG) and Wild Elephant Valley (WEV). Data is an accumulation of 15-day observation. The time for continuous five minutes was recorded as one visit.

Table 1 Visiting frequency (%) of the three major seed dispersers of Ardisia solanacea in two different habitats

种名 Species	生境 Habitats
种名 Species	植物园 XTBG	野象谷 WEV
白喉冠鹎 Alophoixus pallidus	67	25
黑冠黄鹎 Pycnonotus melanicterus	8	32
灰眼短脚鹎 Iole propinqua	5	26
其他 Others	20	17

Table 2 Distance between the fruiting tree and the first stop of visitors (indicated by times and percentage)

种名 Species	植物园 XTBG				野象谷 WEV
种名 Species	<5 m	5-10 m	>10 m	合计 Total	<5 m	5-10 m	>10 m	合计 Total
白喉冠鹎 Alophoixus pallidus	7 (11)	35 (58)	19 (31)	61	2 (6)	30 (91)	1 (3)	33
黑冠黄鹎 Pycnonotus melanicterus	0 (0)	8 (100)	0 (0)	8	10 (24)	31 (73)	1 (3)	42
灰眼短脚鹎 Iole propinqua	0 (0)	3 (100)	0 (0)	3	8 (24)	24 (70)	2 (6)	34
合计 Total	7 (10)	46 (64)	19 (26)	72	20 (18)	85 (78)	4 (4)	109

Table 3 Retention time of Ardisia solanacea seeds in the digestive systems of the three frugivorous birds

种名 Species	滞留时间 Retention time
种名 Species	均值 ± 1标准误 Mean± 1SE	样本数 n	变幅 Range
白喉冠鹎 Alophoixus pallidus	23.6 ± 0.51	5	22.9-23.9
黑冠黄鹎 Pycnonotus melanicterus	22.7 ± 0.53	5	21.7-23.6
灰眼短脚鹎 Iole propinqua	22.4 ± 0.37	5	21.7-23.0

Fig. 2 Degree of seed predation influenced by different treatments, habitats and seed density (Seed predation is indicated by percentage of seed removed. Data are means±1SE. A, Treatments (N = 360): OP, seeds were directly placed on the ground; BE, birds’ visit was excluded, AE, ants’ visit was excluded; BR, both birds and rodents were excluded. B, Different habitats. C, Different seed density: LD, 2 seeds; HD, 10 seeds. Different letters indicate that the mean values are significantly different (P<0.05).

References 86

[1]	Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecology Letters, 6,712-715.
[2]	Beattie AJ, Hughes L (2002) Ant-plant interactions. In:Plant-Animal Interactions: An Evolutionary Approach (eds Herrera CM, Pellmyr O), pp.211-235. Blackwell Science, Oxford.
[3]	Bleher B, Böhning-Gaese K (2001) Consequences of frugivore diversity for seed dispersal, seedling establishment and the spatial pattern of seedlings and trees. Oecologia, 129,385-394.
[4]	Buckley YM, Anderson S, Catterall CP, Corlett RT, Engel T, Gosper CR, Nathan R, Richardson DM, Setter M, Spiegel O, Smith GV, Voigt FA, Weir JES, Westcott DA (2006) Management of plant invasions mediated by frugivore interactions. Journal of Applied Ecology, 43,848-857.
[5]	Cain ML, Milligan BG, Strand AE (2000) Long-distance seed dispersal in plant populations. American Journal of Botany, 87,1217-1227.
[6]	Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science, 290,521-523. URL PMID
[7]	Chapman CS (1989) Primate seed dispersal: the fate of dispersed seeds. Biotropica, 21,148-154.
[8]	Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecology Letters, 7,721-733.
[9]	Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In:Dynamics of Populations: Proceedings of the Advanced Study Institute on Dynamics of Numbers of Populations (eds Den Boer PJ, Gradwell GR),pp.298-310. Center for Agricultural Publishing and Documentation, Wageningen.
[10]	Corlett RT (1998) Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) region. Biology Review, 73,413-448.
[11]	Crawley MJ (1997) Plant-herbivore dynamics. In:Plant Eco- logy (ed. Crawley MJ), pp.401-474. Blackwell Science, Oxford.
[12]	Crawley MJ (2000) Seed predators and plant population dynamics. In:Seeds: The Ecology of Regeneration in Plant Communities (ed. Fenner M), pp.167-182. CAB International, Wallingford.
[13]	Cummings CL, Alexander HM (2002) Population ecology of wild sunflowers: effects of seed density and post-dispersal vertebrate seed predators. Oecologia, 130,274-280.
[14]	Curran LM, Leighton M (2000) Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecological Monographs, 70,101-128.
[15]	De Walt SJ, Denslow JS, Ickes K (2004) Natural enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology, 85,471-483.
[16]	Elton CS (1958) The Ecology of Invasion by Animals and Plants. Methuen, London.
[17]	Fleming TH (1981) Fecundity, fruiting pattern, and seed dispersal in Piper amalgo (Piperaceae), a bat-dispersed tropical shrub . Oecologia, 51,42-46.
[18]	Forget PM, Milleron (1991) Evidence for secondary seed dispersal by rodents in Panama. Oecologia, 87,596-599. URL PMID
[19]	Forget PM, Cuijpers L (2007) Survival and scatterhoarding of frugivores-dispersed seeds as a function of forest disturbance. Biotropica, doi: 10.1111/j.1744-7429.2007.00358.x (OnlineEarly Article)
[20]	Foster BL, Tilman D (2003) Seed limitation and the regulation of community structure in oak savanna grassland. Journal of Ecology, 91,999-1007.
[21]	Galetti M, Alves-Costa CP, Cazetta E (2003) Effects of forest fragmentation, anthropogenic edges and fruit colour on the consumption of ornithocoric fruits. Biological Conservation, 111,269-273.
[22]	Gordon DR, Thomas KP (1997) Florida’s invasion by nonindigenous plants: history,screening, and regulation. In:Strangers in Paradise (eds Simberloff D, Schmitz DC, Brown TC), pp.21-37. Island Press, Washington, DC.
[23]	Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal of fleshy-fruited invasive plants by birds: contri- buting factors and management options. Diversity and Distribution, 11,549-558.
[24]	Gosper CR, Smith GV (2006) Selecting replacements for invasive plants to support frugivores in highly modified sites: a case study focusing on Lantana camara. Ecological Management and Restoration, 7,197-203.
[25]	Herrera CM (2002) Seed dispersal by vertebrates. Plant- Animal Interactions: An Evolutionary Approach (eds Herrera CM, Pellmyr O), pp.185-208. Blackwell Science, Oxford.
[26]	Herrera CM, Jordano P, Lopez-Soria L, Amat JA (1994) Recruitment of a mast-fruiting, bird-dispersed tree: bridging frugivore activity and seedling establishment. Ecological Monographs, 64,315-344.
[27]	Herron PM, Martine CT, Latimer AM, Leicht-Young SA (2007) Invasive plants and their ecological strategies: prediction and explanation of woody plant invasion in New England. Diversity and Distributions, 13,633-644.
[28]	Hinz HL, Schwarzlaender M (2004) Comparing invasive plants from their native and exotic range: What can we learn for biological control? Weed Technology, 18,1533-1541.
[29]	Hobson KA (2005) Using stable isotopes to trace long-distance dispersal in birds and other taxa. Diversity and Distributions, 11,157-164.
[30]	Holmes RJ, Froud-Williams RJ (2005) Post-dispersal weed seed predation by avian and non-avian predators. Agriculture, Ecosystems and Environment, 105,23-27.
[31]	Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13,201-228.
[32]	Howe HF, Schupp EW, Westley LC (1985) Early consequences of seed dispersal for a neotropical tree (Virola surinamensis). Ecology, 66,781-791.
[33]	Hulme PE (1993) Post-dispersal seed predation by small mammals. Symposia of the Zoological Society of London, 65,269-287.
[34]	Janzen DH (1969) Seed eaters versus seed size, number, toxicity and dispersal. Evolution, 23,1-27.
[35]	Janzen DH (1970) Herbivores and the number of tree species in tropical forests. The American Naturalist, 104,501-528.
[36]	Janzen DH (1971) Seed predation by animals. Annual Review of Ecology and Systematics, 2,465-492.
[37]	Julien MH, Griffiths MW (1998) Biological Control of Weeds: A World Catalogue Agents and Their Target Weeds, 4^th edn. CABI Publishing, Wallingford, UK.
[38]	Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution, 17,164-170.
[39]	Knevel IC, Lans T, Menting FBJ, Hertling UM, van der Putten W (2004) Release from native root herbivores and biotic resistance by soil pathogens in a new habitat both affect the alien Ammophila arenaria in South Africa . Oecologia, 141,502-510. DOI URL PMID
[40]	Koop AL (2003) Population dynamics and invasion rate of an invasive, tropical understory shrub,Ardisia elliptica. PhD dissertation, University of Miami, Florida.
[41]	Koop AL (2004) Differential seed mortality among habitats limits the distribution of the invasive non-native shrub Ardisia elliptica. Plant Ecology, 172,237-249.
[42]	Křivánek M, Pyšek P (2006) Predicting invasion by woody species in a temperate zone: a test of three risk assessment schemes in the Czech Republic (Central Europe). Diversity and Distributions, 12,319-327.
[43]	Lambrinos JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology, 85,2061-2070.
[44]	Levin SA, Muller-Landau HC, Nathan R, Chave J (2003) The ecology and evolution of seed dispersal: a theoretical perspective. Annual Review of Ecology, Evolution and Systematics, 34,575-604.
[45]	Lu CH (鲁长虎) (2003) Biology of mistletoe ( Viscum coloratum) and its seed dispersal by frugivorous birds . Acta Ecologica Sinica (生态学报), 23,834-839. (in Chinese with English abstract)
[46]	Lyal CHC, Curran LM (2000) Seed-feeding beetles of the weevil tribe Mecysolobini (Insecta: Coleoptera: Curculionidae) developing in seeds of trees in the Dipterocarpaceae. Journal of Natural History, 34,1743-1847.
[47]	Mack RN (1996) Predicting the identity and fate of plant invaders: emergent and emerging approaches. Biological Conservation, 78,107-121.
[48]	Manson RH, Ostfeld RS, Canham CD (1998) The effects of tree seed and seedling density on predation rates by rodents in old fields. Ecoscience, 5,183-190.
[49]	Manson RH, Stiles EW (1998) Links between microhabitat preferences and seed predation by small mammals in old fields. Oikos, 82,37-50.
[50]	Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature, 421,625-627. DOI URL PMID
[51]	Moran C, Catterall CP, Green RJ, Olsen MF (2004) Fate of feathered fruit-eaters in fragmented forests. In:Conservation of Australia’s Forest Fauna, 2nd edn (ed. Lunney D),pp.699-712. Royal Zoological Society of New South Wales, Sydney.
[52]	Murray KG (1988) Avian seed dispersal of three neotropical gap-dependent plants. Eco1ogical Monographs, 58,271-298.
[53]	Nakagawa M, Takeuchi Y, Kenta T, Nakashizuka T (2005) Predispersal seed predation by insect vs. vertebrate in six dipterocarp species in Sarawak, Malaysia. Biotropica, 37,389-396.
[54]	Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution, 15,278-285. DOI URL PMID
[55]	Neubert MG, Caswell H (2000) Demography and dispersal: calculation and sensitivity analysis of invasion speed for structured populations. Ecology, 81,1613-1628.
[56]	Newingham BA, Callaway RM (2006) Shoot herbivory on the invasive plant,Centaurea maculosa, does not reduce its competitive effects on conspecifics and natives. Oikos, 114,397-406.
[57]	Newmark WD (2006) A 16-year study of forest disturbance and understory bird community structure and composition in Tanzania. Conservation Biology, 20,122-134.
[58]	Ostfeld RS, Manson RH, Canham CD (1997) Effects of rodents on tree invasion of old fields. Ecology, 78,1531-1542.
[59]	Packer A, Clay K (2000) Soil pathogens and spatial pattern of seedling mortality in a temperate tree. Nature, 404,278-281.
[60]	Pratt PD, Rayamajhi MB, Van TK, Center TD, Tipping PW (2005) Herbivory alters resource allocation and compensation in the invasive tree Melaleuca quinquenervia. Ecological Entomology, 30,316-326.
[61]	Primack RG, Miao SL (1992) Dispersal can limit local plant distribution. Conservation Biology, 6,513-519.
[62]	Rejmánek M (1996) A theory of seed plant invasiveness: the first sketch. Biological Conservation, 78,171-181.
[63]	Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology, 77,1655-1661.
[64]	Renne IJ, Barrow WC, Randall LAJ, Bridges WC (2002) Ge- neralized avian dispersal syndrome contributes to Chinese tallow tree ( Sapium sebiferum, Euphorbiaceae) invasiveness . Diversity and Distributions, 8,285-295.
[65]	Restrepo C, Gomez N, Heredia S (1999) Anthropogenic edges, tree fall gaps, and fruit-frugivore interactions in a neotropical montane forest. Ecology, 80,668-685.
[66]	Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions—the role of mutualisms. Biological Review, 75,65-93.
[67]	Santos T, Tellería JL (1994) Influence of forest fragmentation on seed consumption and dispersal of Spanish juniper Juniperus thurifera. Biological Conservation, 70,129-134.
[68]	Schnurr JL, Canham CD, Ostfeld RS, Inouye RS (2004) Neighborhood analyses of small-mammal dynamics: impacts on seed predation and seedling establishment. Ecology, 85,741-755.
[69]	Schupp EW (1990) Annual variation in seedfall, post-dispersal predation, and recruitment of a neotropical tree. Ecology, 71,504-515.
[70]	Seabloom EW, Harpole WS, Reichman OJ, Tilman D (2003) Invasion, competitive dominance, and resource use by exotic and native California grassland species. Proceedings of the National Academy of Sciences, USA, 100,13384-13389.
[71]	Siemann E, Rogers WE (2003) Herbivory, disease, recruitment limitation and success of alien and native tree species. Ecology, 84, 1489-1505.
[72]	Smith AJ (1975) Invasion and ecesis of bird-disseminated woody plants in a temperate forest sere. Ecology, 56,19-34.
[73]	Stohlgren TJ, Schnase JL (2006) Risk analysis for biological hazards: what we need to know about invasive species. Risk Analysis, 26,163-173.
[74]	Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology, 124,S137-S151.
[75]	Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature, 421,628-630. DOI URL PMID
[76]	Torchin ME, Mitchell CE (2004) Parasites, pathogens and invasions by plants and animals. Frontiers in Ecology and the Environment, 2,183-190.
[77]	Toy RJ, Toy SJ (1992) Oviposition preferences and egg survival in Nanophyes shoreae (Coleoptera, Apionidae), a weevil fruit-predator in South-east Asian rain forest . Journal of Tropical Ecology, 8,195-203.
[78]	Van der Wall SB (1997) Dispersal of singleleaf pion pine ( Pinus monophylla) by seed-caching rodents . Journal of Mammalogy, 78,181-191.
[79]	Van der Wall SB, Kuhn KM, Beck MJ (2005) Seed removal, seed predation, and secondary dispersal. Ecology, 86,801-806.
[80]	Westcott DA, Graham DL (2000) Patterns of movement and seed dispersal of tropical frugivore. Oecologia, 122,249-257. DOI URL PMID
[81]	Westerman PR, Hofman A, Vet LEM, van der Werf W (2003) Relative importance of vertebrates and invertebrates in epigaeic weed seed predation in organic cereal fields. Agriculture, Ecosystems and Environment, 95,417-425.
[82]	Wilson DJ, Wright EF, Canham CD, Ruscoe WA (2007) Neighbourhood analyses of tree seed predation by introduced rodents in a New Zealand temperate rainforest. Ecography, 30,105-119.
[83]	Willson MF, Whelan CJ (1990) Variation in postdispersal survival of vertebrate-dispersed seeds: effects of density, habitat, location, season and species. Oikos, 57,191-198.
[84]	Willson MF (1993) Dispersal mode, seed shadows, and colonization patterns. Vegetatio, 108,261-280.
[85]	Wunderle JM (1997) The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. Forest Ecology and Management, 99,223-235.
[86]	Yagihashi T, Hayashida M, Miyamoto T (1999) Effects of bird ingestion on seed germination of two Prunus species with different fruit-ripening seasons . Ecological Research, 14,71-76.