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Seed nutrient content rather than size influences seed dispersal by scatterhoarding rodents in a West African montane forest

Published online by Cambridge University Press:  14 August 2020

Biplang G. Yadok ,
Pierre-Michel Forget ,
Daniel Gerhard ,
Babale Aliyu  and
Hazel Chapman
Biplang G. Yadok*
Affiliation:
School of Biological Sciences, University of Canterbury, PB 4800, Christchurch, New Zealand Nigerian Montane Forest Project, Yelwa village, Taraba State, Nigeria
Pierre-Michel Forget
Affiliation:
Muséum National d’Histoire Naturelle, UMR 7179 MECADEV CNRS-MNHN, 1 avenue du Petit Château, 91800Brunoy, France
Daniel Gerhard
Affiliation:
Department of Mathematics and Statistics, University of Canterbury, PB 4800, Christchurch, New Zealand
Babale Aliyu
Affiliation:
Nigerian Montane Forest Project, Yelwa village, Taraba State, Nigeria Department of Biological Sciences, Gombe State University, Tudun Wada Street, Gombe, Gombe State, Nigeria
Hazel Chapman
Affiliation:
School of Biological Sciences, University of Canterbury, PB 4800, Christchurch, New Zealand Nigerian Montane Forest Project, Yelwa village, Taraba State, Nigeria
*
Author for correspondence: *Biplang G. Yadok, Email: bya20@uclive.ac.nz
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Abstract

Rodents can be important in seed dispersal through their scatterhoarding behaviour, yet, the seed traits that are most influential in seed removal by Afrotropical scatterhoarding rodents remains unclear. Here, we investigated the effect of seed size and nutrient content of four seed species on the scatterhoarding behaviour of rodents in an Afromontane forest, Ngel Nyaki forest, Nigeria. To do this we marked with thread-tags the seeds of Santiria trimera, Beilschmedia mannii, Carapa oreophila and Anthonotha noldeae and observed their fate. We predicted that (1) caching frequency would be higher for larger than smaller seed species; (2) caching frequency would be higher for nutrient-rich than nutrient-poor seeds; (3) larger seeds would be taken across farther distances; and (4) survival of cached seeds would be higher for nutrient-rich seeds. In contrast to studies elsewhere we found no difference in caching probabilities based on seed size, although nutrient-rich (high fat content) seeds had a higher probability of being predated than seeds with lower fat content. Larger and smaller seeds were dispersed over the same distances and nutrient-poor (high fibre content) seeds survived longer in seed caches. Overall, our findings suggest that large, nutrient-rich seed species are less likely to be dispersed by rodents.

Keywords

AfrotropicsAtherurus africanusCricetomys sp. nov.nutrient contentscatterhoarding rodentsseed size
Type
Research Article
Information
Journal of Tropical Ecology , Volume 36 , Issue 4 , July 2020 , pp. 174 - 181
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Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Literature cited

Abiem, I, Arellano, G, Kenfack, D and Chapman, H (2020) Afromontane forest diversity and the role of grassland-forest transition in treee species distribution. Diversity 12, 30. doi: 10.3390/d12010030.CrossRefGoogle Scholar
Aliyu, B, Adamu, H, Moltchanova, E, Forget, P-M and Chapman, H (2014) The interplay of habitat and seed type on scatterhoarding behaviour in a fragmented afromontane forest landscape. Biotropica 46, 264–267.CrossRefGoogle Scholar
Aliyu, B, Thia, JA, Moltchanova, E, Forget, P-M and Chapman, HM (2018) Forest disturbance and seasonal food availability influence a conditional seed dispersal mutualism. Biotropica 50, 750–757.CrossRefGoogle Scholar
AOAC (1990) Official Methods of Analysis. Arlington, VA: Association of Analytical Chemists.Google Scholar
Bogdziewicz, M, Crone, EE and Zwolak, R (2019) Do benefits of seed dispersal and caching by scatterhoarders outweigh the costs of predation? An example with oaks and yellow-necked mice. Journal of Ecology. doi: 10.1111/1365–2745.13307.Google Scholar
Bradbeer, JW (1988) Seed Dormancy and Germination. New York, NY: Chapman and Hall.Google Scholar
Cao, L, Wang, Z, Yan, C, Chen, J, Guo, C and Zhang, Z (2016) Differential foraging preferences on seed size by rodents result in higher dispersal success of medium-sized seeds. Ecology 97, 3070–3078.CrossRefGoogle ScholarPubMed
Chapman, HM, Cordeiro, NJ, Dutton, P, Wenny, D, Kitamura, S, Kaplin, B, Melo, FPL and Lawes, MJ (2016) Seed-dispersal ecology of tropical montane forests. Journal of Tropical Ecology 32, 437–454.CrossRefGoogle Scholar
Chung-MacCoubrey, AL, Hagerman, AE and Kirkpatrick, RL (1997) Effects of tannins on digestion and detoxification activity in gray squirrels (Sciurus carolinensis). Physiological Zoology 70, 270–277.CrossRefGoogle Scholar
Ezeagu, IE (2009) Nutritional value of tropical plant seeds. Agronomy Monographs 51, 39–53.Google Scholar
Forget, P-M (1990) Seed dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana. Journal of Tropical Ecology 6, 459–468.CrossRefGoogle Scholar
Forget, P-M (1992) Seed removal and seed fate in Gustavia superba (Lecythidaceae). Biotropica 24, 408–414.CrossRefGoogle Scholar
Forget, P-M (1994) Recruitment pattern of Vouacapoua americana (Caesalpiniaceae), a rodent-dispersed tree species in French Guiana. Biotropica 6, 408–419.CrossRefGoogle Scholar
Forget, P-M (1996) Removal of seeds of Carapa procera (Meliaceae) by rodents and their fate in rainforest in French Guiana. Journal of Tropical Ecology 12, 751–761.CrossRefGoogle Scholar
Forget, P-M and Vander Wall, SB (2001) Scatter-hoarding rodents and marsupials: convergent evolution on diverging continents. Trends Ecology and Evolution 16, 65–67.CrossRefGoogle ScholarPubMed
Forget, P-M, Milleron, T and Feer, F (1998) Patterns in post-dispersal seed removal by neotropical rodents and seed fate in relation to seed size. In Newbery, DM, Brown, N and Prins, HHT (eds), Dynamics of Tropical Communities. Oxford: Blackwell Science, pp. 25–49.Google Scholar
Forget, P-M, Hammond, DS, Milleron, T and Thomas, R (2002) Seasonality of fruiting and food hoarding by rodents in neotropical forests: consequences for seed dispersal and seedling recruitment. In Levey, DJ, Silva, WR and Galletti, M (eds), Seed Dispersal and Frugivory: Ecology, Evolution, and Conservation. Wallingford: CABI, pp. 241–256.Google Scholar
Forget, P-M, Wenny, D, Lambert, J, Hulme, P and Vander Wall, S (2005) How to elucidate seed fate? A review of methods used to study seed removal and secondary seed dispersal. In Forget, P-M, Lambert, JE, Hulme, P and Vander Wall, SB (eds), Seed Fate: Predation, Dispersal and Seedling Establishment. Wallingford: CABI, pp. 379–394.CrossRefGoogle Scholar
Galetti, M, Donatti, CI, Steffler, C, Genini, J, Bovendorp, RS and Fleury, M (2010) The role of seed mass on the caching decision by agoutis, Dasyprocta leporina (Rodentia: Agoutidae). Zoologia (Curitiba) 27, 472–476.CrossRefGoogle Scholar
Gelman, A, Lee, D and Guo, J (2015) Stan: A probabilistic programming language for Bayesian inference and optimization. Journal of Educational and Behavioural Statistics 40, 530–543.CrossRefGoogle Scholar
Hallwachs, W (1986) Agoutis (Dasyprocta punctata): the inheritors of guapinol (Hymenaea courbaril: Leguminosae). In Estrada, A and Fleming, TH (eds), Frugivores and Seed Dispersal. London: Springer, pp. 285–304.CrossRefGoogle Scholar
Haugaasen, JMT, Haugaasen, T, Peres, CA, Gribel, R and Wegge, P (2010) Seed dispersal of the Brazil nut tree (Bertholletia excelsa) by scatter-hoarding rodents in a central Amazonian forest. Journal of Tropical Ecology 26, 251–262.CrossRefGoogle Scholar
Holl, KD and Lulow, ME (1997) Effects of species, habitat and distance from edge on post-dispersal seed predation in a tropical rain forest. Biotropica 29, 459–468.CrossRefGoogle Scholar
Hoshizaki, K and Hulme, PE (2002) Mast seeding and predator-mediated indirect interactions in a forest community: evidence from post-dispersal fate of rodent-generated caches. In Levey, DJ, Silva, WR and Galetti, M (eds), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. Wallingford: CABI, pp. 227–239.Google Scholar
Jansen, PA, Bartholomeus, M, Bongers, F, Elzinga, JA, Den Ouden, J and Van Wieren, SE (2002) The role of seed size in dispersal by a scatter-hoarding rodent. In Levey, DJ, Silva, WR & Galetti, M (eds), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. Wallingford: CABI, pp. 209–225.Google Scholar
Jansen, PA, Bongers, F and Hemerik, L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecological Monographs 74, 569–589.CrossRefGoogle Scholar
Jansen, PA, Hirsch, BT, Emsens, W-J, Zamora-Gutierrez, V, Wikelski, M and Kays, R (2012) Thieving rodents as substitute dispersers of megafaunal seeds. Proceedings of the National Academy of Sciences USA 109, 12610–12615.CrossRefGoogle ScholarPubMed
Jansen, PA, Visser, MD, Wright, JS, Rutten, G and Muller-Landau, HC (2014) Negative density dependence of seed dispersal and seedling recruitment in a Neotropical palm. Ecology Letters 17, 1111–1120.CrossRefGoogle Scholar
Kuprewicz, EK (2013) Mammal abundances and seed traits control the seed dispersal and predation roles of terrestrial mammals in a Costa Rican forest. Biotropica 45, 333–342.CrossRefGoogle Scholar
Lang, Z and Wang, B (2016) The effect of seed size on seed fate in a subtropical forest, southwest of China. iForest-Biogeosciences and Forestry 9, 652.CrossRefGoogle Scholar
Lewis, CE, Clark, TW and Derting, TL (2001) Food selection by the white-footed mouse (Peromyscus leucopus) on the basis of energy and protein contents. Canadian Journal of Zoology 79, 562–568.CrossRefGoogle Scholar
Lichti, NI, Steele, MA, Zhang, H and Swihart, RK (2014) Mast species composition alters seed fate in North American rodent dispersed hardwoods. Ecology 95, 1746–1758.CrossRefGoogle ScholarPubMed
Lichti, NI, Steele, MA and Swihart, RK (2017) Seed fate and decision-making processes in scatter hoarding rodents. Biological Reviews 92, 474–504.CrossRefGoogle ScholarPubMed
Moore, JE, McEuen, AB, Swihart, RK, Contreras, TA and Steele, MA (2007) Determinants of seed removal distance by scatter hoarding rodents in deciduous forests. Ecology 88, 2529–2540.CrossRefGoogle ScholarPubMed
Moupela, C, Doucet, J, Daïnou, K, Tagg, N, Bourland, N and Vermeulen, C (2014) Dispersal and predation of diaspores of Coula edulis Baill. in an evergreen forest of Gabon. African Journal of Ecology 52, 88–96.CrossRefGoogle Scholar
Muñoz, A and Bonal, R (2008) Are you strong enough to carry that seed? Seed size/body size ratios influence seed choices by rodents. Animal Behaviour 76, 709–715.CrossRefGoogle Scholar
Nyiramana, A, Mendoza, I, Kaplin, BA and Forget, PM (2011) Evidence for seed dispersal by rodents in tropical montane forest in Africa. Biotropica 43, 654–657.CrossRefGoogle Scholar
R Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/.Google Scholar
Rosin, C and Poulsen, JR (2017) Telemetric tracking of scatterhoarding and seed fate in a Central African forest. Biotropica 49, 170–176.CrossRefGoogle Scholar
Seltzer, CE, Kremer, CT, Ndangalasi, HJ and Cordeiro, NJ (2015) Seed harvesting of a threatened African tree dispersed by rodents: is enrichment planting a solution? Global Ecology and Conservation 3, 645–653.CrossRefGoogle Scholar
Smythe, N (1970) Relationships between fruiting seasons and seed dispersal methods in a neotropical forest. American Naturalist 104, 25–35.CrossRefGoogle Scholar
Steele, MA, Knowles, T, Bridle, K and Simms, E (1993) Tannins and partial consumption of acorns; implications for dispersal of oaks by seed predators. American Naturalists 130, 229–238.CrossRefGoogle Scholar
Takahashi, A and Shimada, T (2008) Selective consumption of acorns by the Japanese wood mouse according to tannin content: a behavioral countermeasure against plant secondary metabolites. Ecological Research 23, 1033–1038.CrossRefGoogle Scholar
Vander Wall, SB (1990) Food Hoarding in Animals. Chicago, IL: University of Chicago Press.Google Scholar
Vander Wall, SB (2001) The evolutionary ecology of nut dispersal. Botanical Review 67, 74–117.CrossRefGoogle Scholar
Vander Wall, SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philosophical Transactions of the Royal Society of London B: Biological Sciences 365, 989–997.CrossRefGoogle ScholarPubMed
Vander Wall, SB and Jenkins, SH (2003) Reciprocal pilferage and the evolution of food-hoarding behavior. Behavoural Ecology 14, 656–667.CrossRefGoogle Scholar
Vander Wall, SB, Kuhn, KM and Beck, MJ (2005) Seed removal, seed predation and secondary seed dispersal. Ecology 86, 801–806.CrossRefGoogle Scholar
Wang, B and Chen, J (2009) Seed size, more than nutrient or tannin content, affects seed caching behavior of a common genus of Old World rodents. Ecology 90, 3023–3032.CrossRefGoogle ScholarPubMed
Wang, B and Chen, J (2011) Scatter-hoarding rodents prefer slightly astringent food. PLoS ONE 6, e26424.CrossRefGoogle ScholarPubMed
Wang, B, Wang, G and Chen, J (2012) Scatter-hoarding rodents use different foraging strategies for seeds from different plant species. Plant Ecology 213, 1329–1336.CrossRefGoogle Scholar
Wang, B, Ye, CX, Cannon, CH and Chen, J (2013) Dissecting the decision making process of scatter hoarding rodents. Oikos 122, 1027–1034.CrossRefGoogle Scholar
Wang, B, Chen, J and Corlett, R (2014) Factors influencing repeated seed movements by scatter-hoarding rodents in an alpine forest. Scientific Reports 4, 4786.CrossRefGoogle Scholar
Xiao, Z, Zhang, Z and Wang, Y (2005) Effects of seed size on dispersal distance in five rodent-dispersed fagaceous species. Acta Oecologia 28, 221–229.CrossRefGoogle Scholar
Xiao, Z, Wang, Y, Harris, M and Zhang, Z (2006) Spatial and temporal variation of seed predation and removal of sympatric large-seeded species in relation to innate seed traits in a subtropical forest, Southwest China. Forest Ecology Management 222, 46–54.CrossRefGoogle Scholar
Yadok, BG (2018) Aspects of the behaviour of African giant pouched rats (Cricetomys sp. nov) which impacts seed dispersal of large-seeded tree species in a West African montane forest landscape. PhD Dissertation, University of Canterbury, Christchurch, New Zealand.Google Scholar
Yadok, BG, Gerhard, D, Forget, PM and Chapman, H (2018) Size doesn’t matter: larger Carapa seeds are not dispersed farther by African rodent community. African Journal of Ecology 56, 1028–1033.CrossRefGoogle Scholar
Yadok, BG, Pech, R and Chapman, H (2019 a) Perception of predation risk by African giant pouched rats (Cricetomys sp. nov) is higher in forest-edge microhabitats. Behavioural Processes 168, 103953.CrossRefGoogle ScholarPubMed
Yadok, BG, Forget, P-M, Gerhard, D and Chapman, H (2019 b) Low fruit-crop years of Carapa oreophila drive increased seed removal and predation by scatterhoarding rodents in a West African forest. Acta Oecologica 99. doi: 10.1016/j.actao.2019.103448.CrossRefGoogle Scholar
Yi, X, Wang, Z, Liu, C and Liu, G (2015) Seed trait and rodent species determine seed dispersal and predation: evidences from semi-natural enclosures. IForest 8, 207.CrossRefGoogle Scholar
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