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Canopy gaps promote selective stem-cutting by small mammals of two dominant tree species in an African lowland forest: the importance of seedling chemistry

Published online by Cambridge University Press:  07 October 2015

Julian M. Norghauer ,
Gregory Röder  and
Gaëtan Glauser
Julian M. Norghauer*
Affiliation:
Institute of Plant Sciences, University of Bern, 21 Altenbergrain, 3013, Bern, Switzerland
Gregory Röder
Affiliation:
Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, 2000, Neuchâtel, Switzerland
Gaëtan Glauser
Affiliation:
Neuchâtel Platform of Analytical Chemistry, University of Neuchâtel, Avenue de Bellevaux 51, 2000, Neuchâtel, Switzerland
*
1Corresponding author. Email: [email protected]
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Abstract:

Small mammals can impede tree regeneration by injuring seedlings and saplings in several ways. One fatal way is by severing their stems, but apparently this type of predation is not well-studied in tropical rain forest. Here, we report on the incidence of ‘stem-cutting’ to new, wild seedlings of two locally dominant, canopy tree species monitored in 40 paired forest understorey and gap-habitat areas in Korup, Cameroon following a 2007 masting event. In gap areas, which are required for the upward growth and sapling recruitment of both species, 137 seedlings of the long-lived, light-demanding, fast-growing large tropical tree (Microberlinia bisulcata) were highly susceptible to stem-cutting (83% of deaths) — it killed 39% of all seedlings over a c. 2-y period. In stark contrast, seedlings of the more shade-tolerant, slower-growing tree species (Tetraberlinia bifoliolata) were hardly attacked (4.3%). In the understorey, however, stem-cutting was virtually absent. Across the gap areas, the incidence of stem-cutting of M. bisulcata seedlings showed significant spatial variation that could not be explained significantly by either canopy openness or Janzen–Connell type effects (proximity and basal area of conspecific adult trees). To examine physical and chemical traits that might explain the species difference to being cut, bark and wood tissues were collected from a separate sample of seedlings in gaps (i.e. not monitored for stem-cutting). These analyses suggested that, compared with T. bifoliolata, the lower stem density, higher Mg and K and fatty acid concentrations in bark, and fewer phenolic and terpene compounds in M. bisulcata seedlings made them more palatable and attractive to small-mammal predators, likely rodents. We conclude that selective stem-cutting is a potent countervailing force to the current local canopy dominance of the grove-forming M. bisulcata by limiting the recruitment and abundance of its saplings. Given the ubiquity of gaps and ground-dwelling rodents in pantropical forests, it would be surprising if this form of lethal browsing was restricted to Korup.

Keywords

Africacanopy disturbanceplant recruitmentplant resistance traitsregenerationseedling predationsmall mammalstree phytochemistrytropical forest
Type
Research Article
Information
Journal of Tropical Ecology , Volume 32 , Issue 1 , January 2016 , pp. 1 - 21
Copyright
Copyright © Cambridge University Press 2015 

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References

LITERATURE CITED

ALVAREZ-CLARE, S. & KITAJIMA, K. 2007. Physical defence traits enhance seedling survival of neotropical tree species. Functional Ecology 21:1044–1054.CrossRefGoogle Scholar
ALVAREZ-CLARE, S. & KITAJIMA, K. 2009. Susceptibility of tree seedlings to biotic and abiotic hazards in the understory of a moist tropical forest in Panama. Biotropica 41:47–56.CrossRefGoogle Scholar
BAXTER, R. & HANSSON, L. 2008. Bark consumption by small rodents in the northern and southern hemispheres. Mammal Review 31:47–59.CrossRefGoogle Scholar
BECK, H., GAINES, M. S., HINES, J. E. & NICHOLS, J. D. 2004. Comparative dynamics of small mammal populations in treefall gaps and surrounding understorey within Amazonian rainforest. Oikos 106:27–38.CrossRefGoogle Scholar
BEDOYA-PEREZ, M. A., ISLER, I., BANKS, P. B. & MCARTHUR, C. 2014. Roles of the volatile terpene, 1,8-cineole, in plant-herbivore interactions: a foraging odor cue as well as a toxin? Oecologia 174:827–837.CrossRefGoogle ScholarPubMed
BOZINOVIC, F., NOVOA, F. F. & SABAT, P. 1997. Feeding and digesting fiber and tannins by an herbivorous rodent, Octodon degus (Rodentia: Caviomorpha). Comparative Biochemistry and Physiology Part A: Physiology 118:625–630.CrossRefGoogle ScholarPubMed
BRYANT, J. P., PROVENZA, F. D., PASTOR, J., REICHARDT, P. B., CLAUSEN, T. P. & DUTOIT, J. T. 1991. Interactions between woody-plants and browsing mammals mediated by secondary metabolites. Annual Review of Ecology and Systematics 22:431–446.CrossRefGoogle Scholar
CLARK, C. J., POULSEN, J. R. & LEVEY, D. J. 2012. Vertebrate herbivory impacts seedling recruitment more than niche partitioning or density-dependent mortality. Ecology 93:554–564.CrossRefGoogle ScholarPubMed
COLEY, P. D., BRYANT, J. P. & CHAPIN, F. S. 1985. Resource availability and plant antiherbivore defense. Science 230:895–899.CrossRefGoogle ScholarPubMed
CONNELL, J. H. 1989. Some processes affecting the species composition in forest gaps. Ecology 70:560–562.CrossRefGoogle Scholar
CRAWLEY, M. J. 1983. Herbivory: the dynamics of animal–plant interactions. University of California Press, Berkeley. 437 pp.Google Scholar
DE MATTOS, I. L. & ZAGAL, J. H. 2010. Detection of total phenol in green and black teas by flow injection system and unmodified screen printed electrode. International Journal of Analytical Chemistry 2010:143714.CrossRefGoogle ScholarPubMed
DENSLOW, J. S. 1987. Tropical rain-forest gaps and tree species-diversity. Annual Review of Ecology and Systematics 18:431–451.CrossRefGoogle Scholar
FA, J. E., SEYMOUR, S., DUPAIN, J., AMIN, R., ALBRECHTSEN, L. & MACDONALD, D. 2006. Getting to grips with the magnitude of exploitation: bushmeat in the Cross-Sanaga Rivers region, Nigeria and Cameroon. Biological Conservation 129:497–510.CrossRefGoogle Scholar
FREELAND, W. J. & JANZEN, D. H. 1974. Strategies in herbivory by mammals – the role of secondary compounds. American Naturalist 108:269–289.CrossRefGoogle Scholar
GILL, R. M. A. 1992. A review of damage by mammals in north temperate forests. 2. Small mammals. Forestry 65:281–308.CrossRefGoogle Scholar
GREEN, J. J. & NEWBERY, D. M. 2001. Light and seed size affect establishment of grove-forming ectomycorrhizal rain forest tree species. New Phytologist 151:271–289.CrossRefGoogle ScholarPubMed
GREEN, J. J. & NEWBERY, D. M. 2002. Reproductive investment and seedling survival of the mast-fruiting rain forest tree, Microberlinia bisulcata A. Chev. Plant Ecology 162:169–183.CrossRefGoogle Scholar
HALL, J. S. 2008. Seed and seedling survival of African mahogany (Entandrophragma spp.) in the Central African Republic: implications for forest management. Forest Ecology and Management 255:292–299.CrossRefGoogle Scholar
HANSSON, L. 1973. Fatty substances as attractants for Microtus agrestis and other small rodents. Oikos 24:417–421.CrossRefGoogle Scholar
HANSSON, L. 1991. Bark consumption by voles in relation to mineral contents. Journal of Chemical Ecology 17:735–743.CrossRefGoogle ScholarPubMed
HARPER, J. L. 1977. Population biology of plants. Academic Press, London. 892 pp.Google Scholar
HARTSHORN, G. S. 1978. Tree falls and forest dynamics. Pp. 617–638 in Tomlinson, P. B. & Zimmermann, M. H. (eds.). Tropical trees as living systems. Cambridge University Press, Cambridge.Google Scholar
HJÄLTÉN, J. & PALO, T. 1992. Selection of deciduous trees by free ranging voles and hares in relation to plant chemistry. Oikos 63:477–484.CrossRefGoogle Scholar
HOWARD, W. E., MARSH, R. E. & COLE, R. E. 1968. Food detection by deer mice using olfactory rather than visual cues. Animal Behaviour 16:13–17.CrossRefGoogle ScholarPubMed
IDA, H. & NAKAGOSHI, N. 1996. Gnawing damage by rodents to the seedlings of Fagus crenata and Quercus mongolica var grosseserrata in a temperate Sasa grassland deciduous forest series in southwestern Japan. Ecological Research 11:97–103.CrossRefGoogle Scholar
ICKES, K., PACIOREK, C. J. & THOMAS, S. C. 2005. Impacts of nest construction by native pigs (Sus scrofa) on lowland Malaysian rain forest saplings. Ecology 86:1540–1547.CrossRefGoogle Scholar
JANSEN, P. A., BONGERS, F. & HEMERIK, L. 2004. Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecological Monographs 74:569–589.CrossRefGoogle Scholar
JANZEN, D. H. 1970. Herbivores and number of tree species in tropical forests. American Naturalist 104:501–528.CrossRefGoogle Scholar
JANZEN, D. H. 1971. Seed predation by animals. Annual Review of Ecology and Systematics 2:465–492.CrossRefGoogle Scholar
KINGDON, J. 1997. The Kingdon Field Guide to African mammals. Academic Press, London. 464 pp.Google Scholar
KITAJIMA, K., CORDERO, R. A. & JOSEPH WRIGHT, S. 2013. Leaf life span spectrum of tropical woody seedlings: effects of light and ontogeny and consequences for survival. Annals of Botany 112:685–699.CrossRefGoogle ScholarPubMed
KUIJPER, D. P. J., CROMSIGT, J. P. G. M., CHURSKI, M., ADAM, B., JEDRZEJEWSKA, B. & JEDRZEJEWSKI, W. 2009. Do ungulates preferentially feed in forest gaps in European temperate forest? Forest Ecology and Management 258:1528–1535.CrossRefGoogle Scholar
LAMBERT, T. D., MALCOLM, J. R. & ZIMMERMAN, B. L. 2006. Amazonian small mammal abundances in relation to habitat structure and resource abundance. Journal of Mammalogy 87:766–776.CrossRefGoogle Scholar
LEE, H. K., LEE, H. S. & AHN, Y. J. 1999. Antignawing factor derived from Cinnamomum cassia bark against mice. Journal of Chemical Ecology 25: 1131–1139.CrossRefGoogle Scholar
MALCOLM, J. R. 1995. Forest structure and the abundance of small mammals in Amazonian fragments. Pp. 179–197 in Lowman, M. D. & Nadkarni, N. M. (eds.). Forest canopies. Academic Press, San Diego.Google Scholar
MALCOLM, J. R. 2004. Ecology and conservation of canopy mammals. Pp. 297–331 in Lowman, M. D. & Rinker, H. B. (eds.). Forest canopies. (Second edition). Academic Press, San Diego.CrossRefGoogle Scholar
MALCOLM, J. R. & RAY, J. C. 2000. Influence of timber extraction routes on central African small-mammal communities, forest structure, and tree diversity. Conservation Biology 14:1623–1638.Google ScholarPubMed
MARON, J. L. & CRONE, E. 2006. Herbivory: effects on plant abundance, distribution and population growth. Proceedings of the Royal Society B – Biological Sciences 273:2575–2584.CrossRefGoogle ScholarPubMed
NEWBERY, D. M., ALEXANDER, I. J. & ROTHER, J. A. 1997. Phosphorus dynamics in a lowland African rain forest: the influence of ectomycorrhizal trees. Ecological Monographs 67:367–409.Google Scholar
NEWBERY, D. M., SONGWE, N. C. & CHUYONG, G. B. 1998. Phenology and dynamics of an African rainforest at Korup, Cameroon. Pp. 267–308 in Newbery, D. M., Prins, H. H. T. & Brown, N. D. (eds.). Dynamics of tropical communities. Blackwell Science, Oxford.Google Scholar
NEWBERY, D. M., CHUYONG, G. B. & ZIMMERMANN, L. 2006. Mast fruiting of large ectomycorrhizal African rain forest trees: importance of dry season intensity, and the resource-limitation hypothesis. New Phytologist 170:561–579.CrossRefGoogle ScholarPubMed
NEWBERY, D. M., VAN DER BURGT, X. M., WORBES, M. & CHUYONG, G. B. 2013. Transient dominance in a central African rain forest. Ecological Monographs 83:339–382.CrossRefGoogle Scholar
NORGHAUER, J. M. & NEWBERY, D. M. 2011. Seed fate and seedling dynamics after masting in two African rain forest trees. Ecological Monographs 81:443–468.CrossRefGoogle Scholar
NORGHAUER, J. M. & NEWBERY, D. M. 2013. Herbivores equalize the seedling height growth of three dominant tree species in an African tropical rain forest. Forest Ecology and Management 310:555–566.CrossRefGoogle Scholar
NORGHAUER, J. M. & NEWBERY, D. M. 2014. Herbivores differentially limit the seedling growth and recruitment of two dominant rain forest trees. Oecologia 174:459–469.CrossRefGoogle ScholarPubMed
NORGHAUER, J. M. & NEWBERY, D. M. 2015. Tree size and fecundity influence ballistic seed dispersal of two dominant mast-fruiting species in a tropical rain forest. Forest Ecology and Management 338:100–113.CrossRefGoogle Scholar
NORGHAUER, J. M., MALCOLM, J. R., ZIMMERMAN, B. L. & FELFILI, J. M. 2006. An experimental test of density- and distant-dependent recruitment of mahogany (Swietenia macrophylla) in southeastern Amazonia. Oecologia 148:437–446.CrossRefGoogle ScholarPubMed
NORGHAUER, J. M., GLAUSER, G. & NEWBERY, D. M. 2014. Seedling resistance, tolerance and escape from herbivores: insights from co-dominant canopy tree species in a resource-poor African rain forest. Functional Ecology 28:1426–1439.CrossRefGoogle Scholar
OLAYEMI, A., NICOLAS, V., HULSELMANS, J., MISSOUP, A. D., FICHET-CALVET, E., AMUNDALA, D., DUDU, A., DIERCKX, T., WENDELEN, W., LEIRS, H. & VERHEYEN, E. 2012. Taxonomy of the African giant pouched rats (Nesomyidae: Cricetomys): molecular and craniometric evidence support an unexpected high species diversity. Zoological Journal of the Linnean Society 165:700–719.CrossRefGoogle Scholar
OSTFELD, R. S. & CANHAM, C. D. 1993. Effects of meadow vole population density on tree seedling survival in old fields. Ecology 74:1792–1801.CrossRefGoogle Scholar
OSUNKOYA, O. O., ASH, J. E., GRAHAM, A. W. & HOPKINS, M. S. 1993. Growth of tree seedlings in tropical rain-forests of North Queensland, Australia. Journal of Tropical Ecology 9:1–18.CrossRefGoogle Scholar
PAINE, C. E. T. & BECK, H. 2007. Seed predation by neotropical rain forest mammals increases diversity in seedling recruitment. Ecology 88:3076–3087.CrossRefGoogle ScholarPubMed
PÉREZ-HARGUINDEGUY, N., DIAZ, 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., BUCHMANN, N., FUNES, G., QUETIER, F., HODGSON, J. G., THOMPSON, K., MORGAN, H. D., TER STEEGE, H., VAN DER HEIJDEN, M. G., SACK, L., BLONDER, B., POSCHLOD, P., VAIERETTI, M. V., CONTI, G., STAVER, A. C., AQUINO, S. & CORNELISSEN, J. H. C. 2013. New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61:167–234.CrossRefGoogle Scholar
PIGOTT, C. D. 1985. Selective damage to tree-seedlings by bank voles (Clethrionomys glareolus). Oecologia 67:367–371.CrossRefGoogle ScholarPubMed
RÜGER, N., HUTH, A., HUBBELL, S. P. & CONDIT, R. 2009. Response of recruitment to light availability across a tropical lowland rain forest community. Journal of Ecology 97:1360–1368.CrossRefGoogle Scholar
SATO, T. 2000. Effects of rodent gnawing on the survival of current-year seedlings of Quercus crispula. Ecological Research 15:335–344.CrossRefGoogle Scholar
SCHUPP, E. W. 1988. Seed and early seedling predation in the forest understory and in treefall gaps. Oikos 51:71–78.CrossRefGoogle Scholar
SORK, V. L. 1987. Effects of predation and light on seedling establishment in Gustavia superba. Ecology 68:1341–1350.CrossRefGoogle Scholar
STRUHSAKER, T. T. 1997. Ecology of an African rain forest: logging in Kibale and the conflict between conservation and exploitation. University Press of Florida, Gainsville. 434 pp.Google Scholar
THEIMER, T. C., GEHRING, C. A., GREEN, P. T. & CONNELL, J. H. 2011. Terrestrial vertebrates alter seedling composition and richness but not diversity in an Australian tropical rain forest. Ecology 92:1637–1647.CrossRefGoogle ScholarPubMed
VANDER WALL, S. B. 1998. Foraging success of granivorous rodents: effects of variation in seed and soil water on olfaction. Ecology 79:233–241.CrossRefGoogle Scholar
VANDER WALL, S. B. 2010. How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365:989–997.CrossRefGoogle ScholarPubMed
WATT, A. S. 1919. On the causes of failure of natural regeneration in British oakwoods. Journal of Ecology 7:173–203.CrossRefGoogle Scholar
WATT, A. S. 1923. On the ecology of British beechwoods with special reference to their regeneration. Journal of Ecology 11:1–48.CrossRefGoogle Scholar
WEEKS, H. P. & KIRKPATRICK, C. M. 1978. Salt preferences and sodium drive phenology in fox squirrels and woodchucks. Journal of Mammalogy 59:531–542.CrossRefGoogle Scholar
WESTERHUIS, J. A., HOEFSLOOT, H. C. J., SMIT, S., VIS, D. J., SMILDE, A. K., VAN VELZEN, E. J. J., VAN DUIJNHOVEN, J. P. M. & VAN DORSTEN, F. A. 2008. Assessment of PLSDA cross validation. Metabolomics 4:81–89.CrossRefGoogle Scholar
WORLEY, B. & POWERS, R. 2013. Multivariate analysis in metabolomics. Current Metabolomics 1:92–107.Google ScholarPubMed