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Limited influence of experimentally induced predation risk on granivory in a tropical forest

Published online by Cambridge University Press:  21 February 2022

Alys Granados Open the ORCID record for Alys Granados [Opens in a new window] ,
Henry Bernard  and
Jedediah F. Brodie Open the ORCID record for Jedediah F. Brodie [Opens in a new window]
Alys Granados*
Affiliation:
Department of Zoology, University of British Columbia, Vancouver, BC, Canada
Henry Bernard
Affiliation:
Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia
Jedediah F. Brodie
Affiliation:
Division of Biological Sciences and Wildlife Biology Program, University of Montana, Missoula, MT, United States
*
Author for correspondence: Alys Granados, Email: [email protected]
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Abstract

Seed predation by rodents can strongly influence plant recruitment and establishment. The extent to which predation risk indirectly alters plant survival in tropical forests via impacts on granivory is unclear, making it difficult to assess the cascading impacts of widespread predator loss on tree recruitment and species composition. Experimental field studies that manipulate predation risk can help address these knowledge gaps and reveal whether antipredator responses among small mammals influence plant survival. We used camera traps and seed predation experiments to test the effects of perceived predation risk (via predator urine gel) on foraging behaviour of and seed removal by murid rodents in an unlogged and unhunted rainforest in Malaysian Borneo. We also explored the influence of seed traits (e.g., seed size) on removal by granivores and assessed whether granivore preferences for particular species were affected by predator urine. Murid visits to seed plots were positively related to overall seed removal, but were not affected by predator scent. Granivory was the lowest for the largest-seeded (>6 g) plant in our study, but was not influenced by predation risk. Predator urine significantly affected removal of one seed taxon (Dimoocarpus, ∼0.8 g), suggesting that removal by granivores may be affected by predation risk for some seed species but not others. This could have implications for plant species composition but may not affect the overall level of granivory.

Keywords

Borneocamera trapgranivoreMalaysiaMuridaeolfactory cuepredation riskseed removaltropical forest
Type
Short Communication
Information
Journal of Tropical Ecology , Volume 38 , Issue 4 , July 2022 , pp. 194 - 198
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Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Apfelbach, R, Blanchard, CD, Blanchard, RJ, Hayes, RA and McGregor, IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neuroscience & Biobehavioral Reviews 29, 1123–1144.CrossRefGoogle ScholarPubMed
Bates, DM and Maechler, M (2011) lme4: Linear mixed-effects models using S4 classes. R package version 1.1-7.Google Scholar
Bestion, E, Cucherousset, J, Teyissier, A and Cote, J (2015) Non-consumptive effects of a top-predator decrease the strength of the trophic cascade in a four-level terrestrial food web. Oikos 12, 1597–1603.CrossRefGoogle Scholar
Blackham, GV and Corlett, RT (2015) Post-dispersal seed removal by ground-feeding rodents in tropical peatlands, Central Kalimantan, Indonesia. Scientific Reports 5, 14152.CrossRefGoogle ScholarPubMed
Bowers, MA and Dooley, JL (1993) Predation hazard and seed removal by small mammals: microhabitat versus patch scale effects. Oecologia 94, 247–254.CrossRefGoogle ScholarPubMed
Bramley, GN and Waas, JR (2001) Laboratory and field evaluation of predator odors as repellents for kiore (Rattus exulans) and ship rats (R. rattus). Journal of Chemical Ecology 27, 1029–1047.CrossRefGoogle Scholar
Brewer, S (2001) Predation and dispersal of large and small seeds of a tropical palm. Oikos 92, 245–255.CrossRefGoogle Scholar
Bricker, M, Pearson, D and Maron, J (2010) Small-mammal seed predation limits the recruitment and abundance of two perennial grassland forbs. Ecology 91, 85–92.CrossRefGoogle ScholarPubMed
Brodie, JF, Aslan, CE, Rogers, HS, Redford, KH, Maron, JL, Bronstein, JL and Groves, CR (2014) Secondary extinctions of biodiversity. Trends in Ecology & Evolution 29, 664–672.CrossRefGoogle ScholarPubMed
Brodie, JF and Giordano, A (2013) Lack of trophic release with large mammal predators and prey in Borneo. Biological Conservation 163, 58–67.CrossRefGoogle Scholar
Brown, JS, Morgan, RA and Dow, BD (1992) Patch use under predation risk: II. A test with fox squirrels, Sciurus niger . Annales Zoologici Fennici 29, 311–318.Google Scholar
Buckle, A, Chia, T, Fenn, M and Visvalingam, M (1997) Ranging behaviour and habitat utilisation of the Malayan wood rat (Rattus tiomanicus) in an oil palm plantation in Johore, Malaysia. Crop Protection 16, 467–473.CrossRefGoogle Scholar
Bytheway, JP, Carthey, AJ and Banks, PB (2013) Risk vs. reward: how predators and prey respond to aging olfactory cues. Behavioral Ecology and Sociobiology 67, 715–725.CrossRefGoogle Scholar
Carthey, AJ and Banks, PB (2016) Naiveté is not forever: responses of a vulnerable native rodent to its long term alien predators. Oikos 125, 918–926.CrossRefGoogle Scholar
Charnov, EL (1976) Optimal foraging, the marginal value theorem. Theoretical Population Biology 9, 129–136.CrossRefGoogle ScholarPubMed
Cramer, MJ (2014) Seeds of doubt: feeding preferences of white-footed deer mice (Peromyscus leucopus noveboracensis) and woodland deer mice (Peromyscus maniculatus gracilis) on maple (genus Acer) seeds. Canadian Journal of Zoology 92, 771–776.CrossRefGoogle Scholar
de Guia, AP and Quibod, MNR (2014) Gut analysis of small non-volant mammals of Mt. Makiling, Luzon Island, Philippines. Journal of Environmental Science and Management 17, 63–68.CrossRefGoogle Scholar
Dielenberg, RA and McGregor, IS (2001) Defensive behavior in rats towards predatory odors: a review. Neuroscience & Biobehavioral Reviews 25, 597–609.CrossRefGoogle ScholarPubMed
Dirzo, R and Mendoza, E (2007) Size-related differential seed predation in a heavily defaunated neotropical rain forest. Biotropica 39, 355–362.CrossRefGoogle Scholar
Fendt, M (2006) Exposure to urine of canids and felids, but not of herbivores, induces defensive behavior in laboratory rats. Journal of Chemical Ecology 32, 2617–2627.CrossRefGoogle Scholar
Ferrero, DM, Lemon, JK, Fluegge, D, Pashkovski, SL, Korzan, WJ, Datta, SR, Spehr, M, Fendt, M and Liberles, SD (2011) Detection and avoidance of a carnivore odor by prey. Proceedings of the National Academy of Sciences 108, 11235–11240.CrossRefGoogle ScholarPubMed
Forget, PM and Jansen, PA (2007) Hunting increases dispersal limitation in the tree Carapa procera, a nontimber forest product. Conservation Biology 21, 106–113.CrossRefGoogle ScholarPubMed
Hautier, Y, Saner, P, Philipson, C, Bagchi, R, Ong, RC and Hector, A (2010) Effects of seed predators of different body size on seed mortality in Bornean logged forest. PLoS ONE 5, e11651.CrossRefGoogle ScholarPubMed
Hayes, RA, Nahrung, HF and Wilson, JC (2006) The response of native Australian rodents to predator odours varies seasonally: a by-product of life history variation? Animal Behaviour 71, 1307–1314.CrossRefGoogle Scholar
Hazebroek, H, Adlin, T and Sinun, W (2012) Danum Valley the rainforest. Natural History Publications (Borneo), Kota Kinabalu.Google Scholar
Herman, CS and Valone, TJ (2000) The effect of mammalian predator scent on the foraging behavior of Dipodomys merriami . Oikos 91, 139–145.CrossRefGoogle Scholar
Hernández, L and Laundré, JW (2005) Foraging in the ‘landscape of fear’ and its implications for habitat use and diet quality of elk Cervus elaphus and bison Bison bison. Wildlife Biology 11, 215–220.CrossRefGoogle Scholar
Hulme, PE, Benkman, CW, Herrera, CM and Pellmyr, O (2002) Granivory. Plant–animal interactions: an evolutionary approach. TJ International Ltd, Cornwall.Google Scholar
Kauffman, MJ, Brodie, JF, Jules, ES and Url, S (2013) Are wolves saving Yellowstone’s aspen? A landscape-level test of a behaviorally mediated trophic cascade. Ecology 91, 2742–2755.CrossRefGoogle Scholar
Keesing, F (1998) Impacts of ungulates on the demography and diversity of small mammals in central Kenya. Oecologia 116, 381–389.CrossRefGoogle ScholarPubMed
Laundré, J, Hernández, L, Medina, PL, Campanella, A, López-Portillo, J, González-Romero, A, Grajales-Tam, KM, Burke, AM, Gronemeyer, P and Browning, DM (2014) The landscape of fear: the missing link to understand top-down and bottom-up controls of prey abundance? Ecology 95, 1141–1152.CrossRefGoogle ScholarPubMed
Lenth, R (2020) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.5.2-1.Google Scholar
Lima, SL and Bednekoff, PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. The American Naturalist 153, 649–659.CrossRefGoogle ScholarPubMed
Lima, SL and Dill, LM. (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68, 619–640.CrossRefGoogle Scholar
Lüdecke, D, Ben-Shacar, MS, Patil, I, Waggoner, P and Makowski, D (2021) performance: an R package for assessment, comparison and testing of statistical models. Journal of Open Source Software 6, 3139.CrossRefGoogle Scholar
Mack, AL (1998) An advantage of large seed size: tolerating rather than succumbing to seed predators. Biotropica 30, 604–608.CrossRefGoogle Scholar
Mayor, SJ, Schneider, DC, Schaefer, JA and Mahoney, SP (2009) Habitat selection at multiple scales. Ecoscience 16, 238–247.CrossRefGoogle Scholar
McFrederick, QS, Fuentes, JD, Roulston, T, Kathilankal, JC and Lerdau, M (2009) Effects of air pollution on biogenic volatiles and ecological interactions. Oecologia 160, 411–420.CrossRefGoogle ScholarPubMed
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
Myster, RW and Pickett, S (1993) Effects of litter, distance, density and vegetation patch type on postdispersal tree seed predation in old fields. Oikos, 381–388.CrossRefGoogle Scholar
Neale, JC and Sacks, BN (2001) Resource utilization and interspecific relations of sympatric bobcats and coyotes. Oikos 94, 236–249.CrossRefGoogle Scholar
Orrock, JL and Danielson, BJ (2009) Temperature and cloud cover, but not predator urine, affect winter foraging of mice. Ethology 115, 641–648.CrossRefGoogle Scholar
Orrock, JL, Danielson, BJ and Brinkerhoff, RJ (2004) Rodent foraging is affected by indirect, but not direct, cues of predation risk. Behavioral Ecology 15, 433–437.CrossRefGoogle Scholar
Perez-Ramos, IM, Garcia-De La Cruz, Y and Gomez-Aparicio, L (2017) Contrasting responses of insects and vertebrates as seed consumers of two neotropical oak species: the interactive effects of individual crop size and seed mass. Forest Ecology and Management 401, 99–106.CrossRefGoogle Scholar
Phillips, Q and Phillips, K (2016) Mammals of Borneo and their ecology. Natural History Publications (Borneo), Kota Kinabalu. 400 p.Google Scholar
Preisser, EL, Bolnick, DI and Benard, MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86, 501–509.CrossRefGoogle Scholar
Ramp, D, Russell, BG and Croft, DB (2005) Predator scent induces differing responses in two sympatric macropodids. Australian Journal of Zoology 53, 73–78.CrossRefGoogle Scholar
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.Google Scholar
Rosell, F (2001) Effectiveness of predator odors as gray squirrel repellents. Canadian Journal of Zoology 79, 1719–1723.CrossRefGoogle Scholar
Schmitz, OJ, Krivan, V and Ovadia, O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecology Letters 7, 153–163.CrossRefGoogle Scholar
Sündermann, D, Scheumann, M and Zimmermann, E (2008) Olfactory predator recognition in predator-naive gray mouse lemurs (Microcebus murinus). Journal of Comparative Psychology 122, 146.CrossRefGoogle Scholar
Takahashi, LK, Nakashima, BR, Hong, H and Watanabe, K (2005) The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neuroscience & Biobehavioral Reviews 29, 1157–1167.CrossRefGoogle ScholarPubMed
Thornton, D, Sunquist, ME and Main, MB (2004) Ecological separation within newly sympatric populations of coyotes and bobcats in South-Central Florida. Journal of Mammalogy 85, 973–982.CrossRefGoogle Scholar
Wang, B, Ye, C and Chen, J (2013) Dissecting the decision making process of scatterhoarding rodents. Oikos 122, 1027–1034.CrossRefGoogle Scholar
Wells, K and Bagchi, R (2005) Eat in or take away-Seed predation and removal by rats (muridae) during a fruiting event in a dipterocarp rainforest. Raffles Bulletin of Zoology 53, 281–286.Google Scholar
Wells, K, Pfeiffer, M, Lakim, MB and Kalko, EK (2006) Movement trajectories and habitat partitioning of small mammals in logged and unlogged rain forests on Borneo. Journal of Animal Ecology 75, 1212–1223.CrossRefGoogle ScholarPubMed
Wolff, JO (2004) Scent marking by voles in response to predation risk: a field-laboratory validation. Behavioral Ecology 15, 286–289.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 and Management 222, 46–54.CrossRefGoogle Scholar
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