Scatter-hoarding rodents disperse seeds to safe sites in a fire-prone ecosystem
- 386 Downloads
- 6 Citations
Abstract
Fire can potentially decimate soil seed banks, even for species that are abundant in fire-prone areas. Many plants, like the widespread and dominant members of the genus Arctostaphylos in the fire-prone California Floristic Province, have seeds that (i) have no clear adaptions for dispersal and (ii) experience lethal fire temperatures if present on or near the soil surface. In this study, we aim to resolve these juxtaposed observations by mechanistically determining how one species, Arctostaphylos patula, is dispersed. To distinguish among dispersal modalities and determine the seed shadow, deposition patterns, and the conditions under which seeds germinate, we employed full-shrub exclosure treatments to monitor fruit removal, used a mark-relocation technique by radioactively labeling seeds, identified dispersers using motion-sensor cameras, and surveyed seedlings following fire to relate natural germination patterns to measured patterns from our experiment. Seed removal from exclosure treatments that allowed rodents access to shrubs was higher than those that prevented rodent access to shrubs, and cameras at radioactively labeled-seed stations failed to detect the presence of any other disperser; thus implicating rodents as the primary disperser of A. patula seeds. This evidence is corroborated by our finding from tracking radioactively labeled seeds that the depth at which rodents bury seeds completely overlaps with the depth from which we observed seedlings germinate following two fire events. Our study extends the boundary of what is understood as a scatter-hoarding seed dispersal syndrome and identifies a mechanism that allows populations of Arctostaphylos to exist in spite of recurrent fires that can be lethal to seeds and hazardous to plant populations.
Keywords
Arctostaphylos Dispersal Immaturity risk Mutualism Scatter-hoarding Seed dispersal syndromeNotes
Acknowledgments
Funding was provided by the Whittell Forest Fellowship, UNR-EECB small Grant, and UNR-GSA research grant. The Whittell Forest and Wildlife Area allowed us to conduct our experiments. T. Parker and J. Keeley kindly reviewed the current manuscript. J. Chambers, M. Forister, G. Hoelzer, and S. Mensing kindly provided comments on a previous version of the manuscript. B. Nolting kindly gave feedback on polar coordinates in this Cartesian wold.
References
- Andersen AN (1989) How important is seed predation to recruitment in stable populations of long-lived perennials? Oecologia 81(3):310–315CrossRefGoogle Scholar
- Auld TD (1986a) Population dynamics of the shrub Acacia suaveolens (sm.) willd.: dispersal and the dynamics of the soil seed-bank. Aust J Ecol 11(3):235–254CrossRefGoogle Scholar
- Auld TD (1986b) Population dynamics of the shrub Acacia suaveolens (sm.) willd.: fire and the transition to seedlings. Aust J Ecol 11(4):373–385CrossRefGoogle Scholar
- Barga SC, Vander Wall SB (2013) Dispersal of an herbaceous perennial, Paeonia brownii, by scatter-hoarding rodents. Ecoscience 20(2):172–181. doi: 10.2980/20-2-3594 CrossRefGoogle Scholar
- Barnett RJ (1977) The effect of burial by squirrels on germination and survival of oak and hickory nuts. Am Midl Nat 98:19–30CrossRefGoogle Scholar
- Bolker BM, Pacala SW (1999) Spatial moment equations for plant competition: understanding spatial strategies and the advantages of short dispersal. Am Nat 153(6):575–602CrossRefGoogle Scholar
- Bond WJ, Midgley JJ (2001) Ecology of sprouting in woody plants: the persistence niche. Trends Ecol Evol 16(1):45–51CrossRefPubMedGoogle Scholar
- Borchert M, Schreiner D, Knowd T, Plumb T (2002) Predicting postfire survival in coulter pine (Pinus coulteri) and gray pine (Pinus sabiniana) after wildfire in central California. West J Appl For 17(3):134–138Google Scholar
- Borchert M, Johnson M, Schreiner D, Vander Wall S (2003) Early postfire seed dispersal, seedling establishment and seedling mortality of Pinus coulteri (D. Don) in central coastal California, USA. Plant Ecol 168(2):207–220CrossRefGoogle Scholar
- Bowyer RT, McKenna SA, Shea ME (1983) Seasonal changes in coyote food habits as determined by fecal analysis. Am Midl Nat 109:266–273CrossRefGoogle Scholar
- Bullock JM, Galsworthy SJ, Manzano P, Poschlod P, Eichberg C, Walker K, Wichmann MC (2011) Process-based functions for seed retention on animals: a test of improved descriptions of dispersal using multiple data sets. Oikos 120(8):1201–1208. doi: 10.1111/j.1600-0706.2010.19092.x CrossRefGoogle Scholar
- Chambers JC, MacMahon JA, Haefner JH (1991) Seed entrapment in alpine ecosystems: effects of soil particle size and diaspore morphology. Ecology 72(5):1668–1677CrossRefGoogle Scholar
- Cipollini ML, Stiles EW (1993) Fruit rot, antifungal defense, and palatability of fleshy fruits for frugivorous birds. Ecology 74(3):751–762Google Scholar
- Clark C, Poulsen J, Levey D, Osenberg C (2007) Are plant populations seed limited? a critique and meta-analysis of seed addition experiments. Am Nat 170(1):128–142CrossRefPubMedGoogle Scholar
- Cohen D, Levin SA (1991) Dispersal in patchy environments: the effects of temporal and spatial structure. Theor Popul Biol 39(1):63–99CrossRefGoogle Scholar
- Cousens RD, Dytham C, Law R (2008) Dispersal in plants: a population perspective. Oxford University Press Inc., OxfordCrossRefGoogle Scholar
- Delibes M, Hernandez L, Hiraldo F (1989) Comparative food habits of three carnivores in western Sierra Madre, Mexico. Z Saugetierkunde 54:107–110Google Scholar
- Dennis AJ (2003) Scatter-hoarding by musky rat-kangaroos, Hypsiprymnodon moschatus, a tropical rain-forest marsupial from Australia: implications for seed dispersal. J Trop Ecol 19(06):619–627CrossRefGoogle Scholar
- Enders MS, Vander Wall SB (2012) Black bears Ursus americanus are effective seed dispersers, with a little help from their friends. Oikos 121(4):589–596. doi: 10.1111/j.1600-0706.2011.19710.x CrossRefGoogle Scholar
- Eriksson O, Ehrlén J (1992) Seed and microsite limitation of recruitment in plant populations. Oecologia 91(3):360–364CrossRefGoogle Scholar
- Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194CrossRefGoogle Scholar
- Hanes TL (1971) Succession after fire in the chaparral of southern California. Ecol Monogr 41(1):27–52. doi: 10.2307/1942434 CrossRefGoogle Scholar
- Harper JL (1977) Population biology of plants. Academic Press Inc. (London) Ltd, New YorkGoogle Scholar
- Hastings A (1980) Disturbance, coexistence, history, and competition for space. Theor Popul Biol 18(3):363–373. doi: 10.1016/0040-5809(80)90059-3 CrossRefGoogle Scholar
- Hirsch BT, Kays R, Pereira VE, Jansen PA (2012) Directed seed dispersal towards areas with low conspecific tree density by a scatter-hoarding rodent. Ecol Lett 15(12):1423–1429. doi: 10.1111/ele.12000 CrossRefPubMedGoogle Scholar
- Humphreys AM, Antonelli A, Pirie MD, Linder HP (2011) Ecology and evolution of the diaspore “burial syndrome”. Evolution 65(4):1163–1180. doi: 10.1111/j.1558-5646.2010.01184.x CrossRefPubMedGoogle Scholar
- Jansen PA, Bongers F, Hemerik L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecol Monogr 74(4):569–589CrossRefGoogle Scholar
- Jansen PA, Visser MD, Wright SJ, Rutten G, Muller-Landau HC (2014) Negative density dependence of seed dispersal and seedling recruitment in a neotropical palm. Ecol Lett 17(9):1111–1120. doi: 10.1111/ele.12317 CrossRefPubMedGoogle Scholar
- Janson CH (1983) Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 219(4581):187–189. doi: 10.1126/science.219.4581.187
- Janzen DH (1977) Why fruits rot, seeds mold, and meat spoils. Am Nat 111(980):691–713Google Scholar
- Jordano P (1995) Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant-animal interactions. Am Nat 145(2):163–191. doi: 10.2307/2463122
- Kauffman JB, Martin RE (1991) Factors influencing the scarification and germination of three montane Sierra Nevada shrubs. Northwest Sci 65(4):180–187Google Scholar
- Keeley JE (1977) Seed production, seed populations in soil, and seedling production after fire for two congeneric pairs of sprouting and nonsprouting chaparal shrubs. Ecology 58(4):820–829Google Scholar
- Keeley JE (1987a) Role of fire in seed-germination of woody taxa in California chaparral. Ecology 68(2):434–443CrossRefGoogle Scholar
- Keeley JE (1987b) Ten years of change in seed banks of the chaparral shrubs, Arctostaphylos glauca and A. glandulosa. Am Midl Nat 117:446–448CrossRefGoogle Scholar
- Keeley JE (1991) Seed germination and life history syndromes in the California chaparral. Bot Rev 57(2):81–116Google Scholar
- Keeley JE, Fotheringham C (2000) Role of fire in regeneration from seed, vol 2. CAB International Oxford, OxfordGoogle Scholar
- Keeley JE, Hays RL (1976) Differential seed predation on two species of Arctostaphylos (Ericaceae). Oecologia 24(1):71–81CrossRefGoogle Scholar
- Keeley JE, Fotheringham CJ, Baer-Keeley M (2006) Demographic patterns of postfire regeneration in Mediterranean-climate shrublands of California. Ecol Monogr 76(2):235–255CrossRefGoogle Scholar
- Kelly VR, Parker VT (1990) Seed bank survival and dynamics in sprouting and nonsprouting Arctostaphylos species. Am Midl Nat 124:114–123CrossRefGoogle Scholar
- Korb JE, Johnson NC, Covington WW (2004) Slash pile burning effects on soil biotic and chemical properties and plant establishment: recommendations for amelioration. Restor Ecol 12(1):52–62. doi: 10.1111/j.1061-2971.2004.00304.x CrossRefGoogle Scholar
- Levin SA, Cohen D, Hastings A (1984) Dispersal strategies in patchy environments. Theor Popul Biol 26(2):165–191CrossRefGoogle Scholar
- Levins R, Culver D (1971) Regional coexistence of species and competition between rare species. Proc Natl Acad Sci 68(6):1246–1248PubMedCentralCrossRefPubMedGoogle Scholar
- Lomáscolo SB, Speranza P, Kimball RT (2008) Correlated evolution of fig size and color supports the dispersal syndromes hypothesis. Oecologia 156(4):783–796CrossRefPubMedGoogle Scholar
- Longland WS, Jenkins SH, Wall SBV, Veech JA, Pyare S (2001) Seedling recruitment in Oryzopsis hymenoides: are desert granivores mutualists or predators? Ecology 82(11):3131–3148. doi: 10.2307/2679840
- Mayer J, Khairy K, Howard J (2010) Drawing an elephant with four complex parameters. Am J Phys 78(6):648–649. doi: 10.1119/1.3254017 CrossRefGoogle Scholar
- Moles AT, Ackerly DD, Webb CO, Tweddle JC, Dickie JB, Pitman AJ, Westoby M (2005a) Factors that shape seed mass evolution. Proc Natl Acad Sci USA 102(30):10,540–10,544Google Scholar
- Moles AT, Ackerly DD, Webb CO, Tweddle JC, Dickie JB, Westoby M (2005b) A brief history of seed size. Science 307(5709):576–580. doi: 10.1126/science.1104863 CrossRefPubMedGoogle Scholar
- Moles AT, Ackerly DD, Tweddle JC, Dickie JB, Smith R, Leishman MR, Mayfield MM, Pitman A, Wood JT, Westoby M (2007) Global patterns in seed size. Glob Ecol Biogeogr 16:109–116CrossRefGoogle Scholar
- Moore CM (2014) Seed dispersal and seed dispersal syndromes in manzanitas, and other higher plants. PhD Thesis, University of Nevada, RenoGoogle Scholar
- Moritz MA (2003) Spatiotemporal analysis of controls on shrubland fire regimes: age dependency and fire hazard. Ecology 84(2):351–361. doi: 10.2307/3107890
- Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15(7):278–285Google Scholar
- Nathan R, Klein E, Robledo-Arnuncio J, Revilla E (2012) Dispersal kernels: review. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution, 1st edn. Oxford University Press Inc., OxfordGoogle Scholar
- Nielsen SE, Munro RHM, Bainbridge EL, Stenhouse GB, Boyce MS (2004) Grizzly bears and forestry: II. Distribution of grizzly bear foods in clearcuts of west-central Alberta, Canada. For Ecol Manag 199:67–82CrossRefGoogle Scholar
- Odion DC, Davis FW (2000) Fire, soil heating, and the formation of vegetation patterns in chaparral. Ecol Monogr 70(1):149–169CrossRefGoogle Scholar
- Parker VT (1987) Effect of wet-season management burns on chaparral regeneration: implications for rare species. California Native Plant Society, SacramentoGoogle Scholar
- Parker VT, Kelly VR (1989) Seed banks in California chaparral and other Mediterranean climate shrublands. In: Leck MA, Parker VT, Simpson RL (eds) Ecology of soil seed banks. Academic Press Inc, San Diego, Chap 11, pp 231–256Google Scholar
- Parker VT, Vasey MC, Keeley JE (2012) Arctostaphylos. In: Baldwin BG, Goldman D, Keil R D J Patterson, Rosatti TJ (eds) The Jepson Manual: vascular plants of California, Thoroughly revised and expanded, 2nd edn, University of California PressGoogle Scholar
- Peart DR (1985) The quantitative representation of seed and pollen dispersal. Ecology 66(3):1081–1083. doi: 10.2307/1940567 CrossRefGoogle Scholar
- Peart MH (1984) The effects of morphology, orientation and position of grass diaspores on seedling survival. J Ecol 72(2):437–453. doi: 10.2307/2260057
- R Core Team (2014) R: A language and environment for statistical computing, version 3.1.1—sock it to me. http://www.R-project.org/
- Rogers BJ (1950) The effect of fire on the germination of seed of Arctostaphylos viscida (Parry). Ph.D. Thesis, University of California, BerkeleyGoogle Scholar
- Roth JK, Vander Wall SB (2005) Primary and secondary seed dispersal of bush chinquapin (Fagaceae) by scatterhoarding rodents. Ecology 86:2428–2439CrossRefGoogle Scholar
- Silverman BW (1986) Density estimation for statistics and data analysis. Chapman and Hall, New YorkCrossRefGoogle Scholar
- Silverstein RP (2005) Germination of native and exotic plant seeds dispersed by coyotes (Canis latrans) in southern California. The Southwestern Naturalist 50(4):472–478. doi: 10.1894/0038-4909(2005)050[0472:GONAEP]2.0.CO;2 CrossRefGoogle Scholar
- Smith C, Reichman O (1984) The evolution of food caching by birds and mammals. Annu Rev Ecol Syst 15:329–351CrossRefGoogle Scholar
- Taylor AH (2004) Identifying forest reference conditions on early cut-over lands, Lake Tahoe Basin, USA. Ecol Appl 14:1903–1920CrossRefGoogle Scholar
- Tevis L (1953) Stomach contents of chipmunks and mantled squirrels in northeastern California. J Mammal 34(3):316–324Google Scholar
- Thompson K, Band S, Hodgson J (1993) Seed size and shape predict persistence in soil. Funct Ecol 7:236–241CrossRefGoogle Scholar
- Thomson FJ, Moles AT, Auld TD, Ramp D, Ren S, Kingsford RT (2010) Chasing the unknown: predicting seed dispersal mechanisms from plant traits. J Ecol 98(6):1310–1318. doi: 10.1111/j.1365-2745.2010.01724.x CrossRefGoogle Scholar
- Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75(1):2–16CrossRefGoogle Scholar
- Valido A, Schaefer H, Jordano P (2011) Colour, design and reward: phenotypic integration of fleshy fruit displays. J Evolut Biol 24(4):751–760CrossRefGoogle Scholar
- Van der Pijl L (1982) Principles of dispersal in higher plants. Springer, BerlinCrossRefGoogle Scholar
- Vander Wall SB (1993a) Cache site selection by chipmunks (Tamias spp.) and its influence on the effectiveness of seed dispersal in jeffrey pine (Pinus jeffreyi). Oecologia 96(2):246–252. doi: 10.1007/BF00317738 CrossRefGoogle Scholar
- Vander Wall SB (1993b) A model of caching depth: implications for scatter hoarders and plant dispersal. Am Nat 141:217–232CrossRefPubMedGoogle Scholar
- Vander Wall SB (1994) Seed fate pathways of antelope bitterbrush: dispersal by seed-caching yellow pine chipmunks. Ecology 75(7):1911–1926Google Scholar
- Vander Wall SB (2005) Whittell Forest fuel reduction and ecosystem enhancement plan. University of Nevada Whittell Board of Control, RenoGoogle Scholar
- Vander Wall SB (2008) On the relative contributions of wind versus animals to seed dispersal of four Sierra Nevada pines. Ecology 89(7):1837–1849. doi: 10.1890/07-0409.1 CrossRefPubMedGoogle Scholar
- Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New YorkCrossRefGoogle Scholar
- Warzecha B, Parker VT (2014) Differential post-dispersal seed predation drives chaparral seed bank dynamics. Plant Ecol 215(11):1313–1322. doi: 10.1007/s11258-014-0389-9 CrossRefGoogle Scholar
- Wells PV (2000) The manzanitas of California: also of Mexico and the world. Comstock Bonanza Press, Grass ValleyGoogle Scholar
- Wichmann MC, Alexander MJ, Soons MB, Galsworthy S, Dunne L, Gould R, Fairfax C, Niggemann M, Hails RS, Bullock JM (2009) Human-mediated dispersal of seeds over long distances. Proc Biol Sci R Soc 276(1656):523–532. doi: 10.1098/rspb.2008.1131 CrossRefGoogle Scholar
- Wilson JA, Thomas B (1999) Diet and seed dispersal efficiency of the gray fox (Urocyon cinereoargenteus) in chaparral. Bulletin of the Southern California Academy of Sciences 98:119–126Google Scholar
- Zedler PH (1995) Fire frequency in southern california shrublands: biological effects and management options. In: Keeley JE, Scott T (eds) Wildfires in California brushlands: ecology and resource management, Internationational Association of Wild Fire, pp 101–112Google Scholar
- Zedler PH, Gautier CR, McMaster GS (1983) Vegetation change in response to extreme events: the effect of a short interval between fires in California chaparral and coastal scrub. Ecology 64(4):809–818CrossRefGoogle Scholar